Update the arbiters of the legitimacy of BEF research they once used to be than the means by which we can better predict the consequences of local and global changes in biodiversity. Acknowledgements This manuscript benefited from funds from the National Science Foundation, and critical reading by Daniel Bunker, Daniel Flynn, Claire Jouseau, Nicholas Mirotchnik, Elizabeth Nichols, Matt Palmer, Sara Tjossem, Matthew Bracken and two anonymous reviewers.
References 1 Bracken, M.E. et al. (2008) Functional consequences of realistic biodiversity changes in a marine ecosystem. Proc. Natl. Acad. Sci. U. S. A. 105, 924–928 2 Roscher, C. et al. (2005) Overyielding in experimental grassland communities – irrespective of species pool or spatial scale. Ecol. Lett. 8, 419–429 3 Spehn, E.M. et al. (2005) Ecosystem effects of biodiversity manipulations in European grasslands. Ecol. Monogr. 75, 37–63 4 Hooper, D.U. et al. (2005) Effects of biodiversity on ecosystem functioning: a consensus of current knowledge and needs for future research. Ecol. Monogr. 75, 3–35 5 Worm, B. et al. (2006) Impacts of biodiversity loss on ocean ecosystem services. Science 314, 787–790 6 Cardinale, B.J. et al. (2006) Effects of biodiversity on the functioning of trophic groups and ecosystems. Nature 443, 989–992
Trends in Ecology and Evolution Vol.23 No.8 7 Raffaelli, D. (2004) How extinction patterns affect ecosystems. Science 306, 1141–1142 8 Tilman, D. et al. (2001) Diversity and productivity in a long-term grassland experiment. Science 294, 843–845 9 Zavaleta, E.S. and Hulvey, K.B. (2004) Realistic species losses disproportionately reduce grassland resistance to biological invaders. Science 306, 1175–1177 10 Bunker, D.E. et al. (2005) Species loss and aboveground carbon storage in a tropical forest. Science 310, 1029–1031 11 Solan, M. et al. (2004) Extinction and ecosystem function in the marine benthos. Science 306, 1177–1180 12 McIntyre, P.B. et al. (2007) Fish extinctions alter nutrient recycling in tropical freshwaters. Proc. Natl. Acad. Sci. U. S. A. 104, 4461–4466 13 Daz, S. et al. (2003) Functional diversity revealed by removal experiments. Trends Ecol. Evol. 18, 140–146 14 Power, M.E. et al. (1996) Challenges in the quest for keystones. Bioscience 46, 609–620 15 Cardinale, B.J. et al. (2007) Impacts of plant diversity on biomass production increase through time because of species complementarity. Proc. Natl. Acad. Sci. U. S. A. 104, 18123–18128 16 Kareiva, P. et al. (2007) Domesticated nature: shaping landscapes and ecosystems for human welfare. Science 316, 1866–1869 17 Foley, J.A. et al. (2005) Global consequences of land use. Science 309, 570–574
0169-5347/$ – see front matter ß 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.tree.2008.05.003 Available online 24 June 2008
Research Focus
Reciprocal cooperation in avian mobbing: playing nice pays David J. Wheatcroft and Trevor D. Price Committee on Evolutionary Biology, University of Chicago, 1025 East 57th Street, Chicago, IL 60637, USA
Unrelated passerine birds often join together while mobbing, a widespread antipredator behavior during which birds harass a predator. Although previous analyses concluded that mobbing could not have evolved via reciprocity, Krams and colleagues’ field experiments show that birds preferentially join mobs with neighbors that have aided them previously, suggesting that these birds utilize reciprocity-based strategies involving individual recognition and recollection of previous interactions with others. This implies a level of sophistication in bird communities greater than had previously been realized.
Mobbing behavior Mobbing is an important antipredator behavior in many communities of small passerines [1,2]. The formation of a large group might be critical to the success of a mob at driving a predator away [3], but participants suffer costs in the form of increased predation risks [4]. Despite such costs, mobbing behavior is widespread [1]. The prevalence of cooperation between unrelated individuals continues to be a major unresolved question in evolutionary biology, because individuals that do not participate—‘defectors’— Corresponding author: Wheatcroft, D.J. (
[email protected]).
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can benefit from the behavior of others while incurring none of the costs [5,6]. To explain cooperation, research has focused on behavioral strategies, such as reciprocity, that limit the ability of defectors to persist [5,6]. Animals utilizing reciprocity assist others that have aided them previously but ignore defectors, thereby promoting cooperation over defection [5,6] (Figure 1). Among mobile animals, reciprocity requires individual recognition so that animals can remember the results of previous interactions during future encounters [6]. This requirement led pioneers in the field to dismiss reciprocity as an explanation for cooperative mobbing, because seasonal communities of breeding birds were considered anonymous aggregations [1]. However, recent field experiments by Krams and colleagues [7] show that pied flycatchers (Ficedula hypoleuca) cooperate to drive predators away from the nests of neighbors, but only help those neighbors that have aided them in the past. Reciprocal mobbing in pied flycatchers Krams and colleagues [7] tested how pairs of breeding pied flycatchers respond when a neighboring pair defects against them (Figure 2). They conducted experiments at 44 triplets of nest boxes (A, B, and C) occupied by pairs of flycatchers (pairs A, B, and C, respectively). During phase one of their experiment, the researchers encaged pair B while simultaneously presenting a stuffed owl at nest A.
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This meant that pair B was prevented from joining pair A in mobbing the owl. The third pair at nest C always joined the mob formed by pair A. After an hour, the researchers conducted phase two, in which owls were presented at nests B and C simultaneously, allowing pair A to choose at which nest to mob. In 30 out of 32 trials, pair A mobbed at nest C rather than at nest B. These results imply that pair A remembered that pair C cooperated in phase one and that pair B did not, and used this knowledge to decide which pair to assist in the future. Krams and colleagues [7] also conducted secondary phase two experiments in which they presented the owl at nest B alone. Even in the absence of a choice, pair A ignored the plight of pair B, while pair C joined the mob at nest B.
Figure 1. How reciprocity can promote cooperation. The size of the circles indicates the fitness benefits when individuals A and B interact with a third individual C that is utilizing reciprocity. During the first interaction, individual A cooperates with C, while individual B defects. Individual B does not pay any cost of cooperation and, therefore, obtains a higher fitness benefit than individual A. Thus, for single interactions, defection has higher payoffs than cooperation. However, C reciprocates the behavioral strategies of A and B and will, therefore, refuse to interact with B in the future, while continuing to cooperate with A. As long as there are a sufficient number of interactions, A will continue to accrue small fitness payoffs that cumulatively overwhelm the temptation to defect on the first interaction.
Reciprocity works The results of Krams and colleagues [7] support the hypothesis that mobbing behavior in pied flycatchers is a form of reciprocal cooperation and suggest against simpler explanations for cooperative mobbing, such as byproduct mutualism [8]. In byproduct mutualisms, performing a given behavior benefits individuals even when they are acting alone. Individuals cooperate because coordinating their actions increases the benefits of participation [8]. Participants can form partner preferences based on the previous behavior of others, but cooperate even with disfavored individuals in the absence of a choice [9].
Figure 2. The experiment of Krams and colleagues [7]. Three nest boxes arranged in a rough triangle and spaced roughly 50 m apart were occupied by pied flycatchers. Top line: (a) Phase one—a stuffed tawny owl was placed roughly 1 m from nest A. A mob formed at nest A, but pair B could not join the mob because they had been temporarily encaged. Second line: Two phase two experiments, conducted 1 h after phase one. (b) A stuffed owl was placed at both nests B and C. Pair A joined the mob at C but ignored B. (c) The owl was placed only at nest B. Although pair C joined the mob, pair A did not.
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Update Therefore, during the trials in which the owl model was presented only at nest B, pair A should participate in the mob at nest B. However, pair A did not join the mob at nest B, whereas pair C did. Such retaliation is a hallmark of reciprocity and suggests against byproduct mutualism [8]. Reciprocity promotes cooperation even when mobbing at a neighbor’s nest is costly [5]. Assuming that mutual cooperation produces higher fitness payoffs than mutual defection, pairs that cooperate over a series of interactions can accrue the high benefits of alternately receiving and donating aid, whereas defectors will quickly be shunned by the rest of the community, thereby losing the benefits of long-term cooperation (Figure 1). As a result, reciprocity encourages cooperative behavioral strategies, while discouraging defection [5,6]. Implications of reciprocal mobbing Reciprocity is considered to be relatively rare in the natural world, because it requires significant cognitive capabilities and specific environmental conditions. If participants are unlikely to be recognized or remembered by others, they should be less willing to cooperate because they would likely not benefit from reciprocation. As a result, animals must be able to recognize one another and accurately track which individuals are cooperating to benefit [10,11]. Moreover, participants must interact repeatedly [6] (Figure 1). As a result, animals living in uncertain environments might forgo large potential future benefits for small immediate ones, implying that defection sometimes pays better than cooperation [11]. Krams and colleagues [7] suggest that cooperative mobbing fulfills many of the requirements for reciprocity, and their results show that pied flycatchers individually recognize one another, remember the results of previous encounters with neighboring pairs and utilize a reciprocal strategy when determining whether to mob at one another’s nests. These results complement earlier studies that have demonstrated individual recognition in cooperative systems in which participants were thought unlikely to have the necessary cognitive capabilities [12]. Although many previous experimental tests of reciprocity have suffered from experimental flaws or can more easily be explained by simpler mechanisms, such as byproduct mutualism [11], the novel experimental procedure of Krams and colleagues [7] directly establishes that breeding pairs retaliate against defectors, which has traditionally been difficult to detect. The results of Krams and colleagues [7] suggest that, contrary to previous views, reciprocity plays a role in cooperative mobbing and, hence, might occur more widely in the natural world than is currently thought. Researchers should continue to examine cooperative systems in which reciprocity is considered unlikely owing to the assumption that participants are anonymous. A reciprocal basis for mobbing raises several future research questions. Although the results of Krams and colleagues [7] imply that individuals can recognize one another and remember which neighbors have cooperated, the mechanism responsible for recognition remains unknown. During territory establishment and maintenance, neighboring conspecifics often learn to recognize one another based on songs, calls or plumage [13,14]. Previous 418
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studies have suggested that pied flycatchers can differentiate between individuals’ songs [15], but birds generally do not sing while mobbing. Future studies should examine whether mobbing calls or other individual characteristics, such as plumage, facilitate individual recognition during mobbing interactions. A second open question concerns mobs involving multiple species. The mobs generated during the experiments of Krams and colleagues [7] consisted of secondary participants from several species, which is typical of mobs in nature [1]. It is possible that passerines such as pied flycatchers can recognize multiple individuals from several different species and accurately keep track of which individuals are cooperating. In support of this hypothesis, there is strong evidence for interspecific recognition of mobbing calls [16]. Moreover, recent studies have suggested that mobbing behavior in heterospecific breeding communities depends on interspecific individual recognition, which might develop during the breeding season as birds become acquainted with one another [17]. Although the impressive recognition and memory capabilities of passerines and other non-human animals continue to be demonstrated (e.g. [12]), the presence of multiple species at a large, chaotic mob seems likely to make individual recognition and recollection of previous interactions more difficult [10]. If interspecific individual recognition were unreliable, then the prevalence of mixed-species mobs would be difficult to explain. Worth noting in this context is evidence for positive ecological interactions in some mixed-species communities. In such systems, the presence of one species can have positive fitness effects on another, putatively competing, species owing to the foraging benefits and increased predator vigilance that result from aggregation [17,18]. As a result, heterospecific neighbors rely extensively on one another, potentially providing additional motivation to engage in risky mobbing behavior. To more fully understand heterospecific mobs and to determine whether they, too, are governed by reciprocity, future research should incorporate evidence for underlying positive interactions among different species and focus on how mixed-species mobs are formed. Lastly, Krams and colleagues [7] demonstrate reciprocity over short timescales. It would also be of interest to determine whether reciprocity is preserved over longer chains of interactions, a prerequisite for stable cooperation [5,6]. Playing nice pays Our understanding of the evolution of cooperation has increased greatly with the application of game theoretical models of cooperation to biological systems [5,6], but experimental support for these models has been lacking [11]. Krams et al. [7] show that reciprocity can develop even among seasonal aggregations of breeding birds. Their results invite research into the mechanisms of individual recognition and how vocalizations mediate the formation of cooperative mobs. Other interesting future questions include whether reciprocity also governs heterospecific mobbing interactions, and whether reciprocal interactions are maintained over larger timescales. The incorporation of
Update these results into more precise models of mobbing behavior will enrich our understanding of the evolution of cooperation, one of the more poorly understood problems in evolutionary biology. Acknowledgements We thank I. Krams, E. Scordato and three anonymous reviewers for helpful comments and suggestions.
References 1 Curio, E. (1978) The adaptive significance of avian mobbing. I. Teleonomic hypotheses and predictions. Z. Tierpsychol. 48, 175–183 2 Pavey, C.R. and Smyth, A.K. (1998) Effects of avian mobbing on roost use and diet of powerful owls, Ninox strenua. Anim. Behav. 55, 313–318 3 Flasskamp, A. (1994) The adaptive significance of avian mobbing. V. An experimental test of the ‘move on’ hypothesis. Ethology 96, 322–333 4 Curio, E. and Regelmann, K. (1986) Predator harassment implies a real deadly risk: a reply to Hennessy. Ethology 72, 75–78 5 Nowak, M.A. (2006) Five rules for the evolution of cooperation. Science 314, 1560–1563 6 Axelrod, R. and Hamilton, W.D. (1981) The evolution of cooperation. Science 211, 1390–1396 7 Krams, I. et al. (2008) Experimental evidence of reciprocal altruism in the pied flycatcher. Behav. Ecol. Sociobiol. 62, 599–605 8 Dugatkin, L.A. (1997) Cooperation among Animals: An Evolutionary Perspective. Oxford University Press
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9 Connor, R.C. (1996) Partner preferences in by-product mutualisms and the case of predator inspection in fish. Anim. Behav. 51, 451–454 10 Stevens, J.R. and Hauser, M.D. (2004) Why be nice? Psychological constraints on the evolution of cooperation. Trends Cogn. Sci. 8, 60–65 11 Stevens, J.R. and Stephens, D.W. (2004) The economic basis of cooperation: tradeoffs between selfishness and generosity. Behav. Ecol. 15, 255–261 12 Tebbich, S. et al. (2002) Cleaner fish Labroides dimidiatus recognise familiar clients. Anim. Cogn. 5, 139–145 13 Godard, R. (1991) Long-term memory of individual neighbors in a migratory songbird. Nature 350, 228–229 14 Sharp, S.P. and Hatchwell, B.J. (2005) Individuality in the contact calls of cooperatively breeding long-tailed tits (Aegithalos caudatus). Behaviour 142, 1559–1575 15 Lampe, H.M. and Slagsvold, T. (1998) Female pied flycatchers respond differently to songs of mates, neighbors and strangers. Behaviour 135, 269–285 16 Hurd, C.R. (1996) Interspecific attraction to the mobbing calls of blackcapped chickadees (Parus atricapillus). Behav. Ecol. Sociobiol. 38, 287– 292 17 Krams, I. and Krama, T. (2002) Interspecific reciprocity explains mobbing behaviour of the breeding chaffinches, Fringilla coelebs. Proc. Biol. Sci. 269, 2345–2350 18 Forsman, J.T. et al. (2002) Positive fitness consequences of interspecific interaction with a potential competitor. Proc. Biol. Sci. 269, 1619–1623 0169-5347/$ – see front matter ß 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.tree.2008.04.011 Available online 26 June 2008
Letters
A behavioral perspective on fishing-induced evolution Silva Uusi-Heikkila¨1, Christian Wolter1, Thomas Klefoth1 and Robert Arlinghaus1,2 1
Department of Biology and Ecology of Fishes, Leibniz-Institute of Freshwater Ecology and Inland Fisheries, Mu¨ggelseedamm 310, 12587 Berlin, Germany 2 Inland Fisheries Management Laboratory, Faculty of Agriculture and Horticulture, Humboldt-University at Berlin, Invalidenstrasse 42, 10115 Berlin, Germany
The potential for excessive and/or selective fishing to act as an evolutionary force has been emphasized recently. However, most studies have focused on evolution of lifehistory traits in response to size-selective harvesting. Here we draw attention to fishing-induced evolution of behavioral and underlying physiological traits. We contend that fishing-induced selection directly acting on behavioral rather than on life-history traits per se can be expected in all fisheries that operate with passive gears such as trapping, angling and gill-netting. Recent artificial selection experiments in the nest-guarding largemouth bass Micropterus salmoides suggest that fishing-induced evolution of behavioral traits that reduce exposure to fishing gear might be maladaptive, potentially reducing natural recruitment. To improve understanding and management of fisheries-induced evolution, we encourage greater application of methods from behavioral ecology, physiological ecology and behavioral genetics. The potential for fishing-induced evolution (FIE) has been discussed recently [1,2]. Most studies reviewed in Ref. [1] Corresponding author: Arlinghaus, R. (
[email protected]).
have focused on life-history traits that directly or indirectly determine body size. Under the common scenario of sizeselective harvesting, large fish face a fitness disadvantage that might cause rapid evolution toward earlier maturation at smaller sizes, higher reproductive investment and lower intrinsic growth capacity and, collectively, smaller size-at-age [2]. Such evolution can degrade fisheries yield and other ecological services within decades [2]. Many studies on FIE, however, fall short in addressing the selection pathways that drive the observed life-history changes. For example, evolution of small body size can result from direct selection for decreased intrinsic growth capacity or be a consequence of selection on correlated lifehistory or behavioral traits [3]. Indeed, in some passively operated fishing gears (e.g. trapping, angling, gill-netting), behavioral traits rather than body size per se determine a fish’s vulnerability to capture, and thus its survival and fitness (Figure 1) [3]. In these situations, direct selection on behavior can drive evolutionary changes in correlated lifehistory traits such as growth rate [3] because the more active, bold and vulnerable individuals tend to also grow faster [4,5]. Despite the important role of behavior in influencing catchability in various fisheries [3,6–8], the behavioral dimension of FIE has largely been neglected. 419
