- Professor, Ecology and Evolutionary Biology
- University Distinguished Professor
- Professor, Entomology / Insect Science - GIDP
- Professor, BIO5 Institute
- Ph.D. Ecology and Evolutionary Biology
- University of Michigan, Ann Arbor, Michigan, United States
- Coevolution and Constraints in a Neotropical Fig-Pollinator Wasp Mutualism
- M.S. Ecology and Evolutionary Biology
- University of Michigan, Ann Arbor, Michigan, United States
- B.A. Independent Studies
- Brown University, Providence, Rhode Island, United States
- SEE ATTACHED LIST
- Winter 2011
Dr. Bronstein’s large, active lab focuses on the ecology and evolution of interspecific interactions, particularly on the poorly-understood, mutually beneficial ones (mutualisms). Using a combination of field observations, experiments, and theory, they are examining how population processes, abiotic conditions, and the community context determine net effects of interactions for the fitness of each participant species. Specific conceptual areas of interest include: (i) conflicts of interest between mutualists and their consequences for the maintenance of beneficial outcomes; (ii) the causes and consequences of "cheating" within mutualism; (iii) context-dependent outcomes in both mutualisms and antagonisms; and (iv) anthropogenic threats to mutualisms. With Matthew Mars, she is currently extending these concepts to explore educational "ecosystems" in the state of Arizona, as well as terrorist networks and how principles of ecosystem organization can be used to disrupt them.
Ecology, Species interactions, Professional skills for graduate students, biology outreach to Tucson K-12 schools.
DissertationECOL 920 (Spring 2019)
DissertationEIS 920 (Spring 2019)
ThesisECOL 910 (Spring 2019)
Directed ResearchECOL 392 (Fall 2018)
Directed ResearchECOL 492 (Fall 2018)
DissertationEIS 920 (Fall 2018)
EcologyECOL 302 (Fall 2018)
Fundament Of EcologyECOL 600B (Fall 2018)
Independent StudyECOL 499 (Fall 2018)
ResearchECOL 900 (Fall 2018)
Rsrch Ecology+EvolutionECOL 610A (Fall 2018)
ThesisECOL 910 (Fall 2018)
ResearchECOL 900 (Summer I 2018)
Directed ResearchECOL 492 (Spring 2018)
DissertationECOL 920 (Spring 2018)
DissertationEIS 920 (Spring 2018)
Honors ThesisECOL 498H (Spring 2018)
Independent StudyECOL 599 (Spring 2018)
Directed ResearchECOL 492 (Fall 2017)
DissertationECOL 920 (Fall 2017)
DissertationEIS 920 (Fall 2017)
EcologyECOL 302 (Fall 2017)
Fundament Of EcologyECOL 600B (Fall 2017)
Honors ThesisECOL 498H (Fall 2017)
Independent StudyECOL 399 (Fall 2017)
Rsrch Ecology+EvolutionECOL 610A (Fall 2017)
ResearchBIOC 900 (Summer I 2017)
Directed ResearchECOL 492 (Spring 2017)
DissertationECOL 920 (Spring 2017)
Honors ThesisECOL 498H (Spring 2017)
Independent StudyECOL 499 (Spring 2017)
ResearchECOL 900 (Spring 2017)
Directed ResearchECOL 392 (Fall 2016)
Directed ResearchNSCS 492 (Fall 2016)
DissertationECOL 920 (Fall 2016)
EcologyECOL 302 (Fall 2016)
Fundament Of EcologyECOL 600B (Fall 2016)
Honors ThesisECOL 498H (Fall 2016)
Independent StudyECOL 499 (Fall 2016)
ResearchECOL 900 (Fall 2016)
Rsrch Ecology+EvolutionECOL 610A (Fall 2016)
- Bronstein, J. (2015). Mutualism. Oxford University Press.More infoEdiror: Bronstein, JL
- Bronstein, J. (2015). The study of mutualism. In Mutualism. Oxford University Press.
- Murray, K. G., & Bronstein, J. (2014). Plant/animal interactions. In The Natural History of a Tropical Cloud Forest, second edition. Oxford University Press.
- Murray, K. G., & Bronstein, J. (2012). Plant/animal interactions. In The Natural History of a Tropical Cloud Forest, second edition. Oxford University Press.
- Bronstein, J. (2011). Antagonisms and mutualisms: interactions among plant/animal interactions. In Plant-Animal Interactions in the Tropics.
- Bronstein, J., Eliyahu, D., McCall, A., Lauck, M., & Trachtenbrodt, A. (2015). Minute pollinators: the role of thrips (Thysanoptera) as pollinators of pointleaf manzanita, Arctostaphylos pungens (Ericaceae). Journal of Pollination Biology, 16, 64-71.
- Bronstein, J., Jones, E., Afkhami, M., Akcay, E., Bshary, R., Frederickson, M., Heath, K., Hoeksema, J., Ness, J., Pankey, S., Porter, S., Sachs, J., Scharnagl, K., & Friesen, M. (2015). Cheaters must prosper: reconciling theoretical and empirical perspectives on cheating in mutualism. Ecology Letters, 18, 1270-1284.
- Kevin, F., Joshua, N., Bronstein, J., & William, M. (2015). The demographic consequences of mutualism: ants increase host plant fruit production but not population growth. Oecologia, 435-446.
- Marazzi, B., Franklin, K., Sommers, P., Lopez, B., Bronstein, J., Bustamante Ortega, E., Burquez, A., Medellin, R., & Aslan, C. (2014). Plant biotic interactions in the Sonoran Desert: Conservation challenges and future directions.. Journal of the Southwest, 457-501.
- Rafferty, N., CaraDonna, P., & Bronstein, J. (2015). Phenological shifts and the fate of mutualisms. Oikos, 124, 14-21.
- Brodie, J., Aslan, C., Rogers, H., Redford, K., Maron, J., Bronstein, J., & Groves, C. (2014). Secondary extinctions of biodiversity. Trends in Ecology and Evolution, 29, 664-672.
- Bronstein, J. L., Armbruster, W. S., & Thompson, J. N. (2014). Understanding evolution and the complexity of species interactions using orchids as a model system. New Phytologist, 202(2), 373-375.
- Chamberlain, S., Rudgers, J., & Bronstein, J. (0). How context-dependent are species interactions?. Ecology Letters.
- Fitzpatrick, G., & Bronstein, J. (2014). Thermal tolerance affects mutualist attendance in an ant-plant mutualism. Oecologia.
- Miranda, V., Navarro, P., Davidowitz, G., Bronstein, J., & Stock, S. (2013). Effect of insect host age and diet on the fitness of the entomopathogenic nematode-bacteria mutualism. Symbiosis, 61, 145-153.More infoDOI: 10.1007/s13199-013-0266-7
- Suni, S., Bronstein, J., & Brosi, B. (2014). Spatial and temporal genetic differentiation among forest fragments for a tropical bee species. Biotropica, 46, 202-209.
- Bronstein, J. L. (2013). Letter from the editor. American Naturalist, 181(1), 1-3.
- Bronstein, J., & Lanan, M. (2013). An ant's eye view of an ant-plant protection mutualism. Oecologia, 172, 779-790.
- Bronstein, J., Rafferty, N., CaraDonna, P., Burkle, L., & Iler, A. (2013). Phenological overlap of interacting species in a changing climate: an assessment of available approaches. Ecology and Evolution. doi:10.1002/ece3.668
- Contreras, H. L., Goyret, J., Arx, M. v., Pierce, C. T., Bronstein, J. L., Raguso, R. A., & Davidowitz, G. (2013). The effect of ambient humidity on the foraging behavior of the hawkmoth Manduca sexta. Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology, 199(11), 1053-1063.More infoPMID: 23756587;Abstract: The foraging decisions of flower-visiting animals are contingent upon the need of an individual to meet both energetic and osmotic demands. Insects can alter their food preferences to prioritize one need over the other, depending on environmental conditions. In this study, preferences in nectar sugar concentrations (0, 12, 24 %) were tested in the hawkmoth Manduca sexta, in response to different levels of ambient humidity (20, 40, 60, and 80 % RH). Moths altered their foraging behavior when placed in low humidity environments by increasing the volume of nectar imbibed and by consuming more dilute nectar. When placed in high humidity environments the total volume imbibed decreased, because moths consumed less from dilute nectars (water and 12 % sucrose). Survivorship was higher with higher humidity. Daily foraging patterns changed with relative humidity (RH): moths maximized their nectar consumption earlier, at lower humidities. Although ambient humidity had an impact on foraging activity, activity levels and nectar preferences, total energy intake was not affected. These results show that foraging decisions made by M. sexta kept under different ambient RH levels allow individuals to meet their osmotic demands while maintaining a constant energy input. © 2013 Springer-Verlag Berlin Heidelberg.
- Fitzpatrick, G., Davidowitz, G., & Bronstein, J. L. (2013). An herbivore's thermal tolerance is higher than that of the ant defenders in a desert protection mutualism. Sociobiology, 60(3), 252-258.More infoAbstract: In North American deserts, many species of cactus attract ants to their extrafloral nectaries; the ants actively defend the food source, and hence the plant, against herbivores. In thermally extreme environments, however, networks of positive and negative interactions like these are likely to be sensitive to the thermal limitations of each of the interacting species. We compared the thermal tolerance of a common phytophagous cactus bug, Narnia pallidicornis (Hemiptera: Coreidae), to that of the ants that defend the cactus Ferocactus wislizeni in the Sonoran Desert, USA. We used flow-through respirometry to experimentally determine the thermal limit of the herbivore and compared this to the thermal limits of the ant defenders, determined previously. In the field, we recorded herbivore frequency (proportion of plants with N. pallidicornis) and abundance (the number of N. pallidicornis per plant) in relation to ambient temperature, ant species presence and identity, and fruit production. We show that N. pallidicornis has a higher thermal tolerance than the four most common ant mutualists, and in the laboratory can survive very high temperatures, up to 43°C. Herbivore frequency and abundance in the field were not related to the daily high temperatures observed. Plants that were not defended by ants were occupied by more N. pallidicornis, although they showed no reduction in fruit set. Therefore, herbivory is likely to continue on fishhook barrel cacti even at high temperatures, especially those temperatures beyond the thermal tolerance of the ant defenders. The consequences of increased herbivory, however, remain unclear. Mutualisms are essential for ecosystem functioning; it is important to understand the thermal sensitivity of these interactions, especially in light of expected increases in global temperature regimes.
- Marazzi, B., Bronstein, J. L., & Koptur, S. (2013). The diversity, ecology and evolution of extrafloral nectaries: Current perspectives and future challenges. Annals of Botany, 111(6), 1243-1250.More infoPMID: 23704115;PMCID: PMC3662527;Abstract: BackgroundPlants in over one hundred families in habitats worldwide bear extrafloral nectaries (EFNs). EFNs display a remarkable diversity of evolutionary origins, as well as diverse morphology and location on the plant. They secrete extrafloral nectar, a carbohydrate-rich food that attracts ants and other arthropods, many of which protect the plant in return. By fostering ecologically important protective mutualisms, EFNs play a significant role in structuring both plant and animal communities. And yet researchers are only now beginning to appreciate their importance and the range of ecological, evolutionary and morphological diversity that EFNs exhibit.ScopeThis Highlight features a series of papers that illustrate some of the newest directions in the study of EFNs. Here, we introduce this set of papers by providing an overview of current understanding and new insights on EFN diversity, ecology and evolution. We highlight major gaps in our current knowledge, and outline future research directions. Conclusions Our understanding of the roles EFNs play in plant biology is being revolutionized with the use of new tools from developmental biology and genomics, new modes of analysis allowing hypothesis-testing in large-scale phylogenetic frameworks, and new levels of inquiry extending to community-scale interaction networks. But many central questions remain unanswered; indeed, many have not yet been asked. Thus, the EFN puzzle remains an intriguing challenge for the future. © 2013 The Author. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved.
- Marazzi, B., Conti, E., Sanderson, M. J., McMahon, M. M., & Bronstein, J. -. (2013). Diversity and evolution of a trait mediating ant-plant interactions: Insights from extrafloral nectaries in Senna (Leguminosae). Annals of Botany, 111, 1263–1275.
- Barron-Gafford, G., Rascher, U., Bronstein, J., Davidowitz, G., Chaszar, B., & Huxman, T. (2012). Herbivory of wild Manduca sexta causes fast down-regulation of photosynthetic efficiency in Datura wrightii: an early signaling cascade visualized by chlorophyll fluorescence. Photosynthesis Research, 113, 249-260.
- Boyle, W. A., & Bronstein, J. L. (2012). Phenology of tropical understory trees: Patterns and correlates. Revista de Biologia Tropical, 60(4), 1415-1429.More infoPMID: 23342499;Abstract: Reproductive phenologies of plants are constrained by climate in highly seasonal regions. In contrast, plants growing in wet tropical forests are freed from many abiotic constraints, which in canopy tree communities lead to a rich diversity of phenological patterns within and among individuals, species and communities. However, basic descriptions of tropical phenological patterns and the processes that shape them are rare. Here, we document the individual-, population-, and landscape-level phenological patterns of two dominant families of understory woody plants important to avian frugivores, the Melastomataceae and Rubiaceae, along an elevational transect in Costa Rica. The 226 individual plants belonging to 35 species in this study, varied in the number of reproductive bouts/year, and the timing, duration, and synchrony of reproductive stages. This variation was not related to factors related to their interactions with mutualists and antagonists, nor did it appear to be constrained by phylogeny. Diverse phenological patterns among species led to relatively aseasonal patterns at the community and landscape level. Overall, evidence for biotic processes shaping temporal patterns of fruiting phenology was weak or absent. These findings reveal a number of unexplained patterns, and suggest that factors shaping phenology in relatively aseasonal forests operate in idiosyncratic ways at the species level.
- Bronstein, J., & Barker, J. (2015). Temporal structure in cooperative interactions: what does the timing of exploitation tell us about its cost?. PLoS Biology.
- Bronstein, J., Aslan, C., Rogers, H., Gedan, K., Brodie, J., Palmer, T., & Young, T. (2015). Leveraging nature's backup plans to incorporate species interactions and resilience into restoration. Restoration Ecology.
- Bronstein, J., Franklin, K., Sommers, P., Aslan, C., Lopez, B., Bustamante, E., Burquez, A., Medellin, R., & Marazzi, B. (2015). Plant biotic interactions in the Sonoran Desert: Current knowledge and future research perspectives. International Journal of Plant Sciences.
- Bronstein, J., Lanan, M. C., Dornhaus, A., Jones, E. I., Waser, A., & Bronstein, J. -. (2012). The trail less traveled: individual decision-making and its effect on group behavior. PloS one, 7(10).More infoSocial insect colonies are complex systems in which the interactions of many individuals lead to colony-level collective behaviors such as foraging. However, the emergent properties of collective behaviors may not necessarily be adaptive. Here, we examine symmetry breaking, an emergent pattern exhibited by some social insects that can lead colonies to focus their foraging effort on only one of several available food patches. Symmetry breaking has been reported to occur in several ant species. However, it is not clear whether it arises as an unavoidable epiphenomenon of pheromone recruitment, or whether it is an adaptive behavior that can be controlled through modification of the individual behavior of workers. In this paper, we used a simulation model to test how symmetry breaking is affected by the degree of non-linearity of recruitment, the specific mechanism used by individuals to choose between patches, patch size, and forager number. The model shows that foraging intensity on different trails becomes increasingly asymmetric as the recruitment response of individuals varies from linear to highly non-linear, supporting the predictions of previous work. Surprisingly, we also found that the direction of the relationship between forager number (i.e., colony size) and asymmetry varied depending on the specific details of the decision rule used by individuals. Limiting the size of the resource produced a damping effect on asymmetry, but only at high forager numbers. Variation in the rule used by individual ants to choose trails is a likely mechanism that could cause variation among the foraging behaviors of species, and is a behavior upon which selection could act.
- Bronstein, J., Rafferty, N., & Bertelson, D. (2015). Later flowering is associated with a compressed flowering season and reduced reproductive output in an early season floral resource. Oikos.
- Bronstein, J., Whitlock, M., Bruna, E., Ellison, A., Fox, C., McPeek, M., Moore, A., Noor, M., Rausher, M., Riesberg, L., Ritchie, M., & Shaw, R. (2015). A balanced data archiving policy for long-term studies. Trends in Ecology and Evolution.
- Jones, E. I., Bronstein, J. L., & Ferrière, R. (2012). The fundamental role of competition in the ecology and evolution of mutualisms. Annals of the New York Academy of Sciences, 1256(1), 66-88.More infoPMID: 22583047;Abstract: Mutualisms are interspecific interactions that yield reciprocal benefits. Here, by adopting a consumer-resource perspective, we show how considering competition is necessary in order to understand the evolutionary and ecological dynamics of mutualism. We first review the ways in which competition shapes the ecology of mutualisms, using a graphical framework based on resource flows rather than net effects to highlight the opportunities for competition. We then describe the known mechanisms of competition and show how it is a critical driver of the evolutionary dynamics, persistence, and diversification of mutualism. We argue that empirical and theoretical research on the ecology and evolution of mutualisms will jointly progress by addressing four key points: (i) the existence and shape of physiological trade-offs among cooperation, competition, and other life-history and functional traits; (ii) the capacity for individuals to express conditional responses to variation in their mutualistic and competitive environment; (iii) the existence of heritable variation for mutualistic and competitive traits and their potentially conditional expression; and (iv) the structure of the network of consumer-resource interactions in which individuals are embedded. © 2012 New York Academy of Sciences.
- Mars, M. M., Bronstein, J. L., & Lusch, R. F. (2012). The value of a metaphor: Organizations and ecosystems. Organizational Dynamics, 41(4), 271-280.
- Richardson, L., & Bronstein, J. (2012). Reproductive biology of pointleaf manzanita (Arctostaphylos pungens) and the pollinator-nectar robber spectrum. Journal of Pollination Ecology, 9, 115-123.
- Boyle, W., Conway, C., & Bronstein, J. (2011). Why do some, but not all, tropical birds migrate? A comparative study of diet breadth and fruit preference. Evolutionary Ecology, 25, 219-236.
- Bshary, R., & Bronstein, J. (2011). A general scheme to predict partner control mechanisms in pairwise cooperative interactions between unrelated individuals. Ethology, 117, 271-283.
- Lanan, M. C., Dornhaus, A., & Bronstein, J. L. (2011). The function of polydomy: The ant Crematogaster torosa preferentially forms new nests near food sources and fortifies outstations. Behavioral Ecology and Sociobiology, 65(5), 959-968.More infoAbstract: Many ant species are polydomous, forming multiple spatially segregated nests that exchange workers and brood. However, why polydomy occurs is still uncertain. We investigated whether colonies of Crematogaster torosa form new polydomous nests to better exploit temporally stable food resources. Specifically, we tested the effect of food presence or absence and distance on the likelihood that colonies would form a new nest. Because this species also forms little-known structures that house only workers without brood (outstations), we also compared the function of this structure with true nests. Laboratory-reared colonies were connected to a new foraging arena containing potential nest sites with or without food for 4 months. When food was present, most colonies formed polydomous nests nearby and the remainder formed outstations. When food was absent, the behavior of colonies differed significantly, frequently forming outstations but never polydomous nests. Distance had no effect on the type of structure formed, but when food was present, a larger proportion of the workforce moved shorter distances. Workers often fortified the entrances to both structures and used them for storage of dried insect tissue ("jerky"). In an investigation of spatial fidelity, we found that workers on the between-nest trail were associated with the original nest, whereas workers collecting food were more likely to be associated with the new nest or outstation. C. torosa appears to have a flexible colony structure, forming both outstations and polydomous nests. Polydomous nests in this species were associated with foraging and were only formed near food resources. © 2010 Springer-Verlag.
- Alarcon, R., Riffell, J. A., Davidowitz, G. -., Hildebrand, J. G., & Bronstein, J. -. (2010). Sex-dependent variation in the floral preferences of the hawkmoth Manduca sexta. Animal Behavior, 80, 289-296.
- Irwin, R. E., Bronstein, J. L., Manson, J. S., & Richardson, L. (2010). Nectar robbing: Ecological and evolutionary perspectives. Annual Review of Ecology, Evolution, and Systematics, 41, 271-292.More infoAbstract: Not all floral visitors attracted to flowers are pollinators. Instead, some visitors circumvent the floral opening, usually removing nectar without contacting the anthers andor stigma. Here we review the evolutionary ecology of nectar robbing from both the plant and animal perspective. Effects of robbing on female and male components of plant reproduction range from negative to positive. Their underlying mechanisms are diverse, including direct effects and indirect effects mediated through changes in pollination. We detail how plants may be able to deter robbers through morphological and chemical traits. For the evolutionary ecology of robbing to move beyond a phytocentric perspective, studies must also address the causes of robbing and the consequences for both robbers and pollinators. We use an energetics approach to evaluate these causes and consequences. Finally, we highlight unanswered questions in need of further research. Copyright © 2010 by Annual Reviews. All rights reserved.
- Kiers, E. T., Palmer, T. M., Ives, A. R., Bruno, J. F., & Bronstein, J. L. (2010). Mutualisms in a changing world: An evolutionary perspective. Ecology Letters, 13(12), 1459-1474.More infoPMID: 20955506;Abstract: There is growing concern that rapid environmental degradation threatens mutualistic interactions. Because mutualisms can bind species to a common fate, mutualism breakdown has the potential to expand and accelerate effects of global change on biodiversity loss and ecosystem disruption. The current focus on the ecological dynamics of mutualism under global change has skirted fundamental evolutionary issues. Here, we develop an evolutionary perspective on mutualism breakdown to complement the ecological perspective, by focusing on three processes: (1) shifts from mutualism to antagonism, (2) switches to novel partners and (3) mutualism abandonment. We then identify the evolutionary factors that may make particular classes of mutualisms especially susceptible or resistant to breakdown and discuss how communities harbouring mutualisms may be affected by these evolutionary responses. We propose a template for evolutionary research on mutualism resilience and identify conservation approaches that may help conserve targeted mutualisms in the face of environmental change. © 2010 Blackwell Publishing Ltd/CNRS.
- Palmer, T. M., Doak, D. F., Stanton, M. L., Bronstein, J. L., Kiers, E. T., Young, T. P., Goheen, J. R., & Pringle, R. M. (2010). Synergy of multiple partners, including freeloaders, increases host fitness in a multispecies mutualism. Proceedings of the National Academy of Sciences of the United States of America, 107(40), 17234-17239.More infoPMID: 20855614;PMCID: PMC2951420;Abstract: Understanding cooperation is a central challenge in biology, because natural selectionshouldfavor "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.
- Bronstein, J. L. (2009). The evolution of facilitation and mutualism. Journal of Ecology, 97(6), 1160-1170.More infoAbstract: 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. © 2009 British Ecological Society.
- Bronstein, J. L., Huxman, T., Horvath, B., Farabee, M., & Davidowitz, G. (2009). Reproductive biology of Datura wrightii: the benefits of a herbivorous pollinator.. Annals of botany, 103(9), 1435-1443.More infoPMID: 19287014;PMCID: PMC2701751;Abstract: BACKGROUND AND AIMS: A deeper understanding of mutualism can be reached by studying systems with measurable costs and benefits. Most studies of this type focus on an unusual class of obligate, species-specific pollination mutualisms. The interaction between Datura wrightii (Solanaceae) and the hawkmoth Manduca sexta offers similar advantages but greater generality. Adult moths both nectar at and deposit eggs on the same plant; larvae are herbivorous. The antagonistic component of this interaction has been well studied. Here the role of M. sexta as a pollinator of D. wrightii, particularly in the context of this moth's frequent nectaring visits to the bat-pollinated plant Agave palmeri, is documented. METHODS: Hand-pollinations were used to determine breeding system and the reproductive consequences of mixed loads of A. palmeri and D. wrightii pollen. Plants and moths were caged overnight to assess whether nectaring visits led to fruit and seed set. Finally, pollen deposited on field-collected stigmas was identified, with a particular focus on documenting the presence of D. wrightii and A. palmeri grains. KEY RESULTS: Datura wrightii is highly self-compatible, and a visit that deposits either outcross or self pollen almost doubles fruit and seed set compared with unvisited flowers. Manduca sexta transferred enough pollen to produce fruit and seed sets comparable to hand-pollination treatments. Agave palmeri did not interfere with D. wrightii success: in the field, stigmas received almost pure D. wrightii pollen, and hand-addition of large quantities of A. palmeri pollen had no measurable effect on fruit and seed set. CONCLUSIONS: The floral visitation component of the D. wrightii-M. sexta interaction is indeed mutualistic. This finding is essential background to future development of this interaction as a model system for studying mutualism's costs and benefits. It is already proving valuable for dissecting third-species effects on the outcome of mutualism. Results indicate that M. sexta's heavy visitation to A. palmeri has no negative effect on the benefits conferred to D. wrightii. However, it can be predicted to augment M. sexta populations to the point where the costs of the interaction begin to exceed its benefits.
- Estes, A. M., Hearn, D. J., Bronstein, J. L., & Pierson, E. A. (2009). The olive fly endosymbiont, "Candidatus Erwinia dacicola," switches from an intracellular existence to an extracellular existence during host insect development. Applied and Environmental Microbiology, 75(22), 7097-7106.More infoPMID: 19767463;PMCID: PMC2786516;Abstract: As polyphagous, holometabolous insects, tephritid fruit flies (Diptera: Tephritidae) provide a unique habitat for endosymbiotic bacteria, especially those microbes associated with the digestive system. Here we examine the endosymbiont of the olive fly [Bactrocera oleae (Rossi) (Diptera: Tephritidae)], a tephritid of great economic importance. "Candidatus Erwinia dacicola" was found in the digestive systems of all life stages of wild olive flies from the southwestern United States. PCR and microscopy demonstrated that "Ca. Erwinia dacicola" resided intracellularly in the gastric ceca of the larval midgut but extracellularly in the lumen of the foregut and ovipositor diverticulum of adult flies. "Ca. Erwinia dacicola" is one of the few nonpathogenic endosymbionts that transitions between intracellular and extracellular lifestyles during specific stages of the host's life cycle. Another unique feature of the olive fly endosymbiont is that unlike obligate endosymbionts of monophagous insects, "Ca. Erwinia dacicola" has a G+C nucleotide composition similar to those of closely related plantpathogenic and free-living bacteria. These two characteristics of "Ca. Erwinia dacicola," the ability to transition between intracellular and extracellular lifestyles and a G+C nucleotide composition similar to those of free-living relatives, may facilitate survival in a changing environment during the development of a polyphagous, holometabolous host. We propose that insect-bacterial symbioses should be classified based on the environment that the host provides to the endosymbiont (the endosymbiont environment). Copyright © 2009, American Society for Microbiology. All Rights Reserved.
- Jones, E. I., Ferrìre, R., & Bronstein, J. L. (2009). Eco-evolutionary dynamics of mutualists and exploiters. American Naturalist, 174(6), 780-794.More infoPMID: 19845459;Abstract: With the growing recognition of exploiters as a prominent and enduring feature of many mutualisms, there is a need to understand the ecological and evolutionary dynamics of mutualisms in the context of exploitation. Here, we model coevolution between mutualist and exploiter birth rates, using an obligate pollinating seed parasite mutualism associated with a nonpollinating exploiter as a reference system. In this system, mutualist and exploiter larvae parasitize the host plant, competing for and consuming seeds. Evolution of the mutualist determines which exploiters can invade successfully. Subsequent coevolution with an exploiter has a strong, predictable influence on mutualist-exploiter coexistence, mutualist and exploiter phenotypes, and species abundances. Weak mutualist competition promotes "evolutionary purging" of the exploiter, while weak exploiter competition leads to "evolutionary suicide" of the system. When stable, long-term coexistence occurs, we identify two main "trait-abundance syndromes" that have three novel implications. (1) Persistent, highly parasitic exploiters can be favored by coevolution. (2) Even then, the density of coevolved mutualists can be high. (3) Low plant density results primarily from the evolution of mutualist, not exploiter, birth rate and density. To evaluate these predictions, studies are needed that identify and compare populations with and without exploiters and compare life-history traits of mutualists and exploiters. © 2009 by The University of Chicago.
- Ness, J. H., Morris, W. F., & Bronstein, J. L. (2009). For ant-protected plants, the best defense is a hungry offense. Ecology, 90(10), 2823-2831.More infoPMID: 19886490;Abstract: 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. © 2009 by the Ecological Society of America.
- Alarcón, R., Davidowitz, G., & Bronstein, J. L. (2008). Nectar usage in a southern Arizona hawkmoth community. Ecological Entomology, 33(4), 503-509.More infoAbstract: 1. Hawkmoths (Sphingidae) are important plant associates at two lifehistory stages: larvae are herbivorous, whereas adults are nectar feeders and often pollinators. The diversity and identities of plants used for nectar is poorly known, however. 2. This study takes a community-level approach to hawkmoth nectar plant usage in a semi-arid grassland habitat in southern Arizona, U.S.A. 3. Pollen carried on the proboscis was identified from over 700 individuals of 14 hawkmoth species attracted to lights over a 2-year period. 4. Two plant species dominated pollen loads, suggesting that hawkmoths use these species extensively as nectar sources: Datura wrightii (Solanaceae), a classic hawkmothpollinated plant, and Agave palmeri (Agavaceae), which is known to be used extensively by bats. Field surveys indicate that both species are relatively rare in the flowering community. Little or no pollen was present on the moths from the most common plant species in flower during the study. 5. The dominance of Agave in pollen loads suggests that this typically bat-pollinated species may be subsidising pollinator populations of the hawkmoth-pollinated flora. 6. Three groups of hawkmoths within this community are identified based on larval diets (reported in the literature) and adult diets (documented here): those that, at a given site, heavily exploit the same plant species at both life-history stages (Manduca sexta and M. quinquemaculata); those that have broad local associations at both life-history stages (Hyles lineata); and those that exhibit narrow but non-overlapping local associations at the two life-history stages (all other hawkmoths at this site). © 2008 The Royal Entomological Society.
- Bronstein, J. L., Izhaki, I., Nathan, R., Tewksbury, J. J., Spiegel, O., Lotan, A., & Altstein, O. (2007). Fleshy-fruited plants and frugivores in desert ecosystems. Seed Dispersal: Theory and its Application in a Changing World, 148-177.
- Ferrière, R., Gauduchon, M., & Bronstein, J. L. (2007). Evolution and persistence of obligate mutualists and exploiters: Competition for partners and evolutionary immunization. Ecology Letters, 10(2), 115-126.More infoPMID: 17257099;Abstract: Mutualisms are ubiquitous in nature, as is their exploitation by both conspecific and heterospecific cheaters. Yet, evolutionary theory predicts that cheating should be favoured by natural selection. Here, we show theoretically that asymmetrical competition for partners generally determines the evolutionary fate of obligate mutualisms facing exploitation by third-species invaders. When asymmetry in partner competition is relatively weak, mutualists may either exclude exploiters or coexist with them, in which case their co-evolutionary response to exploitation is usually benign. When asymmetry is strong, the mutualists evolve towards evolutionary attractors where they become extremely vulnerable to exploiter invasion. However, exploiter invasion at an early stage of the mutualism's history can deflect mutualists' co-evolutionary trajectories towards slightly different attractors that confer long-term stability against further exploitation. Thus, coexistence of mutualists and exploiters may often involve an historical effect whereby exploiters are co-opted early in mutualism history and provide lasting 'evolutionary immunization' against further invasion. © 2007 Blackwell Publishing Ltd/CNRS.
- Bronstein, J. L., Alarcón, R., & Geber, M. (2006). The evolution of plant-insect mutualisms. New Phytologist, 172(3), 412-428.More infoPMID: 17083673;Abstract: Mutualisms (cooperative interactions between species) have had a central role in the generation and maintenance of life on earth. Insects and plants are involved in diverse forms of mutualism. Here we review evolutionary features of three prominent insect-plant mutualisms: pollination, protection and seed dispersal. We focus on addressing five central phenomena: evolutionary origins and maintenance of mutualism; the evolution of mutualistic traits; the evolution of specialization and generalization; coevolutionary processes; and the existence of cheating. Several features uniting very diverse insect-plant mutualisms are identified and their evolutionary implications are discussed: the involvement of one mobile and one sedentary partner; natural selection on plant rewards; the existence of a continuum from specialization to generalization; and the ubiquity of cheating, particularly on the part of insects. Plant-insect mutualisms have apparently both arisen and been lost repeatedly. Many adaptive hypotheses have been proposed to explain these transitions, and it is unlikely that any one of them dominates across interactions differing so widely in natural history. Evolutionary theory has a potentially important, but as yet largely unfilled, role to play in explaining the origins, maintenance, breakdown and evolution of insect-plant mutualisms. © The Authors (2006).
- Ness, J. H., Morris, W. F., & Bronstein, J. L. (2006). Integrating quality and quantity of mutualistic service to contrast ant species protecting Ferocactus wislizeni. Ecology, 87(4), 912-921.More infoPMID: 16676535;Abstract: Generalized, facultative mutualisms are often characterized by great variation in the benefits provided by different partner species. This variation may be due to differences among species in the quality and quantity of their interactions, as well as their phenology. Many plant species produce extrafloral nectar, a carbohydrate-rich resource, to attract ant species that can act as "bodyguards" against a plant's natural enemies. Here, we explore differences in the quality and quantity of protective service that ants can provide a plant by contrasting the four most common ant visitors to Ferocactus wislizeni, an extrafloral nectary-bearing cactus in southern Arizona. The four species differ in abundance when tending plants, and in the frequency at which they visit plants. By adding surrogate herbivores (Manduca sexta caterpillars) to plants, we demonstrate that all four species recruit to and attack potential herbivores. However, their per capita effectiveness in deterring herbivores (measured as the inverse of the number of workers needed to remove half of the experimentally added caterpillars) differs. Using these among-species differences in quality (per capita effectiveness) and quantity (number of workers that visit a plant and frequency of visitation), we accurately predicted the variation in fruit production among plants with different histories of ant tending. We found that plant benefits (herbivore removal and maturation of buds and fruits) typically saturated at high levels of ant protection, although plants could be "well defended" via different combinations of interaction frequency, numbers of ant workers per interaction, and per capita effects. Our study documents variation among prospective mutualists, distinguishes the components of this variation, and integrates these components into a predictive measure of protection benefit to the plant. The method we used to average saturating benefits over time could prove useful for quantifying overall service in other mutualisms. © 2006 by the Ecological Society of America.
- Kjellberg, F., Bronstein, J. L., Ginkel, G. v., Greeff, J. M., Moore, J. C., Bossu-Dupriez, N., Chevolot, M., & Michaloud, G. (2005). Clutch size: A major sex ratio determinant in fig pollinating wasps?. Comptes Rendus - Biologies, 328(5), 471-476.More infoPMID: 15948636;Abstract: Under local mate competition, sex ratio theory predicts that increasing numbers of ovipositing females (foundresses) on a site should lead to higher proportions of males in their broods. Fig pollinators have confirmed this prediction. It is also predicted that with decreasing clutch size, solitary foundresses should produce increasing proportions of sons. We show this to be true. Further, when several females compete, brood size decreases. As a result, the proportion of males increases, and this could provide a mechanistic explanation of sex ratio response to numbers of colonizing females. Therefore, sex ratio data on fig wasps need to be reassessed to determine whether females 'count' other foundresses, as is generally accepted, or whether they simply 'count' the number of eggs that they lay. © 2005 Académie des sciences. Published by Elsevier SAS. All rights reserved.
- Morris, W. F., Wilson, W. G., Bronstein, J. L., & Ness, J. H. (2005). Environmental forcing and the competitive dynamics of a guild of cactus-tending ant mutualists. Ecology, 86(12), 3190-3199.More infoAbstract: 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. © 2005 by the Ecological Society of America.
- Adler, L. S., & Bronstein, J. L. (2004). Attracting antagonists: Does floral nectar increase leaf herbivory?. Ecology, 85(6), 1519-1526.More infoAbstract: 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 or 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.
- Bshary, R., & Bronstein, J. L. (2004). Game Structures in Mutualistic Interactions: What Can the Evidence Tell Us About the Kind of Models We Need?. Advances in the Study of Behavior, 34, 59-101.More infoAbstract: Currently, there is little information transfer between empiricists working on cooperative interactions between species (mutualism) and theoreticians who model possible scenarios for the evolution and maintenance of cooperation between unrelated individuals. Furthermore, both theoretical and behavioral approaches often fail to consider ecological parameters that influence behavior. Our goal is to present the wealth of empirical knowledge (both behavioral and ecological) on mutualistic systems in a structure that may facilitate communication between empiricists and theoreticians. We have chosen eight broad categories of mutualisms that have been intensely studied and that are relatively well understood. For each system, we assess possible states of 12 parameters that can help theoreticians to construct game structures of mutualisms that are built on current empirical knowledge. We point out how ecological variables may influence behavioral decisions in ways not identified by our parameters. Finally, we elucidate similarities between mutualistic systems with respect to game structures that may not be expected given the diversity of mutualisms with respect to ecological and evolutionary background. On the basis of these results, we promote an interactive approach with models based on empirical knowledge, amenable to further testing. © 2004 Elsevier Inc. All rights reserved.
- Holland, J. N., Bronstein, J. L., & DeAngelis, D. L. (2004). Testing hypotheses for excess flower production and low fruit-to-flower ratios in a pollinating seed-consuming mutualism. Oikos, 105(3), 633-640.More infoAbstract: Pollinator attraction, pollen limitation, resource limitation, pollen donation and selective fruit abortion have all been proposed as processes explaining why hermaphroditic plants commonly produce many more flowers than mature fruit. We conducted a series of experiments in Arizona to investigate low fruit-to-flower ratios in senita cacti, which rely exclusively on pollinating seed-consumers. Selective abortion of fruit based on seed predators is of particular interest in this case because plants relying on pollinating seed-consumers are predicted to have such a mechanism to minimize seed loss. 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. Fruit set of natural- and hand-pollinated flowers were not different, supporting the resource, rather than pollen, limitation hypothesis. Senita did abort fruit, but not selectively based on pollen quantity, pollen donors, or seed predators. Collectively, these results are consistent with sex allocation theory in that resource allocation to excess flower production can increase pollen dispersal and the male fitness function of flowers, but consequently results in reduced resources available for fruit set. Inconsistent with sex allocation theory, however, fruit production and the female fitness function of flowers may actually increase with flower production. This is because excess flower production lowers pollinator-to-flower ratios and results in fruit abortion, both of which limit the abundance and hence oviposition rates, of pre-dispersal seed predators.
- Ness, J. H., & Bronstein, J. L. (2004). The effects of invasive ants on prospective ant mutualists. Biological Invasions, 6(4), 445-461.More infoAbstract: Ants are recognized for their abilities both to engage in mutualistic interactions with diverse taxa, and to invade and dominate habitats outside their native geographic range. Here, we review the effects of invasive ants on three guilds of mutualists: ant-dispersed plants, ant-tended arthropods, and ant-tended plants. We contrast how those three guilds are affected by invasions, how invasive ants differ from native ants in their interactions with those guilds, and how the seven most invasive ant species differ amongst themselves in those interactions. Ant-dispersed plants typically suffer from interactions with invasive ants, a result we attribute to the small size of those ants relative to native seed-dispersing ants. Effects on the ant-tended arthropods and plants were more frequently positive or non-significant, although it is unclear how often these interactions are reciprocally beneficial. For example, invasive ants frequently attack the natural enemies of these prospective mutualists even in the absence of rewards, and may attack those prospective mutualists. Many studies address whether invasive ants provide some benefit to the partner, but few have asked how invasives rank within a hierarchy of prospective mutualists that includes other ant species. Because ant invasions typically result in the extirpation of native ants, this distinction is highly relevant to predicting and managing the effects of such invasions. Interspecific comparisons suggest that invasive ants are poorer partners of ant-dispersed plants than are most other ants, equally effective partners of ant-tended arthropods, and perhaps better partners of ant-tended plants. Last, we note that the invasive ant taxa differ amongst themselves in how they affect these three mutualist guilds, and in how frequently their interactions with prospective mutualists have been studied. The red imported fire ant, Solenopsis invicta, appears particularly likely to disrupt all three mutualistic interactions, relative to the other six invasive species included in this review.
- Ness, J. H., Bronstein, J. L., Andersen, A. N., & Holland, J. N. (2004). Ant body size predicts dispersal distance of ant-adapted seeds: Implications of small-ant invasions. Ecology, 85(5), 1244-1250.More infoAbstract: The services provided within a community can change as the species composition of that community changes. For example, ant-seed dispersal mutualisms can be disrupted in habitats dominated by invasive ants. We propose that this disruption is related to changes in mean ant body size, given that invasive ants are smaller than most native seed-dispersing ants. We demonstrate that the mean and maximum distances that ants transport seeds adapted for ant dispersal increase with worker body size, and that this relationship is an accelerating power function. This pattern is consistent among three ant subfamilies that include most seed-dispersing ants as well as most invasive ant species, is generalizable across ant species and communities, and is independent of diaspore mass. Using a case study, we demonstrate that both the mean body size of seed-collecting ants and seed dispersal distances are decreased in sites invaded by Solenopsis invicta, the imported red fire ant. Furthermore, we demonstrate that the mean size of seed-collecting ants at a seed depot or within a community is a useful predictor of mean seed dispersal distances at those sites. Last, we show that small seed-collecting ants and decreased seed dispersal distances are common features of sites occupied by invasive ants. The link between ant body size and seed dispersal distance, combined with the dominance of invaded communities by typically small ants, predicts the disruption of native ant-seed dispersal mutualisms in invaded habitats.
- Bronstein, J. L., Wilson, W. G., & Morris, W. F. (2003). Ecological Dynamics of Mutualist/Antagonist Communities. American Naturalist, 162(4 SUPPL.), S24-S39.More infoPMID: 14583855;Abstract: One approach to understanding how mutualisms function in community settings is to model well-studied pairwise interactions in the presence of the few species with which they interact most strongly. In nature, such species are often specialized antagonists of one or both mutualists. Hence, these models can also shed light on the problem of when and how mutualisms are able to persist in the face of exploitation. We used spatial stochastic simulations to model the ecological dynamics of obligate, species-specific mutualisms between plants and pollinating seed parasite insects (e.g., yuccas and yucca moths) in the presence of one of two obligate antagonist species: flower-feeding insects (florivores) or insects that parasitize seeds but fail to pollinate (exploiters). Our results suggest that mutualisms can persist surprisingly well in the presence of highly specialized antagonists but that they exhibit distinctly different temporal and spatial dynamics when antagonists are present. In our models, antagonists tend to induce oscillations in the mutualist populations. As the number of per capita visits by antagonists increase, the system's oscillatory dynamics become more extreme, finally leading to the extinction of one or more of the three species. When the antagonists exhibit high per capita visitation frequencies and long dispersal distances, significant spatial patchiness emerges within these tripartite interactions. We found surprisingly little difference between the ecological effects of florivores and exploiters, although in general florivores tended to drive themselves (and sometimes the mutualists) to extinction at parameter values at which the exploiters were able to persist. These theoretical results suggest several testable hypotheses regarding the ecological and evolutionary persistence of mutualisms. More broadly, they point to the critical importance of studying the dynamics of pairwise interactions in community contexts.
- Morris, W. F., Bronstein, J. L., & Wilson, W. G. (2003). Three-way coexistence in obligate mutualist-exploiter interactions: The potential role of competition. American Naturalist, 161(6), 860-875.More infoPMID: 12858272;Abstract: Many mutualisms host "exploiter" species that consume the benefits provided by one or both mutualists without reciprocating. Exploiters have been widely assumed to destabilize mutualisms, yet they are common. We develop models to explore conditions for local coexistence of obligate plant/pollinating seed parasite mutualisms and nonpollinating exploiters. As the larvae of both pollinators and (at a later time) exploiters consume seeds, we examine the importance of intraspecific and (asymmetric) interspecific competition among and between pollinators and exploiters for achieving three-way coexistence. With weak intra- and interspecific competition, exploiters can invade the stable mutualism and coexist with the mutualists (either stably or with oscillations), provided the exploiters' intrinsic birthrate (bE) slightly exceeds that of the pollinators. At higher bE, all three species go locally extinct. When facing strong interspecific competition, exploiters cannot invade and coexist with the mutualists if intraspecific competition in pollinators and exploiters is weak. However, strong intraspecific competition in pollinators and exploiters facilitates exploiter invasion and coexistence and greatly expands the range of bE over which stable coexistence occurs. Our results suggest that mutualist/exploiter coexistence may be more easily achieved than previously thought, thus highlighting the need for a better understanding of competition among and between mutualists and exploiters.
- Wilson, W. G., Morris, W. F., & Bronstein, J. L. (2003). Coexistence of mutualists and exploiters on spatial landscapes. Ecological Monographs, 73(3), 397-413.More infoAbstract: Mutualisms are almost ubiquitously exploited by species that gain the benefits that mutualists offer to each other, but that offer nothing in return. This paper investigates the possible dynamical outcomes of a mechanistically formulated model system, involving two obligate mutualists and one exploiter. The model is based conceptually on a mutualism between a plant species and its pollinating seed parasite, in the presence of an obligate, nonpollinating seed parasite. Of particular interest are the conditions under which the exploiter species can invade and coexist with a mutualism that, by itself, possesses an equilibrium stabilized by other density-dependent regulating factors. Two types of models are used in the analyses: a deterministic, nonspatial model described by a set of discrete time equations, and an individual-based simulation incorporating stochastic interactions and spatial structure. Comparing the results of these two models uncovers the temporal dynamics of both well-mixed local systems and spatially distributed populations. Using these two situations, we examine how the predictions of the nonspatial model are affected by habitat structure. In the nonspatial case, and without the exploiters, there are typically two stable equilibria: one having zero densities for both mutualist species, and the other having nonzero densities. This bi-stability is a characteristic feature of obligate mutualisms. When the exploiter species is included, the system always retains the stability of the zero-density equilibrium, but the dynamics of the upper equilibrium can be more complicated, including limit cycle and extinction dynamics. Simulation results demonstrate that spatial structure is a highly stabilizing influence on the three-species system as long as the exploiter's dispersal distance is large relative to the seed dispersal distance of the plant species. Given this condition, the model predicts spatial distributions that are marked by a patchy distribution of plants, with mutualists and exploiters situated about these patches.
- Ferriere, R., Bronstein, J. L., Rinaldi, S., Law, R., & Gauduchon, M. (2002). Cheating and the evolutionary stability of mutualisms. Proceedings of the Royal Society B: Biological Sciences, 269(1493), 773-780.More infoPMID: 11958708;PMCID: PMC1690960;Abstract: Interspecific mutualisms have been playing a central role in the functioning of all ecosystems since the early history of life. Yet the theory of coevolution of mutualists is virtually nonexistent, by contrast with well-developed coevolutionary theories of competition, predator-prey and host-parasite interactions. This has prevented resolution of a basic puzzle posed by mutualisms: their persistence in spite of apparent evolutionary instability. The selective advantage of 'cheating', that is, reaping mutualistic benefits while providing fewer commodities to the partner species, is commonly believed to erode a mutualistic interaction, leading to its dissolution or reciprocal extinction. However, recent empirical findings indicate that stable associations of mutualists and cheaters have existed over long evolutionary periods. Here, we show that asymmetrical competition within species for the commodities offered by mutualistic partners provides a simple and testable ecological mechanism that can account for the long-term persistence of mutualisms. Cheating, in effect, establishes a background against which better mutualists can display any competitive superiority. This can lead to the coexistence and divergence of mutualist and cheater phenotypes, as well as to the coexistence of ecologically similar, but unrelated mutualists and cheaters.
- Holland, J. N., DeAngelis, D. L., & Bronstein, J. L. (2002). Population dynamics and mutualism: Functional responses of benefits and costs. American Naturalist, 159(3), 231-244.More infoPMID: 18707376;Abstract: We develop an approach for studying population dynamics resulting from mutualism by employing functional responses based on density-dependent benefits and costs. These functional responses express how the population growth rate of a mutualist is modified by the density of its partner. We present several possible dependencies of gross benefits and costs, and hence net effects, to a mutualist as functions of the density of its partner. Net effects to mutualists are likely a monotonically saturating or unimodal function of the density of their partner. We show that fundamental differences in the growth, limitation, and dynamics of a population can occur when net effects to that population change linearly, unimodally, or in a saturating fashion. We use the mutualism between senita cactus and its pollinating seed-eating moth as an example to show the influence of different benefit and cost functional responses on population dynamics and stability of mutualisms. We investigated two mechanisms that may alter this mutualism's functional responses: distribution of eggs among flowers and fruit abortion. Differences in how benefits and costs vary with density can alter the stability of this mutualism. In particular, fruit abortion may allow for a stable equilibrium where none could otherwise exist.
- Bronstein, J. L. (2001). The costs of mutualism. American Zoologist, 41(4), 825-839.More infoAbstract: Mutualisms arc 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, prédation, 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.
- Bronstein, J. L. (2001). The exploitation of mutualisms. Ecology Letters, 4(3), 277-287.More infoAbstract: Mutualisms (interspecific cooperative interactions) are ubiquitously exploited by organisms that obtain the benefits mutualists offer, while delivering no benefits in return. The natural history of these exploiters is well-described, but relatively little effort has yet been devoted to analysing their ecological or evolutionary significance for mutualism. Exploitation is not a unitary phenomenon, but a set of loosely related phenomena: exploiters may follow mixed strategies or pure strategies at either the species or individual level, may or may not be derived from mutualists, and may or may not inflict significant costs on mutualisms. The evolutionary implications of these different forms of exploitation, especially the threats they pose to the stability of mutualism, have as yet been minimally explored. Studies of this issue are usually framed in terms of a "temptation to defect" that generates a destabilizing conflict of interest between partners. I argue that this idea is in fact rather inappropriate for interpreting most observed forms of exploitation in mutualisms. I suggest several alternative and testable ideas for how mutualism can persist in the face of exploitation.
- Hossaert-Mckey, M., & Bronstein, J. L. (2001). Self-pollination and its costs in a monoecious fig (Ficus aurea, Moraceae) in a highly seasonal subtropical environment. American Journal of Botany, 88(4), 685-692.More infoPMID: 11302855;Abstract: 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.
- Kjellberg, F., Jousselin, E., Bronstein, J. L., Patel, A., Yokoyama, J., & Rasplus, J. -. (2001). Pollination mode in fig wasps: The predictive power of correlated traits. Proceedings of the Royal Society B: Biological Sciences, 268(1472), 1113-1121.More infoPMID: 11375097;PMCID: PMC1088715;Abstract: The over 700 species of Ficus are thought to have co-speciated with their obligate pollinators (family Agaonidae). Some of these wasp species pollinate figs actively, while others are passive pollinators. Based on direct observations of mode of pollination in 88 species, we show that mode of pollination can confidently be predicted from fig traits only (anther-to-ovule ratio) or from wasp traits only (presence of coxal combs). The presence of pollen pockets is not a predictor of mode of pollination. Data, direct and indirect, on 142 species, demonstrate numerous cases of the loss of active pollination and suggest one or few origins of active pollination. Hence, active pollination, an impressive example of the sophisticated traits that may result from mutualistic coevolution, depends on selective forces that can be overcome in some species, allowing reversions. Despite frequent loss, active pollination remains the predominant mode of pollination in Ficus.
- Law, R., Bronstein, J. L., & Ferrière, R. (2001). On mutualists and exploiters: Plant-insect coevolution in pollinating seed-parasite systems. Journal of Theoretical Biology, 212(3), 373-389.More infoPMID: 11829358;Abstract: We investigate the coevolution of time of flowering and time of pollinator emergence in an obligate association between a plant and an insect that both pollinates and parasitizes flowers. Numerical analysis shows that the system in general evolves towards a time of flowering different from the time favoured by the abiotic environment. The equilibrium towards which the system evolves is a local fitness maximum (an ESS) with respect to mutational variation in flowering time but, for the insect, it can be a local fitness minimum at which selection on mutational variation in the time of insect emergence is disruptive. A consequence of evolutionary convergence to a fitness minimum is that pollinators having an earlier phenology can coexist with pollinators having a later phenology. Since late emerging insects are more likely to encounter and oviposit within previously pollinated flowers, their effect on the plant is more exploitative, leading them to function as cheaters within the system. Thus, in the long term, pollinators and exploiters are likely to be found in stable coexistence in pollinating seed-parasite systems. © 2001 Academic Press.
- Bronstein, J. L. (1999). Natural history of Anidarnes bicolor (Hymenoptera: Agaonidae), a galler of the Florida strangling fig (Ficus aurea). Florida Entomologist, 82(3), 454-461.More infoAbstract: The natural history of Anidarnes bicolor (Ashmead) Boucek (Hymenoptera: Agaonidae: Sycophaginae), a host-specific galler of the Florida strangling fig (Ficus aurea, Moraceae), is described. A. bicolor females oviposit through the outside of the globular fig inflorescence; offspring feed on sterile tissue within galls induced on the inner wall of fig. Oviposition coincides with entry of the pollinators (Pegoscapus mexicanus; Hymenoptera: Agaonidae: Agaoninae) into the fig, and does not interfere with pollination. Pollinator presence is in fact crucial to A. bicolor success, because unpollinated, galled figs are aborted by the tree. However, A. bicolor may nevertheless reduce pollinator success: maturation of pollinator offspring appears to be negatively affected by the developing A. bicolor galls. Although the composition of the wasp community associated with the native Florida figs is relatively well-known, this is one of the first studies of the natural history of one of the non-pollinator species.
- Bronstein, J. L. (1998). The contribution of ant-plant protection studies to our understanding of mutualism. Biotropica, 30(2), 150-161.More infoAbstract: One common class of ant-plant mutualism involves ants that defend plants from natural enemies in return for food and sometimes shelter. Studies of these interactions have played a major role in shaping our broad understanding of mutualism. Their central contribution has come via their development of approaches to measuring the benefits, costs, and net outcomes of mutualism, and their explicit consideration of variability in all of these phenomena. Current research on these interactions is suggesting ecological and evolutionary hypotheses that may be applicable to many other forms of mutualism. It is also generating comparative data for testing the few general theories about mutualism that currently exist.
- Bronstein, J. L., Vernet, D., & Hossaert-McKey, M. (1998). Do fig wasps interfere with each other during oviposition?. Entomologia Experimentalis et Applicata, 87(3), 321-324.
- Bronstein, J. L., & Ziv, Y. (1997). Costs of two non-mutualistic species in a yucca/yucca moth mutualism. Oecologia, 112(3), 379-385.More infoAbstract: Mutualisms often involve significant costs for participants. Costs are inflicted by mutualists themselves, as well as by associated, non-mutualistic species. These costs are rarely quantified, however, particularly the ones extrinsic to the pairwise interaction. We compare costs inflicted by an obligate mutualist pollinator and two common exploiters of an Arizona yucca over a 2-year period. The magnitude of seed damage from seed and fruit-feeding beetle larvae (Carpophilus longus, Nitidulidae) was similar to damage from the seed-eating larvae of Yucca schottii's pollinator moth Tegeticula yuccasella (Prodoxidae), averaging about 15 seeds destroyed per fruit in each case. The two seed predators usually fed within the same fruits, although rarely side by side. In contrast, the presence of fruit-galling moth larvae (Prodoxus y-inversus, Prodoxidae) appeared to benefit the yucca: individual Tegeticula destroyed only half as many seeds in galled fruits as they did in ungalled fruits. We discuss three general implications of these results. Firstly, the costs of non-mutualists to the two mutualistic partners are not necessarily parallel. Secondly, measurable costs of non-mutualists do not necessarily translate into an impact on the success of the mutualism itself, because they may be incurred after mutualistic activities take place. Finally, the costs of mutualists to each other can differ substantially depending on the presence or absence of non-mutualistic species.
- Anstatt, M. -., Bronstein, J. L., & Hossaert-McKey, M. (1996). Resource allocation: A conflict in the fig/fig wasp mutualism?. Journal of Evolutionary Biology, 9(4), 417-428.More infoAbstract: Conflicts of interest are omnipresent between mutualist species. In the monoecious fig/pollinator wasp mutualism, each female flower produces either a seed or a pollinator offspring (which has fed on a single seed). Pollen from a syconium (i.e. fig, a closed urn-shaped inflorescence) is only dispersed by female pollinator offspring born in this syconium. Thus the fig tree is selected to produce both seed and pollinator offspring whereas for the pollinator there is no short term advantage in seed production. Using controlled pollination experiments (pollen injection, and foundress introduction), we show that 1) The relative proportion of seeds and pollinator offspring produced (i.e., the effective allocation between female and mule function) depends mainly on the number of foundresses that entered the syconium. 2) Many female flowers within every syconium mature neither a seed nor a wasp (from 25% to 33%). 3) All the female flowers within u syconium that are not vacant at maturity have the potential to produce a seed, and at least 80% of them can produce a pollinator. Several hypotheses concerning mechanisms that govern the partitioning between seed and wasp production are discussed, and their evolutionary consequences are considered.
- Anstett, M. C., Kjellberg, F., & Bronstein, J. L. (1996). Waiting for wasps: Consequences for the pollination dynamics of Ficus pertusa L.. Journal of Biogeography, 23(4), 459-466.More infoAbstract: Pollination of fig trees depends on mutualist wasps that reproduce within their flowers. Until recently, it was assumed that there was a short window of time during which a fig crop could be pollinated. Hence, pollination of figs was thought to depend on extreme efficiency of the wasps in locating receptive trees. In that context, extensive data on the Costa Rican fig tree Ficus pertusa L. have been very difficult to understand. In F. pertusa, figs of different crops attract wasps at different stages of their development. The crops that attract wasps the earliest in their development are the most heavily visited ones, but mature the fewest pollinator offspring and seeds on a per-fig basis. Using simulation models of pollinator population dynamics and field data, we show that (i) attractiveness of a crop is prolonged, (ii) wasps prefer large figs when given a choice, and (iii) the observed pattern of preferential early visitation of crops can be explained by temporal variations in pollinator abundance. This emphasizes the importance of population-level mechanisms to explain the fig/fig wasp mutualism.
- Bronstein, J. L., & Hossaert-McKey, M. (1996). Variation in reproductive success within a subtropical fig/pollinator mutualism. Journal of Biogeography, 23(4), 433-446.More infoAbstract: Plants pollinated by specialists are often thought to receive exceptionally high-quality pollinator service, but in relatively low and unpredictable quantities. We examine and reject this hypothesis for an obligate mutualism between a subtropical New World fig (Ficus aurea) and its species-specific pollinator (Pegoscapus jimenezi). Fig wasps lay eggs within the flowers they pollinate; their offspring destroy a large proportion of fig's seeds. In a 6-year study of this interaction in Florida, U.S.A., we found that pollination intensity was in fact relatively high. Also contrary to expectations, reproductive success of both mutualists (as well as other wasps cohabiting the figs) was extremely variable and generally low, at three different scales of sampling: among figs from a single crop of one tree (thirty-four figs), among crops produced at different times by that tree (126 figs), and across trees over a 1-year period (379 figs). Although variable, fig contents were not completely unpredictable. For example, seed and wasp numbers increased with the number of flowers in a fig, and female and male flower numbers increased together. Little is yet known about the causes either of these relationships or of the massive fig-to-fig variation itself, although there is some evidence that they exist in other fig species as well. Further investigations of these patterns should shed new light on the ecology and evolution of this mutualism.
- Smith, C. M., & Bronstein, J. L. (1996). Site variation in reproductive synchrony in three neotropical figs. Journal of Biogeography, 23(4), 477-486.More infoAbstract: To investigate the persistence of figs and their short-lived pollinators in highly seasonal environments and in small populations, three native figs were studied near the edge of their range in Sonora, Mexico. The reproductive phenologies of Ficus insipida (Willd.) and F. petiolaris (H.B.K.) were contrasted between a drier site with small populations and a wetter site with large populations. In addition, F. pertusa (L.) phenology was censused in the wetter site and compared with findings from Central America, Trees from smaller populations in the drier site produced less synchronous crops. Individuals within populations became reproductively synchronized at the population level but rapidly attained asynchrony in the drier site because of a breakdown in within-tree crop synchrony. Sexual-phase overlap occurred in all species and sites. Intraspecific variation in reproductive phenology may explain the persistence of figs and fig wasps in highly seasonal environments and small populations.
- Ziv, Y., & Bronstein, J. L. (1996). Infertile seeds of Yucca schottii: A beneficial role for the plant in the yucca-yucca moth mutualism?. Evolutionary Ecology, 10(1), 63-76.More infoAbstract: The yucca-yucca moth interaction is a classic case of obligate mutualism. Female moths pollinate and oviposit in the gynoecium of the flower; however, maturing larvae eat a fraction of the developing seeds. We studied within-fruit distributions of four seed types (fertile, infertile, eaten and uneaten seeds) in order to evaluate costs and benefits in a Yucca schottii population in southeastern Arizona. We focused on how the spatial arrangement of seeds affected larval behaviour and, hence, the costs of the mutualism to the yucca. Infertile seeds were distributed throughout both infested and uninfested locules. Additionally, moth larvae feeding in a single locule preferred fertile seeds and even avoided infertile seeds and left the fruit significantly more often when they encountered infertile seeds. We suggest that, regardless of the cause of infertile seeds, they function as blocking units within seed locules and therefore reduce seed predation by moth larvae. We also suggest that, together with certain other fruit traits, the presence of infertile seeds promotes the evolutionary stability of this pollination mutualism. © 1996 Chapman & Hall.
- Bronstein, J. L. (1995). The plant-pollinator landscape. Mosaic landscapes and ecological processes, 256-288.More infoAbstract: Pollinators feed on patchily distributed plants, forcing them to decide when to move between patches and when to switch plant species. The "plant-pollinator landscape' is shaped by an interacting set of plant and pollinator attributes: flowering phenology sets the distance that pollinators need to travel between patches of a given species to obtain sufficient food, while the pollinators' search capacities and dietary specificity determines the likelihood that they can and will make that journey. These sets of traits do not vary independently, allowing us to identify several characteristic landscapes and the types of organisms that occupy them. This chapter describes five such landscapes, attempting in each case to determine whether phenological variation within plant species helps to explain the ability of pollinators to persist. The first two landscapes are occupied by highly specialized pollinators and (respectively) synchronously flowering and asynchronously flowering plants. Intraspecific phenological variation is likely to have critical consequences for pollinator persistence in these two landscapes. The third and fourth landscapes are occupied by relatively generalized pollinators and (respectively) synchronously flowering and asynchronously flowering plants. The former is probably the most common landscape, encompassing most temperate plant-pollinator interactions. Pollinators in these landscapes are less likely to be strongly influenced by phenological variation in any one of their resource plants, due to their ability to switch foods easily while remaining local. The fifth landscape is occupied by generalist pollinators that may migrate. Little is known about resource use of individual migrants, but it is possible that at least some of them rely on geographical gradients in flowering time of certain preferred species. -from Author
- Bronstein, J. L., & Hossaert-Mckey, M. (1995). Hurricane Andrew and a Florida fig pollination mutualism: resilience of an obligate interaction. Biotropica, 27(3), 373-381.More infoAbstract: Reports on the recovery of a Florida fig pollination mutualism devastated by Hurricane Andrew in August 1992. Damage to Ficus aurea included loss of all leaves and fruits and many branches, as well as the presumed local extinction of its pollinator Pegoscapus jimenezi. Within five months, however, fig flowering phenology and fig wasp abundance had recovered to near prehurricane levels. Unusual phenological traits of F. aurea may have aided in the rapid reestablishment of pollinator populations; also, the wasps may have previously underappreciated capacities for long distance movements. This study suggests that obligate interactions can be resilient to certain population-level catastrophes. -from Authors
- Bronstein, J. L. (1994). Conditional outcomes in mutualistic interactions. Trends in Ecology and Evolution, 9(6), 214-217.More infoPMID: 21236825;Abstract: Interspecific interactions are traditionally displayed in a grid in which each interaction is placed according to its outcome (positive, negative or neutral) for each partner. However, recent field studies consistently find the costs and benefits that determine net effects to vary greatly in both space and time, inevitably causing outcomes within most interactions to vary as well. Interactions show 'conditionally' when costs and benefits, and thus outcomes, are affected in predictable ways by current ecological conditions. The full range of natural outcomes of a given association may reveal far more about its ecological and evolutionary dynamics than does the average outcome at a given place and time.
- Bronstein, J. L. (1994). Our current understanding of mutualism. Quarterly Review of Biology, 69(1), 31-51.More infoAbstract: It is widely believed that mutualisms, interspecific interactions that benefit both species, have been grossly neglected relative to their true importance in nature. I have reviewed the recent primary literature in order to assess quantitatively the frequency of studies of mutualism, the types of questions they address, and their general scientific approach. All articles appearing from 1986 to 1990 in nine major journals that publish ecological and evolutionary research were examined. It is clear that mutualism research is not in fact rare. Studies of interspecific interactions made up about 22 % of the over 4500 articles published during this period; of these, about one-quarter investigated some form of mutualism. Over 90 % of them investigated plant-animal interactions, primarily pollination (52 %) and seed dispersal (31 %), a bias probably related in part to the particular journals examined. The diversity of questions addressed in these articles was surprisingly low. The majority (63 %) focused simply on identifying the mutualists of some species of interest. Furthermore, almost all studies were unilateral, that is, they focused on only one of the interacting species, plants being studied much more frequently than their animal partners. Mutualism studies do not appear to have focused on mutualism as a form of interaction in the same way as studies of competition and predation. Rather, researchers have treated mutualism primarily as a life history attribute of one of the two partners. Consequently, although an impressive amount of information has accumulated about these interactions, we are still far from achieving an overall picture that transcends the boundaries of particular taxa or combinations of taxa. Three other obstacles have prevented data on mutualisms from being brought together: the historical isolation of studies of different kinds of mutualism, a nearly total disconnection between mutualism theories and empirical studies, and the unilateral approach almost always used to study these bilateral interactions. I identify eight research questions whose answers have the potential to reveal broad-based generalizations about the evolution and ecology of mutualism.
- Bronstein, J. L., & Patel, A. (1992). Causes and consequences of within-tree phenological patterns in the Florida strangling fig, Ficus aurea (Moraceae). American Journal of Botany, 79(1), 41-48.More infoAbstract: The obligate pollinators of figs, species-specific agaonid wasps, benefit figs only by transporting pollen between trees; larvae are seed predators. But given 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 fig phenology has evolved to assure outcrossing. However, some fig species show distinct within-tree 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. The authors have rejected the validity of this Seasonality Hypothesis for Ficus aurea near its northern range limit. Crops of individual trees were most, not least synchronous during the coldest, driest months of two years. Maximum asynchrony occurred in seasons that were probably most favourable for wasp transit between trees, but 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. -from Authors
- Bronstein, J. L. (1991). The nonpollinating wasp fauna of Ficus pertusa: exploitation of a mutualism?. Oikos, 61(2), 175-186.More infoAbstract: Reports on the three undescribed wasp species (Chalcidoidea: Torymidae: Sycophaginae) commonly associated with a neotropical fig, focusing on their dependence on the mutualism between F. pertusa and its pollinator Pegoscapus silvestrii, and their impact upon it. The species exploiting F. pertusa feed on nourishing tissue that they induce within fig ovaries that are unexploited by the pollinators, rather than on developing pollinators or seeds. Thus, in this case any costs to the mutualists should be indirect and probably small. F. pertusa's torymid species can only reproduce if females have oviposited within pollinated syconia, since trees abscise nearly all unpollinated ones early in development. Torymid oviposition was delayed relative to pollination, and in the one species investigated, females discriminated among syconia and chose to oviposit in pollinated ones. Offspring depend on the pollinators' male offspring to create an escape passage out of the mature syconium, and maturation times of all wasp species within the syconium are highly synchronized. -from Author
- Bronstein, J. L., Gouyon, P. -., Gliddon, C., Kjellberg, F., & Michaloud, G. (1990). The ecological consequences of flowering asynchrony in monoecious figs: a simulation study. Ecology, 71(6), 2145-2156.More infoAbstract: For plants with temporally separate sexual phases to outcross, population-level flowering asynchrony is necessary, but this can decrease the resource base available for pollinators. In figs, flowering is synchronous within a tree and the specialist pollinators/seed predators can only survive briefly away from trees. Consequently, population-level flowering asynchrony must extend year-round for pollinators to persist locally. In repeated stochastic simulations using phenological traits of Ficus natalensis, a median of 95 trees was required to produce an asynchronous sequence that could maintain local pollinator populations for 4 yr. However, many trees in those simulated populations were either male-sterile (10%) or both male- and female-sterile (35%), because their sexual phases were not well timed with the opposite phases of other trees. Sterility within a population approached zero at 2-3 times the critical population size. Both the predicted critical population size and frequency of success of the trees within it depended strongly on the duration of reproductive episodes and the intervals between episodes. Doubling the length of time over which individuals could donate pollen resulted in a 39% decrease in critical population size and a 27% increased likelihood that individuals would achieve at least some reproductive success. -from Authors
- Bronstein, J. L. (1989). A mutualism at the edge of its range. Experientia, 45(7), 622-637.More infoAbstract: Comparing populations that differ in access to mutualists can suggest how traits associated with these interactions have evolved. I discuss geographical and seasonal variation in the success of a primarily tropical mutualism (the fig/pollinator interaction), and evaluate some possible adaptations allowing it to persist at the edge of its range. Pollinators probably have difficulty in seasonal sites because 1) fig trees flower rarely in winter and 2) trees that do flower are less detectable and more difficult to reach. Fig biologists believe that seasonality must have selected for adaptations allowing pollinators to survive winter. However, geographical comparisons do not support two current ideas, the synchrony-breakdown hypothesis and the specificity-breakdown hypothesis. I pose two alternatives: plasticity of fruit and wasp developmental time, and adaptations of free-living fig wasps. I also distinguish between the impact of seasonality on monoecious versus dioecious figs; the latter group appear better adapted to reproduce in cool climates. A combination of comparative, observational, and experimental approaches has great potential for advancing our understanding of mutualisms. © 1989 Birkhäuser Verlag Basel.
- Bronstein, J. L., & McKey, D. (1989). The fig/pollinator mutualism: A model system for comparative biology. Experientia, 45(7), 601-604.
- Bronstein, J. L. (1988). Limits to fruit production in a monoecious fig: consequences of an obligate mutualism. Ecology, 69(1), 207-214.More infoAbstract: The Costa Rican fig tree, Ficus pertusa, is pollinated by a species-specific wasp (Agaonidae) whose female offspring transfer pollen between trees. Pollination success (the proportion of inflorescences pollinated) ranged from 1-100% and averaged only 65%. Resource availability evidently was limiting to fruit set as well: every crop abscised many inflorescences at a predictable point during growth. This abscission period usually preceded the brief but variably timed period of pollinator arrivals; in most cases every pollinated, undamaged inflorescence set fruit. Fruit abortion would not be expected in plants that evolved under conditions of pollen limitation; although pollinators have been thought to be overabunadnt in highly coevolved pollination mutualisms, figs' unique flowering phenology may in fact make pollen limitation common. The fact that future pollen carriers as well as seeds mature within fruits may also help explain these unusual fruit maturation patterns. -from Author
- Bronstein, J. L. (1988). Mutualism, antagonism, and the fig-pollinator interaction. Ecology, 69(4), 1298-1302.More infoAbstract: Examines the role of style lengths in the interaction between the common monoecious Ficus pertusa species and its pollinator Pegoscapus silvestrii (Agaonidae). The author first predicts seed and wasp production from measurements of fig styles and wasp ovipositors, then compares predicted and actual numbers produced. Several other, as yet untested, factors that may limit pollinator fecundity as suggested. The study was conducted in Monteverde, Puntarenas Province, Costa Rica. -from Author
- Bronstein, J. L. (1988). Predators of fig wasps. Biotropica, 20(3), 215-219.More infoAbstract: Predators inflict high mortality on the 4 species of wasps associated with the fig Ficus pertusa in Monteverde, Costa Rica. One of these wasps is the obligated pollinator of the fig. The natural histories of several predators are described: an ant that feeds on wasps arriving to oviposit, moth and weevil larvae that destroy wasps as they develop within the fruits, a staphylinid beetle that feeds on mature wasps before they leave the fruits, and a group of birds that gleans wasps as they leave. The synchrony of arrival and departure of pollinators from the fig trees probably make them the species least vulnerable to predation. -from Author
- Bronstein, J. L. (1987). Maintenance of species-specificity in a Neotropical fig- pollinator wasp mutualism.. Oikos, 48(1), 39-46.More infoAbstract: Specificity at different stages in the interaction was studied in a common neotropical fig, Ficus pertusa, particularly in relation to its sympatric congener F. tuerckheimii. 99% of pollinators arriving at sticky traps on flowering figs were the specialist species. Foreign pollinators virtually never entered F. pertusa syconia to oviposit or emerged from mature fruits. Pollinators arrive at F. pertusa trees in a one-day burst that is well timed with the presence of unpollinated syconia, providing evidence for the existence of a species-specific volatile attractant. Some nonpollinating wasps associated with F. pertusa appear to use the same attractant to locate the tree.-from Author
- Bronstein, J. L., & Hoffmann, K. (1987). Spatial and temporal variation in frugivory at a Neotropical fig, Ficus pertusa.. Oikos, 49(3), 261-268.More infoAbstract: A total of 26 species of birds in 10 families took F. pertusa fruit. Visitors' identity, abundance, and importance (estimated by an index of the number of fruits removed) all varied among trees and over time for individual trees. Compared with its obligate, species-specific pollination mutualism, F. pertusa's highly variable interactions with its present-day disperser assemblage are less likely to be products of coevolution. -from Authors
- Rathet, I., & Bronstein, J. L. (1987). Dead acacia thorns: an undescribed arthropod habitat.. American Midland Naturalist, 118(1), 205-210.More infoAbstract: Some 25% of the hollow thorns of Acacia collinsii and 29% of those of A. cornigera at Palo Verde National Park, Guanacaste Province, Costa Rica were inhabited by arthropods. The fauna is composed of arthropods from 3 classes and 11 orders with ants, thrips, centipedes and larvae of various insect taxa most common. Overall, arthropods exhibited no trend towards use of thorns of a particular size or height on the plant, but Pseudomyrmex ants were found in larger than average A. cornigera thorns and centipedes in higher than average A. collinsii thorns. Several taxa occurred wholly or predominantly on one of the Acacia species. Hollow thorns appear to be an overabundant resource commonly available to arthropods once resident ants have deserted the dead or dying plant.-from Authors
- Bronstein, J., Nogueira, A., Rando, J., Alcantara, S., Guimaraes, E., Marazzi, B., & Rey, P. (2015, Spring). Evolution of mutualistic traits in the genus Chamaecrista: A starting point for a study case. Legume Morphology Symposium and Workshop. Botocatu, Brazil: Legume Morphology Working Group.
- Bronstein, J. (2014, Fall). ADVANCE Distinguished Lecturer. Department of Biology. Florida: University of West Florida.
- Bronstein, J. (2014, Fall). Departamento Biologie Geral. Departamento Biologie Geral. Brazil: Universidade Federal de Minas Gerais.
- Bronstein, J. (2014, Fall). Department of Biology. Department of Biology. Riverside, CA: University of California at Riverside.
- Bronstein, J. (2014, Fall). Ecological Society of America. Ecological Society of America. Sacramento, CA.More infothree papers
- Bronstein, J. (2014, Fall). Fritz Mueller Symposium. Fritz Mueller Symposium. Sao Paulo, Brazil: Universidade de Sao Paulo.
- Bronstein, J. (2014, Fall). Within and between-species cooperation: an overview and historical perspective. International Society for Behavioral Ecology. New York, NY.More infoOther information: co-organizer of symposium, “Within and between-species cooperation: what are the similarities and differences?”
- Bronstein, J. (2013, Fall). A general introduction to cheating in mutualism. New Phytologist Symposium: Orchid Symbiosis: Models for Evolutionary Ecology. Cosenza, Italy.
- Bronstein, J. (2013, Fall). Department of Integrative Biology. Department of Integrative BiologyUniversity of Texas.
- Bronstein, J. (2013, Fall). The dark side of mutualism. Scandinavian Society for Pollination Biology. Finland: Lammi Biological Station.More infokeynote address
- Bronstein, J., & Bronstein, J. (2013, Fall). Ecological Society of America. Ecological Society of America. Minneapolis, MN.
- Bronstein, J. (2012, Fall). Botanical Society of America. Botanical Society of America. Milwaukee, WI.More infoone paper
- Bronstein, J. (2012, Fall). Botanical Society of America. Botanical Society of America. Portland, OR.More infotwo papers
- Bronstein, J. (2012, Fall). Relative humidity affects foraging decisions in desert hawkmoths. Israel Entomological Society. Beersheva, Israel.
- Bronstein, J. (2011, Fall). Botanical Society of America. Botanical Society of America. Austin, TX.More infotwo papers
- Bronstein, J. (2011, Fall). Center for Insect Science Spring Hexapodium. Center for Insect Science Spring Hexapodium. Tucson, AZ.
- Bronstein, J. (2011, Fall). Mathematical Biosciences Institute. Coevolution Workshop, Synthesis Panel. Columbus, OH.
- Bronstein, J. (2010, Fall). Department of Biology. Department of Biology. Reno, NV: University of Nevada at Reno.
- Bronstein, J. (2010, Fall). Department of Ecology and Evolution. Department of Ecology and Evolution. Davis, CA: University of California at Davis.
- Bronstein, J. (2010, Fall). Department of Ecology and Evolutionary Biology. Department of Ecology and Evolutionary Biology. Irvine, CA: University of California at Irvine.
- Bronstein, J. (2010, Fall). Department of Ecology and Evolutionary Biology. Department of Ecology and Evolutionary BiologyCornell University.
- Bronstein, J. (2010, Fall). Departments of Botany and Zoology. Departments of Botany and ZoologyOklahoma State University.
- Bronstein, J. (2010, Fall). Ecological Society of America. Ecological Society of America. Pittsburgh, PA.More infoone paper
- Bronstein, J. (2010, Fall). University of Arizona’s GK12 program: challenges and successes. GK12 Program Symposium. Pittsburgh, PA: Ecological Society of America.
- Bronstein, J., & Reinthal, P. (2010. A new approach to teaching evolution(pp 1861-1863).More infoVolume: 64; Review of: C. Zimmer, The Tangled Bank: An Introduction to Evolution
- Bronstein, J. (2013, Fall). Mutualism and symbiosis. Oxford Online Bibliography: Ecology.
- Fitzpatrick, G., & Bronstein, J. (2011, Fall). Mutualism. Encyclopedia of Sustainability 5/10: Ecosystem Management and Sustainability.More infoPublisher: Berkshire Publishing Group, Great Barrington, Mass