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The exploitation of mutualisms

Judith L. Bronstein

Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, AZ 85721, U.S.A.

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First published: 20 December 2001
Cited by: 269
Judith L.Bronstein E‐mail: judieb@email.arizona.edu

Abstract

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.

Number of times cited: 269

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  • , Fig Wasps: A Staple Food for Ants on Ficus, Biotropica, 40, 2, (190-195), (2007).
  • , INVISIBLE FLORAL LARCENIES: MICROBIAL COMMUNITIES DEGRADE FLORAL NECTAR OF BUMBLE BEE‐POLLINATED PLANTS, Ecology, 89, 9, (2369-2376), (2008).
  • , MIMICS AND MAGNETS: THE IMPORTANCE OF COLOR AND ECOLOGICAL FACILITATION IN FLORAL DECEPTION, Ecology, 89, 6, (1583-1595), (2008).
  • , Conflict, cheats and the persistence of symbioses, New Phytologist, 177, 4, (849-858), (2008).
  • , The cleaning goby mutualism: a system without punishment, partner switching or tactile stimulation, Journal of Zoology, 276, 3, (306-312), (2008).
  • , The evolutionary ecology of cheating: does superficial oviposition facilitate the evolution of a cheater yucca moth?, Ecological Entomology, 33, 6, (765-770), (2008).
  • , Strategies of a parasite of the ant–Acacia mutualism, Behavioral Ecology and Sociobiology, 10.1007/s00265-007-0520-1, 62, 6, (953-962), (2007).
  • , Neotyphodium endophyte infection frequency in annual grass populations: relative importance of mutualism and transmission efficiency, Proceedings of the Royal Society B: Biological Sciences, 275, 1637, (897), (2008).
  • , Life‐History Differences among Coral Reef Sponges Promote Mutualism or Exploitation of Mutualism by Influencing Partner Fidelity Feedback, The American Naturalist, 171, 5, (597), (2008).
  • , A seed predator drives the evolution of a seed dispersal mutualism, Proceedings of the Royal Society B: Biological Sciences, 275, 1645, (1917), (2008).
  • , Arabidopsis thaliana and the Robin Hood parasite: a chivalrous oomycete that steals fitness from fecund hosts and benefits the poorest one?, Biology Letters, 4, 5, (526), (2008).
  • , Mutualism, Encyclopedia of Ecology, 10.1016/B978-008045405-4.00673-X, (2485-2491), (2008).
  • , Moths that Vector a Plant Pathogen also Transport Endophytic Fungi and Mycoparasitic Antagonists, Microbial Ecology, 56, 4, (742), (2008).
  • , Factors Affecting the Evolution of Bleaching Resistance in Corals, The American Naturalist, 171, 2, (E72), (2008).
  • , Does having multiple partners weaken the benefits of facultative mutualism? A test with cacti and cactus‐tending ants, Oikos, 116, 3, (500-512), (2006).
  • , DENSITY‐DEPENDENT EFFECTS OF ANTS ON SELECTION FOR BUMBLE BEE POLLINATION IN POLEMONIUM VISCOSUM, Ecology, 88, 5, (1202-1209), (2007).
  • , Predicting the effects of nectar robbing on plant reproduction: implications of pollen limitation and plant mating system, American Journal of Botany, 94, 12, (1935-1943), (2007).
  • , Holy alliances?, New Phytologist, 175, 4, (602-605), (2007).
  • , Evolution and persistence of obligate mutualists and exploiters: competition for partners and evolutionary immunization, Ecology Letters, 10, 2, (115-126), (2007).
  • , A review of myrmecophily in ant nest beetles (Coleoptera: Carabidae: Paussinae): linking early observations with recent findings, Naturwissenschaften, 94, 11, (871), (2007).
  • , Integrating cooperative breeding into theoretical concepts of cooperation, Behavioural Processes, 76, 2, (61), (2007).
  • , Human selection and the relaxation of legume defences against ineffective rhizobia, Proceedings of the Royal Society B: Biological Sciences, 274, 1629, (3119), (2007).
  • , Interactive effects of builders and exploiters on environmental quality and the outcome of competition between the two, Journal of Theoretical Biology, 249, 1, (46), (2007).
  • , Topological keystone species complexes in ecological interaction networks, Community Ecology, 8, 1, (1), (2007).
  • , The roles of sensory traps in the origin, maintenance, and breakdown of mutualism, Behavioral Ecology and Sociobiology, 61, 9, (1321), (2007).
  • , Do exaptations facilitate mutualistic associations between invasive and native species?, Biological Invasions, 9, 6, (623), (2007).
  • , The evolution of plant–insect mutualisms, New Phytologist, 172, 3, (412-428), (2006).
  • , The surprising diversity of ascomycetous mycorrhizas, New Phytologist, 170, 3, (421-423), (2006).
  • , Complex interactions on fig trees: ants capturing parasitic wasps as possible indirect mutualists of the fig–fig wasp interaction, Oikos, 113, 2, (344-352), (2006).
  • , Specific pollinators reveal a cryptic taxon in the bird orchid, Chiloglottis valida sensu lato (Orchidaceae) in south-eastern Australia, Australian Journal of Botany, 54, 1, (53), (2006).
  • , An empirical test of partner choice mechanisms in a wild legume-rhizobium interaction, Proceedings of the Royal Society B: Biological Sciences, 273, 1582, (77), (2006).
  • , Selection for protection in an ant-plant mutualism: host sanctions, host modularity, and the principal-agent game, Proceedings of the Royal Society B: Biological Sciences, 10.1098/rspb.2005.3273, 273, 1586, (595-602), (2006).
  • , Ectomycorrhizal fungal communities of nursery-inoculated seedlings outplanted on clear-cut sites in northern Alberta, Canadian Journal of Forest Research, 36, 7, (1684), (2006).
  • , Topological keystone species in ecological interaction networks: Considering link quality and non-trophic effects, Ecological Modelling, 196, 3-4, (365), (2006).
  • , Vocal mimicry by a passerine bird attracts other species involved in mixed-species flocks, Animal Behaviour, 72, 2, (471), (2006).
  • , Impact of the Third Trophic Level in an Obligate Mutualism: Do Yucca Plants Benefit from Parasitoids of Yucca Moths?, International Journal of Plant Sciences, 167, 1, (119), (2006).
  • , Unifying the Theories of Inclusive Fitness and Reciprocal Altruism, The American Naturalist, 168, 2, (252), (2006).
  • , Soil fauna–microbe interactions: towards a conceptual framework for research, European Journal of Soil Biology, 10.1016/j.ejsobi.2006.07.007, 42, (S54-S60), (2006).
  • , Interactions among nectar robbing, floral herbivory, and ant protection in Linaria vulgaris, Oikos, 110, 3, (497-506), (2005).
  • , Understanding mutualism when there is adaptation to the partner, Journal of Ecology, 93, 2, (305-314), (2004).
  • , Exploitation of a specialized mutualism by a deceptive orchid, American Journal of Botany, 92, 8, (1342-1349), (2005).
  • , The evolutionary ecology of myco‐heterotrophy, New Phytologist, 167, 2, (335-352), (2005).
  • , On the origins of extreme mycorrhizal specificity in the Monotropoideae (Ericaceae): performance trade‐offs during seed germination and seedling development, Molecular Ecology, 14, 5, (1549-1560), (2005).
  • , The iterated continuous prisoner's dilemma game cannot explain the evolution of interspecific mutualism in unstructured populations, Journal of Theoretical Biology, 232, 1, (99), (2005).
  • , BORDER COLLISION BIFURCATIONS IN THE EVOLUTION OF MUTUALISTIC INTERACTIONS, International Journal of Bifurcation and Chaos, 15, 07, (2179), (2005).
  • , Ecology and Evolution of Aphid-Ant Interactions, Annual Review of Ecology, Evolution, and Systematics, 36, 1, (345), (2005).
  • , Limiting cheaters in mutualism: evidence from hybridization between mutualist and cheater yucca moths, Proceedings of the Royal Society B: Biological Sciences, 272, 1577, (2195), (2005).
  • , Client fish ectoparasite loads and cleaner shrimp Urocaridella sp. c hunger levels affect cleaning behaviour, Animal Behaviour, 70, 5, (991), (2005).
  • , Catching ants with honey: an experimental test of distraction and satiation as alternative modes of escape from flower-damaging ants, Oecologia, 144, 1, (80), (2005).
  • , Re‐evaluating the role of selective abscission in moth/yucca mutualisms, Oikos, 105, 3, (449-460), (2004).
  • , The interaction of a Botanophila fly species with an exotic Epichloë fungus in a cultivated grass: fungivore or mutualist?, Entomologia Experimentalis et Applicata, 112, 2, (99-105), (2004).
  • , TESTING THE OUT‐OF‐FLORIDA HYPOTHESIS ON THE ORIGIN OF CHEATING IN THE YUCCA YUCCA MOTH MUTUALISM, Evolution, 58, 10, (2266-2279), (2007).
  • , ATTRACTING ANTAGONISTS: DOES FLORAL NECTAR INCREASE LEAF HERBIVORY?, Ecology, 85, 6, (1519-1526), (2004).
  • , Guards and thieves: antagonistic interactions between two ant species coexisting on the same ant‐plant, Ecological Entomology, 29, 3, (345-352), (2004).
  • , Feeding insects with a phytopathogenic fungus influences their diapause and population dynamics, Ecological Entomology, 29, 6, (711-717), (2004).
  • , The evolutionary implications of exploitation in mycorrhizas, Canadian Journal of Botany, 82, 8, (1110), (2004).
  • , Records of chironomidae larvae living on other aquatic animals in Brazil, Biota Neotropica, 4, 2, (1), (2004).
  • , TESTING THE OUT-OF-FLORIDA HYPOTHESIS ON THE ORIGIN OF CHEATING IN THE YUCCA–YUCCA MOTH MUTUALISM, Evolution, 58, 10, (2266), (2004).
  • , Environmental heterogeneity and the evolution of mutualism, Ecological Complexity, 1, 4, (329), (2004).
  • , Game Structures in Mutualistic Interactions: What Can the Evidence Tell Us About the Kind of Models We Need?, , 10.1016/S0065-3454(04)34002-7, (59-101), (2004).
  • , Evolution of obligate pollination mutualism in New Caledonian Phyllanthus (Euphorbiaceae), American Journal of Botany, 91, 3, (410-415), (2004).
  • , Conflicts between plants and pollinators that reproduce within inflorescences: evolutionary variations on a theme, Oikos, 100, 1, (3-14), (2003).
  • , COEXISTENCE OF MUTUALISTS AND EXPLOITERS ON SPATIAL LANDSCAPES, Ecological Monographs, 73, 3, (397-413), (2003).
  • , Sex choice in plants: facultative adjustment of the sex ratio in the perennial herb Begonia gracilis, Journal of Evolutionary Biology, 16, 6, (1177-1185), (2003).
  • , Regulation of moth–yucca mutualisms: mortality of eggs in oviposition‐induced ‘damage zones’, Ecology Letters, 6, 5, (440-447), (2003).
  • , Interacting Guilds: Moving beyond the Pairwise Perspective on Mutualisms, The American Naturalist, 162, S4, (S10), (2003).
  • , Ecological Persistence of the Plant‐Mycorrhizal Mutualism: A Hypothesis from Species Coexistence Theory, The American Naturalist, 162, S4, (S40), (2003).
  • , A comparative analysis of morphological and ecological characters of European aphids and lycaenids in relation to ant attendance, Oecologia, 135, 3, (422), (2003).
  • , Three‐Way Coexistence in Obligate Mutualist‐Exploiter Interactions: The Potential Role of Competition, The American Naturalist, 161, 6, (860), (2003).
  • , Growth, physiology, and chemistry of mycorrhizal and nonmycorrhizalTypha latifolia seedlings, Wetlands, 23, 4, (890), (2003).
  • , Ecological Dynamics of Mutualist/Antagonist Communities, The American Naturalist, 162, S4, (S24), (2003).
  • , Competition and Coexistence: Exploring Mechanisms That Restrict and Maintain Diversity within Mutualist Guilds, The American Naturalist, 162, S4, (S63), (2003).
  • , Fine‐level mycorrhizal specificity in the Monotropoideae (Ericaceae): specificity for fungal species groups, Molecular Ecology, 11, 3, (557-569), (2002).
  • , Origin of a complex key innovation in an obligate insect-plant mutualism, Proceedings of the National Academy of Sciences, 99, 8, (5498), (2002).
  • , Flower mites and nectar production in six hummingbird-pollinated plants with contrasting flower longevities, Canadian Journal of Botany, 80, 11, (1216), (2002).
  • , Ecology of Mutualisms, eLS, (1-9), (2016).
  • , The Costs of Mutualism, American Zoologist, 41, 4, (825), (2001).
  • , The Costs of Mutualism1, American Zoologist, 41, 4, (825), (2001).
  • , On Mutualists and Exploiters: Plant–insect Coevolution in Pollinating Seed–parasite Systems, Journal of Theoretical Biology, 212, 3, (373), (2001).
  • , Research on mutualisms between native and non-native partners can contribute critical ecological insights, NeoBiota, 10.3897/neobiota.26.8837, 26, (39-54), (2015).
  • , Acquisition of Uropygial Gland Microbiome by Hoopoe Nestlings, Microbial Ecology, 10.1007/s00248-017-1125-5, (2017).
  • , Field experiments show contradictory short‐ and long‐term myrmecochorous plant impacts on seed‐dispersing ants, Ecological Entomology, , (2018).
  • , May furtive predation provide enemy free space in ant-tended aphid colonies?, PLOS ONE, 10.1371/journal.pone.0204019, 13, 10, (e0204019), (2018).
  • , Recipient-Biased Competition for an Intracellularly Generated Cross-Fed Nutrient Is Required for Coexistence of Microbial Mutualists, mBio, 10.1128/mBio.01620-17, 8, 6, (e01620-17), (2017).