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University of Groningen Ecosystem Assembly Rules Schrama, Maarten University of Groningen Ecosystem assembly rules Schrama, Maarten; Berg, Matty P.; Olff, Han Published in: Ecology DOI: 10.1890/11-1102.1 IMPORTANT NOTE: You are advised to consult the publisher's version (publisher's PDF) if you wish to cite from it. Please check the document version below. Document Version Publisher's PDF, also known as Version of record Publication date: 2012 Link to publication in University of Groningen/UMCG research database Citation for published version (APA): Schrama, M., Berg, M. P., & Olff, H. (2012). Ecosystem assembly rules: The interplay of green and brown webs during salt marsh succession. Ecology, 93(11), 2353-2364. https://doi.org/10.1890/11-1102.1 Copyright Other than for strictly personal use, it is not permitted to download or to forward/distribute the text or part of it without the consent of the author(s) and/or copyright holder(s), unless the work is under an open content license (like Creative Commons). Take-down policy If you believe that this document breaches copyright please contact us providing details, and we will remove access to the work immediately and investigate your claim. Downloaded from the University of Groningen/UMCG research database (Pure): http://www.rug.nl/research/portal. For technical reasons the number of authors shown on this cover page is limited to 10 maximum. Download date: 23-09-2021 Ecology, 93(11), 2012, pp. 2353–2364 Ó 2012 by the Ecological Society of America Ecosystem assembly rules: the interplay of green and brown webs during salt marsh succession 1,3 2 1 MAARTEN SCHRAMA, MATTY P. BERG, AND HAN OLFF 1Community and Conservation Ecology Group, Centre for Ecological and Evolutionary Studies (CEES), University of Groningen, P.O. Box 11103, 9700CC, Groningen, The Netherlands 2Department of Ecological Sciences, VU University, Amsterdam, De Boelelaan 1085, 1081 HV Amsterdam, The Netherlands Abstract. Current theories about vegetation succession and food web assembly are poorly compatible, as food webs are generally viewed to be static, and succession is usually analyzed without the inclusion of higher trophic levels. In this study we present results from a detailed analysis of ecosystem assembly rules over a chronosequence of 100 years of salt marsh succession. First, using 13 yearlong observations on vegetation and soil parameters in different successional stages, we show that the space-for-time substitution is valid for this chronosequence. We then quantify biomass changes for all dominant invertebrate and vertebrate species across all main trophic groups of plants and animals. All invertebrate and vertebrate species were assigned to a trophic group according to feeding preference, and changes in trophic group abundance were quantified for seven different successional stages of the ecosystem. We found changes from a marine-fueled, decomposer-based (brown) food web in early stages to a more terrestrial, plant-based, herbivore-driven (green) food web in intermediate succession stages, and finally to a decomposer-based, terrestrial-driven food web in the latest stages. These changes were accompanied not only by an increase in live plant biomass and a leveling toward late succession but also by a constant increase in the amount of dead plant biomass over succession. Our results show that the structure and dynamics of salt marsh food webs cannot be understood except in light of vegetation succession, and vice versa. Key words: chronosequence; detritivore; ecosystem assembly rules; food web; herbivore; salt marsh; Schiermonnikoog, The Netherlands; succession. INTRODUCTION one of the trophic levels, and the interplay among One of the central issues in ecology is how ecological trophic levels sets the equilibrium community composi- forces shape communities of species that interact across tion of each (Schoener 1983, de Ruiter et al. 1995, multiple trophic levels. Studies of vegetation succession Berlow et al. 2004, Moore et al. 2004, Rooney et al. and food web assembly have generated many insights on 2008). This means that current theories of vegetation this topic. Although quite separate, vegetation succes- succession and food web assembly are poorly compat- ible, which calls for studies that better integrate food sion has generally been viewed as a linked plant- and web structure with the dynamics of vegetation succes- soil-driven process in which the focus is on plant sion (Schmitz et al. 2006). This requires new insights colonization, facilitation (soil modification), and inter- into how entire ecosystems assemble over time, not only specific competition/exclusion among plant species as communities at specific trophic levels. driving forces, all within this one trophic level (Clements Several authors have raised objections to the strongly 1916, Miles and Walton 1993). More recently, this is plant-centered view of community assembly and succes- combined with research on plant traits into the study of sion (Odum 1969, Connell and Slatyer 1977) and have community assembly rules. Compositional changes in argued for a more integrative approach that explicitly connected trophic levels (herbivores, predators, decom- takes plants and higher trophic levels from both the posers) in such successional ecosystems have long been ‘‘green web’’ (herbivore-based, with abundant predators assumed to be the derivative of such plant-driven of herbivores) and ‘‘brown web’’ (detritivore-based, with succession (Connell and Slatyer 1977). Food web abundant predators of detritivores) into account (Con- ecologists, on the other hand, have mostly viewed nell and Slatyer 1977, Moore et al. 2004, De Deyn and communities as static entities in which plants are just Van der Putten 2005). Initial studies on multitrophic community organization along gradients of primary Manuscript received 17 June 2011; revised 22 February 2012; productivity predict that herbivore densities first in- accepted 7 May 2012. Corresponding Editor: E. M. Bruna. crease, with more plant productivity and control plant 3 Present address: Department of Terrestrial Ecology, Netherlands Institute of Ecology, P.O. Box 50, 6700 AB standing biomass at the same level (green web interac- Wageningen, The Netherlands. tions), until predation (Oksanen et al. 1981) or plant E-mail: [email protected] quality (Van de Koppel et al. 1996) limit further growth 2353 2354 MAARTEN SCHRAMA ET AL. Ecology, Vol. 93, No. 11 of the herbivore population. Other studies have focused small internal output of material is often present in this more on the interactions between plants, organic matter state. The last state (Fig. 1D) is fundamentally different production, and decomposer densities (brown web from Fig. 1A as it is characterized as a large, but low- interactions; Berendse et al. 1994, Moore et al. 2004, quality plant production (high C:N ratio), which leads Wardle et al. 2004, Berg and Bengtsson 2007). However, to a small green web and a large brown web, as observed in some of the most intensively studied successions, in boreal forests (Hilli et al. 2010), for example. In such plants were found to play a minor role in the first stages situations, decomposition by fungi and bacteria of dead of succession (Edwards and Sugg 1993, Kaufmann 2001, plant material is essential to facilitate higher trophic Hodkinson et al. 2004) or were not even present at all levels (macrodetritivores and their predators), as the (Payne 1965, Polis and Hurd 1995, Hodkinson et al. quality of the undecomposed plant material is insuffi- 2001). This raises general questions about the extent to cient to support most herbivores. Not only may these which the green and the brown food webs determine the different configurations represent different types of onset and outcome of succession and how the impor- ecosystems, but we also propose that they can represent tance of these food web components changes over the different stages of ecosystem succession, thus revealing course of primary succession. processes of ecosystem assembly. The challenge, then, is to show how the interplay In this study, a thorough documentation of the long- between vegetation succession and food web ecology term succession of a salt marsh food web is presented as leads to ecosystem assembly over time. In particular, can a first step in this research agenda on ecosystem we identify ‘‘ecosystem assembly rules’’ based on assembly rules, which links succession and food web variation in average traits among trophic groups that structure, with equal attention to its green and brown govern ecosystem development over time? Thereby, we parts, resulting in such ecosystem assembly rules. We expand on the current agenda of ‘‘community assembly chose a salt marsh ecosystem for this study because this rules,’’ which are based on variation in traits among habitat is characterized by a limited number of species species within trophic groups (Levin et al. 2001, that are all able to cope with the generic physical and Mutshinda et al. 2009). As mentioned, many have chemical stress factors (like flooding, salinity, waterlog- stressed the importance of the interactions between ging, anaerobic conditions, H2S toxicity). We performed detritivores and herbivores in shaping the trophic a complete analysis of the dynamics of all main trophic structure of ecosystems, but how both the brown web groups of both the green and brown web along a 100 (detritivore-based, sensu Moore et al. 2004) and the year-old salt marsh chronosequence. First, we quantified green web (herbivore-based) interact over succession is the biomass for each
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