Global Change Biology (2015) 21, 3971–3981, doi: 10.1111/gcb.13019

Size-balanced community reorganization in response to nutrients and warming DAVID J. MCELROY1, EOIN J. O’GORMAN2, FLORIAN D. SCHNEIDER3, H A N N E H E T J E N S 4 , P R U N E L E M E R R E R 5 , R O S S A . C O L E M A N 1 and M A R K E M M E R S O N 6 , 7 1 Coastal & Marine Ecosystems Group, School of Biological Sciences, The University of Sydney, Sydney, NSW 2006, Australia, 2 Imperial College London, Silwood Park Campus, Buckhurst Road, Ascot, Berkshire SL5 7PY, UK, 3Institut des Sciences de l’Evolution, Universite de Montpellier, CNRS, IRD, EPHE, CC065, Place Eugene Bataillon, 34095 Montpellier Cedex 05, France, 4 Department of Environmental Biology, Radboud University, Heyendaalseweg 135, 6525 AJ Nijmegen, Netherlands, 5Universite d’Avignon et des Pays du Vaucluse, IUT Genie Biologique Option Agronomie, Site Agroparc, BP 1207, 84911 Avignon Cedex 9, France, 6Institute of Global Food Security, School of Biological Sciences, Queen’s University Belfast, 97 Lisburn Road, Belfast BT9 7BL, UK, 7Queen’s University Marine Laboratory, 12-13, The Strand, Portaferry BT22 1PF, UK

Abstract It is widely accepted that global warming will adversely affect ecological communities. As ecosystems are simultaneously exposed to other anthropogenic influences, it is important to address the effects of climate change in the context of many stressors. Nutrient enrichment might offset some of the energy demands that warming can exert on organisms by stimulating growth at the base of the food web. It is important to know whether indirect effects of warming will be as ecologically significant as direct physiological effects. Declining body size is increasingly viewed as a universal response to warming, with the potential to alter trophic interactions. To address these issues, we used an outdoor array of marine mesocosms to examine the impacts of warming, nutrient enrichment and altered top-predator body size on a community comprised of the predator (shore crab Carcinus maenas), various grazing detritivores (amphipods) and algal resources. Warming increased mortality rates of crabs, but had no effect on their moulting rates. Nutrient enrichment and warming had near diametrically opposed effects on the assemblage, confirming that the ecological effects of these two stressors can cancel each other out. This suggests that nutrient-enriched systems might act as an energy refuge to populations of species under metabolic constraints due to warming. While there was a strong difference in assemblages between mesocosms containing crabs compared to mesocosms without crabs, decreasing crab size had no detectable effect on the amphipod or algal assemblages. This suggests that in allometrically balanced communities, the expected long-term effect of warming (declining body size) is not of similar ecological consequence to the direct physiological effects of warming, at least not over the six week duration of the experiment described here. More research is needed to determine the long-term effects of declining body size on the bioenergetic balance of natural communities. Keywords: allometry, body size, climate change, food web, intertidal, nutrient, over-fishing, temperature, trophic cascade Received 14 September 2014; revised version received 1 June 2015 and accepted 18 June 2015

Introduction Ecosystems consist of many species that interact with their environment and each other and may be depicted as food webs describing ‘who eats whom’ (Elton, 1927). The way in which species contribute to the functioning of a food web is constrained by specific biological and environmental conditions (Montoya et al., 2006), which are subject to alteration by anthropogenic drivers such as the increase in atmospheric CO2, overexploitation of natural ecosystems and the overapplication of agricultural fertilizers (Millenium Ecosystem Assessment 2005). In these food webs, 95% of species tend to be no Correspondence: David J. McElroy, tel. +61293512590, fax +61293516713, e-mail: [email protected]

© 2015 John Wiley & Sons Ltd

more than three links apart (Williams et al., 2002), and seemingly small perturbations to a single species may be swiftly communicated to the entire web (O’Gorman & Emmerson, 2010). There is potential for such small effects to cause catastrophic phase shifts, for example where the depletion of top predators has led to systems dominated by primary producers or gelatinous consumers such as comb jellies (Borer et al., 2006; Daskalov et al., 2007). Due to anthropogenic CO2 emissions, a global increase in mean surface temperature of at least 1.5– 2 °C is expected by 2100 (IPCC 2013). Warming can disrupt the total energy of an ecosystem by directly altering the rate (Nemani et al., 2003) and type (J€ ohnk et al., 2008) of primary production, while simultaneously modifying the ability of consumers to regulate

3971

3972 D . J . M C E L R O Y et al. these changes (Sanford, 2002). This strengthening of regulatory top-down effects is in part due to the direct effect that temperature has on accelerating individual metabolism, which varies depending on body size and trophic position (P€ ortner, 2002; Brown et al., 2004; Brose et al., 2012). This increased demand for metabolic upkeep leaves less energy available for growth and reproduction, and the avoidance of disease and parasitism (Dobson & Carper, 1992; Christensen et al., 2011). An indirect effect of future climate scenarios is that differential tolerances to warming between organisms of varying body size are likely to favour smaller-bodied individuals and species, a process that has already been widely observed (Daufresne et al., 2009; Gardner et al., 2011; Sheridan & Bickford, 2011; Reuman et al., 2014). Changes in body mass might occur due to the competitive exclusion of larger organisms in favour of smaller individuals and species that need less food, grow faster and reproduce earlier (Daufresne et al., 2009; Reuman et al., 2014). Many predator populations have already experienced a disproportionate decline in average body size (e.g. Audzijonyte et al., 2013). In aquatic ecosystems, this may also be exacerbated by size-selective harvesting, which leads to the direct removal of the oldest and largest top predators and results in a contemporary evolutionary pressure that selects for rapid growth and early reproduction (Enberg et al., 2012). Many food webs are characterized by predators eating prey that are within a range of optimal sizes (Hall et al., 1976), and a decline in the body size of upper trophic level organisms may result in an allometric trophic cascade, with alternating release from, and increases in, predation pressure across multiple trophic levels (Jochum et al., 2012). Subsequently, it has become increasingly apparent that changes in size structure have far-reaching effects that are comparable to the removal of entire species (Audzijonyte et al., 2013). Direct warming and changes in population size structure may also interact to produce synergistic or antagonistic effects that are sometimes seen when other stressors combine (Crain et al., 2008). For instance, warming accelerates growth in aquatic systems and fast-growing individuals are more vulnerable to fishing because they forage with greater risk (Biro & Post, 2008). Stressors associated with future climate change might also interact with present day stressors where ecological impacts have already been documented (Christensen et al., 2006). The nutrient status of coastal waters has risen greatly over the last two centuries (Smith et al., 1999), a phenomenon that will be exacerbated by climate change-induced increases in the intensity of episodic rainfall events over the coming decades (Christensen & Christensen, 2003). Eutrophication may promote dominance of a subset of species due to

reduced competition for basal resources (Pearson & Rosenberg, 1978) or lead to alterations in community structure (O’Gorman et al., 2012). Nutrient enrichment may increase primary production in some species (McGlathery et al., 2007), but as respiration is more sensitive to warming than photosynthesis (Yvon-Durocher et al., 2010), increased temperature might counteract enrichment through increased demand for resources (Rall et al., 2010). Additionally, warming might favour smaller-bodied organisms that require fewer resources, but this advantage could be lost when the productivity of a system is enhanced through nutrient enrichment (Binzer et al., 2012). Thus, the effects of warming and nutrient enrichment might cancel each other out at the community level, although these impacts will be moderated by species-specific responses. Trophic cascades mediated by global change can shift the flow of energy and nutrients throughout a system (Jochum et al., 2012), resulting in the creation of new communities which might have altered functioning or productivity (Petchey et al., 1999). This increases uncertainty for the delivery of economically valuable services that are the higher-level products of fine-scale ecosystem and food web processes (Worm et al., 2006). It is not yet known how the effects of direct warming, decreasing predator body size and eutrophication may interact as they are communicated through food webs. Understanding the interplay between the direct and indirect effects of these stressors is critical for predicting ecological responses to the challenges already faced on a daily basis and the likely changes that will be encountered in the near future (Christensen et al., 2006). Here, a number of hypotheses were tested in temperate mesocosms as mimics of naturally occurring rock pools: (H1) warming increases (a) growth as indicated by moulting rates and (b) mortality of crabs; (H2) warming affects interaction strengths between crabs and the rest of the community; (H3) nutrient enrichment affects interaction strengths between crabs and the rest of the community; (H4) decreasing top-predator body mass affects top-down control with effects cascading to the basal algal assemblage; and (H5) assemblage responses to all three stressors will be interactive, such that the reciprocal effects of decreasing predator body size, warming and nutrient enrichment on producer and primary consumer biomass are likely to influence each other if H2, H3 and H4 are correct.

Materials and methods

Experimental set-up The experiment was performed over 6 weeks in a mesocosm facility at Queen’s University Marine Laboratory in Portaferry, © 2015 John Wiley & Sons Ltd, Global Change Biology, 21, 3971–3981

F O O D W E B C H A N G E D U E T O M U L T I P L E S T R E S S O R S 3973 Northern Ireland, from mid-April to early June 2013. An array of 100 mesocosms (60 9 40 9 23.5 cm; 45 L capacity) was supplied with fresh, gravel-filtered seawater, pumped from the adjacent Strangford Lough (52.3809 °N, 5.5486 °W). A coarse grade of filter allowed the passage of meiofauna, microfauna and algal spores, such that each mesocosm experienced a semi-natural degree of connectivity to the Lough and facilitated the import of species, particularly the opportunistic filamentous brown alga Ectocarpus sp. The experimental facility was outside and unsheltered, so experienced fluctuations in temperature representative of nearby intertidal systems. Water was delivered to the mesocosms via overhead dump buckets, simulating turbulence characteristics of the natural shore and providing an aerated water supply at a continuous rate of approximately 1.5 L min 1. All experimental specimens were collected from the shoreline of Strangford Lough and adjacent to the laboratory. Five types of living algae were added to all mesocosms in relative quantities similar to those found on the shoreline where they were collected (Vye et al., 2014): Fucus serratus (21 g), Corallina spp. (16 g), Cladophora spp. (4 g), Mastocarpus stellatus (3 g) and Ulva lactuca (1 g). Some of the ephemeral filamentous brown alga Ectocarpus sp. grew in all mesocosms over the course of the experiment. Biomass (wet weight) was determined after excess seawater had been removed in a salad spinner. Algae were secured to an extruded mesh inlay (20 mm mesh size) using commercial garden wire, with the exception of U. lactuca, which was allowed to float freely to mimic natural conditions (Bulnheim, 1979). All algal species were given 48 hours to acclimate after deployment to the tanks before mobile invertebrates were introduced. To reduce the effect of imported epifauna, the algae and mesh were washed in a 10 g L 1 pyrethrum-based pesticide bath (Vitax Py Spray Insect Killer Concentrate) and then rinsed prior to placement in the experimental mesocosms. A random mix of 125 amphipods (generalist grazers and detritivores, including at least seven species of Chaetogammarus, Gammarus, Orchestria and Talitrus amphipod) were added to all tanks on six occasions over the course of the experiment. Shore crabs, Carcinus maenas, were considered to be an omnivorous top predator in the experiment. All crabs were kept in separate holding tanks and acclimated to control conditions prior to the start of the experiment and treatments were applied over the following 6 weeks.

Experimental design The initial deployment of the experiment had three treatment factors in an orthogonal design: warming (two levels, ambient temperature vs. increased temperature), nutrient enrichment (two levels, ambient and enriched) and top-predator body size (five levels of average crab size: extra small, small, medium, large and a control containing no crabs). Each treatment combination (2 9 2 9 5) gave a total of 20 treatments that were replicated five times. All treatments were allocated at random to the 100 mesocosms in the facility. Thirty mesocosms were ultimately excluded from the experiment for various reasons including faulty meshing allowing amphipods to escape (20 mesocosms), a water pressure failure (six mesocosms),

© 2015 John Wiley & Sons Ltd, Global Change Biology, 21, 3971–3981

imperfect delivery of the nutrient treatment (two mesocosms) and damage sustained due to leaky sample jars (two mesocosms), thus leaving 70 valid mesocosms in total for the analysis. Seven to twelve measurements of temperature were taken in each mesocosm during the experiment with an in-tank aquarium thermometer (DX, UK). The ambient seawater temperature in the experiment was 8.6 °C, and this was increased to a maximum of 14.8 °C in the elevated temperature treatments through the addition of aquarium heaters (EliteTM 300 W thermostats, Rolf C. Hagen (UK) Ltd., Castleford, UK). This led to an increase in the mean (+3.5 °C) and standard deviation (0.8 °C) of temperature, thereby imitating the range of possible warming of up to +6 °C expected for global oceanic waters by the end of the century (IPCC 2013). Consistent with other experiments performed in this particular array of outdoor mesocosms, fluctuations in experiment temperatures are unlikely to be as great as those observed in natural rockpools in the UK (Morris & Taylor, 1983; Mrowicki & O’Connor, 2014). As the actual temperature observed varied between mesocosms, the mean temperatures for each mesocosm over time were used as continuous covariates in the subsequent analysis. Nutrient treatments reflected the ambient concentrations found in Strangford Lough and a representative level of eutrophication consistent with that commonly observed in coastal marine habitats (Smith et al., 1999). Untreated seawater used in the background level of nutrient treatments contained 1.63  0.07 lm L 1 DIN, 0.38  0.01 lm L 1 phosphate and 0.68  0.03 lm L 1 ammonium (mean  SE; Vye et al., 2014), which is typical of low summer nutrient concentrations in this region (Hydes et al., 1999). Enrichment was achieved by addition of 140 g of Osmocote Pro 3-4M (Everris, UK) contained in four perforated 50-mL falcon tubes (Fredriksen et al., 2005). The tubes were secured to the extruded mesh in each mesocosm with cable ties. Identical tubes containing gravel were included as procedural controls in unenriched mesocosms. Osmocote Pro 3-4M is a slow-release fertilizer that is pelletized with an external resin coat that releases nutrients at a set rate over the life of the pellet. This product contains 17N:5P:8K as well as smaller proportions of Mg, Fe and Cu. Previous studies for the mesocosm array used here have shown that this quantity of Osmocote elevates inorganic nitrogen content by 1.112  0.112 lm L 1, phosphate content by 0.376  0.024 lm L 1 and ammonium content by 1.007  0.091 lm L 1 (Vye et al., 2014). This increase of approximately 70% on the background concentrations found in Strangford Lough is similar to the strength of enrichments found in other studies on the effects of nutrients (Worm et al., 2000). The binary presence/absence of nutrients variable used in the initial experimental set-up was used as a factor in the subsequent analyses. Body sizes of the system’s top predator, the shore crab C. maenas, were altered to reflect a skew towards smaller toppredator body masses, representing climate-driven changes in size structure (Daufresne et al., 2009; Gardner et al., 2011; Sheridan & Bickford, 2011). The experiment began with a control containing no crabs and four treatment levels of average top-predator body mass (M = 0, 1, 2, 4 or 8 g, wet weight in the extra small, small, medium and large treatment level,

F O O D W E B C H A N G E D U E T O M U L T I P L E S T R E S S O R S 3979 only, that is this analysis only provides correlative evidence of species interactions balancing direct consumption as well as indirect facilitation via trophic cascades. However, these scenarios are likely as algae are a welldocumented resource for marine gammarid amphipods (Cruz-Rivera & Hay, 2000; Fredriksen et al., 2005). Furthermore, crabs are known to be omnivorous on algae and amphipods (Jochum et al., 2012), with a preference for crustaceans over algae (Grosholz & Ruiz, 1996).

tors are more vulnerable to extinction than lower trophic levels (Petchey et al., 1999), the understanding of mechanisms leading to a balanced, allometric massabundance scaling remains important. This, combined with the opposed effects of warming and nutrients on species interactions, suggests that complex, interactive effects of anthropogenic stressors will be of importance for ecosystem responses to environmental change.

Acknowledgements

Effects of body size We found no evidence to support the hypothesis that long-term changes in top-predator body size, as an indirect consequence of warming, can create size-mediated trophic cascades. The scaling of top-predator body mass and abundance in our experiment followed the size structure of natural intertidal populations (O’Gorman & Emmerson, 2010; Schneider et al., 2012). We suggest that if changes in the average body size of predators follow allometric constraints of mass-abundance scaling, then any trophic effects due to reduced body size and/or biomass would be counterbalanced to some extent by higher abundances in the predator population. This balance might be the consequence of population dynamics in food webs that emerge from metabolic constraints on the individual level (Ehnes et al., 2014). However, population dynamics are often modelled at much longer timescales (Persson et al., 1998), and the experiments performed here may not have been long enough for a population dynamic feedback to occur. Another experiment that used a similarly rigorous body size treatment found a significant sizedriven trophic cascade in response to a reduction in body mass of C. maenas (Jochum et al., 2012). The different outcome of these two experiments may be due to the level of realism (mesocosms versus in situ cages), the range of top-predator body sizes used (1–8 g vs. 6–24 g) and/or mortality in the top-predator treatment (replacement versus no replacement of dead crabs). Thus, the dynamic processes behind allometric massabundance scaling involve complex feedbacks that are still widely unresolved and we propose that further research should aim to resolve the highly dynamic conditions for top-down cascading effects of changes in top-predator body size.

Interactive effects of stressors We found no evidence that the indirect effect of warming leading to declining body size (Daufresne et al., 2009; Sheridan & Bickford, 2011) is as strong as direct physiological effects of warming and nutrients. However, given that under a future warming, large preda© 2015 John Wiley & Sons Ltd, Global Change Biology, 21, 3971–3981

This work was funded by an Australian Postgraduate Award from the University of Sydney to DM. Further financial support came from a Paris Goodsell Grant in Aid (USYD), the Ruhm Fellowship (USYD), the Irish Marine Institute, NERC grants NE/ L011840/1 and NE/I009280/2, and an Australian Bicentennial Scholarship (King’s College London). Queen’s University Belfast and Queen’s University Marine Laboratory provided infrastructure and support. This is publication ISEM 2015-127. We are also grateful for the comments of the anonymous reviewers whose constructive criticisms were extremely useful.

References Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecology, 26, 32–46. Audzijonyte A, Kuparinen A, Gorton R, Fulton EA (2013) Ecological consequences of body size decline in harvested fish species: positive feedback loops in trophic interactions amplify human impact. Biology Letters, 9, 20121103. Berlow EL, Neutel AM, Cohen JE et al. (2004) Interaction strengths in food webs: issues and opportunities. Journal of Animal Ecology, 73, 585–598. Binzer A, Guill C, Brose U, Rall BC (2012) The dynamics of food chains under climate change and nutrient enrichment. Philosophical Transactions of the Royal Society B: Biological Sciences, 367, 2935–2944. Biro PA, Post JR (2008) Rapid depletion of genotypes with fast growth and bold personality traits from harvested fish populations. Proceedings of the National Academy of Sciences of the United States of America, 105, 2919–2922. Borer ET, Halpern BS, Seabloom EW (2006) Asymmetry in community regulation: effects of predators and productivity. Ecology, 87, 2813–2820. Brose U, Dunne JA, Montoya JM, Petchey OL, Schneider FD, Jacob U (2012) Climate change in size-structured ecosystems. Philosophical Transactions of the Royal Society B: Biological Sciences, 367, 2903–2912. Brown JH, Gillooly JF, Allen AP, Savage VM, West GB (2004) Toward a metabolic theory of ecology. Ecology, 85, 1771–1789. Bulnheim HP (1979) Comparative studies on the physiological ecology of five euryhaline Gammarus species. Oecologia, 44, 80–86. Christensen JH, Christensen OB (2003) Climate modelling: severe summertime flooding in Europe. Nature, 421, 805–806. Christensen MR, Graham MD, Vinebrooke RD, Findlay DL, Paterson MJ, Turner MA (2006) Multiple anthropogenic stressors cause ecological surprises in boreal lakes. Global Change Biology, 12, 2316–2322. Christensen AB, Nguyen HD, Byrne M (2011) Influence of ocean hypercapnia and ocean warming on metabolic rate of the ophiuroid Ophionereis schayeri. Journal of Experimental Marine Biology and Ecology, 403, 31–38. Clarke KR, Somerfield PJ, Chapman MG (2006) On resemblance measures for ecological studies, including taxonomic dissimilarities and a zero-adjusted Bray-Curtis coefficient for denuded assemblages. Journal of Experimental Marine Biology and Ecology, 330, 55–80. Cohen J (1988) Statistical Power Analysis for the Behavioral Sciences. L. Erlbaum Associates, Hillsdale, NJ. Connell SD, Russell BD, Irving AD (2011) Can strong consumer and producer effects be reconciled to better forecast ‘catastrophic’ phase-shifts in marine ecosystems? Journal of Experimental Marine Biology and Ecology, 400, 296–301. Crain CM, Kroeker K, Halpern BS (2008) Interactive and cumulative effects of multiple human stressors in marine systems. Ecology Letters, 11, 1304–1315.

F O O D W E B C H A N G E D U E T O M U L T I P L E S T R E S S O R S 3975 tion between warming and nutrient enrichment (Table 1). However, negative effects of warming or nutrient enrichment on species within the amphipod and algal assemblage were compensated by positive effects on others, obscuring any overall trends in amphipod abundance or algal biomass (Figs 1 and 2). Examining the species-specific changes with warming and nutrient enrichment reveals opposing effects on the overall assemblage (see opposing vectors for warming and nutrients in Fig. 1). Specifically, the main effect of warming decreased interaction strengths between crabs and C. marinus and Cladophora sp., but increased interaction strengths between crabs and C. stoerensis, U. lactuca and F. serratus and had very little effect on small amphipods, G. finmarchius, Ectocarpus sp. M. stellatus and Corallina sp. (Fig. 2). The main effect of adding nutrients decreased interaction strengths between crabs and U. lactuca and M. stellatus, while it increased interactions strengths between crabs and C. marinus and G. finmarchius (Fig. 2; see Supporting information Figure S6-S8 for further detail). Thus, the hypotheses (H2 and H3) that warming and nutrients affect the interaction strengths between crabs and other species are supported. Ultimately, the effects of warming depended on the level of nutrients, that is species responded to warming at either background or enriched levels of nutrients (Fig. 3). This interactive effect of warming and nutrients manifested differently in the amphipod and algal assemblages such that amphipod species only responded to warming at background levels of nutrients, while algal species only responded to warming at

accepted, enabling rejection of the relevant null hypotheses (Hector et al., 2010). Shepard diagrams were used to visually determine the spread of distortion stress in all resemblance matrices created from the dependent data. For all analyses, interaction terms with a P-value equal to or greater than 0.25 were pooled with the residual, which greatly reduces the rate of type II errors (Underwood, 1997; Mundry & Nunn, 2009). Effect sizes between treatment mean interactions strengths (Cohen’s d; Cohen, 1988) were calculated to show the differences in amphipod abundance and algal biomass between mesocosms with and without crabs.

Results

Carcinus maenas moults and mortality Temperature had no effect on moulting rates, thereby rejecting the hypothesis (H1a) that warming increases crab growth rates. Warming significantly increased the probability of any given individual dying during the 6 weeks of the experiment, thus supporting H1b that warming increases mortality of crabs. There was no effect of crab size or nutrient enrichment on moulting or mortality rates in crabs, nor any interactive effects of the experimental factors (Table 1). This suggests that the effect of warming was consistent across changes in predator body size and the nutrient status of the experimental water.

Assemblage response Interaction strengths of crabs on the amphipod and algal assemblage were altered by a significant interac-

Table 1 Single-factor analyses with two covariates testing the null hypotheses that rates of moulting and mortality in the crab Carcinus maenas, and interaction strengths between C. maenas and various species of amphipod and algae are not affected by: (a) warming, a continuous covariate; (b) crab size, a continuous covariate; (c) nutrients, a fixed factor with two levels (background and enriched). The warming and crab size covariates and the moulting and mortality rates were log(x + 1)-transformed before analysis. For PERMANOVA, euclidean distances were used to calculate the resemblance matrix based on interaction strength between crabs and each other species. Interaction terms with a P > 0.25 were pooled with the residual so that those terms that explain the least variation are pooled first. This was performed to increase the power of tests (Underwood, 1997; Mundry & Nunn, 2009) and pooled terms are marked as such. This led to a total of three, three and two degrees of freedom being pooled with the residual for moulting, mortality and interaction strength analyses, respectively. Significant values are highlighted in bold ANCOVA

ANCOVA

PERMANOVA

Crab moulting

Crab mortality

Amphipod and algae community

Source

MS (df)

F

P

MS (df)

F

P

MS (df)

Pseudo-F

P

Unique permutations

Warming Crab size Nutrients w 9 cs w9n cs 9 n w 9 cs 9 n Pooled residual

0.07 (1) 0.07 (1) 0.002 (1) 0.14 (1) Pooled Pooled Pooled 2.38 (51)

1.46 1.43 0.04 2.93

0.23 0.24 0.83 0.09

0.29(1) 0.07 (1) 0.01 (1) Pooled 0.13 (1) Pooled Pooled 0.06 (51)

4.67 1.18 0.21

0.04 0.28 0.65

4.50 1.24 6.09

0.001 0.27 0.0002

9942 9959 9936

2.10

0.154

12.32 (1) 3.4 (1) 16.69 (1) Pooled 6.36 (1) 4.74 (1) Pooled 2.66 (44)

2.32 1.73

0.045 0.12

9953 9947

© 2015 John Wiley & Sons Ltd, Global Change Biology, 21, 3971–3981

3976 D . J . M C E L R O Y et al.

PCO 2 (21.7% of total variation)

2

C. marinus

1

G.duebensis G. salinus

Nutrient enrichment Cladophora Corallina T. saltador

0

Orchestria sp

Increasing crab size C. stoerensis Ectocarpus G.zaddachi M. stellatus F. serratus

Warming U. lactuca

−1

Small amphipods

−2 −2

−1

0

1

2

PCO 1 (31.6% of total variation) Fig. 1 Euclidean ordination of mesocosms (points) based on the resemblance matrix created from interaction strengths between C. maenas and various amphipod and algal species, which was analysed with PERMANOVA. This plot allows comparison of species (black vectors and names; underlined names are algae) with the predictor variables crab size, warming and nutrient enrichment (grey vectors) in multivariate space. Longer vectors indicate a stronger correlation. The circle indicates the boundary for a correlation of 1.

Interaction strengths of crabs on amphipods

(a)

Background nutrients

0

(b)

Enriched nutrients 0

Rare amphipods

−1

−1

C. stoerensis C. marinus sm.amphipods

−2

−2

−3

−3

−4

−4 8

9

10

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12

13 14 15

(c) Interaction strengths of crabs on algae

enriched levels of nutrients. The overall effect of warming on the interaction strengths of crabs on the amphipod assemblage was neutralized by varied responses of the amphipod species at both background and enriched nutrient levels (Fig. 3 black lines; Fig. S1). Specifically, at background nutrient levels, interaction strengths between crabs and C. marinus decreased with warming, while interaction strengths between crabs and C. stoerensis increased with warming (Figs 3 and S2). In contrast, the overall interaction strength of crabs on the algal assemblage increased with warming under enriched nutrient levels, while being insignificant at background nutrient levels (Fig. 3 black lines; Fig. S1). Specifically, at enriched nutrient levels, the interaction strengths of crabs on Cladophora sp. decreased with warming, while the interaction strengths on U. lactuca, F. serratus and Ectocarpus increased in warmer conditions (Figs 3, S3 and S4). Mesocosms containing crabs had more amphipods and less algae than the crab-free controls (Cohen’s d: 3.03 and 0.23, respectively; Fig. 4), suggesting that the presence of the top predator caused a trophic cascade. The dominant groups of amphipods were ‘small amphipods’, C. marinus and G. finmarchius (69%, 21% and 4% of amphipod individuals in the experiment, respectively; see Table S1) which were clearly under top-down pressure by crabs and grew to higher

8

9

10

11

12

13 14 15

(d)

0.4

0.4

F. serratus Cladophora M. stellatus Corallina Ectocarpus U. lactuca

0.2 0.0 −0.2 −0.4 −0.6

0.2 0.0 −0.2 −0.4 −0.6

−0.8

−0.8 8

9

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Temperature [°C]

13 14 15

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13 14 15

Temperature [°C]

Fig. 2 Interaction strengths between C. maenas and (1) the abundance of amphipod species (a, b) and (2) biomass of algal species (c, d) at various degrees of warming in the absence (a, c) and presence (b, d) of nutrient enrichment. Note that the ranges of the y-axes differ between amphipods and algae. Warming has been plotted as six bins within the temperature range of the experimental treatment, equidistant on log-scale (breaks at 8.4, 9.3, 10.3, 11.3, 12.5, 13.9, 15.3 °C; the 3rd bin of the temperature range was empty for the unenriched treatments); short tick marks show the distribution of individual replicates. Black lines and points show overall effect on amphipods and algae. Grey lines and circles denote the average interaction strengths on each species. © 2015 John Wiley & Sons Ltd, Global Change Biology, 21, 3971–3981

F O O D W E B C H A N G E D U E T O M U L T I P L E S T R E S S O R S 3977 (a)

(c)

(e)

Interaction strengths of crabs on amphipods

0

0

Rare amphipods

C. stoerensis sm.amphipods C. marinus

C. storensis sm.amphipods C. marinus

−1

−1

−2 −3

−2 −3 L

M

S

XS

−4

−4 8

9

10

11 12 13

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(b) Interaction strengths of crabs on algae

Rare amphipods

Background

(d) U. lactuca F. serratus Cladophora M. stellatus Corallina Ectocarpus

0.25 0.00 −0.25 −0.50 8

9

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11 12 13

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Enriched

6 5

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(f) F. serratus Cladophora Corallina M. stellatus Ectocarpus U. lactuca Background

Temperature [°C]

Enriched

Nutrient level

0.4 0.2 0.0 −0.2 L

M

S

−0.4

XS

−0.6 8

6 5

4

3

2

1

Crab size [g]

Fig. 3 Main effects of warming (a, b), nutrients enrichment (c, d) and crab size (e, f) on average interaction strengths between crabs and individual species of amphipods (a, c, e) and algae (b, d, f). Black lines and points show overall effect on amphipods and algae. For ease of illustration, warming has been plotted as six bins within the temperature range of the experimental treatment, equidistant on log-scale (breaks at 8.4, 9.3, 10.3, 11.3, 12.5, 13.9, 15.3 °C). Short tick marks show the distribution of individual replicates. Note that the ranges of the y-axes differ between amphipods and algae.

abundances as crabs were absent (Fig. 4). The effect of crab presence on algae was less pronounced in general and varied around zero with the dominant groups of algae being F. serratus (36% of algal biomass in the experiment), which responded positively to crab presence and Corallina sp. (40% of algal biomass) which was negatively affected by crabs (Fig. 4). While crab absence affected the assemblage, the reduction in crab size had no detectable effect on top-down control (Table 1), thereby rejecting the hypothesis (H4) that decreasing top-predator body mass can lead to trophic cascades. As we determined no effect of crab size to counter the mixed effects of warming and nutrients, we partly reject H5, concluding instead that while the effects of warming and nutrients interactively counterbalance each other, the effect of top-predator body size on top-down control is not interacting with the other drivers.

Discussion

Effects of warming on crab mortality and moulting Warming increased rates of mortality in C. maenas, suggesting that greater metabolic demand for food may have led to increased rates of starvation-associated mortality, as demonstrated elsewhere (Ehnes et al., 2011). Warming can make organisms more susceptible to disease, which might have increased mortality rates as seen for species of abalone and sea urchin (Friedman © 2015 John Wiley & Sons Ltd, Global Change Biology, 21, 3971–3981

et al., 1997; Lester et al., 2007). While it is generally believed that ectothermic organisms respond to warming with increased growth (Reitzel et al., 2004) and moulting (Fowler et al., 1971) and this effect declines as individuals age and increase in size (Sutcliffe et al., 1981), no such effect of temperature or body size on moulting rates was observed (Table 1). While the potential for a moulting response to warming and body size may have been restricted by food availability in the mesocosms (Klein Breteler, 1975), it appears that warming does not influence the population size structure of crabs over the timescales examined here.

Effects of warming and nutrients on the amphipod and algal assemblage The main effects of warming and nutrient enrichment had opposing influences on the amphipod and algal assemblage such that patterns of interaction strengths in cooler mesocosms were similar to those observed in nutrient-enriched mesocosms, while patterns of interaction strengths in warmer mesocosms were analogous to those seen in mesocosms with background nutrient levels. This might be because nutrients increase productivity and warming increases rates of consumption, two opposing effects that can cancel each other out to some extent, as suggested by experiments with pond food webs (Shurin et al., 2012). The ability to adapt physiologically to changing environmental conditions such as tem-

3978 D . J . M C E L R O Y et al.

40

300

30 200 20 100

10 0

0 Absent

Extra small

Small

(b)

Medium

Large

(c) 15

Amphipod abundance [ind.per mesocosm]

Algae biomass (grey) [g per mesocosm]

50

400

Corallina sm.amphipods F. serratus C. marinus Cladophora C. stoerensis M. stellatus

100 75 50 25 0 Absent Present

U lactuca Rare amphipods Ectocarpus

10

5

Algae biomass (grey) [g per mesocosm]

Amphipod abundance [ind.per mesocosm]

(a)

0 Absent Present

Crabs Fig. 4 (a) Effect of crab presence and size on total amphipod abundance (individuals per mesocosm) and algal biomass (grey boxplots, g per mesocosm). Effect of crab presence on abundance of individual species of (b) amphipods and (c) algae.

perature is species specific, with responses potentially due to pre-adaptation to certain conditions, via phenotypic plasticity and acclimatization potential (Bulnheim, 1979; Somero, 2005; L opez-Maury et al., 2008). It is expected that under future warming scenarios, some species will thrive at their new temperature range, while other species will not be as competitive and decline possibly to extinction, thus resulting in the evolution of novel communities (Lurgi et al., 2012). If nutrients and warming do cancel each other out as our results suggest, less competitive species and communities that are still within their physiological limits could persist longer in nutrient rich systems; that is, nutrient rich systems might act as an ‘energy refuge’ for species suffering from increased metabolic requirements in warmer environments. None of the observed effects of warming or nutrients were consistent across all species of amphipod or all species of algae, with the actual effects of warming and nutrients having manifested as an interaction between both stressors. Warming altered crabs-amphipod and crabs-algae interactions at background and enriched levels of nutrients, respectively, suggesting that the response of a species to the direct influence of the stressors was mediated by their trophic roles as grazers and primary producers. This suggests that the documented physiological effects of warming and nutrients on individual species (reviewed in Tilman et al., 1982; Brown et al., 2004) may be mediated by, for example, trophic interactions. The more negative effects of crabs on C. marinus in response to warming at background levels

of nutrients mirrors the short-term responses to warming shown in laboratory predator–prey experiments (Rall et al., 2010). This effect was likely due to the increased metabolic demand of the crabs in the warmer environment (Brown et al., 2004). Conversely, there was no effect of warming on interaction strengths between crabs and any species of algae at background levels of nutrients. This is probably because warming also increases primary production, so that the greater grazing pressure exerted by amphipods in the warmer mesocosms was largely negated (Shurin et al., 2012). In the enriched mesocosms, warming increased interaction strengths between crabs and Ectocarpus sp., U. lactuca and F. serratus, that is the net consequence of crabs on these algae changed from inhibitory to beneficial effects. This suggests that production of these algae in the warm, nutrient rich environment was more than sufficient to meet the metabolic demand of the amphipod grazers and any direct consumption by crabs (Power, 1992). The assemblage level response to warming and nutrients might also be due to competition between amphipod and algal species. For example, interaction strengths between crabs and C. stoerensis increased in response to warming, that is the species became less constrained by crab presence, which is the opposite pattern to that seen for C. marinus and rare amphipods. This phenomenon might be indicative of indirect ecological interactions between these prey species, whereby C. stoerensis gained a competitive advantage as populations of C. marinus, and the rare amphipod species were suppressed to a greater extent by enhanced predation pressure with warming. Indeed, reduced competition has been broadly shown to result in greater positive effects on organisms than decreasing predation pressure (Gurevitch et al., 2000). In a similar vein, interaction strengths of crabs on Cladophora sp. decreased with warming at enriched nutrient levels, that is to lower biomass, while other species (U. lactuca, F. serratus and Ectocarpus sp.) exhibited increased interaction strengths and biomass. This might be due to Cladophora sp. being at a competitive disadvantage in warmer, nutrient rich environments, as has been seen for some stenothermal intertidal species that are less able to compete outside their natural thermal limits (Somero, 2010). Such compensatory indirect effects greatly reduce the ability of managers to predict whole community responses to environmental changes (Menge, 1995; Connell et al., 2011). Thus, it remains important to examine the responses of target species to different stressors in a wider ecological context that includes multiple environmental variables and the consumers, resources and competitors of the target species. It should be noted that the trophic and competitive relationships described here are phenomenological © 2015 John Wiley & Sons Ltd, Global Change Biology, 21, 3971–3981

F O O D W E B C H A N G E D U E T O M U L T I P L E S T R E S S O R S 3979 only, that is this analysis only provides correlative evidence of species interactions balancing direct consumption as well as indirect facilitation via trophic cascades. However, these scenarios are likely as algae are a welldocumented resource for marine gammarid amphipods (Cruz-Rivera & Hay, 2000; Fredriksen et al., 2005). Furthermore, crabs are known to be omnivorous on algae and amphipods (Jochum et al., 2012), with a preference for crustaceans over algae (Grosholz & Ruiz, 1996).

tors are more vulnerable to extinction than lower trophic levels (Petchey et al., 1999), the understanding of mechanisms leading to a balanced, allometric massabundance scaling remains important. This, combined with the opposed effects of warming and nutrients on species interactions, suggests that complex, interactive effects of anthropogenic stressors will be of importance for ecosystem responses to environmental change.

Acknowledgements

Effects of body size We found no evidence to support the hypothesis that long-term changes in top-predator body size, as an indirect consequence of warming, can create size-mediated trophic cascades. The scaling of top-predator body mass and abundance in our experiment followed the size structure of natural intertidal populations (O’Gorman & Emmerson, 2010; Schneider et al., 2012). We suggest that if changes in the average body size of predators follow allometric constraints of mass-abundance scaling, then any trophic effects due to reduced body size and/or biomass would be counterbalanced to some extent by higher abundances in the predator population. This balance might be the consequence of population dynamics in food webs that emerge from metabolic constraints on the individual level (Ehnes et al., 2014). However, population dynamics are often modelled at much longer timescales (Persson et al., 1998), and the experiments performed here may not have been long enough for a population dynamic feedback to occur. Another experiment that used a similarly rigorous body size treatment found a significant sizedriven trophic cascade in response to a reduction in body mass of C. maenas (Jochum et al., 2012). The different outcome of these two experiments may be due to the level of realism (mesocosms versus in situ cages), the range of top-predator body sizes used (1–8 g vs. 6–24 g) and/or mortality in the top-predator treatment (replacement versus no replacement of dead crabs). Thus, the dynamic processes behind allometric massabundance scaling involve complex feedbacks that are still widely unresolved and we propose that further research should aim to resolve the highly dynamic conditions for top-down cascading effects of changes in top-predator body size.

Interactive effects of stressors We found no evidence that the indirect effect of warming leading to declining body size (Daufresne et al., 2009; Sheridan & Bickford, 2011) is as strong as direct physiological effects of warming and nutrients. However, given that under a future warming, large preda© 2015 John Wiley & Sons Ltd, Global Change Biology, 21, 3971–3981

This work was funded by an Australian Postgraduate Award from the University of Sydney to DM. Further financial support came from a Paris Goodsell Grant in Aid (USYD), the Ruhm Fellowship (USYD), the Irish Marine Institute, NERC grants NE/ L011840/1 and NE/I009280/2, and an Australian Bicentennial Scholarship (King’s College London). Queen’s University Belfast and Queen’s University Marine Laboratory provided infrastructure and support. This is publication ISEM 2015-127. We are also grateful for the comments of the anonymous reviewers whose constructive criticisms were extremely useful.

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Supporting Information Additional Supporting Information may be found in the online version of this article: Table S1. Raw data (.xls) for the amphipod (abundance per mesocosm) and algal (biomass per mesocosm) community including treatment levels and continuous explanatory variables (average temperature [°C] and average crab size [g wet mass]). Appendix S1. We illustrate the effects of temperature and nutrients on individual species using ANCOVA and further investigate the effect of crab size using factorial PERMANOVA on the whole assemblage and Tukey’s post-hoc tests on the individual species.