Herms 1992

VOLUME 67, No.
3 THE QUARTERL Y REVIEW OF BIOLOGY SEPTEMBER 1992
THE DILEMMA OF PLANTS: TO GROW OR DEFEND
DANIEL A. HERMS
The Dow Gardens, 1018 West Main Street
Midland, Michigan 48640 USA and
Departmentof Entomology, Pesticide ResearchCenter,Michigan State University
East Lansing, Michigan 48824 USA
WILLIAMJ. MATTSON
USDA North CentralForest ExperimentStation, East Lansing, Michigan 48823 USA and
Departmentof Entomology, Pesticide ResearchCenter,Michigan State University
East Lansing, Michigan 48824 USA
ABSTRACT
Physiologicalandecological constraintsplaykeyrolesin theevolutionofplantgrowthpatterns,
especiallyin relationtodefensesagainstherbivores. Phenotypic andlifehistorytheories areunified
within thegrowth-differentiation balance(GDB) framework,formingan integrated systemof
theoriesexplaining andpredictingpatternsofplantdefenseandcompetitive interactionsin ecological
and evolutionary time.
Plantactivityat thecellularlevelcan beclassifiedas growth(cell divisionandenlargement)
of differentiation
(chemicalandmorphological changesleadingto cellmaturation andspecializa-
tion). The GDB hypothesis of plant defenseis premisedupona physiologicaltrade-offbetween
growthand differentiation processes.The trade-offbetweengrowthand defenseexistsbecause
secondary metabolism andstructuralreinforcement arephysiologicallyconstrained in dividingand
enlargingcells,andbecausetheydivertresources from theproduction of newleafarea.Hencethe
dilemmaof plants. Theymustgrowfast enoughto compete, yet maintainthedefensesnecessary
to survivein thepresenceof pathogensand herbivores.
Thephysiological trade-offbetweengrowthanddifferentiation processes interacts
withherbivory
andplant-plantcompetition to manifestitselfas a genetictrade-offbetween growthand defense
in theevolutionofplantlifehistorystrategies.Evolutionary theoriesofplantdefensearereviewed.
Wealsoextenda standard growthratemodelbyseparating its ecologicalandevolutionary compo-
nents,andformalizing theroleof competitionin theevolutionofplantdefense.Weconclude with
a conceptualmodelof theevolutionofplantdefensein whichplantphysiological trade-offs interact
with theabioticenvironment, competitionand herbivory.
INTRODUCTION theory of plant defense has not kept pace. The

complexity of the subject has hindered the
IN RECENT YEARS, empirical studies of development of a synthetic framework, be-
plant/herbivore interactions have increased cause any comprehensive treatment of plant
exponentially (Scriber and Ayres, 1988), but defense theory must transcend both the disci-
progress toward a unifying and organizing plines and the levels of biological organiza-
The QuarterlyReview of Biology, September 1992, Vol. 67, No. 3

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284 THE QUARTERLYREVIEW OF BIOLOGY VOLUME 67
tion. We review and synthesize the literature lamina unfolding is a diminishing function of
addressing physiological and ecological con- cell division, but an increasing function of cell
straints on the expression and evolution of enlargement (Dale, 1976, 1988). The final
plant defense against herbivores. Phenotypic stages of leaf growth result from cell expan-
and life history theories are unified within the sion caused by turgor pressure resulting from
growth-differentiation balance (GDB) frame- vacuolization (Dale, 1976). Even after leaves
work, forming an integrated system of theo- reach full size, cytoplasm and secondary cell
ries explaining and predicting patterns of wall synthesis continue to increase the dry
plant defense in ecological and evolutionary weight of the cell (Wareing and Phillips,
time. The objective is to generate testable pre- 1981). The pattern of growth within a leaf
dictions that would otherwise remain unap- is not uniform. For example, epidermal cells
parent or ambiguous. mature before palisade cells and, in many di-
Our major premise is that the allocation of cots, cells in the tips of leaves cease division
resources by plants to chemical and structural before those in the base (Boyer, 1988; Dale,
defenses decreases growth by diverting re- 1988). Depending on species and environ-
sources from the production of leaf area and mental conditions, the course of leaf growth
other vegetative structures. This trade-off has may range from a few days to several weeks
ecological consequences that affect the success (McIntyre, 1987; Dale, 1988).
or failure of particular resource partitioning Cellular differentiation processes include
the chemical changes that occur in maturing
and allocation patterns in particular environ-
cells, and the resultant morphological changes
ments. Hence the dilemma of plants: They
leading to qualitative differences among cells
must grow fast enough to compete, and yet
and cell specialization. Differentiation pro-
maintain the physiological adaptations (de-
cesses tend to follow cell division and enlarge-
fenses) necessary for survival in the presence
ment, although overlap occurs (Loomis, 1932,
of herbivores and pathogens.
1953; Wareing and Phillips, 1981). Examples
of cellular differentiation processes include
PHYSIOLOGICAL CONSTRAINTS the thickening of leaf cuticle and secondary
ON PLANT DEFENSE cell walls, production of wax and cellular in-
clusions, and secondary metabolism (Loomis,
Growth and Differentiation:Cellular Processes 1932, 1953; B6hm, 1977; Luckner and No-
Plant growth and development occurs at ver, 1977; Luckner, 1980; Wiermann, 1981;
the cellular level through the processes of cell Lindsey and Yeoman, 1983; Lorio, 1986,
division, cell enlargement, and cell differenti- 1988). At higher levels of organization, cellu-
ation (Loomis, 1953; Wareing and Phillips, lar differentiation processes result in the de-
1981). Growth consists of cell division fol- velopment of vascular tissue, resin ducts, se-
lowed by cell enlargement, and leads to an cretory glands, trichomes, spines, and other
irreversible change in plant size. Both cell di- specialized tissues.
vision and expansion are resource demand- Secondary metabolism includes the biosyn-
thesis, transport, accumulation and storage
ing, with precise requirements for light, wa-
of metabolic products of the shikimic, polyke-
ter, minerals, temperature, photoassimilates,
tide and mevalonic pathways, as well as path-
growth regulators, the regulating effects of
ways generating alkaloids, glucosinolates
neighboring cells, and other factors (Dale,
and other compounds (Bohm, 1977; Luckner
1976, 1988; McIntyre, 1987; Boyer, 1988; and Nover, 1977; Luckner, 1980; Wiermann,
Patrick, 1988). Early stages of leaf growth, 1981; Torssell, 1983). Unlike the products of
before and after budbreak, consist almost en- primary metabolism that are common to all
tirely of cell division with cell numbers per leaf plants, the secondary metabolic profile of dif-
increasing exponentially until the leaf lamina ferent plant species varies considerably, re-
has unfolded. Thereafter, the rate of increase flecting evolutionary history and taxonomic
in cell number slows as the proportion of di- relationships (Ehrlich and Raven, 1964;
viding cells declines as a negative logistic Bate-Smith, 1984; Gottlieb, 1989, 1990; Har-
function of time. Hence, leaf growth after borne, 1990).

SEPTEMBER 1992 THE DILEMMA OF PLANTS. TO GROW OR DEFEND 285
CertainDifferentiation
Processes
Limit Herbivory walls, vacuoles, idioblasts, resin ducts, latici-
fers, and other specialized structures required
Although primary roles for secondary me-
for their compartmentation (Orians and Jan-
tabolites have been implicated in some physi-
zen, 1974; B6hm, 1977; Jalal and Collin,
ological processes (Seigler and Price, 1976;
1977; Wiermann, 1981; Lindsey and Yeo-
Seigler, 1977), defense is generally assumed
man, 1983; Hrazdina and Wagner, 1985;
to be their raison d'etre (Fraenkel, 1959;
Mersey and Cutler, 1986; Collin, 1987; Sa-
Whittaker and Feeny, 1971; Levin, 1976a; kuta and Komanine, 1987; Aerts et al., 1991;
Swain, 1977; McKey, 1979; Rhoades, 1985; Cotton et al., 1991; Kim and Mahlberg,
Williams et al., 1989; Harborne, 1990). In- 1991; Koops and Groeneveld, 1991; Lewin-
deed, secondarymetabolitesthat deter coloni- sohn, Gijzen, Savage, and Croteau, 1991;
zation and feeding are primary reasons why Wagner, 1991). In meristematic (dividing)
plants escape the vast majority of herbivores cells, the limited expression of secondary me-
occurring in their environment (Dethier, tabolism is apparently a fundamental con-
1980; Bernays and Chapman, 1987). Differ- straint, as this pattern is observed with few
entiation processesthat result in structuralre- exceptions in bacteria, fungi and animals, as
inforcement (e. g., toughened leaves, tri- well as in higher plants (Luckner and Nover,
chomes and spines) are also criticalplant traits 1977).
that limit herbivory (Levin, 1973; Coley, In a seeming paradox, concentrations of
1983, 1987; Pollard and Briggs, 1984; Coo- some secondary metabolites (particularly low-
per and Owen-Smith, 1986; Schoener, 1988). molecular-weight phenolics, terpenes and al-
There are, of course, no absolute barriers kaloids) are highest during early stages of
to herbivory (Mattson et al., 1988). Herbi- seedling growth and leaf expansion, and/or
vores have evolved a number of strategies for are synthesized only in young tissue (Dement
circumventing the resistance mechanisms of and Mooney, 1974; Cates and Rhoades,
their hosts, including physical sabotage of 1977; Frischknecht et al., 1986; Potter and
structuraland chemical defense systems(Car- Kimmerer, 1986; Puttick, 1986; Mauffette
roll and Hoffman, 1980; Dillon et al., 1983; and Oechel, 1989; Aerts et al., 1991; Fuji-
Tallamy, 1985; Compton, 1987; Dussourd mori et al., 1991; Porter et al., 1991; Singh et
and Eisner, 1987; Roy and Bergeron, 1990; al., 1991). Plants may overcome ontogenetic
Dussourd and Denno, 1991), and the enzy- constraints on secondary metabolism in a num-
matic detoxification of secondary metabolites ber of ways.
(Dowd et. al., 1983; Brattsten, 1988; Lind-
Stored Secondary Metabolites
roth, 1991). Some herbivores sequester plant
secondarymetabolites for deterring their own Previously synthesized secondary metabo-
predators (Eisner et al., 1974; Brower and lites may be stored for use when and where
their biosynthesis is constrained (Bryant et
Glazier, 1975; Peterson et al., 1987; Pasteels
et al., 1988; Bopre, 1990; Bjorkman and al., 1983). Many plants secrete stored pheno-
Larsson, 1991), repelling competing herbi- lic or terpenoid resins over newly expanding
vores (Raupp et al., 1986), or pheromone pre-foliage (Curtis and Lersten, 1974; Rhoades,
cursors (Hughes, 1974; Bopre, 1990). Some 1977; Dell and McComb, 1978; Shain and
insects even use secondary metabolites as nu-Miller, 1982; Williams et al., 1983; Johnson
trients (Kato, 1978; Bernays and Woodhead, et al., 1984; Fahn, 1988; Zobel and Brown,
1982; Bernays et al., 1983). 1990a,b). Inactive meristematic cells may
store previously formed secondary metabo-
lites in small vesicles that later fuse with the
CellularOntogeny
Constrains Metabolism
Secondary
vacuole as it develops during cell growth
In developing tissue, secondary metabolite (Rao, 1988). Several studies show concentra-
production can be constrained by the lack of tions of secondary metabolites to be highest
enzymatic machinery necessary for their syn- in buds (or at budbreak) and then to decline as
thesis, and the lack of fully developed cell leaves expand (Crankshaw and Langenheim,

1981; Palo, 1984; Horner, 1988; Mauffette Growth processes demand particularly
and Oechel, 1989; Hatcher, 1990). Some high levels of limited plant resources (Chung
plants provision seeds with high concentra- and Barnes, 1980a,b; McLaughlin et al.,
tions of secondary metabolites, possibly to 1980; Patrick, 1988). Therefore, during peri-
protect the seed and the rapidly growing seed- ods of intense growth, secondary metabolism
ling before it has developed the capability to may be substrate and/or energy limited (Cro-
synthesize significant quantities on its own teau et al., 1972; Mooney and Chu, 1974;
(Janzen, 1971; McKey, 1974; Wink and Orians andJanzen, 1974; Luckner and Nover,
Witte, 1985; Frischknecht et al., 1986; Sel- 1977; Margna, 1977; Mooney et al., 1983;
mar et al., 1988; Bodnaryk and Palaniswamy, Gulmon and Mooney, 1986; Margna et al.,
1990). 1989; Chapin, 1991). Trade-offs are inevita-
ble because the resource requirements of sec-
Precocious Differentiation of ondary metabolism are also substantial (Cro-
Compartmentation Sites teau et al., 1972; Chung and Barnes, 1977;
Ontogenetic constraints on secondary me- Chew and Rodman, 1979; McDermitt and
tabolism can vanish rapidly. Secondary me- Loomis, 1981; Gulmon and Mooney, 1986;
tabolites are frequently concentrated in epi- Williams et al., 1987; Lambers and Rychter,
dermal cells (Levin, 1976a; McClure, 1979; 1990). The cost of synthesizing a phenolic
Wiermann, 1981; Neumann et al., 1991), resin, a cyanogenic glycoside, and an alkaloid
which are among the first cells in leaves to have been minimally estimated at about 2.6,
mature (Dale, 1988). In soxne plants, epithe- 2.8 and 5.0 g CO2 per g metabolite, respec-
lial ducts, laticifers, glandular trichomes, and tively (Gulmon and Mooney, 1986).
other cells specialized for the synthesis and Furthermore, primary and secondary met-
accumulation of secondary metabolites are abolic pathways share common precursors
differentiated during early stages of leaf and and intermediates (Margna, 1977; McClure,
seedling development (Vogelmann et al., 1979; Lindsey and Yeoman, 1983; Baldwin
1987; Gilliland et al., 1988;Jahnen and Hahl- et al., 1987; Margna et al., 1989). Jensen
brock, 1988; Williams and Ellis, 1989; Kim (1985) estimated that at least 60 percent of
and Mahlberg, 1991). total plant biomass is composed of molecules
that transversed the shikimate pathway, which
Whole-PlantResource Trade-Offs Constrain gives rise to certain amino acid precursors
SecondaryMetabolism (tryptophan, phenylalanine and tyrosine) of
Constraints operating at higher levels of or- protein, phenolics, alkaloids and cyanogenic
ganization can limit secondary metabolism in glycosides. Phenylalanine is the rate-limiting
ontogenetically "capable" tissues. Plants have precursor for phenylpropanoid synthesis (e.g.,
limited resources to support their physiologi- lignin, flavonoids and condensed tannins),
cal processes, hence all requirements cannot and at the same time is an essential amino
be met simultaneously, and trade-offs occur acid for protein synthesis (Margna, 1977; Mc-
among growth, maintenance, storage, repro- Clure, 1979; da Cunha, 1987; Margna et al.,
duction and defense. Consequently, there is 1989). Plant growth is heavily dependent on
sequential growth and maturation of tis- protein synthesis for the manufacture of pho-
sues within organs and organs within plants, tosynthetic, biosynthetic and regulatory en-
and/or strong inverse relationships between zymes, as well as for structural protein. As
the -allocation of resources to growth and non- such, phenolic synthesis competes with growth
growth processes (Mooney, 1972; Mooney for common substrate (Margna, 1977; Phil-
and Chu, 1974; Gifford and Evans, 1981; lips and Henshaw, 1977; Margna et al.,
Bryant et al., 1983; Mooney et al., 1983; Gif- 1989). Alkaloid synthesis, with its amino acid
ford et al., 1984; Bloom et al., 1985; Coley et precursors, also competes directly with pro-
al., 1985; Bazzaz et al., 1987; Loehle, 1988; tein synthesis, and consequently with growth
Loomis et al., 1990; Chapin, 1991; K6rner, (Lindsey and Yeoman, 1983; Hegnauer,
1991). 1988). Acetyl CoA serves as the precursor for

terpenoids and also the entry point to the mous, in that the translocation of resources
Kreb's cycle (Gray, 1987). within and among them can be restricted
Trade-offs between primary and secondary (Watson and Casper, 1984; Dickson, 1989;
metabolism are well documented in cell cul- Wardlaw, 1990). However, the degreeof mod-
tures (Phillips and Henshaw, 1977; Lindsey ular integration varies among species on a
and Yeoman, 1983; Collin, 1987) and at the continuum from nearly complete autonomy
whole plant level. Many intraspecific com- to high interdependence (Watson and Cas-
parisons document physiological trade-offs per, 1984). In spite of their semiautonomous
between growth rate and secondary metabo- nature, competition among modules for lim-
lism in both wild and crop species (Hanover, ited resourcesis well documented(Gill, 1986).
1966a; del Moral, 1972; Mooney and Chu, Even though the growth and reproductionof
1974; Podstolski et al., 1981; Krischik and some modules may be supported at the ex-
Denno, 1983; Mihaliak and Lincoln, 1985, pense of others, the "competitive"pattern of
1989a; Waring et al., 1985; Coley, 1986;
resource partitioning among modules should
Larsson et al., 1986; Lorio and Sommers,
be adaptive (Hardwick, 1986; Loomis et al.,
1986; Bryant, 1987; Bryant, Chapin, Rei-
1990). The survival of each module is ulti-
chardt, and Clausen, 1987; Bryant, Clausen,
mately dependent on the survivalof the genet,
Reichardt, McCarthy, and Werner, 1987;
hence there should be strong selection against
Lightfoot and Whitford, 1987, 1989; Ap-
"'selfish"interactions among modules that de-
pleton and van Staden, 1989; Glyphis and
Puttick, 1989; Hrutfiord and Gara, 1989;
creasethe inclusive fitnessof their "metapopu-
Margna et al., 1989). Bjorkman and Ander-
lation,"the genet (J. White, 1979, 1984; Hard-
son (1990) have also documented a trade-off wick, 1986; Tuomi and Vuorisalo, 1989a,b).
between growth and structural defenses (the Patterns of resource use within a plant are
elaboration of which diverts resources from determined by within-module allocation, as
the production of leaf area) in South Ameri- well as between-module (whole plant) parti-
can blackberry (Rubus bogotensis). tioning priorities. For example, individual
leaves and modules do not export assimilates
Modular ConstructionAffects Resource until their own growth requirements have
Use Priorities been met (McLaughlin et al., 1979; Dickson,
Growth and differentiation processes occur
1989; Wardlaw, 1990; Dickson and Isebrands,
at the cellular level, but their functional inte-
1991). At the level of the whole plant, patterns
gration at higher levels of organization shapes
of resource distribution reflect the power of
the structure and function of the plant (Ware- modules to draw assimilates (i.e., their sink
ing and Phillips, 1981). Higher plants can be strength), which is a function of: (a) the num-
considered an integrated network of cellular ber of meristems giving rise to modules, (b)
systems. These systems are organized into the rate of module initiation per meristem, (c)
specialized morphological subunits (modules) the developmental fate of the module (i.e.,
among which the distribution of limited re- vegetative and/or reproductive), (d) the rate
sources is regulated through complex source/ and duration of the growth of each module,
sink relationships (Loomis et al., 1990). Mod- and (e) the nature of vascular connections
ules are repeated multicellular units originat- among modules (Harper and White, 1974;
ing from single meristems, that combine to Harper and Bell, 1979; Watson and Casper,
form higher levels of organization from roots 1984; Halle, 1986; Hardwick, 1986; Dickson,
and branches to entire plants (Harper and 1989; Haukioja et al., 1990; Dickson and Ise-
White, 1974; Harper and Bell, 1979; Watson brands, 1991).
and Casper, 1984; Halle, 1986; Barlow, 1989; When environmental conditions are favor-
Tuomi and Vuorisalo, 1989a,b). Higher able, vegetative growth generally receives re-
plants grow by means of the reiterated pro- source priority over secondary metabolism
duction of these modules. and storage (Mooney and Chu, 1974; Chung
Modules within a plant are semiautono- and Barnes, 1980a,b; Waring and Pitman,

1985; Bazzaz et al., 1987; Chapin et al., Primary Rolesfor SecondaryMetabolites

1990; Dickson and Isebrands, 1991). Conse- Decrease Their Cost as Defenses
quently, quantitative variation in the second- Defense is not the only role of secondary
ary metabolism of plants is a function of varia-
metabolites in plants (Seigler and Price, 1976;
tion in the rate and duration of growth of Seigler, 1977). Other functions include at-
individual modules, as well as the proportion
traction of pollinators (anthocyanins and fla-
of modules undergoing growth at any one
vonoids) (Brehm and Krell, 1975; Rhoades,
time. If a large proportion of modules within a
1979), protection from UV light (phenolic
plant are undergoing growth simultaneously,
resins, anthocyanin, flavonoids) (Rhoades,
secondary metabolism will be limited by lack
1977; Lee and Lowry, 1980; Caldwell et al.,
of substrate (Mooney and Chu, 1974; Orians
1983; Les and Sheridan, 1990), structural
andJanzen, 1974; Luckner and Nover, 1977;
support (lignin and tannins) (Rhodes, 1985;
Margna, 1977; Mooney et al., 1983; Gulmon
Haslam, 1988; Chalker-Scott and Krahmer,
and Mooney, 1986; Margna et al., 1989;
1989), temporary nutrient storage (alkaloids
Chapin, 1991). In plants with indeterminate
patterns of growth, some modules continue to and cyanogenic glycosides) (Wink and Witte,
grow after others have matured (e.g., Clau- 1985; Selmar et al., 1988; Harborne, 1990;
sen and Kozlowski, 1965; Kozlowski and Poulton, 1990), phytohormone regulation (fla-
Clausen, 1966). Secondary metabolism in vonoids and other simple phenolics) (Rhodes,
mature modules will be limited if they export 1985; Doberski, 1986; Jacobs and Rubery,
much of their photoassimilates to strong vege- 1988; Chalker-Scott and Krahmer, 1989),
tative or reproductive "sinks" undergoing drought resistance (tannins, phenolic resins)
rapid growth. (Rhoades, 1977; Bariska and Pizzi, 1986;
Pizzi and Cameron, 1986; Meinzer et al.,
The OpportunityCost of Plant Defense 1990), facilitation of nutrient uptake (pheno-
The relative growth rate (RGR) of a plant lics) (Boyer et al., 1989; Baas, 1990), protec-
is equal to the product of its net assimilation tion of roots from acidic and reducing envi-
rate (NAR) (net carbon accumulation per ronments (tannins) (Kimura and Wada,
unit of time) and leaf area ratio (LAR) (ratio 1989), and mediators of plant relationships
of total leaf area to total plant dry mass) with symbiotic nitrogen-fixing bacteria (fla-
(Hunt, 1978; Lambers, 1987): vonoids) (Peters et al., 1986; Baas, 1990; Hart-
wig et al., 1990; Lynn and Chang, 1990).
RGR = NAR * LAR. Furthermore, some secondary metabolites
may be metabolized and returned to the re-
In both wild plants and domesticated crops,
source pool available for primary metabo-
differences in growth rates and dry matter
lism, further attenuating their costs (Rob-
accumulation result primarily from differences
inson, 1974; Seigler and Price, 1976; Wink
in patterns of resource partitioning rather
and Witte, 1985; Frischknecht et al., 1986;
than differences in NAR. It is the differential
investment of photoassimilates into new leaf Selmar et al., 1988; Harborne, 1990; but see
area that is largely responsible for both geno- Mihaliak et al., 1991). The diverse roles of
typic and phenotypic differences in growth secondary metabolites in plants may decrease
rates (Potter and Jones, 1977; Gifford and their opportunity costs as defensive com-
Evans, 198 1; Gifford et al., 1984; Lambers, pounds.
1987; Patrick, 1988; Poorter, 1990; Poorter
ResourceAvailability and Source/SinkInteractions
and Remkes, 1990; Poorter et al., 1990; Cha-
pin, 1991; K6rner, 1991). Hence, there is a Plants export carbon from sources (leaves
very substantial "opportunity cost" of plant de- and storage organs) to sinks (active meristems
fense. Secondary metabolism and the elabo- and sites of reserve accumulation) via phloem
ration of structural defenses decreases growth transport (Wareing and Patrick, 1975). Sink
by diverting resources from the production strength (the relative ability of different sinks
of new leaf area (Chapin, 1989; Fagerstrom, to attract carbon) is a product of sink size
1989; Baas, 1990; Korner, 1991). and activity; actively growing meristems are

especially strong photosynthetic sinks (Ho, Nonlinear Effects of ResourceAvailability on

1988; Dickson, 1989; Wardlaw, 1990; Dick- SecondaryMetabolism
son and Isebrands, 1991; K6rner, 1991; Lux- The exact form of the trade-off function be-
more, 1991). Strong meristematic activity re- tween growth and secondary metabolism has
quires copious supplies of water and nutrients yet to be established for any plant species. How-
to drive cell division and expansion. Hence, ever, source/sink theory predicts a nonlinear
sink strength is a function of resource avail- relationship between growth rate, secondary
ability (Wareing and Patrick, 1975; Agren, metabolism, and consequently plant defense
1985a, 1988; McIntyre, 1987; Daie, 1988; (Mattson and Haack, 1987a; Tuomi, Nie-
Hirose, 1988a; Patrick, 1988; Wardlaw, 1990; meld, Chapin, Bryant, and Siren, 1988; Eng-
Chapin, 1991; Luxmore, 1991). lish-Loeb, 1989, 1990; Horner, 1990) (Fig. 1).
Photosynthesis and growth do not respond In resource-rich environments, growth pro-
equally to gradients of water and nutrients. cesses receive allocation priority for resources
Growth processes are slowed considerably by (Bazzaz et al., 1987), decreasing the relative
even moderate shortages of nutrients or water. availability of carbon for the support of sec-
Net photosynthesis, however, is not as sen- ondary metabolism and structural reinforce-
sitive to resource limitation (Hsiao, 1973; ment. Hence, within a population, the fastest
Chapin, 1980a; Bradford and Hsiao, 1982; growing plants will be the least resistant to
McDonald et al., 1986; Daie, 1988; Dietz, (but perhaps the most tolerant of) herbivores
1989; K6rner, 1991; Luxmore, 1991). Con- (Bryant et al., 1983; Mihaliak and Lincoln,
sequently, environments suitable for growth 1985; Larsson et al., 1986; Bryant, 1987; Bry-
are only a small subset of those suitable for ant, Chapin, Reichardt, and Clausen, 1987;
net carbon fixation. Thus, when moderate Bryant, Clausen, Reichardt, McCarthy, and
nutrient deficiency or drought impose sink
limitations upon growth, carbohydrates accu-
mulate in excess of growth requirements
(Chapin, 1980a; McDonald et al., 1986; Net
Assimilation
Daie, 1988; Dietz, 1989; Chapin et al., 1990;
Wardlaw, 1990). The accumulation of carbo-
hydrates, however, may eventually inhibit Relative
Growth Rate
photosynthesis through negative feedback
mechanisms (Neales and Incoll, 1968; Wat-
son and Casper, 1984; Foyer, 1987, 1988;
Secondary
K6rner, 1991; Luxmore, 1991). Metabolism
Source strength is a function of the avail-
ability of carbon for export (Wareing and Pat-
rick, 1975). At very low resource levels (light, Low High
moisture and nutrients) photosynthesis (car- Resource Availability
bon assimilation) and growth are both lim-
FIG. 1. NORMS OF REACTION FOR NET
ited. In source-limited plants, primary meta-
ASSIMILATION RATE, RELATIVE
bolic processes and maintenance respiration GROWTH RATE, AND SECONDARY
may receive priority use of limited carbon METABOLISM IN RESPONSE TO
(Waring and Pitman, 1985). Increased re- CHANGING RESOURCE
source availability will increase both the pho- AVAILABILITY
tosynthetic and growth rates of source-limited At low to moderate levels of resource availability
plants. Enhanced atmospheric CO2 generally (light, water and nutrients), rates of net assimila-
increases the growth of C3 plants by enhancing tion, growth and secondary metabolism are posi-
tively correlated. At moderate to high levels of
net assimilation and resource use efficiency,
resource availability, net assimilation rate is con-
suggesting that plants chronically experience stant, relative growth rate and secondary metabo-
a degree of source limitation (Strain, 1985; lism are inversely correlated, and the physiological
Idso and Kimball, 1988; Bazzaz, 1990; Far- trade-off between growth and secondary metabo-
rar and Williams, 1991; Hilbert et al., 1991). lism is apparent.

Werner, 1987; Hrutfiord and Gara, 1989; to use observational data to test the hypothesis
Room et al., 1989; Kimberling et al., 1990). that a trade-off occurs between them. For ex-
This observation lies at the heart of the "vigor ample, Denslow et al. (1987, 1990) and Briggs
hypothesis" of Price (1991). and Schultz (1990) questioned the existence
Environmental constraints on growth can of a trade-off between growth and secondary
mitigate the cost of defense. Any factor that metabolism based on their findings of positive
limits growth more than photosynthesis, such correlations between growth rate and concen-
as moderate drought, moderate nutrient limi- trations of secondary metabolism. As re-
tation, and low temperature (Chapin, 1980a; source availability (light, water and nutrients)
Bradford and Hsiao, 1982; Daie, 1988; Pol- increases from low to moderate, however, net
photosynthesis also increases. Increased car-
lock, 1990; Wardlaw, 1990), will increase the
bon assimilation creates the possibility for posi-
carbon pool available for allocation to second-
tive correlations between growth and second-
ary metabolism with little or no trade-off with
ary metabolism despite competition for a
growth (Mattson, 1980; Bryant et al., 1983,
common resource base (i.e., van Noordwijk
1985, 1988; Gershenzon, 1984; Mihaliak and and deJong, 1986) (Fig. 1). Bryant et al. (1983)
Lincoln, 1985, 1989a; Waring et al., 1985; and Tuomi, Niemela, Chapin, Bryant, and
Larsson et al., 1986; Lorio, 1986, 1988; Bry- Siren (1988) predicted this pattern with re-
ant, 1987; Bryant, Chapin, Reichardt, and spect to phenotypic plasticity in growth and
Clausen, 1987; Bryant, Clausen, Reichardt, secondary metabolism. At moderate to high
McCarthy, and Werner, 1987; Lightfoot and resource levels, where net photosynthesis is
Whitford, 1987, 1989; Mihaliak et al., 1987; close to maximum, the physiological trade-off
Muller et al., 1987, 1989; Glyphis and Puttick, becomes evident as a negative correlation be-
1989; Charles et al., 1990; Horner, 1990). tween growth and secondary metabolism
Hence, sink-limited plants will be more resis- (Fig. 1). Thus, it is not possible to infer the
tant to herbivores than plants experiencing lack of a physiological trade-off between growth
no environmental limitations upon growth. and secondary metabolism, unless the rate of
They may have little capacity, however, to change in resource acquisition is known.
compensate for the herbivory they do experi-
Phenotypic Variationin SecondaryMetabolism.
ence.
Two Hypotheses
At very low resource levels, both growth
and photosynthesis are highly constrained. Plant resistance to herbivores results from
Essential primary metabolic processes and the interaction of a suite of genetically based
baseline maintenance may receive priority chemical and structural traits. Phenotypic
use of limited carbon. Because of energy and variation in herbivore resistance, however,
results primarily from variation in plant nu-
substrate limitation, carbon-based secondary
trient and secondary metabolite concentra-
metabolism and herbivore resistance gener-
tions. Two conceptually similar hypotheses
ally decline (Bryant et al., 1983; Waring and
have been advanced to predict environmental
Pitman, 1985). Consequently, shading gen-
effects on the phenotypic expression of sec-
erally decreases plant resistance to herbivores, ondary metabolism: (1) the carbon/nutrient
including bark beetles (Waring and Pitman, balance (CNB) hypothesis (Bryant et al., 1983;
1985; Christiansen et al., 1987), browsing Tuomi et al., 1984; Tuomi, Niemela, Cha-
mammals (Bryant, 1987; Bryant, Chapin, pin, Bryant, and Siren, 1988; Reichardt et
Reichardt, and Clausen, 1987), insect foli- al., 1991), and (2) the growth-differentiation
vores (Larsson et al., 1986), and fungal path- balance (GDB) hypothesis (Loomis, 1932,
ogens (Matson and Waring, 1984; Entry et 1953; Lorio, 1986, 1988).
al., 1986). Furthermore, carbon-limited plants
will have very limited ability to tolerate her- The Carbon/Nutrient Balance Hypothesis
bivory (e.g., McGraw et al., 1990). Bryant et al. (1983) originally formulated
A nonlinear relationship between growth the CNB hypothesis to explain the effects of
and secondary metabolism makes it difficult fertilization and shade on phenotypic variation

in secondary metabolism. The CNB hypothe- been shown to increase concentrations of

sis predicts that concentrations of carbon-based N-based secondary metabolites (Nowacki et
secondary metabolites (e.g., terpenes, pheno- al., 1976; Mattson, 1980; Gershenzon, 1984)
lics, and other compounds that have only C, and decrease concentrations of C-based sec-
H and 0 as part of their structure) will be ondary metabolites (Mihaliak and Lincoln,
positively correlated with the carbon/nutrient 1985; Waring et al., 1985; Larsson et al.,
(C/N) ratio of the plant. Conversely, concen- 1986; Bryant, 1987; Bryant, Chapin, Reich-
trations of nitrogen-based secondary metabo- ardt, and Clausen, 1987; Bryant, Clausen,
lites (e.g., alkaloids, nonprotein amino acids, Reichardt, McCarthy, and Werner, 1987;
cyanogenic compounds, proteinase inhibi- Lightfoot and Whitford, 1987, 1989; Mihal-
tors, and others having N as part of their iak et al., 1987; Glyphis and Puttick, 1989;
structure) are predicted to be inversely corre- Price et al., 1989; Waterman and Mole, 1989).
lated with the C/N ratio of the plant (Bryant Shading has been shown to increase concen-
et al., 1983). trations of N-based secondary metabolites
The CNB hypothesis is based upon the fol- (Van Horne et al., 1988), and decrease con-
lowing premises. Moderate nutrient deficiency centrations of C-based secondary metabolites
limits growth more than photosynthesis. (Woodhead, 1981; Waterman et al., 1984;
Hence, nutrient-deficient plants accumulate Waring et al., 1985; Larsson et al., 1986;
carbohydrates, increasing the C/N ratio within Bryant, 1987; Bryant, Chapin, Reichardt,
and Clausen, 1987; Mole et al., 1988; Van
the plant. Carbohydrates accumulated in ex-
Horne et al., 1988; Nichols-Orians, 1991).
cess of growth requirements are allocated to
C-based secondary metabolites. In contrast, The CNB Hypothesis Extendedto
increased nutrient uptake in fertile soils de- Sex-Biased Herbivory
creases the C/N ratio within the plant; C-based
In dioecious species, male plants may gen-
secondary metabolism declines as growth re-
erally experience greater herbivory than fe-
ceives allocation priority. As other factors be-
males (Danell et al., 1985, 1991; Lovett Doust
gin to limit growth, nitrogen assimilated in
and Lovett Doust, 1985; Agren, 1987; Elm-
excess of growth requirements may be allo-
qvist et al., 1988; Alliende, 1989; Boecklen et
cated to the production of N-based secondary
al., 1990; Jing and Coley, 1990; Krischik and
metabolites.
Denno, 1990). This pattern of sex-biased her-
Light intensity can also affect the C/N bal-
bivory may be explained by the CNB hypoth-
ance within the plant, and consequently sec- esis.
ondary metabolism. Shade decreases the C/N The reproductive structures of many spe-
ratio of plants by limiting carbon assimilation cies are photosynthetic, contributing in vary-
more than nutrient uptake. Concentrations ing degrees to their own economy of energy
of C-based secondary metabolites decline as and biomass (Bazzaz et al., 1979; Reekie and
limited available carbon is allocated to growth. Bazzaz, 1987a; Cipollini and Levey, 1991).
Nitrogen assimilated in excess of growth re- Furthermore, enhanced sink strength associ-
quirements, however, may be diverted to N- ated with rapidly developing reproductive
based secondary metabolic pathways. On the structures may stimulate increased photosyn-
other hand, increased light intensity is pre- thesis in nearby source leaves through feed-
dicted to increase net photosynthesis, thereby back-mediated effects (Neales and Incoll, 1968;
increasing the C/N ratio within the plant, and Watson and Casper, 1984; Foyer, 1987, 1988;
concentrations of C-based secondary metabo- Luxmore, 1991).
lites. Concentrations of N-based secondary While reproductive structures contribute
metabolites are predicted to decline as N is directly and indirectly to their own carbon
allocated to photosynthetic and growth pro- requirements, the substantial nutrient invest-
cesses. ment required for their maturation is ob-
Substantial experimental and correlative tained in full from the rest of the plant (Moo-
evidence supports the CNB hypothesis (Wa- ney, 1972; Sinclair and de Wit, 1975; Bazzaz
terman and Mole, 1989). Fertilization has et al., 1979; Thompson and Stewart, 1981;

292 THE QUARTERLYRE VIEW OF BIOLOGY VOLUME 67
Alpert et al., 1985). As a result, the diversion tance or DIR) (Wallner and Walton, 1979;
of nutrients from vegetative to reproductive Werner, 1979; Haukioja, 1980, 1982; Schultz
structures may be proportionally greater than and Baldwin, 1982; Tuomi et al., 1984; Hau-
that of carbon (Sinclair and de Wit, 1975; van kioja and Neuvonen, 1985; Neuvonen et al.,
Andel and Vera, 1977; Wallace and Rundel, 1987; Bryant et al., 1991), whereas equiva-
1979; Lovett Doust, 1980; Thompson and lent defoliation of evergreens usually does not
Stewart, 1981; Williams and Bell, 1981; (Niemela et al., 1984, 1991; Bryant et al.,
Mooney and Gulmon, 1982; Bullock, 1984; 1988, 1991; Wagner, 1988). The CNB hy-
Bazzaz and Reekie, 1985; Reekie and Baz- pothesis has been extended to explain this
zaz, 1987b; Allen and Antos, 1988). Hence, phenomenon, proposing that this pattern
differential partitioning of nutrients to repro- stems from fundamental differences in the
ductive structures may increase the C/N ratio carbon partitioning patterns of deciduous and
in the foliage. The effect should be strongest evergreen plants (Tuomi et al., 1984, 1990;
Niemela et al., 1984, 1991; Bryant et al.,
in female plants because the maturation of
1988, 1991; Tuomi, Niemela, Chapin, Bry-
fruit and seeds requires a proportionally higher
ant, and Siren, 1988).
nutrient investment than does the maturation
During the growing season, most of the nu-
of male reproductive structures (Wallace and
trient capital of deciduous trees is contained
Rundel, 1979; Bullock, 1984; Antos and Al- within the foliage. Substantial carbon re-
len, 1990; Cipollini and Stiles, 1991). Thus, serves, however, remain in the roots and
female plants are predicted to grow slower, other woody tissues. Consequently, defolia-
have higher concentrations of C-based sec- tion of deciduous species can result in the loss
ondary metabolites, and be more resistant to of proportionally more nutrients than carbon,
herbivores than conspecific males. In accord, and thus a relative nutrient deficiency in the
male plants are generally reported to grow plant (Chapin, 1980b; Tuomi et al., 1984;
faster (Lloyd and Webb, 1977; Wallace and Chapin, Shaver, and Kedrowski, 1986; Mi-
Rundel, 1979; Bullock, 1984; Hoffmann and haliak and Lincoln, 1989b; Bryant et al.,
Alliende, 1984; Allen and Antos, 1988; Clark 1991). Furthermore, defoliation-induced stress
and Clark, 1988; Ramp and Stephenson, may result in fine-root mortality, decreasing
1988; Snow and Whigham, 1989; Antos and nutrient uptake, and thus further aggravating
Allen, 1990; Jing and Coley, 1990; Krischik the nutrient deficiency (Bryant et al., 1988;
and Denno, 1990), experience greater herbiv- Tuomi et al., 1990). The net result may be an
ory (Danell et al., 1985, 1991; Lovett Doust increased C/N ratio in years following defolia-
and Lovett Doust, 1985; Agren, 1987; Elm- tion, resulting in increased concentrations of
qvist et al., 1988; Alliende, 1989; Boecklen et C-based secondary metabolites (Tuomi et al.,
al., 1990;Jing and Coley, 1990; Krischik and 1984, 1990; Bryant et al., 1988, 1991; Tu-
Denno, 1990), and have lower concentrations omi, Niemeli, Chapin, Bryant, and Siren,
of secondary metabolites or less tough foliage 1988).
(Palo, 1984; Price et al., 1989; Boecklen et Evergreens store a larger proportion of car-
al., 1990; Jing and Coley, 1990; Krischik and bon in their foliage than do deciduous species.
Denno, 1990). A similar pattern may occur Hence, carbon and nutrient reserves are lost
in monoecious species, with the C/N ratio of in similar proportions when evergreens are
the foliage, C-based secondary metabolism, defoliated (Bryant et al., 1983, 1988; Tuomi,
and herbivore resistance increasing in pro- Niemela, Chapin, Bryant, and Siren, 1988).
Furthermore, coniferous evergreens and slow-
portion with female reproductive effort.
growing deciduous species that have been de-
foliated may not replace carbon as rapidly as
The CNB Hypothesis Extendedto
nutrients because of their inherently low rates
Delayed InducedResistance
of photosynthesis (Bond, 1989; Sprugel,
Defoliation of deciduous trees sometimes 1989; Bryant et al., 1991). Hence, their defo-
increases resistance to herbivores in the years liation can result in a relative carbon defi-
following defoliation (delayed induced resis- ciency within the plant (Ericsson et al., 1980;

SEPTEMBER 1992 THE DILEMMA OF PLANTS: TO GROW OR DEFEND 293
Bryant et al., 1991; Niemela et al., 1991), and then it may be triggered by herbivore-specific
consequently undiminished or even increased cues, and natural defoliation may result in a
foliar nutrient concentrations (Piene, 1980; stronger DIR than artificial defoliation; this
Piene and Percy, 1984; Bryant et al., 1991; prediction is not derivable from the CNB hy-
Niemela et al., 1991). The predicted result is pothesis (Haukioja and Neuvonen, 1985;
a decreased C/N balance, decreased concen- Haukioja et al., 1985).
trations of C-based secondary metabolites, Tests of these hypotheses have yielded sup-
and no DIR (Niemela et al., 1984; Tuomi et port for both. Consistent with the CNB hy-
al., 1984; Bryant et al., 1988, 1991; Tuomi, pothesis: (1) the expression of DIR in moun-
Niemela, Chapin, Bryant, and Siren, 1988). tain birch was localized, being confined to
branches defoliated the previous year, and not
detected in neighboring undamaged branches
The Carbon/Nutrient Balance Hypothesis: on the same tree (Tuomi, Niemela, Rousi,
Evaluating the Evidence Siren, and Vuorisalo, 1988); (2) defoliation
resulted in a relative nutrient deficiency and
DIR. IncidentalEffect of Defoliation or DIR in three fast-growing species, but in-
Evolved Response to Herbivory? creased nutrient concentrations and decreased
herbivore resistance in three slow-growing
Is DIR an incidental consequence of defoli-
species (Bryant et al., 1991); and (3) in the
ation-induced alterations in the C/N balance same study, Bryant et al. (1991) found the
of the plant or adaptive plasticity evolved in presence and absence of DIR to be opposite
response to herbivory (Haukioja, 1980; Tu- that predicted, based on historical patterns of
omi et al., 1984, 1990; Haukioja and Neuvo- herbivory experienced by the six species.
nen, 1985; Bryant et al., 1988, 1991; Tuomi, Consistent with the active defense hypothe-
Niemela, Chapin, Bryant, and Siren, 1988; sis: (1) DIR in mountain birch (Betula pu-
Tuomi, Niemela, Rousi, Siren, and Vuori- bescens)was stronger in trees from within than
salo, 1988)? Divergent predictions can be de- from outside the historical outbreak range of
rived from the two hypotheses. The active the autumnal moth (Epirrita autumnata)(Hau-
defense hypothesis predicts that the presence kioja, 1980); (2) fertilization strengthened
or strength of DIR should correspond with a DIR and did not shorten its relaxation time
plant's evolutionary history of herbivory; the in mountain birch (Haukioja and Neuvonen,
CNB hypothesis predicts DIR should be inde- 1985; Haukioja et al., 1985); (3) defoliation
pendent of historical patterns of herbivory of mountain birch by E. autumnataresulted in
(Bryant et al., 1991). The CNB hypothesis stronger DIR than artificial defoliation (Hau-
predicts DIR should be weak or nonexistent kioja and Neuvonen, 1985); and (4) in a com-
in nutrient-rich environments, where nutri- parison of four deciduous species, DIR was
ents lost as a result of defoliation are more strongest in the two species with historical as-
sociations with outbreak herbivores, even
rapidly replaced; this prediction cannot be de-
though they were the slowest growing of the
rived from the active defense hypothesis
four species (Neuvonen et al., 1987).
(Haukioja et al., 1985; Tuomi, Niemela,
Chapin, Bryant, and Siren, 1988). Tuomi, SecondaryMetabolism Is Not Consistently
Niemela, Rousi, Siren, and Vuorisalo (1988) Linked to the C/N Balance of the Plant
and Tuomi et al. (1990) argue that because of Not all data are consistent with the CNB
the semiautonomous nature of plant modules hypothesis. In some cases, fertilization in-
(Watson and Casper, 1984), the CNB hy- creased concentrations of C-based secondary
pothesis predicts the effects of defoliation metabolites (Clark and Menary, 1980; Muz-
should be localized within damaged modules ika et al., 1989; Bj6rkman et al., 1991; Rousi
and branches; a systemic response (detectable et al., 1991), or had no effect (Chapin, Shaver,
in modules distant from the site of injury) and Kedrowski, 1986; Rousi et al., 1987).
would be more consistent with the active de- In others studies, shading had no effect on
fense hypothesis. If DIR is an active defense, C-based secondary metabolism (Lincoln and

294 THE QUARTERLY RE VIEW OF BIOLOGY VOLUME 67
Langenheim, 1978; Langenheim et al., 1981; onstrated that the previously observed rapid
Lincoln and Mooney, 1984). The evidence metabolic turnover of terpenes in peppermint
from experiments addressing the effects of (Mentha x piperita) was an experimental arti-
drought and enhanced CO2 on secondary me- fact. They suggested that other cases also be
tabolism also appears inconsistent with the reexamined before this phenomenon is as-
CNB balance hypothesis. Moderate drought sumed to be a general occurrence.
stress may generally decrease the C/N bal- The presence of internal metabolic trade-
ance in the plant because carbon acquisition offs may provide an alternative explanation
is limited more than nutrient uptake (Hosner to secondary metabolic turnover for inter-
et al., 1965; Viets, 1972; Bloom et al., 1985; preting some data inconsistent with the CNB
Rego et al., 1986; Mattson and Haack, 1987a). hypothesis. Within a plant, changes in the
Hence, the increased concentrations of N- concentrations of individual secondary me-
based secondary metabolites observed in some tabolites are not always correlated with over-
drought-stressed plants are consistent with all changes in total secondary metabolism
the CNB hypothesis (Ball and Hoveland, (e.g., Gilmore, 1977; Berenbaum et al., 1986;
1978; Briske and Camp, 1982; Frischknecht Coassini Lokar et al., 1987; Zangerl and Ber-
et al., 1987). The increased concentrations of enbaum, 1987; Hegerhorstetal., 1988; Muz-
C-based secondary metabolites observed in ika et al., 1989; Reichardt et al., 1991). If two
other plants, however, appear inconsistent compounds originate from different branches
within the same pathway, concentrations of
(del Moral, 1972; Gershenzon, 1984; Lorio
one compound may increase at the expense
and Sommers, 1986; Allen et al., 1987; Ra-
of the other (Chew and Rodman, 1979; Bald-
machandra Reddy and Rama Das, 1988;
win et al., 1987; Berenbaum and Zangerl,
Charles et al., 1990; Horner, 1990; Ross and
1988; Hegerhorst et al., 1988).
Berisford, 1990; Rhizopoulou and Diaman-
The CNB hypothesis predicts that carbohy-
toglou, 1991). Enhanced C02 generally in-
drates accumulated in excess of growth re-
creases the C/N ratio within the plant by in-
quirements will be allocated to C-based sec-
creasing carbon assimilation and decreasing
ondary metabolism, but does not predict how
foliar nutrient concentrations (Strain, 1985; those carbohydrates will be distributed among
Idso and Kimball, 1988; Bazzaz, 1990). In the diverse pathways and compounds present
the few existing studies, however, enhanced within plants. Dynamic compounds (e.g.,
CO2 had no effect on secondary metabolite phenolic glycosides) are often present in small
concentrations (Stuhlfauth et al., 1987; Fajer, concentrations. Hence, changes in their con-
1989; Fajer et al., 1989; Lincoln and Couvet, centrations will not substantially affect total
1989; Johnson and Lincoln, 1990). secondary metabolism. They may increase as
As Reichardt et al. (1991) point out, in total secondary metabolism declines and vice
many of the studies apparently inconsistent versa. On the other hand, secondary metabo-
with the CNB hypothesis, concentrations of lites that accumulate in high concentrations
individual "dynamic" secondary metabolites (often stable end products such as condensed
(compounds that are continually catabolized tannins and surface resins) are more likely to
and resynthesized) were quantified. They ar- be directly correlated with total allocation to
gue that measuring static concentrations of secondary metabolism. Studies that measure
such compounds underestimates their true rate concentrations of the compounds present in
of production. The CNB hypothesis may pre- highest concentrations (or ideally, total out-
dict most accurately environmental effects on put of secondary metabolic pathways) repre-
stable "end products" with little or no metabolic sent the best tests of the CNB hypothesis.
turnover (e.g., condensed tannins and lignin
which remain in senescent foliage, and insolu- The Growth-Differentiation
ble, nonvolatile resins secreted over plant sur- Balance Hypothesis
faces), the final concentrations of which repre- The GDB hypothesis (Loomis, 1932, 1953;
sent cumulative production (Reichardt et al., Lorio, 1986, 1988; Tuomi et al., 1990) pro-
1991). Mihaliak et al. (1991), however, dem- vides a framework for understanding pheno-

typic variation in secondary metabolism that the source/sink balance within the plant. The
is similar, but more comprehensive than that growth rate of C3 plants generally increases as
of the CNB hypothesis. As with the CNB hy- a result of increased source strength (Strain,
pothesis, the fundamental premise of the 1985; Idso and Kimball, 1988; Bazzaz, 1990;
GDB hypothesis is the existence of a physio- Farrar and Williams, 1991). The effects of
logical trade-off between growth and differen- enhanced CO2 on sink activity, however, are
tiation processes, including secondary metab- not well understood (Farrar and Williams,
olism. The GDB hypothesis differs from the 1991), but are likely to interact in complex
CNB hypothesis by explicitly addressing the ways with temperature, soil fertility, and wa-
very important developmental constraints on ter availability (Farrar and Williams, 1991;
secondary metabolism, as well as all extrinsic Hilbert et al., 1991). In the few experimental
factors affecting secondary metabolism. The tests, enhanced atmospheric CO2 has had lit-
GDB hypothesis subsumes the CNB hypothe- tle effect on secondary metabolism (Stuhl-
sis, predicting that any environmental factor fauth et al., 1987; Fajer, 1989; Fajer et al.,
that slows growth more than photosynthesis 1989; Lincoln and Couvet, 1989; Johnson
can increase the resource pool available for and Lincoln, 1990).
allocation to secondary metabolism (Loomis, The CNB hypothesis is often sufficient to
1932, 1953). Hence, the predictions of the explain phenotypic patterns in secondary me-
CNB hypothesis are a subset of the predic- tabolism because nutrient availability is a ma-
tions of the GDB hypothesis. jor factor limiting primary production on a
In the cases of source limitation imposed by global scale (Agren, 1985b). The GDB hy-
shade and sink limitation imposed by nutrient pothesis, however, addresses all environmen-
deficiency (be it the result of environmental tal factors affecting source-sink interactions,
impoverishment, defoliation, or reproductive thereby providing a more complete frame-
effort), the predictions of the GDB and CNB work for understanding phenotypic patterns
hypotheses are the same. Only the GDB hy- of secondary metabolism.
pothesis, however, predicts that sink limitation
imposed by extrinsic factors such as moderate Is PhenotypicPlasticity in Secondary
drought (Hsiao, 1973; Bradford and Hsiao, MetabolismAdaptive?
1982; Daie, 1988; Wardlaw, 1990; Luxmore,
1991) and low temperature (Pollock, 1990; Life history theory assumes that natural se-
K6rner, 1991) will result in the accumulation lection has shaped resource allocation pat-
of carbohydrates, and increased concentra- terns so as to maximize fitness (within genetic
tions of secondary metabolism. Consistent constraints) in different environments (Cody,
with the GDB hypothesis, several studies have 1966; Stearns, 1976, 1989a; Southwood, 1988;
shown concentrations of secondary metabo- Tilman, 1990). Plant fitness is strongly corre-
lites and other products of cellular differen- lated with the plant's ability to acquire and
tiation to increase in response to moderate retain resources. Within a population this abil-
drought (del Moral, 1972; Gershenzon, 1984; ity is usually positively correlated with growth
Lorio and Sommers, 1986; Allen et al., 1987; rate (Harper and White, 1974; Werner, 1975;
Mattson and Haack, 1987a,b; Ramachandra Solbrig, 1981; Westoby, 1984; Bloom et al.,
Reddy and Rama Das, 1988; Charles et al., 1985; Coleyetal., 1985; Bazzazetal., 1987;
1990; Ross and Berisford, 1990; Premachan- Pearcy et al., 1987; Peet and Christensen,
dra et al., 1991) and low temperature (Lin- 1987; Chapin, 1988; Fagerstr6m, 1989).
coln and Langenheim, 1978; Firmage, 1981; Hence, adaptive patterns of source-sink inter-
Appleton and van Staden, 1989; but see action should tend to maximize growth rate
Laine and Henttonen, 1987). within environmental constraints.
Extending the predictions of the GDB hy- The potential adaptiveness of phenotypic
pothesis to the effects of increased atmospheric plasticity is well recognized (Bradshaw, 1965;
CO2 on secondary metabolism requires an un- Caswell, 1983; Via and Lande, 1985; Grime
derstanding of how enhanced CO2 will alter et al., 1986; Schlichting, 1986; Schlichting

296 THE QUARTERLY REVIEW OF BIOLOGY VOLUME 67
and Levin, 1986; Stearns, 1989b; West-Eber- creased secondary metabolism will be favored
hard, 1989). Plasticity may enable plants to if that investment enhances plant fitness to a
assume the most adaptive phenotype in a par- degree greater than would the same resource
ticular environment, buffering the effects of investment in an alternative process such as
spatial and temporal variation in resource storage or growth. Increased secondary me-
availability (Grime et al., 1986; Robinson, tabolism in response to sink-limitation im-
1986; Crick and Grime, 1987; Szaniawski, posed by drought or nutrient limitation may
1987; West-Eberhard, 1989; Farrar and Wil- enhance survival by increasing stress toler-
liams, 1991). Plants display phenotypic plas- ance in harsh environments (del Moral, 1972;
ticity in such traits as growth rate, leaf area, Rhoades, 1977; Bariska and Pizzi, 1986;
root:shoot ratio, nutrient absorption rate, and Pizzi and Cameron, 1986; Moreland and
secondary metabolism (Chapin, 1980a; Bryant Novitzky, 1988; Meinzer et al., 1990), and
et al., 1983; Grime et al., 1986; Robinson, defense when the plant has limited ability to
compensate (via growth) for herbivory (Bry-
1986; Agren and Ingestad, 1987; Hirose,
ant et al., 1983; Gershenzon, 1984).
1988a,b; Hilbert, 1990). Species with inher-
Before a plastic response can be assumed
ently high growth rates may be generally
to be adaptive, it must be determined that
more plastic than those of slower growth
the plasticity results from genetically based
(Grime, 1979; Chapin, 1980a; Bryant et al.,
changes in the organism (developmental con-
1983; Grime et al., 1986). version) rather than a passive and incidental
Phenotypic patterns of secondary metabo- response to a variable environment (pheno-
lism may represent adaptive uses of limited typic modulation) (Smith-Gill, 1983). This
resources (del Moral, 1972; Gershenzon, has not been conclusively demonstrated in the
1984; Zangerl and Berenbaum, 1990). Geno- case of secondary metabolism. In many cases,
type x environment interactions (i.e., non- changes in secondary metabolism are corre-
parallel norms of reaction) represent the ge- lated with changes in the C/N balance of the
netic variation necessary for the evolution of plant. Experimental evidence, however, sug-
adaptive patterns of phenotypic plasticity, gests that phenotypic variation in secondary
and are commonly found when looked for metabolism results from highly regulated
(Bradshaw, 1965; Via and Lande, 1985; changes in biosynthetic pathways in response
Schlichting, 1986; Stearns, 1989b; van Noor- to environmental cues rather than an inciden-
dwijk, 1989). The presence of intraspecific tal response to environmental variation (del
variation in norms of reaction for secondary Moral, 1972; Chapin, Shaver, and Kedrow-
metabolism has been demonstrated in Abies ski, 1986; Mole et al., 1988; Lincoln and
grandis (grand fir) (Muzika et al., 1989), Men- Couvet, 1989; Johnson and Lincoln, 1990).
tha x verticillata(mint) hybrids (Maffei, 1990),
and Pastinaca sativa (wild parsnip) (Zangerl GROWTH-DIFFERENTIATION BALANCE
and Berenbaum, 1990). AND THE EVOLUTION OF PLANT
If phenotypic plasticity in secondary me- LIFE HISTORY STRATEGIES
tabolism is adaptive, then predicting patterns Interspecific comparisons reveal that in-
of secondary metabolism in response to envi- herently fast-growing plants have lower levels
ronmental variation requires a knowledge of of defense than inherently slow growing spe-
the costs and benefits of the different alloca- cies, and also generally experience higher lev-
tion patterns in the different environments. els of herbivory (Cates and Orians, 1975; Bry-
Three extreme phenotypes are possible: (1) ant and Kuropat, 1980; Chapin, 1980a; Coley,
rapid growth coupled with low secondary me- 1980, 1983, 1988; Mattson, 1980; Bryant et
tabolism, (2) slow growth coupled with high al., 1983, 1989; Coley et al., 1985; MacLean
secondary metabolism, and (3) slow growth and Jensen, 1985; Sheldon, 1987; Loehle,
coupled with low secondary metabolism (and 1988; Pimentel, 1988; Price, 1991). This pat-
high carbohydrate storage). Limited resources tern results from the genotypic manifestation of
preclude the fourth possibility of rapid growth the physiological trade-off between cell growth
coupled with high secondary metabolism. In- and differentiation processes.

This trade-off has ecological consequences ation processes, and vice versa. For example,
that affect the evolution of particular resource the growth of all higher plants is dependent on
allocation patterns in specific environments. the differentiation of vascular tissue (Wareing
In the rest of the paper, we relate the GDB and Phillips, 1981). Conversely, the elabora-
balance concept to the evolution of plant life tion of resin ducts and other specialized tis-
history patterns, focusing on these conse- sues differentiated for the compartmentation
quences. In doing so, we try to construct a of secondary metabolites is dependent on cell
hierarchical framework, linking physiologi- growth. Indeed, their size and number may
cal, ecological and evolutionary theories into be proportional to the growth rate of the plant
a unified system of theories explaining and during their construction phase (e.g., Bjork-
predicting patterns of plant defense in ecologi- man et al., 1991). Nonetheless, many differ-
cal and evolutionary time. entiation processes, including the production
of secondary metabolites and structural traits
The Growth-Differentiation
that limit herbivory, divert resources from the
Life History Continuum
production of leaf area, and thus act to con-
Stearns (1976) defined a life history tactic strain plant growth.
"as a set of coadapted traits designed by natu- The patterns we discuss are well recognized
ral selection to solve particular ecological and underpin other theories of plant life his-
problems" (p. 4). Competition and herbivory tory evolution (Grime, 1977, 1979; South-
(macro- and micro-) are the dominant biotic wood, 1977; Greenslade, 1983; Coley et al.,
forces that affect the fitness of plants. In con- 1985; Taylor et al., 1990). Growth-dominated
cert with abiotic factors, they shape the evolu- plants correspond with the competitive and
tion of plant life history tactics. Selection ex-
ruderal strategies of Grime (1977, 1979). They
erted by competitors and herbivores interacts
inhabit resource-rich environments, grow rap-
with resource availability to result in fitness
idly, possess low quantitative levels of chemi-
trade-offs associated with different resource
cal defenses, and are often characteristic of
allocation patterns in different environments.
early stages of secondary succession (Grime,
The set of integrated physiological traits that
1979; Coley et al., 1985; Huston and Smith,
minimizes the cost of these trade-offs in a par-
1987; Taylor et al., 1990). Differentiation-
ticular environrmient will be favored by natu-
dominated species have experienced "adver-
ral selection. We rank these sets of coadapted
sity-selection" (Southwood, 1977, 1988; Green-
traits along a growth-differentiation (G-D)
continuum of life history tactics. slade, 1983; Sibly and Grime, 1986) leading
Plant strategies can be classified according to the evolution of traits consistent with the
to the cumulative strength of growth relative stress tolerant strategy of Grime (1977, 1979).
to differentiation processes occurring within They typically inhabit resource-limited envi-
the plant, as indicated by the proportion of ronments, grow slowly, possess high levels of
total available resources allocated to each of defenses, and often occupy late-successional
these processes. Growth-dominated plants in- sites (Grime, 1979; Coley et al., 1985; Hus-
vest a high proportion of their resources into ton and Smith, 1987; Taylor et al., 1990).
processes and structures further enhancing The location of a species along the G-D
resource acquisition, resulting in high relative continuum of life history tactics may corre-
growth rates. Differentiation-dominated plants spond most closely to the degree of"I (Impov-
invest a high proportion of their resources into erishment)-selection" (sensu Taylor et al.,
the nongrowth processes and structures re- 1990) experienced by the plant. I-selection
quired to retain and make efficient use of intensifies as the mean annual magnitude of
resources under adverse environmental con- environmental carrying capacity (in the ab-
ditions and/or intense herbivory. The conse- sence of disturbance) decreases (Taylor et al.,
quence is a low relative growth rate. 1990). We predict that the proportion of re-
Obviously, growth processes are depen- sources allocated to differentiation processes
dent on and highly integrated with differenti- will increase as I-selection intensifies. Physio-

logical characteristics of growth-dominated TABLE 1

and differentiation-dominated plants are sum- Summaryof traitspredictedto be characteristic
of
marized in Table 1. growth-and differentiation-dominated
The G-D continuum differs from related perennialplants
life history classifications of Grime (1977, Differen-
1979), Southwood (1977, 1988), Greenslade Growth tiation
(1983), Coley et al. (1985), and Taylor et al. dominated dominated
(1990) by emphasizing the physiological pro- Plant trait plants plants
cesses and constraints underlying the tactics, Relative growth rate high low
rather than the habitats in which they evolve. Resource acquisition rate high low
Thus, we feel that the G-D continuum pro- Resource use efficiency low high
vides a useful framework, facilitating recogni- Resource turnover rate high low
tion and understanding of the physiological Allocation to leaf area high low
Storage reserves low high
and ecological constraints underlying the evo-
Degree of sclerophylly low high
lution of these tactics.
Secondary metabolism low high
Respiration rate high low
ECOLOGICAL CONSTRAINTS ON THE Proportion of respiratory
EVOLUTION OF PLANT DEFENSE energy supporting
The physiological trade-off between growth maintenance low high
Phenotypic plasticity high low
and differentiation processes constrains the
Constitutive resistance to
evolutionary responses of plants as they inter-
herbivores low high
act with their biotic and abiotic environ- Induced resistance to her-
ments. As plants respond to selection imposed bivores high low
by competition, their potential evolutionary Competitive ability
responses to herbivory become limited. Com- Resource-rich
petition occurs when two plants require the environments high low
same resources that are in short supply, re- Resource-limited
sulting in the decreased performance of one environments low high
or both (Grime, 1979; Tilman, 1985). Com- Sources: Grime, 1979; Chapin, 1980a; Coley et al.,
petition for several resources may occur si- 1985; Coley, 1987; Huston and Smith, 1987; Chapin et
al., 1990.
multaneously, and the relative ability of a
plant to acquire different resources may vary
(Tilman, 1985, 1986, 1988, 1990). The com-
petitive ability of a plant is ultimately mea-
and Keddy, 1986a,b; Shipley and Keddy,
sured by its ability to reproduce relative to
1988; McGraw and Chapin, 1989), and vice
other species with which it competes, and is a
function of the following traits: (1) the plant's versa (Chapin, 1980a; Shipley and Keddy,
rate of resource acquisition, (2) the rate at 1988; McGraw and Chapin, 1989).
which acquired resources are lost, and (3) the Traits conferring herbivore resistance and
efficiency of conversion of acquired resources competitive ability exhibit high phenotypic
to biomass (Goldberg, 1990). and genetic integration (sensu Schlichting,
Trade-offs may occur among traits maxi- 1989), hence the trade-offs between competi-
mizing competitive ability in different environ- tive ability in different environments have im-
ments resulting in genotype x environment portant implications for the evolution of plant
interactions in competitive ability (Shipley defense. Trade-offs among traits conferring
and Keddy, 1988; Tilman, 1988, 1990; Ber- competitive ability and herbivore resistance
endse and Elberse, 1990a,b). Plants adapted occur in high resource environments because
to resource-rich environments may have a of competition for a shared resource base. No
competitive advantage over plants adapted to such trade-offs occur in low resource environ-
resource-limited environments when they are ments because secondary metabolism may
grown together under high resource condi- enhance stress tolerance and competitive abil-
tions (Mahmoud and Grime, 1976; Wilson ity, as well as herbivore resistance.

Resource-RichEnvironmentsFavor Inducible Resistance

Growth-DominatedPlants Rapid inducible resistance (rapid accumu-
In resource-rich environments abiotic con- lation of secondary metabolites in response to
straints on plant strategies are minimal, and injury from insects or pathogens) may be an
a variety of allocation strategies with different adaptation minimizing the cost of defense
growth rates are theoretically possible (Til- (Edwards and Wratten, 1983; Haukioja,
man, 1988, 1990; Smith and Huston, 1989). 1990). Unlike constitutive resistance (resis-
The carrying capacity of even the richest envi- tance mechanisms present prior to injury),
ronments is limited, however, and slow- the cost of rapid inducible resistance is in-
growing plants risk the preemption of water, curred only when needed. This cost, how-
nutrients, light and space by faster-growing ever, may be substantial if the response is
competitors. Competition limits the potential intense and sustained (Baldwin et al., 1990).
successful allocation patterns in resource-rich The expression of induced resistance may
environments (Mooney and Dunn, 1970; Til- be limited to rapidly growing plants and tis-
man, 1988, 1990; Smith and Huston, 1989). sues, being weak or nonexistent in slow grow-
Competitive success in resource-rich envi- ing plants and tissues (Haukioja and Nie-
ronments requires rapid acquisition of re- meli, 1979; Wratten et al., 1984; Braga et
sources, and thus is dependent upon maximal al., 1986, 1991; Edwards and Wratten, 1987;
allocation of resources to the vegetative struc- Frischknecht et al., 1987; Baldwin, 1988;
Apostol et al., 1989). In cell cultures, induc-
tures (stems, foliage and roots) used to ac-
tion is strongest in growing cells, but growth
quire those resources (Grime, 1977, 1979;
is temporarily interrupted upon induction as
Tilman, 1988, 1990). Associated traits in-
resources are diverted from primary to sec-
clude high intrinsic rates of growth, nutrient
ondary metabolic pathways (da Cunha, 1987;
uptake, photosynthesis, respiration, transpi-
Eilert, 1987; Threlfall and Whitehead, 1988).
ration and allocation to leaf area (Grime,
Detoxification enzymes may protect imma-
1977, 1979; Bazzaz, 1979; Chapin, 1980a,
ture cells from autotoxicity during wound-
1988; Mooney and Gulmon, 1982; Grime et
induced secondary metabolite accumulation
al., 1986; Chapin et al., 1987; Huston and
(McKey, 1974; Hendry, 1986). Constitutive
Smith, 1987; Gaudet and Keddy, 1988; Gold-
levels of detoxification enzymes decline as
berg, 1990; Taylor et al., 1990; Berendse and
cells mature, however, their synthesis may
Elberse, 1990a,b).
continue to be induced by the same elicitors
that induce secondary metabolism (Hendry,
Optimal Defense in Growth-DominatedPlants
1986).
Lost growth and resource acquisition is the The biological significance of induced resis-
greatest cost of defense in resource-rich envi- tance has been questioned because of the lack
ronments (Chapin, 1989; Fagerstr6m, 1989). of studies demonstrating dramatic effects on
These indirect costs, coupled with the direct herbivore fitness parameters (Fowler and
costs of energy and biomass invested in their Lawton, 1985). Because of the semiautono-
construction and maintenance, constrain the mous nature of plant modules coupled with
evolution of high levels of defense in resource- the ability of plants to compensate (to varying
rich environments (Feeny, 1976; Rhoades degrees) for herbivory, the impact of a given
and Cates, 1976; Rhoades, 1979; Bryant et amount of herbivory on plant growth and re-
al., 1983; Coley et al., 1985; Coley, 1987). production is less when it is dispersed among
Growth-dominated plants, however, possess many modules rather than concentrated on a
adaptations that optimnizethe benefits of mini- few (Stephenson, 1980; Watson and Casper,
mal defensive investments, thus their realized 1984; Marquis, 1988, 1992; Tuomi, Nie-
cost of defense may be small. In fact, efforts meli, Rousi, Siren, and Vuorisalo, 1988). A
to detect and measure this cost in plants with primary effect of inducible resistance may be
rapid inherent growth rates have met with to disperse the consumption of free-feeding
little success (Simms and Rausher, 1987, 1989; herbivores such as Lepidoptera larvae (Ed-
Brown, 1988). wards and Wratten, 1983, 1987; Silkstone,

1987; Gibberd et al., 1988; Wratten et al., ments where these nutrients are unlikely to
1988; Croxford et al., 1989; Raupp and Sa- limit growth (Levin, 1976b; Mattson, 1980;
dof, 1989; but see Bergelson et al., 1986 and Bernays, 1983; Bryant et al., 1983). These
Bergelson and Lawton, 1988), thereby min- metabolites may often be metabolized and re-
imizing impact on any one module and on cycled through primary metabolism (Rob-
overall fitness reduction of the plant (Janzen, inson, 1974; Seigler and Price, 1976; Wink
1979). Dispersal may also increase the expo- and Witte, 1985; Frischknecht et al., 1986;
sure of herbivores to natural enemies, poten- Selmaretal., 1988; Harborne, 1990). Hence,
tially providing plants with an indirect benefit these "qualitative"secondary metabolites (sensu
of induced secondary metabolism (Schultz, Feeny, 1976) may be cost effective for two
1983a,b; but see Bergelson and Lawton, 1988). reasons: they are effective at low concentra-
The dispersion of feeding is due presumably tions, and they are removed only temporarily
to the local accumulation of secondary metab- from the plant's primary metabolic resource
olites with deterrent properties. Inducible re- pool (but see Mihaliak et al., 1991).
sistance may be favored by natural selection Plants may further optimize a small defen-
if it decreases the negative impact of herbiv- sive investment by allocating secondary me-
ory on whole plant fitness, even without de- tabolites in direct proportion to tissue value
creasing herbivore fitness or the total tissue and vulnerability (McKey, 1974, 1979; Feeny,
loss sustained by the plant (Janzen, 1979; 1976; Rhoades and Cates, 1976; Rhoades,
Haukioja, 1990; Haukioja et al., 1990). Zan- 1979). For example, Nitao and Zangerl (1987)
gerl and Berenbaum (1990) provide the first found that furanocoumarin concentrations
evidence for heritable variation in induced increased in the reproductive structures of
plant resistance to an insect. Pastinaca sativa (wild parsnip) during the de-
Rapidly induced resistance (hypersensitiv- velopmental stages at which their loss to her-
ity) may have more direct and profound ef- bivores would have the greatest negative im-
fects on less mobile and imbedded insects such pact on fitness.
as bark beetles, leafminers, galling insects, Metabolites that result in little or no feed-
and adelgids (Fernandes, 1990). These in- ing when present in small concentrations have
sects generally have a more intimate and spe- an especially favorable cost:benefit ratio for
cific ecological and evolutionary relationship the plant. In fact, behavioral deterrents may
with their hosts than do free-feeding folivores, be the primary reason why plants escape the
creating the opportunity for the evolution of vast majority of herbivores present in their
more specific host defenses (Mattson et al., environments (Dethier, 1980; Bernays and
1988; Fernandes, 1990). Chapman, 1987). Because some deterrents
are nontoxic when ingested, it has been ques-
Potent but Low Levels of tioned whether behavioral deterrents repre-
Constitutive Defenses sent evolved defenses to herbivores (Bernays
The defenses of growth-dominated plants and Graham, 1988; Wrubel and Bernays,
adapted to resource-rich habitats are often 1990). If herbivory decreases plant fitness,
based on low concentrations of highly potent, however, the evolution of secondary metabo-
low-molecular-weight toxins and deterrents. lites that decrease herbivory should be fa-
Often these are highly oxygenated carbon- vored, regardless of whether they are toxic to
based compounds, such as polyketides and organisms that avoid them.
terpenoids (Gottlieb, 1989), or nitrogen-based
and sulfur-based compounds such as alka- Circumventing the Opportunity
loids, cyanogenic glycosides and glucosino- Cost of Secondary Metabolism
lates (McKey, 1974, 1979; Feeny, 1976; Immature leaves are most nutritious to her-
Levin, 1976a,b; Rhoades and Cates, 1976; bivores because of their high concentrations
Mattson, 1980; Mooney et al., 1983; Coley of nutrients and water, and low concentra-
et al., 1985). The reliance on nitrogen-based tions of structural components (Coley, 1980,
and/or sulfur-based toxins may be especially 1983; Mattson, 1980; Ayres and MacLean,
prevalent in plants evolving in fertile environ- 1987; Mattson and Scriber, 1987; Kursar and

SEPTEMBER 1992 THEDILEMMAOFPLANTS: TOGROWORDEFEND 301
Coley, 1991). Consequently, young leaves fre- penoid resins over newly expanding foliage
quently experience higher levels of herbivory (Rhoades, 1977; Dell and McComb, 1978;
than mature leaves (Coley, 1980; Krischik Williams et al., 1983; Johnson et al., 1984;
and Denno, 1983; Raupp and Denno, 1983; Fahn, 1988; Zobel and Brown, 1990a,b). Cot-
Ernest, 1989; Mitchell Aide and Lodofio, tonwood (Populus deltoides) buds accumulate
1989; Nuniez-Farfan and Dirzo, 1989). Yet, resin in late summer and secrete it over
at least in indeterminate plants, the value of emerging leaves the following spring, thus en-
a leaf is highest when it is young, because the hancing their resistance to a leaf beetle (Curtis
future return on photoassimilates reinvested and Lersten, 1974) and gypsy moth (Lyman-
into vegetative structures declines as the leaf tria dispar) (Meyer and Montgomery, 1987).
ages (Harper, 1989). Thus it should be adap- The resistance of young cottonwood leaves
tive to defend young leaves. A dilemma re- to gypsy moth declines rapidly as the leaves
sults because increased defense during can- expand (Meyer and Montgomery, 1987) and
opy expansion diverts resources from more the surface resin is diluted, volatilized and/or
leaf production. weathered (Shain and Miller, 1982). While
The opportunity cost of defense will vary, late-season secondary metabolism may not
however, depending upon when it is assessed decrease the current year's growth, it may di-
over the course of the plant activity cycle. In vert resources from the storage reserves
many ecosystems, soil moisture and micro- needed to support maximal growth the follow-
bial-mediated nutrient availability peak early ing season (Chapin et al., 1990).
in the growing season (Chapin, 1980a; Gut-
schick, 1981; Lee et al., 1981). Accordingly, Bimodality in Phenological
many plants complete their growth phase with Patterns of Leaf Defense
an intense but short flush corresponding with Concentrations of low-molecular-weight
the temporal availability of the resources re- secondary metabolites are frequently highest
quired to drive growth. This is followed by a in buds and immature leaves, and decline as
longer period of differentiation and continued leaves expand (McKey, 1974; Rhoades and
photoassimilation. As growth slows, alloca- Cates, 1976; Cates and Rhoades, 1977; Palo,
tion to other processes such as defense and 1984; Frischknecht et al., 1986; Aerts et al.,
storage often increases (Mooney and Chu, 1991; Porter et al., 1991). These initial defen-
1974; McLaughlin and McConathy, 1979; sive investments may appear substantial when
Chung and Barnes, 1980a; Dickson, 1989; expressed as a foliar concentration. Concen-
Chapin et al., 1990; Wardlaw, 1990). These trations calculated for small immature leaves,
processes are then supported without a trade- however, do not necessarily translate into
off with growth (i.e., Tuomi et al., 1983). large absolute investments based on the total
Thus, secondary metabolites may be synthe- pool of resources driving canopy expansion
sized when the opportunity costs are low, and (McKey, 1974; Aerts et al., 1991). As leaf mat-
stored for future use when defense is con- uration proceeds, concentrations of these quali-
strained. tative defenses generally decline as a result of
Secondary metabolites may often be bio- dilution as leaves expand and/or the cycling of
synthesized late in the season and used for the low-molecular-weight secondary metabolites
defense of overwintering buds and expanding into primary metabolism (Wink and Witte,
tissue (Bryant et al., 1983). For example, the 1985; Frischknecht et al., 1986; Selmar et al.,
surface resins providing birch (Betula spp.) 1988; Bodnaryk and Palaniswamy, 1990; Zo-
twigs with browsing resistance (Reichardt et bel and Brown, 1990a,b). Low-molecular-
al., 1984; Rousi et al., 1991) are biosynthe- weight phenolics may be converted to lignin
sized before and after periods of intensive or tannin polymers (Dawra et al., 1988). As
growth (Lapinjoki et al., 1991), and the resin leaf maturation proceeds, leaves are protected
duct system protecting some conifers from by increasing concentrations of high-molecu-
bark beetles is constructed after the period of lar-weight polymers such as lignin and tannins
intense growth (Lorio, 1986, 1988). ("quantitative" defenses) and structural de-
Many plants secrete stored phenolic or ter- fenses (Dement and Mooney, 1974; Mooney

and Chu, 1974; Feeny, 1976; Rhoades and through minor mutations in metabolic path-
Cates, 1976; Cates and Rhoades, 1977; ways, however, resulting in the production of
McKey, 1979; Coley, 1983; Potter and Kim- a more diverse and/or toxic array of metabo-
merer, 1986; Cates, 1987; Mattson and lites (Berenbaum, 1978, 1981, 1983; Bowers
Scriber, 1987; Hatcher, 1990). Bimodality in and Puttick, 1988; Berenbaum et al., 1989,
phenological patterns of leaf defense appears 1991; Jones and Firn, 1991). A battery of
to be a general phenomenon, and may explain secondary metabolites provides the potential
the observation of Coleman (1986) that leaves for simultaneous resistance to a variety of her-
are most vulnerable to herbivores and stress bivores (Levin, 1976a; McKey, 1979; Bowers
as they make the transition from photosyn- and Puttick, 1988; Pearson, 1989; Jones and
thetic sinks to photosynthetic sources. Firn, 1991). Furthermore, some of the di-
verse secondary metabolites possessed by in-
Genetic Mosaics and Qualitative Variation dividual plants may be synergistic in their
The modular construction of plants may antiherbivore activity, enhancing the benefit:
have important evolutionary implications for cost ratio of a given defense investment (Mc-
plant defense (although there is little support- Key, 1979; Berenbaum, 1985; Kubo and
ing empirical evidence). This may be espe- Hanke, 1985; Berenbaum et al., 1991). Qual-
cially true of fast-growing plants that have the itative changes in secondary metabolism that
potential for large increases in their number do not alter the balance of resources between
of modules from one year to the next. Unlike growth and secondary metabolism will have
animals that maintain a separate germ line, no cost to the plant in the form of reduced
plants are characterized by somatic embryo- competitive ability.
genesis in which all tissues retain the potential Rapid evolution of variation in plant chem-
for reproductive differentiation. Consequently, istry could result from changes in the expres-
somatic mutations within a tissue may be trans- sion and repression of already existing meta-
mitted to all progenal modules, incorporated bolic pathways, rather than their de novo
into their gametes, and passed to future gen- generation. Novel secondary metabolites not
erations (Whitham and Slobodchikoff, 1981; detected in the intact plant are sometimes bio-
Mattson et al., 1982; Buss, 1983; Whitham synthesized in cell culture (Jalal and Collin,
et al., 1984; Jerling, 1985; Tuomi and Vuori- 1977; DiCosmo and Towers, 1984; Ban-
salo, 1989a,b). In fact, genetic mosaicism in thorpe and Brown, 1989). This phenomenon
plants is well documented (Whitham et al., suggests the existence of repressed pathways.
1984). A mosaic of variable defensive traits Somatic mutation in regulatory genes may
could be adaptive, allowing long-lived and result in qualitative variation in the expres-
clonally reproducing plants to negate the ap- sion of secondary metabolism, permitting a
parent evolutionary advantage of short-lived, rapid evolutionary response to herbivory
rapidly evolving herbivores (Whitham and (Bowers and Puttick, 1988; Jones and Firn,
Slobodchikoff, 1981; Whitham et al., 1984; 1991).
Antolin and Strobeck, 1985).
Qualitative variation may represent an Defensive Mutualisms
adaptive alternative to quantitative increases Plants may co-opt the third trophic level as
in constitutive defense (Bowers and Puttick, part of their own defense (Price et al., 1980;
1988; Pearson, 1989; Jones and Firn, 1991). Barbosa and Saunders, 1985; Wisdom, 1985).
Indeed, plants may have evolved specific ad- Defensive mutualisms may be a relatively in-
aptations for maintaining phytochemical di- expensive alternative to defensive chemistry,
versity (Jones and Firn, 1991). If an herbi- lacking the biosynthetic and maintenance
vore is capable of detoxifying a particular costs of secondary metabolism (Rehr et al.,
secondary metabolite, then incremental in- 1973). Ants frequently serve as "pugnacious
creases in secondary metabolism will not nec- bodyguards," actively defending plants from
essarily equate to incremental increases in de- herbivores in return for shelter and/or nour-
fense (Tallamy and Krischik, 1989). Plants ishing secretions from extrafloral nectaries
may increase their resistance to herbivores (Janzen, 1966; Bentley, 1977; Beattie, 1985).

The activity of pugnacious bodyguards is of- through the synthesis of secondary metabo-
ten primarily associated with young, vigor- lites (Carroll, 1988; Clay, 1988, 1990). Endo-
ously growing tissue (Janzen, 1972; Down- phytes may provide plants with novel chemi-
hower, 1975; Bentley, 1977; Letoumeau, cal defenses (Carroll, 1988), allowing plants
1983; McKey, 1984; Koptur, 1985). As such, to circumvent phylogenetic constraints on the
they may be valuable adaptations for the de- evolution of new secondary metabolites (i.e.,
fense of undifferentiated tissue in which Harborne, 1990).
chemical and structural defense is physiologi-
cally constrained (McKey, 1984). Compensatory Responses to Herbivory
Plants may regulate the activity and com- Compensatory growth may represent an
position of secretions, optimizing their cost: evolved alternative to chemical defense as a
benefit ratio (Bentley, 1977). Piper cenocladum strategy for reducing net losses to herbivores,
fails to produce food bodies harvested by ants especially in resource-rich environments sub-
when ants are absent (Risch and Rickson, ject to intense and predictable herbivory (Matt-
1981). Extrafloral nectaries of Prunus serotina son and Addy, 1975; McNaughton, 1983;
(black cherry) are most active during the nar- Mattson et al., 1988, 1991; van der Meijden
row phenological window in which its major et al., 1988; Chapin and McNaughton, 1989;
defoliator, Malacosomaamericanum,is most sus- Westoby, 1989). Such is the case in the Ser-
ceptible to ant predation (which also coincides engeti grasslands, subarctic salt marshes, and
with leaf expansion) (Tilman, 1978). Finally, coral reef systems, where as much as 90 per-
artificial defoliation of Impatiens sultani in- cent of net primary production is consumed
duces a short-term increase in the amino acid annually by herbivores (McNaughton, 1984;
concentration of its secretion, increasing the Hay and Fenical, 1988; Westoby, 1989).
cost of the secretion, and potentially the bene- Compensation is based on primary metabolic
fit. It is not known, however, if its increased activity, hence it does not incur the opportu-
nutritional value attracts more bodyguards nity costs associated with chemical defense
(Smith et al., 1990). (Mattson et al., 1988, 1991). Furthermore, the
Some plants may actively recruit the natu- response directly enhances competitive ability.
ral enemies of their herbivores. In response Plants adapted to heavy grazing have
to herbivore damage, some plants release vol- evolved compensatory mechanisms that may
atile chemicals that attract predators and par- allow grazed plants to approach or even ex-
asites of the herbivore (Dicke and Sabelis, ceed their net production in the absence of
1990; Dicke et al., 1990; Whitman and Eller, herbivores (McNaughton, 1983; Paige and
1990; Turlings et al., 1990). Recruiting body- Whitham, 1987; Hay and Fenical, 1988; West-
guards by releasing low concentrations of vol- oby, 1989). Compensatory growth may result
atiles only when herbivores are present and from altered allocation patterns that increase
feeding may be an especially cost-effective de- the proportion of plant biomass allocated to
fense strategy (Dicke and Sabelis, 1990). foliage production, and/or increased rates of
Many plants shelter predacious mites in photosynthesis in remaining foliage (Wareing
domatia elaborated on maturing leaves and et al., 1968; Verkaar et al., 1986; Brown and
branches (O'Dowd and Willson, 1989, 1991; Ewel, 1988; Oesterheld and McNaughton,
Willson, 1991). Nearby domatia garrison 1988, 1991;Prinsetal., 1989; Stafford, 1989;
mites for the rapid colonization and protec- Welter, 1989). Higher net photosynthesis in
tion of new growth where they consume phy- defoliated plants may result from increased
tophagous mites and fungi (O'Dowd and allocation of nitrogen to photosynthetic en-
Willson, 1989, 1991). Domatia may be espe- zymes (Wareing et al., 1968; Kolodny-Hirsch
cially cheap as they require only their initial et al., 1986), improved water balance (Turner
formation (O'Dowd and Willson, 1989). and Heichel, 1977; Heichel and Turner,
Endophytic fungi systemically infect and 1983), increased light penetration within the
form nonpathogenic mutualisms with plants, canopy (Welter, 1989), and/or enhanced nu-
deriving energy from their host while pro- trient availability resulting from defoliation-
tecting it from herbivores and pathogens induced increases in the rate of nutrient cy-

cling (Mattson and Addy, 1975; Chapin, berg, 1990). Stress-tolerant plants also allo-
Vitousek, and Van Cleve, 1986; McNaugh- cate an especially high proportion of available
ton et al., 1988; Westoby, 1989). Little or energy to maintenance respiration (G. J. Tay-
no compensation occurs in nutrient-stressed lor, 1989). An inherently low rate of growth
or water-stressed plants (Coughenour et al., may be an inevitable consequence of these
1985; McNaughton and Chapin, 1985; Ver- traits (Chapin, Groves, and Evans, 1989;
kaar et al., 1986; Chapin and McNaughton, Poorter, 1990). Growth rate has been shown
1989; Georgiadis et al., 1989; Maschinski to be inversely correlated with tolerance to
and Whitham, 1989; Stafford, 1989). nutrient (Shipley and Keddy, 1988) and wa-
The high degree of integration among ter limitation (Premachandra et al., 1991).
modules characteristic of grasses and some
other species (Watson and Casper, 1984) may Low Resources Favor Substantive
contribute to compensatory ability. This inte- Constitutive Chemical Defense
gration may facilitate the rapid mobiliza- In resource-limited environments, several
tion of stored resources. The exchange of re- factors interact to favor the selection of high
sources among ramets of clonal plants may levels of secondary metabolism. These in-
allow an integrated response to herbivory at clude intense selection pressure from herbi-
the genet level (Marshall and Sagar, 1965; vores, low opportunity cost of carbon-based
Ashmun et al., 1982; Welker et al., 1985, secondary metabolism, and the direct contri-
1987; Schmid et al., 1990). bution of secondary metabolism to competi-
tive ability. Traits minimizing herbivory in
ResourceScarcityFavors resource-limited environments are important
Differentiation-DominatedPlants because of the low potential of plants in these
Although competition occurs in low re- environments to compensate for herbivory
source environments (Fowler, 1986; Chapin, through growth, coupled with the lengthy ex-
McGraw, and Shaver, 1989; DiTommaso and posure of long-lived foliage to herbivores
Aarssen, 1989; Tilman, 1989; Tilman and (Janzen, 1974; McKey et al., 1978; Bryant
Cowan, 1989; Taylor et al., 1990), environ- and Kuropat, 1980; Chapin, 1980a; Gartlan
mental constraints on plant growth may limit et al., 1980; Mattson, 1980; Chabot and
its intensity (Reader and Best, 1989; Kadmon Hicks, 1982; Bryant et al., 1983, 1988; Coley
and Shmida, 1990; Reader, 1990). In con- et al., 1985; Southwood et al., 1986; Coley,
trast to resource-rich environments where 1987; Oksanen, 1990; D. R. Taylor et al.,
competitive success is dependent on maximiz- 1990).
ing the rate of resource acquisition, success in The physiological and ecological constraints
resource-limited environments (light, nutri- on the evolution of chemical defenses in plants
ents, and water) is dependent on the more are diminished in resource-limited environ-
conservative strategy of maximizing the re- ments. When shortages of nutrients and/or
tention and efficient use of scarce resources water limit growth, the opportunity cost (in
(Grime, 1979; Chapin, 1980a, 1988; Chabot the form of sacrificed growth) of secondary
and Hicks, 1982; Vitousek, 1982; Grime et metabolism is low (Coley et al., 1985; Cha-
al., 1986; Tilman, 1988, 1990; Berendse and pin, 1989; Fagerstrom, 1989; Oksanen, 1990).
Elberse, 1990a,b; Goldberg, 1990; Taylor et In fact, plants adapted to resource-limited en-
al., 1990). Correlated traits include low meta- vironments are characterized by a substantial
bolic rates, sclerophyllous long-lived leaves, investment in carbon-based allelochemicals
high rates of nutrient retranslocation prior to (Janzen, 1974; McKey et al., 1978; Gartlan
tissue abscission, high root:shoot ratios, and et al., 1980; Mattson, 1980; Bryant et al.,
growth rate insensitivity coupled with luxury 1983, 1985; Coley et al., 1985; Reichardt et
consumption in response to pulses of in- al., 1990). Structural defenses in the form of
creased resources (Grime, 1977, 1979; Cha- thorns and spines may be less common in re-
pin, 1980a, 1988; Grubb, 1986; Grime et al., source-limited than in resource-rich environ-
1986; Chapin et al., 1987; Huston and Smith, ments (Campbell, 1986; Owen-Smith and
1987; Berendse and Elberse, 1990a,b; Gold- Cooper, 1987), possibly because their elabo-

ration is dependent on growth processes. Al- most advantageous when they occur against
though high levels of secondary metabolism low background levels of other defenses. In
may not divert resources from growth in re- agreement, Lewinsohn, Gijzen, and Croteau
source-limited environments, trade-offs may (1991) found the wound-induced accumula-
occur between secondary metabolism and the tion of monoterpenes in the stems of conifer
accumulation of storage carbohydrates and/or saplings to be inversely correlated with their
the high level of maintenance respiration nec- constitutive secondary metabolite levels.
essary to tolerate adverse environmental con-
ditions. Nutritional Barriers to Herbivory
The low nutritional quality of plants grow-
Inducible Defenses Are Limited ing in resource-limited environments may
Rapid inducible resistance may generally provide a substantial ecological (T. C. R.
be weak or nonexistent in the leaves of slow- White, 1978, 1984; Mattson, 1980) and evo-
growing plants and modules (Braga et al., 1986, lutionary (Southwood, 1973) barrier to her-
1991; Edwards and Wratten, 1987; Frisch- bivory. Herbivory may, in fact, select for
knecht et al., 1987; Apostol et al., 1989; Hau- traits that further lower the nutritional quality
kioja, 1990). This may result from inherent of their hosts, including the dilution of essen-
physiological constraints. The biosynthesis of tial nutrients and the evolution of indigestible
phytoalexins requires rapid de novo synthesis structural components such as cellulose, hemi-
of proteins (Dixon, 1986; Ebel, 1986). Thus, cellulose and lignin (T. C. R. White, 1978;
their production may be limited to tissue with Neuvonen and Haukioja, 1984; Mattson and
high metabolic activity containing high levels Scriber, 1987; Pimentel, 1988; Duchesne and
of water, nitrogen and other nutrients (Braga Brainerd, 1989; Lundberg and Astrom,
etal., 1986, 1991; Eilert, 1987; Apostoletal., 1990; Abe, 1991; Haukioja et al., 1991). Nu-
1989). This may impose a major constraint trient dilution, however, can be a double-
on phytoalexin synthesis in differentiation- edged sword if herbivores increase their con-
dominated plants. Furthermore, the speed of sumption to compensate for a low-quality diet
the induction process largely governs its effi- (Moran and Hamilton, 1980; Price et al.,
cacy, because defenses must build faster than 1980; Clancy and Price, 1987). Among in-
the growth and spread of the colonizing organ- sects, compensatory consumption may be a
isms. Differentiation-dominated plants may be common phenomenon (Slansky and Feeny,
poorly adapted to utilize such defenses be- 1977; Johnson et al., 1985; Slansky and
cause of hydraulic constraints on the translo- Scriber, 1985; Lincoln et al., 1986; M. F. J.
cation of hormonal signals, nutrients, and/or Taylor, 1989; Simpson and Simpson, 1990;
metabolites to and from sites of herbivore in- Slansky, in press). The plant can nevertheless
jury (e.g., Braga et al., 1991). Foliar-induced benefit if herbivore mortality rates increase
resistance is not common in conifers (Wagner, concomitantly with consumption through in-
1988), the leaves of which are poorly vascu- creased exposure to parasites, predators and
larized and have lower rates of solute trans- pathogens, or heightened deleterious effects
port compared to those of angiosperms (Bond, of ingested allelochemicals (Lawton and Mc-
1989). Neill, 1979; Schultz, 1983a,b; Wisdom, 1985;
Ecological constraints may also limit the Loader and Damman, 1991; Slansky, in
adaptive value of rapid induced resistance in press). Moreover, compensatory feeding is
differentiation-dominated plants. High con- seldom perfect so that reproductive capacities
stitutive levels of secondary metabolites may are usually diminished, resulting in a lower
decrease the benefit of inducible resistance be- potential rate of population increase (Neuvo-
cause incremental increases in secondary me- nen and Haukioja, 1984; Slansky and Scriber,
tabolism are unlikely to be effective against 1985; Slansky, in press).
colonizing organisms with detoxification sys- The balance of evidence suggests that low
tems adapted to the already high constitutive nutritive quality, high concentrations of sec-
concentrations of secondary metabolites (Matt- ondary metabolism, and tough, sclerophyl-
son et al., 1988). Inducible defenses may be lous foliage interact to provide formidable

barriers to herbivory in low resource environ- tion, photooxidation, desiccation) (del Moral,
ments (Bryant and Kuropat, 1980; Coley, 1972; Moreland and Novitzky, 1988; Meinzer
1980, 1983, 1987; Mattson, 1980; Bryant et et al., 1990); and (3) for the removal of the
al., 1983; Mattson and Scriber, 1987; Slan- otherwise toxic levels of free ammonia that
sky, in press). generally accumulate in response to stress
(Rabe, 1990), by cycling the ammonia through
Correlated Selection for Differentiation the shikimic acid pathway resulting in pheno-
Processes by Herbivory, Competition, lic accumulation as phenylalanine is continu-
and the Abiotic Environment ally synthesized and subsequently deami-
In resource-limited environments, differ- nated. All of the preceding may interact to
entiation processes that limit herbivory may select for a role of secondary metabolism in
also contribute to the competitive success of decreasing feedback inhibition of photosyn-
the plant. For example, sclerophyllous leaves thesis in low resource environments (Haslam,
may enhance tolerance to drought stress and 1986).
nutrient limitation as well as represent a sig-
nificant barrier to herbivory (Loveless, 1962; THE EVOLUTION OF PLANT DEFENSE
Coley, 1983; Grubb, 1986; Oertli et al., 1990). It has been argued that herbivores have lit-
Foliar surface resins may protect plants from tle effect on plant fitness (Jermy, 1984). A
desiccation in arid environments (Rhoades, large number of studies, however, document
1977; Meinzer et al., 1990), and tannins may negative effects of herbivory on components
contribute to drought tolerance by increasing of plant fitness including survival, growth,
the elastic resilience of cell walls (Bariska and reproduction and competitive ability (Jan-
Pizzi, 1986; Pizzi and Cameron, 1986). Sec- zen, 1971; Rockwood, 1973; Wargo, 1977;
ondary metabolites may also directly increase Morrow and LaMarche, 1978; Bentley and
competitive ability through allelopathic ef- Whittaker, 1979; Rausher and Feeny, 1980;
fects on neighboring plants (Fowler, 1986). Krischik and Denno, 1983; Louda, 1984;
Increased secondary metabolism may con- Marquis, 1984, 1992; Wright et al., 1984;
tribute to the maintenance of high levels of Crawley, 1985, 1989a,b; Belsky, 1986; Cot-
photosynthesis. Under growth-limiting condi- tam et al., 1986; Elmqvist et al., 1987; Paulis-
tions, end-product accumulation can result in sen, 1987; Hendrix 1988; Sacchi et al., 1988;
feedback inhibition of photosynthesis (Neales Myster and McCarthy, 1989; Wisdom et al.,
and Incoll, 1968; Foyer, 1987, 1988; Korner, 1989; Louda et al., 1990; Prins and Nell,
1991; Luxmore, 1991). Photosynthates, how- 1990b; Wong et al., 1990; Strauss, 1991).
ever, may be shunted into secondary meta- Direct evidence that herbivores can select
bolic pathways minimizing the accumulation for enhanced plant defense is accumulating
of photosynthetic end products at their site (Simms and Fritz, 1990; Marquis, 1991). Dif-
of synthesis, possibly resulting in increased ferent genotypes within a population must be
carbon accumulation (overflow metabolism) impacted differentially by herbivores if her-
(Hoffmann, 1985; Haslam, 1986; Moleetal., bivory is to select for increased resistance.
1988; Waterman and Mole, 1989). Such variation has been shown to exist in Piper
We propose three adaptive hypotheses for arieianum(Marquis, 1984,1990). Genetic vari-
the existence of overflow metabolism sus- ation also exists within Salix lasiolepis (arroyo
tained by secondary metabolite synthesis in willow) for resistance to a gall-forming sawfly
low resource environments. Overflow metab- (Fritz and Price, 1988; Fritz, 1990), which
olism may provide: (1) the photosynthates can have negative effects on reproduction
needed to support the high level of mainte- (Sacchi et al., 1988). Maddox and Root (1987)
nance respiration required to tolerate adverse demonstrated heritable variation in Solidago
environmental conditions (Gale and Zeroni, altissima (goldenrod) resistance to a number
1985; G. J. Taylor, 1989); (2) the high con- of insects. Ipomoeapupurea (annual morning
centrations of secondary metabolites required glory) was shown to experience directional
for herbivore defense (Coley et al., 1985) and selection from insect herbivores for increased
protection from abiotic stress (e. g., UV radia- resistance to the Heliothis zea (corn earworm)

SEPTEMBER 1992 THEDILEMMA OFPLANTS: TO GROWOR DEFEND 307
(Rausher and Simms, 1989; Simms and et al., 1988). Furthermore, patterns of defen-
Rausher, 1989). sive investment will reflect the frequency and
The existence of genetic variation in pat- severity of herbivory experienced by popula-
terns of secondary metabolism within plant tions over evolutionary time (Feeny, 1976;
species (Hanover, 1966b; McKey, 1979; Ju- Rhoades and Cates, 1976; Chew and Court-
vik and Stevens, 1982; Berenbaum et al., ney, 1991).
1986; McDougal and Parks, 1986; Sanlaville
et al. , 1988; Altman et al., 1989; Kakes, 1989; Resource Availability:
Matzinger et al., 1989; Mihaliak et al., 1989; The Growth Rate Hypothesis
Zangerl and Berenbaum, 1990) creates the The resource availability hypothesis ex-
potential for herbivores to exert selection on tends the optimal defense hypothesis, pre-
those patterns. Berenbaum et al. (1986) dem- dicting that the optimal level of defense will
onstrated experimentally that insects can ex- vary with the growth rate of the plant (Coley
ert selection on plant secondary chemistry. et al., 1985; Coley, 1987; Jing and Coley,
In fact, phylogenetic patterns in angiosperms 1990). The quantity of resources (water, nu-
indicate that the trend has been toward the trients and light) available in the environment
evolution of more toxic secondary metabolites to support growth interacts with herbivory to
(Gottlieb, 1989, 1990; Harborne, 1990). determine quantitative patterns of defense
(Janzen, 1974; Bryant et al., 1983; Coley et
EvolutionaryModels of Plant Defense al., 1985; Coley, 1987). As the potential
Three contrasting yet complementary evo- growth rate of the plant decreases, the optimal
lutionary models have emerged to explain level of defense increases (Coley et al., 1985).
quantitative and qualitative patterns of plant In resource-rich habitats, competition favors
defense. They are the optimal defense hy- fast-growing plants with low levels of defense
pothesis (e.g., McKey, 1974; Feeny, 1976; that detract minimally from growth. In un-
Rhoades and Cates, 1976; Rhoades, 1979), productive habitats, limited resources con-
and two variants of the resource availability strain the ability of plants to compensate for
hypothesis: the growth rate hypothesis (Coley herbivory. Furthermore, the opportunity cost
et al., 1985; Coley, 1987), and the environ- of defense is low because of environmental
mental constraint hypothesis (Bryant et al., constraints on growth. Hence, high levels of
1985, 1988; Tuomi, Niemela, Chapin, Bry- defense are favored.
ant, and Siren, 1988). They differ in their
assumptions regarding the selective forces Resource Availability:
shaping the quantitative patterns of defense The Environmental Constraint Hypothesis
and the cost of the trade-off between growth Bryant et al. (1985, 1988) and Tuomi, Nie-
and defense. meld, Chapin, Bryant, and Siren (1988) pro-
pose a more restrictive view of the resource
The Optimal Defense Hypothesis availability hypothesis. Unlike the growth rate
The optimal defense hypothesis assumes hypothesis, the environmental constraint hy-
that defenses are costly because they divert pothesis does not require that quantitative
resources from growth, and that herbivory is patterns of defense represent optimal re-
the primary selective force shaping quantita- sponses to selection. Instead, the physio-
tive patterns of secondary metabolism (Mc- logical responses of plants to resource avail-
Key, 1974; Feeny, 1976; Rhoades and Cates, ability govern quantitative levels of plant
1976; Rhoades, 1979; Fagerstrom et al., 1987). defense and constrain the coevolutionary re-
The hypothesis predicts that because defenses lationships between plants and herbivores
are costly, resources are allocated to defense (Bryant et al., 1988).
in ways that optimize that investment. Plants The thesis that habitat quality constrains
will defend tissues in direct proportion to the genetically based quantitative patterns of sec-
cost of their loss. Easily replaced, less critical ondary metabolism is based in part on the
tissues and organs will be less defended than assumption that there is little or no cost associ-
hard-to-replace, indispensable ones (Mattson ated with the production of carbon-based sec-

ondary metabolites (Bryant et al., 1985). This by herbivores and competitors also correlates
thesis stems from observed phenotypic pat- well with resource availability. Resource avail-
terns of secondary metabolism in response to ability per se poses no inherent physiological
changes in resource availability: plants in constraints on the evolution of plant defense
resource-limited environments divert carbon or on coevolutionary interactions between
reserves accumulated beyond growth require- herbivores and plants. The evolution of high
ments to secondary metabolism without a levels of defense is possible in any environ-
trade-off with growth (Bryant et al., 1985; ment if herbivory is important enough.
Tuomi, Niemela, Chapin, Bryant, and Si- Competition is the major force that con-
ren, 1988). On the other hand, the same strains the evolution of plant defense. In
plants in resource-rich environments grow many environments, competition may be a
faster, but with a decreased allocation to sec- more important evolutionary force than her-
ondary metabolism. Thus the interpretation bivory (Tilman, 1990; Mattson et al., 1991).
is that insofar as a secondary metabolism is Indeed, the greatest impact of herbivores on
supported only by resources acquired in ex- plant fitness may be the effects that herbivores
cess of primary metabolic requirements: de- have on the ability of plants to compete (Louda
fense bears no cost (Bryant et al., 1985; Tu- et al., 1990; Prins and Nell, 1990a). Further-
omi, Niemela, Chapin, Bryant, and Siren, more, environmental factors affect the nature
1988). Tuomi, Niemela, Chapin, Bryant, of selection pressure from competition, hence
and Siren (1988) emphasized this point, stat- resource availability plays a modulating role
ing that their allocation model based on re- in the evolution of plant defense. In resource-
source availability ". . . differs from the opti- rich environments, increased defense com-
mal defense theory of Rhoades (1979) in that promises competitive ability. Genetically based
it implies no reduction in growth to support trade-offs between traits conferring competi-
carbon-based resistance; instead allocation to tive ability and those conferring herbivore re-
secondary metabolite production occurs only sistance constrain the evolution of increased
when growth demands for carbon have been defense. In resource-limited environments,
met" (p. 59). Tuomi, Niemela, Chapin, Bry- on the other hand, herbivore resistance is of-
ant, and Siren (1988) concluded that this allo- ten compatible with (and in some cases con-
cation model alone does not allow herbivores ferred directly by) traits conferring competi-
to exert selection on quantitative levels of sec- tive ability. There are few inviolate constraints
ondary metabolism, but they may shape the on the evolution of high levels of defense.
form this investment takes. The role of competition in shaping the re-
The crucial point of this specific model is source allocation patterns of plants is implicit
the extent to which secondary metabolism is within optimization theories of plant defense
supported by excess resources. Even if the (McKey, 1974; Feeny, 1976; Rhoades and
model may account for some aspects of phe- Cates, 1976; Rhoades, 1979; Bryant et al.,
notypic plasticity, there may still be a back- 1983; Coley et al., 1985; Coley, 1987). In the
ground level of secondary metabolism deter- following discussion, we extend the growth
mined by selection, depending on the costs rate model of Coley et al. (1985) to emphasize
and benefits of secondary metabolism. This the central role of competition in the evolution
requires evidence for genetic trade-offs (nega- of plant defense.
tive genetic correlation between growth and
defense, see, Reznick, 1985; Reznick et al., The GrowthRate Model Extended
1986). This point will be developed in more Coley et al. (1985) formalized their evolu-
detail as it relates to the evolution of plant tionary theory of plant defense with the fol-
defense. lowing equation:
CompetitionIs the Optimizerin Optimal Defense dC/dt = G * C * (11-kD )(H-mD').
Interspecific patterns of plant defense cor- Realized growth (dC/dt) is equal to the maxi-
relate well with patterns of resource availabil- mum inherent growth rate of the plant per-
ity because the nature of selection imposed mitted by the abiotic environment (G, in

g g-' d-l) multiplied by the initial biomass of ulation ( = Rmaxof Grime and Hunt, 1975).
the plant (C, in g), multiplied by the propor- It represents the potential growth rate obtain-
tional reduction in potential growth rate as a able under optimal conditions, and integrates
result of resources invested in defense (1 - the selective forces [competition (C), herbiv-
kD , in g g-1), minus the reduction in realized ory (H), and the abiotic environment (E)] act-
growth due to herbivory (H - mD', in g d-l). ing on the growth rate of the population:
The reduction in growth due to herbivory is
RGRp f ((RGRmax - (RGRmax
equal to the potential herbivore pressure in
the habitat assuming no defense (H), minus -kD-)), C, H, E).
the degree that herbivory is decreased by de-
This states that the potential inherent
fense (mDO)(parameters k and a are defined
growth rate evolved by a plant population
as constants that relate an investment in de-
(RGRp) is a function of the magnitude of dif-
fense to a reduction in growth; parameters m
ference in relative growth rates between the
and 3 are constants that determine the shape
undefended (RGRmax) and the variously de-
of the defense effectiveness curve) (Coley et al.,
fended genotypes (RGRmax - kBY), and the
1985). This model combines evolutionary
relative magnitude of the evolutionary impor-
(evolved defense) and ecological terms (her-
tance (sensu Welden and Slauson, 1986) of
bivory), to calculate realized growth (in eco-
the concomitant, often interacting selection
logical time). The evolutionary and ecological
pressures from C, H, and E. This model as-
effects of competition and the abiotic environ-
sumes no cost of traits maximizing competi-
ment are implicit, but subsumed in the G vari-
tive ability in the absence of competitors (an
able.
assumption that may not hold for the produc-
The model can be extended by formalizing
tion of allelopathic secondary metabolites).
the competition and environmental compo-
We define the ecological component of the
nents in evolutionary and ecological time.
model using the following equation:
Furthermore, by separating the evolutionary
and ecological components, assumptions re- RGRr = RGRp(1 - mcE - pev - nhP)
garding the evolutionary cost of defense can
be clarified. Testable alternative predictions where RGRr (realized relative growth rate)
of the growth rate (Coley et al., 1985; Coley, is equal to the potential growth rate (RGRp)
1987) and environmental constraint hypothe- diminished by the percent reductions (ecolog-
ses (Bryant et al., 1985, 1988; Tuomi, Nie- ical intensity sensu Welden and Slauson,
meld, Chapin, Bryant, and Siren, 1988) re- 1986) caused by competition (c), by the abi-
garding the cost of defense can be derived otic environment (e), and finally by herbivory
from the model. (h) (parameters m and E, p and v, and n and
The extended model uses the following p relate the effectiveness of adaptations for
terms: buffering the negative effects of competition,
the abiotic environment, and herbivory, re-
RGRmax, RGRp and RGRr. spectively, to their effect on the growth rate
RGRmax = the maximum inherent relative of the plant).
growth rate that a plant could have evolved in The ecological intensity of herbivory can
a particular abiotic environment. It directly be further defined where:
reflects historical environmental variables, 1 - (nhP) = 1 - (vr -ud7),
integrating the mean level of resource avail-
ability that a plant population has experi- with d equal to the decrease in growth rate
enced over evolutionary time. It is independent caused by plant tissue destroyed by herbi-
of the effects of competitors and herbivores. vores and r equal to the increase in growth
Hence, RGRmax is equal for all species of a rate due to regrowth (compensatory growth)
given growth form that have evolved in a following herbivory (parameters u and y, and
given environment. v and -q relate the effectiveness of defensive
RGRp = the potential inherent relative and compensatory adaptations, respectively,
growth rate actually evolved by the plant pop- for limiting the negative effects of herbivory

on growth rate). Hence, the ecological com- in a negative genetic correlation between
ponent of the model becomes: growth rate and defense that is independent
of resource availability in evolutionary time.
RGRr = RGRp(1 - mcE- pe" - ud + vr"). In this case, there is a cost to defense, and a
Hence, RGRp(1 - mcE- pev - ud + vr") is
equivalent to G in the model of Coley et al.,
1985. This equation assumes that the ecologi-
cal effects of competition (c), the abiotic envi-
a Net
ronment (e), and herbivory (h) operate inde- Assimilation
=
pendently in their effects on RGRr. Clipping R G R max /< (RGR, RGR_) RGR
and competition were found to have additive Realized Relative
/ / V ~~~~Growth Rate
effects on the growth and reproduction ofAris- (RGR,)
tolochiareticulata(Fowler and Rausher, 1985), Secondary
providing some justification for this assump-
b A v Is~~~~~~~~~~~m
tion.
b Net
Comparingthe Optimal Defense and Assimilation -
EnvironmentalConstraintModels RGRmax -------

(RGR < RGRma)
-______t<\ ___ _______-RGRP
This extended model facilitates compari-
son of the assumptions and predictions of op- //
Scondary
Mtabolism /
timal defense (Rhoades, 1979) and environ- / / / ~~~Realized

Relative
Growth Rate
mental constraint (Bryant et al., 1985, 1988; (RGR,)
Tuomi, Niemela, Chapin, Bryant, and Si- Low High
Resource Availability
ren, 1988) hypotheses, and their implications
for the cost of defense. The environmental FIG. 2. COMPARISON OF MEAN NORMS OF
constraint hypothesis emphasizes abiotic con- REACTION FOR NET ASSIMILATION
straints on the evolution of constitutive de- RATE, RELATIVE GROWTH RATE,
AND SECONDARY FOR
fense and assumes that plants evolve growth METABOLISM,
rates close or equal to the maximum potential Two POPULATIONS (A AND B) OF

THE SAME SPECIES, WHICH
permitted by the abiotic environment. Im-
EVOLVED IN EQuIVALENT
plicitly, there is little reduction in growth re- ABIOTIC ENVIRONMENTS
sulting from the evolved level of defense. Bry- Population A evolved according to the environ-
ant et al. (1985, 1988) and Tuomi, Niemela, mental constraint model (Bryant et al., 1985,
Chapin, Bryant, and Siren (1988) emphasize 1988; Tuomi, Niemela, Chapin, Bryant, and Si-
that only photosynthates accumulated in ex- ren, 1988) with an inherent growth rate (RGRp)
cess of growth requirements are allocated to equal to the maximum permitted by its abiotic
secondary metabolism, thus there is no phe- environment (RGRmax). Only photosynthates ac-
cumulated in excess of growth requirements are
notypic or genetic trade-off associated with
allocated to secondary metabolism, hence there is
defense (RGRp = RGRmax and kD' = 0)
no phenotypic or genotypic trade-off between
[Fig. 2(a)]. Thus, under optimal environ- growth and secondary metabolism (kD' = 0).
mental conditions for growth, RGR, = When individuals of population A are grown under
RGRP = RGRmax [Fig. 2(a)]. It should be optimal environmental conditions, RGR, = RGRP
noted that the growth rate model (Coley et = RGRmax. Population B evolved according to the
al., 1985) does not make this restrictive as- optimal defense model (McKey, 1974; Rhoades,
sumption, but does emphasize that quantita- 1979; Coley et al., 1985). Herbivory has selected
tive levels of defense are primarily determined for increased secondary metabolism, and conse-
quently for an inherent growth rate (RGRp) less
by resource availability:
than the maximum permitted by its abiotic environ-
Alternatively, herbivory may select for in- ment (RGRmax). Hence, there is a genetic trade-off
creased defense, reducing the inherent growth between growth rate and secondary metabolism
rate of the plant below its evolutionary poten- (kD' > 0). When individuals of population B are
tial given its abiotic environment (RGRp < grown under optimal environmental conditions,
RGRmaxand kDa > 0) [Fig. 2(b)]. This results RGRr = RGRP < RGRmax.

primary assumption of optimal defense the- can select for increased defense at the expense
ory is met. of growth (RGRp < RGRmax) supports the
To summarize, environmental constraint alternative of optimal defense.
theory predicts that resource availability is the The evolutionary impact of herbivory on
primary determinant of evolved level of de- plant defense can be tested by making intra-
fense, and that RGRp will always be equal or specific comparisons across a series of habitats
close to RGRmax (growth is not sacrificed to with similar levels of resources but differing
support defense and defense has no cost), i.e., in herbivore pressure. Higher concentrations
plants evolving under similar conditions of of secondary metabolites and lower growth
resource availability will evolve similar growth rates associated with more intense herbivory
rates, even if subjected to different intensities would support the assumptions of the optimal
of herbivory. Optimal defense theory predicts defense theory of Rhoades (1979). If resources
that herbivores can select for a RGRP that lost by the faster growing genotypes were bal-
is less than RGRmax (growth is sacrificed to anced by the decreased rate of resource acqui-
support defense; defense is costly). Plants sition by the better defended genotypes, intra-
evolving under similar conditions of resource specific comparisons of genotypes within a
availability can evolve different growth rates population revealing a balanced polymor-
if they experience different intensities of her- phism for growth and defense would also con-
bivory. stitute evidence for optimal defense. Models
of Augner et al. (1991), which incorporate
Testing the Hypotheses competition and herbivory, suggest that mod-
Variation between species is vast relative erate levels of herbivory can maintain genetic
to the variation within species (Southwood, variation for growth rate and secondary me-
1988). Thus, the existence of life history tac- tabolism within plant populations and com-
tics has been more apparent at higher taxo- munities. Low and high levels of herbivory,
nomic levels (Stearns, 1980), and it is not however, will result in directional selection for
surprising that hypotheses addressing the rapid growth and strong defense, respectively
evolution of defense in plants have been devel- (Augner et al., 1991).
oped and tested primarily with interspecific There is limited experimental evidence
comparisons (Feeny, 1976; Rhoades and from intraspecific studies demonstrating ge-
Cates, 1976; Grime, 1979; Bryant et al., netically based trade-offs between growth rate
1983, 1989; Coley, 1983, 1987, 1988; Coley and/or reproductive fitness and secondary
et al. , 1985; Loehle, 1988). Interspecific com- metabolism (Hanover, 1966a; Cates, 1975;
parisons allow the inference of process from Dirzo and Harper, 1982; Dirzo, 1984; Beren-
the identification of pattern (Keddy, 1989). baum et al., 1986; Coley, 1986; Kakes, 1989).
Evidence for the microevolutionary processes Studies implicating herbivores as the force se-
leading to the evolution of life history pat- lecting for higher levels of secondary metabo-
terns, however, may best be discovered by lism, however, are confounded by differences
making intraspecific comparisons in resource in abiotic environments, with the more resis-
allocation patterns, focusing on the selection tant genotypes generally inhabiting the less
pressures maintaining genetic variation within favorable habitat. In these cases, the environ-
species (Stearns, 1976; Futuyma and Mor- mental constraint hypothesis cannot be elimi-
eno, 1988; but see Stearns, 1980). nated.
Both the environmental constraint and op- Cates (1975) demonstrated genetic varia-
timal defense models of plant defense predict tion within Asarum caudatum(wild ginger) for
genetically based, intraspecific variation in growth rate and resistance to the herbivorous
growth rate and secondary metabolism. The slug Ariolimax columbianus, with the faster-
environmental constraint hypothesis repre- growing genotypes being less well defended.
sents a physiological null model: herbivores The fast-growing genotypes, however, inhab-
do not select for increased defense at the ex- ited the most favorable environment, while
pense of growth (i.e., RGRp = RGRmax). On the defended genotypes were generally re-
the other hand, demonstration that herbivory stricted to drier habitats (Cates, 1975). Simi-

larly, genetically based differences in sec- between growth and differentiation processes,
ondary chemistry were found in different if primary metabolism (Y) increases, then sec-
populations of Pastinaca sativa (wild parsnip) ondary metabolism (X) must decrease (and
(Zangerl and Berenbaum, 1990) and Satureja vice versa). Therefore, given the plant has a
douglasii (Lincoln and Langenheim, 1979). specified level of resources available for allo-
The populations experiencing the highest lev- cation, each possible allocation pattern can be
els of herbivory had the highest levels of sec- represented by a unique set of [X,,Y,I paired
ondary metabolism, but they also inhabited values (Fig. 3). Plotting these points yields a
less favorable abiotic environments. line segment showing the allocation trajectory
A number of studies suggest that the cyano- (norm of reaction) for that plant. An individ-
genic morphs of Trifoliumrepensand Lotus cor- ual plant in a particular environment at any
niculatusare more resistant to herbivores (Ellis given time is represented by a discrete point
et al., 1977a; Jones et al., 1978; Dirzo and on the line. By plotting the mean value for all
Harper, 1982; Dirzo, 1984; Compton and individuals, an entire population is repre-
Jones, 1985; Burgess and Ennos, 1987), but sented by a discrete point.
they are inferior competitors compared to the Welden and Slauson (1986) distinguished
acyanogenic morphs (Foulds and Grime, between the intensity and importance of
1972; Dirzo and Harper, 1982; Burgess and
Ennos, 1987; Kakes, 1989, 1990; Noitsakis
andJacquard, 1992). Furthermore, some evi-
dence suggests that the distribution of the cy- a EvolutionaryImportance of Herbivory
Low High
anogenic morphs coincides with that of their
H, H2
important herbivores (Ellis et al., 1977a,b; 100\ II
Compton et al., 1983). These patterns of dis-
tribution, however, also coincide with abiotic 2 Genotype A
*0
gradients, thereby again confounding the in-
terpretation (Hughes, 1991). I_~~~~~~C
The Evolution of Plant Allocation Trajectories: c 0 10C

Competitionand HerbivoryConsidered
We will conclude and summarize with a
0 X 100 100
mechanistic conceptual model of the evolution
of plant resource allocation patterns (Fig. 3).
The model is based upon the plant's physio- Ftcy 3. b~~~~~~~~~~~~~~~~
C U LT OF
logical and ecological constraints resulting in eD = G~~enot eni oi Curen Phoooniai

CenoMPEtITIONy(C)nDtH EBI (
the trade-off between growth and differentia- 0 \Low
tion, and incorporates the effects of natural 0 100
selection from herbivores and competitors.

Resource availability mediates the evolution- b
|_Percent of Current Photosynthate
Allocated to Secondary Metabolism (Defense)
ary outcome. FIG. 3. CONCEPTUAL MODEL OF THE EFFECTS OF

Plants allocate their photoassimilates to cur- COMPETITION (C) AND HERBIVORY (H)
rent use or storage. Current photosynthate ON THE EVOLUTION OF PLANT RESOURCE
is further allocated to primary (growth and ALLOCATION PATTERNS IN VARYING
maintenance) or secondary metabolic processes ENVIRONMENTS
(defense). Stored photoassimilates can be con- (a) Stable polymorphism (genotypes A and B) is
sidered future allocation to primary and/or maintained by disruptive selection in environ-
secondary metabolism. For any given plant, ments in which the evolutionary importance of
herbivory relative to competition is low and high,
the percentage of currently available photo-
respectively. (b) Directional selection exerted on
synthate allocated to primary metabolism (Y) populations A and B in an environment in which
and the percentage allocated to secondary me- herbivoryand competition are of equal importance
tabolism (X) can be (at least theoretically) deter- results in the evolution of genotype C. See text for
mined. Because of the physiological trade-off additional details.

forces of natural selection. Intensity is the limitation depress the realized growth rate of
amount of change in growth rate, fecundity, genotype A well below its genetic potential,
size, or fitness of an individual caused by one and genotype A cannot compete successfully.
selective force independent of changes caused In an environment in which the importance
by others. Importance is the degree to which of competition (C3) and herbivory (H3) are
a selective force contributes to the overall equal, both genotypes A and B face direc-
change in fitness relative to other selective tional selection [Fig. 3(b)]. The population of
factors. If we assume competition and herbiv- genotype A is under pressure from herbivores
ory to be the dominant biotic forces exerting to evolve increased defense, while the popula-
selection upon plant allocation patterns, then tion of genotype B is under pressure from
as the evolutionary importance of one in- competition to evolve a faster growth rate at
creases, the importance of the other must de- the expense of secondary metabolism. The
crease. two populations may converge on genotype
Extending the scale of the model from phys- C, which will be maintained by stabilizing
iological to ecological-evolutionary, we im- selection exerted by the opposing pressures of
pose upon the X and Y axes the evolutionary competition and herbivory.
importance of herbivory and competition, re- In summary, physiological constraints re-
spectively (Fig. 3). We assume that their evo- sult in a trade-off between the high rate of
lutionary importance as selection pressures growth needed to compete and the differentia-
affecting the relative growth rates of plants tion processes that limit herbivory. The mix
are inversely correlated and are determined of genotypes that survive in a plant popula-
by the level of resources in the environment tion will depend on pressures exerted by com-
available to support growth (e.g., Bryant et petition and herbivory, their relative impor-
al., 1983; Coley, 1985; Reader and Best, 1989; tance being determined by the environment
Oksanen, 1990; Reader, 1990). As resource in which the interaction is played out. Compe-
availability increases, the importance of com- tition and herbivory will favor a certain subset
petition relative to herbivory increases. Con- of carbon allocation patterns [XI,Y,l for each
versely, as resource availability decreases, the given environment. As selection from compe-
importance of competition relative to herbiv- tition and herbivory varies over time, one or
ory declines. We also assume, however, that the other may become more important in di-
the importance of herbivory can vary within recting the evolution of the plant population.
an environment independently of resource Phenotypic plasticity in response to environ-
availability. mental variation will buffer these opposing
In Figure 3(a), intraspecific genetic varia- effects of selection. Plant species with broad
tion is sustained by disruptive selection ex- distributions covering many different habi-
erted by contrasting environments. Genotype tats having selection pressures varying in im-
A has evolved in an environment in which the
portance may evolve stable polymorphisms
importance of competition (C1) is greater than for allocation to growth and differentiation.
the importance of herbivory (H1). Genotype
A is favored in this environment over geno-
ACKNOWLEDGMENTS
type B because of faster growth rate. Geno-
type B, although well defended (but conse- The support of this research by the U.S.D.A.
quently, slower growing) cannot compete through award 87-FSTY-9-0270 is gratefully ac-
knowledged. We thank Matt Ayres, Cathy Bris-
successfully in the absence of herbivores. Ge-
tow, John Bryant, Richard Dickson, James Han-
notype B has evolved in an environment in
over, Kelly Johnson, Stig Larsson, Ralph Lewis,
which competition (C2) is less important rela- Craig Loehle, Peter Lorio, Jim Miller, Dave Niel-
tive to herbivory (H2), due either to resource sen, James Nitao, Peter Price, Peter Smith, Ned
limitation or more intense herbivory. Geno- Walker, and two anonymousreviewersfor thought-
type B, by virtue of its slower growth rate and ful criticismsthat substaniallyimproved this manu-
higher allocation to defense, is favored. In script. We also thank the many authors who re-
this environment, herbivores and/or resource sponded to our requests for reprints.

REFERENCES
Abe, T. 1991. Cellulose as a defense system of ceptibility to a fungal elicitor. Plant Cell Rep., 7:
terrestrial plants. Oikos, 60: 127-133. 692-695.
Aerts, R. J., W. Snoeijer, 0. Aerts-Teerlink, Appleton, M. R., andJ. van Staden. 1989. The
E. van der Meijden, and R. Verpoorte. 1991. relationship between season, growth and iso-
Control and biological implications of alkaloid prenoid biosynthesis in Parthenium argentatum.
synthesis in Cinchona seedlings. Phytochemistry, J. Plant Physiol., 134:524-532.
0
30:3571-3577. Ashmun, J. W., R. J. Thomas, and L. F. Pitelka.
Agren, G. I. 1985a. Theory for growth of plants 1982. Translocation of photoassimilates be-
derived from the nitrogen productivity con- tween sister ramets in two rhizomatous forest
cept. Physiol. Plant., 64:17-28. herbs. Ann. Bot. (Lond.), 49:403-415.
. 1985b. Limits to plant production. J Augner, M., T. Fagerstriim, andJ. Tuomi. 1991.
Theor. Biol., 113:89-92. Competition, defense and games between plants.
. 1988. Ideal nutrient productivities and Behav. Ecol. Sociobiol., 29:231-234.
nutrient proportions in plant growth. Plant Cell Ayres, M. P., and S. F. MacLean, Jr. 1987. De-
Environ., 11:613-620. velopment of birch leaves and the growth ener-
Agren, G. I., and T. Ingestad. 1987. Root:shoot getics of Epirrita autumnata(Geometridae). Ecol-
ratio as a balance between nitrogen productiv-
ogy, 68:558-568.
ity and photosynthesis. Plant Cell Environ., 10: Baas, W. J. 1990. Secondary plant compounds,
0 579-586. their ecological significance and consequences
Agren, J. 1987. Intersexual differences in phe- for the carbon budget: introduction of the carbon/
nology and damage by herbivores and patho- nutrient-cycle theory. In H. Lambers, M. L.
gens in dioecious Rubus chamaemorusL. Oeco- Cambridge, H. Konings, T. L. Pons (eds.),
logia, 72:161-169.
Causesand Consequencesof Variationin GrowthRate
Allen, G. A., and J. A. Antos. 1988. Relative
and Productivity of Higher Plants, pp. 313-340.
reproductive effort in males and females of the
SPB Academic Publishing, The Hague.
dioecious shrub Oemleriacerasiformis. Oecologia,
Baldwin, I. T. 1988. Damaged-induced alkaloids
76:111-118.
in tobacco: Pot-bound plants are not inducible.
Allen, S. G., F. S. Nakayama, D. A. Dierig, and
B. A. Rasnick. 1987. Plant water relations,
J. Chem. Ecol., 14:1113-1120.
Baldwin, I. T., J. C. Schultz, and D. Ward. 1987.
photosynthesis, and rubber content of young
Patterns and sources of leaf tannin variation
guayule plants during water stress. Agron. J,
in yellow birch (Betula allegheniensis) and sugar
79: 1030-1035.
maple (Acersaccharum).J. Chem. Ecol., 13:1069-
Alliende, M. C. 1989. Demographic studies of a
1078.
dioecious tree. II. The distribution of leaf pre-
Baldwin, I. T., C. L. Sims, and S. E. Kean. 1990.
dation within and between trees. J. Ecol., 77:
The reproductive consequences associated with
1048-1058.
inducible alkaloidal responses in wild tobacco.
Alpert, P., E. A. Newell, C. Chu, J. Glyphis,
Ecology, 71:252-262.
S. L. Gulmon, D. Y. Hollinger, N. D. John-
son, H. A. Mooney, and G. Puttick. 1985. Al- Ball, D. M., and C. S. Hoveland. 1978. Alkaloid
location to reproduction in the chaparral shrub, levels in Phalaris aquatica L. as affected by envi-
Diplacus aurantiacus. Oecologia, 66:309-316. ronment. Agron. j, 70:977-981.
Altman, D. W., R. D. Stipanovic, andJ. H. Bene- Banthorpe, D. V., and G. D. Brown. 1989. Two
dict. 1989. Terpenoid aldehydes in upland cot- unexpected coumarin derivatives from tissue
tons. II. Genotype-environment interactions. cultures of compositae species. Phytochemistry,
Crop Sci., 29:1451-1456. 28:3003-3007.
Antolin, M. F., and C. Strobeck. 1985. The popu- Barbosa, P., andJ. A. Saunders. 1985. Plant allelo-
lation genetics of somatic mutation in plants. chemicals: linkages between herbivores and
Am. Nat., 126:52-62. their natural enemies. Recent Adv. Phytochem.,
Antos,J. A., andG. A. Allen. 1990. A comparison 19: 107-137.
of reproductive effort in the dioecious shrub Bariska, M., and A. Pizzi. 1986. The interaction
Oemleriacerasiformisusing nitrogen, energy and of polyflavonoid tannins with wood cell-walls.
biomass as currencies. Am. Midl. Nat., 124: Holzforschung, 40:299-302.
254-262. Barlow, P. W. 1989. Meristems, metamers and
Apostol, I., P. S. Low, and P. Heinstein. 1989. modules and the development of shoot and root
Effect of age of cell suspension cultures on sus- systems. Bot. J Linn. Soc., 100:255-279.

Bate-Smith, E. C. 1984. Age and distribution of 1989. Chemical barriers to adaptation by a spe-
galloyl esters, iridoids and certain other repel- cialist herbivore. Oecologia, 80:501-506.
lents in plants. Phytochemistry,23:945-950. Berenbaum, M. R., A. R. Zangerl, and J. K.
Bazzaz, F. A. 1979. The physiological ecology of Nitao. 1986. Constraints on chemical coevolu-
plant succession. Annu. Rev. Ecol. Syst., 10:351- tion: wild parsnips and the parsnip webworm.
371. Evolution, 40:1215-1228.
. 1990. The response of natural ecosystems Berendse, F., andW. T. Elberse. 1990a. Competi-
to the rising global CO2 levels. Annu. Rev. Ecol. tion and nutrient losses from the plant. In
Syst., 21:167-196. H. Lambers, M. L. Cambridge, H. Konings,
Bazzaz, F. A., R. W. Carlson, andJ. L. Harper. and T. L. Pons (eds.), Causesand Consequencesof
1979. Contribution to reproductive effort by Variationin GrowthRate and Productivityof Higher
photosynthesis of flowers and fruits. Nature, Plants, pp. 269-284. SPB Academic Publish-
279:554-555. ing, The Hague.
Bazzaz, F. A., N. R. Chiariello, P. D. Coley, , and . 1990b. Competition and nu-
and L. F. Pitelka. 1987. Allocating resources to trient availability in heathland and grassland
reproduction and defense. BioScience,37:58-67. ecosystems. In J. B. Grace and D. Tilman
Bazzaz, F. A., and E. G. Reekie. 1985. The mean- (eds.), Perspectiveson Plant Competition, pp. 93-
116. Academic Press, San Diego.
ing and measurement of reproductive effort in
Bergelson, J., S. Fowler, and S. Hartley. 1986.
plants. In J. White (ed.), Studies on Plant Demog-
The effects of foliage damage on casebearing
raphy: A Festschriftfor John L. Harper, pp. 373- moth larvae, Coleophoraserratella, feeding on
387. Academic Press, New York.
birch. Ecol. Entomol., 11:241-250.
Beattie, A. J. 1985. The EvolutionaryEcology of Ant-
Bergelson, J., andJ. H. Lawton. 1988. Does fo-
Plant Mutualisms. Cambridge University Press,
liage damage influence predation on the insect
Cambridge. herbivores of birch? Ecology, 69:434-445.
Belsky, A. J. 1986. Does herbivory benefit plants? Bernays, E. A. 1983. Nitrogen in defence against
A review of the evidence. Am. Nat., 127:870- insects. In J. A. Lee, S. McNeil, and I. H.
892. Rorison (eds.), Nitrogen as an Ecological Factor,
Bentley, B. L. 1977. Extrafloral nectaries and pro- pp. 321-344. Blackwell Scientific, Oxford.
tection from pugnacious bodyguards. Annu. Bernays, E. A., D. J. Chamberlain, and S. Wood-
Rev. Ecol. Syst., 8:407-427. head. 1983. Phenols as nutrients for a phytoph-
Bentley, S., and J. B. Whittaker. 1979. Effects agous insect Anacridium melanorhodon.J. Insect
of grazing by a chrysomelid beetle, Gastrophysa Physiol., 29:535-539.
viridula, on competition between Rumex obtusi- Bernays, E. A., and R. F. Chapman. 1987. Chem-
folius and Rumex crispus. J. Ecol., 67:79-90. ical deterrence of plants. In J.H. Law (ed.),
Berenbaum, M. 1978. Toxicity of a furanocouma- Molecular Entomology, Vol. 49, pp. 108-116.
rin to armyworms: a case of biosynthetic escape Alan R. Liss, New York.
from insect herbivores. Science, 201:532-534. Bernays, E. A., and M. Graham. 1988. On the
1981. Toxicity of angular furanocouma- evolution of host specificity in phytophagous
rins to swallowtail butterflies: escalation in a arthropods. Ecology, 69:886-892.
coevolutionary arms race? Science, 212:927- Bernays, E. A., and S. Woodhead. 1982. Plant
929. phenols utilized as nutrients by a phytophagous
. 1983. Coumarins and caterpillars: a case insect. Science, 216:201-203.
for coevolution. Evolution, 37:163-179. Bj6rkman, C., and D. B. Anderson. 1990. Trade-
. 1985. Brementown revisited: interactions off among antiherbivore defences in a South
among allelochemicals in plants. Recent Adv. American blackberry (Rubus bogotensis). Oeco-
logia, 85:247-249.
Phytochem., 19:139-169.
Bjorkman, C., and S. Larsson. 1991. Pine sawfly
Berenbaum, M. R., J. K. Nitao, and A. R. Zan-
defence and variation in host plant resin acids:
gerl. 1991. Adaptive significance of furano-
a trade-off with growth. Ecol. Entomol., 16:283-
coumarin diversity in Pastinaca sativa (Apia-
289.
ceae). J. Chem. Ecol., 17:207-215. Bjorkman, C., S. Larsson, and R. Gref. 1991.
Berenbaum, M. R., and A. R. Zangerl. 1988. Effects of nitrogen fertilization on pine needle
Stalemates in the coevolutionary arms race: chemistry and sawfly performance. Oecologia,
syntheses, synergisms, and sundry other sins. 86:202-209.
In K. C. Spencer (ed.), Chemical Mediation of Bloom, A. J., F. S. Chapin III, and H. A. Moo-
Coevolution,pp. 113-132. Academic Press, San ney. 1985. Resource limitation in plants-an
Diego. economic analogy. Annu. Rev. Ecol. Syst., 16:
Berenbaum, M. R., A. R. Zangerl, and K. Lee. 363-392.

Bodnaryk, R. P., and P. Palaniswamy. 1990. Glu- Trade-offs among growth, reproduction and
cosinolate levels in cotyledons of mustard, Bras- defense. Oecologia, 83:32-37.
szcaljunceaL. and rape, B. napus L. do not deter- Briske, D. D., and B. J. Camp. 1982. Water stress
mine feeding rates of flea beetle, Phyllotreta increases alkaloid concentrations in threadleaf
cruciferae(Goeze).J. Chem.Ecol., 16:2735-2746. groundsel (Seneciolongilobus). WeedSci., 30: 106-
Boecklen, W. J., P. W. Price, and S. Mopper. 108.
1990. Sex and drugs and herbivores: sex-biased Brower, L. P., and S. C. Glazier. 1975. Localiza-
herbivory in arroyo willow (Salix lasiolepis). tion of heart poisons in the monarch butterfly.
Ecology, 71:581-588.
Science, 188:19-25.
B6hm, H. 1977. Secondary metabolism in cell cul-
Brown, B. J., and J. J. Ewel. 1988. Responses
tures of higher plants and problems of differen-
to defoliation of species-rich and monospecific
tiation. In M. Luckner, L. Nover, and H. Bohm
tropical plant communities. Oecologia, 75:12-
(eds.), SecondaryMetabolism and Cell Differentia-
tion, pp. 104-123. Springer-Verlag, New York. 19.
Bond, W. J. 1989. The tortoise and the hare: ecol- Brown, D. G. 1988. The cost of plant defense: an
ogy of angiosperm dominance and gymnosperm experimental analysis with inducible protein-
persistence. Biol. J. Linn. Soc., 36:227-249. ase inhibitors in tomato. Oecologia,76:467-470.
Bopre, M. 1990. Lepidoptera and pyrrolizidine Bryant, J. P. 1987. Feltleaf willow-snowshoe hare
alkaloids. Exemplification of complexity in interactions: plant carbon/nutrient balance and
chemical ecology. J. Chem. Ecol., 16:165-185. floodplain succession. Ecology, 68:1319-1327.
Bowers, M. D., and G. M. Puttick. 1988. Re- Bryant, J. P., F. S. Chapin III, and D. R. Klein.
sponse of generalist and specialist insects to 1983. Carbon/nutrient balance of boreal plants
qualitative allelochemical variation. J. Chem. in relation to vertebrate herbivory. Oikos, 40:
Ecol., 14:319-334. 357-368.
Boyer, J. s. 1988. Cell enlargement and growth- Bryant, J. P., F. S. Chapin III, P. Reichardt,
induced water potentials. Physiol. Plant., 73: and T. Clausen. 1985. Adaptation to resource
311-316. availability as a determinant of chemical de-
Boyer, R. F., H. M. Clark, and S. Sanchez. 1989. fense strategies in woody plants. Recent Adv.
Solubilization of ferrihydrite iron by plant phe- Phytochem., 19:219-237.
nolics: a model for rhizosphere processes. J. Bryant, J. P., F. S. Chapin III, P. Reichardt, and
Plant Nutr., 12:581-592.
T. Clausen. 1987. Response of winter chemical
Bradford, K. J., and T. C. Hsiao. 1982. Physio-
defense in Alaska paper birch and green alder to
logical responses to moderate water stress. In
manipulation of plant carbon/nutrient balance.
0. L. Lange, P. S. Nobel, C. B. Osmond, and
H. Ziegler (eds.), PhysiologicalPlant Ecology, H.I Oecologia, 72:510-514.
WaterRelations and CarbonAssimilation, pp. 263- Bryant, J. P., T. P. Clausen, P. B. Reichardt,
324. Springer-Verlag, Berlin. M. C. McCarthy, and R. A. Werner. 1987.
Bradshaw, A. D. 1965. Evolutionary significance Effect of nitrogen fertilization upon the second-
of phenotypic plasticity in plants. Adv. Genet., ary chemistry and nutritional value of quaking
13:115-155. aspen (Populus tremuloides Michx.) leaves for
Braga, M. R., M. C. M. Young, S. M. C. Die- the large aspen tortrix (Choristoneuraconflictana
trich, and 0. R. Gottlieb. 1991. Phytoalexin (Walker)). Oecologia, 73:513-517.
induction in Rubiaceae. J. Chem. Ecol., 17: Bryant, J. P., I. Heitkonig, P. Kuropat, and
1079-1090. N. Owen- Smith. 1991. Effects of severe defoli-
Braga, M. R., M. C. M. Young,J. V. A. Ponte, ation on the long-term resistance to insect at-
S. M. C. Dietrich, V. de P. Emerenciano, and tack and on leaf chemistry in six woody species
0. R. Gottlieb. 1986. Phytoalexin production of the southern African savanna. Am. Nat., 137:
in plants of tropical environment. Biochem. Syst.
50-63.
Ecol., 14:507-514.
Bryant, J. P., and P. J. Kuropat. 1980. Selection
Brattsten, L. B. 1988. Enzymic adaptations in
of winter forage by subarctic browsing verte-
leaf-feeding insects to host-plant allelochemi-
14:1919-1939. brates: the role of plant chemistry. Annu. Rev.
cals.J. Chem. Ecol.,
Brehm, B. G., and D. Krell. 1975. Flavonoid lo- Ecol. Syst., 11:261-285.
calization in epidermal papillae of flower petals: Bryant, J. P., P. J. Kuropat, S. M. Cooper,
a specialized adaptation for ultraviolet absorp- K. Frisby, and N. Owen-Smith. 1989. Re-
tion. Science, 190:1221-1223. source availability hypothesis of plant antiher-
Briggs, M. A., andJ. C. Schultz. 1990. Chemical bivore defence tested in a South African sa-
defense production in Lotus corniculatus L. II. vanna ecosystem. Nature, 340:227-229.

Bryant, J. P., J. Tuomi, and P. Niemelii. 1988. of wild plants. Annu. Rev. Ecol. Syst., 11:233-
Environmental constraint of constitutive and 260.
long-term inducible defenses in woody plants. . 1980b. Nutrient allocation and responses
In K. C. Spencer (ed.), Chemical Mediation of to defoliation in tundra plants. Arct. Alp. Res.,
Coevolution,pp. 367-389. Academic Press, San 12:553-563.
Diego. . 1988. Ecological aspects of plant mineral
Bullock, S. H. 1984. Biomass and nutrient alloca- nutrition. In B. Tinker and A. Lauchli (eds.),
tion in a neotropical dioecious palm. Oecologia, Advancesin Plant Nutrition, Vol. 3. Praeger, New
63:426-428. York.
Burgess, R. S. L., and R. A. Ennos. 1987. Selec- . 1989. The cost of tundra plant structures:
tive grazing of acyanogenic white clover: varia- evaluation of concepts and currencies. Am.
tion in behaviour among populations of the slug Nat., 133:1-19.
Derocerasreticulatum. Oecologia, 73:432-435. . 1991. Integrated responses of plants to
Buss, L. W. 1983. Evolution, development, and stress. BioScience, 41:29-36.
the units of selection. Proc. Natl. Acad. Sci. USA, Chapin, F. S., III, A. J. Bloom, C. B. Field, and
80:1387-1391. R. H. Waring. 1987. Plant responses to multi-
Caldwell, M. M., R. Robberecht, and S. D. Flint. ple environmental factors. BioScience, 37:49-
1983. Internal filters: prospects for UV-accli- 57.
mation in higher plants. Physiol. Plant., 58:445- Chapin, F. S., III, R. H. Groves, and L. T. Evans.
450. 1989. Physiological determinants of growth
Campbell, B. M. 1986. Plant spinescence and her- rate in response to phosphorous supply in wild
bivory in a nutrient poor ecosystem. Oikos, 47: and cultivated Hordeum species. Oecologia, 79:
168-172. 96-105.
Carroll, C. R., and C. A. Hoffman. 1980. Chemi- Chapin, F. S., III, J. B. McGraw, and G. R.
cal feeding deterrent mobilized in response to Shaver. 1989. Competition causes regular
insect herbivory and counteradaptation by Epi- spacing of alder in Alaskan shrub tundra. Oeco-
lachna tredecimnotata.Science, 209:414-416. logia, 79:412-416.
Carroll, G. 1988. Fungal endophytes in stems and Chapin, F. S., III, and S. J. McNaughton. 1989.
leaves: from latent pathogen to mutualistic Lack of compensatory growth under phospho-
symbiont. Ecology, 69:2-9. rous deficiency in grazing-adapted grasses from
the Serengeti Plains. Oecologia, 79:551-557.
Caswell, H. 1983. Phenotypic plasticity in life-
history traits: demographic effects and evolu- Chapin, F. S., III, E.-D. Schulze, and H. A. Moo-
ney. 1990. The ecology and economics of stor-
tionary consequences. Am. Zool., 23:35-46.
age in plants. Annu. Rev. Ecol. Syst., 21:423-
Cates, R. G. 1975. The interface between slugs
447.
and wild ginger: some evolutionary aspects.
Chapin, F. S., III, G. R. Shaver, and R. A. Ked-
Ecology, 56:391-400.
rowski. 1986. Environmental controls over car-
. 1987. Influence of biological rhythms, tis-
bon, nitrogen, and phosphorus fractions in Eri-
sue development, and physiological state of
ophorumvaginatumin Alaskan tussock tundra. J.
plants and insects on their interactions. In
Ecol., 74:167-195.
V. Labeyrie, G. Fabres, and D. Lachaise (eds.),
Chapin, F. S., III, P. M. Vitousek, and K. Van
Insects-Plants, pp. 175-182. Junk, Dordrecht.
Cleve. 1986. The nature of nutrient limitation
Cates, R. G., and G. H. Orians. 1975. Succes- in plant communities. Am. Nat., 127:48-58.
sional status and the palatability of plants to Charles, D.J., R.J.Joly, andJ. E. Simon. 1990.
generalized herbivores. Ecology, 56:410-418. Effects of osmotic stress on the essential oil con-
Cates, R. G., and D. F. Rhoades. 1977. Patterns tent and composition of peppermint. Phytochem-
in the production of antiherbivore defenses in istry, 29:2837-2840.
plant communities. Biochem. Syst. Ecol., 5:185- Chew, F. S., and S. P. Courtney. 1991. Plant
193. apparency and evolutionary escape form insect
Chabot, B. F., and D. J. Hicks. 1982. The ecology herbivory. Am. Nat., 138:729-750.
of leaf life spans. Annu. Rev. Ecol. Syst., 13:229- Chew, F. S., andJ. E. Rodman. 1979. Plant re-
259. sources for chemical defense. In G.A. Rosen-
Chalker-Scott, L., and R. L. Krahmer. 1989. Mi- thal and D.H. Janzen (eds.), Herbivores: Their
croscopic studies of tannin formation and dis- Interaction with Secondary Plant Metabolites, pp.
tribution in plant tissues. In R. W. Hem- 271-307. Academic Press, New York.
mingway and J. J. Karchesy (eds.), Chemistry Christiansen, E., R. H. Waring, and A. A. Ber-
and Significance of Condensed Tannins, pp. 345- ryman. 1987. Resistance of conifers to bark
368. Plenum Press, New York. beetle attack: searching for general relation-
Chapin, F. S., III, 1980a. The mineral nutrition ships. For. Ecol. Manage., 22:89-106.

Chung, H.-H., and R. L. Barnes. 1977. Photo- . 1986. Costs and benefits of defense by
synthate allocation in Pinus taeda. I. Substrate tannins in a neotropical tree. Oecologia,70:238-
requirements for synthesis of shoot biomass. 241.
-Can.J. For. Res., 7:106-111. * 1987. Interspecific variation in plant
, and . 1980a. Photosynthate alloca- anti-herbivore properties: the role of habitat
tion in Pinus taeda. II. Seasonal aspects of photo- quality and rate of disturbance. New Phytol.,
synthate allocation to different biochemical 106 (Suppl.):251-263.
fractions in shoots. Can. J. For. Res., 10:338- . 1988. Effects of plant growth rate and leaf
347. lifetime on the amount and type of anti-
, and 1980b. Photosynthate alloca-
herbivore defense. Oecologia, 74:531-536.
tion in Pinus taeda. III. Photosynthate economy:
Coley, P. D., J. P. Bryant, and F. S. Chapin III.
its production, consumption and balance in
1985. Resource availability and plant antiher-
shoots during the growing season. Can. J. For
bivore defense. Science, 230:895-899.
Res., 10:348-356.
Cipollini, M. L., and D. J. Levey. 1991. Why Collin, H. A. 1987. Determinants of yield of sec-
some fruits are green when they are ripe: car- ondary products in plant tissue cultures. Adv.
bon balance in fleshy fruits. Oecologia, 88:371- Bot. Res., 13:145-187.
377. Compton, S. G. 1987. Aganais speciosa and Danaus
Cipollini, M. L., and E. W. Stiles. 1991. Costs of chrysippus(Lepidoptera) sabotage the latex de-
reproduction in Nyssa sylvatica: sexual dimor- fences of their host plants. Ecol. Entomol , 12:
phism in reproductive frequency and nutrient 115-118.
flux. Oecologia, 86:585-593. Compton, S. G., and D. A. Jones. 1985. An inves-
Clancy, K. M., and P. W. Price. 1987. Rapid tigation of the responses of herbivores to cyano-
herbivore growth enhances enemy attack: Sub- genesis in Lotus corniculatusL. Biol. J Linn. Soc.,
lethal plant defenses remain a paradox. Ecology, 26:21-38.
68:733-737. Compton, S. G., D. Newsome, and D. A. Jones.
Clark, D. B., and D. A. Clark. 1988. Leaf produc- 1983. Selection for cyanogenesis in the leaves
tion and the cost of reproduction in the neotrop- and petals of Lotus corniculatusL. at high lati-
ical rain forest cycad, Zamia skinneri. J. Ecol., tudes. Oecologia, 60:353-358.
76:1153-1163.
Cooper, S. M., and N. Owen-Smith. 1986. Effects
Clark, R. J., and R. C. Menary. 1980. The effect
of plant spinescence on large mammalian her-
of irrigation and nitrogen on the yield and com-
bivores. Oecologia, 68:446-455.
position of peppermint oil (Mentha piperita L.).
Cottam, D. A., J. B. Whittaker, and A. J. C.
Aust. J. Agric. Res., 31:489-498.
Clausen, J. J., and T. T. Kozlowski. 1965. Het- Malloch. 1986. The effects of chrysomelid bee-
erophyllous shoots in Betula papyrifera. Nature, tle grazing and plani competition on the growth
205:1030-1031. of Rumex obtusifolius. Oecologia, 70:452-456.
Clay, K. 1988. Fungal endophytes of grasses: a Cotton, C. M., L. V. Evans, andJ. W. Gramshaw.
defensive mutualism between plants and fungi. 1991. The accumulation of volatile oils in whole
Ecology, 69:10-16. plants and cell cultures of tarragon (Artemisia
.1990. Fungal endophytes of grasses. Annu. dracunculus).J. Exp. Bot., 42:365-375.
Rev. Ecol. Syst., 21:275-297. Coughenour, M. B., S. J. McNaughton, and
Coassini Lokar, L. V. Maurich, G. Mellerio, L. L. Wallace. 1985. Responses of an African
M. Moneghini, and L. Poldini. 1987. Varia- tall-grass (Hyparrheniafilipendulastapf.) to defo-
tion in terpene composition of Artemisia alba in liation and limitations of water and nitrogen.
relation to environmental conditions. Biochem. Oecologia, 68:80-86.
Syst. Ecol., 15:327-333. Crankshaw, D. R., andJ. H. Langenheim. 1981.
Cody, M. L. 1966. A general theory of clutch size.
Variation in terpenes and phenolics through
Evolution, 20:174-184.
leaf development in Hymenaea and its possible
Coleman, J. S. 1986. Leaf development and leaf
significance to herbivory. Biochem. Syst. Ecol.,
stress: increased susceptibility associated with
sink-source transition. TreePhysiol. , 2:289-299. 9:115-124.
Coley, P. D. 1980. Effects of leaf age and plant life Crawley, M. J. 1985. Reduction of oak fecundity
history patterns on herbivory. Nature, 284:545- by low density herbivore populations. Nature,
546. 314: 163-164.
1983. Herbivory and defensive character- . 1989a. Insect herbivores and plant popu-
istics of tree species in a lowland tropical forest. lation dynamics. Annu. Rev. Entomol., 34:531-
Ecol. Monogr., 53:209-233. 564.

SEPTEMBER 1992 THE DILEMMA OFPLANTS. TO GROW OR DEFEND 319
. 1989b. The relative importance of verte- Denslow, J. S., J. C. Schultz, P. M. Vitousek,

brate and invertebrate herbivores in plant pop- and B. R. Strain. 1990. Growth responses of
ulation dynamics. In E. A. Bernays (ed.), In- tropical shrubs to treefall gap environments.
sect-Plant Interactions, Vol. 1, pp. 45-71. CRC Ecology, 71:165-179.
Press, Boca Raton. Denslow,J. S., P. M. Vitousek, andJ. C. Schultz.
Crick,J. C., andJ. P. Grime. 1987. Morphologi- 1987. Bioassays of nutrient limitation in a tropi-
cal plasticity and mineral nutrient capture in cal rain forest soil. Oecologia, 74:370-376.
two herbaceous species of contrasted ecology. Dethier, V. G. 1980. Evolution of receptor sensi-
New Phytol., 107:403-414. tivity to secondary plant substances with special
Croteau, R., A. J. Burbott, and W. D. Loomis. references to deterrents. Am. Nat., 115:45-66.
1972. Apparent energy deficiency in mono- and Dicke, M., and M. W. Sabelis. 1990. Does it pay
sesqui-terpene biosynthesis in peppermint. plants to advertize for body guards? Towards
Phytochemistry,11:2937-2948. a cost-benefit analysis of induced synomone
Croxford, A. C., P. J. Edwards, and S. D. Wrat- production. In H. Lambers, M. L. Cambridge,
ten. 1989. Temporal and spatial variation in H. Konings, and T. L. Pons (eds.), Causes and
palatability of soybean and cotton leaves follow- Consequencesof Variationin Growth Rate and Pro-
ing wounding. Oecologia, 79:520-525. ductivityofHigher Plants, pp. 341-358. SPB Aca-
Curtis,J. D., and N. R. Lersten. 1974. Morphol- demic Publishing, The Hague.
ogy, seasonal variation, and function of resin Dicke, M., T. A. Van Beek, M. A. Posthumus,
glands on buds and leaves of Populus deltoides N. Ben Dom, H. Van Bokhoven, and iE De
(Salicaceae). Am. J. Bot., 61:835-845. Groot. 1990. Isolation and identification of vol-
da Cunha, A. 1987. The estimation of L-phenylal- atile kairomone that affects acarine predator-
anine ammonia-lyase shows phenylpropanoid prey interactions. Involvement of host plant in
biosynthesis to be regulated by L-phenylala- its production. J. Chem. Ecol., 16:381-396.
nine supply and availability. Phytochemistry,26: Dickson, R. E. 1989. Carbon and nitrogen alloca-
2723-2727. tion in trees. Ann. Sci. For., 46(Suppl.):631s-
Daie, J. 1988. Mechanism of drought-induced al- 647s.
terations in assimilate partitioning and trans- Dickson, R. E., andJ. G. Isebrands. 1991. Leaves
port in crops. CRC Crit. Rev. Plant Sci., 7:117- as regulators of stress response in plants. In
137. H. A. Mooney, W. E. Winner, and E. J. Pell
Dale, J. E. 1976. Cell division in leaves. In M. M. (eds.), Integrated Response qf Plants to Multiple
Yeoman (ed.), Cell Division in Higher Plants, pp. Stresses, pp. 3-34. Academic Press, New York.
314-345. Academic Press, London. DiCosmo, F., and G. H. N. Towers. 1984. Stress
and secondary metabolism in cultured plant
.1988. The control of leaf expansion. Annu.
cells. Recent Adv. Phytochem., 18:97-175.
Rev. Plant Physiol. Plant Mol. Biol., 39:267-295.
Dietz, K.-J. 1989. Leaf and chloroplast develop-
Danell, K., T. Elmqvist, L. Ericson, and A. Salo-
ment in relation to nutrient availability.J. Plant
monson. 1985. Sexuality in willows and prefer-
Physiol., 134:544-550.
ence by bark-eating voles: Defence or not?
Dillon, P. M., S. Lowrie, and D. McKey. 1983.
Oikos, 44:82-90.
Disarming the "evil woman": Petiole constric-
Danell, K., J. Hjalten, L. Ericson, and T. Elm-
tion by a sphingid larva circumvents mechani-
qvist. 1991. Vole feeding on male and female
cal defenses of its host plant, Cnidoscolus urens
willow shoots along a gradient of plant produc-
(Euphorbiaceae). Biotropica, 15:112-116.
tivity. Oikos, 62:145-152. Dirzo, R. 1984. Herbivory: a phytocentric over-
Dawra, R. K., H. P. S. Makkar, and B. Singh. view. In R. Dirzo and J. Sarukhan (eds.), Per-
1988. Total phenolics, condensed tannins, and spectiveson Plant PopulationBiology, pp. 141-165.
protein-precipitable phenolics in young and Sinauer, Sunderland.
mature leaves of oak species. J. Agric. Food Dirzo, R., andJ. L. Harper. 1982. Experimental
Chem., 36:951-953. studies on slug-plant interactions. IV. The per-
Dell, B., and A. J. McComb. 1978. Plant resins- formance of cyanogenic and acyanogenic
their formation, secretion, and possible func- morphs of Trifolium repensin the field. J. Ecol.,
tions. Adv. Bot. Res., 6:278-3 16. 70:119-138.
del Moral, R. 1972. On the variability of chlo- DiTommaso, A., and L. W. Aarssen. 1989. Re-
rogenic acid concentration. Oecologia, 9:289- source manipulations in natural vegetation: a
300. review. Vegetatio,84:9-29.
Dement, W. A., and H. A. Mooney. 1974. Sea- Dixon, R. A. 1986. The phytoalexin response:
sonal variation in the production of tannins and elicitation, signalling and control of host gene
cyanogenic glucosides in the Chaparral shrub, expression. Biol. Rev. Camb. Philos. Soc., 61:
Heteromelesarbutifolia. Oecologia, 15:65-76. 239-291.

Doberski, J. 1986. Simple phenolic compounds of spider mites to drought stressed host plants.
and the growth of plants: a short review.J. Biol. Ecol. Entomol., 14:45-55.
Educ., 20:96-98. . 1990. Plant drought stress and outbreaks
Dowd, P. F., C. M. Smith, and T. C. Sparks. of spider mites: a field test. Ecology, 71:1401-
1983. Detoxification of plant toxins by insects. 1411.
Insect Biochem., 13:453-468. Entry, J. A., N. E. Martin, K. Cromack, Jr.,
Downhower, J. F. 1975. The distribution of ants and S. G. Stafford. 1986. Light and nutrient
on Cecropialeaves. Biotropica, 7:59-62. limitation in Pinus monticola: seedling suscep-
Duchesne, L. C., and R. E. Brainerd. 1989. Cellu- tibility to Armillaria infection. For. Ecol. Manage.
lose and the evolution of plant life. BioScience, 17:189-198.
39:238-241. Ericsson, A., S. Larsson, and. 0. Tenow. 1980.
Dussourd, D. E., andR. F. Denno. 1991. Deacti- Effects of early and late season defoliation on
vation of plant defense: correspondence be- growth and carbohydrate dynamics in Scots
tween insect behavior and secretory canal ar- pine.J Appl. Ecol., 17:747-769.
chitecture. Ecology, 72:1383-1396. Ernest, K. A. 1989. Insect herbivory on a tropical
Dussourd, D. E., and T. Eisner. 1987. Vein- understory tree: effects of leaf age and habitat.
cutting behavior: insect counterploy to the latex Biotropica, 21:194-199.
defense of plants. Science, 237:898-901. Fagerstrom, T. 1989. Anti-herbivory chemical de-
Ebel, J. 1986. Phytoalexin synthesis: the biochem- fense in plants: a note on the concept of cost.
ical analysis of the induction process. Annu. Rev. Am. Nat., 133:281-287.
Phytopathol., 24:235-264. Fagerstr6m, T., S. Larsson, and O. Tenow. 1987.
Edwards, P. J., and S. D. Wratten. 1983. Wound On optimal defence in plants. Funct. Ecol., 1:
induced defences in plants and their conse- 73-81.
quences for patterns of insect grazing. Oecologia, Fahn, A. 1988. Secretory tissues in vascular
59:88-93. plants. New Phytol., 108:229-257.
, and . 1987. Ecological significance Fajer, E. D. 1989. The effects of enriched CO2
of wound-induced changes in plant chemistry. atmospheres on plant-insect herbivore interac-
In V. Labeyrie, G. Fabres, and D. Lachaise tions: growth responses of larvae of the specialist
(eds.), Insects-Plants, pp. 213-218 Junk, Dor- butterfly, Junonia coenia (Lepidoptera: Nymph-
drecht. alidae). Oecologia, 81:514-520.
Ehrlich, P. R., and P. H. Raven. 1964. Butterflies Fajer, E. D., M. D. Bowers, and F. A. Bazzaz.
and plants: a study in coevolution. Evolution, 1989. The effects of enriched carbon dioxide
18:586-608. atmospheres on plant-insect herbivore interac-
Eilert, U. 1987. Elicitation: methodology and as- tions. Science, 243:1198-1200.
pects of application. In F. Constabel and I. K. Farrar, J. F., and M. L. Williams. 1991. The
Vasil (eds.), Cell Cultureand Somatic Cell Genetics effects of increased atmospheric carbon dioxide
and temperature on carbon partitioning, source-
of Plants, Vol. 4: Cell Culture in Phytochemis-
sink relations and respiration. Plant Cell Envi-
try, pp. 153-196. Academic Press, San Diego.
ron., 14:819-830.
Eisner, T., J. S. Johnessee, J. Carrel, L. B.
Feeny, P. 1976. Plant apparency and chemical de-
Hendry, andJ. Meinwald. 1974. Defensive use
fense. Recent Adv. Phytochem., 10: 1-40.
by an insect of a plant resin. Science, 184:996-
Fernandes, G. W. 1990. Hypersensitivity: a ne-
999.
glected plant resistance mechanism against in-
Ellis, W. M., R. J. Keymer, and D. A. Jones.
sect herbivores. Environ. Entomol., 19:1173-
1977a. On the polymorphism of cyanogenesis 1182.
in Lotus corniculatusL. VIII. Ecological studies Firmage, D. H. 1981. Environmental influences
in Anglesey. Heredity, 39:45-65. on the monoterpene variation in Hedeomadrum-
, and . 1977b. The defen- mondii. Biochem. Syst. Ecol., 9:53-58.
sive function of cyanogenesis in natural popula- Foulds, W., andJ. P. Grime. 1972. The response
tions. Experientia, 33:309-311. of cyanogenic and acyanogenic phenotypes of
Elmqvist, T., L. Ericson, K. Danell, and A. Salo- Trifolium repensto soil moisture supply. Heredity,
monson. 1987. Flowering, shoot production, 28: 181-187.
and vole bark herbivory in a boreal willow. Fowler, N. 1986. The role of competition in plant
Ecology, 68:1623-1629. communities in arid and semiarid regions.
and . 1988. Lati- Annu. Rev. Ecol. Syst., 17:89-110.
tudinal sex ratio variation in willows, Salix spp., Fowler, N. L., and M. D. Rausher. 1985. Joint
and gradients in vole herbivory. Oikos, 51:259- effects of competitors and herbivores on growth
266. and reproduction in Aristolochia reticulata. Ecol-
English-Loeb, G. M. 1989. Nonlinear responses ogy, 66:1580-1587.

Fowler, S. V., andJ. H. Lawton. 1985. Rapidly Gifford, R. M., and L. T. Evans. 1981. Photosyn-
induced defenses and talking trees: the devil's thesis, carbon partitioning, and yield. Annu.
advocate position. Am. Nat., 126:181-195. Rev. Plant Physiol., 32:485-509.
Foyer, C. H. 1987. The basis for source-sink inter- Gifford, R. M.,J. H. Thorne, W. D. Hitz, and
action in leaves. Plant Physiol. Biochem., 25:649- R. T. Giaquinta. 1984. Crop productivity and
657. photoassimilate partitioning. Science, 255:801-
1988. Feedback inhibition of photosyn- 808.
thesis through source-sink regulation in leaves. Gill, D. E. 1986. Individual plants as genetic mo-
Plant Physiol. Biochem., 26:483-492. saics: ecological organisms versus evolutionary
Fraenkel, G. S. 1959. The raisond'etreof secondary individuals. In M.J. Crawley (ed.), Plant Ecol-
plant substances. Science, 129:1466-1470. ogy, pp. 321-343. Blackwell Scientific, Oxford.
Frischknecht, P. M., M. Battig, and T. Baumann. Gilliland, M. G., M. R. Appleton, andJ. Van
1987. Effect of drought and wounding stress on Staden. 1988. Gland cells in resin canal epithe-
indole alkaloid formation in Catharanthusroseus. lia in guayule (Partheniumargentatum)in relation
Phytochemistry,26:707-710. to resin and rubber production. Ann. Bot., 61:
Frischknecht, P. M., J. Ulmer-Dufek, and T. W. 55-64.
Baumann. 1986. Purine alkaloid formation in Gilmore, A. R. 1977. Effects of soil moisture stress
buds and developing leaflets of Coffea arabica: on monoterpenes in loblolly pine. J. Chem.
expression of an optimal defence strategy? Phy- Ecol., 3:667-676.
tochemistry,25:613-616. Glyphis, J. P., and G. M. Puttick. 1989. Pheno-
Fritz, R. S. 1990. Effects of genetic and environ- lics, nutrition and insect herbivory in some gar-
mental variation on resistance of willow to saw- rigue and maquis plant species. Oecologia, 78:
flies. Oecologia, 82:325-332. 259-263.
Fritz, R. S., and P. W. Price. 1988. Genetic varia- Goldberg, D. E. 1990. Components of resource
tion among plants and insect community struc- competition in plant communities. In J. B.
ture: willows and sawflies. Ecology, 69:845-856. Grace and D. Tilman (eds.), Perspectiveson Plant
Fujimori, N., T. Suzuki, and H. Ashihara. 1991. Competition, pp. 27-49. Academic Press, San
Seasonal variations in biosynthetic capacity for Diego.
the synthesis of caffeine in tea leaves. Phytochem- Gottlieb, 0. R. 1989. The role of oxygen in phyto-
istry, 30:2245-2248. chemical evolution towards diversity. Phyto-
Futuyma, D.J., and G. Moreno. 1988. The evolu- chemistry, 28:2545-2558.
tion of ecological specialization. Annu. Rev. .1990. Phytochemicals: differentiation and
Ecol. Syst., 19:207-233. function. Phytochemistry,29:1715-1724.
Gale, J., and M. Zeroni. 1985. The cost to plants
Gray,J. C. 1987. Control of isoprenoid biosynthe-
of different strategies of adaptation to stress and
sis in higher plants. Adv. Bot. Res., 14:25-91.
the alleviation of stress by increasing assimila-
Greenslade, P. J. M. 1983. Adversity selection
tion. Plant Soil, 89:57-67.
and the habitat templet. Am. Nat., 122:352-
Gartlan, S. J., D. B. Mckey, P. G. Waterman,
365.
C. N. Mbi, and T. S. Struhsaker. 1980. A
Grime, J. P. 1977. Evidence for the existence of
comparative study of the phytochemistry of two
three primary strategies in plants and its rele-
African rain forests. Biochem. Syst. Ecol., 8:40 1-
vance to ecological and evolutionary theory.
422.
Am. Nat., 111:1169-1194.
Gaudet, C. L., and P. A. Keddy. 1988. A compar-
ative approach to predicting competitive ability .1979. Plant Strategiesand VegetationProcesses.
from plant traits. Nature, 334:242-243. Wiley, Chichester.
Georgiadis, N.J., R. W. Ruess, S. J. McNaugh- Grime,J. P.,J. C. Crick, andJ. E. Rincon. 1986.
ton, and D. Western. 1989. Ecological condi- The ecological significance of plasticity. In
tions that determine when grazing stimulates D. H. Jennings and A. J. Trewavas (eds.), Plas-
grass production. Oecologia, 81:316-322. ticity in Plants, pp. 5-29. The Company of Biolo-
Gershenzon,J. 1984. Changes in the levels of plant gists Limited, Cambridge.
secondary metabolites under water and nutri- Grime, J. P., and R. Hunt. 1975. Relative growth-
ent stress. In B. N. Timmermann, C. Steelink, rate: its range and adaptive significance in a
and F. A. Leows (eds.), PhytochemicalAdaptations local flora. J. Ecol., 63:393-422.
to Stress. Plenum Press, New York. Grubb, P. J. 1986. Sclerophylls, pachyphylls and
Gibberd, R., P. J. Edwards, and S. D. Wratten. pyncophylls: the nature and significance of hard
1988. Wound-induced changes in the accept- leaf surfaces. In B. Juniper and R. Southwood
ability of tree-foliage to Lepidoptera: within- (eds.), Insects and the Plant Surface, pp. 137-150.
leaf effects. Oikos, 51:43-47. Edward Arnold, London.

Gulmon, S. L., and H. A. Mooney. 1986. Costs foliators: defensive or incidental? Ecology, 66:
of defense and their effects on plant productiv- 1303-1308.
ity. In T. J. Givnish (ed.), On the Economy of Haukioja, E., and P. Niemela. 1979. Birch leaves
Plant Form and Function, pp. 681-698. Cam- as a resource for herbivores: seasonal occur-
bridge University Press, Cambridge. rence of increased resistance in foliage after me-
Gutschick, V. P. 1981. Evolved strategies in nitro- chanical damage of adjacent leaves. Oecologia,
gen acquisition by plants. Am. Nat., 118:607- 39: 151-159.
637. Haukioja, E., K. Ruohomaki, J. Senn, J. Suo-
Halle, F. 1986. Modular growth in seed plants. mela, and M. Walls. 1990. Consequences of
Philos. Trans. R. Soc. Lond. B. Biol. Sci., 313: herbivory in the mountain birch (Betula pu-
77-87. bescensssp tortuosa):importance of the functional
Hanover, J. W. 1966a. Environmental variation organization of the tree. Oecologia,82:238-247.
in the monoterpenes of Pinus monticola Dougl. Haukioja, E., K. Ruohomaki, J. Suomela, and
Phytochemistry,5:713-717. T. Vuorisalo. 1991. Nutritional quality as a
. 1966b. Genetics of terpenes. I. Gene con- defense against herbivores. For. Ecol. Manage.,
trol of monoterpene levels in Pinus monticola 39:237-245.
Dougl. Heredity, 21:73-84. Haukioja, E., J. Suomela, and S. Neuvonen.
1985. Long-term inducible resistance in birch
Harborne, J. B. 1990. Constraints on the evolu-
foliage: triggering cues and efficacy on a defoli-
tion of biochemical pathways. Biol. J. Linn.
ator. Oecologia, 65:363-369.
Soc., 39:135-151.
Hay, M. E., and W. Fenical. 1988. Marine plant-
Hardwick, R. C. 1986. Physiological consequences
herbivore interactions: the ecology of chemical
of modular growth in plants. Philos. Trans. R.
defense. Annu. Rev. Ecol. Syst., 19:111-145.
Soc. Lond. B. Biol. Sci., 313:161-173.
Hegerhorst, D. F., R. B. Bhat, D. J. Weber, and
Harper, J. L. 1989. The value of a leaf. Oecologia,
E. D. McArthur. 1988. Seasonal changes of
80:53-58.
selected secondary plant products in Chryso-
Harper, J. L. and A. D. Bell. 1979. The popula- thamnusnauseosusssp. turbinatus. GreatBasin Nat.
tion dynamics of growth form in organisms Mem., 48:1-8.
with modular construction. In R. M. Ander- Hegnauer, R. 1988. Biochemistry, distribution
son, B. D. Taylor, and L. R. Taylor (eds.), and taxonomic relevance of higher plant alka-
Population Dynamics, pp. 29-52. Blackwell Sci- loids. Phytochemistry,27:2423-2427.
entific, Oxford. Heichel, G. H., and N. C. Turner. 1983. CO2
Harper, J. L. and J. White. 1974. The demogra- assimilation of primary and regrowth foliage of
phy of plants. Annu. Rev. Ecol. Syst., 5:419-463. red maple (Acer rubrumL.) and red oak (Quercus
Hartwig, U. A., C. A. Maxwell, C. M. Joseph, rubraL.): response to defoliation. Oecologia,57:
and D. A. Phillips. 1990. Chrysoeriol and lute- 14-19.
olin released from alfalfa seeds induce nod genes Hendrix, S. D. 1988. Herbivory and its impact on
in Rhizobium meliloti. Plant Physiol., 92:116-122. plant reproduction. In J. L. Doust and L. L.
Haslam, E. 1986. Secondary metabolism-fact Doust (eds.), Plant ReproductiveEcology: Patterns
and fiction. Nat. Prod. Rep., 3:217-249. and Strategies, pp. 246-263. Oxford University
1988. Plant polyphenols (syn. vegetable Press, New York.
tannins) and chemical defense -a reappraisal. Hendry, G. 1986. Why do plants have cytochrome
J. Chem. Ecol., 14:1789-1805. P-450? Detoxification versusdefence. New Phy-
Hatcher, P. E. 1990. Seasonal and age-related tol., 102:239-247.
variation in the needle quality of five conifer Hilbert, D. W. 1990. Optimization of plant root:
species. Oecologia, 85:200-212. shoot ratios and internal nitrogen concentra-
tion. Ann. Bot., 66:91-99.
Haukioja, E. 1980. On the role of plant defences in
the fluctuation of herbivore populations. Oikos, Hilbert, D. W., A. Larigauderie, andJ. F. Reyn-
olds. 1991. The influence of carbon dioxide and
35:202-213.
daily photon-flux density on optimal leaf nitro-
. 1982. Inducible defences of white birch to
gen concentration and root:shoot ratio. Ann.
a geometrid defoliator, Epirrita autumnata. Pro-
Bot., 68:365-376.
ceedings of the Fifth International Symposium on Hirose, T. 1988a. Nitrogen availability, optimal
Insect-Plant Relationships, pp. 199-203. Pudoc, shoot/root ratios and plant growth. In M. J. A.
Wageningen. Werger, P. J. M. van der Aart, H. J. During,
. 1990. Induction of defenses in trees. Annu. and J. T. A. Verhoeven (eds.), Plant Form and
Rev. Entomol., 36:25-42. VegetationStructure:Adaptation, Plasticity and Rela-
Haukioja, E., and S. Neuvonen. 1985. Induced tion to Herbivory, pp. 135-145. SPB Academic
long-term resistance of birch foliage against de- Publushing, The Hague.

. 1988b. Modelling the relative growth rate enzymes of phenylpropanoid pathways in de-
as a function of plant nitrogen concentration. veloping parsley seedlings. Planta, 173:453-
Physiol. Plant., 72:185-189. 458.
Ho, L. C. 1988. Metabolism and compartmenta- Jalal, M. A. F., and H. A. Collin. 1977. Polyphe-
tion of imported sugars in sink organs in rela- nols of mature plant, seedling and tissue cul-
tion to sink strength. Annu. Rev. Plant Physiol. tures of Theobromacacao. Phytochemistry,16:1377-
Mol. Biol., 39:355-378. 1380.
Hoffmann, A. J., and M. C. Alliende. 1984. Inter- Janzen, D. H. 1966. Coevolution of mutualism
actions in the patterns of vegetative growth and between ants and acacias in Central America.
reproduction in woody dioecious plants. Oeco- Evolution, 20:249-275.
logia, 61:109-114. . 1971. Seed predation by animals. Annu.
Hoffmann, P. 1985. Ecophysiological aspects of Rev. Ecol Syst., 4:465-493.
biomass production in higher plants. Photosynth. . 1972. Protection of Barteria (Passiflora-
Res., 7:3-17. ceae) by Pachysimaants (Pseudomyrmecinae) in
Horner, J. D. 1988. Astringency of Douglas-fir a Nigerian rain forest. Ecology, 53:885-892.
foliage in relation to phenology and xylem pres- . 1974. Tropical blackwater rivers, ani-
sure potential. J. Chem. Ecol., 14:1227-1237. mals, and mast fruiting by the Dipterocarpa-
. 1990. Nonlinear effects of water deficits ceae. Biotropica, 6:69-103.
on foliar tannin concentration. Biochem. Syst. . 1979. New horizons in the biology of plant
Ecol., 18:211-213. defenses. In G. A. Rosenthal and D. H. Janzen
Hosner,J. F., A. L. Leaf, R. Dickson, andJ. B. (eds.), Herbivores. Their Interactionwith Secondary
Hart, Jr. 1965. Effects of varying soil moisture Plant Metabolites, pp. 33 1-350. Academic Press,
upon the nutrient uptake of four bottomland Orlando.
tree species. Soil Sci. Soc. Am. Proc., 29:313- Jensen, R. A. 1985. The shikimate/arogenate path-
316. way: link between carbohydrate metabolism
Hrazdina, G., and G.J. Wagner. 1985. Compart- and secondary metabolism. Physiol. Plant., 66:
mentation of plant phenolic compounds; sites 164-168.
of synthesis and accumulation. In C. F. van Jerling, L. 1985. Are plants and animals alike? A
Sumere and P. J. Lea (eds.), Annual Proceedings note on evolutionary plant population ecology.
of thePhytochemicalSocietyof Europe, Vol. 25: The Oikos, 45:150-153.
Biochemistry of Plant Phenolics, pp. 119-133. Jermy, T. 1984. Evolution of insect/host plant re-
Clarendon Press, Oxford. lationships. Am. Nat., 124:609-630.
Hrutfiord, B. F., and R. I. Gara. 1989. The ter- Jing, S. W., and P. D. Coley. 1990. Dioecy and
pene complement of slow and fast growing
herbivory: the effect of growth rate on plant
Sitka spruce terminals as related to Pissodesstrobi
defense in Acer negundo. Oikos, 58:369-377.
(Peck) (Col., Curculionidae) host selection.].
Johnson, N. D., S. A. Brain, and P. R. Ehrlich.
Appl. Entomol., 108:21-23.
1985. The role of leaf resin in the interaction
Hsiao, T. C. 1973. Plant responses to water stress.
between Eriodictyon californicum (Hydrophylla-
Annu. Rev. Plant Physiol., 24:519-570.
ceae) and its herbivore, Trirhabda diducta
Hughes, M. A. 1991. The cyanogenic polymor-
(Chrysomelidae). Oecologia, 66:106-1 10.
phism in Trifolium repensL. (white clover). He-
Johnson, N. D., C. C. Chu, P. R. Ehrlich, and
redity, 66:105-115.
Hughes, P. R. 1974. Myrcene: a precursor of H. A. Mooney. 1984. The seasonal dynamics
pheromones in Ips beetles.]. InsectPhysiol., 20: of leaf resin, nitrogen, and herbivore damage
1271-1275. in Eriodictyoncalifornicumand their parallels in
Hunt, R. 1978. Plant GrowthAnalysis. Edward Ar- Diplacus aurantiacus. Oecologia, 61:398-402.
nold, London. Johnson, R. H., and D. E. Lincoln. 1990. Sage-
Huston, M., and T. Smith. 1987. Plant succes- brush and grasshopper responses to atmo-
sion: life history and competition. Am. Nat., spheric carbon dioxide concentration. Oeco-
130: 168-198. logia, 84:103-1 10.
Idso, S. B., and B. A. Kimball. 1988. Atmospheric Jones, C. G., and R. D. Firn. 1991. On the evolu-
CO2 enrichment and plant dry matter content. tion of plant secondary chemical diversity. Phi-
Agric. For. Meteorol., 43:171-181. los. Trans. R. Soc. Lond. Biol. Sci., 333:273-280.
Jacobs, M., and P. H. Rubery. 1988. Naturally Jones, D. A., R. J. Keymer, and W. M. Ellis.
occurring auxin transport regulators. Science, 1978. Cyanogenesis in plants and animal feed-
241:346-349. ing. InJ. B. Harborne (ed.), BiochemicalAspects
Jahnen, W., and K. Hahlbrock. 1988. Differential of Plant and Animal Coevolution,pp. 21-34. Aca-
regulation and tissue-specific distribution of demic Press, London.

Juvik,J. A., and M. A. Stevens. 1982. Inheritance oecious shrub Baccharis halimifolia (Composi-
of foliar a-tomatine content in tomatoes.J. Am. tae). Oecologia, 83:182-190.
Soc. Hortic. Sci., 107:1061-1065. Kubo, I., and F. J. Hanke. 1985. Multifaceted
Kadmon, R., and A. Shmida. 1990. Competition chemically based resistance in plants. Recent
in a variable environment: an experimental Adv. Phytochem., 19:171-194.
study in a desert annual plant population. Isr. Kursar, T. A., and P. D. Coley. 1991. Nitrogen
J. Bot., 39:403-412. content and expansion rate of young leaves of
Kakes, P. 1989. An analysis of the costs and bene- rain forest species: implications for herbivory.
fits of the cyanogenic system in Trifolium repens Biotropica 23:141-150.
L. Theor. Appl. Genet., 77:111-118. Laine, K. M., and H. Henttonen. 1987. Pheno-
. 1990. Properties and functions of the cy- lics/nitrogen ratios in the blueberry Vaccinium
anogenic system in higher plants. Euphytica, 48: myrtillus in relation to temperature and micro-
25-43. tine density in Finnish Lapland. Oikos, 50:389-
Kato, M. 1978. Phenols as indispensible compo- 395.
nents of the synthetic diet of the silkworm, Bom- Lambers, H. 1987. Does variation in photosyn-
byx mori. Entomol. Exp. Appl., 24:285-290. thetic rate explain variation in growth rate and
Keddy, P. A. 1989. Competition. Chapman and yield? Neth. J. Agric. Sci., 35:505-519.
Hall, London. Lambers, H., and A. M. Rychter. 1990. The bio-
Kim, E.-S., and P. G. Mahlberg. 1991. Secretory chemical background of variation in respira-
cavity development in glandular trichomes of tion rate: respiratory pathways and chemical
Cannabis sativa L. (Cannabaceae). Am. J. Bot., composition. In H. Lambers, M. L. Cam-
78:220-229. bridge, H. Konings, and T. L. Pons (eds.),
Kimberling, D. N., E. R. Scott, and P. W. Price. Causesand Consequencesof Variationin GrowthRate
1990. Testing a new hypothesis: plant vigor and Productivity of Higher Plants, pp. 199-225.
and phylloxera distribution on wild grape in SPB Academic Publishing, The Hague.
Arizona. Oecologia, 84:1-8. Langenheim,J. H., S. P. Arrhenius,J. C. Nasci-
Kimura, M., and H. Wada. 1989. Tannins in mento. 1981. Relationship of light intensity to
mangrove tree roots and their role in the root leaf resin composition and yield in the tropical
environment. Soil Sci. Plant Nutr., 35:101-108. Leguminous genera Hymenaea and Copaifera.
Kolodny-Hirsch, D. M., J. A. Saunders, and Biochem. Syst. Ecol., 9:27-37.
F. P. Harrison. 1986. Effects of simulated to- Lapinjoki, S. P., H. A. Elo, and H. T. Taipale.
bacco hornworm (Lepidoptera: Sphingidae) 1991. Development and structure of resin
defoliation on growth dynamics and physiology glands on tissues of Betulapendula Roth. during
growth. New Phytol., 117:219-223.
of tobacco as evidence of plant tolerance to leaf
Larsson, S., A. Wiren, L. Lundgren, and T. Er-
consumption. Environ. Entomol., 15:1137-1144.
icsson. 1986. Effects of light and nutrient stress
Koops, A. J., and H. W. Groeneveld. 1991. Tri-
on leaf phenolic chemistry in Salix dasycladosand
terpenoid biosynthesis in the etoliated seedling
susceptibility to Galerucellalineola (Coleoptera).
of Euphorbia lathyris L. Developmental changes
Oikos, 47:205-210.
and the regulation of local triterpenoid produc-
Lawton,J. H., and S. McNeill. 1979. Between the
tion. J. Plant Physiol., 138:142-149.
devil and the deep blue sea: on the problem of
Koptur, S. 1985. Alternative defenses against her- being a herbivore. Symp. Br. Ecol. Soc., 20:223-
bivores in Inga (Fabaceae: Mimosoideae) over 244.
an elevational gradient. Ecology, 66:1639-1650. Lee, D. W., andJ. B. Lowry. 1980. Young-leaf
K6rner, Ch. 1991. Some often overlooked plant anthocyanin and solar ultraviolet. Biotropica,
characteristics as determinants of plant growth: 12:75-76.
a reconsideration. Funct. Ecol., 5:162-173. Lee, J. A., R. Harmer, and R. Ignaciuk. 1981.
Kozlowski, T. T., andJ.J. Clausen. 1966. Shoot Nitrogen as a limiting factor in plant communi-
growth characteristics of heterophyllous woody ties. InJ. A. Lee, S. McNeill, and I. H. Rori-
plants. Can. J. Bot., 44:827-843. son (eds.), Nitrogen as an Ecological Factor, pp.
Krischik, V. A., and R. F. Denno. 1983. Individ- 95-112. Blackwell Scientific, Oxford.
ual, population, and geographic patterns in Les, D. H., and D.J. Sheridan. 1990. Biochemical
plant defense. In R. F. Denno and M. S. Mc- heterophylly and flavonoid evolution in North
Clure (eds.), VariablePlants and Herbivoresin Nat- American Potamogeton(Potamogetonaceae). Am.
ural and Managed Systems, pp. 463-512. Aca- J. Bot., 77:453-465.
demic Press, New York. Letourneau, D. K. 1983. Passive aggression: an
and . 1990. Patterns of growth, alternative hypothesis for the Piper-Pheidoleas-
reproduction, defense, and herbivory in the di- sociation. Oecologia, 60:122-126.

Levin, D. A. 1973. The role of trichomes in plant rapae to natural enemies. Ecology, 72:1586-
defense. Q. Rev. Biol., 48:3-15. 1590.
. 1976a. The chemical defenses of plants Loehle, C. 1988. Tree life history strategies: the
to pathogens and herbivores. Annu. Rev. Ecol. role of defenses. Can. . For. Res., 18:209-222.
Syst., 7:121-159. Loomis, R. S., Y. Luo, and P. L. Kooman. 1990.
* 1976b. Alkaloid-bearing plants: an eco- Integration of activity in the higher plant. In
geographic perspective. Am. Nat., 110:261- R. Rabinge, J. Goudriaan, H. van Keulen,
284. F. W. T. Penning de Vries, and H. H. van
Lewinsohn, E., M. Gijzen, and R. Croteau. 199 1. Laar (eds.), TheoreticalProductionEcology. Reflec-
Defense mechanisms of conifers. Differences in tions andProspects, pp. 105-124. Pudoc, Wagen-
constitutive and wound-induced monoterpene ingen.
biosynthesis among species. Plant Physiol., 96: Loomis, W. E. 1932. Growth-differentiation bal-
44-49. ance vs. carbohydrate-nitrogen ratio. Proc. Am.
Lewinsohn, E., M. Gijzen, T. J. Savage, and Soc. Hortic. Sci., 29:240-245.
R. Croteau. 1991. Defense mechanisms of co- . 1953. Growth and differentiation-an in-
nifers. Relationship of monoterpene cyclase ac- troduction and summary. In W. E. Loomis
tivity to anatomical specialization and oleoresin (ed.), Growth and Differentiation in Plants, pp.
monoterpene content. Plant Physiol., 96:38-43. 1-17. Iowa State College Press, Ames.
Lightfoot, D. C., and W. G. Whitford. 1987. Lorio, P. L., Jr. 1986. Growth-differentiation bal-
Variation in insect densities on desert creo- ance: a basis for understanding southern pine
sotebush: Is nitrogen a factor? Ecology, 68:547- beetle-tree interactions. For. Ecol. Manage., 14:
557. 259-273.
,and . 1989. Interplant variation in . 1988. Growth and differentiation-balance
creosotebush foliage characteristics and canopy relationships in pines affect their resistance to
arthropods. Oecologia, 81:166-175. bark beetles (Coleoptera: Scolytidae). In W. J.
Lincoln, D. E., and D. Couvet. 1989. The effect of Mattson, J. Levieux, and C. Bernard-Dagan
carbon supply on allocation to allelochemicals (eds.), Mechanismsof WoodyPlant DefensesAgainst
and caterpillar consumption of peppermint. Insects. Searchfor Pattern, pp. 73-92. Springer-
Oecologia, 78:112-114. Verlag, New York.
Lincoln, D. E., D. Couvet, and N. Sionit. 1986. Lorio, P. L.,Jr., and R. A. Sommers. 1986. Evi-
dence of competition for photosynthates be-
Response of an insect herbivore to host plants
grown in carbon dioxide enriched atmo- tween growth processes and oleoresin synthesis
in Pinus taeda L. Tree Physiol., 2:30 1-306.
spheres. Oecologia, 69:556-560.
Louda, S. M. 1984. Herbivore effect on stature,
Lincoln, D. E., andJ. H. Langenheim. 1978. Ef-
fruiting, and leaf dynamics of a native crucifer.
fect of light and temperature on monoterpenoid
Ecology, 65:1379-1386.
yield and composition in Saturejadouglasii. Bio-
Louda, S. M., K. H. Keeler, and R. D. Holt.
chem. Syst. Ecol., 6:21-32.
1990. Herbivore influence on plant perfor-
, and . 1979. Variation of Satureja
mance and competitive interactions. In J. B.
douglasii monoterpenoids in relation to light in-
Grace and D. Tilman (eds.), Perspectiveson Plant
tensity and herbivory. Biochem. Syst. Ecol., 7:
Competition,pp. 413-444. Academic Press, San
289-298. Diego.
Lincoln, D. E., and H. A. Mooney. 1984. Herbiv- Loveless, A. R. 1962. Further evidence to support
ory on Diplacus aurantiacus shrubs in sun and a nutritional interpretation of sclerophylly.
shade. Oecologia, 64:173-176. Ann. Bot., 26:551-561.
Lindroth, R. L. 199 1. Differential toxicity of plant Lovett Doust, J. 1980. Experimental manipula-
allelochemicals to insects: roles of enzymatic tion of patterns of resource allocation in the
detoxification systems. In E. A. Bernays (ed.), growth cycle reproduction of Smyrniumolusatrum
Insect-PlantInteractions,Vol. III, pp. 2-33. CRC L. Biol. J. Linn. Soc., 13:155-166.
Press, Boca Raton. Lovett Doust, J., and L. Lovett Doust. 1985. Sex
Lindsey, K., and M. M. Yeoman. 1983. The rela- ratios, clonal growth and herbivory in Rumex
tionship between growth rate, differentiation acetosella. In J. White (ed.), Studies on Plant De-
and alkaloid accumulation in cell cultures. J mography:A Festschriftfor John L. Harper, pp.
Exp. Bot., 34:1055-1065. 327-341. Academic Press, London.
Lloyd, D. G., and C. J. Webb. 1977. Secondary Luckner, M. 1980. Expression and control of sec-
sex characters in plants. Bot. Rev., 43:177-216. ondary metabolism. In E. A. Bell and B. V.
Loader, C., and H. Damman. 1991. Nitrogen Charlwood (eds.), SecondaryPlant Products,Vol.
content of food plants and vulnerability of Pieris 8, pp. 23-63. Springer-Verlag, Berlin.

Luckner, M., and L. Nover. 1977. Expression of lates in Lolium multflorum Lam. Ann. Bot., 29:
secondary metabolism: an aspect of cell spe- 365-370.
cialization of microorganisms, higher plants, Maschinski, J., and T. G. Whitham. 1989. The
and animals. In M. Luckner, L. Nover, and continuum of plant responses to herbivory: the
H. Bohm (eds.), SecondaryMetabolism and Cell influence of plant association, nutrient avail-
Differentiation, pp. 2-102. Springer-Verlag, ability, and timing. Am. Nat., 134:1-19.
Berlin. Matson, P. A., and R. H. Waring. 1984. Effects
Lundberg, P., and M. Astrom. 1990. Low nutri- of nutrient and light limitation on mountain
tive quality as a defense against optimally for- hemlock: susceptibility to laminated root rot.
aging herbivores. Am. Nat., 135:547-562. Ecology, 65:1517-1524.
Luxmore, R. J. 1991. A source-sink framework
Mattson, W. J. 1980. Herbivory in relation to
for coupling water, carbon, and nutrient dy-
plant nitrogen content. Annu. Rev. Ecol. Syst.,
namics of vegetation. TreePhysiol., 9:267-280.
11:119-161.
Lynn, D. G., and M. Chang. 1990. Phenolic sig-
Mattson, W. J., and N. D. Addy. 1975. Phytopha-
nals in cohabitation: implications for plant de-
gous insects as regulators of forest primary pro-
velopment. Annu. Rev. Plant Physiol Plant Mol.
duction. Science, 190:515-522.
Biol., 41:497-526.
Mattson, W. J., and R. A. Haack. 1987a. The
MacLean, S. F.,Jr., andT. S.Jensen. 1985. Food
plant selection by insect herbivores in Alaskan role of drought stress in provoking outbreaks of
arctic tundra: the role of plant life form. Oikos, phytophagous insects. In P. Barbosa andJ. C.
44:211-221. Schultz (eds.), Insect Outbreaks, pp. 365-407.
Maddox, G. D., and R. B. Root. 1987. Resistance Academic Press, New York.
to 16 diverse species of herbivorous insects , and . 1987b. The role of drought
within a population of goldenrod, Solidago altis- in outbreaks of plant-eating insects. BioScience,
sima: genetic variation and heritability. Oeco- 37:110-118.
logia, 72:8-14. Mattson, W. J., D. A. Herms, J. A. Witter, and
Maffei, M. 1990. Plasticity and genotypic varia- D. C. Allen. 1991. Woody plant grazing sys-
tion in some Mentha x verticillatahybrids. Bio- tems: North American outbreak folivores and
chem. Syst. Ecol., 18:493-502. their host plants. In Y. N. Baranchikov, W. J.
Mahmoud, A., andJ. P. Grime. 1976. An analysis Mattson, F. P. Hain, and T. L. Payne (eds.),
of competitive ability in three perennial ForestInsect Guilds: Patternsof Interactionwith Host
grasses. New Phytol., 77:431-435. Trees, pp. 53-84. U.S. Dep. Agric. Northeast
Margna, U. 1977. Control at the level of substrate For. Exp. Stn., Radnor, Pa., Gen. Tech. Rep.
supply-an alternative in the regulation of phe- NE-153.
nylpropanoid accumulation in plant cells. PhIy- Mattson, W. J., R. K. Lawrence, R. A. Haack,
tochemistry, 16:419-426. D. A. Herms, and P. J. Charles. 1988. Defen-
Margna, U., E. Margna, and T. Vainjarv. 1989. sive strategies of woody plants against different
Influence of nitrogen nutrition on the utiliza- insect-feeding guilds in relation to plant ecolog-
tion of L-phenylalanine for building flavonoids ical strategies and intimacy of association with
in buckwheat seedling tissues. J. Plant Physiol.,
insects. In W. J. Mattson, J. Levieux, and
134:697-702. C. Bernard-Dagan (eds.), Mechanisms of Woody
Marquis, R. J. 1984. Leaf herbivores decrease fit-
Plant Defenses Against Insects: Searchfor Pattern,
ness of a tropical plant. Science, 226:537-539.
pp. 3-38. Springer-Verlag, New York.
. 1988. Intra-crown variation in leaf her-
Mattson, W. J., N. Lorimer, and R. A. Leary.
bivory and seed production in striped maple,
1982. Role of plant variability (trait vector dy-
AcerpensylvanicumL. (Aceraceae). Oecologia,77:
51-55. namics and diversity) in plant/herbivore inter-
. 1990. Genotypic variation in leaf damage actions. In H. M. Heybroek, B. R. Stephan,
in Piper arieianum(Piperaceae) by a multispecies and K. von Weissenberg (eds.), Resistance to
assemblage of herbivores. Evolution, 44:104- Diseases and Pests in Forest Trees, pp. 295-303.
120. Pudoc, Wageningen.
.1991. Evolution of resistance in plants to Mattson, W.J., andJ. M. Scriber. 1987. Nutri-
herbivores. Evol. Trends Plants, 5:23-29. tional ecology of insect folivores of woody
. 1992. A bite is a bite is a bite? Constraints plants: nitrogen, water, fiber, and mineral con-
on response to folivory in Piper arieianum (Pip- siderations. In F. Slansky andJ. G. Rodriguez
eraceae). Ecology, 73:143-152. (eds.), Nutritional Ecologyof Insects, Mites, Spiders
Marshall, C., and G. R. Sagar. 1965. The influ- and Related Invertebrates,pp. 105-146. John Wi-
ence of defoliation on the distribution of assimi- ley, New York.

Matzinger, D. F., E. A. Wernsman, and W. W. Barnes, and N. T. Edwards. 1980. Seasonal

Weeks. 1989. Restricted index selection for to- changes in energy allocation by white oak (Quer-
tal alkaloids and yield in tobacco. CropSci., 29: cus alba). Can. J. For. Res., 10:379-388.
74-77. McLaughlin, S. B., R. K. McConathy, and
Mauffette, Y., and W. C. Oechel. 1989. Seasonal B. Beste. 1979. Seasonal changes in within-
variation in leaf chemistry of the coast live oak canopy allocation of "4C-photosynthate by
Quercusagrifolia and implications for the Califor- white oak. For. Sci., 25:361-370.
nia oak moth Phryganidia californica. Oecologia, McNaughton, S. J. 1983. Compensatory plant
79:439-445. growth as a response to herbivory. Oikos, 40:
McClure, J. W. 1979. The physiology of phenolic 329-336.
compounds in plants. Recent Adv. Phytochem., . 1984. Grazing lawns: animals in herds,
12 :525-556. plant form, and coevolution. Am. Nat., 124:
McDermitt, D. K., and R. S. Loomis. 1981. Ele-
863-886.
mental composition of biomass and its relation
McNaughton, S. J., and F. S. Chapin III. 1985.
to energy content, growth efficiency, and growth
Effects of phosphorus nutrition and defoliation
yield. Ann. Bot., 48:275-290.
on C4 graminoids from the Serengeti plains.
McDonald, A. J. S., T. Lohammar, and A. Erics-
son. 1986. Uptake of carbon and nitrogen at Ecology, 66:1617-1629.
McNaughton, S. J., R. W. Ruess, and S. W.
decreased nutrient availability in small birch
(Betula pendula Roth.) plants. Tree Physiol., 2: Seagle. 1988. Large mammals and process dy-
61-71. namics in African ecosystems. BioScience, 38:
McDougal, K. M., and C. R. Parks. 1986. Envi- 794-800.
ronmental and genetic components of flavonoid Meinzer, F. C., C. S. Wisdom, A. Gonzalez-
variation in red oak, Quercusrubra.Biochem. Syst. Coloma, P. W. Rundel, and L. M. Schultz.
Ecol., 14:291-298. 1990. Effects of leaf resin on stomatal behaviour
McGraw,J. B., and F. S. Chapin III. 1989. Com- and gas exchange of Larreatridentata(DC.) Cov.
petitive ability and adaptation to fertile and in- Funct. Ecol., 4:579-584.
fertile soils in two Eriophorum species. Ecology, Mersey, B. G., and A.J. Cuttler. 1986. Differen-
70:736-749. tial distribution of specific indole alkaloids in
McGraw,J. B., K. W. Gottschalk, M. C. Vavrek, leaves of Catharanthusroseus. Can. J. Bot., 64:
and A. L. Chester. 1990. Interactive effects of 1039-1045.
resource availabilities and defoliation on photo- Meyer, G. A., and M. E. Montgomery. 1987.
synthesis. growth, and mortality of red oak Relationships between leaf age and the food
seedlings. Tree Physiol., 7:247-254. quality of cottonwood foliage for the gypsy
McIntyre, G. I. 1987. The role of water in the moth, Lymantria dispar. Oecologia, 72:527-532.
regulation of plant development. Can. J. Bot., Mihaliak, C. A., D. Couvet, and D. E. Lincoln.
65: 1287-1298. 1987. Inhibition of feeding by a generalist in-
McKey, D. 1974. Adaptive patterns in alkaloid sect due to increased volatile leaf terpenes un-
physiology. Am. Nat., 108:305-320. der nitrate-limiting conditions. J. Chem. Ecol.,
1979. The distribution of secondary com- 13: 2059-2067.
pounds within plants. In G. A. Rosenthal and
, and . 1989. Genetic and
D. H. Janzen (eds.), Herbivores. TheirInteraction
environmental contributions to variation in leaf
with SecondaryPlantMetabolites, pp. 56-133. Aca-
mono- and sesquiterpenes of Heterothecasubaxil-
demic Press, New York.
laris. Biochem. Syst. Ecol., 17:529-533.
. 1984. Interaction of the ant-plant Leo-
nardoxaafricana (Caesalpiniaceae) with its obli- Mihaliak, C. A.,J. Gershenzon, and R. Croteau.
gate inhabitants in a rainforest in Cameroon. 1991. Lack of rapid monoterpene turnover in
Biotropica, 16:81-99. rooted plants: implications for theories of plant
McKey, D., P. G. Waterman, C. N. Mbi, J. S. chemical defense. Oecologia, 87:373-376.
Gartlan, and T. T. Struhsaker. 1978. Phenolic Mihaliak, C. A., and D. E. Lincoln. 1985. Growth
content of vegetation in two African rain for- pattern and carbon allocation to volatile leaf
ests: ecological implications. Science, 202:61- terpenes under nitrogen-limiting conditions in
63. Heterotheca subaxillaris (Asteraceae). Oecologia,
McLaughlin, S. B., and R. K. McConathy. 1979. 66:423-426.
Temporal and spatial patterns of carbon alloca- , and . 1989a. Changes in leaf
tion in the canopy of white oak. Can. J. Bot., mono- and sesquiterpene metabolism with ni-
57:1407-1413. trate availability and leaf age in Heterothecasub-
McLaughlin, S. B., R. K. McConathy, R. L. axillaris. J. Chem. Ecol., 15:1579-1588.

, and . 1989b. Plant biomass parti- late concentration in the leaf: a review of the
tioning and chemical defense: response to defo- hypothesis. Bot. Rev., 34:107-125.
liation and nitrate limitation. Oecologia,80:122- Neumann, G., A. El-Aschker, and B. Schwem-
126. mle. 1991. L-phenylalanine ammonia-lyase
Mitchell Aide, T., and E. C. Londoiio. 1989. The and chalcone synthase in seedlings of Oenothera:
effects of rapid leaf expansion on the growth plasmotype dependent regulation and tissue
and survivorship of a lepidopteran herbivore. specific distribution.J. Plant Physiol., 138:263-
Oikos, 55:66-70. 269.
Mole, S., J. A. M. Ross, and P. G. Waterman. Neuvonen, S.,and E. Haukioja. 1984. Low nutri-
1988. Light-induced variation in phenolic lev- tive quality as defence against herbivores: in-
els in foliage of rain-forest plants. I. chemical duced responses in birch. Oecologia, 63:71-74.
changes. J. Chem. Ecol., 14:1-21. Neuvonen, S., E. Haukioja, and A. Molarius.
Mooney, H. A. 1972. The carbon balance of 1987. Delayed inducible resistance against a
plants. Annu. Rev. Ecol. Syst., 3:315-346. leaf-chewing insect in four deciduous tree spe-
Mooney, H. A., and C. Chu. 1974. Seasonal car- cies. Oecologia, 74:363-369.
bon allocation in Heteromelesarbutifolia, a Cali- Nichols-Orians, C. M. 1991. The effect of light on
fornia evergreen shrub. Oecologia, 14:295-306. foliar chemistry, growth and susceptibility of
Mooney, H. A., and E. L. Dunn. 1970. Conver- seedlings of a canopy tree to an attine ant. Oeco-
gent evolution of mediterranean-climate ever- logia, 86:552-560.
green sclerophyll shrubs. Evolution, 24:292- Niemela, P., J. Tuomi, and T. Lojander. 1991.
303. Defoliation of the scots pine and performance
Mooney, H. A., and S. L. Gulmon. 1982. Con- of diprionid sawflies. J. Anim. Ecol., 60:683-
straints on leaf structure and function in refer- 692.
ence to herbivory. BioScience, 32:198-206. Niemela, P. ,J. Tuomi, R. Mannila, and P. Ojala.
Mooney, H. A., S. L. Gulmon, and N. D. John- 1984. The effect of previous damage on the
son. 1983. Physiological constraints on plant quality of Scots pine foliage as food for Diprio-
chemical defenses. In P. A. Hedin (ed.), Plant nid sawflies. Z. Angew. Entomol., 98:33-43.
Resistance to Insects. American Chemical Soci- Nitao, J. K., and A. R. Zangerl. 1987. Floral
ety, Washington D. C. development and chemical defense allocation
Moran, N., and W. D. Hamilton. 1980. Low nu- in wild parsnip (Pastinaca sativa). Ecology, 68:
tritive quality as defense against herbivores. J. 521-529.
Theor. Biol., 86:247-254. Noitsakis, B., and P. Jacquard. 1992. Competi-
Moreland, D. E., and W. P. Novitzky. 1988. In- tion between cyanogenic and acyanogenic
terference by flavone and flavonols with morphs of Trifolium repens. Theor. Appl. Genet.,
chloroplast-mediated electron transport and 83:443-450.
phosphorylation. Phytochemistry,27:3359-3366. Nowacki, E., M. Jurzysta, P. Gorski, D. No-
Morrow, P. A., and V. C. LaMarche. 1978. Tree wacka, and G. R. Waller. 1976. Effect of nitro-
ring evidence for chronic insect suppression of gen nutrition on alkaloid metabolism in plants.
productivity in subalpine Eucalyptus. Science, Biochem. Physiol. Pflanz. (BPP), 169,S:231-240.
201:1244-1246. Nuniez-Farfan, J., and R. Dirzo. 1989. Leaf sur-
Muller, R. N., P. J. Kalisz, and T. W. Kimmerer. vival in relation to herbivory in two tropical
1987. Intraspecific variation in production of pioneer species. Oikos, 54:71-74.
astringent phenolics over a vegetation-resource O'Dowd, D. J., and M. F. Willson. 1989. Leaf
availability gradient. Oecologia, 72:211-215. domatia and mites on Australasian plants: eco-
Muller, R. N., P. J. Kalisz, and J. 0. Luken. logical and evolutionary implications. Biol. J
1989. Fine root production of astringent pheno- Linn. Soc., 37:191-236.
lics. Oecologia, 79:563-565. , and . 1991. Associations between
Muzika, R. M., K. S. Pregitzer, andJ. W. Han- mites and leaf domatia. TrendsEcol. &Evol., 6:
over. 1989. Changes in terpene production fol- 179-182.
lowing nitrogen fertilization of grand fir (Abies Oertli,J.J., S. H. Lips, and M. Agami. 1990. The
grandis (Dougl.) Lindl.) seedlings. Oecologia,80: strength of sclerophyllous cells to resist collapse
485-489. due to negative turgor pressure. Acta eEcol., 1 1:
Myster, R. W., and B. C. McCarthy. 1989. Ef- 281-289.
fects of herbivory and competition on survival Oesterheld, M., and S. J. McNaughton. 1988.
of Carya tomentosa (Juglandaceae) seedlings. Intraspecific variation in the response of Them-
Oikos, 56:145-148. eda triandra to defoliation: the effect of time of
Neales, T. F., and L. D. Incoll. 1968. The control recovery and growth rates on compensatory
of leaf photosynthesis rate by the level of assimi- growth. Oecologia, 77:181-186.

SEPTEMBER 1992 7HE DILEMMA OFPLANTS. TO GROWOR DEFEND 329
, and . 1991. Effect of stress and growth and foliar nutrients of young balsam fir.
time for recovery on the amount of compensa- For. Sci., 26:665-673.
tory growth after grazing. Oecologia, 85:305- Piene, H., and K. E. Percy. 1984. Changes in
313. needle morphology, anatomy, and mineral con-
Oksanen, L. 1990. Predation, herbivory, and tent during the recovery of protected balsam fir
plant strategies along gradients of primary pro- trees initially defoliated by the spruce bud-
ductivity. InJ. B. Grace and D. Tilman (eds.), worm. Can. J. For. Res., 14:238-245.
Perspectiveson Plant Competition.Academic Press, Pimentel, D. 1988. Herbivore population feeding
San Diego. pressure on plant hosts: feedback evolution and
Orians, G. H., andD. H. Janzen. 1974. Why are host conservation. Oikos, 53:289-302.
embryos so tasty? Am. Nat., 108:581-592. Pizzi, A., and F. A. Cameron. 1986. Flavonoid tan-
Owen-Smith, N., and S. M. Cooper. 1987. Palat- nins -structural wood components for drought-
ability of woody plants to browsing ruminants resistance mechanisms of plants. Wood Sci.
in a South African Savanna. Ecology, 68:319- Technol., 20:119-124.
331. Podstolski, A., J. Sznajder, and G. Wichowska.
Paige, K. N., and T. G. Whitham. 1987. Over- 1981. Accumulation of phenolics and growth
compensation in response to mammalian her- rate of barley seedlings (Hordeum vulgare L.).
bivory: the advantage of being eaten. Am. Nat., Biol. Plant. (Prague), 23:120-127.
129: 407-416. Pollard, A. J., and D. Briggs. 1984. Genecological
Palo, R. T. 1984. Distribution of birch (Betula studies of Urtica dioica L. III. Stinging hairs and
spp.), willow (Salix spp.), and poplar (Populus plant-herbivore interactions. New Phytol., 97:
spp.) secondary metabolites and their potential 507-522.
role as chemical defense against herbivores. J Pollock, C. J. 1990. The response of plants to tem-
Chem. Ecol., 10:499-520. perature change. J. Agric. Sci., Cambr., 115: 1-5.
Pasteels, J. M., M. Rowell-Rahier, and M. J. Poorter, H. 1990. Interspecific variation in rela-
Raupp. 1988. Plant-derived defense in Chryso- tive growth rate: on ecological causes and phys-
melid beetles. In P. Barbosa and D. Letour- iological consequences. In H. Lambers, M. L.
neau (eds.), Novel Aspects of Insect-Plant Interac- Cambridge, H. Konings, and T. L. Pons
tions, pp. 235-272. John Wiley, New York. (eds.), Causes and Consequencesof Variation in
Patrick, J. W. 1988. Assimilate partitioning in re- GrowthRate and Productivityof Higher Plants, pp.
lation to crop productivity. HortScience, 23:33- 45-68. SPB Academic Publishing, The Hague.
40. Poorter, H., and C. Remkes. 1990. Leaf area ratio
Paulissen, M. A. 1987. Exploitation by, and the and net assimilation rate of 24 wild species dif-
effects of, caterpillar grazers on the annual, fering in relative growth rate. Oecologia,83:553-
Rudbeckia hirta (Compositae). Am. Midl. Nat., 559.
117:439-441. Poorter, H., C. Remkes, and H. Lambers. 1990.
Pearcy, R. W., 0. Bjorkman, M. M. Caldwell, Carbon and nitrogen economy of 24 wild spe-
J. E. Keeley, R. K. Monson, and B. R. Strain. cies differing in relative growth rate. Plant Phys-
1987. Carbon gain by plants in natural envi- iol., 94:621-627.
ronments. BioScience, 37:21-29. Porter, A. J. R., A. M. Morton, G. Kiddle, K. J.
Pearson, D. L. 1989. What is the adaptive signifi- Doughty, and R. M. Wallsgrove. 1991. Varia-
cance of multicomponent defensive reper- tion in the glucosinolate content of oilseed rape
toires? Oikos, 54:251-253. (Brassica napus L.) leaves. I. Effect of leaf age
Peet, R. K., and N. L. Christensen. 1987. Compe- and position. Ann. Appl. Biol., 118:461-467.
tition and tree death. BioScience, 37:586-595. Potter, D. A., and T. W. Kimmerer. 1986. Sea-
Peters, N. K.,J. W. Frost, and S. R. Long. 1986. sonal allocation of defense investment in Ilex
A plant flavone, luteolin, induces expression opaca Aiton and constraints on a specialist leaf-
of Rhizobium meliloti nodulation genes. Science, miner. Oecologia, 69:217-224.
233:977-980. Potter, J. W., and J. W. Jones. 1977. Leaf area
Peterson, S. C., N. D.Johnson, andJ. L. LeGuy- partitioning as an important factor in growth.
ader. 1987. Defensive regurgitation of allelo- Plant Physiol., 59:10-14.
chemicals derived from host cyanogenesis by Poulton, J. E. 1990. Cyanogenesis in plants. Plant
eastern tent caterpillar. Ecology, 68:1268-1272. Physiol., 94:40 1-405.
Phillips, R., and G. G. Henshaw. 1977. The regu- Premachandra, G. S., H. Saneoka, M. Kanaya,
lation of synthesis of phenolics in stationary and S. Ogata. 1991. Cell membrane stability
phase cell cultures of Acer pseudoplatanus L. J. and leaf surface wax content as affected by in-
Exp. Bot., 28:785-794. creasing water deficits in maize. J. Exp. Bot.,
Piene, H. 1980. Effects of insect defoliation on 42: 167-171.

Price, P. W. 1991. The plant vigor hypothesis and the effect of Battus philenor on Aristolochia reticu-
herbivore attack. Oikos, 62:244-251. lata. Ecology, 61:905-917.
Price, P. W., C. E. Bouton, P. Gross, B. A. Mc- Rausher, M. D., and E. L. Simms. 1989. The
Pheron, J. N. Thompson, and A. E. Weis. evolution of resistance to herbivory in Ipomoea
1980. Interactions among three trophic levels: purpurea. I. Attempts to detect stabilizing selec-
influence of plants on interactions between in- tion. Evolution, 43:563-572.
sect herbivores and natural enemies. Annu. Rev. Reader, R. J. 1990. Competition constrained by
Ecol. Syst., 11:41-65. low nutrient supply: an example involving Hier-
Price, P. W., G. L. Waring, R. Julkunen-Tiitto, aciumfioribundumWimm and Grab. (Composi-
J. Tahvanainen, H. A. Mooney, and T. P. tae). Funct. Ecol., 4:573-577.
Craig. 1989. Carbon-nutrient balance hypoth- Reader, R. J., and B. J. Best. 1989. Variation in
esis in within-species phytochemical variation competition along an environmental gradient:
of Salixlasiolepis. J Chem. Ecol., 15:1117-1131. Hieraciumfloribundumin an abandoned pasture.
Prins, A. H., and H. W. Nell. 1990a. Positive and J. Ecol., 77:673-684.
negative effects of herbivory on the population Reekie, E. G., and F. A. Bazzaz. 1987a. Repro-
dynamics of Seneciojacobaea L. and Cynoglossum ductive effort in plants. 1. Carbon allocation to
officinale L. Oecologia, 83:325-332. reproduction. Am. Nat., 129:876-896.
and .1990b. The impact of herbiv- , and . 1987b. Reproductive effort
ory on plant numbers in all life stages of Cyno- in plants. 2. Does carbon reflect the allocation
glossum officinale L. and Seneciojacobaea L. Acta. of other resources. Am. Nat., 129:897-906.
Bot. Neerl., 39:275-284. Rego, T. J., N. J. Grundon, C. J. Asher, and
Prins, A. H., H. J. Verkaar, and M. van den D. G. Edwards. 1986. Effects of water stress on
Herik. 1989. Responses of Cynoglossumofficinale nitrogen nutrition of grain sorghum. Aust. J.
L. and Seneciojacobaea L. to various degrees of Plant Physiol., 13:499-508.
defoliation. New Phytol., 111:725-731. Rehr, S. S., P. P. Feeny, and D. H.Janzen. 1973.
Puttick, G. M. 1986. Utilization of evergreen and Chemical defence in Central American non-
deciduous oaks by the Californian oak moth ant-acacias. J. Anim. Ecol., 42:405-416.
Phryganidia californica. Oecologia, 68:589-594. Reichardt, P. B., J. P. Bryant, B. J. Anderson,
Rabe, E. 1990. Stress physiology: the functional D. Phillips, T. P. Clausen, M. Meyer, and
significance of the accumulation of nitrogen- K. Frisby. 1990. Germacrone defends Labra-
containing compounds. J. Hortic. Sci., 65:23 1- dor tea from browsing by snowshoe hares. J.
243. Chem. Ecol., 16:1961-1970.
Ramachandra Reddy, A., and V. S. Rama Das.
Reichardt, P. B.,J. P. Bryant, T. P. Clausen, and
1988. Enhanced rubber accumulation and rub-
G. D. Weiland. 1984. Defense of winter-dor-
ber transferase activity in guayule under water
mant Alaska paper birch against snowshoe
stress. J. Plant Physiol., 133:152-155.
hares. Oecologia, 65:58-59.
Ramp, P. F., and S. N. Stephenson. 1988. Gender
Reichardt, P. B., F. S. Chapin III, J. P. Bryant,
dimorphism in growth and mass partitioning
B. R. Mattes, and T. P. Clausen. 1991. Car-
by box-elder (Acer negundoL.). Am. Midl. Nat.,
bon/nutrient balance as a predictor of plant de-
119:420-430.
fense in Alaskan balsam poplar: potential im-
Rao, K. S. 1988. Fine structural details of tannin
accumulations in non-dividing cambial cells. portance of metabolite turnover. Oecologia, 88:
Ann. Bot., 62:575-581. 401-406.
Raupp, M. J., and R. F. Denno. 1983. Leaf age Reznick, D. 1985. Costs of reproduction: an eval-
as a predictor of herbivore distribution and uation of the empirical evidence. Oikos, 44:257-
abundance. In R. F. Denno and M. S. Mc- 267.
Clure (eds.), VariablePlants and Herbivoresin Nat- Reznick, D. N., E. Perry, andJ. Travis. 1986.
ural and Managed Systems, pp. 91-124. Academic Measuring the cost of reproduction: a comment
Press, New York. on papers by Bell. Evolution, 40:1338-1344.
Raupp, M. J., F. R. Milan, P. Barbosa, and Rhizopoulou, S., and S. Diamantoglou. 1991.
B. A. Leonhardt. 1986. Methylcyclopentanoid Water stress-induced diurnal variations in leaf
monoterpenes mediate interactions among in- water relations, stomatal conductance, soluble
sect herbivores. Science, 232:1408-1410. sugars, lipids and essential oil content of Origa-
Raupp, M. J., and C. S. Sadof. 1989. Behavioral num majorana L. J. Hortic. Sci., 66:119-125.
responses of a leaf beetle to injury-related changes Rhoades, D. F. 1977. Integrated antiherbivore,
in its salicaceous host. Oecologia, 80:154-157. antidesiccant, and ultraviolet screening proper-
Rausher, M. D., and P. Feeny. 1980. Herbivory, ties of creosotebush resin. Biochem. Syst. Ecol.,
plant density, and plant reproductive success: 5:281-290.

. 1979. Evolution of plant chemical defense and Somatic Cell Geneticsof Plants, Vol. 4: Cell
against herbivores. In G. A. Rosenthal and Culture in Phytochemistry, pp. 97-114. Aca-
D. H. Janzen (eds.), Herbivores:TheirInteraction demic Press, San Diego.
with SecondaryPlant Metabolites, pp. 3-54. Aca- Sanlaville, C., M.Jay, andJ. Guiard. 1988. Phe-
demic Press, Orlando. nolic variation in the progeny of the cultivated
1985. Offensive-defensive interactions sunflower. Biochem. Syst. Ecol., 16:269-272.
between herbivores and plants: their relevance Schlichting, C. D. 1986. The evolution of pheno-
in herbivore population dynamics and ecologi- typic plasticity in plants. Annu. Rev. Ecol. Syst.,
cal theory. Am. Nat., 125:205-238. 17:667-693.
Rhoades, D. F., and R. G. Cates. 1976. Toward . 1989. Phenotypic integration and envi-
a general theory of plant antiherbivore chemis- ronmental change. BioScience, 39:460-464.
try. Recent Adv. Phytochem., 10: 168-2 13. Schlichting, C. D., and D. A. Levin. 1986. Pheno-
Rhodes, M. J. C. 1985. The physiological signifi- typic plasticity: an evolving plant character.
cance of plant phenolic compounds. In C. F. Biol. J. Linn. Soc., 29:37-47.
Van Sumere and P. J. Lea (eds.), Annual Pro- Schmid, B., S. L. Miao, and F. A. Bazzaz. 1990.
ceedingsof the PhytochemicalSoczetyof Europe, Vol. Effects of simulated root herbivory and fertil-
25: The Biochemistry of Plant Phenolics, pp. izer application on growth and biomass alloca-
99-117. Clarendon Press, Oxford. tion in the clonal perennial Solidago canadensis.
Risch, S. J., and F. R. Rickson. 1981. Mutualism Oecologia, 84:9-15.
in which ants must be present before plants Schoener, T. W. 1988. Leaf damage in island but-
produce food bodies. Nature, 291:149-150. tonwood, Conocarpuserectus: correlations with
Robinson, D. 1986. Compensatory changes in the pubescence, island area, isolation and the dis-
partitioning of dry matter in relation to nitro- tribution of major carnivores. Oikos, 53:253-
gen uptake and optimal variations in growth. 266.
Ann. Bot., 58:841-848. Schultz, J. C. 1983a. Impact of variable plant de-
Robinson, T. 1974. Metabolism and function of fensive chemistry on susceptibility of insects to
alkaloids in plants. Science, 184:430-435. natural enemies. In P. A. Hedin (ed.), Plant
Rockwood, L. L. 1973. The effect of defoliation on Resistanceto Insects, pp. 37-54. American Chem-
seed production of six Costa Rican tree species. ical Society, Washington D. C.
Ecology, 54:1363-1369. . 1983b. Habitat selection and foraging tac-
Room, P. M., M. H. Julien, and I. W. Forno. tics of caterpillars in heterogeneous trees. In
1989. Vigorous plants suffer most from herbi- R. F. Denno and M. S. McClure (eds.), Vari-
vores: latitude, nitrogen and biological control able Plants and Herbivoresin Natural and Managed
of the weed Salvinia molesta. Oikos, 54:92-100. Systems,pp. 61-90. Academic Press, New York.
Schultz, J. C., and I. T. Baldwin. 1982. Oak leaf
Ross, D. W., and C. W. Berisford. 1990. Nan-
quality declines in response to defoliation by
tucket pine tip moth (Lepidoptera: Tortri-
gypsy moth larvae. Science, 217:149-151.
cidae): response to water and nutrient status of
Scriber,J. M., and M. P. Ayres. 1988. Leaf chem-
loblolly pine. For. Sci., 36:719-733.
istry as a defense against insects. ISI Atlas Sci.
Rousi, M.,J. Haggman, andJ. P. Bryant. 1987.
Anim. Plant Sci., 1:117-123.
The effect of bark phenols upon mountain hare
Seigler, D. S. 1977. Primary roles for secondary
barking of winter-dormant Scots pine. Holarct.
compounds. Biochem. Syst. Ecol., 5:195-199.
Ecol., 10:60-64.
Seigler, D. S., and P. W. Price. 1976. Secondary
Rousi, M., J. Tahvanairnen, and I. Uotila. 1991. compounds in plants: primary functions. Am.
A mechanism of resistance to hare browsing in
Nat., 110:101-105.
winter-dormant European white birch (Betula Selmar, D., R. Lieberei, and B. Biehl. 1988. Mo-
pendula). Am. Nat., 137:64-82. bilization and utilization of cyanogenic glyco-
Roy, J., and J.-M. Bergeron. 1990. Branch- sides. Plant Physiol., 86:711-716.
cutting behavior by the vole (Microtus pennsyl- Shain, L., andJ. B. Miller. 1982. Pinocembrin:
vanicus). A mechanism to decrease toxicity of an antifungal compound secreted by leaf glands
secondary metabolites in conifers. J. Chem. of eastern cottonwood. Phytophathology,72:877-
Ecol., 16:735-741. 880.
Sacchi, C. F., P. W. Price, T. P. Craig, andJ. K. Sheldon, S. P. 1987. The effects of herbivorous
Itami. 1988. Impact of shoot galler attack on snails on submerged macrophyte communities
sexual reproduction in the arroyo willow. Ecol- in Minnesota lakes. Ecology, 68:1920-1931.
ogy, 69:2021-2030. Shipley, B., and P. A. Keddy. 1988. The relation-
Sakuta, M., and A. Komamine. 1987. Cell growth ship between relative growth rate and sensitiv-
and accumulation of secondary metabolites. In ity to nutrient stress in twenty-eight species of
F. Constabel and I. K. Vasil (eds.), Cell Culture emergent macrophytes. J. Ecol., 76:1101-1110.

Sibly, R. M., andJ. P. Grime. 1986. Strategies Solbrig, 0. T. 1981. Studies on the population
of resource capture by plants - evidence for ad- biology of the genus Viola. II. The effect of plant
versity selection. J. Theor. Biol., 118:247-250. size on fitness in Viola sororia. Evolution, 35:
Silkstone, B. E. 1987. The consequence of leaf 1080-1093.
damage for subsequent insect grazing on birch Southwood, T. R. E. 1973. The insect/plant rela-
(Betula spp.): a field experiment. Oecologia, 74: tionship - an evolutionary perspective. In
149-152. H. F. van Emden (ed.), Insect/Plant Relation-
Simms, E. L., and R. F. Fritz. 1990. The ecology ships, pp. 3-30. John Wiley, London.
and evolution of host-plant resistance to insects. 1977. Habitat, the templet for ecological
Trends Ecol. & Evol., 5:356-360. strategies?J. Anim. Ecol., 46:337-365.
Simms, E. L., and M. D. Rausher. 1987. Costs . 1988. Tactics, strategies, and templets.
and benefits of plant resistance to herbivory. Oikos, 52:3-18.
Am. Nat., 130:570-581. Southwood, T. R. E., V. K. Brown, and P. M.
, and . 1989. The evolution of resis- Reader. 1986. Leaf palatability, life expectancy
tance to herbivory in Ipomoeapurpurea.II. Natu- and herbivore damage. Oecologia, 70:544-548.
ral selection by insects and costs of resistance. Sprugel, D. G. 1989. The relationship of ever-
Evolution, 43:573-585. greenness, crown architecture, and leaf size.
Simpson, S. J., and C. L. Simpson. 1990. The Am. Nat., 133:465-479.
mechanisms of nutritional compensation by Stafford, R. A. 1989. Allocation responses of Abu-
phytophagous insects. In E. A. Bernays (ed.), tilon theophrastito carbon and nutrient stress.
Insect-Plant Interactions, Vol. II. CRC Press. Am. Midl. Nat., 121:225-231.
Boca Raton. Stearns, S. C. 1976. Life-history tactics: a review
Sinclair, T. R., and C. T. de Wit. 1975. Photosyn- of ideas. Q Rev. Biol., 51:3-47.
thate and nitrogen requirements for seed pro- . 1980. A new view of life-history evolution.
duction by various crops. Science, 189:565-567. Oikos, 35:266-281.
Singh, N., R. Luthra, and R. S. Sangwan. 1991. -. 1989a. Trade-offs in life-history evolu-
Mobilization of starch and e. iential oil biogene- tion. Funct. Ecol., 3:259-268.
sis during leaf ontogeny of lemongrass (Cymbo- . 1989b. The evolutionary significance of
pogon flexuosus Stapf.). Plant Cell Physiol., 32: phenotypic plasticity. BioScience, 39:436-445.
803-811. Stephenson, A. G. 1980. Fruit set, herbivory, fruit
Slansky, F., Jr. In press. Allelochemical/nutrient reduction, and the fruiting strategy of Catalpa
interactions in herbivore nutritional ecology. speciosa (Bignoniaceae). Ecology, 61:57-64.
In G. A. Rosenthal and M. R. Berenbaum Strain, B. R. 1985. Physiological and ecological
controls on carbon sequestering in terrestrial
(eds.), Herbivores. Their Interactionwith Secondary
ecosystems. Biogeochemistry,1:219-232.
Plant Metabolites, Vol. II. 2nd ed. Academic
Strauss, S. Y. 1991. Direct, indirect, and cumula-
Press, New York.
tive effects of three native herbivores on a
Slansky, F.,Jr., and P. Feeny. 1977. Stabilization
shared host plant. Ecology, 72:543-558.
of the rate of nitrogen accumulation by larvae
Stuhlfauth, T., K. Klug, and H. P. Fock. 1987.
of the cabbage butterfly on wild and cultivated
The production of secondary metabolites by
food plants. Ecol. Monogr., 47:209-228.
Digitalis lanata during CO2 enrichment and wa-
Slansky, F., Jr., andJ. M. Scriber. 1985. Food
ter stress. Phytochemistry,26:2735-2739.
consumption and utilization. In G. A. Kerkut Swain, T. 1977. Secondary compounds as protec-
and L. I. Gilbert (eds.), ComprehensiveInsect tive agents. Annu. Rev. Plant Physiol., 28:479-
Physiology, Biochemistry, and Pharmacology, pp. 501.
87-163. Pergamon Press, Oxford. Szaniawski, R. K. 1987. Plant, stress and homeo-
Smith, L. L.,J. Lanza, and G. C. Smith. 1990. stasis. Plant Physiol. Biochem., 25:63-71.
Amino acid concentrations in extrafloral nectar Tallamy, D. W. 1985. Squash beetle feeding be-
of Impatiens sultani increase after simulated her- havior: an adaptation against induced cucurbit
bivory. Ecology, 71:107-115. defenses. Ecology, 66:1574-1579.
Smith, T., and M. Huston. 1989. A theory of the Tallamy, D. W., and V. A. Krischik. 1989. Varia-
spatial and temporal dynamics of plant commu- tion and function of cucurbitacins in Cucurbita:
nities. Vegetatio,83:49-69. an examination of current hypotheses. Am.
Smith-Gill, S. J. 1983. Developmental plasticity: Nat., 133:766-786.
developmental conversion versus phenotypic Taylor, D. R., L. W. Aarssen, and C. Loehle.
modulation. Am. Zool., 23:47-55. 1990. On the relationship between r/K selec-
Snow, A. A., and D. F. Whigham. 1989. Costs of tion and environmental carrying capacity: a
flower and fruit production in Tipularia discolor new habitat templet for plant life history strate-
(Orchidaceae). Ecology, 70:1286-1293. gies. Oikos, 58:239-250.

SEPTEMBER 1992 THE DILEMMA OFPLANTS. TO GROW OR DEFEND 333
Taylor, G. J. 1989. Maximum potential growth and S. Neuvonen. 1984. Nutrient stress: an
rate and allocation of respiratory energy as re- explanation for plant anti-herbivore responses
lated to stress tolerance in plants. Plant Physiol. to defoliation. Oecologia, 61:208-210.
Biochem., 27:605-611. Tuomi,J., P. Niemela, M. Rousi, S. Siren, and
Taylor, M. F. J. 1989. Compensation for variable T. Vuorisalo. 1988. Induced accumulation of
dietary nitrogen by larvae of the salvinia moth. foliage phenols in mountain birch: branch re-
Funct. Ecol., 3:407-416. sponse to defoliation? Am. Nat., 132:602-608.
Thompson, K., and A. J. A. Stewart. 1981. The Tuomi, J., P. Niemela, and S. Siren. 1990. The
measurement and meaning of reproductive ef- Panglossian paradigm and delayed inducible
fort in plants. Am. Nat., 117:205-21 1. accumulation of foliar phenolics in mountain
Threlfall, D. R., and I. M. Whitehead. 1988. birch. Oikos, 59:399-410.
Co-ordinated inhibition of squalene synthetase Turlings, T. C. J., J. H. Tumlinson, and W. J.
and induction of enzymes of sesquiterpenoid Lewis. 1990. Exploitation of herbivore-
phytoalexin biosynthesis in cultures of Nicotiana induced plant odors by host-seeking parasitic
tabacum. Phytochemistry,27:2567-2580. wasps. Science, 250:1251-1253.
Tilman, D. 1978. Cherries, ants and tent caterpil- Turner, N. C., and G. H. Heichel. 1977. Stomatal
lars: timing of nectar production in relation to development and seasonal changes in diffusive
susceptibility of caterpillars to ant predation. resistance of primary and regrowth foliage of
Ecology, 59:686-692. red oak (Quercus rubra L.) and red maple (Acer
. 1985. The resource-ratio hypothesis of rubrumL.). New Phytol., 78:71-81.
plant succession. Am. Nat., 125:827-852. van Andel, J., and F. Vera. 1977. Reproductive
. 1986. Resources, competition, and the allocation in Senecio sylvaticus and Chamaenerion
dynamics of plant communities. In M. J. angustifoliumin relation to mineral nutrition. J.
Crawley (ed.), Plant Ecology. Blackwell Scien- Ecol., 65:747-758.
tific, Oxford. van der Meijden, E., M. Wijn, and H. J. Verkaar.
.1988. Plant Strategiesand the Dynamics and 1988. Defence and regrowth, alternative plant
Structureof Plant Communities.Princeton Univer- strategies in the' struggle against herbivores.
sity Press, Princeton. Oikos, 51:355-363.
. 1989. Competition, nutrient reduction Van Horne, B., T. A. Hanley, R. G. Cates, J. D.
and the competitive neighborhood of a bunch- McKendrick, and J. D. Horner. 1988. Influ-
grass. Funct. Ecol., 3:215-219. ence of seral stage and season on leaf chemistry
. 1990. Constraints and tradeoffs: toward a of southeastern Alaska deer forage. Can. J. For.
Res., 18:90-99.
predictive theory of competition and succes-
van Noordwijk, A. J. 1989. Reaction norms in
sion. Oikos, 58:3-15.
genetical ecology. BioScience, 39:453-458.
Tilman, D., and M. L. Cowan. 1989. Growth of
van Noordwijk, A. J., and G. deJong. 1986. Ac-
old field herbs on a nitrogen gradient. Funct.
quisition and allocation of resources: their in-
Ecol., 3:425-438.
fluence on variation in life history tactics. Am.
Torssell, K. B. G. 1983. Natural Product Chemistry.
Nat., 128:137-142.
A MechanisticandBiosyntheticApproachto Secondary
Verkaar, H. J., E. van der Meijden, and L. Bree-
Metabolism. Wiley, Chichester.
baart. 1986. The responses of Cynoglossumoffici-
Tuomi, J., and T. Vuorisalo. 1989a. Hierarchical
nale L. and VerbascumthapsusL. to defoliation in
selection in modular organisms. TrendsEcol. & relation to nitrogen supply. New Phytol., 104:
Evol., 4:209-213. 121-129.
, and . 1989b. What are the units of Via, S., and R. Lande. 1985. Genotype-environ-
selection in modular organisms? Oikos, 54:227- ment interaction and the evolution of pheno-
233. typic plasticity. Evolution, 39:505-522.
Tuomi, J., T. Hakala, and E. Haukioja. 1983. Viets, F. G.,Jr. 1972. Water deficits and nutrient
Alternative concepts of reproductive effort, availability. In T. T. Kozlowski (ed.), Water
costs of reproduction, and selection in life- Deficits and Plant Growth, Vol. III: Plant Re-
history evolution. Am. Zool., 23:25-34. sponses and Control of Water Balance, pp.
Tuomi, J., P. Niemela, F. S. Chapin III, J. P. 217-239. Academic Press, New York.
Bryant, and S. Siren. 1988. Defensive responses Vitousek, P. 1982. Nutrient cycling and nutrient
of trees in relation to their carbon/nutrient bal- use efficiency. Am. Nat., 119:553-572.
ance. In W. j. Mattson, J. Levieux, and C. Ber- Vogelmann, A. F.,J. C. Turner, and P. G. Mahl-
nard-Dagan (eds.), Mechanisms of Woody Plant berg. 1987. Cannabinoid occurrence in seed-
DefensesAgainst Insects: Searchfor Pattern,pp. 57- lings of Cannabissativa L.: quantitation in seed-
72. Springer-Verlag, New York. lings of known age and primary leaf length. Bot.
Tuomi, J., P. Niemela, E. Haukioja, S. Siren, Gaz., 148:468-474.

Wagner, G. J. 1991. Secreting glandular tribution in plants. Ann. Rev. Ecol. Syst., 15:233-
chomes: more than just hairs. Plant Physiol. , 96: 258.
675-679. Welden, C. W., and W. L. Slauson. 1986. The
Wagner, M. R. 1988. Induced defenses in pon- intensity of competition versus its importance:
derosa pine against defoliating insects. In an overlooked distinction and some implica-
W. J. Mattson, J. Levieux, and C. Bernard- tions. Q. Rev. Biol., 61:23-44.
Dagan (eds.), Mechanismsof WoodyPlant Defenses Welker, J. M., D. D. Briske, and R. W. Weaver.
Against Insects: Searchfor Pattern, pp. 14 1-155. 1987. Nitrogen-i5 partitioning within a three
Springer-Verlag, New York. generation tiller sequence of the bunchgrass
Wallace, C. S., and P. W. Rundel. 1979. Sexual Schizachyriumscoparium:response to selective de-
dimorphism and resource allocation in male foliation. Oecologia, 74:330-334.
Welker,J. M., E.J. Rykiel,Jr., D. D. Briske, and
and female shrubs of Simmondsiachinensis. Oeco-
J. D. Goeschl. 1985. Carbon import among
logia, 44:34-39.
vegetative tillers within two bunchgrasses: as-
Wallner, W. E., and G. S. Walton. 1979. Host
sessment with carbon- 11 labelling. Oecologia,
defoliation: a possible determinant of gypsy
67:209-212.
moth population quality. Ann. Entomol. Soc.
Welter, S. C. 1989. Arthropod impact on plant gas
Am., 72:62-67. exchange. In E. A. Bernays (ed.), Insect-Plant
Wardlaw, I. F. 1990. The control of carbon parti- Interactions, Vol. 1, pp. 135-150. CRC Press,
tioning in plants. New Phytol., 116:341-381. Boca Raton.
Wareing, P. F., M. M. Khalifa, and K. J. Treh- Werner, P. A. 1975. Predictions of fate from ro-
arne. 1968. Rate-limiting processes in photo- sette size in teasel (Dipsacusfullonum L.). Oeco-
synthesis at saturating light intensities. Nature, logia, 20:197-201.
220:453-457. Werner, R. A. 1979. Influence of host foliage on
Wareing, P. F., andJ. Patrick. 1975. Source-sink development, survival, fecundity, and oviposi-
relations and the partition of assimilates in the tion of the spear-marked black moth, Rheumapt-
plant. In J. P. Cooper (ed.), Photosynthesisand era hastata (Lepidoptera: Geometridae). Can.
Productivity in Different Environments, pp. 481- Entomol., 111:317-322.
499. Cambridge University Press, Cambridge. West-Eberhard, M. J. 1989. Phenotypic plasticity
Wareing, P. F., and I. D. J. Phillips. 1981. Growth and the origins of diversity. Annu. Rev. Ecol.
and Differentiation in Plants. 3rd ed. Pergamon Syst., 20:249-278.
Press, Oxford. Westoby, M. 1984. The self-thinning rule. Adv.
Wargo, P. M. 1977. Armillariella mellea and Agrilus Ecol. Res., 14:167-225.
. 1989. Selective forces exerted by verte-
bilineatus and mortality of defoliated oak trees.
brateherbivoresonplants. TrendsEcol. &Evol.,
For. Sci., 23:485-492.
4:115-117.
Waring, R. H., A. J. S. McDonald, S. Larsson,
White, J. 1979. The plant as a metapopulation.
T. Ericsson, A. Wiren, E. Arwidsson, A. Erics- Annu. Rev. Ecol. Syst., 10:109-145.
son, and T. Lohammar. 1985. Differences in . 1984. Plant metamerism. In R. Dirzo and
chemical composition of plants grown at con- J. Sarukhan (eds.), Perspectiveson Plant Popula-
stant relative growth rates with stable mineral tion Ecology, pp. 15-47. Sinauer, Sunderland.
nutrition. Oecologia, 66:157-160. White, T. C. R. 1978. The importance ofa relative
Waring, R. H., and G. B. Pitman. 1985. Modi- shortage of food in animal ecology. Oecologia,
fying lodgepole pine stands to change suscepti- 33:71-86.
bility to mountain pine beetle attack. Ecology, . 1984. The abundance of invertebrate her-
66:889-897. bivores in relation to the availability of nitrogen
Waterman, P. G., and S. Mole. 1989. Extrinsic in stressed food plants. Oecologia, 63:90-105.
factors influencing production of secondary Whitham, T. G., and C. N. Slobodchikoff. 1981.
metabolites in plants. In E. A. Bernays (ed.), Evolution by individuals, plant-herbivore in-
Insect-Plant Interactions, Vol. 1, pp. 107-134. teractions, and mosaics of genetic variability:
the adaptive significance of somatic mutations
CRC Press, Boca Raton.
in plants. Oecologia, 49:287-292.
Waterman, P. G., J. A. M. Ross, and D. B.
Whitham, T. G., A. G. Williams, and A. M. Rob-
McKey. 1984. Factors affecting levels of some inson. 1984. The variation principle: individ-
phenolic compounds, digestibility, and nitro- ual plants as temporal and spatial mosaics of
gen content of the mature leaves of Barteriafistu- resistance to rapidly evolving pests. In P. W.
losa (Passifloraceae). J. Chem. Ecol., 10:387- Price, C. N. Slobodchikoff, and W. S. Gaud
401. (eds.), A New Ecology. A Novel Approachto Inter-
Watson, M. A., and B. B. Casper. 1984. Morpho- active Systems, pp. 15-51. John Wiley, New
genetic constraints on patterns of carbon distri- York.

SEPTEMBER 1992 THE DILEMMA OF PLANTS: TO GROWOR DEFEND 335
Whitman, D. W., and F. J. Eller. 1990. Parasitic nosa against a specialist herbivore. J. Chem.
wasps orient to green leaf volatiles. Chemoecol- Ecol., 11:1553-1565.
ogy, 1:69-75. Wisdom, C. S., C. S. Crawford, and E. F. Aldon.
Whittaker, R. H., and P. P. Feeny. 1971. Allelo- 1989. Influence of insect herbivory on photo-
chemics: chemical interactions between spe- synthetic area and reproduction in Gutierrezia
cies. Science, 171:757-770. species.J. Ecol., 77:685-692.
Wiermann, R. 1981. Secondary plant products Wong, M., S. J. Wright, S. P. Hubbell, and
and cell and tissue differentiation. In E. E. R. B. Foster. 1990. The spatial pattern and
Conn (ed.), The Biochemistryof Plants, Vol. 7: reproductive consequences of outbreak defolia-
Secondary Plant Products, pp. 85-116. Aca- tion in Quararibeaasterolepis, a tropical tree. J.
demic Press, New York. Ecol., 78:579-588.
Williams, D. H., M. J. Stone, P. R. Hauck, and Woodhead, S. 1981. Environmental and biotic
S. K. Rahman. 1989. Why are secondary me- factors affecting the phenolic content of differ-
tabolites (natural products) biosynthesized? J. ent cultivars of Sorghum bicolor.J. Chem. Ecol.,
Nat. Prod. (Lloydia), 52:1189-1208. 7:1035-1047.
Williams, K. S., D. E. Lincoln, and P. R. Ehrlich. Wratten, S. D., P. J. Edwards, and I. Dunn. 1984.
1983. The coevolution of Euphydryaschalcedona Wound-induced changes in the palatability of
butterflies and their larval host plants. I. Larval Betula pubescens and B. pendula. Oecologia, 61:
feeding behavior and host plant chemistry. 372-375.
Oecologia, 56:323-329. Wratten, S. D., P. J. Edwards, and L. Winder.
Williams, K., F. Percival, J. Merino, and H. A. 1988. Insect herbivory in relation to dynamic
Mooney. 1987. Estimation of tissue construc- changes in host plant quality. Biol. J. Linn. Soc.,
tion cost from heat of combustion and organic 35:339-350.
Wright, L. C., A. A. Berryman, and B. E. Wick-
nitrogen content. Plant Cell Environ., 10:725-
man. 1984. Abundance of the fir engraver, Scol-
734.
ytus ventralis, and the Douglas-fir beetle, Den-
Williams, R. B., and K. L. Bell. 1981. Nitrogen
droctonuspseudotsugae,following tree defoliation
allocation in Mojave desert winter annuals.
by the Douglas-fir tussock moth, Orgyiapseudo-
Oecologia, 48:145-150.
tsugata. Can. Entomol., 116:293-305.
Williams, R. D., and B. E. Ellis. 1989. Age and
Wrubel, R. P., and E. A. Bernays. 1990. Effects
tissue distribution of alkaloids in Papaversomnif-
of ingestion of some non-host plant secondary
erum. Phytochemistry,28:2085-2088.
compounds on larvae of Manduca sexta. Entomol.
Willson, M. F. 1991. Foliar shelters for mites in Exp. Appl., 54:125-130.
the eastern deciduous forest. Am. Midl. Nat., Zangerl, A. R., and M. R. Berenbaum. 1987.
126:111-117. Furanocoumarins in wild parsnip: effects of
Wilson, S. D., and P. A. Keddy. 1986a. Species photosynthetically active radiation, ultraviolet
competitive ability and position along a natural light, and nutrients. Ecology, 68:516-520.
stress/disturbance gradient. Ecology, 67:1236- , and . 1990. Furanocoumarin in-
1242. duction in wild parsnip: genetics and popula-
, and . 1986b. Measuring diffuse tional variation. Ecology, 71:1933-1940.
competition along an environmental gradient: Zobel, A. M., and S. A. Brown. 1990a. Dermati-
results from a shoreline plant community. Am. tis-inducing furanocoumarins on leaf surfaces
Nat., 127:862-869. of eight species of Rutaceous and Umbellifer-
Wink, M., and L. Witte. 1985. Quinolizidine al- ous plants. J. Chem. Ecol., 16:693-700.
kaloids as nitrogen source for lupin seedlings , and . 1990b. Seasonal changes of
and cell cultures. Z. Naturforsch., 40c:767-775. furanocoumarin concentrations in leaves of
Wisdom, C. S. 1985. Use of chemical variation Heracleum lanatum. J. Chem. Ecol., 16:1623-
and predation as plant defenses by Enceliafari- 1634.


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VOLUME 67, No.

3 THE QUARTERL Y REVIEW OF BIOLOGY SEPTEMBER 1992

THE DILEMMA OF PLANTS: TO GROW OR DEFEND

INTRODUCTION theory of plant defense has not kept pace. The

The QuarterlyReview of Biology, September 1992, Vol. 67, No. 3

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1985; Bazzaz et al., 1987; Chapin et al., Primary Rolesfor SecondaryMetabolites

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especially strong photosynthetic sinks (Ho, Nonlinear Effects of ResourceAvailability on

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in secondary metabolism. The CNB hypothe- been shown to increase concentrations of

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logical characteristics of growth-dominated TABLE 1

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Resource-RichEnvironmentsFavor Inducible Resistance

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CompetitionIs the Optimizerin Optimal Defense dC/dt = G * C * (11-kD )(H-mD').

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EnvironmentalConstraintModels RGRmax -------

timal defense (Rhoades, 1979) and environ- / / / ~~~Realized

rates close or equal to the maximum potential Two POPULATIONS (A AND B) OF

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The Evolution of Plant Allocation Trajectories: c 0 10C

logical and ecological constraints resulting in eD = G~~enot eni oi Curen Phoooniai

selection from herbivores and competitors.

ary outcome. FIG. 3. CONCEPTUAL MODEL OF THE EFFECTS OF

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. 1989b. The relative importance of verte- Denslow, J. S., J. C. Schultz, P. M. Vitousek,

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Matzinger, D. F., E. A. Wernsman, and W. W. Barnes, and N. T. Edwards. 1980. Seasonal