Generalist Flowers, Biodiversity and Florivory: Implications for Angiosperm Origins

Author(s): Dawn Frame

Source: Taxon, Vol. 52, No. 4 (Nov., 2003), pp. 681-685
Published by: International Association for Plant Taxonomy (IAPT)
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 2003:681-685
TAXON 52 · November Frame* Generalistflowers,biodiversity
and florivory

Generalistflowers,biodiversityand florivory:implicationsforangiosperm
origins
Dawn Frame

UniversityHerbarium,Universityof California,Berkeley,1001 ValleyLife Science Building #2465,Berkeley,

California94720 U.S.A., and Herbarium,Institutede Botanique, 163 rue A. Broussonnet,34090 Montpellier,
France. aurora@isem.univ-montp2.fr

evolutionwith particularemphasis on herbivoryprovides the starting

A briefoverview of arthropod/insect
anditis notedthatangio-
overtime.The term"flower"is defined,
pointfordiscussionofincreasedherbivory
spermflowersare distinguishedby theiredibility.It is observedthatthephenomenonof florivoryis a primary
interaction,
plant-animal is a secondary
as onepossibleoutcomeof theeatingofflowers,
andpollination, phe-
nomenon.An hypothesis
reconciling arethemosteatenof all plantgroupsand the
thefactsthatangiosperms
mostsuccessfulin termof numberof species is proposed. Fromtheperspectiveof a floralmorphologist,I dis-
cuss what a generalistfloweris and how archaic angiospermsare characterizedby thisflowertype.Biodiver-
sityargumentsunderpina discourse on why researchersshould investigategeneralistflowersand florivory.

KEYWORDS: angiosperms,arthropod,edibility,evolution,generalistflower,herbivory,insect,radiation.

E THE FOSSIL RECORD 1994). Here again, it is important

Arthropod-plant areancientassociations
interactions
that doubtlessdate fromaquatic ancestorsof both
groups.Withthegradualdevelopment of plantscapable
of colonizingterrestrial habitats(especiallyvascular
plants)therewere accompanying arthropods, probably
mostlypredatory, livingamongthe shoots(Kukalova-
Peck, 1991). Detritivory of animaland plantremainsis
likelytoo (see Shear& Kukalovai-Peck, 1990).The first
evidenceofsporefeedingdatesfromtheendoftheLate
Silurian(Labandeira,2002), and thereis evidenceof
stemwoundingin LowerDevonianplantsby earlyter-
restrial
arthropods (Scott& al., 1992;Labandeira, 2002).
Leaf herbivory is recordedlater,and makesitsfirst
appearance in the middle Pennsylvanian(Upper
Carboniferous) (Scott & al., 1992; Labandeira,2002).
The comparatively late appearanceof thisformof her-
bivoryrelatesto the relativeindigestibility of leaves
(Martin, 1991), to low leaf nutritionalcontent
(Southwood,1973), and the fact thattherewere not
manyleavesnorleaf-likeappendageshavinglargelami-
na in theLate Devonian;it wasn'tuntiltheCarbonifer-
ous thatthese became common(Scott & al., 1992).
Winged insects,Pterygota,appear firstin the fossil
recordattheEarly(Mississippian)to Late Carboniferous
(Pennsylvanian) boundary(Wootton,1990). The devel-
opmentof flight is presumedto be intimately connected
withassociationof insectsandplants,and is believedto
have been in itsearliestforma sortof parachuting and
glidingdownfromplantstems(Wootton, 1976;Brodsky,
Devonianplantswereof smallstature.
to point out that
LowerDevonian
plantsusuallydid not surpasshalf a meterin height
(Chaloner& MacDonald,1980); bytheUpperDevonian
the treehabithad become establishedand some trees
attainedheightsof about 30 m (Willis & McElwain,
2002). The development offlightin insectsmaybe relat-
becomingtaller.
ed to plantsprogressively
In fact,bytheearliestPennsylvanian, thetwomajor
groupsof flyinginsectsare recordedand had already
beguntheirradiation:Palaeoptera-insectshavingtheir
wings permanentlyoutstretched(except for the
palaeopterous Diaphanopterodea, whichcould foldtheir
wings,a case of convergence), and Neoptera-insects
havingfoldablewings(Wootton,1990). Anothermajor
advancewas thedevelopment of neopterousendoptery-
goty in the Pennsylvanian(Kukalova-Peck, 1991;
Labandeira& Phillips,1996),whereinthewingsdevel-
op beneaththe thoraciccuticle and not externally
(Carpenter, 1977). Endopterygoty in combination with
holometabolous development by meansof pupae allow
theimmature stages(larvae)tobe verydifferentfromthe
adult,to occupydifferent environments, and to feedon
differentfoods and substrates.The Endopterygota (=
Holometabola)makeup about88% of all extantinsects
today.The insectfaunaofthePermianwas probablythe
mostdiversein termsof basal bauplan,notnecessarily
speciesrichness,thanat anyothertimein thehistory of
theclassInsecta(Carpenter, 1977).Certaingroups(espe-
ciallyamongthePalaeoptera),whichhad begunradia-
tionsduringtheUpperCarboniferous, beganto decline

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Frame* Generalistflowers,biodiversity
and florivory
fromtheLowerto Middle Permian,and alongsidethis
insectfauna,in theLowerPermian,"thefoundations of
themodemfaunawerebeinglaid" (Wootton,1990). Of
particular interest was the appearanceof the exoptery-
gote orders Hemipteraand Thysanoptera,and the
endopterygote orderColeoptera.It is likelythatas some
ofthepalaeopterous ordersdeclined,otherinsectgroups
movedintonichestheyleftbehindor nichesthatwere
createdbyclimaticandvegetational changes.Forexam-
ple, changesin thecoal swampflorasfromthe Upper
Carboniferous to Permian(see Stewart& Rothwell,
1993), and finallythe disappearancealtogether of this
environmentand associated vegetationduring the
Permianarelikelyto havehad an influence on theinsect
fauna associatedwith it (see Labandeira& Phillips,
1996). It is worthy ofnotethatthisphenomenon was not
confined to Paleoptera, butotherordersofthePaleozoic
entomofauna also experienced replacement.
SomeofthePermianinsectordersbecameextinct by
theMesozoic,andbytheearlyJurassic, theinsectfauna
is essentially a modern one (Carpenter, 1977).
Hymenoptera and Diptera date back to the Triassic,
althoughtruehymenopteran socialitymusthave origi-
nated in the mid-Cretaceous (Rasnitsyn, 2002);
Lepidoptera maketheirappearanceintheLowerJurassic
(Whalley,1986).
From the available evidenceof the fossilrecord,
thereis a distinctincreaseovertimein theamountand
diversity of insectherbivory (Labandeira,2002). This
trendculminates intheangiosperms as themosteatenof
all plants.Herbivory is generallyregardedin a negative
lightfortheobviousreasonthatit is destructive. Yet,if
we look at plantsthatare much less eaten,such as
conifersand cycads,theyexhibitnowherenearthesuc-
cess, in terms of number and diversity,of the
angiosperms. Farrell(1998) providesevidencethather-
bivorousbeetlesassociatedwithangiosperms areconsid-
erablygreaterin overallnumbersand specificdiversity
thanthose associatedwithgymnosperms. Further,he
mentions thereis also greaterdiversity in themannerof
eating angiospermsas compared to gymnosperms
(Farrell,1998).1willaddthatthisprobably holdstruefor
all otherplantsas well. An argument has been putfor-
ward thatfernsare eaten by arthropods as much as
angiospermsof similar morphologicalcomplexity
(Auerbach& Hendrix,1980); however,it is impossible
to evaluatesuch propositions because thedata on fern
herbivory are inadequate,and it is difficult to equate
morphological complexity of extantfernswiththatof
angiosperms. Whatcan be said is thatin termsof organ-
ization(bauplan)and construction (gestalt)angiosperms
are farmorecomplexand thenumberand diversity of
theirassociatedentomofauna morediverse.Justas extant
ferns(whichsurvivetothepresent daylargelybecauseof
682
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TAXON 52 · November2003: 681-685
theirhighdependenceon vegetativereproduction) are
limitedin termsof species richnessand highertaxa
diversityby theirmorphological organizationand con-
struction,so too are theyconstrainedat thelevelof the
numberand diversityof theirinsectassociations.For
example,fernsporangiaare relatively uniform whereas
angiosperms displaya bewildering diversityof sporo-
phytereproductive structures.
Returningtothesuccessof
the angiosperms, it is evidentthatthe progenitors of
angiosperms had an organizational
plan flexibleenough
to assuretheirfuture In myopinion,two
diversification.
other key factors, "innovations" if you will, of
angiosperms are theenclosureof ovulesin a carpeland
especiallytherapidity ofreproduction(Cronquist,1988).
Angiosperms takeon theorderof a monthor twofrom
pollinationto seed production,as comparedwithgym-
nospermswhichmaytakefromaboutthreemonthsbut
morecommonlyone to two yearsdependinguponthe
group(Cronquist, 1988).
E WHAT IS A FLOWER?
For the purposesof our discussion,I use a very
broadmorphological definitionforflower:a shootbear-
ing fertileand associated sterile appendages (see
Weberling, 1989). Undersucha definition, it is evident
that,forexample,gymnospermous femalestrobiliare
homologousto angiospermous inflorescences and that
gymnosperms bear flowersjust as angiospermsdo.
Again, reallywhat differentiates most angiosperms is
theiredibility
as comparedtootherplantgroups,andthis
extendsto theirflowers.Theyare farmoreedible,and
angiosperm floralmorphology and biologymayevince
veryspecificspatialand temporal relationshipsto insect
visitorswhether theypollinatethefloweror not(Frame
& Durou,2001). Studieshave focusedon pollination,
and almostnothingis knownof florivory (floralher-
bivory),whenin fact,it is the latterthatis the funda-
mentalphenomenon. Pollination,as one possibleout-
comeofflorivory, is thus,a secondary phenomenon.
* CHICKEN OR EGG-WHICH CAME
FIRST?
It is generallyassumedthatangiospermradiation
occurredfirstandin itswakefollowedinsectdiversifica-
tion(Ehrlich& Raven,1964).On theotherhand,as pre-
viouslymentioned, itis evidentthatbytheearlyJurassic
theinsectfaunais essentiallya modemone,hencepre-
datingangiosperms oranything thatwe wouldrecognize
as an angiosperm. Reiterating, it seems likelythatthe
greatsuccessof angiosperms is linkedto thefactthat
TAXON 52 · November2003: 681-685 Frame* Generalistflowers,biodiversity
and florivory

theyare themosteatenof all plants.Possiblywhatdis- products,such as nectar.I would suggestthatthisis a

tinguishes angiosperms is thattheyhavemanagedtoper- veryold phenomenon, and thatspores,prepollenand
fecta systemthatallowsthemto be eaten,butwithspa- pollen,nectar,etc.,werefairlyfreelyavailable;thecon-
tial and temporalcontrolson consumption eitherat the sumptionof megaspores,however,has been restricted.
levelofthetissue,organ,individual, orpopulation. Such Conversely, thereis a longfossilrecordofseedpredation
a system argues for the concomitantradiationof (Labandeira,2002).
angiospermswithinsects.Like the proverbialchicken Ifwe turnourattention to extantarchaicangiosperm
and egg,itwill be difficult to decidewhichcame firstif flowers,it can be statedthattheyare "generalist" flow-
itwasn'tconcomitant; in anycase, therecouldnothave ers, thatis, theyhave an open morphology and allow
been a greatdifference in thetimingas it seemsthatthe entryto a comparatively wide rangeof insectvisitors
synergy of herbivorous interaction may verywell have (thisis notto say thatall generalist flowersare archaic;
led to theradiations (Wootton,1990). It is probablethat manyhighlyderivedfamilies arecharacterized bygener-
whilemanyinsecttaxa radiatedalongsideangiosperms, alist "blossoms",e.g., Compositaeand Umbelliferae).
subsetsof insectgroupsradiatedafterthem.Further, I Based bothon personalobservation and theliterature,
it
suggest that whichever group gave rise to the is clearthattherearealwaysseveralordersofinsectsvis-
angiospermsis likelyto have experiencedthegreatest itingflowers ofarchaicangiosperms (Thien& al.,2000).
herbivory, bothin termsof degreeand type.No detailed It is almostguaranteedthatone will findmembersof
herbivory studiesofMiddleto LateJurassic fossilplants Coleoptera, Diptera,Thysanoptera, andpossiblyLepido-
exist,noris ita simplematter toexploreas fewgoodfos- ptera and/orHymenoptera.The principalpollinator
sil florasare knownfromthisperiod(Labandeira,pers. varies,but even so, it is onlya questionof relatively
comm.).Severalauthors haverelatedtheobservedrisein superficialchanges in morphologicaland biological
insect family diversity(especially holometabolous modesthatdetermine whichoftheaforementioned insect
insects)duringtheMesozoic to associationswithseed ordersrepresent the principalpollinatorsin each case.
plantsin generaland not a particularsubsetof them This probablyholds trueforangiospermancestorsas
(Labandeira& Sepkoski,1993; Jarzembowski & Ross, well. Such a notionis harmoniouswithBemhardt&
1996). One piece of evidencesupporting thisis thatthe Thien's(1987) suggestion thatproto-angiosperm flowers
most archaicmembersof insectordershavinga high were generalistentomophiles, and with Labandeira's
numberof phytophagoustaxa (e.g., Hymenoptera, proposal(1998) that"basal lineagesof modeminsect
Lepidoptera, Phytophaga oftheColeoptera)arebelieved pollinatorsoriginatedduringthe Jurassicprobablyas
to be primitively associatedwithgymnosperms (Farrell, generalistson seed plants".Whatwe observeon a mor-
1998; Labandeira,pers.comm.,butsee Schneider& al., phologicallygeneralist flowernow as a principalpolli-
2002). Thereis no contradiction here.Theveryimportant natoris nota dependableindicator of whichinsectwas
plant-associated groupssuch as Coleoptera,Thysano- theprincipal pollinator a millionor less yearsago. What
ptera,Diptera,Hymenoptera, and Lepidopterabeganto can be said withgreatercertainty, is thattherewere
diversify priorto thedevelopment of angiosperms, and membersof at leasttwo(and probablymore)different
theirdiversification seeminglyacceleratedin the late insectordersvisitingtheseflowersto eat,thatis, they
Mesozoic (withtheexceptionofThysanoptera) at about wereflorivores.
thetimeof appearanceof theangiosperms (see fig.2 in
Labandeira& Sepkowski,1993). If the modeminsect
revolution was sparkedby associationswithseed plants,
it was kindledin angiosperm and achieved * BIODIVERSITY
progenitors
its greatestexpressionin relationship to theirmodem In termsof speciesnumber, thehighest"biodiversi-
forebearers-the angiosperms. ty" is foundamong arthropodsand vascularplants.
Returningto the concept of the edibility of Recentestimates suggestthatthereis on theorderof4-6
angiosperms, andparticularly theirflowers, to theextent millionarthropod species(Novotny& al., 2002), with
thatthefloweris meantto be eaten,whicheveranimal phytophagous insectsmakingup thegreatest partof this
does thisis "legitimate". In fact,changesin floralform number. By no meansa close second,vascularplantsare
as a consequenceofflorivory commonly does notinhib- abouta tenthas numerous (300,000-500,000;Heywood,
itpollination, although visitsofefficient pollinators may 1997), the most speciose group of which being
be decreased(Clements& Long, 1923; Malo & al., angiosperms.
2001), and in rare cases even enhancesit if nectar On theone hand,florivoresarenotconsidered when
becomesexposed(Clements& Long, 1923). It is inter- estimatingnumbers ofphytophagous insects,as anything
estingto notethattheeatingof ovulesis rarebutpollen visitingtheflowerfallsintothedomainof pollination,
is liberallyofferedas wellas epidermal cells and/or their and thereis a generallack of recognition thatthis is

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Frame* Generalistflowers,biodiversity
and florivory TAXON 52 · November2003: 681-685

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