Journal of Animal Ecology 2013, 82, 717–720
doi: 10.1111/1365-2656.12099
IN FOCUS
Fear begets function in the ‘brown’ world of detrital food webs
Species of predaceous beetle (top: Agonum impressum) and large (middle: Pheretima aspergillum) and small earthworms (bottom: Aporrectodea nocturna) used to quantify the direct effects of predation on earthworm density and behavior, and indirect effects of predation on soil properties and above-ground plant biomass.
Zhao, C., Griffin, J., Wu, X. & Sun, S. (2013) Predatory beetles facilitate plant growth by driving earthworms to lower soil layers. Journal of Animal Ecology, 82, 749–758.
Theory suggests that predators in detritus-based food webs should negatively influence plants, through direct effects on plant-facilitating detritivores. In a three-level food web of predaceous beetles, earthworms and plants, Zhao et al. (2013) report evidence to the contrary. They found that predators drove positive indirect effects on both plant-facilitating soil properties and aboveground plant biomass and that these positive effects were driven by predator-mediated vertical shifts in detritivore habitat use. Their study reinforces the importance of trait-mediated indirect interactions across both ‘green’ and ‘brown’ trophic cascades and emphasizes that understanding the spatial dimension of trophic cascade mechanisms remains a critical research priority.
In this issue, Zhao et al. (2013) take a pioneering step towards understanding trophic cascades dynamics in the ‘brown’ world of detrital food webs. Despite the fundamental important of detritus pathways to ecosystem functioning, we have remarkably little understanding of how predators might influence the structure of detrital food webs. This research gap is particularly important, given that the influence of predators in detritus-based systems is expected to operate in opposite ways than the ‘green’ world of plant-based systems. Classic trophic cascade the*Correspondence author. E-mail: [email protected]
ory suggests that predators will indirectly facilitate plant growth by negatively influencing the density or behaviour of herbivores that consume plants (Hairston, Smith & Slobodkin 1960; Beckerman, Uriarte & Schmitz 1997). In contrast, because detritivores often have strongly positive influences on plant growth, decreases in detritivore abundance due to increased predation should act to reduce plant growth (Wu et al. 2011). In a novel experiment that quantified detritivore (earthworms) activity and impacts on both soil properties and plant biomass in the presence of predators (predaceous beetles), Zhao et al. (2013) provide strong and novel evidence to the contrary – reporting
© 2013 The Authors. Journal of Animal Ecology © 2013 British Ecological Society
718 E. Nichols that predators can also exert a positive influence on plant growth in detrital food webs. Zhao and colleagues explain these counter-intuitive results as the effect of behavioural responses by earthworms to the threat of beetle predation, where the mere risk of predation by beetles was capable of inducing striking vertical shifts in habitat use by one species of earthworm. By carefully linking this predator avoidance behaviour with positive changes in plant productivity, their work represents the first-ever demonstration of behaviour-mediated indirect interactions in a faecal detritus system. Along the way, Zhao and colleagues further advance our understanding of the role of species’ traits in important ecosystem processes and make significant headway towards redressing the longstanding research lack in faecal detritus food webs. Using a series of experimental chambers in an alpine meadow system on the Tibetan Plateau Zhao et al. (2013) manipulated the presence or absence of predaceous beetles (Agonum impressum) and quantified earthworm (Aporrectodea nocturna and Pheretima aspergillum) abundance, soil properties and the biomass of grasses and forbs in an upper and lower soil profiles. As beetle predators forage predominantly on the ground surface, this study design allowed tracking of the responses of earthworms, soil properties and plant productivity separately in areas of predation risk and refuge (the upper and lower soil profiles, respectively). The authors reported similar abundances of both worm species in the presence or absence of beetle predators, suggesting the absence of predator-mediated suppression of worm density. However, the presence of predators near the soil surface affected the vertical distribution of large (but not small) worms. The majority of P. aspergillum individuals sought refuge in the lower soil strata, far from the reach of beetle predators. The subsequent increased earthworm activity in this lower soil profile influenced a range of soil chemical and physical properties, with cas-
(b)
(a)
Trophic cascade model
cading effects on plant productivity. For example, soil bulk density was similar between soil strata in both predator-free and control treatments; however, it declined in the lower layer in the presence of predators. Similarly, soil water content in the lower layer increased in the presence of predators, while no differences were observed within the upper layer. The authors also found that soil organic matter content, nitrogen and phosphorus were higher in the upper layer in the absence of predation. Yet the presence of predators, these values were higher in the lower layer, mirroring the habitat shift of large earthworms. Critically, these changes in the vertical distribution of soil properties were associated with strong positive changes in above-ground plant biomasses and weakly positive changes in below-ground root biomass. Zhao and colleague’s findings advance our understanding of trophic cascades in at least four ways. First, by exploring the controlling role of predators in a detritus food web, the results help redress the paucity of empirical work in decomposer systems (Moore et al. 2004). Empirical examples of faecal detritus system cascades are rare, despite the importance to ecosystem functioning of detritus decomposition generally (Moore et al. 2004) and faecal detritus decomposition in particular (Bardgett & Wardle 2003). Even for the arguably best-studied set of faecal decomposers (Scarabaeine dung beetles), published examples of predator influence on detrital-web trophic cascades are limited to a single study, notably by the same research team (Wu et al. 2011). This lack of empirical work matters because we lack sufficient examples of predator-modified detritus pathways to understand the generalizability or consistency of their mechanisms (Shurin, Gruner & Hillebrand 2006). Predator influence is expected to operate differently in plant and detritus-based webs (Srivastava et al. 2009). Top-down effects in the ‘green’ world should indirectly facilitate plant growth (Fig 1a), via by controlling on her-
–
(c)
(d)
–
Mechanism
Predatormediated reduction in herbivory rates
Predatormediated reduction in detritivore density
Predator-mediated Predatorreduction mediated vertical herbivore fecal habitat shift by detritivores resource availability
Example
Moran & Hurd 1998
Wu et al. 2011
Nichols et al. 2009
Zhao et al. 2013
Fig. 1. Four heuristic models of trophic cascade structure. (a) Classic top-down regulation in plant-based pathways is expected to positively influence plant biomass, productivity or diversity through predator-mediated reductions in herbivory or trampling. Top-down regulation in the faecal detritus pathway may be mediated by distinct mechanisms. (b) Predation-mediated reductions in detritivore density drive cascading negative indirect effects on plant-facilitating processes including vertical nutrient transport and pedoturbation. (c) Predation-mediated changes in herbivore density or spatial distribution influence on herbivore-donations of faecal resources, with negative fitness effects on faecal detritivores and subsequent reductions in plant-facilitating processes. (d) Predation-avoidance behaviours by detritivores influence the spatial distribution of plant-facilitating processes, including vertical nutrient transport and pedoturbation. © 2013 The Authors. Journal of Animal Ecology © 2013 British Ecological Society, Journal of Animal Ecology, 82, 717–720
From fear to function in detritus food webs bivore abundance and diversity (density-mediated indirect interactions) (Oksanen et al. 1981; Schmitz et al. 2000) or by influencing herbivore behaviour, physiology or stoichiometry (trait-mediated indirect interactions) (Beckerman, Uriarte & Schmitz 1997; Werner & Peacor 2003; Hawlena et al. 2012). In contrast, predator control within the ‘brown’ world could operate by three distinct and possibly interactive mechanisms (Fig. 1b–d). First, predators in tri-trophic webs could negatively influence plant growth via negative effects on detritivore-mediated plant-facilitating processes (Fig. 1b). For example, Wu et al. (2011) reported that predator suppression of dung beetle density led to reduced faecal detritus transport rates, with cascading negative effects on plant biomass. Predators in four-level food webs could alternatively suppress plant growth via direct negative effects on herbivore densities, with subsequent indirect impacts on detritivores (and consequently plant growth) through faecal resource limitation (Fig. 1c). Such processes might be expected following mammal species declines (Wardle & Bardgett 2004). Zhao et al. (2013) present novel evidence for a third mechanism, a positive tritrophic interaction mediated by predator-induced vertical habitat shifts (Power 1984; Fig. 1d). As such traitmediated mechanisms are likely to be widespread across systems where burrowing detritivores face predation risk from above-ground predators (Young 1980), they are also likely to interact with density-mediated processes (Wu et al. 2011). Expanding our portfolio of empirical examples of detritus-web cascades will be a critical step in understanding the generality of these varied mechanisms. Second, their work contributes more broadly towards understanding top-down control in donor-based resource systems. Top-down control in green-world systems often involves compensatory plant responses to herbivory, which can play a large role in overall cascade structure and strength (Polis 1999; Srivastava et al. 2009). In contrast, the obvious lack of compensatory responses by detritus could weaken detrital cascades relative to plantbased webs as commonly suggested (Dyer & Letourneau 2003) or alternatively strengthen them, by tightly coupling consumption to resource depletion. Given the importance of decomposition to ecosystem function, understanding the strength and dynamics of top-down regulation in terrestrial detritus systems is clearly of basic and applied concern. Third, the strong functional consequences of the predator-induced vertical shifts in habitat use documented by Zhao and colleagues join current effects to understand the spatial implications of different trophic cascade mechanisms. In particular, trait-mediated mechanisms appear to influence the spatial distribution of consumers and resources more strongly than density-based mechanisms, by separating habitat space (and subsequent influences on ecological processes) into areas of risk and refuge (Matassa & Trussell 2011). Given the centrality of spatial heterogeneity to species coexistence and other funda-
719
mental ecological interactions (Holt 1984), exploration of these spatial dimensions is a key frontier issue in the study of trophic cascades. Finally, the results reported here shed additional light on the possible role of species’ traits in structuring important ecosystem processes. While species effects on both trophic interactions and ecosystem function are clearly dependent on species’ traits (Hooper et al. 2005), research efforts into biodiversity-ecosystem-function and trophic cascade research have remained remarkably independent (Reiss et al. 2009). The results of Zhao et al. (2013) strongly hint that species’ traits may provide a much needed link between these horizontal and vertical food web processes. Specifically, they reported that positive predator-mediated influences on plant growth were linked to the increased activity of large – but not small-bodied worms. These results echo recent findings that body size critically influences both the strength of predator–prey interactions across trophic levels (Wu et al. 2011) and biodiversity–ecosystem function relationships within the detrivore trophic level (Slade, Mann & Lewis 2011). In doing so, their work lends considerable weight to claims that body size may act as a universally important trait within food web processes (Berlow et al. 2004; Wood et al. 2010). While further examination of the generality of these behaviour-mediated effects in decomposer food webs will be needed, the study by Zhao and colleagues adds considerable evidence that trait-mediated indirect interactions are indeed fundamental trophic cascade mechanisms in both brown and green worlds. Elizabeth Nichols1,2* Lancaster Environment Centre, Lancaster University, Lancaster LA1 4YQ, UK 2 Department of Ecology, Institute of Bioscience, University of S~ ao Paulo, S~ ao Paulo, SP, 05508-900, Brazil 1
References Bardgett, R.D. & Wardle, D.A. (2003) Herbivore-mediated linkages between aboveground and belowground communities. Ecology, 84, 2258–2268. Beckerman, A.P., Uriarte, M. & Schmitz, O.J. (1997) Experimental evidence for a behavior-mediated trophic cascade in a terrestrial food chain. Proceedings of the National Academy of Sciences of the United States of America, 94, 10735–10738. Berlow, E.L., Neutel, A.M., Cohen, J.E., de Ruiter, P.C., Ebenman, B., Emmerson, M. et al. (2004) Interaction strengths in food webs: issues and opportunities. Journal of Animal Ecology, 73, 585–598. Borer, E.T., Seabloom, E.W., Shurin, J.B., Anderson, K.E., Blanchette, C.A., Broitman, B., Cooper, S.D. & Halpern, B.S. (2005) What determines the strength of a trophic cascade? Ecology, 86, 528–537. Borer, E.T., Seabloom, E.W., Shurin, J.B., Anderson, K.E., Blanchette, C.A., Broitman, B. et al. (2005) What determines the strength of a trophic cascade? Ecology, 86, 528–537. Dyer, L.A. & Letourneau, D. (2003) Top-down and bottom-up diversity cascades in detrital vs. living food webs. Ecology Letters, 6, 60–68. Hairston, N.G., Smith, F.E. & Slobodkin, L.B. (1960) Community structure, population control, and competition. The American Naturalist, 4, 421–425. Hawlena, D., Strickland, M.S., Bradford, M.A. & Schmitz, O.J. (2012) Fear of predation slows plant-litter decomposition. Science, 336, 1434– 1438.
© 2013 The Authors. Journal of Animal Ecology © 2013 British Ecological Society, Journal of Animal Ecology, 82, 717–720
720 E. Nichols Holt, R.D. (1984) Spatial heterogeneity, indirect interactions and the coexistence of prey species. The American Naturalist, 124, 337–406. Hooper, D.U., Chapin, F.S., Ewel, J.J., Hector, A., Inchausti, P., Lavorel, S., Lawton, J.H., Lodge, D.M., Loreau, M., Naeem, S., Schmid, B., Setala, H., Symstad, A.J., Vandermeer, J.H. & Wardle, D.A. (2005) Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecological Monographs, 75, 3–35. Matassa, C.M. & Trussell, G.C. (2011) Landscape of fear influences the relative importance of consumptive and nonconsumptive predator effects. Ecology, 92, 2258–2266. Moore, J., Berlow, E., Coleman, D., de Ruiter, P., Dong, Q., Hastings, A., Johnson, N., McCann, K., Melville, K., Morin, P., Nadelhoffer, K., Rosemond, A., Post, D., Sabo, J., Scow, K., Vanni, M. & Wall, D. (2004) Detritus, trophic dynamics and biodiversity. Ecology Letters, 7, 584–600. Nichols, E., Gardner, T.A., Peres, C.A., Spector, S. & Scarabaeinae Res, N. (2009) Co-declining mammals and dung beetles: an impending ecological cascade. Oikos, 118, 481–487. Oksanen, L., Fretwell, S.D., Arruda, J. & Niemela, P. (1981) Exploitation ecosystems in gradients of primary productivity. American Naturalist, 118, 240–261. Polis, G.A. (1999) Why are parts of the world green? Multiple factors control productivity and the distribution of biomass. Oikos, 86, 3–15. Power, M.E. (1984) Depth distributions of armored catfish – predator induced resource avoidance. Ecology, 65, 523–528. Reiss, J., Bridle, J.R., Montoya, J.M. & Woodward, G. (2009) Emerging horizons in biodiversity and ecosystem functioning research. Trends in Ecology & Evolution, 24, 505–514. Schmitz, O.J., Hamback, P.A. & Beckerman, A.P. (2000) Trophic cascades in terrestrial systems: a review of the effects of carnivore removals on plants. American Naturalist, 155, 141–153.
Shurin, J.B., Gruner, D.S. & Hillebrand, H. (2006) All wet or dried up? Real differences between aquatic and terrestrial food webs. Proceedings of the Royal Society B-Biological Sciences, 273, 1–9. Slade, E.M., Mann, D.J. & Lewis, O.T. (2011) Biodiversity and ecosystem function of tropical forest dung beetles under contrasting logging regimes. Biological Conservation, 144, 166–174. Srivastava, D.S., Cardinale, B.J., Downing, A.L., Duffy, J.E., Jouseau, C., Sankaran, M. & Wright, J.P. (2009) Diversity has stronger top-down than bottom-up effects on decomposition. Ecology, 90, 1073–1083. Wardle, D.A. & Bardgett, R.D. (2004) Human-induced changes in large herbivorous mammal density: the consequences for decomposers. Frontiers In Ecology And The Environment, 2, 145–153. Werner, E.E. & Peacor, S.D. (2003) A review of trait-mediated indirect interactions in ecological communities. Ecology, 84, 1083–1100. Wood, S.A., Lilley, S.A., Schiel, D.R. & Shurin, J.B. (2010) Organismal traits are more important than environment for species interactions in the intertidal zone. Ecology Letters, 13, 1160–1171. Wu, X., Duffy, J.E., Reich, P.B. & Sun, S. (2011) A brown-world cascade in the dung decomposer food web of an alpine meadow: effects of predator interactions and warming. Ecological Monographs, 81, 313–328. Young, O.P. (1980) Predation by tiger beetles (Coleoptera: Cicindelidae) on dung beetles (Coleoptera: Scarabaeidae) in Panama. The Coleopterists Bulletin, 34, 63–65. Zhao, C., Griffin, J., Wu, X. & Sun, S. (2013) Predatory beetles facilitate plant growth by driving earthworms to lower soil layers. Journal of Animal Ecology, 82, 749–758. Received 18 April 2013; accepted 8 May 2013 Handling Editor: Corey Bradshaw
© 2013 The Authors. Journal of Animal Ecology © 2013 British Ecological Society, Journal of Animal Ecology, 82, 717–720
doi: 10.1111/1365-2656.12099
IN FOCUS
Fear begets function in the ‘brown’ world of detrital food webs
Species of predaceous beetle (top: Agonum impressum) and large (middle: Pheretima aspergillum) and small earthworms (bottom: Aporrectodea nocturna) used to quantify the direct effects of predation on earthworm density and behavior, and indirect effects of predation on soil properties and above-ground plant biomass.
Zhao, C., Griffin, J., Wu, X. & Sun, S. (2013) Predatory beetles facilitate plant growth by driving earthworms to lower soil layers. Journal of Animal Ecology, 82, 749–758.
Theory suggests that predators in detritus-based food webs should negatively influence plants, through direct effects on plant-facilitating detritivores. In a three-level food web of predaceous beetles, earthworms and plants, Zhao et al. (2013) report evidence to the contrary. They found that predators drove positive indirect effects on both plant-facilitating soil properties and aboveground plant biomass and that these positive effects were driven by predator-mediated vertical shifts in detritivore habitat use. Their study reinforces the importance of trait-mediated indirect interactions across both ‘green’ and ‘brown’ trophic cascades and emphasizes that understanding the spatial dimension of trophic cascade mechanisms remains a critical research priority.
In this issue, Zhao et al. (2013) take a pioneering step towards understanding trophic cascades dynamics in the ‘brown’ world of detrital food webs. Despite the fundamental important of detritus pathways to ecosystem functioning, we have remarkably little understanding of how predators might influence the structure of detrital food webs. This research gap is particularly important, given that the influence of predators in detritus-based systems is expected to operate in opposite ways than the ‘green’ world of plant-based systems. Classic trophic cascade the*Correspondence author. E-mail: [email protected]
ory suggests that predators will indirectly facilitate plant growth by negatively influencing the density or behaviour of herbivores that consume plants (Hairston, Smith & Slobodkin 1960; Beckerman, Uriarte & Schmitz 1997). In contrast, because detritivores often have strongly positive influences on plant growth, decreases in detritivore abundance due to increased predation should act to reduce plant growth (Wu et al. 2011). In a novel experiment that quantified detritivore (earthworms) activity and impacts on both soil properties and plant biomass in the presence of predators (predaceous beetles), Zhao et al. (2013) provide strong and novel evidence to the contrary – reporting
© 2013 The Authors. Journal of Animal Ecology © 2013 British Ecological Society
718 E. Nichols that predators can also exert a positive influence on plant growth in detrital food webs. Zhao and colleagues explain these counter-intuitive results as the effect of behavioural responses by earthworms to the threat of beetle predation, where the mere risk of predation by beetles was capable of inducing striking vertical shifts in habitat use by one species of earthworm. By carefully linking this predator avoidance behaviour with positive changes in plant productivity, their work represents the first-ever demonstration of behaviour-mediated indirect interactions in a faecal detritus system. Along the way, Zhao and colleagues further advance our understanding of the role of species’ traits in important ecosystem processes and make significant headway towards redressing the longstanding research lack in faecal detritus food webs. Using a series of experimental chambers in an alpine meadow system on the Tibetan Plateau Zhao et al. (2013) manipulated the presence or absence of predaceous beetles (Agonum impressum) and quantified earthworm (Aporrectodea nocturna and Pheretima aspergillum) abundance, soil properties and the biomass of grasses and forbs in an upper and lower soil profiles. As beetle predators forage predominantly on the ground surface, this study design allowed tracking of the responses of earthworms, soil properties and plant productivity separately in areas of predation risk and refuge (the upper and lower soil profiles, respectively). The authors reported similar abundances of both worm species in the presence or absence of beetle predators, suggesting the absence of predator-mediated suppression of worm density. However, the presence of predators near the soil surface affected the vertical distribution of large (but not small) worms. The majority of P. aspergillum individuals sought refuge in the lower soil strata, far from the reach of beetle predators. The subsequent increased earthworm activity in this lower soil profile influenced a range of soil chemical and physical properties, with cas-
(b)
(a)
Trophic cascade model
cading effects on plant productivity. For example, soil bulk density was similar between soil strata in both predator-free and control treatments; however, it declined in the lower layer in the presence of predators. Similarly, soil water content in the lower layer increased in the presence of predators, while no differences were observed within the upper layer. The authors also found that soil organic matter content, nitrogen and phosphorus were higher in the upper layer in the absence of predation. Yet the presence of predators, these values were higher in the lower layer, mirroring the habitat shift of large earthworms. Critically, these changes in the vertical distribution of soil properties were associated with strong positive changes in above-ground plant biomasses and weakly positive changes in below-ground root biomass. Zhao and colleague’s findings advance our understanding of trophic cascades in at least four ways. First, by exploring the controlling role of predators in a detritus food web, the results help redress the paucity of empirical work in decomposer systems (Moore et al. 2004). Empirical examples of faecal detritus system cascades are rare, despite the importance to ecosystem functioning of detritus decomposition generally (Moore et al. 2004) and faecal detritus decomposition in particular (Bardgett & Wardle 2003). Even for the arguably best-studied set of faecal decomposers (Scarabaeine dung beetles), published examples of predator influence on detrital-web trophic cascades are limited to a single study, notably by the same research team (Wu et al. 2011). This lack of empirical work matters because we lack sufficient examples of predator-modified detritus pathways to understand the generalizability or consistency of their mechanisms (Shurin, Gruner & Hillebrand 2006). Predator influence is expected to operate differently in plant and detritus-based webs (Srivastava et al. 2009). Top-down effects in the ‘green’ world should indirectly facilitate plant growth (Fig 1a), via by controlling on her-
–
(c)
(d)
–
Mechanism
Predatormediated reduction in herbivory rates
Predatormediated reduction in detritivore density
Predator-mediated Predatorreduction mediated vertical herbivore fecal habitat shift by detritivores resource availability
Example
Moran & Hurd 1998
Wu et al. 2011
Nichols et al. 2009
Zhao et al. 2013
Fig. 1. Four heuristic models of trophic cascade structure. (a) Classic top-down regulation in plant-based pathways is expected to positively influence plant biomass, productivity or diversity through predator-mediated reductions in herbivory or trampling. Top-down regulation in the faecal detritus pathway may be mediated by distinct mechanisms. (b) Predation-mediated reductions in detritivore density drive cascading negative indirect effects on plant-facilitating processes including vertical nutrient transport and pedoturbation. (c) Predation-mediated changes in herbivore density or spatial distribution influence on herbivore-donations of faecal resources, with negative fitness effects on faecal detritivores and subsequent reductions in plant-facilitating processes. (d) Predation-avoidance behaviours by detritivores influence the spatial distribution of plant-facilitating processes, including vertical nutrient transport and pedoturbation. © 2013 The Authors. Journal of Animal Ecology © 2013 British Ecological Society, Journal of Animal Ecology, 82, 717–720
From fear to function in detritus food webs bivore abundance and diversity (density-mediated indirect interactions) (Oksanen et al. 1981; Schmitz et al. 2000) or by influencing herbivore behaviour, physiology or stoichiometry (trait-mediated indirect interactions) (Beckerman, Uriarte & Schmitz 1997; Werner & Peacor 2003; Hawlena et al. 2012). In contrast, predator control within the ‘brown’ world could operate by three distinct and possibly interactive mechanisms (Fig. 1b–d). First, predators in tri-trophic webs could negatively influence plant growth via negative effects on detritivore-mediated plant-facilitating processes (Fig. 1b). For example, Wu et al. (2011) reported that predator suppression of dung beetle density led to reduced faecal detritus transport rates, with cascading negative effects on plant biomass. Predators in four-level food webs could alternatively suppress plant growth via direct negative effects on herbivore densities, with subsequent indirect impacts on detritivores (and consequently plant growth) through faecal resource limitation (Fig. 1c). Such processes might be expected following mammal species declines (Wardle & Bardgett 2004). Zhao et al. (2013) present novel evidence for a third mechanism, a positive tritrophic interaction mediated by predator-induced vertical habitat shifts (Power 1984; Fig. 1d). As such traitmediated mechanisms are likely to be widespread across systems where burrowing detritivores face predation risk from above-ground predators (Young 1980), they are also likely to interact with density-mediated processes (Wu et al. 2011). Expanding our portfolio of empirical examples of detritus-web cascades will be a critical step in understanding the generality of these varied mechanisms. Second, their work contributes more broadly towards understanding top-down control in donor-based resource systems. Top-down control in green-world systems often involves compensatory plant responses to herbivory, which can play a large role in overall cascade structure and strength (Polis 1999; Srivastava et al. 2009). In contrast, the obvious lack of compensatory responses by detritus could weaken detrital cascades relative to plantbased webs as commonly suggested (Dyer & Letourneau 2003) or alternatively strengthen them, by tightly coupling consumption to resource depletion. Given the importance of decomposition to ecosystem function, understanding the strength and dynamics of top-down regulation in terrestrial detritus systems is clearly of basic and applied concern. Third, the strong functional consequences of the predator-induced vertical shifts in habitat use documented by Zhao and colleagues join current effects to understand the spatial implications of different trophic cascade mechanisms. In particular, trait-mediated mechanisms appear to influence the spatial distribution of consumers and resources more strongly than density-based mechanisms, by separating habitat space (and subsequent influences on ecological processes) into areas of risk and refuge (Matassa & Trussell 2011). Given the centrality of spatial heterogeneity to species coexistence and other funda-
719
mental ecological interactions (Holt 1984), exploration of these spatial dimensions is a key frontier issue in the study of trophic cascades. Finally, the results reported here shed additional light on the possible role of species’ traits in structuring important ecosystem processes. While species effects on both trophic interactions and ecosystem function are clearly dependent on species’ traits (Hooper et al. 2005), research efforts into biodiversity-ecosystem-function and trophic cascade research have remained remarkably independent (Reiss et al. 2009). The results of Zhao et al. (2013) strongly hint that species’ traits may provide a much needed link between these horizontal and vertical food web processes. Specifically, they reported that positive predator-mediated influences on plant growth were linked to the increased activity of large – but not small-bodied worms. These results echo recent findings that body size critically influences both the strength of predator–prey interactions across trophic levels (Wu et al. 2011) and biodiversity–ecosystem function relationships within the detrivore trophic level (Slade, Mann & Lewis 2011). In doing so, their work lends considerable weight to claims that body size may act as a universally important trait within food web processes (Berlow et al. 2004; Wood et al. 2010). While further examination of the generality of these behaviour-mediated effects in decomposer food webs will be needed, the study by Zhao and colleagues adds considerable evidence that trait-mediated indirect interactions are indeed fundamental trophic cascade mechanisms in both brown and green worlds. Elizabeth Nichols1,2* Lancaster Environment Centre, Lancaster University, Lancaster LA1 4YQ, UK 2 Department of Ecology, Institute of Bioscience, University of S~ ao Paulo, S~ ao Paulo, SP, 05508-900, Brazil 1
References Bardgett, R.D. & Wardle, D.A. (2003) Herbivore-mediated linkages between aboveground and belowground communities. Ecology, 84, 2258–2268. Beckerman, A.P., Uriarte, M. & Schmitz, O.J. (1997) Experimental evidence for a behavior-mediated trophic cascade in a terrestrial food chain. Proceedings of the National Academy of Sciences of the United States of America, 94, 10735–10738. Berlow, E.L., Neutel, A.M., Cohen, J.E., de Ruiter, P.C., Ebenman, B., Emmerson, M. et al. (2004) Interaction strengths in food webs: issues and opportunities. Journal of Animal Ecology, 73, 585–598. Borer, E.T., Seabloom, E.W., Shurin, J.B., Anderson, K.E., Blanchette, C.A., Broitman, B., Cooper, S.D. & Halpern, B.S. (2005) What determines the strength of a trophic cascade? Ecology, 86, 528–537. Borer, E.T., Seabloom, E.W., Shurin, J.B., Anderson, K.E., Blanchette, C.A., Broitman, B. et al. (2005) What determines the strength of a trophic cascade? Ecology, 86, 528–537. Dyer, L.A. & Letourneau, D. (2003) Top-down and bottom-up diversity cascades in detrital vs. living food webs. Ecology Letters, 6, 60–68. Hairston, N.G., Smith, F.E. & Slobodkin, L.B. (1960) Community structure, population control, and competition. The American Naturalist, 4, 421–425. Hawlena, D., Strickland, M.S., Bradford, M.A. & Schmitz, O.J. (2012) Fear of predation slows plant-litter decomposition. Science, 336, 1434– 1438.
© 2013 The Authors. Journal of Animal Ecology © 2013 British Ecological Society, Journal of Animal Ecology, 82, 717–720
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