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Assured Fitness Returns Favor Sociality in a Mass-Provisioning Sweat Bee, Megalopta Genalis (Hymenoptera: Halictidae)

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Assured Fitness Returns Favor Sociality in a Mass-Provisioning Sweat Bee, Megalopta Genalis (Hymenoptera: Halictidae) Behav Ecol Sociobiol (2003) 54:14–21 DOI 10.1007/s00265-003-0589-0 ORIGINAL ARTICLE Adam R. Smith · William T. Wcislo · Sean O’Donnell Assured fitness returns favor sociality in a mass-provisioning sweat bee, Megalopta genalis (Hymenoptera: Halictidae) Received: 8 April 2002 / Revised: 23 January 2003 / Accepted: 24 January 2003 / Published online: 19 March 2003 Springer-Verlag 2003 Abstract Assured fitness returns models for the evolu- Introduction tion of sociality emphasize the selective value of ensuring that offspring receive adequate parental care to reach Although much attention has been focused on the role of maturity. If a member of a social group dies, it can accrue high relatedness in promoting the evolution of eusociality returns on investment in offspring through the efforts of via kin selection (Hamilton 1964, reviewed in Queller and surviving social partners. We provide evidence that in the Strassmann 1998), recent studies of sweat bees (Halicti- mass-provisioning, facultatively social sweat bee Mega- dae) highlight the importance of extrinsic factors in lopta genalis, adult presence in the nest throughout brood favoring social over solitary behavior (Wcislo 1997a, development provides protection from ant predation. 2000). While some species of halictid bees are obligately Nests with adults present were well protected, and brood and permanently eusocial, members of some populations in nests with adults removed suffered higher predation. express both solitary reproduction and eusociality (re- Females in observation nests showed effective defensive viewed in Wcislo 1997a, 2000). Because of their ability to behavior against experimentally introduced ants, and bees switch between modes of social organization, individuals in natural nests repulsed naturally occurring ant raids. may exhibit solitary behavior when it is advantageous Megalopta nest architecture and behavior are such that over social behavior, and vice versa. Although current the brood of several cooperating females can be defended social flexibility may not represent an intermediate step with little additional cost relative to solitary nesting. The toward an evolutionary endpoint of obligate eusociality, benefits of cooperative defense may favor group living in socially flexible species can be used to test hypotheses for mass provisioning bees. Our observations and experi- the costs and benefits of group living (Danforth and ments suggest that parental care throughout brood devel- Eickwort 1997; Wcislo and Danforth 1997; Danforth opment can be adaptive in mass provisioning species, 2002; Soucy and Danforth 2002). supporting the predictions of assured fitness returns A key question that must be addressed in any expla- models. nation for the expression of social behavior is: Why do some adults forgo direct reproduction and act as helpers Keywords Assured fitness returns · Social evolution · rather than leave to found their own nests? Assured fitness Ant predation · Brood defense returns (AFR) models argue that patterns of adult mortality combine with offspring dependence on parental care to select for group living (Queller 1989, 1994, 1996; Strass- mann and Queller 1989; Gadagkar 1990, 1991; Bull and Schwarz 2001). AFR models posit that group living is selectively favored because it increases the likelihood of Communicated by R.F.A. Moritz fitness payoffs to parental and kin investment. In a social A. R. Smith ()) · S. O’Donnell group, if an adult dies before the brood reach maturity, Animal Behavior Area, Department of Psychology, other adults remain to provide parental care. Studies of University of Washington, progressive provisioning species (those species that must Seattle, WA 98195, USA feed offspring repeatedly throughout larval development) e-mail: [email protected] such as paper wasps and hover wasps (Vespidae), and Tel.: +1-206-5250403 Fax: +1-206-6853157 allodapine bees (Apidae) support AFR models (Queller 1989; Gadagkar 1990; Bull and Schwarz 1996, 1997; W. T. Wcislo Schwarz et al. 1997, 1998; Field et al. 2000; Hogendoorn et Smithsonian Tropical Research Institute, al. 2001). In these cases the benefits are clear, because Unit 0948, APO AA 34002, Panama 15 progressively provisioned offspring would starve without 7951'W), Panam Province, Republic of Panam. BCNM is a continual feeding by adults. lowland tropical semi-deciduous moist forest with a pronounced dry season, usually from mid-December through mid-April (Rau Some social insect species, including halictid bees, are 1933; Leigh 1999). mass provisioners, meaning that females provide all necessary food for offspring development before laying an egg (Wilson 1971; Michener 1974). Because offspring Overview of natural history could potentially reach maturity even if the parent died M. genalis are collected at light traps the year round on BCI (Wolda immediately after oviposition, AFR models were not and Roubik 1986; Roubik and Wolda 2001), but they provision initially applied to mass provisioners (Queller 1989; nests and reproduce primarily in the dry season and first half of the Gadagkar 1990). However, mass-provisioned offspring wet season (for details of their nesting and social biology, see may be dependent on other forms of parental care, such as Arneson and Wcislo 2003; W.T. Wcislo et al., unpublished data.). Nests occur in relatively dry, broken sticks that are usually defense against nest predation and parasitism (Queller suspended in tangles of vegetation (Fig. 1; Sakagami 1964; Janzen 1994; Eickwort et al. 1996; Kukuk et al. 1998). For 1968). The nest entrance has a constricted collar made of chewed example, Eickwort et al. (1996) showed that the brood of wood, with a diameter slightly wider than the resident(s)’ head naturally orphaned solitary nests of a mass-provisioning, (Fig. 1c). The entrance opens into a single tunnel that has cells adjacent to it; cell entrances are flush with the tunnel wall (Fig. 1b). facultatively social bee, Halictus rubicundus, suffered At the start of the dry season, most nests (>75%) contain a greater fly parasitism than those with adults present at the solitary female. Females forage during the approximately 1.5 h time of nest collection. Similarly, Kukuk et al. (1998) after sunset and before dawn. Development from egg to adult takes showed that in the communal bee Lasioglossum approximately 35 days. Newly eclosed females are fed by older adult(s) for 1–14 days, and may then disperse or join the natal nest. hemichalceum, unattended brood suffered greater ant Females younger than 2 weeks have undeveloped ovaries. predation than brood protected by an adult. These studies Later in the dry season ~25–50% of nests have multiple females, were correlational. Experimental demonstration of selec- presumably because some daughters joined their natal nests. Multi- tive disadvantages if brood are orphaned would argue for female nests average 2.5€0.09 (SE) females, but group size varies the importance of parental care throughout brood devel- seasonally. Multi-female nests have up to ten females, although nests with more than four females are uncommon. Throughout the opment, and confirm the applicability of AFR models to year, some bees establish new nests, as inferred from the continual mass provisioning species. occurrence of singleton nests with one or a few brood cells. We used the facultatively social, Neotropical sweat Within multi-female observation nests, a dominant bee is bee Megalopta genalis (Halictidae: Augochlorini) to generally larger, older, mated and has fully developed ovaries; she rarely forages and frequently receives nectar from a subordinate experimentally test whether defense against predators via trophallaxis. In contrast, the subordinate(s) tend to be younger, may select for group living in a mass provisioning smaller, mated or unmated, and have slender or developed ovaries; species. Ant predation is a major threat to many social they are the primary foragers and frequently give nectar to insects (Jeanne 1975; Hlldobler and Wilson 1990; dominants via trophallaxis. The first brood has a female-biased sex ratio and the proportion of males increases throughout the Schwarz et al. 1998), and is especially strong in the season. Brood rearing is not synchronized and adults continue to tropics (Jeanne 1979; Kojima 1993). Thus, we focused forage as brood develop. The distribution of reproduction within our studies on M. genalis defense against ant predation. natural multi-female nests is not known, but based on dissections We investigated what contribution, if any, adult Mega- lopta made to nest defense against ants. If the brood rely on adult protection, Megalopta could realize improved fitness by living in groups and thereby avoid brood orphanage. We conducted three field studies. First, we observed naturally occurring M. genalis defense against ant preda- tion. We next experimentally removed adults from some M. genalis colonies, and predicted that nests with adult females would suffer less ant predation than orphaned nests. Finally, we observed bees in artificial nests to document their responses to invading ants, and we tested for the application of ant repellent chemicals at the nest entrance. We discuss the implications of our results for the adaptive value of group living in Megalopta, and in other mass provisioning species. Fig. 1a–c Megalopta genalis nest architecture. Both scale Methods bars=1 cm. a Cells inside the nest, constructed of chewed wood fiber: c exposed cells, o cells’ natural opening. b Sealed, Study site provisioned
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