Comparative Community Ecology Studies on Old World Figs and Fig Wasps Carole Kerdelhue, Jean-Pierre Rossi, Jean Yves Rasplus
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Comparative community ecology studies on old world figs and fig wasps Carole Kerdelhue, Jean-Pierre Rossi, Jean Yves Rasplus To cite this version: Carole Kerdelhue, Jean-Pierre Rossi, Jean Yves Rasplus. Comparative community ecology studies on old world figs and fig wasps. Ecology, Ecological Society of America, 2000, 81 (10), pp.2832-2849. 10.1890/0012-9658(2000)081[2832:CCESOO]2.0.CO;2. hal-02696029 HAL Id: hal-02696029 https://hal.inrae.fr/hal-02696029 Submitted on 1 Jun 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Ecology, 81(10), 2000, pp. 2832±2849 q 2000 by the Ecological Society of America COMPARATIVE COMMUNITY ECOLOGY STUDIES ON OLD WORLD FIGS AND FIG WASPS CAROLE KERDELHUE ,1,3 JEAN-PIERRE ROSSI,2 AND JEAN-YVES RASPLUS1,4 1Institut National de la Recherche AgronomiqueÐCentre National de la Recherche Scienti®que, Laboratoire Populations, GeÂneÂtique et Evolution, 91198 Gif-sur-Yvette Cedex, France 2Universite Paris VI, Laboratoire d'Ecologie des Sols Tropicaux, Centre ORSTOM d'Ile de France, 32 avenue Varagnat, 93143 Bondy Cedex, France Abstract. Ficus and their species-speci®c pollinator wasps (Agaonidae) form a re- markable plant±insect obligate mutualism. Each monoecious ®g species also shelters a community of nonpollinating chalcids, composed of both gallmakers and parasitoids. The few previous studies that took these species into account aimed at determining their potential effect on the mutualism. To go further, we argue that the ®g wasps represent an interesting model for studies of community ecology. Figs and ®g wasps of different groups were studied in CoÃte d'Ivoire to quantify local ecological interactions. Regardless of their ®g host or taxonomical position, we identi®ed three ecological groups of nonpollinating ®g wasps on the basis of their timing of oviposition in the ®g and on their oviposition behavior. Pollinating and nonpollinating ®g wasps were shown to interact intimately, and to have a signi®cant effect on the host plant in at least some cases. Each species of the community seems to preferentially oviposit in a part of the female ¯owers, depending on their depth inside the ®g. Convergence in ®g exploitation thus exists in various chalcid lineages, and the community structure and organization are very similar between ®g species. Concepts developed in parasitoid community ecology could now be tested on this promising model. Key words: community structure; competition; Ficus; ®g; gallmakers; guild; interactions; mu- tualism; niche; nonpollinating ®g wasps; parasitoids; path analysis; pollination. INTRODUCTION (Schoenly et al. 1991). To understand which parameters Studying entire communities is one of the major (historical as well as ecological) in¯uence the func- challenges of ecological science. Insects have long tional organization of a community, and what major proved to be an ideal model on which to build com- forces have shaped it (see Grandcolas 1998), many au- munity ecology theories and to test subsequent hy- thors have conducted comparative studies on parasitoid potheses. Due mainly to the potential role of parasitoids communities associated with related hosts such as Mac- in biological control, but also because of their species rolepidoptera (Sheehan 1994) or grass chalcids (Dawah richness and diversity, most published insect commu- et al. 1995), or on phytophagous communities asso- nity studies (either modeling works or ®eld data anal- ciated with related host plants (Compton et al. 1989, yses) are centered on host±parasitoid relationships and ZwoÈlfer and Brandl 1989, Frenzel and Brandl 1998). aim at understanding species diversity (e.g., Jones and Broader comparative studies are also available (Hirose Lawton 1991, Cornell and Lawton 1992, Hochberg and 1994, Hawkins and Mills 1996). However, due to in- Hawkins 1992, Dawah et al. 1995), community satu- herent complexity, quantitative interactions between ration (Lawton and Price 1979, Hawkins and Compton species belonging to the same community are rarely 1992, Hawkins and Mills 1996), or long-term system analyzed, even though they remain of considerable im- stability (Hassell and May 1974, Pacala and Hassell portance to understanding the constraints that in¯uence 1991, Holt and Hassell 1993, Wilson et al. 1996). Pre- community evolution and structuring (Memmott et al. vious studies have underlined the importance of iden- 1994, Dettner et al. 1997). The purpose of the present tifying species guilds (Mills 1994), and of understand- work is to quantitatively analyze species interactions ing a community through its functional structure and within four chalcid communities associated with Ficus the food web relationships of the composing species species in Africa, and to determine and compare the intrinsic pressures that can shape their structure and Manuscript received 4 January 1999; revised 21 September 1999; accepted 29 September 1999. functioning. 3 Present address: Institut National de la Recherche Agron- Almost all of the ;750 Ficus species (Moraceae, see omique, Station de Zoologie ForestieÁre, BP 20619 Ardon, Berg 1989) is involved in a species-speci®c obligate 45166 Olivet Cedex, France. mutualism with its pollinator chalcid wasp (Hymenop- 4 Present address: Institut National de la Recherche Agron- omique, Laboratoire de ModeÂlisation et Biologie Evolutive, tera: Agaonidae), which also strictly depends on its host 488 rue Croix de Lavit, F-34090 Montpellier, France. ®g for reproduction (Ramirez 1970, Galil 1977, Wiebes 2832 October 2000 FIG AND FIG WASP COMMUNITIES 2833 1979). The system is one of the very few examples of for the impact they have on the ®g±pollinator mutu- probable plant±insect coevolution (Kjellberg et al. alism (Galil et al. 1970, Bronstein 1991, West and Herre 1987b, Anstett et al. 1997). Moreover, each monoe- 1994, Cook and Power 1996, Kerdelhue and Rasplus cious ®g species also harbors a diversity of nonpolli- 1996b, West et al. 1996). We argue that the ®g wasps nating chalcid wasps (up to 30 species [Compton and also represent an ideal model for community ecology Hawkins 1992]) which strictly develop in the ®g ¯ow- studies, and will allow documentation of community ers as parasitoids or gallmakers (Galil et al. 1970, Bron- structure (see the ®rst studies by Compton and Hawkins stein 1991, West and Herre 1994, Kerdelhue and Ras- 1992, Hawkins and Compton 1992) and within- and plus 1996b, West et al. 1996), and that are speci®cally between-guild species interactions, as well as studies associated with the host plant. Interestingly, the ®ve of the ecological impact on the host plant, which is recognized nonpollinating wasp subfamilies were re- usually dif®cult to quantify (Kerdelhue and Rasplus cently proved to have evolved from at least three in- 1996b, West et al. 1996). We propose a functional rath- dependent lineages, and to be of recent evolutionary er than a taxonomical model of the whole system or- origin compared to the pollinator clade (Rasplus et al. ganization based on a comparative study of four mon- 1998). Consequently, comparing communities in which oecious African ®g systems. A comparison is made different chalcid subfamilies are involved will allow between these African models and the American ®g us to look for convergence of community organization species that have previously been well studied (sub- and niche utilization in independent lineages, and to genus Pharmacosycea and subgenus Urostigma section test whether or not similar ecological trade-offs exist Americana: Bronstein 1991, West and Herre 1994, within each community. West et al. 1996, Herre and West 1997). The subgenus Each ®g wasp community is centered on a number Ficus is not considered in our work, since it is con- of gallmakers that oviposit directly in the female ¯ow- stituted of dioecious species on which the nonpolli- ers, which are packed in up to four layers in the ®g nating ®g wasp communities are very limited (Ker- cavity. Each ¯ower can receive one egg, and subse- delhue and Rasplus 1996a). quently turns into a gall that will enable the develop- ment of one single larva. Some species, including the MATERIALS AND METHODS pollinator, enter the ®g to lay eggs, whereas others Study site remain on the external side of the syconium and pierce the ®g wall using a long ovipositor. Each species arrives The study was carried out in the Lamto Ecological on the ®g at a speci®c development time. The number Station (58029 W, 6 8139 N), located in CoÃte d'Ivoire, of oviposition sites available to the gallmakers is thus 160 km northwest of Abidjan. The area is located in a discrete factor that may be limiting. The different the southern part of the arboreous savanna which pen- species will possibly compete for that resource, espe- etrates the partially destroyed rain forest of the southern cially if they can reach the same ovary layer. If a non- Ivory Coast. pollinating species lays an egg in an ovule that would Natural history have produced a seed, it may further have a negative impact on the ®g female function. All nonpollinating Figs and pollinators.ÐA monoecious ®g is a closed gallmakers drain energetic resources from the host in¯orescence that contains tens to thousands of both plant. Moreover, as the pollinator larvae will spread female and male ¯owers. When the female primordia the pollen produced by its native ®g, any species that reach maturity, the syconium emits speci®c volatile competes with the pollinator foundress will have a neg- compounds (Ware et al. 1993, Hossaert-McKey et al.