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Consumers Control Diversity and Functioning of a Natural Marine Ecosystem

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Consumers Control Diversity and Functioning of a Natural Marine Ecosystem Consumers Control Diversity and Functioning of a Natural Marine Ecosystem Andrew H. Altieri¤a, Geoffrey C. Trussell*, Patrick J. Ewanchuk¤b, Genevieve Bernatchez, Matthew E. S. Bracken Marine Science Center, Northeastern University, Nahant, Massachusetts, United States of America Abstract Background: Our understanding of the functional consequences of changes in biodiversity has been hampered by several limitations of previous work, including limited attention to trophic interactions, a focus on species richness rather than evenness, and the use of artificially assembled communities. Methodology and Principal Findings: In this study, we manipulated the density of an herbivorous snail in natural tide pools and allowed seaweed communities to assemble in an ecologically relevant and non-random manner. Seaweed species 21 21 evenness and biomass-specific primary productivity (mg O2 h g ) were higher in tide pools with snails because snails preferentially consumed an otherwise dominant seaweed species that can reduce biomass-specific productivity rates of algal assemblages. Although snails reduced overall seaweed biomass in tide pools, they did not affect gross primary 21 21 21 22 productivity at the scale of tide pools (mg O2 h pool or mg O2 h m ) because of the enhanced biomass-specific productivity associated with grazer-mediated increases in algal evenness. Significance: Our results suggest that increased attention to trophic interactions, diversity measures other than richness, and particularly the effects of consumers on evenness and primary productivity, will improve our understanding of the relationship between diversity and ecosystem functioning and allow more effective links between experimental results and real-world changes in biodiversity. Citation: Altieri AH , Trussell GC, Ewanchuk PJ, Bernatchez G, Bracken MES (2009) Consumers Control Diversity and Functioning of a Natural Marine Ecosystem. PLoS ONE 4(4): e5291. doi:10.1371/journal.pone.0005291 Editor: Stuart A. Sandin, University of California San Diego, United States of America Received December 1, 2008; Accepted March 19, 2009; Published April 22, 2009 Copyright: ß 2009 Altieri et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: Funded by Three Seas Marine Biology Program and grants from the US National Science Foundation (OCE-0648525 and OCE-0727628 to G. C. Trussell and OCE-0549944 to S. L. Williams and M. E. S. Bracken). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. * E-mail: [email protected] ¤a Current address: Department of Ecology and Evolutionary Biology, Brown University, Providence, Rhode Island, United States of America ¤b Current address: Department of Biology, Providence College, Providence, Rhode Island, United States of America Introduction abundances rather than by reducing species richness via extinction [5,12,13]. To date, our understanding of the importance of Biodiversity influences ecosystem functions and services (e.g., evenness effects on ecosystem function is largely based on primary productivity, nutrient cycling, food production) because of experimental plant communities, where the relative abundance species’ traits and interactions in mixed assemblages [1,2]. Our of primary producers is directly manipulated [6]. This approach understanding of the links between biodiversity and ecosystem has led to important insights, but like randomly constructed function has been predominantly shaped by experiments involving experiments examining richness effects [e.g., 14,15], it does not assembled communities where species are present at the same fully incorporate ecological interactions such as herbivory that relative density; thus, diversity is often defined solely in terms of generate natural patterns of evenness and richness [7,13]. species richness [3–5]. This emphasis on richness rather than other Although consumers can mediate the abundance and species measures of diversity, particularly in mesocosm or horticultural composition of primary producers [8,16–19] and thereby settings, has limited our ability to generalize experimental results influence productivity and other ecosystem functions, the gener- to natural systems where ecological processes determine the ality of these consumer effects across natural ecosystems remains composition and relative species abundance (evenness) of plant poorly understood [20]. A better understanding of biodiversity- assemblages [5–10]. functioning relationships requires field experiments where varia- Mounting evidence indicates that evenness is a component of tion in ecological interaction strengths are allowed to drive biodiversity that can influence ecosystem function [4–6,10,11]. the emergence of natural, non-random patterns of diversity Attention to the link between evenness and ecosystem function is [7,8,21–23]. critical because ecological interactions and human activities, such In this study, we manipulated the abundance of a dominant as targeted harvests, often modify evenness by skewing species herbivorous snail (Littorina littorea, hereafter Littorina) in rocky shore PLoS ONE | www.plosone.org 1 April 2009 | Volume 4 | Issue 4 | e5291 Consumers Control Diversity tide pool communities and then measured the productivity and biodiversity (richness, evenness, and diversity) of the resulting seaweed assemblages. Littorina grazing has long been recognized as a driver of intertidal algal diversity [19], and recent experiments have demonstrated the general importance of algal species richness and identity in mediating primary productivity [24,25]. We removed existing algal biomass from tide pools to mimic natural winter storm disturbance and then allowed algal communities to develop in response to different snail densities. This approach resulted in ecologically realistic, non-random assemblages that reflected the trophic structure, dispersal, disturbance, and other processes of a natural system. Moreover, tide pools isolated at low tide provided a unique opportunity to measure community composition and productivity at a naturally defined spatial scale. We found that consumers had strong effects on evenness (but not richness) that were accompanied by increased rates of algal productivity. Our results highlight the importance of examining realistic, consumer-driven changes in evenness to better under- stand the links between biodiversity and ecosystem functioning. Results Grazing by snails increased tide pool seaweed species evenness (P = 0.05, Table S1, Fig. 1A) and biomass (g m22;P,0.001, Table S1, Fig. 1B). Increases in snail density were also associated with 21 21 enhanced biomass-specific productivity (mg O2 h g ) of tide pool macroalgae (P = 0.01, Table S2, Fig. 1C). This result was not due to snail respiration, because we found no relationship between snail density and respiration (O2 consumption) rates in tide pools (F1,20 = 0.007, P = 0.933). Even after accounting for the inhibiting effect of algal biomass (g/L) on biomass-specific productivity (F1,19 = 20.7, P,0.001), there was a positive relationship between algal species evenness and biomass-specific productivity (F1,19 = 15.0, P = 0.001; Fig. 2). Due to this grazer-mediated Figure 1. Mean (+SE) (A) species evenness, (B) final standing enhancement of biomass-specific productivity, snails had no effect crop biomass, and (C) biomass-specific productivity of tide on whole tide pool gross productivity (P = 0.22, Table S2) or area- pool seaweed communities at different snail densities. Since specific productivity (P = 0.47, Table S2), despite their reduction of snail enhancement of both evenness (P = 0.05) and biomass-specific productivity (P = 0.01) counteracted their reduction of algal biomass algal standing crop biomass. (P,0.0001), productivity at the scale of the entire pool did not differ Snails did not influence any metrics of diversity other than among snail treatments (P = 0.22). evenness. Species richness (S), Shannon-Wiener’s H9, and doi:10.1371/journal.pone.0005291.g001 Figure 2. Influence of seaweed species evenness on biomass-specific productivity in tide pools. The positive relationship between biomass-specific productivity and seaweed species evenness (P = 0.001) held even after accounting for the potential effects of biomass variation on productivity (see Results). Symbols indicate pools of different snail densities: 0 per m2 (circles), 150 per m2 (triangles), and 250 per m2 (squares). doi:10.1371/journal.pone.0005291.g002 PLoS ONE | www.plosone.org 2 April 2009 | Volume 4 | Issue 4 | e5291 Consumers Control Diversity Simpson’s D did not vary across snail treatments (P$0.73 for all mechanisms underlying the relationship between biodiversity and analyses, Table S1). Species identity was also similar across all ecosystem function [9]. levels of snail grazing, with 11 of 15 algal taxa found at all 3 snail Although snails strongly influenced algal species evenness, they densities, and the other 4 species occurring only rarely (each in 3 did not affect other aspects of diversity (i.e., species identity, species or fewer of the 36 experimental tide pools). Although high and low richness, Shannon-Wiener’s H9, and Simpson’s D). These results snail densities similarly increased algal
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