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Oecologia (Berl) (1982) 54:101 107
9 Springer-Veriag 1982
Coevolution of Pierid Butterflies and Their Cruciferous Foodplants
V. Habitat Selection, Community Structure and Speciation
Steven P. Courtney*Department of Zoology, University of Durham, EnglandSummary. Early models of hostplant exploitation by phytopha-gous insects suffer from unwarranted assumptions and may notbe generally applicable. Wordmodels of the co-evolutionary ap-proach may assume unwarranted evolutionary stability in 'stra-tegic' explanations, whilst mathematical models derived fromearlier optimal-diet studies are unrealistic and unwieldy. A simplearithmetic model synthesises these two approaches, using thetwo parameters of foodplant suitability and availability. Host-plant use by the butterfly
Anthocharis cardamines,
previouslythought to be maladaptively polyphagous, is shown to be optimalunder prevailing conditions of short search time. The predictionsof the model for hostplant use and community structure of but-terflies and other phytophagous insects are tested and, in largepart, corroborated. Monophagy and monophagic forms of oligo-phagy are shown to be favoured by: long adult lifespan; lowsearch costs to females; search images (whether visual or olfacto-ry) ; batch-laying of eggs; high differential in foodplant suitabili-ty.
The paradigm of insect-plant coevolution is well-established andused generally to explain the patterns of hostplant use by insects.However, despite the efforts of Levins and MacArthur (1969),Jaenike (1978) and others, the coevolutionary approach seemslittle wedded to the corpus of ecological thought, deriving fromMacArthur, which uses analytical models, particularly in thestudy of diet width (Emlen 1966; Pulliam 1974). The two ap-proaches were developed contemporaneously, particularly byEhrlich and Raven (1965) and MacArthur and Pianka (1966),but have concentrated on different subject matterns; insect/plantcoevolutionary studies have been largely concerned with the me-chanics of allelochemical and other interactions, and the adapta-tions employed by insects to exploit defended resources. In thispaper I analyse foodplant exploitation by the Pierinae butterfly
Anthocharis cardamines
(L.), and derive a model combining ele-ments of both foodplant suitability and of search time. Thismodel belongs to the general family of optimal diet models(Sih 1979) but, unlike most of these, is constructed in termsof individual fitness rather than some (arguably) fitness-relatedquality, such as energy. Thus this optimality based study refutesthe argument of Lewontin (1977) that all such optimisation mod-els make large assumptions concerning relation to fitness. Predic-tions made from the model appear generally supported and pro-
* Present Address:
Department of Zoology, P.O. Box 147, Universityof Liverpool, Englandvide a framework on which to understand the diversity of food-plant exploitation strategies to be observed in butterflies andother phytophagous insects.Wiklund (1974a) characterised two forms of olioligophagyas practised by insects. In one form (the 'polyphagic type')an insect population uses all available hostplants of a narrowrange of species, showing no preference for any one; in theother form (the 'monophagous type'), the insect uses only onehostplant species in any one population, although using manyspecies over its whole geographical range. Examples of the twotypes are respectively the butterflies
Artogeia rapae
(L.) (Takata1961) and
Euphydryas editha
Bois. (White and Singer 1974).Studies on other butterfly species of either type have emphasisedthe importance of the relative suitabilities of different foodplantsfor larval development, and of the availability and predictabilityof foodplants, in determining which strategy is adopted (Wiklund1973, 1975; Chew 1975, 1977a; Wiklund and Ahrberg 1978;Rodman and Chew 1980). In the earlier papers of this series(Chew 1975, 1977a) it was shown that oviposition behaviourof Nearctic Pierinae agreed well with the suitability of hostplantsfor larval survival, females avoiding oviposition on poisonousCruciferae, with the exception of
Thalspi arvense
L., which isa recent introduction and may be behaviourally indistinguishablefrom acceptable hostplants (Rodman and Chew 1980). Howeverit was subsequently shown that one Palaearctic Pierinae member,
A. cardamines,
laid proportionately most eggs on the worst food-plants available to it
(Hesperis matronalis
L. and
Barbarea wdgar-is
R.Br.) - exactly the reverse of the distribution predicted(Courtney 1981). Differences in eggloads upon cruciferous host-plants were shown to be caused by differences in foodplantapparency; those species which successfully kill
A. cardamines
larvae being larger or persisting longer and hence more easilyperceived by females searching for oviposition sites (Courtney1982). The causes underlying greater use of poor foodplantswere thus established, but there remains yet the problem ofdiet width - why are species which kill larvae used at all?
A. car-damines
eggs laid upon the major hostplant
Alliaria petiotata
Bieb. have a chance of surviving to the adult stage some fiveto six times that of eggs laid upon
H. rnatronalis.
A. petio-lata
is an abundant crucifer, with most oviposition sites unex-ploited by
A. cardamines,
the 'polyphagous type' pattern offoodplant use by the butterfly requires explanation. Wiklundand Ahrberg (1978) have suggested that hostplant use by
A. car-damines
reflects unpredictability in foodplant abundance andin mortality associated with different host species. I now examinethis and other hypotheses for populations of
A. cardamines
stud-ied in Northern England. Primary data and details of studysites are given by Courtney (1980, in prep.).0029-8549/82/0054/0101/$01.40
102Four hypotheses are suggested to explain the use of lesssuitable hostplants by
A. cardamines."
Hypothesis l:Females are unable to distinguish differenthostplant species.Hypothesis 2: Insufficient time has elapsed for evolution toproduce discrimination.Hypothesis 3 : The apparent lack of selectivity is a strategyin time and/or space against resource unpredictability.Hypothesis 4: Females are in fact maximizing reproductiveeffort, laying eggs on poor hostplants as a consequence of timeconstraints.
The Evidence
Stanton (1979), in research on chemotactile stimulation and ovi-position of legume-feeding Pieridae, emphasised the need to re-cognise physiological limitations to discrimination by female but-terflies amongst foodplants. Polyphagy is unsurprising if foodplants are indistinguishable from one another. However, in anumber of different crucifer-feeding species, insects have beenshown to distinguish between different glucosinolates, each cru-cifer species typically having a unique profile of these precursorsof the primary defence chemicals, the mustard oils (Nair et al.1973; Hicks 1974; Sehgal and Vjagir 1977; Nielsen 1978). Rod-man and Chew (1980) have argued that Pierinae females arewell able to distinguish between Cruciferae by such glucosinolateprofiles, except for certain cases where different species sharesimilar profiles.
H. matronalis and B. vulgaris
contain quite dif-ferent glucosinolates to
A. petiolata
(Kjaer 1976). AdditionallySalmon (in prep.) shows convincingly that larvae of two Pierinaespecies are well able to distinguish amongst Co. Durham Cruci-ferae by chemosensory means. Thus it seems reasonable to as-sume that discrimination by females does or could exist in
A. car-damines
if selection is favourable. Hypothesis l is not favouredon available evidence.Chew (1977a, b) showed that oviposition on inappropriatehostplants by Nearctic Pierinae was in part explainable by histor-ical factors. She argued that
Thlaspi arvense,
which kills larvaeof North American
Artogeia napi
(L.), and which is an intro-duced species, has not been present in the butterfly's environmentlong enough for avoidance behaviour to evolve. Maynard Smith(1978) has detailed other similar examples of 'evolutionary lag',such as the inappropriate clutch size of some seabirds (Nelson1964). Of the two hostplants species poor for
A. cardamines
larvalsurvival, one
(H. matronalis)
is an introduced species in Britain.The introduction is probably of long standing, and the hostplanthas been known for
A. cardamines
since Newman (1869) re-corded both
H. matronalis
B. vulgaris
amongst the four host-plants most commonly used. One specimen of
A. cardamines
taken in Co. Durham in the year 1855 was found to bear pollenof
H. matronalis
when examined microscopically; thus it seemsthat the butterfly and crucifer have co-existed in the study areafor at least 125 insect generations, arguably long enough foravoidance behavior to evolve ((Jones 1977) has shown how food-plant location behavior of
A. rapae
has changed in populationsderived from common stock in the 19th Century). On the conti-nent of Europe,
H. matronalis
is native and has probably beenin proximity with
A. cardamines
for millenia; in Italy, at least,the plant is regularly used as a host (C.J. Hill, pers. comm.).'Evolutionary lag', Hypothesis 2, does not appear tenable.Several authors have argued that the 'polyphagous type'of oligophagy is practised by Pierinae as a response to the unpre-dictability of larval foodplants and related mortality factors ineither space or time, or in both.
A. rapae
(Takata, 1961),
A. napi
(Chew 1977a) and
A. cardamines
(Wiklund and Ahrberg 1978)are all held to adopt this strategy in order to overcome fluctua-tions in resource availability and suitability. Chew emphasisedthe importance of variation in foodplant species in space; thisdoes not appear to be a satisfactory explanation for
A. carda-mines
in northern England. In 30 populations on a transectspread across some 75 km distance of the northern Pennines,taking in several habitat types,
A. cardamines
was always asso-ciated with the foodplants
A. petiolata
Cardamine pratensis
L. (Table 1). These two foodplants are amongst the best availablefor larval survival (Courtney t981) and are those typically re-garded as the hosts of the butterfly in both Britain and Sweden.Of 48 British correspondents, only one has recorded an
A. carda-mines
population which does not feed on either of these species.
A. cardamines
females which oviposited only on these two cru-civers would not therefore experience substantially less predicta-bility of foodptant species in space. Foodplant unpredictabilityin time is also unlikely to favour polyphagic strategies in British
A. cardamines.
At one major study site, Durham, the numberof available hostplants was counted annually for 1977 to 1980(Table 2). It is seen that although some variance occurs, in thefour years of study,
A. petiolata
dominated the crucifer commun-ity of the riverbank study site. However, in Sweden more dramat-ic variations in crucifer abundance may occur in early succes-sional habitat (C. Wiklund, pers. comm.).Wiklund and Ahrberg (1978) have emphasised that unpredic-tability of some foodplant associated mortality (such as drowningon marsh species) will lead to selection against specialisationon single hostplant species. Present evidence from northern En-gland suggests strongly that most differences in larval mortalityon different hostplants are however predictable. Based on a studyof the survival of 1,798 individuals in the wild, I have arguedthat most differences in mortality reflect differences in the qualityof the Cruciferae themselves as larval food, with mechanicaland chemical defences killing many larvae on
H. matronalis
B. vulgaris
(Courtney 1981). Similarly
B. vulgaris
is seen to bea poor foodplant for
spp. not only in Co. Durham,but also in Sweden (C. Wiklund, pers. comm.) and the U.S.A.(Chew 1977b). In the long term, evolution against the use ofsuch a consistently poor foodplant should have occurred. Fe-males of
A. napi
A. cardamines
avoid ovipositing on
which contains cardenolides, allelochemicals which seemto kill 100% of larvae grazing on the plants of this genus (Chew1977; Wiklund and Ahrberg 1978). Additional problems alsooccur with the hypothesis of Wiklund and Ahrberg, and other'strategic' formulations, not least the difficulty of investigatinglong-term processes. A major objection is that in situations ofat least short term predictability (as at Durham), 'polyphagoustype' oligophagy will not be evolutionarily stable against inva-sion by monophagous strategists. Polymorphism for the differentstrategies would then be expected (since monophagy will alwayslead to higher fitness in predictable conditions); Chew (1977a)has shown that this does not occur in oligophagous Pierinae.The maintenance of a pure 'polyphagous type' strategy by thewhole population may then require group selection scenariosunder this model. One further problem with the use of strategicexplanations is that they explain even results exactly contraryto those predicted, for instance in the study of Rausher (1979),and used
a posteriori
they cease to have any claim to testability.Hypothesis 3 is not corroborated by available evidence. Theremaining hypothesis holds that the behaviour of femlaes, inovipositing on foodplants as they are found, is adaptive whentime in which to locate hosts is limited. This hypothesis suggeststhat polyphagic strategists will always be favoured and hence
Table I. The principal and subsidiary hostplants of
A. cardamines
at 30 study sites in the North of England.Details of study sites are given by Courtney (1980)Locality Hostplants Locality HostplantsPrincipal SubsidiaryPrincipal SubsidiaryChester-Ie-Street ApFinchale ApBrasside CpDurham Sands ApDurham Ap HmShincliffe Hall Ap HmField Station CpCassop Vale CpBear Park CpLangley Moor Ap CpCroxdale ApBrancepeth CpWitton Park Ap HmWitton-le-Wear Ap HmWolsingham A Ca CpWolsingham B ApBy Hm Stanhope ApDarlington ApWinston Ap Ca BvBv Hm Ovington ApBr Bv Cp So Barnard Castle ApBo Bv Egglestone Ap Cp HmAp Middleton ApDent Bank Cp ApColdberry CpCa Bv Wearhead Cp ApBv Cp Hm Alston Ca Cp Hm Co No TaTynehead Ca CpBr Bv Nenthead CpBr Bv Langwathby Cp NoAp By Hm RsCpKey:Ap AUiariapetiolata Ca Cardamine amara No Nasturtium officinaleBo Brassicaoleracea Cp Cardamine pratensis Rs Rorippa sylvestrisBr Brassica apa Co Cochlearia officinalis So Sisymbrium officinaleBv Barbarea vulgaris Hm Hesperis matronalis Ta Thlaspi alpestre103
2. The number of individuals of major cruciferous hostplantspecies at Durham in the years 1977 to 1980. Counts were madeto the nearest 10
(A. petiolata)
or 5 (other species), on patches ofriverbank1977 1978 1979 1980
4,350 10,320 3,100 7,010
Hesperis matronalis
195 230 115 390
Barbarea vulgaris
235 225 75 450"
Brassica rapa
410 185 85 70
Sisymbrium officinale
45 55 80 290 aa On newly fallow agricultural land in 1980predicts a pure population of polyphagic type, unlike Hypothe-sis 3. The major mortality factor in a key-factor analysis ofthe Durham
A. cardamines
population is failure of females tolay all their eggs (Courtney in prep.). In 1977, the year in whichfecundity was highest, only 15% of eggs were successfully laid.In comparison to this shortfall of eggs, foodplant associatedmortality is small, and if the two selection pressures are in oppo-sition, it is readily seen that selection for increased fecunditymight outweigh that for increased specificity of foodplant choice.It is suggested that, at Durham,
A. cardamines
females whichsearch only for the best foodplants will lay less eggs than thosewhich are indiscriminate, and overall fitness of such femaleswill be lower when fecundity differences exceed those of larvalsurvival Put simplistically, females will often do better to layeggs on bad plants, rather than leave those eggs unlaid. I nowdevelop a simple model to show that these conditions hold atDurham. In Swedish populations females may search for 2 hor more without finding hosts (C. Wiklund, pets. comm.) andit is likely that this model is applicable to all
A. cardamines
The Model
The relationship between host specificity and searching time inphytophagous insects has been addressed by Levins and MacAr-thur (1969) and Jaenike (1978). However these models have cer-tain assumptions unsuitable here; that of Levins and MacArthurassumes that insects are unable to distinguish alternative hostsas either 'good' or 'bad', and must use either one or all availablediet items; additionally it assumes that monophagy is ancestral,when in Pierinae the converse is implied. Neither model is easilyapplicable to the case ofA
and a new, simpler modelwas derived, which may prove more generally applicable.Let there be N foodplants, with j strategies of exploitingthem, each successive strategy adding the next most favourablefoodplant to the diet of the herbivore. Let tj be the searchingtime taken to find one plant under each strategy. When allhostplants are equally abundant:tl = 2t2 = 3t3 =
Let T be the total time available to a searching female, ex-pressed in units of tN, that is the number of oviposition sitesto be found in this time under strategy N. The number of eggslaid by each strategist
(E )
is then
where x is the maximum number of eggs to be laid and a isthe proportion of necessary time available.T
and takes values from 0 to 1, any excess over 1 being ignored.Then the fitness of strategy
j (Wj)
is :

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