Search

INTRODUCTION Biotic interactions are vital to ecosystem functioning. Interactions among individuals lie at the core of population and community dynamics, and therefore play a central role in the existence and [...]

Understanding cooperation is a central challenge in biology, because natural selection should favor 'free-loaders' that reap benefits without reciprocating. For interspecific cooperation (mutualism), most approaches to this paradox focus on costs and benefits of individual partners and the strategies mutualists use to associate with beneficial partners. However, natural selection acts on lifetime fitness, and most mutualists, particularly longer-lived species interacting with shorter-lived partners (e.g., corals and zooxanthellae, tropical trees and mycorrhizae) interact with multiple partner species throughout ontogeny. Determining how multiple partnerships might interactively affect lifetime fitness is a crucial unexplored link in understanding the evolution and maintenance of cooperation. The tropical tree Acacia drepanolobium associates with four symbiotic ant species whose short-term individual effects range from mutualistic to parasitic. Using a long-term dataset, we show that tree fitness is enhanced by partnering sequentially with sets of different ant symbionts over the ontogeny of a tree. These sets include a 'sterilization parasite' that prevents reproduction and another that reduces tree survivorship. Trees associating with partner sets that include these 'parasites' enhance lifetime fitness by trading off survivorship and fecundity at different life stages. Our results demonstrate the importance of evaluating mutualism within a community context and suggest that lifespan inequalities among mutualists may help cooperation persist in the face of exploitation. Acacia drepanolobium | cooperation | plant defense | life history theory | ant-plant doi/ 10.1073/pnas.1006872107

To link to full-text access for this article, visit this link: http://dx.doi.org/10.1016/j.anbehav.2010.05.007 Byline: Ruben Alarcon (a), Jeffrey A. Riffell (b), Goggy Davidowitz (c), John G. Hildebrand (b), Judith L. Bronstein (d) Abstract: Studies of plant-pollinator interactions have often documented species differences in preferences for floral advertisements and rewards. However, the contribution of intraspecific variation in behaviours, especially between sexes, remains less understood. We explored resource preference and resource use by male and female Manduca sexta hawkmoths, relative to two important nectar resources in southern Arizona, U.S.A. Manduca sexta is the major pollinator of one of these species (Datura wrightii, Solanaceae). Because females must also seek out D. wrightii as an oviposition resource, females were predicted to feed upon it more than would males, which should be free to choose the best nectar resource. Using naA[macron]ve laboratory-reared moths in flight arena experiments, we found that both sexes preferred Datura wrightii over Agave palmeri (Agavaceae). Exposure to only one species and an odourless paper control, however, revealed sex-specific differences in foraging behaviour, with females feeding longer from A. palmeri and males feeding longer from D. wrightii, leading us to reject our hypothesis. Differences in feeding preferences directly translated into differences in energy intake. Females gained significantly more energy than did males by feeding from A. palmeri. We also examined whether behavioural preferences of moths in the laboratory translated into foraging behaviour in the field. Pollen load analysis of moths caught in 2004 showed that females carried significantly more A. palmeri pollen than did males, whereas males carried more D. wrightii pollen than did females. Whereas most studies examine pollination associations at the species level, our results highlight the potential importance of between-sex variation in floral visits. Author Affiliation: (a) California State University Channel Islands, Camarillo, CA, U.S.A. (b) Division of Neurobiology and Center for Insect Science, Arizona Research Laboratories University of Arizona, Tucson, AZ, U.S.A. (c) Department of Entomology, University of Arizona, Tucson, AZ, U.S.A. (d) Ecology and Evolutionary Biology, University of Arizona, Tucson, AZ, U.S.A. Article History: Received 24 December 2009; Revised 9 February 2010; Accepted 16 April 2010 Article Note: (miscellaneous) MS. number: A09-00808R

To authenticate to the full-text of this article, please visit this link: http://dx.doi.org/10.1111/j.1365-2745.2009.01566.x Byline: Judith L. Bronstein (*) Keywords: co-evolution; community; evolution; facilitation; mutualism; plant-plant interactions; positive interactions; specialization Abstract: Summary 1. While the relationship between facilitation and competition has been explored extensively in recent years, there is also a natural link between facilitation and mutualism, as both are interspecific interactions that confer benefits. Yet, the relationship between these two interactions has been minimally explored. 2. Here, I explore parallels and differences between mutualism and facilitation. Five focal areas organize current research on mutualism evolution: trait evolution; the continuum from specialization to generalization; the evolutionary origins and maintenance of the interaction; co-evolution of partners; and the prevalence and implications of cheating. These foci are also helpful for investigating how facilitation evolves, a much less explored issue. 3. Testable hypotheses regarding the evolution of facilitation include the following: selection should be stronger on traits of facilitated species than on traits of facilitators; facilitative interactions with mutualistic (++) and commensal (+0) outcomes should exhibit greater evolutionary stability than those with antagonistic (+-) outcomes; co-evolution should be possible in mutualistic and antagonistic facilitation only; when co-evolution occurs, it should produce a geographic mosaic of interaction outcomes; and antagonistic facilitation could lead to selection on facilitators to either escape or to tolerate the neighbours that benefit from them. 4.Synthesis. Three gaps in our knowledge currently impede progress on evolutionary questions surrounding facilitation. First, reciprocal effects are rarely investigated; facilitation might evolve like mutualism, commensalism or antagonism, depending on effects on the facilitator species. Secondly, the genetics of relevant traits are not yet well explored; the traits themselves are better known for facilitator species than for the facilitated, which are more likely to evolve in the context of the interaction. Finally, the fitness costs and benefits associated with facilitation have rarely been measured. Filling these gaps should permit rapid progress in understanding how facilitation arises, persists and evolves. Article History: Received 12 May 2009; accepted 7 August 2009 Handling Editor: Rob Brooker Article note: (*) Correspondence author. E-mail: judieb@email.arizona.edu

Animal foraging has been characterized as an attempt to maximize the intake of carbon and nitrogen at appropriate ratios. Plant species in over 90 families produce carbohydrate-rich extrafloral nectar (EFN), a resource attractive to ants and other omnivorous insects. This attraction can benefit the plant if those arthropods subsequently attack herbivores. This protective response has been attributed to the increased visitation and 'ownership' of plants that provide a predictable source of fuel. Here, we propose and test an alternative (but non-mutually exclusive) hypothesis, that access to C-rich carbohydrates increases the ants' desire for N-rich protein and hence the likelihood that they will attack herbivorous insects on the host plant. This 'deficit hypothesis' would be rejected if (1) EFN were itself a sufficiently balanced food source in terms of C and N, (2) ant dietary preferences were similar in the presence vs. absence of EFN, (3) protein-hungry ants were not more predaceous, or (4) ants provided access to protein were more aggressive toward potential prey items than were ants provided access to carbohydrates. We test these predictions in a protective mutualism between a guild of desert ants and the barrel cactus Ferocactus wislizeni. C:N ratios of EFN exceeded that of ants or potential prey items by an order of magnitude (i.e., EFN is an N-poor food for ants). Baiting studies demonstrated that plant-tending ant species recruited more workers to N-rich protein baits than to C-rich sugar baits; this difference was more pronounced when the ants had access to F. wislizeni EFN. From these data, we infer that protein is a valuable resource and that its relative value increases when carbohydrates are readily available. Moreover, ant colonies provided access to supplemental carbohydrates responded more aggressively to surrogate herbivores than did control colonies (to which no additional resources were provided) or colonies provided protein. These results support the predictions of the 'deficit' hypothesis, wherein plant protection is elicited by plant-mediated dietary imbalances. Key words: ants; barrel cactus; carbohydrates; C:N ratio; desert ant guild, Desert Laboratory, Tucson, Arizona, USA; extrafloral nectar; Ferocactus wislizeni; foraging; mutualism; rewards.

Spatiotemporal variability in floral resources can have ecological and evolutionary consequences for both plants and the pollinators on which they depend. Seldom, however, can patterns of flower abundance and visitation in the field be linked with the behavioral mechanisms that allow floral visitors to persist when a preferred resource is scarce. To explore these mechanisms better, we examined factors controlling floral preference in the hawkmoth Manduca sexta in the semiarid grassland of Arizona. Here, hawkmoths forage primarily on flowers of the bat-adapted agave, Agave palmeri, but shift to the moth-adapted flowers of their larval host plant, Datura wrightii, when these become abundant. Both plants emit similar concentrations of floral odor, but scent composition, nectar, and flower reflectance are distinct between the two species, and A. palmeri flowers provide six times as much chemical energy as flowers of D. wrightii. Behavioral experiments with both nai've and experienced moths revealed that hawkmoths learn to feed from agave flowers through olfactory conditioning but readily switch to D. wrightii flowers, for which they are the primary pollinator, based on an innate odor preference. Behavioral flexibility and the olfactory contrast between flowers permit the hawkmoths to persist within a dynamic environment, while at the same time to function as the major pollinator of one plant species. flower visitation | foraging behavior | moth | pollination

In generalized, multispecies mutualisms, competition among members of one guild can influence the net benefits that each species in the other guild receives. Hence seasonal factors that affect the dynamics of competition can also affect net benefits, especially if the benefit or cost of mutualism also varies seasonally. In the Sonoran Desert, two common species of generalist ants compete for access to extrafloral nectaries on the fishhook barrel cactus Ferocactus wislizeni, but their relative abundances vary seasonally; one ant dominates more cacti in winter/spring, and the other in summer/autumn. Recently, a third ant species, which also varies in abundance seasonally, has appeared at our study sites and is competing with resident ants for access to cactus nectaries. This empirical system motivated us to examine a metapopulation model of competition for patches in an open system with periodic forcing. We use the model to: (1) illustrate three ways in which competing species may differ in their sensitivities to environmental conditions that are consistent with seasonally displaced patterns of abundance; (2) ask under what conditions the invasion of a third competitor into a two-species system could alter the sensitivity of the system to environmental forcing at low vs. high frequency; and (3) show how differences among competitors in the pattern of seasonal forcing alone can dramatically alter the outcome of a competitor invasion. We discuss implications of these results for the ways in which seasonal variation among competing mutualists, and the benefits and costs of mutualism, may affect the functioning of generalized, facultative mutualisms. Key words: ant-plant mutualism; coherence number; competition; environmental forcing; Ferocactus wislizeni; metapopulation; resonance; seasonality; transfer function.

Traits that are attractive to mutualists may also attract antagonists, resulting in conflicting selection pressures. Here we develop the idea that increased floral nectar production can, in some cases, increase herbivory. In these situations, selection for increased nectar production to attract pollinators may be constrained by a linked cost of herbivore attraction. In support of this hypothesis, we report that experimentally supplementing nectar rewards in Datura stramonium led to increased oviposition by Manduca sexta, a sphingid moth that pollinates flowers, but whose larvae feed on leaf tissue. We speculate that nectar composition may provide information about plant nutritional status of defense that floral visitors could use to make oviposition decisions. Thus, selection by floral visitors and leaf herbivores may be inextricably intertwined, and herbivores may represent a relatively unexplored agent of selection on nectar traits. Key words: Datura stramonium; herbivory; Manduca sexta; mutualista; natural selection; nectar composition; nectar reward; oviposition; pollination.

Mutualisms are of central importance in biological systems. Despite growing attention in recent years, however, few conceptual themes have yet to be identified that span mutualisms differing in natural history. Here I examine the idea that the ecology and evolution of mutualisms are shaped by diverse costs, not only by the benefits they confer. This concept helps link mutualism to antagonisms such as herbivory, predation, and parasitism, interactions defined largely by the existence of costs. I first briefly review the range of costs associated with mutualisms, then describe how one cost, the consumption of seeds by pollinator offspring, was quantified for one fig/pollinator mutualism. I compare this cost to published values for other fig/pollinator mutualisms and for other kinds of pollinating seed parasite mutualisms, notably the yucca/yucca moth interaction. I then discuss four issues that fundamentally complicate comparative studies of the cost of mutualism: problems of knowing how to measure the magnitude of any one cost accurately; problems associated with using average estimates in the absence of data on sources of variation; complications arising from the complex correlates of costs, such as functional linkages between costs and benefits; and problems that arise from considering the cost of mutualism as a unilateral issue in what is fundamentally a reciprocal interaction. The rich diversity of as-yet unaddressed questions surrounding the costs of mutualism may best be investigated via detailed studies of individual interactions.

Larval development of the species-specific pollinators (Agaonidae, Hymenoptera) of the two native Florida fig species is markedly temperature-sensitive. Census data from a site near Miami indicate that Pegoscapus assuetus (the pollinator of Ficus citrifolia) and Pegoscapus jimenezi (the pollinator of Ficus aurea) take 7-8% longer to develop for each 1 C decrease in ambient temperature. However, development does not slow sufficiently to permit the wasps to remain within their sheltered larval habitat (the fig inflorescence) throughout winter, a season in which the short-lived adults have little chance of finding an oviposition site. The difficulty of wasp persistence through winter is probably a major factor limiting most fig-pollinator mutualisms to the tropics. The ability of a few species to persist at the northern limits of some subtropical regions, such as in S Florida, remains unexplained.

The obligate pollinators of figs (Ficus, Moraceae), species-specific agaonid wasps, benefit figs only by transporting pollen between trees; larvae are seed predators. But the high risk of mortality in flight between trees, adult wasps should prefer to pollinate and oviposit within inflorescences (syconia) at the same tree at which they developed. Flowering within individuals is tightly synchronous in most species, while different trees flower out of phase with each other, suggesting that fit phenology has evolved to assure outcrossing. However, some fig species show distinct within-three flowering asynchrony. It has been suggested that such asynchrony is an adaptation by which figs in seasonal environments can reduce pollinator mortality, by permitting wasps to persist on individual trees at times when flight would be impossible. We have evaluated and rejected the validity of this Seasonality Hypothesis for the Florida strangling fig, Ficus aurea, near its northern range limit. Crops of individual trees were most, not least, synchronous during the coldest, driest months of 2 years. Maximum asynchrony occurred in seasons that were probably most favorable for wasp transit between trees. However, temporal overlap of the phenological stages that permit wasps to remain on their natal trees was always very rare, implying that consecutive cohorts of developing syconia may be spaced in time to limit this occurrence. We suggest alternative costs and benefits for these phenological traits, as well as the proximate mechanisms that might produce them.

A combination of PCR and microscopy techniques is employed to explain the characteristics of the olive fly endosymbionts, Candidatus Erwinia dacicola. The migration of the endosymbionts from an intracellular existence to an extracellular existence during the host insect development process is also discussed.

A series of experiments were conducted in Arizona to investigate low fruit-to-flower ratios in senita cacti that rely exclusively on pollinating seed-consumers. It was found that pollinator attraction and pollen dispersal increased with flower number, but fruit set did not, refuting the hypothesis that excess flowers increase fruit set by attracting more pollinators.

The unusual floral phenology of most monoecious figs, related to their highly specialized pollination mutualism with agaonid wasps, combines pronounced dichogamy at the level of inflorescences and individuals with population-level asynchrony in flowering. This floral phenology ensures that outcrossing strongly predominates. Fig populations may thus be expected to possess deleterious recessive alleles that lead to inbreeding depression when selfing does occur. However, whether monoecious figs are self-compatible and whether selfing results in inbreeding depression have never been investigated. Using wasps as 'pollination tools' and exploiting infrequent overlap in male and female phases on the same tree, we conducted controlled selfed and outcrossed pollination experiments in Ficus aurea. Our results show that this species is totally self-compatible. No negative effects of selfing could be demonstrated on syconium retention, number of vacant ovaries, seed set, or seed germination. However, wasp production had a tendency to be higher after self-pollination. While it is possible that inbreeding depression is expressed at later developmental stages, its absence at the early stages we examined is nonetheless surprising for a plant expected to be highly outcrossed. It is likely that selection pressures other than avoidance of inbreeding are responsible for the evolution and maintenance of the unusual floral phenology of figs. Key words: Ficus; Florida; inbreeding depression; mutualism; phenology; pollination; seasonal environment; self-compatibility; selfing.

Abrahamson, Warren G., and Arthur Edward Weis. 1997. Princeton University Press, Princeton, New Jersey. xiii + 456 p. $75.00, £60.00 (cloth), ISBN: 0-691-03733-7 (alk paper); $29.95, £24.95 (paper), ISBN: 0-691-01208-3 [...]

Symbioses are intimate relationships between species that often last for the entire lifetime of both partners. Despite the undeniable importance of symbiotic interactions in natural systems, most ecologists have paid [...]