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Los patrones de aparicin y polimorfismo masculino en la avispa no-polinizadora de los higos Aepocerus sp. (Torymidae)
Emergence patterns and male polymorphism in the nonpollinating fig wasp Aepocerus sp. (Torymidae)
This study was designed to investigate a perceived male dimorphism in the nonpollinating fig wasp Aepocerus sp. (Torymidae), as well as to examine emergence schedules of males and females as well as of different male morphs. I collected 100 Ficus pertusa figs and preserved the wasps that emerged from each fig every day for five days. I counted the number of male and female Aepocerus sp. that emerged from each fig each day, and I measured body size and degree of wing patchiness in males to assess whether the species exhibits male dimorphism. I found that males tend to emerge earlier (avg = 3.02 1.14 days, N = 528) than females (avg = 3.44 1.18 days, N = 340)(t = -5.601, p < 0.001). Male body sizes ranged from 1.1 to 2.5 mm with an average of 1.764 mm 0.20 (N = 528) and followed a roughly normal distribution. Across all males, wing patchiness was positively correlated with body size (R2 = 0.541, p < 0.001, N = 528) and body size was negatively correlated with day of emergence (R2 = 0.066, p < 0.001, N = 528). I observed two male morphs, distinguished most clearly by the appearance of their abdomens (rather than by body size or wing patchiness, as previously believed). Males with opaque abdomens tended to be smaller (avg = 1.57 0.02 mm, N = 78) than males with translucent abdomens (avg = 1.80 0.05 mm, N = 450)(t = 8.847, p < 0.001) and also tended to emerge later (avg = 3.65 1.32 days, N = 78) than males with translucent abdomens (avg = 2.91 1.02 days, N = 450)(t = -5.834, p < 0.001). My results highlight the need for further study of Aepocerus sp. in order to understand developmental mechanisms for male morphs.
Este estudio fue diseado para investigar un notorio dimorfismo masculino en la avispa no-polinizadora de los higos Aepocerus sp. (Torymidae), as como examinar los horarios de aparicin de los machos y las hembras, al igual que de los diferentes morfos masculinos.
Text in English.
Sexual dimorphism (Animals)
Tropical Ecology 2008
Nonpollinating fig wasp--Costa Rica
Ecologa Tropical 2008
t Monteverde Institute : Tropical Ecology
1 Emergence Patterns and Male Polymorphism in the Nonpollinating Fig Wasp Aepocerus sp. Torymidae Katelyn Burgess Department of Biology, College of William & Mary ABSTRACT This study was designed to investigate a perceived male dimorphism in the nonpo llinating fig wasp Aepocerus sp. Torymidae, as well as to examine emergence schedules of males and females as well as of different male morphs. I collected 100 Ficus pertusa figs and preserved the wasps that emerged from each fig every day for five days . I counted the number of male and female Aepocerus sp. that emerged from each fig each day, and I measured body size and degree of wing patchiness in males to assess whether the species exhibits male dimorphism. I found that males tend to emerge earlier avg = 3.02 Â± 1.14 days, N = 528 than females avg = 3.44 Â± 1.18 days, N = 340 t = 5.601, p < 0.001. Male body sizes ranged from 1.1 to 2.5 mm with an average of 1.764 mm Â± 0.20 N = 528 and followed a roughly normal distribution. Across all males , wing patchiness was positively correlated with body size R 2 = 0.541, p < 0.001, N = 528 and body size was negatively correlated with day of emergence R 2 = 0.066, p < 0.001, N = 528. I observed two male morphs, distinguished most clearly by the appea rance of their abdomens rather than by body size or wing patchiness, as previously believed. Males with opaque abdomens tended to be smaller avg = 1.57 Â± 0.02 mm, N = 78 than males with translucent abdomens avg = 1.80 Â± 0.05 mm, N = 450 t = 8.847, p < 0.001 and also tended to emerge later avg = 3.65 Â± 1.32 days, N = 78 than males with translucent abdomens avg = 2.91 Â± 1.02 days, N = 450 t = 5.834, p < 0.001. My results highlight the need for further study of Aepocerus sp. in order to understand developmental mechanisms for male morphs. RESUMEN Este estudio fue diseÃ±ado para investigar un notorio dimorfismo en los machos de la avispa no polinizadora de higos Aepocerus sp. Torymidae, asÃ como examinar los tiempos de eclosiÃ³n de machos y hembra s y de las diferentes formas de los machos. ColectÃ© 100 frutos de Ficus pertusa y se conservaron las avispas que eclosionaron de cada higo cada dÃa durante cinco dÃas. ContÃ© el nÃºmero de hembras y machos de Aepocerus sp. que eclosionan de cada higo diar iamente, y medÃ el tamaÃ±o corporal y el patrÃ³n de manchas en las alas para calcular el dimorfismo exhibido por los machos. EncontrÃ© que los machos tienden a eclosionar mÃ¡s temprano prom = 3.02 Â± 1.14 dÃas , N = 528 que las hembras prom = 3.44 Â± 1.18 dÃas , N = 340 t = 5.601, p < 0.001. El tamaÃ±o corporal de los machos varia de 1.1 a 2.5 mm con un promedio de 1.764 mm Â± 0.20 N = 528 y sigue una distribuciÃ³n normal. Entre todos los machos, el patrÃ³n de manchas en las alas estÃ¡ correlacionado positiva mente con el tamaÃ±o corporal R 2 = 0.541, p < 0.001, N = 528 y el tama Ã± o corporal esta negativamente correlacionado con el d Ãa de eclosiÃ³n R 2 = 0.066, p < 0.001, N = 528. ObservÃ© dos morfos en machos, distinguidos claramente por la apariencia del abdo men mÃ¡s que por el tamaÃ±o corporal o el patrÃ³n de manchas en las alas, como creÃa previamente . Machos con abdÃ³menes opacos tienden a ser mÃ¡s pequeÃ±os prom = 1.57 Â± 0.02 mm, N = 78 que los que tienen abdÃ³menes translÃºcidos prom = 1.80 Â± 0.05 mm, N = 450 t = 8.847, p < 0.001 y tambiÃ©n tienden a eclosionar mÃ¡s tarde prom = 3.65 Â± 1.32 dÃas , N = 78 que los machos con abdÃ³menes translÃºcidos prom = 2.91 Â± 1.02 dÃas , N = 450t = 5.834, p < 0.001. Mis resultados sugieren un futuro estudio en Aepocerus sp . en orden para entender mecanismos de desarrollo en los morfos de los machos. INTRODUCTION Figs Ficus , Family Moraceae are some of the most abundant tropical trees in the world. Globally, there are approximately 900 described species, with at least 6 5 in Costa Rica alone
2 Janzen 1979. They are characterized in part by their round, hollow inflorescences syconia which are lined with tiny florets containing a single ovary. It is inside these syconia that one of the most complex and fascinating mutua lisms known occurs. Each species of fig is pollinated by a unique species of wasp Family Agaonidae. When a female agaonid wasp arrives at a receptive syconium, she enters and, once inside, she crawls along the florets, laying eggs as well as spreading pollen carried from another fig. She dies once oviposition is complete, but her larvae develop, feeding off the ovary tissue. Once mature, the wingless agaonid males emerge from the ovaries first, remain in the hollow space where they seek females with whom they copulate. Males then cut an exit hole through the fig tissue and die soon thereafter. However, females, laden with pollen, exit through the hole to seek another tree with receptive figs, where the cycle begins anew Janzen 1983. Besides these pollinators, figs are also host to a number of nonpollinator wasp species. These nonpollinators are believed to be somewhat less host specific, and there may be many different nonpollinator species associated with a single species of fig. Among the nonp ollinators are those of the family Torymidae. Rather than ovipositing from within the syconium, torymid females use their ovipositors to puncture the syconium wall from the outside to reach unoccupied ovaries in which to deposit their eggs. Upon maturation , torymids exit the syconium via the hole chewed out by male agaonids. Thus, torymids are highly dependent upon agaonids, both for their escape route and because the fig tree will likely abort any syconia which are not pollinated Bronstein 1991; West et a l. 1996. Some torymids differ greatly from agaonids in terms of mating. Aepocerus sp. is one such species. These wasps are specific to Ficus pertusa , a common fig tree in the Monteverde area. While agaonids copulate prior to the females exit from the sy conium, Aepocerus sp. males and females emerge from the fruit first, then copulate outside. Additionally, this species exhibits extreme male polymorphism and associated alternative mating strategies which, despite their uniqueness and curiosity, have been poorly studied. Some males are larger with brownish patches on their forewings while others are smaller and have clear forewings. Larger males are aggressive and wait for emerging females by the syconium exit hole, attacking competitors Bronstein 1991, and smaller males wait at a distance from the exit hole and sneak copulations K. Masters, personal communication. The degree to which these represent distinct morphs versus a continuum has not previously been studied. Assuming that there are in fact tw o distinct Aepocerus sp. male morphs with associated mating strategies, it is of interest to consider how such a situation arises. How these two behaviors can occur in one species has been debated, as it would seem that one would be more successful and for ce the other out of existence Cade 1980. However, it appears that they may be examples of what are referred to as Evolutionarily Stable Strategies ESS. An ESS is a strategy which, when a certain frequency of the population adopts it, is unbeatable r eproductively compared to a given set of alternatives Cade 1980. Evolution generally favors males who will act aggressively for immediate reproductive payoff, meaning that associated traits like developed secondary sex characteristics will be selected for as well. This explains the existence of the larger, patchy winged Aepocerus sp. males who exhibit fighting behavior. These males should have more copulations in a given time period relative to the smaller males, however they also experience the energe tic costs of larger body size and patch development, as well as decreased lifespan due to fighting. On the other hand, smaller males should be competitive because they have lower energetic costs and increased survivorship. While they may not copulate as of ten as the larger males in a given period of time, they should come out even
3 over their lifespans. The relative strategy frequencies should theoretically be kept at equilibrium because the benefits of a strategy increase if its frequency decreases. Hence , they persist simultaneously because they balance one another. It is also of interest to consider how the male morphs develop, i.e. whether it is under genetic or environmental control, or some combination of the two. A number of studies have focused on organisms exhibiting similar male polymorphisms to address this very question. For example, Emlen 1997 studied the beetle Onthophagus acuminatus , which has male dimorphism as well as associated aggressive and sneaker mating strategies. His study con cluded that higher diet quality resulted in the larger, more aggressive male phenotype, regardless of parent phenotypes, suggesting a strong environmental control. Additionally, Kurziel & Knowles 2002 investigated the amphipod Jassa marmorata , which show s a similar trend in males, and concluded that a higher quality diet as well as a longer development time led to the more aggressive male. Given these findings, I hypothesized that Aepocerus sp. male polymorphism is strongly influenced by environmental fa ctors during development, including the time spent in development . This study was designed to investigate the relationship between the time of emergence from the syconium i.e. development time and the male morphs, as well as the correlation between male size and wing patchiness i.e. development time and degree of polymorphism. I predicted that there would be a strong correlation between male body size and wing patchiness, and that larger, more aggressive males would emerge later than the smaller sneak er males. MATERIALS & METHODS I used a F. pertusa individual in the backyard of the CÃ©spedes Marin family in CaÃ±itas, Costa Rica, near the entrance to la Finca Los Cruz. I collected 100 figs with newly formed exit holes over the course of two days. Eac h fig was placed in a separate jar. Once a day for five days, I removed the wasps that had emerged from each fig and preserved them in ethanol in Petri dishes labeled by fig and day. I counted the number of male and female Aepocerus sp. individuals that e merged from each fig on each day. Day 1 represents the first day on which male Aepocerus sp. males emerged from figs. I also measured the males from head to abdomen, using a dissecting microscope fitted with an ocular micrometer. Finally, I scored the degree of patchiness of each male s forewings. I found that males could have patches of variable size on the tips of their forewings, near their wing joints, in both places, or in neither. Based on that, I made a scale from one to six in order to score eac h individual. The scale was as follows: 1 no patches; 2 very faint patches near wing joints; 3 small patches near wing joints; 4 distinct patches near wing joints; 5 small patches on wing tips and near wing joints; 6 strong patches on wing tips and near wing joints Figure 1a f, respectively. I tested for a correlation between male body size and wing patchiness using a regression analysis. I also tested for a correlation between male body size and day of emergence using a regression analysis. I used t tests to analyze: 1 the difference between average male and female day of emergence; 2 the difference between the average body sizes of the two male morphs; and 3 the difference between average days of emergence for the two male morphs.
4 R ESULTS I collected 340 Aepocerus sp. females and 528 Aepocerus sp. males. Males tended to emerge earlier avg = 3.02 Â± 1.14 days, N = 528 than females avg = 3.44 Â± 1.18 days, N = 340 t = 5.601, p < 0.001 Figure 2. Male body sizes ranged from 1.1 t o 2.5 mm with an average of 1.764 mm Â± 0.20 N = 528 and followed a roughly normal distribution Figure 3. I observed two male morphs: one with a fatter, opaque black abdomen and clear forewings opaque morph, Figure 1a, and one with a narrower, tra nslucent abdomen and variable wing patchiness translucent morph, Figure 1b f . Opaque morph males were generally smaller avg = 1.57 Â± 0.02 mm, N = 78 than translucent morph males avg = 1.80 Â± 0.05 mm, N = 450 t = 8.847, p < 0.001. Translucent morph males generally emerged earlier avg = 2.91 Â± 1.02 days, N = 450 than opaque morph males avg = 3.65 Â± 1.32 days, N = 78 t = 5.834, p < 0.001 Figure 4. Across all males, wing patchiness was positively correlated with body size R 2 = 0.541, p < 0.0 01, N = 528Figure 5 and body size was negatively correlated with day of emergence R 2 = 0.066, p < 0.001, N = 528 Figure 6. DISCUSSION My results show that males generally emerge from figs earlier than females, which fits my original predictions. A epocerus sp. males wait for females at exit holes as they emerge so that they can copulate with them, so it is logical that males would emerge first. Further, my results show that females emerged only a little less than half a day after males. The amount o f time that a male has to wait outside a fig for females to emerge presumably has implications for that male s fitness, since he is susceptible to predators and environmental threats in the meantime Bronstein 1988. This short lag time may have evolved in order to give most males just enough time to leave the fig before females emerge, minimizing time spent exposed on the fig surface. It would be interesting to assess the rate of male mortality in Aepocerus sp. as they wait for females, relative to their o wn days of emergence. The male phenotype has proven to be more complex than previously understood. Bronstein 1991 described a male dimorphism distinguished by body size and the presence or absence of wing patches. Specifically, she noted a small, clear winged morph and a large, patch winged morph. However, my results show that male body size is continuous and positively correlated with a continuum of wing patchiness, suggesting that size or wing patchiness alone are not enough to distinguish between morphs. I did note a distinct male dimorphism, but one that differed somewhat from Bronstein s. One morph that I saw probably roughly the one Bronstein referred to as small, clear winged was generally smaller and always had clear forewings, but, notabl y, also had a fatter, more opaque abdomen, which I found to be the most distinctive characteristic of the morph. The other male morph that I observed had a narrower, more translucent abdomen as well as forewings exhibiting a continuum from clear to very pa tchy. Henceforth, the morphs will be referred to as opaque and translucent, respectively, to reflect the most clearly distinguishing characteristic between them. Within the translucent morph, there is considerable polymorphism. Wing patchiness increa ses along with body size, so the smallest translucent morph males tend to have very small, faint patches or none at all, and the biggest translucent morph males tend to have large, distinct
5 patches. It seems then that I have observed a male dimorphism in A epocerus sp., with the translucent morph exhibiting further polymorphism in terms of wing patchiness. It is of interest to consider how such male phenotypic variability arises developmentally. Bronstein 1991 noted that large, patch winged males roug hly equivalent to my translucent morph employ an aggressive mating tactic, defending the exit hole against competitors. Small, clear winged males roughly my opaque morph were observed to wait farther off to sneak copulations. While I did not include a behavioral study in my work, I noted the same trends in casual observations. These factors combined that the translucent morph males are generally larger, patchier, and more aggressive would appear to suggest that they might emerge later than the opaque morph males, since it seems as though they would require more time to develop. On the contrary, my results indicated that translucent morph males generally emerged almost a day earlier than opaque morph males, suggesting that development time alone is no t responsible for morph determination. Of course, it is possible that the translucent morph males were not laid at the same time as the opaque morph males, or even by the same female. Or, maybe the translucent morph males are larger, patchier, and more a ggressive because they had greater access to resources in development. The effects of differential nutrition in development of fig wasps has not been studied, but in studies on amphipods and beetles that show similar male dimorphism and associated alterna tive mating strategies, better nutrition led to larger, more aggressive male morphs Emlen 1997; Kurziel and Knowles 2002. If resources are the deciding factor here, those resources could come from two possible sources. First, it may be that nutrient availability is not uniform throughout a fig, so that two wasps in a single fig receive unequal resources and hence develop at different rates and to different degrees. If this were true, however, one could expect to find an equal degree of polymorphism i n female Aepocerus sp. and in other species of fig wasps, unless Aepocerus sp. male development just happens to be more strongly affected by resource availability. Besides the resources from figs, it could also be that males receive different amounts of n utrients from their eggs. Perhaps female Aepocerus sp. invest more in some eggs than others, leading those larvae developing from eggs with higher nutrients to grow bigger and more quickly than males developing from lower quality eggs. Expanding on thi s idea, if female Aepocerus sp. have lower and higher quality eggs, it would make sense that they might oviposit their better eggs first and their lower quality ones later on. If so, it could help explain why the opaque morph males emerged later than t he translucent morph males. The results of my study raise a number of questions about Aepocerus sp., which only serve to highlight how little, is known about this fascinating species. Further research is needed on the developmental mechanism or mechanisms by which the male dimorphism and translucent male polymorphism arise. It would be of interest in the future to conduct studies assessing the degree of genetic relatedness between male morphs, or to manipulate nutrient availability for Aepocerus sp. male larvae to test for developmental effects. Both studies would help to shed some light on the mysteries of male morph determination in this species.
6 ACKNOWLEDGEMENTS My sincere thanks to Karen Masters for introducing me to this amazing species, for h elping me to design my study, and for lending her support and enthusiasm along the way. Thanks to the CÃ©spedes Marin family for use of their fig tree, and especially to AngÃ©lica and Alejandra for helping me to collect figs. Thanks to Taegan McMahon and Pab lo Allen for helping me re learn statistics. Thanks to the EstaciÃ³n BiolÃ³gica de Monteverde for providing me with the resources to conduct my project and a gorgeous location in which to do it. And finally, a huge thank you to my parents for sending me off to the rainforest. It has been quite an adventure. LITERATURE CITED BRONSTEIN, J. L. 1988. Predators of fig wasps. Biotropica. 203: 215 219. ----------. 1991. The nonpollinating wasp fauna of Ficus pertusa : exploitation of a mutualism? Oikos. 61: 175 186. CADE, W. 1980. Alternative male reproductive behaviors. The Florida Entomologist. 631: 30 45. EMLEN, D. J. 1997. Diet alters male horn allometry in the beetle Oncophagus acuminatus Coleoptera: Scarabaeidae. Proceedings of the Royal Society of London: Biological Sciences. 2641381: 567 574. JANZEN, D. H. 1979. How to be a fig. Annual Review of Ecology and Systematics. 10: 13 51. ---------. 1983. Blastophaga and other Agaonidae. In D. H. Janzen Ed.. Costa Rican Natural History, The Unive rsity of Chicago Press, Chicago, Illinois, pp. 696 700. KURDZIEL, J. P. AND L. L. KNOWLES. 2002. The mechanics of morph determination in the amphipod Jassa : Implications for the evolution of alternative male phenotypes. Proceedings of the Royal Society of London: Biological Sciences. 2691502: 1749 1754. WEST, S. A., E. A. HERRE, D. M. WINDSOR AND P. R. S. GREEN. 1996. The ecology and evolution of New World non pollinating fig wasp communities. Journal of Biogeography. 234: 447 458.
7 FIGURES FIGURE 1. Representatives of the wing patchiness scale in Aepocerus sp. males from 1 to 6 a f, respectively. a is an opaque morph; b f are translucent morphs. Photos not of equal magnification. FIGURE 2. Number of mal e and female Aepocerus sp. that emerged from figs each day. Males N = 528 generally emerged earlier than females N = 430t = 5.601, p < 0.001. 0 50 100 150 200 250 1 2 3 4 5 Day of emergence # Individuals Males Females a b c d e f
8 FIGURE 3. Aepocerus sp. male body size followed a roughly normal distribution N = 528. FIGURE 4. Number of Aepocerus sp. opaque morph males N = 78 and translucent morph males N = 450 that emerged from figs each day. Translucent morphs generally emerged earlier than opaque morphs t = 5.834, p < 0.001. 0 50 100 150 200 250 1.1-1.3 1.4-1.6 1.7-1.9 2.0-2.2 2.3-2.5 Body size mm # Individuals 0 20 40 60 80 100 120 140 160 180 1 2 3 4 5 Day of emergence # Individuals Opaque Morphs Translucent Morphs
9 FIGURE 5. Relationship between male body size and wing patchiness in Aepocerus sp. Wing patchiness tended to increase along with male body size R 2 = 0.541, p < 0.001, N = 528. FIGURE 6. Relationship between day of emergence from figs and body size in Aepocerus sp. males. Larg er males tended to emerge earlier than smaller males R 2 = 0.066, p < 0.001, N = 528. 0 1 2 3 4 5 6 7 0.8 1.3 1.8 2.3 2.8 Body size mm Wing patchiness 0.8 1.0 1.2 1.4 1.6 1.8 2.0 2.2 2.4 2.6 2.8 0 1 2 3 4 5 6 Day of emergence Body size mm