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The Ecology and Evolution of the New World Non-Pollinating Fig Wasp

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The Ecology and Evolution of the New World Non-Pollinating Fig Wasp Journalof Biogeography (1996) 23, 447-458 The ecologyand evolutionof the New Worldnon-pollinating figwasp communities STUART A. WEST', EDWARD ALLEN HERRE2, DONALD M. WINDSOR2 and PHILIP R. S. GREEN' 'Departmentof Biology,Imperial College at SilwoodPark, Ascot,Berkshire SL5 7PY, U.K and 2SmithsonianTropical Research Institute, Apartado2072, Balboa, Republicof Panama Abstract. We present data on several previously of pollinatorwasps and viable seeds. Some of the species undescribedspecies fromsix genera of New World non- investigatedare parasitoidsof othernon-pollinating species. pollinatingfig wasps. We show that many of thesespecies We examinethe importance of thevarious forms of spatial have a negativeeffect on the reproductivesuccess of both heterogeneityin theparasitism rate that can act to stabilise the pollinatorwasps and the host figs.Our resultssuggest the host-parasitoidinteraction. Finally, we discuss the that the two most abundant genera of non-pollinating factorsunderlying the large variation in theabundance and wasps, the Idarnes and the Critogaster,compete for the diversityof the non-pollinatingwasps both among and same pool of femaleflowers as the pollinatingwasps in the withinfruit crops. Urostigmaand Pharmacosyceafigs, respectively. Wasps from the genusAepocerus induce and develop withinlarge galls, Key words. Ficus, parasitoid, parasites, coevolution, in the Urostigmafigs. By drainingresources from the fruit density dependence, spatial heterogeneity,community thesewasps may have a detrimentaleffect on theproduction structure. success of the pollinatingwasps and also the host figs,by 1. INTRODUCTION reducingthe figs'ability to dispersepollen (West & Herre, The wasp species that are only able to develop withinthe 1994). In contrast,species which merely gall the fruitwall fruitof fig trees are collectivelytermed fig wasps. These or unoccupiedovaries may have less obvious costs to their species include both mutualisticpollinators and parasitic hosts. non-pollinators.While the fig trees are completelydependent In thisstudy we describevarious aspects of the ecology upon the pollinatorsfor the dispersal of pollen between of thenon-pollinating wasps associatedwith two subgenera fruit,the non-pollinators provide no apparentservice. Each of monoeciousNew Worldfigs (Ficus, subgenera Urostigma figspecies usually has a singlespecies specificpollinating and Pharmacosycea).We found threecommon genera of wasp species (Ramirez, 1970; Wiebes, 1979; Herre et al., non-pollinatingwasps associatedwith the Urostigmafigs in 1996b). These pollinatingwasps are all membersof the Panama: IdarnesWalker, Aepocerus Mayr and Physothorax chalcidoid family,Agaonidae, and have relativelysimilar Mayr.The Idarnescan be furthersplit into two very different lifecycles. The non-pollinatingwasps also generallyappear groups which we have referredto as Idarnes and Idarnes to be species-specificto a singlefig species (Gordh, 1975; (incerta)(see section2). The majorityof thespecies that we Ulenberg,1985; van Noort, 1991; Boucek, 1993; Machado, have examinedare undescribed.However, molecular work et al., 1996). However,a singlefig species may have several suggeststhat a distinctspecies of each of the four wasp associated non-pollinatingwasp species (e.g. Compton & groups is found in most of the Urostigmafig species Hawkins,1992). These non-pollinatingwasp speciesbelong (Machado et al., 1996; Table 2). While the differentspecies to severalchalcidoid families and show a largerange of life- withineach of these four groups appear to use the same cycles(Boucek, 1988, 1993). resourcesfor larval development,members of the different Verylittle is knownabout the biologyof any of thenon- groups tend to use differentresources (Table 1). All the pollinatingfig wasps. Basic questionsinclude: what are the Idarnes species develop withinfemale flowers, which they resourcesutilized for larval growthby these wasps, and appear to competefor with the pollinatingwasps (West & does theirpresence have any detrimentalcost to theirhost Herre,1994; section3). The Aepocerusand Idarnes(incerta) fig?These questions are closely linked because the effect wasps developwithin much larger galls whichprotrude into that differentspecies have on the reproductivesuccess of the centreof the fruitand appear to arise fromfemale theirhosts will depend upon theirlarval diet. For example, flowersand possiblythe fruit wall (section2.2). The fourth species which are competitors or parasitoids of the and finalgroup are the Physothorax,which are parasitoids pollinatorswill have a direct effecton the reproductive of the Aepoceruswasps. ( 1996 BlackwellScience Ltd 447 448 StuartA. Westet al. 050 ? ctc Big 0- ~~~~~~~~~~~~~~~~~+ -C -~~~~~~~~~~~~~~~cC O $ ct ~ ~ ~ c-c~ -o -o c~~~~~~ z~~~~c C' ct I, 0 o -~~~~~~~~~~~~~~~~~CdCdd' ~ ~ ~ - ~ 7 0c ;- = = ;! B v=, 3 _ o o o o o > ? o - cd D 0 5ct 3 c*: 4Sa bD ~ ~ ~ ~ ~ ~ 0I ct boEi >d ddC Q0 *d 0 0 0~~~~~~~~~~~~~~~~~b0b H d C-d >00 HSm mm ct ~ ~ ~ ~ ~ lcwl cec t 96,Junlo igorpy 3 4-5 Non-pollinatingfig wasps 449 In the Pharmacosyceafigs that we have studiedthere are 1989;Ware et al., 1993).These foundress wasps subsequently only two common types of non-pollinatingwasps, both die inside the fruit.The proportionof the flowersin each belongingto the genus CritogasterMayr. The two types fruitthat begin to develop is dependentupon the number can easily be distinguishedby the colour of the female's of foundressesthat entered that fruit (Herre, 1989). Fruits body and themorphology of themales (section2). As with thatare not pollinatedare usuallyaborted (e.g. Compton, the Urostigmawasps, a distinctspecies from each of these Ross & Thornton,1994). groupsis generallyfound in each of the Pharmacosyceafig The female flowerswithin the fruitshow continuous species (Machado et al., 1996). Both these types of variationin lengthof styleranging from those with ovaries Critogasterappear to competefor female flowers with the close to the hollow centreof the fruit;that is, close to the pollinatingwasps in a similarway to the Idarnes wasps stigmaticsurfaces (short-styled flowers) to thosewith ovaries (section3.2). close to thewall of thefruit, far from the stigmatic surfaces The firstaim of this paper is to answer fundamental (long-styledflowers). The ovariesof theshort-styled flowers questionsabout thebiology of thesenon-pollinating wasps. are closerto theovipositing foundress wasps. Of theflowers Initiallywe describein detail the naturalhistory of the figs that develop, the long-styledflowers tend, in general,to and wasps studied(section 2). Followingthis, we quantify develop as viable seeds,whereas the seeds developingfrom theeffects that the Idarnes, Critogaster and Aepoceruswasps short-styledflowers tend to be eatenby thewasps' offspring have on viable seed and pollinatorwasp productionand, (Herre, 1989). It should,however, be noted thatvariation therefore,the reproductivesuccess of theirhosts (section in stylelength is gradual and by no means bimodal, and 3). We thenuse theseresults to inferthe larval dietsof the that the characterizationof flowersas 'short' and 'long' wasps (section3). styledis an oversimplificationmade purelyfor convenience Our second aim is to show the ways in which non- (see also Verkerke,1986,1989; Bronstein, 1988a,b; Compton pollinatingfig wasps can be used to examinemore general & Nefdt,1990). biologicalquestions. For example,considerable theoretical Justbefore final ripeningof the fruittakes place, the and empiricalattention has been paid to the factorsthat winglessmales of thepollinating wasps chew theirway out may explainthe persistenceof host-parasitoidinteractions of the flowersin which they have developed. They then (reviewedin Hassell & Godfray,1992; Jones,Hassell & crawl around the interiorof the fruitsearching for flowers May, 1994). Parasitoids such as Physothoraxand their which contain femalewasps. The males chew open these Aepocerushosts may provide useful systems for the empirical flowersand matewith the females. The femalesthen emerge study of potentialstabilizing effects of various formsof fromtheir flowers and gatherpollen, before leaving through parasitoid aggregation at many differentspatial and a hole in the fruitwall chewedby the male wasps. temporalscales. In this studywe examinethe relationship betweenpercentage parasitism and host density,and the 2.2. The non-pollinatingwasps factors that may contributeto the stability of their interaction,using data from the fruitof a single crop Beforeexamining each genus in more detail we will first (section4). As a second example we considerpatterns at establishthe featureswhich are commonto the biologyof the communitylevel. Specifically,we discuss factorsthat all the non-pollinatingwasps thatwe have examinedhere. may influencethe abundance and diversityof the various First,unlike the pollinator females, all thespecies considered typesof non-pollinatingwasps across differentfig species in this study oviposit fromoutside the fruitwall (Table (section5). 1). Other studies have shown that some species of non- pollinatingwasps do enterthe fruitto oviposit(see Galil & Eiskikowitch,1969; Murray, 1989; Compton, 1993b). 2. BACKGROUND BIOLOGY Secondly,all the non-pollinatingwasps emergefrom their flowersat approximatelythe same timeas the pollinators 2.1. The figsand their pollinators and exitthe fruit through the hole chewedby thepollinator We sampled naturallyoccurring fig species in the vicinity males.The non-pollinatorwasps thereforedepend upon the of the Panama Canal. The figspecies are grouped
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