Thesis in pdf
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Thesis in pdf
Thesis for the degree of Doctor of Philosophy Ecological disturbances: The Good, the Bad and the Ugly J. Robin Svensson 2010 Department of Marine Ecology - Tjärnö University of Gothenburg 45296 Strömstad SWEDEN © J. Robin Svensson 2010 All rights reserved. No part of this publication may be reproduced or transmitted, in any form or by any means, without written permission. ISBN 978-91-628-8200-6 Printed by Geson Hylte Tryck, Göteborg, Sweden 2010 Ecological disturbances Till Ivar och Kerstin Karlsson, och Nils-Erik Hjertquist 2 J. Robin Svensson Svensson, J. Robin 2010. ECOLOGICAL DISTURBANCES: THE GOOD, THE BAD AND THE UGLY. Abstract. This thesis focuses on the definitions, characterizations and quantifications of ecological disturbances, as well as hypotheses on their impacts on biological communities. The most prominent model on effects of disturbance on diversity is the Intermediate Disturbance Hypothesis (IDH), which is utilized in management of national reserves, has received over 3300 citations and has been corroborated by a multitude of studies from terrestrial and aquatic systems. According to the predictions of the IDH, diversity is high at intermediate levels of disturbance due to coexistence of competitors and colonizers. At low levels of disturbance diversity will be low due to competitive exclusion and few species can persist at high levels of disturbance. In an extension of the IDH, the Dynamic Equilibrium Model (DEM) predicts that the effects of disturbance depend on the productivity of communities, because at high growth rates a stronger disturbance is required to counteract increased rates of competitive exclusion. The IDH and the DEM were tested in a field experiment on effects of physical disturbance (scraping) and productivity (nutrient availability) on hard-substratum assemblages in paper I, where the patterns predicted by the IDH, but not the DEM, were observed. This outcome shows the importance of the nature of productivity alterations, as the productivity treatment had a general positive effect on growth rates but only marginal effects on the dominant species, thereby leaving rates of competitive exclusion unaffected. In paper II I tested another extension of the IDH, which predicts that smaller, more frequent disturbances will have different effects on diversity compared to larger, less frequent disturbances. In this experiment I used two different regimes of disturbance, small and frequent vs. large and infrequent disturbances, while the overall rate (the product of area and frequency) was kept equal for both regimes. At the site where the IDH was supported, the regime with a large proportion of the area disturbed infrequently showed higher richness, due to a stronger decrease of dominants, compared to the regime with a small proportion disturbed frequently. In addition to these significant differences in diversity effects between different disturbance regimes, it may also matter what agent of disturbance that is causing the damage. In paper III I contrasted the effects of a physical disturbance (wave-action) to that of a biological disturbance (grazing), as well as their respective interactions with productivity in a multifactorial design tested on natural epilithic assemblages. The composition of assemblages and the total species richness was significantly affected by physical disturbance and interactively by biological disturbance and productivity. The algal richness was significantly affected by productivity and biological disturbance, whereas the invertebrate richness was affected by physical disturbance. The results show, for the first time, that biological disturbance and physical disturbance interact differently with productivity due to differences in the distribution and selectivity among disturbances. In paper IV I investigate how the choice of diversity measure may impact the outcomes of tests of the IDH, which, surprisingly, has not previously been discussed. This was done by an extensive literature review and meta-analysis on published papers as well as by two different approaches to mathematical modelling. Both models support the IDH when biodiversity is measured as species richness, but not evenness. The meta-analysis showed that two-thirds of the published studies in the survey present different results for different diversity measures. Hence, the choice of diversity measure is vital for the outcome of tests of the IDH and related models. Key words: competitive exclusion; DEM; disturbance; diversity; evenness; IDH; marine assemblages; productivity; rate of disturbance; regime; species richness; Tjärnö, Sweden. 3 Ecological disturbances ISBN: 978-91-628-8200-6 Populärvetenskaplig sammanfattning Som den skamlöst fyndiga titeln syftar till så kan ekologiska störningar se väldigt olika ut och ha helt olika effekter på den biologiska mångfalden. Men innan vi ger oss i kast med en djupare tolkning av detta, bör vi bena ut vad en störning egentligen är. Exempel på vanliga störningar i naturen är skogsbränder, stormar, översvämningar, vågor, trålning, föroreningar, uttorkning samt istäcken och drivved som skrapar bort arter på hårda bottnar. Lite ibland räknas även biologiska störningar, d.v.s. djur som tuggar i sig andra djur och växter, eller djur som i ren illvilja eller okunskap trampar ihjäl levande varelser i sin väg. För att krångla till detta en smula så får inte allting som kan ge upphov till skada kallas för en störning, utan i likhet med samhället i stort finns även här vissa som är mer jämlika än andra. Definitioner på vad som får räknas som en faktisk störning finns det lika många som antalet GAIS supportrar; ungefär nio. Enligt den mest konkreta och lätthanterliga definitionen ska en störning döda eller avlägsna organismer i ett samhälle (område med samexisterande arter), och därigenom underlätta för nya arter att etablera sig. Den till synes harmlösa bisatsen om etableringsmöjligheter får oanat stor betydelse när man testar ekologiska förklaringsmodeller om störning och biodiversitet. Överlag sunda läsare undrar nu förmodligen vad i hela Hisingen en ekologisk förklaringsmodell är. Dessvärre kan jag inte skryta med att detta är lika komplicerat som det låter. En förklaringsmodell, eller hypotes, inom ekologi går helt sonika ut på att förklara ett fenomen eller samspel i naturen. I merparten av mina många experiment (tre) har jag undersökt om ’the Intermediate Disturbance Hypothesis’ (IDH) verkligen stämmer. Denna hypotes går i princip ut på att ’Lagom är bäst’ och passar därför väl in i den svenska kulturen. Anledning till att just lagom störning är bäst är att då finns flest antal arter, eftersom alla arter dör ut om det blir för mycket störning och att bara en art kommer ta över hela samhället om det inte finns någon störning alls. Det sistnämnda kallas ’konkurrensuteslutning’ och innebär, kanske inte helt otippat, att en art kan konkurera så effektivt att den utesluter alla andra arter ur ett område om ingenting stoppar den. Exempel på när detta sker i naturen är barrskogar och musselbankar, där en eller ett fåtal arter helt egoistiskt kan ta upp väldigt stora områden. Om en störning kommer in och dödar ett antal individer i dessa områden kan andra, nya, arter etablera sig på den nyligen frigjorda ytan eller marken. Antalet arter i området ökar då alltså, och är man lite fin i kanten kan man istället uttrycka detta som att den biologiska mångfalden höjts. En annan väldigt rolig hypotes, som bygger på den ovan nämnda IDH, kallas ’the Dynamic Equilibrium Model’ (DEM). Tillägget i denna hypotes är att mängden störning som är lagom beror på hur fort arterna i ett samhälle växer. Desto fortare arterna växer, desto kraftigare störning krävs för att bryta konkurrensuteslutning av någon självupptagen liten gynnare. Dessa två hypoteser, IDH och DEM, är vad jag, två GAIS:are och ett gäng ohängda tyskar testar på marina hårdbottensamhällen, bestående av anemoner, havsborstmaskar, havstulpaner, hydroider, musslor, mossdjur, svampdjur, sjöpungar samt grön-, brun- och rödalger, i den första artikeln i avhandlingen. De andra nagelbitarna till artiklar handlar även de om hypoteserna IDH och DEM, om än lite mer indirekt och med större fokus på själva störningsmekanismerna. Den näst första artikeln handlar om störningar som är lika stora i total omfattning, men där en störning som sker dubbelt så ofta då påverkar en hälften så stor yta. Skillnaden vi hittade här var att störning med stor yta som skedde mer sällan gav upphov till fler arter, eftersom detta mer effektivt 4 J. Robin Svensson kunde bryta de slemmiga sjöpungarnas konkurrensuteslutning. I det tredje experimentet slängde vi ett getöga på skillnaderna mellan samhällen på stenar som skrapar mot varandra i vågrörelser (fysisk störning), jämfört med samhällen på stenar som blir mumsade på av promiskuösa strandsnäckor (biologisk störning), samt vilken effekt dessa olika störningar får i samspel med hur fort samhällen tillväxer (produktivitet). Förutom att de olika typerna av störning interagerade på olika sätt med tillväxthastigheten, hade de även olika stor effekt djuren och växterna (algerna) i samhällena. Den fjärde och sista artikeln är mer lik en debattartikel, fast med stöd av matematisk modellering och en litteraturundersökning, där jag väldigt ödmjukt påstår att alla andra som jobbar med ekologiska störningar och biodiversitet gör fel, medan jag själv tvivelsutan gör allt rätt. Anledningen till felaktigheterna är att en del testar hypoteser om förändring i antal arter med ett mått på hur jämt arter är fördelade istället för hur många de är. Detta är lite som när Kurt Olsson frågade Patrik Sjöberg hur brett han har hoppat, eller som att räkna antalet äpplen i päronträd, makrillar i änglaklacken eller marxister i vita huset. Summan av kardemumman, efter ett halvt decennium på skattepengar och ett ointagligt rekord i spindelharpan, är alltså att effekterna av störning hänger på vilken slags störning som sker, hur man väljer att mäta den, samt vilka arter som finns i samhället där störningen inträffar. Vill man testa hypoteser om biodiversitet och störning lite grann, så spelar det även roll hur stark konkurrensen mellan arter och nyetableringen av arter är, samt vilket mått på biologisk mångfald som används i studien. 5 Ecological disturbances LIST OT PAPERS This thesis is a summary of the following papers: Paper I Svensson, J. R., M. Lindegarth, M. Siccha, M. Lenz, M. Molis, M. Wahl, and H. Pavia. 2007. Maximum species richness at intermediate frequencies of disturbance: Consistency among levels of productivity. Ecology 88:830-838. Paper II Svensson, J. R., M. Lindegarth, and H. Pavia. 2009. Equal rates of disturbance cause different patterns of diversity. Ecology 90:496-505. Paper III Svensson, J. R., M. Lindegarth, and H. Pavia. 2010b. Physical and biological disturbances interact differently with productivity: effects on floral and faunal richness. Ecology 91:3069-3080. Paper IV Svensson, J. R., M. Lindegarth, P. R. Jonsson, and H. Pavia. The Intermediate Disturbance Hypothesis predicts different effects on species richness and evenness. Manuscript. Papers I, II and III was reprinted with the kind permission of from the Ecological Society of America. 6 J. Robin Svensson What is ecological disturbance, really? .................................................................................. 8 Definitions of disturbance ...................................................................................................... 8 Agents of disturbance............................................................................................................. 9 Components and quantities of disturbance........................................................................... 11 Differences between Disturbance, Perturbation and Stress ................................................. 13 Ecological Theories on Disturbance ..................................................................................... 15 The Intermediate Disturbance Hypothesis (IDH) ................................................................ 15 The Dynamic Equilibrium Model (DEM)............................................................................ 17 Additional related models .................................................................................................... 19 Prerequisites for the IDH and the DEM .............................................................................. 21 Aspects of Colonization ....................................................................................................... 21 Aspects of Competition........................................................................................................ 22 Considerations of diversity.................................................................................................... 24 Conclusions ............................................................................................................................. 25 References ............................................................................................................................... 26 Acknowledgements................................................................................................................. 32 7 Ecological disturbances What is ecological disturbance, really? Since this thesis is entirely devoted to ecological disturbances, we might as well start at the beginning. That is, to elucidate the concept of ‘disturbance’. There are quite a few definitions of disturbance that I will explain and discuss in the first section, whereafter I move on to agents of disturbance, followed by measures and components of disturbance. An agent of disturbance is the instrument that causes the damage, such as an animal, waves or fire. The components of disturbance are the properties of the damaging force of the disturbance agent, i.e. the heat of the fire, the strength of the waves and the extent of borrowing by an animal. The issues regarding agents and components of disturbance are discussed in paper I and specifically tested in papers II and III. Should I not have failed entirely in my attempt at illuminating the audience on the topic of disturbance in these earlier sections, she or he will have an appropriate background for the following sections on ecological theories on disturbance. More specifically, I will sort out the most prominent hypotheses and models on the effects of disturbance on biodiversity, i.e. the Intermediate Disturbance Hypothesis (IDH) and the Dynamic Equilibrium Model (DEM), as well as a few related models on colonization and the specific components of disturbance. The IDH predicts maximum diversity at intermediate levels of disturbance, whereas the DEM predicts that the level of disturbance required to maximize diversity depends on the level of productivity. The IDH is tested by manipulative experimentation in papers I-III and theoretically evaluated in paper IV, and tests of the DEM is incorporated in the experiments in papers I and III. Furthermore, I will present and discuss a number of possible prerequisites, or assumptions, which these models may rely on. In conclusion, readers that have the stamina to go through the entire thesis will be handsomely rewarded by superior knowledge about definitions, agents and components of disturbance as well as of theories on disturbance and their associated predicaments. Hence, they will know what ecological disturbance really is. Definitions of disturbance There are quite a few definitions of disturbance, which may or may not help the reader depending on their complexity and explicitness. The most straightforward definition is that by Grime (1977), who defines disturbance as partial or total destruction of biomass. Although simplicity is something to strive for, especially to increase the operationalization of a definition for manipulative experiments, a too simple definition can include processes and mechanism that may in fact only have a marginal effect on species assemblages. The definition by Pickett and White (1985) where disturbance is “…any relative discrete event in time that disrupts ecosystems, community, or population structure and changes resources, substrate availability, or the physical environment”, is also very broad. Although this definition is undoubtedly more explicit, it still encompasses many events that occur naturally and frequently without necessarily have any measurable effects on either diversity or density of species. An extension to this definition was added by Pickett et al. (1989), in which “Disturbance is a change in the minimal structure caused by a factor external to the level of interest”. A benefit with this hierarchical view of disturbance is that one must consider the scale at which a certain disturbance operates. For instance, an herbivorous insect can be a disturbance to the leaves of a single tree, whereas if the study site is an entire forest it may be more relevant to consider wind-throws by hurricanes or large scale forest fires. However, this hierarchal view does not compensate for the drawbacks of the broadness of the original definition. Notable distinctions in definitions comes from of Pain and Levin (1981) and Reynolds et al. (1993), who argue that disturbance should be defined exclusively based on its measurable 8 J. Robin Svensson effect on ecological communities. In contrast to descriptions encompassing a range of different processes (c.f. Pickett and White 1985). According to Pain and Levin (1981), “Patch birth rate, and mean and maximum size at birth” can be used as “adequate indices of disturbance.” The definition of a ‘patch’ here is the primary substratum, i.e. space, that is affected by the disturbance. Similarly, Reynolds et al. (1993) defines disturbances as ”primarily non-biotic, stochastic events that results in distinct and abrupt changes in the composition and which interfere with internally-driven progress towards self-organisation and ecological equilibrium; such events are understood to operate through the medium of (e.g.) weather and at the frequency scale of algal generation times”. As indicated by the subordinate clause in this definition, it is explicitly intended for studies on phytoplankton, and the definition by Pain and Levin (1981) only holds for communities where primary space is the limiting resource. Hence, while both definitions are useful within their own fields of study, they will not hold for ecological studies on disturbance and diversity in general. The more operational definitions of disturbance include the alterations of resources as a consequence of a disturbing force. For instance, Shea et al. (2004) define disturbance as an event which “alters the niche opportunities available to the species in a system” by removing biomass and “freeing up resources for other organisms to use” or in any other way cause “a direct shift in available nutrients”. Similarly, Mackey and Currie (2000) define disturbance as “a force often abrupt and unpredictable, with a duration shorter than the time between disturbance events, that kills or badly damages organisms and alters the availability of resources”. The inclusion of freeing of resources is important because this is the characteristic of a disturbance which may ultimately lead to a positive effect on diversity, if the availability of resources enables, or maintains, coexistence in a community. According to Sousa (1984), disturbance is defined as “…a discrete, punctuated killing, displacement, or damaging of one or more individuals (or colonies) that directly or indirectly creates an opportunity for new individuals (or colonies) to become established.” Hence, instead of considering availability or resources, which may or may not affect recruitment, this definition goes straight to the core of the potential for a disturbance to mediate coexistence. That is, opportunities for recruitment created, directly or indirectly, by disturbance, because without new species recruiting into the space freed by disturbance diversity cannot increase (Osman 1977, Collins et al. 1995, Huxham et al. 2000). Thus, like many other researchers, I find this definition of disturbance to be the most practical and operational for investigations of patterns between diversity and disturbance. Consequently, the definition of disturbance by Sousa (1984) will be used throughout this thesis, with the addition that the disturbance should be ecologically relevant for the system under study. Similar to the arguments by Pickett et al. (1989), a disturbance should be considered in relation to scale, but also to relevance of agents and components of disturbance for the specific system and/or the phenomena the model or hypothesis is intended to explain. Agents of disturbance The mechanisms and processes that are inflicting damage upon species assemblages are called agents of disturbance. Commonly, researchers on disturbance distinguish between biological and physical agents of disturbance (McGuinness 1987, Wootton 1998, Sousa 2001), while some authors use more explicit subdivision (Menge and Sutherland 1987). In order to give a clear picture of what these agents are, I will describe some of the more common agents of disturbance used in previous studies. Examples of agents of physical disturbance include anoxia (Diaz and Rosenberg 1995), boat traffic (Willby et al. 2001), desiccation (Lenz et al. 2004), deposition (Miyake and Nakano 2002), drifting logs (Dayton 1971), erosion (Fox 9 Ecological disturbances 1981), fire (Eggeling 1947), floods (Lake et al. 1989), ice-scouring (Gutt and Piepenburg 2003), pesticides (Szentkiralyi and Kozar 1991), pollution (Benedetti-Cecchi et al. 2001), sediment movement (Cowie et al. 2000), temperature (Flöder and Sommer 1999), tilling (Wilson and Tilman 2002), trawling (Tuck et al. 1998), tree poisoning (Sheil 2001), tree lopping (Vetaas 1997), wind (Molino and Sabatier 2001), wave action (McGuinness 1987), and even warfare (Rapport et al. 1985). Biological disturbances are mainly predation (Talbot et al. 1978) and grazing (Collins 1987), although some authors add algal whiplash (Dayton 1975), burrowing (Guo 1996), disease (Ayling 1981), parasites (Mouritsen and Poulin 2005) and trampling (Eggeling 1947). Due to the differences among these agents of disturbance, agents are commonly divided into groups based on their functional or mechanical characterizations. Menge and Sutherland (1987) divide the agents of disturbance into four different groups: physical disturbance, physiological disturbance, biological disturbance and predation/grazing. Physical disturbance is produced by mechanical forces (e.g. movement of air, water, and sediment), whereas physiological disturbance is the lethal effects produced by biochemical reactions (influenced by e.g. temperature, light or salinity). Biological disturbance is the lethal effects of the activities of mobile animals (e.g. trampling, burrowing, and digging), and predation and grazing is defined as mortality resulting from consumption by animals. In a similar fashion, Wootton (1998) suggests that the effects of consumers should be considered separate to the effects from physical disturbance, because “the biota of the community is less likely to directly control the dynamics of the latter”. That is, agents of biological disturbance may be density dependent to a much higher degree than agents of physical disturbance. Fig. 1 Disturbance treatment in papers I and II. Physical scraping of settling panels removing all organisms from a given percentage (i.e. 20 or 40 %) of the panel at each disturbance event. 10 An even more important distinction between agents, than those given above, is based on their possibility for selectiveness in the damage they exert. Grazing and predation have been argued to be unsuitable agents of disturbance in studies on disturbancediversity patterns, because consumers, unlike physical agents, may have preferences in prey species (e.g. McGuinness 1987, Sousa 2001). Due to this predicament, Sousa (2001) J. Robin Svensson reserves the term disturbance to include “damage, displacement or mortality caused by physical agents or incidentally by biotic agents”, thus, excluding consumption by grazers and predators. Since this possible high degree of selectivity has no comparison in physical disturbances, outcomes of studies on disturbance using biological agents may be confounded and, therefore, not generally applicable. For instance, if a consumer prefers prey species that are inferior competitors, this biological disturbance will increase the rate of competitive exclusion instead of breaking the dominance of competitive superiors. This degree of selectivity may be even more complex in disturbance-diversity models that include productivity, i.e. the DEM, because grazers have been shown to prefer plants with higher nutrient content in both terrestrial (Onuf et al. 1977) and marine systems (Cruz-Rivera and Hay 2000). Accordingly, in paper III I show that a biological disturbance (grazing by periwinkles) and productivity interactively affected the number of macroalgal species, whereas the physical disturbance (wave-action) only affected the number of invertebrate species in natural marine epilithic assemblages. These patterns were, in part, explained by differences in the degree of selectivity between disturbances. Accordingly, the non-selective physical disturbance (scraping) in papers I and II (Fig. 1) affected all groups of species in the hard-substratum assemblages; annelids, barnacles, bryozoans, hydroids, mussels, seaanemones, sponges and tunicates, as well as green, brown and red macroalgae. Thus, in contrast to the plain distinction between biological and physical agents of disturbance, a more operationally beneficial distinction may be that between selective and non-selective agents of disturbance. Components and quantities of disturbance In relation to agents of disturbance, i.e. ‘what is disturbing’, there are also components of disturbance, i.e. ‘how is it disturbing’. These components, also called attributes (Shea et al. 2004), commonly differ in the way they are characterized and measured. According to Osman and Whitlach (1978), “a disturbance agent will have two components, frequency and magnitude”, where frequency is how often a patch is disturbed and the magnitude refers to the number of disturbed patches. Wootton (1998) identifies three components of disturbance “increasing average mortality, increasing temporal variability, and increasing spatial heterogeneity”. There are, however, many more components of disturbance. These may be divided into conceptual and operational terms of disturbance. The conceptual terms; level, intensity, severity, magnitude, regime, timing, and shape, are intended to verbally explain or describe aspects of disturbance, whereas the operational; frequency, extent, duration, time, size, rate and predictability, can be measured using their defined quantities (Table 1). The drawback with the inexplicitly defined conceptual terms is that they are not easily generalized among studies. For example, ‘intensity’ has been used to describe a variety of experimental manipulations and variables, such as penetration depth per bite by limpets (Steneck et al. 1991), type of mechanical scrubbing (McCabe and Gotelli 2000) and degree of oscillation in sediment (Garstecki and Wickham 2003). Similarly, ‘magnitude’ can be a general description, occasionally used synonymously to level, intensity and severity. However, magnitude can also be used for more specific measures, such as the number of patches affected by disturbance (Osman and Whitlatch 1978) and the percentage of biomass removed by floods (Kimmerer and Allen 1982). The fact that the units and meaning of disturbance can be unclear, and differ among studies (Pickett and White 1985, Sousa 2001, Shea et al. 2004), may be a consequence of the unclear formulations of the hypotheses the studies aim to test. This is because the most prominent models on patterns between disturbance and diversity (see section: ecological theories on disturbance) are conceptual 11 Ecological disturbances models based on relatively scaled variables (Schoener 1972, Peters 1991). However, in order to evaluate general ecological theories, it is important that concepts are commensurable among studies. Table 1 Conceptual and operational terms of disturbance commonly used in ecological studies. Term Meaning Quantity Conceptual Generic term for the types and components of disturbance currently acting in a given area - ‘level’ General description of overall amount of disturbance - ‘severity’ General description used synonymously to intensity and magnitude, and/or specific for damage caused - ‘intensity’ General description used synonymously to severity and magnitude, and/or specific for disturbing force - ‘magnitude’ General description, but also used synonymously to severity and intensity - ‘regime’ ‘timing’ ‘shape’ When a disturbance occurs and influence of the current conditions at that time Specific shape (i.e. oval, rectangular, square) of two- or three-dimensional space disturbed - Operational -1 ‘frequency’ Number of disturbance events per unit time time ‘time’ Period of time since last disturbance event time ‘duration’ The amount of time a disturbance event lasts time ‘phasing’ ‘predictability’ Temporal pattern of disturbance Variance in mean time between disturbances "S", i.e. time variance ‘size’ Size of an individual disturbance events ‘extent’ ‘rate’ Total two- or three-dimensional space disturbed Product of area and frequency area area or volume -1 area x time One effort to increase the commensurability among studies on disturbance is the proposal of the term ‘rate’ of disturbance by Miller (1982), where rate is the sum of the size of all disturbance events in a given area per unit time, i.e. the product of area and frequency of disturbance. This is comparable to the argument of Osman and Whitlach (1978), who suggested that disturbance is composed of the two components frequency and magnitude, although they did not suggest a general joint measure. Similarly, Petraitis et al. (1989) defines ‘intensity’ as the product of area and frequency (not be confused with the common definition of the term intensity; Connell 1978, Sousa 1984, Shea et al. 2004). Taking into account the combined effects of area and frequency is important, because information about one of these components makes little sense without the context of the other. For instance, specifying an experimental manipulation where a community is disturbed once a week is completely 12 J. Robin Svensson uninformative if we do not know the extent of the damage. Without doubt, the differences in effects on diversity will differ massively if the area disturbed each week is 1% of the total area compared to if it is 99%. However, disturbances composed of area and frequency are not the only ones that would benefit from a measure that combines the quantities of components. For example, in experiments on forest fires the temperature is vital for the effects on communities (e.g. Gignoux et al. 1997), and this can be combined with both the extent and the duration for increased commensurability among studies. Although the combined effects of disturbance components are always implicit in experimental studies, it is necessary to transform the measure of disturbance into a joint measure, i.e. rate, in order to put any experimental result into a wider context, and to allow for direct and meaningful comparisons among studies. The main benefit of careful specifications of the components of disturbance is that they give information of the manner in which a particular disturbance is exerted. Even for joint measures, such as rate, it is important to specify each component clearly. This is important because disturbances that are equal in extent can nonetheless have significantly different effects on diversity, depending on how the disturbance is distributed (Bertocci et al. 2005, papers II and III). In paper II I show that equal rates of disturbance may still give different patterns in diversity depending on the specific combination of area and frequency, i.e. the regime of disturbance. In accordance with the predictions by Miller (1982), the regime with small, frequent disturbances favoured colonizing species, whereas large, less frequent disturbances favoured competitive dominants. On a similar note, Bender et al. (1984) identified two different types of disturbance, pulse and press, defined as instantaneous alteration of species number (pulse) and the sustained alteration of species densities (press). The distinction between two clearly different mechanisms of disturbance, which may nonetheless be equal in total extent, can be useful for predictions of patterns of diversity. In paper III, the biological, continuous small-scale, disturbance (i.e. press) differed in effects on diversity from the physical disturbance, instantaneous removal or damage of individuals (i.e. pulse). This shows that clear specification of components of disturbance is important, because the way the damage of a given disturbance is exerted can be vital for the outcome of studies on disturbance-diversity patterns. Differences between Disturbance, Perturbation and Stress In ecological studies, the two concepts ‘perturbation’ and ‘stress’ are often used synonymously to disturbance (e.g. Connell 1978, Bender et al. 1984, Rapport et al. 1985). Processes and mechanisms that are generally described as disturbance may instead be classified as either perturbation (Webster and Patten 1979, Lane 1986) or stress (e.g. McGuinness 1987), and the terms perturbation and stress are often used interchangeably with disturbance without explicitly definitions of any of the terms (e.g. Caswell and Real 1987, Davies et al. 1999). Similarly, the term perturbation can be used to refer to the effects of stress on a system (Petraitis et al. 1989) and the term stress can be used to describe a perturbation (Odum et al. 1979). That these three terms are used haphazardly can be problematic, because definitions of ecological phenomena may be vital for experimental design in tests of hypotheses. Especially, since the concept of disturbance is in itself a quagmire, confounding it with stress or perturbation would be severely suboptimal. The most clear distinction among these three terms is that between disturbance and stress, where disturbance is generally considered to cause more severe damage (Grime 1977, Pickett et al. 1989, Wootton 1998). Among the most common mechanisms and processes 13 Ecological disturbances described as stress are desiccation (Dayton 1971), pollutant discharges (Rapport et al. 1985) and fluctuations in temperature (Jackson 1977), nutrients (Menge and Sutherland 1987) and light (Grime 1977). According to Grime (1977) stress in plant communities is defined as “the external constraints which limit the rate of dry-matter production of all or part of the vegetation”, which is clearly distinct from disturbance events that “limit the plant biomass by causing its destruction”. Wootton (1998) makes a similar distinction between stress and disturbance, where the upper limit of what can be defined as stress is mortality. Stress is here defined by “causing changes in performance as opposed to mortality”, and he states that stress can also “reduce conversion efficiency or increase metabolic costs”. This view is also shared by Sousa (2001) who states that the difference between disturbance and stress, although possibly caused by the same agent, is that disturbance only occurs when “an organisms tolerance is exceeded, resulting in its death or sufficient loss of biomass that the recruitment or survival of other individuals is affected”. Pickett et al. (1989) defines stress as a “change in the interaction maintaining a minimal structure”, caused “directly or indirectly by an external factor”. For example, an herbivorous insect can be a disturbance to a leaf by disrupting its physiological integrity, but a stress to the plant because leaf damage may affect the performance and reproduction of the plant. Thus, the same mechanism will be classified as either disturbance or stress depending on the level of interest (Pickett et al. 1989). Rapport et al. (1985) defines stress as “an external force or factor, or stimulus that causes changes in the ecosystem, or causes the ecosystem to respond, or entrains ecosystemic dysfunctions that may exhibit symptoms”. This definition is not among the more operational, since it is only applicable at the ecosystem level and it is not intuitive what a symptom of an ecosystemic dysfunction may be. Another thought-provoking definition of stress is that by Rykiel in which stress is “a physiological or functional effect; the physiological response of an individual, or the functional response of a system caused by disturbance or other ecological process; relative to a specified reference condition; characterized by direction, magnitude, and persistence; a type of perturbation”. Thus, according to this definition, stress is a type of perturbation that is the effect of disturbance. Here, I much prefer the views of Grime (1977), Wootton (1998) and Sousa (2001), where stress is generally distinguished from disturbance as nonlethal effects and responses. Agents of perturbation are commonly similar to those of disturbance and stress, such as flood scouring (Webster and Patten 1979), environmental variation (Lane 1986), alteration of species densities (Bender et al. 1984). Furthermore, this concept is also used for processes and mechanisms that are not easily defined, such as departure from a normal state (Pickett and White 1985), divergence in spatial organization of badger populations due to bovine tuberculosis (Tuyttens et al. 2000) and the falling of leaves on spider webs (Leclerc 1991). Moreover, the term unperturbed is used by Padisak (1993) to describe systems unaffected by either disturbance or stress. Although definitions of perturbation are scarce in the literature, there are a few notable exceptions. Rykiel (1985) defines perturbation as “the response of an ecological component or system to disturbance or other ecological process as indicated by deviations in the values describing the properties of the component or system; relative to a specified reference condition; characterized by direction, magnitude, and persistence”. Hence, according to Rykiel (1985) disturbance is the agent causing damage whereas perturbation, as well as stress, is the effects of a disturbance. Distinguishing between the cause and effect of disturbances is not unimportant, for instance, if a process defined as disturbance does not invoke any measurable response in the recipient community it is questionable whether a disturbance has really occurred. However, this interpretation of the terms has not been widely accepted, which is likely due to the rather counter-intuitive terminology of stress- and 14 J. Robin Svensson perturbation-causing disturbances. Another exception is the definition by Picket and White (1985), where perturbation is “a departure (explicitly defined) from a normal state, behaviour, or trajectory (also explicitly defined)”. Although this definition is rather unclear and exceptionally broad, it may in this case be both appropriate and useful. In the sense that Padisak (1993) uses the term, but in contrast to Rykiel (1985), it may be beneficial to reserve a word that describes process and mechanisms that can be either disturbance or stress, or in fact neither. Ecological Theories on Disturbance Disturbance has been recognized as a structuring force in ecological communities since the beginning of the last century (Cooper 1913). However, it was not until the 1970ies that disturbance was regarded as a key process in general ecological theory (Dayton 1971, Grime 1973, Levin and Paine 1974). Since then, a number of hypotheses have been proposed to address the involvement of disturbance in ecological phenomena. These hypotheses mainly concern succession and biodiversity (Connell 1978, Miller 1982, Dial and Roughgarden 1998), but also on evolutionary processes (Benmayor et al. 2008), biological invasions (Davis et al. 2000) and ecosystem functions (Cardinale and Palmer 2002). More recently, the productivity in natural communities, another key process in ecology (Connell and Orias 1964, Tilman 1980, Abrams 1995), has been suggested to act in concert with disturbance, which may explain more complex patterns in species diversity (Huston 1979, Kondoh 2001, Worm et al. 2002). The following sections will focus on the most common hypotheses and models on effects of disturbance on biological diversity, the interactive effects of disturbance and productivity, as well as possible assumptions or prerequisites that these models may rely on. The Intermediate Disturbance Hypothesis (IDH) The most prominent theory on disturbance, and possibly ecology in general, is the Intermediate Disturbance Hypothesis (IDH; Connell 1978) (Fig. 2). The original paper by Connell (1978) has been cited over 3300 times and the IDH also represents one of few well established ecological theories with an impact on management of marine and terrestrial national reserves and parks, e.g. Yellowstone National Park, USA (Wootton 1998). The origin of the IDH is, however, debated (Wilkinson 1999). Even though J. H. Connell is commonly credited as the originator of the IDH, his main argumentation relies on the much earlier work of Eggeling (1947) on patterns of diversity in African rain forests (see: Fig. 1 in Connell 1978). In his article, Wilkinson (1999) also identifies three well-known authors who all, prior to the work of Connell, discussed relatively higher diversity at some form of intermediate level of disturbance; E. P. Odum (1963), J. P. Grime (1973), and H. S. Horn (1975). Similarly, Osman (1977) identified “an optimal frequency of disturbance at which diversity is maximized” in his study on marine epifaunal communities, which he argues is caused by reductions at high and low levels of disturbance “because of a decrease in the number of species present or an increase in dominance”. Surprisingly, neither of Odum (1963), Grime (1973), Horn (1975) or Osman (1977) is cited in the review article by Connell (1978). The IDH predicts that diversity will reach its maximum at intermediate levels of disturbance, while remaining low at high and low levels of disturbance (Fig. 2). The rationale for this is that at low levels of disturbance strong competitors exclude competitively inferior species and communities are dominated by a few species. Intermediate levels of disturbance, however, disrupt competitive hierarchies by increasing levels of mortality and thus making free space 15 Ecological disturbances available for recruitment of competitively inferior species. At successively higher levels of disturbance, recruitment cannot balance the high levels of mortality and slow recruiting High Diversity B A Low A C High Disturbance B C Fig. 2 The hump-shaped pattern between disturbance and diversity as predicted by the Intermediate Disturbance Hypothesis (IDH). The mechanisms of the IDH are illustrated by settling panels (A, B and C) used in papers I and II. At point A diversity is low due to competitive exclusion, at point B coexistence is enabled by freeing space for new species, and at point C few species survive due to high level of disturbance. species disappear from the community. The drawback of this straightforward logic, and hence its conceptual appeal, is that it has received criticism from both empirical and theoretical studies for being too simplistic (Pacala and Rees 1998, Huxham et al. 2000, Shea et al. 2004). Furthermore, a literature review revealed that only 20 % of the studies on effects of disturbance on diversity showed the unimodal pattern predicted by the IDH (Mackey and Currie 2001). Nevertheless, the IDH has been supported in field experiments in terrestrial (e.g. Armesto and Pickett 1985, Collins 1987, Molino and Sabatier 2001), freshwater (e.g. Padisak 1993, Reynolds 1995, Flöder and Sommer 1999) and marine communities (e.g. Osman 1977, Sousa 1979a, Valdivia et al. 2005), as well as in laboratory experiments (e.g. Widdicombe and Austen 1999, Buckling et al. 2000, Cowie et al. 2000) and model evaluations (Petraitis et al. 1989, Dial and Roughgarden 1998, Li et al. 2004). In accordance with these studies, the characteristic hump-shape pattern between disturbance and diversity was observed in papers I, II and IV. The apparent simplicity of the IDH may, however, be slightly deceiving. There are, in fact, many aspects of the IDH and the way that disturbance may determine levels of diversity. Although I will spare the reader yet another section on components of disturbance, there are 16 J. Robin Svensson some fundamental differences among the mechanisms of disturbance in relation to the hypothesis that should be noted. For instance, how often a disturbance occurs (i.e. frequency), how large the disturbance is (i.e. area or extent) and time since the last disturbance (i.e. time). Even though they are all interrelated, through the main rationale of disrupting competitive exclusion, the underlying mechanisms may be different. In the case of frequency, high levels of diversity can be maintained if the disturbance events occur often enough to prevent any one species from achieving dominance, while not occurring so often that only few species can persist. When the extent of disturbance is considered, areas that are too large will eliminate all species, areas that are too small will have little or no impact, whereas intermediate areas may disrupt competitive exclusion and allow establishment of new species in the disturbed patches. In comparison, the time aspect states that high diversity will be observed at some point in time after recolonization of the disturbed area, but before the community returns to its successional climax (i.e. dominance by few species). The main difference here is commonly referred to as the ‘between patch’ vs. ‘within patch’ mechanisms (e.g. Wilson 1990), or sometimes as the resetting of a patch successional clock vs. the creation of a successional mosaic (e.g. Chesson and Huntly 1997). This distinction is articulated in a straightforward way by Wilson (1994): “A single patch does not have a frequency of disturbance, only a time since last disturbance”. Albeit a bit drastic, it has been suggested that the within patch aspect is not a mechanisms of coexistence, as much as a mere observation of succession (Wilson 1990, Wilson 1994, Chesson and Huntly 1997). In contrast, the successional mosaic, or between patch, explanation relies on disturbances occurring in a greater area, where disturbed patches are all in different stages of succession and may, thus, together compose a high regional diversity (Levin and Paine 1974, Chesson and Huntly 1997, Sheil and Burslem 2003). One way to resolve the discussion about the differences between the within-patch and the between-patch mechanisms of the IDH, could be to consider the different components of disturbance, i.e. how the damage from the disturbance is exerted. Bender et al. (1984) distinguishes between ‘pulse disturbance’, i.e. instantaneous alteration of species number, and ‘press disturbance’, i.e. the sustained alteration of species densities (see also section ‘Components and quantities of disturbance’). A press disturbance could unceasingly prevent competitive exclusion of a dominant species, which yields higher within-patch diversity. In contrast, a pulse disturbance would provide patches of different successional stages and ages (younger more r-selected and older more K-selected species), giving rise to the higher between-patch diversity. Hence, this subdivision of disturbance could perhaps be a missing link in the so far unresolved issue (see Sheil and Burslem 2003) of differentiating the withinpatch from the between-patch mechanisms of the IDH. The Dynamic Equilibrium Model (DEM) The Dynamic Equilibrium Model (DEM; Huston 1979, Kondoh 2001) relies on the same general coexistence mechanisms as the IDH (Fig. 3). At low levels of disturbance one, or few, species will dominate and exclude all other species, and at high levels of disturbance very few species can persist, while coexistence is possible at intermediate levels. The addition in the multifactorial model DEM is that the relationship between disturbance and diversity is modified by the level of productivity. Huston (1979) suggested that increased productivity, and thus growth rates of individuals and populations, means that a more severe disturbance is required to prevent competitive exclusion. Consequently, at low productivity, and slow growth rates, maximum diversity is observed already at low levels of disturbance because competitive exclusion occurs at a lower rate. Thus, the shape of the relationship between 17 Ecological disturbances disturbance and diversity is predicted to be of three general types: monotonically decreasing (at low productivity), unimodal (when productivity is intermediate) and monotonically increasing (when productivity is high). Although the DEM has not been experimentally evaluated nearly as much as the IDH, there are corroborating manipulative studies from aquatic as well as terrestrial systems (e.g.Turkington et al. 1993, Worm et al. 2002, Jara et al. 2006). However, in paper I, there was no effect on diversity of the manipulated increase in productivity, whereas maximum species richness was observed at intermediate levels of physical disturbance, in accordance with the IDH. This is likely explained by the productivity treatment, which, despite a general effect on growth rates of algae, did not affect the competitive dominants in the hard substratum assemblages. Thus, the rate of competitive exclusion was not measurably affected and more frequent disturbance was consequently not required to prevent exclusion of inferior competitors at high levels of productivity. Diversity High Low P-high Disturban ce P-intermediate High P-low Fig. 3 The patterns predicted by the Dynamic Equilibrium Model (DEM). At low levels of productivity, maximum diversity is observed already at low levels of disturbance due to low rates of competitive exclusion. At intermediate levels of productivity intermediate levels of disturbance is required, and high levels of productivity high levels of disturbance is required, in order to disrupt competitive exclusion by dominants and free resources for colonizing species. Similar to the IDH, agents and components of disturbance may influence the outcome of tests on the DEM. For instance, biological and physical agents may differ in selectivity (McGuinness 1987, Wootton 1998, Sousa 2001) and consumers often prefer prey with higher nutrient content (Emlen 1966, Onuf et al. 1977, Pavia and Brock 2000). One indication of a discrepancy between agents of disturbance is that interactive effects between biological disturbance and productivity has been observed in many studies from various environments (see Proulx and Mazumder 1998 and references therein), whereas tests of the DEM using physical disturbance have more variable outcomes (e.g. Turkington et al. 1993, Death and Winterbourn 1995, Death 2002, Jara et al. 2006). In paper III, in order to test for possible differences among agents, I contrasted the effects of a biological to that of a physical disturbance in an experiment on the DEM. Using natural sessile assemblages on boulders (i.e. epilithic communities) composed of invertebrates and macroalgae, I tested for interactive 18 J. Robin Svensson effects between productivity (high vs. ambient), physical disturbance (simulated wave-action at five distinct frequencies) and biological disturbance (grazing by periwinkles manipulated as absent or present). The number of algal species was interactively affected by productivity and biological disturbance, whereas the invertebrate richness was affected by physical disturbance only. This may in part be explained by difference in degree of selectivity between agents, but, more interestingly, also in the way the damage is exerted. When biomass is slowly reduced, as exerted by the biological, continuous small-scale disturbance (i.e. press disturbance; Bender et al. 1984), this effect can more easily be counteracted by increased growth of the affected organisms (Huston 1979, Kondoh 2001). In contrast, increased individual growth rate cannot easily compensate for instantaneous loss of individuals, as exerted by the physical disturbance (i.e. pulse disturbance; Bender et al. 1984). In accordance with these arguments and our results, Kneitel and Chase (2004), the only previous study that has tested for interactions of all three factors, also found that biological disturbance (predation), but not physical disturbance (drying), and productivity interactively affected species richness. Thus, agents and components of disturbance may not only influence disturbance-diversity patterns, but also the specific interactive effects between disturbance and productivity on biological diversity of natural communities. Additional related models The only model on effects of disturbance on diversity that specifically considers the different components of disturbance is that by Miller (1982). In his article, he introduces the term ‘rate’ of disturbance, i.e. the product of area and frequency, which, thus, takes into account the total amount of disturbance inflicted upon a community (see also section ‘Components and quantities of disturbance’). According to Miller (1982), small, frequent disturbances favour species with rapid vegetative growth (i.e. ‘competitors’), whereas large, less frequent disturbances favour species with high capacity for dispersal (i.e. ‘colonizers’) due to the differences in perimeter to area ratios among patches. Although Miller (1982) predominantly focuses on the area of disturbance, the other component of the rate, frequency, is equally important. Similar to variations in area, differences in frequency and timing of disturbance will influence the abundance and composition of natural communities (Sousa 2002). This is because species are likely to increase in abundance when the disturbance regime matches their preferred recruitment time (Underwood and Anderson 1994, Crawley 2004). Furthermore, because of the natural large variation in temporal distribution of propagules among species (Roughgarden et al. 1988, Underwood and Anderson 1994) a single large disturbance can only be colonized by the propagules that are available at the specific time when a limiting resource, i.e. space, is made free. In paper II I tested the model by Miller (1982), or more specifically if the specific combination if area and frequency matters even if the rate is kept constant. In accordance with the predictions by Miller (1982), the regime with small, frequent disturbances favoured colonizing species, whereas large, less frequent disturbances favoured competitive dominants. Thus, as is claimed in the title, equal rates of disturbance did cause different patterns in diversity. In a model on the importance of the timing of disturbance, Abugov (1982) introduces the concept of disturbance ‘phasing’. Abugov (1982) distinguishes between disturbances that are phased compared to those that are unphased. A phased disturbance means that all patches are cleared simultaneously, and the patches are termed to be ‘in phase’. Conversely, during unphased disturbance, the probability of a patch being cleared by disturbance is independent of the disturbance of other patches. Phased disturbances are considered to be more large scale disturbance events such as storms or forest fires, whereas constant predation is given as an 19 Ecological disturbances example of unphased disturbance. The outcome of Abugov’s model showed that highest diversity always occurred at intermediate levels of disturbance, regardless of the degree of phasing, but also that the diversity at any given level of disturbance depend on the degree of phasing. Furthermore, similar to the multifactorial model DEM, high levels of diversity was observed at intermediate degree of phasing at intermediate levels of disturbance. The idea of phasing is similar to that of temporal variability in disturbance, which has been shown to affect the community structure of benthic assemblages on rocky shores (i.e. Bertocci et al. 2005, but see: Sugden et al. 2007). It is also similar to the concepts of ‘Nonadditivity’ (Chesson 2000), ‘Storage Effect’ (Chesson and Huntly 1997) and ‘Spatiotemporal Niche Creation’ (Pacala and Rees 1998). The key argumentation in these concepts is that coexistence is enabled because different species utilize different spatiotemporal niches. The spatiotemporal niches may differ, depending on environmental fluctuations or disturbance, in the amount of available resources, the free space for settling and in their current stage of succession (Amarasekare et al. 2004, Roxburgh et al. 2004, Shea et al. 2004). Due to the suggestions of coexistence mechanisms that are consider to be alternative, the IDH and the DEM have been argued to give “inadequate, inconsistent, or improbable explanations” of species coexistence (see: Chesson and Huntly 1997). However, the main mechanism of coexistence in all these concepts, including phasing and temporal variability, is that different patches are at different successional stages and/or differ in availability of resources. Hence, it could be argued that they are all describing the ‘between-patch’, or ‘successional mosaic’, aspect of the IDH, where coexistence is maintained, or enabled, by disturbance, because patches at different stages in succession differ in species composition. In their investigation of the theoretical validity of the IDH, Dial and Roughgarden (1998) found what they call ‘the intermediate area hypothesis’ and ‘the intermediate recruitment hypothesis’. In contrast to most other models on disturbance (Petraitis et al. 1989, Chesson and Huntly 1997, Kondoh 2001), their mathematical model incorporates the dynamics of pelagic larvae and benthic adults, as well as hierarchal competition for the limiting resource space. The larval-benthic dynamics was purposely considered because the pattern predicted by the IDH is often observed in communities where species have long-lived propagules and space-limited adults, such as marine invertebrates, macroalgae and seed plants (Sousa 1979a, Sousa 1979b, Molino and Sabatier 2001, Jara et al. 2006). More specifically, in these systems the disturbance only affects the sessile adults, while leaving the propagule mortality unaffected (Dial and Roughgarden 1998). The two key points of the outcome of the model was that the IDH is a moderate to high settlement phenomenon, and that a subordinate species must have an adaptation allowing it to survive and/or colonize at levels of disturbance that are lethal to the dominant, if disturbance, area, or settlement is to allow coexistence. According to Dial and Roughgarden (1998), these two key points show that the IDH is not a universal phenomenon, which also leads to the additional outcome of the model, the intermediate area and recruitment hypotheses. If the level of disturbance, at an intermediate value, is kept constant, intermediate levels of recruitment lead to coexistence among species. This is explained by the exclusion of the subordinate species of a dominant superior at high recruitment, and at low recruitment the dominant cannot exist. However, in their model, area is equivalent to settlement, thus, yielding a similar intermediate area effect, where smaller habitats can favour subordinate species’ coexistence with a dominant species. Although it could be argued that the proposed hypotheses are in fact already inherent functions of the IDH, since diversity cannot increase if no new species settle (Osman 1977, Huxham et al. 2000, papers II and III), it may still be noteworthy to point out that disturbance is not the only way exclusion can be prevented and coexistence maintained. Furthermore, it gives important 20 J. Robin Svensson insights in the underlying mechanisms of coexistence for the IDH, as well as the possible prerequisites for observing the pattern predicted by the IDH discussed in the next section. Prerequisites for the IDH and the DEM In response to the inconsistencies in the outcome of manipulative tests of the IDH (reviewed by Mackey and Currie 2001), several authors have suggested that the predictions of the IDH relies on a number of prerequisites. The most common prerequisites, or assumption, are competitive exclusion (Fuentes and Jaksic 1988), large regional species pool (Osman 1977), multiple stages in succession (Collins and Glenn 1997), nonlinear resource use (Chesson and Huntly 1997), availability of spatiotemporal niches (Pacala and Rees 1998) and trade-offs between competition and tolerance (Petraitis et al. 1989) and between competition and colonisation (Dial and Roughgarden 1998). Furthermore, Menge and Sutherland (1987) argued that the effects of disturbance depends on the amount of environmental stress in the system. However, the constructive criticism in the suggestions of the prerequisites primarily concerns aspects of two key processes; competition and colonization. Aspects of Colonization According to Dial and Roughgarden (1998), the IDH is a ”moderate-to-high settlement phenomenon”, and Collins et al. (1995) pointed out that it is settlement by propagules that may allow for increases in diversity, not disturbance per se. That colonization is important in order for disturbance to have a positive effect on diversity is intuitive and logic. Diversity cannot increase if there are no available propagules to occupy the space, or any other limiting resource, which is freed by disturbance (Sousa 2001). Another suggested prerequisite, that is equally straightforward, but maybe less intuitive, is the importance of a large regional species pool (Osman 1977). This is because diversity cannot increase if the propagules that establish in the cleared space, are the same species that originally inhabit the assemblage. This was clearly shown in a manipulative experiment by Huxham et al. (2000), where the species pool in the intertidal macrofaunal communities was too small to allow for settlement of new species in the assemblages subjected to disturbance. Low rate of colonization is also something that may explain the lack of positive effects of disturbance on diversity in paper III and at one of three sites in paper II. In the experiment on the effects of physical and biological disturbance and productivity on natural epilithic assemblages (paper III), the recruitment of new species occurred at a rate that was not sufficient to counteract the negative effects of disturbance. Similarly, in paper II, the physical disturbance did not have a significant effect on the richness of the hard substratum assemblages at one site, where richness was generally low and new species did not settle in disturbed patches. In contrast to paper III, this experiment was setup in the waters of the Tjärnö archipelago, where the regional species pool and availability of propagules per definition was natural. However, it has previously been shown that local hydrodynamics in areas near this site may hamper the settling of invertebrate larvae (Berntsson et al. 2004, Jonsson et al. 2004), which also could explain the surprisingly low total cover in the controls assemblages at this site. Thus, local hydrodynamics may be of equal importance to the availability of propagules and the size of the regional species pool, for the outcome of manipulative experiments on the effects of disturbance on diversity. 21 Ecological disturbances Aspects of Competition The other key process in the suggested prerequisites, competition, was mentioned already by Connell (1978), who considered competitive exclusion to be an assumption for the coexistence facilitating mechanism of disturbance. Similar to the arguments for colonization, disturbance cannot increase diversity if there is no exclusion process to interrupt by removing the dominant(s) and allow new species to establish in a community (Huston 1979, Sousa 1984, 2001). This is also linked to the suggested trade-off between competition and colonization. If the inferior species cannot out-compete the dominant at colonizing newly freed substrata, competitive exclusion may not be prevented and diversity will not increase in response to disturbance (Dial and Roughgarden 1998). Similarly, for the trade-off between competition and disturbance tolerance, the inferior species must be better adapted to cope with destructive events, either by physiological tolerance or other means such as fast growth and re-colonization (Petraitis et al. 1989). Thus, in order for a disturbance to facilitate coexistence, the dominant species must be comparatively more susceptible to the damage exerted. Furthermore, the dominant species must also be able to maintain their competitive advantage in the absence of disturbance (Connell 1978). The importance of competition for the outcome of experiments on disturbance is clearly shown in paper II, where the three different responses to disturbance at the three different sites clearly corresponded to the differences in species composition (fig. 4). Competitive exclusion was evident at the site where support for the IDH was found, as also observed in paper I, whereas increasing levels of disturbance only decreased diversity at the site lacking clear dominants in the undisturbed controls. Although assemblages at the third site also lacked dominants, there was no effect of disturbance because the initial diversity was so low that even the limited colonization in this area could counteract the effects of disturbance. Consequently, the same disturbance can give widely different patterns in diversity depending on the composition of species, and the level of competition, in communities. In order to disrupt the competitive advantage of dominants, the destructive event of a disturbance must potentially affect all species in a similar manner, or, conversely, fall heavier on the competitive dominants. The problem with possible selectivity of agents has been discussed for manipulations of disturbance, but not for manipulations of productivity. This lack of considerations of selectivity in agents may severely confound tests of the DEM. The DEM predicts that competitive exclusion will increase with productivity, thus requiring a stronger disturbance to be disrupted, but if the inferior competitors are more strongly affected by the productivity treatment this could instead slow down the rate of exclusion. This would cause diversity to peak at lower, rather than the predicted higher, intensities of disturbance. The issue of the selectivity of agents of productivity was clearly shown in paper I, where the IDH was supported, but the DEM was not. The most likely explanation for this outcome is that the dominant species exerting competitive exclusion, the tunicate Ciona intestinalis, was unlikely to benefit from the manipulation of nutrient availability. Hence, even though the productivity treatment had a general, positive, effect on growth rates in the assemblages, the rate of competitive exclusion did not increase, and higher levels of disturbance was consequently not required to maximize diversity. Even in studies that recognize the issue of selectivity, there is a practical difficulty of designing a non-selective agent of productivity in manipulative experiments. Experimental manipulation of productivity in tests of the DEM is commonly done indirectly, i.e. by adding nutrients or organic matter (Turkington et al. 1993, Widdicombe and Austen 2001, Worm et al. 2002, Kneitel and Chase 2004, Jara et al. 2006, Canning-Clode et al. 2008, Sugden et al. 2008). In such manipulations it is necessary to test independently whether the actual experimental treatment (the adding of nutrients or organic matter) has an effect on productivity. Without evidence for an actual increase in productivity 22 J. Robin Svensson a 10 Species Richness b Site 1 Site 2 Site 3 9 8 7 6 5 4 0 5 10 15 20 25 Rate of Disturbance 30 (cm2 35 40 45 / week) Fig 4 Three significantly different communities at sites 1, 2 and 3 which showed three different responses to disturbance in paper II. (a) Species composition, as well as pictures, of the control assemblages at sites 1, 2 and 3 and (b) responses to rates of physical disturbance, significant quadratic and linear quadratic components, respectively, at sites 1 and 2, and no significant pattern at site 3. 23 Ecological disturbances experiments cannot perform an adequate test of the DEM, and without information on the selectivity of the agent of productivity the outcome of tests cannot be adequately interpreted. Unfortunately, this issue is generally overlooked (e.g. Widdicombe and Austen 2001, Scholes et al. 2005, Jara et al. 2006). Nevertheless, if predictions about effects of productivity and disturbance on diversity are to be tested in field experiments, indirect manipulations, such as adding nutrients or organic matter, may be the only conceivable solution. Considerations of diversity Something that is conspicuously absent in the literature is a discussion on the potentially large variation in outcomes among studies depending on the measure of diversity that is used in tests of the IDH. As discussed in the earlier sections, nearly every aspect of disturbance has been considered, e.g. the definitions, the agents, the components, the quantities, how the damage from disturbance is exerted and a multitude of prerequisites have been suggested to explain inconsistencies in outcomes of the IDH. In addition, many other aspects of the IDH have been discussed, such as alternative mechanisms underlying coexistence (Pacala and Rees 1998), influence of the characteristics of communities (Fuentes and Jaksic 1988), interactive effects of disturbances (Collins 1987), importance of the specific traits of individual species (Haddad et al. 2008) and the context dependence of intermediacy (Shea et al. 2004). Yet, despite over 3300 citations of Connell (1978) and ample attention in the scientific literature, no one has considered the response variable for the conceptual model IDH, i.e. the aspect of diversity. Consequently, in paper IV I investigated how the measure of diversity may affect the outcome of studies on effects of disturbance on diversity. This was done by scrutinizing the original formulations of the models, conducting a meta-analysis of previously published studies and through two different approaches to mathematical modelling. In the formulation of the IDH, Connell (1978) uses the word diversity without any further definition, while Huston (DEM; 1979) rejects all various indices and considers diversity to be solely richness and evenness. In the model presented by Miller (1982) diversity is defined as a measure that includes both “species abundance and number”. However, neither Huston nor Miller makes an effort to explain what kind of effects disturbance would have on species abundances in contrast to the number of species. In the meta-analysis I investigated if all measures of diversity show the same response in studies that use two or measures of diversity within the same experiment. The mathematical modelling was performed using one already established spatially implicit model (Kondoh 2001) and one spatially explicit automation model, in order to specifically contrast the responses to disturbance of the two major components of diversity: richness and evenness. Both models support the IDH when biodiversity is measured as species richness, but, in contrast, predict that evenness increases monotonically with increasing levels of disturbance. The meta-analysis showed that two-thirds of the published studies in the survey present different results for different diversity measures, and the comparisons between richness and evenness showed an even higher degree of dissimilarity. In addition, when the analyses from papers I and II were rerun to include evenness as response variable (these results were not included in any of the papers), the same patterns as in the models emerges. Hence, in accordance with the predictions of the two model, species richness was maximized at intermediate levels of disturbance, and evenness showed linear increases with increasing rates of disturbance (Evenness: linear component MS=0.95, F=28.7, p<0.01; MS=1.75, F=81.8, p<0.01, respectively, quadratic component MS=0.010, F=0.30, p=0.58; MS=0.0052, F=0.24, p=0.63, respectively, Fig. 5). Thus, the meta-analysis, as well as the 24 J. Robin Svensson mathematical two models and the re-analysis of previous field experiments clearly show that the measure of diversity is vital for outcomes of tests of the IDH. 0,4 16 0,35 14 0,25 10 0,2 8 6 Richness 4 Evenness 0,15 Evenness 0,3 12 0,1 7 0.7 0.6 6 Evenness 5 0.4 0 0,0 0,2 0,4 0,6 0,8 4 1,0 20 0.00 d 1,2 0.3 0.20 0.40 0.60 0.80 9 0.8 14 0,8 Richness 12 Evenness 10 0,6 8 0,4 6 4 0,2 Evenness 1 Species Richness 18 16 1.00 0.7 8 0.6 7 0.5 Richness 6 Evenness 5 Evenness 0 Species Richness 0.5 Richness 0,05 2 b c Evenness 18 Species Richness Species Richness a 0.4 0.3 2 0 0 0,0 0,2 0,4 0,6 Magnitude of Disturbance 0,8 1,0 4 0.00 0.2 0.20 0.40 0.60 0.80 1.00 Frequency of Disturbance Fig. 5 Hump-shaped patterns between species richness and disturbance, but linear increases in evenness, in the two models from paper IV (a and b) as well as the re-analyzed results from the field experiments in papers I (c) and II (d). Conclusions In this thesis I have clearly (i.e. hopefully) shown that the definition of disturbance can influence the outcome of studies, depending on which characteristics of disturbances a particular definition encompasses. The type of agent that is causing the disturbance is crucial, because selectivity can differ among disturbance agents and biological agents may choose prey depending on nutritional value. Different components of disturbance can affect communities in different ways, and even the specific proportions of area and frequency within the same rate of disturbance can cause different patterns in diversity. The effects of disturbance will also to a large extent depend on the species composition of the community upon which it is inflicted. In tests of hypotheses on disturbance-diversity pattern, outcomes are generally influenced by the rate of competition, the availability of propagules, the regional species pool and interactions with the abiotic environment. Experimental tests of models that include productivity should also include explicit investigations of whether the manipulative treatment significantly affects the overall productivity, as well as the recognition of the possible selectivity of productivity agents. Furthermore, the measure of diversity used as response variable is vital for the outcome of tests of hypotheses on effects of disturbance on diversity. Clearly, there are many aspects to consider in experimental design and interpretation of results in disturbance-diversity studies. Consequently, in order to increase the generality and commensurability among studies, it will be of great benefit if experimenters (i) define the type of disturbance used in the study, (ii) assign ecologically relevant agents of disturbance and productivity with quantifiable components, (iii) recognize the characteristics of the community the disturbance is inflicted upon, and (iv) specify, and justify, the measure of diversity to be used in tests of hypotheses on effects of disturbance on diversity. 25 Ecological disturbances References Abrams, P. A. 1995. Monotonic or Unimodal Diversity Productivity Gradients - What Does Competition Theory Predict. Ecology 76:2019-2027. Abugov, R. 1982. Species diversity and phasing of disturbance. Ecology 63:289 – 293 Amarasekare, P., M. F. Hoopes, N. Mouquet, and M. Holyoak. 2004. Mechanisms of coexistence in competitive metacommunities. American Naturalist 164:310-326. Armesto, J. J. and S. T. A. Pickett. 1985. 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Detta trots initierandet av ett mått på en tillsynes kvantifierbar tidsrymd kallad ”nästa vecka”, där saker som utlovas hända inom denna tidsrymd, namnet till trots, aldrig inträffar veckan efter det yttrades. Mina kunskaper inom kvantfysik, parallella universa och strängteori är väldigt begränsade, men jag antar att det är någon ytterligare dimension här som jag ännu inte fått grepp om. Ett annat bra knep, som utövas i den icke-omänskliga tidsrymden, har beskrivits av förbipasserande finlandssvenskar som ”Vad fan gör ni på era möten egentligen? Ni sitter helt tysta och stirrar förvirrat upp i taket varje gång man går förbi!”. Förutom att detta är ett tydligt tecken på total inkompetens från alla inblandade, har det även lett till storslagna vetenskapliga genombrott som av internationellt erkända forskare officiellt benämnts som ”a fundamental flaw in the authors logic” och ”the conclusions of the work are not supported by the data”. Trots att 50 % av handledarna föreslog kollektivt självmord som respons på kritiken, röstades detta förslag (uppenbarligen) ned av hela 67 % av de mer livslustsfyllda medförfattarna. Mer konkreta framsteg är kunskapsöverflyttning från Nycklebybor till Majornabor inom statistikens svårbegripliga värld, där ofattliga akronymer (CAP, SNK, MDS, anova, permanova) lärts ut med ett leende på GAIS-läpparna, citerandes en mer filosofisk approach som i stora drag går ut på att ’tortera datan med olika analyser tills den erkänner’. Det hemliga epitetet ’HH’, som visat sig vara helt oförknippat med 30-talets Centraleuropa, har även lömskt, genom att tvinga fram oändligt många versioner av varje manus, lärt mej tekniken för gränslös episkhet oberoende av data. Lite som när Daniel Larusso vaxade Kesuke Miyagi’s bilar, svärandes samt ovetandes om tragglandets potentiella storhet. Framåt slutet i en tillsynes oändlig GAISdimma har det även funnits en Åtvidabergiansk fyr, i vars ljus planer smitts, modeller uppkommit, hypoteser utbenats och elektronisk post besvarats, smått chockerande, redan samma dag. Slutklämligen, utan er hade detta aldrig gått. Flertalet kemiekologiska G-människor har funnits vid min sida där stöttande aktiviteter inte bara inneburit balkongvistande rusdrycksinmundigande, utan även nakenbadande, trolldegsskapande, kemisk analys-assistans, vågmaskinssnickrande, hälsovådliga undervattensaktiviteter, nikotin-snikande, tröstlöst trålletande, fältmässigt Jägermeister shottande och klippstrands överblickande butterkaksätande. Till detta gäng hör även min kontorssambo som inte bara guidat mej genom hela Honshu och Hokkaido, utan även förklarar för mej obegripliga saker som projektuppföljning i datalagret och elektronisk fakturahantering. I Tjärnös begynnelse fanns smålänningar och dalmasar, men även nollåttor, Disney-karaktärer och finnar av båda kön. Skåningar, som det finns alldeles för många av, har lyckligtvis befunnits på behörigt avstånd, men som trots detta, och gärna i kombination med en viss smålänning, ständigt lyckas leta upp en och håna ens fiskekunskaper. There has also been a sensei in the underappreciated art of sandwich making, who relentlessly remind me that things are rarely as good as they seem, and his beloved wife who initially adopted me as a second boyfriend, only to leave me heartbroken for Sverker’s southern regions. Eftersom det finns ett oändligt antal oidentifierbara kräk och slemmiga växter i havsdjupen har jag varit helt beroende de barmhärtiga samariterna Elisabet, Anneli, Fredrik P och Hans-G. I stark kontrast till mentala prövningar finns en slagsmålsklubb som äger rum på Tjärnö skola varje onsdag, där revben brutits, blåa ögon mottagits och utdelats av Per B, Erik B, Swantje, Greg, Fidde, Micke, Lars, Finn, Petri, Tuuli, Ankan, Erkan, Göran, Gunnar, Henke, Mats, Martin G, Martin S, Malin, Piff, Puff, Erika, Andreas, Anders, Geno, Josefin, Carl-Johan, Johanna, 32 J. Robin Svensson Johan E, Johan H, Johan R, Johan W, Hanna H, Hanna S, Eva-Lotta, Mia, Filip, Stina, Rickard Lasse Pereyrasson och många, många fler. I slutet på flertalet välbehövliga flyktförsök från en öde ö fanns ett stadsdelsstort högkvarter idogt bevakat av MB, Åsmund, DAF, Pejlert, Mr. Däjvid, Greken samt även Ryssen och Dödskristian, där i rusdryckernas glada brödraskap energi återskapats, smärta och glädje delats och livslånga minnen bildats. Nästgårds har jag även funnit landets vänaste prinsessa som, förutom av mej påtvingad korrekturläsning, håller mej på topp genom överraskningsbrottning likt Kato i Clouseaus kylskåp, och som dragit upp mej ur träsket och visat mej en värld fylld av ’hummer och rosa champagne’. Till sist min familj som funnits där, inte bara under doktorand-perioden, utan alltid. 33 Paper I Paper II PAPER Paper III I Paper IV Paper V “I have opinions of my own, strong opinions, but I don't always agree with them.” - George H. W. Bush Paper VI Ecology, 88(4), 2007, pp. 830–838 Ó 2007 by the Ecological Society of America MAXIMUM SPECIES RICHNESS AT INTERMEDIATE FREQUENCIES OF DISTURBANCE: CONSISTENCY AMONG LEVELS OF PRODUCTIVITY J. ROBIN SVENSSON,1,5 MATS LINDEGARTH,1 MICHAEL SICCHA,2 MARK LENZ,3 MARKUS MOLIS,4 MARTIN WAHL,3 1 AND HENRIK PAVIA 1 Department of Marine Ecology, Göteborg University, Tjärnö Marine Biological Laboratory, 452 96 Strömstad, Sweden 2 Institute for Geological Science, Eberhard Karls University Tübingen Sigwartstr.10, 72076 Tübingen, Germany 3 Leibniz-Institute for Marine Science, Düsternbrooker Weg 20, 24105 Kiel, Germany 4 Biologische Anstalt Helgoland, Alfred Wegener Institute for Polar and Marine Research, Marine Station, Kurpromenade 201, 27498 Helgoland, Germany Abstract. Development of a mechanistic understanding and predictions of patterns of biodiversity is a central theme in ecology. One of the most influential theories, the intermediate disturbance hypothesis (IDH), predicts maximum diversity at intermediate levels of disturbance frequency. The dynamic equilibrium model (DEM), an extension of the IDH, predicts that the level of productivity determines at what frequency of disturbance maximum diversity occurs. To test, and contrast, the predictions of these two models, a field experiment on marine hard-substratum assemblages was conducted with seven levels of disturbance frequency and three levels of nutrient availability. Consistent with the IDH, maximum diversity, measured as species richness, was observed at an intermediate frequency of disturbance. Despite documented effects on productivity, the relationship between disturbance and diversity was not altered by the nutrient treatments. Thus, in this system the DEM did not improve the understanding of patterns of diversity compared to the IDH. Furthermore, it is suggested that careful consideration of measurements and practical definitions of productivity in natural assemblages is necessary for a rigorous test of the DEM. Key words: competitive exclusion; disturbance; productivity; species richness. INTRODUCTION Spatial and temporal patterns of diversity in natural communities are central themes in classical natural history as well as in contemporary theoretical ecology (e.g., Huston 1994, Hubbell 2001). Throughout history the magnitude of existing biological diversity and its heterogeneous distribution have continuously challenged ecologists to develop and test models to explain patterns at a multitude of temporal and spatial scales, using increasingly more complex models (e.g., Connell 1978, Huston 1994, Hubbell 2001). Some of these models have been based on biological interactions (e.g., Miller 1958, Fischer 1960, Paine 1966, Paine and Vadas 1969, Menge and Sutherland 1987), while others have primarily focused on abiotic processes (e.g., Hutchinson 1961, Levin and Paine 1974, Connell 1978, Paine and Levin 1981). Many of these ideas rely on disturbances to disrupt the effects of biological interactions, such as competitive exclusion, on diversity. A variety of abiotic (e.g., fire, wind, wave action, and drifting logs) and biotic factors (e.g., grazing, predation, and trampling) may act as agents of disturbance, depending on the specific Manuscript received 8 June 2006; revised 25 September 2006; accepted 29 September 2006. Corresponding Editor: S. G. Morgan. 5 E-mail: [email protected] 830 properties of the particular ecological system. There is also a range of definitions of what constitutes an actual disturbance. Grime (1977) defined disturbance as partial or total destruction of biomass. Sousa (1984) extended this definition by adding that disturbance also creates opportunities for new individuals to become established. Pickett and White (1985) have a broader definition where disturbance is ‘‘. . . any relative discrete event in time that disrupts ecosystems, community, or population structure and changes resources, substrate availability, or the physical environment.’’ Thus, despite some ambiguity in the definition of the concept of disturbance, it has direct effects on vital rates and population dynamics and it is therefore a potentially useful generalization. One important conceptual formulation of the effects of natural disturbances on diversity is the intermediate disturbance hypothesis, IDH (Connell 1978). The IDH predicts that diversity will be large at intermediate rates of disturbance and smaller at higher and lower rates of disturbance. The rationale for this idea is that at low rates of disturbance strong competitors exclude competitively inferior species and communities are dominated by a few species. Intermediate rates of disturbance, however, disrupt competitive hierarchies by increasing rates of mortality and thus making free space available for recruitment of competitively inferior species. At successively higher rates of disturbance, recruitment April 2007 DISTURBANCE, PRODUCTIVITY, AND DIVERSITY cannot balance the high rates of mortality, and slowrecruiting species disappear from the community. Findings consistent with the predictions of the IDH have been made in manipulative studies in both terrestrial (e.g., Molino and Sabatier 2001, Anderson et al. 2005) and marine (e.g., Osman 1977, Sousa 1979, Valdivia et al. 2005, Patricio et al. 2006) ecosystems. However, contradictory observations have also been made (Lake et al. 1989, Collins et al. 1995, Gutt and Piepenburg 2003), and due to difficulties of incorporating all components of natural environments, laboratory studies are often relatively less supportive (Cowie et al. 2000). In summary, the IDH has been an influential concept in research and also as a tool in management of nature reserves (Wootton 1998). In response to observations that did not appear consistent with the IDH, Huston (1979) suggested that the relationship between disturbance and diversity is modified by the level of productivity. Using a dynamic equilibrium model (DEM), Huston (1979, later elaborated by Kondoh 2001) suggested that increased productivity, and thus growth rates of individuals and populations, means that a more severe disturbance is required to prevent competitive exclusion. As a consequence, maximum diversity is observed at lower intensities of disturbance when productivity is low, compared to when productivity is high. The shape of the relationship between disturbance and diversity may therefore be of three general types: monotonically decreasing (at low productivity), unimodal (when productivity is intermediate), and monotonically increasing (when productivity is high). These three types of relationships have been observed in various habitats (e.g., Mackey and Currie 2001), but evidence from explicit manipulative studies demonstrating the interactive effects of disturbance and productivity is scarce (Rashit and Bazin 1987, Widdicombe and Austen 2001). One pioneering test in marine rocky environments is the study by Worm et al. (2002), who observed interactive effects of nutrient enrichment and disturbance (grazing by mesoherbivores) on algal diversity, which they found consistent with those predicted by the DEM. The development from a simple general model involving only one factor, into a more complex and detailed model involving multiple factors, may represent important conceptual progress within a field of research (e.g., Hilborn and Mangel 1997, Underwood 1997). The benefit of a more complex model is that it may be used to accurately predict a more diverse set of conditions with little discrepancy due to approximation (Zucchini 2000). There are, however, no guarantees that a complex model is more powerful than a simple one (e.g., Zucchini 2000, Ginzburg and Jensen 2004). This is because a complex model has a greater uncertainty, as it requires more parameters to be estimated. Thus, in terms of predictive power, the utility of a complex model relies on whether the reduction of error due to approximation is larger than the increase in error due to estimation. 831 Indeed, from observational data it appears that the great range of observed responses of diversity to disturbance (Mackey and Currie 2001) can potentially be more accurately represented if productivity is included (Huston 1979). Whether this really is the case in a wide range of ecological systems remains to be tested in manipulative experiments. In this study we contrast predictions from the IDH to those of the DEM in a marine hard-substratum community. Physical disturbance and nutrient availability were manipulated in subtidal communities in the field, with seven distinct frequencies of disturbance and three levels of nutrient availability. Manipulative studies on epibenthic assemblages have made important contributions to the development and testing of general ecological models (e.g., Paine 1966, Dayton 1971, Lubchenco and Menge 1978, Sousa 1979). Due to their potential for quick recovery, epibenthic assemblages have proven particularly useful for investigating disturbance–diversity patterns over ecologically relevant time scales in manipulative studies (e.g., Worm et al. 2002, Bertocci et al. 2005, Jara et al. 2006). MATERIALS AND METHODS Study site The field experiment was conducted in the vicinity of Tjärnö Marine Biological Laboratory on the west coast of Sweden. The experimental sites were two bays located ;1 km apart (58852.92 0 N, 1188.31 0 E and 58852.17 0 N; 1188.82 0 E for sites 1 and 2, respectively). Site 1 has an average depth of 8 m and is surrounded by muddy and rocky shores. The surrounding cliffs were covered with red, green, and brown macroalgae as well as mussels and tunicates. Site 2 has an average depth of 6 m and is surrounded by sandy beaches and boulder fields. Site 2 also has an extensive Zostera meadow and the boulders were commonly overgrown by fucoids, barnacles, and mussels. The grazers in this system are exclusively socalled mesoherbivores, such as amphipods, isopods, and littorinid gastropods (Pavia et al. 1999, Wikstrom et al. 2006). Gastropods were effectively excluded from reaching the panels due to the positioning and construction of the experimental units (see Experimental design), and because of the low abundance of crustacean mesoherbivores in the vicinity of the experimental units, possible effects of grazing are not likely to have affected the results of this study. The waters off the Swedish west coast are generally low in nutrients during the summer months (Nilsson 1991), and nutrients therefore become a limiting resource in this system (Soderstrom 1996). Experimental design Mooring units, made from 2100 3 250 3 4 mm polyvinyl chloride (PVC) strips bent into a ring, were hung from a buoy ;0.5 m below the water surface. In this way, benthic consumers were excluded from the setup. The rings were deployed on 1 March to allow settling and establishment of communities before the 832 J. ROBIN SVENSSON ET AL. experimental manipulation started on 12 May. The experimental manipulation had a duration of 24 weeks and was terminated on 27 October 2004. On each ring 10 PVC panels (150 3 150 3 3 mm), roughened with emery paper, were attached with cable ties. The panels were randomly allocated to combinations of seven disturbance levels and three nutrient levels. Disturbance treatments consisted of a manual removal of biomass from two randomly selected nonoverlapping areas, each covering 10% of the panel area, at each disturbance event. The scraping not only kills or damages individuals, but also facilitates recruitment by the freed substratum, and the disturbance is therefore coherent with the definition by Sousa (1984). This disturbance was applied at six different frequencies: every second, fourth, sixth, eighth, 10th, and 12th week (treatments D1–D6), or left undisturbed (treatment D0). Treatments D0–D6 were present in all rings, with two replicates of D0 on each ring, and the remaining two panels were randomly assigned disturbance treatments to allow additional replication within rings. One of three different levels of nutrient enrichment was applied to each ring by attaching 10 fertilizer bags (1-mm mesh) among the panels. For the highest level of enrichment (Nþþ), bags were filled with 100 g of fertilizer; for the moderately enriched level (Nþ), bags were filled with gravel and 50 g fertilizer, and bags with ambient nutrient concentration (N0) were filled only with gravel. The slow-release Plantacote Depot 6-M, (5.7% NO3, 8.3% NH4, 9% P2O5, and 15% K2O; Aglukon, Düsseldorf, Germany) was used as fertilizer due to its steady release rate in relation to mass, where a doubling in mass leads to twice the amount of nutrients being released (Worm et al. 2000). Each level of nutrient availability was replicated on four randomly assigned rings. All bags were placed inside the rings at the start of the experiment and changed every fourth week in order to have constant nutrient release throughout the experiment. Sampling Sampling of abundance of each species and composition of the experimental communities was done before the start of the manipulation and thereafter every eighth week until the termination of the experiment. Data on undisturbed communities obtained from the sampling after eight weeks were used for testing effects of nutrient availability on algal cover. The time of sampling was selected to be early in the growth season to minimize confounding influences of competition. Data from the last sampling after 24 weeks were used for the main analyses, i.e., the tests of the IDH and the DEM, and data on undisturbed communities from all sampling events were used for studying changes in the communities over time. Panels were detached and brought into the laboratory submerged in seawater, kept under running seawater in the laboratory during the entire sampling procedure, and brought back into the field Ecology, Vol. 88, No. 4 within 16 hours of each sampling event. Before sampling, the back side and edges of all panels were scraped clean and their wet mass was measured. The percentage cover of bare space and sessile species was then estimated in 5% intervals using a 15 3 15 cm plastic grid (mesh size 5 cm2). A 1-cm margin to all edges of the panels was not assessed, and the percentage cover of species with a small holdfast and wide thallus was estimated from the two-dimensional projection of the organism on the panel. Sessile epibionts were also accounted for. Thus, total cover was allowed to exceed 100%. Statistical analyses The data on species richness were analyzed with analysis of variance (ANOVA) using Statistica 6.0 (Statsoft Incorporated, Tulsa, Oklahoma, USA). The models were tested, with species richness as a measure of diversity, following the elaboration of the DEM by Kondoh (2001). Hypotheses about effects of main factors and interactions were tested using the following general linear model: Xijklm ¼ l þ Si þ Nj þ SNij þ Dk þ SDik þ NDjk þ SNDijk þ RðSNÞlðijÞ þ DRðSNÞklðijÞ þ eijklm where l is the overall mean, site (Si) is a random factor with two levels, nutrient enrichment (Nj) and disturbance frequency (Dk) are fixed factors with three and seven levels respectively, ring (R[SN]l(ij)) is a nested random factor with four levels, and eijklm is a random deviation. Due to loss of one ring and lack of complete replication of all levels of disturbance on each ring, type III sums of squares was used for estimation (Henderson 1953). The residual was estimated from the variability between undisturbed panels and from the additional replicated treatments within each ring. To optimize statistical power of tests, post hoc elimination and pooling of negligible variance components (i.e., if P . 0.25) were performed (Winer et al. 1991, Underwood 1997). Support for either of the two models, IDH or DEM, is provided by two different terms in the linear model. The IDH is supported if there is a significant effect of disturbance and if the relationship between richness and disturbance is unimodal with an optimum at intermediate levels of disturbance. This is equivalent to the presence of a significant quadratic component in a polynomial regression. In contrast the DEM is supported by a significant interaction between disturbance and nutrient enrichment. The predictions of the DEM then need to be further evaluated using polynomial regression within individual levels of nutrient enrichment. A fundamental premise for any experimental support for the DEM is that the nutrient treatments actually cause an increased primary productivity. In order to detect effects on productivity as a consequence of the nutrient treatment, differences in cover of macroalgae April 2007 DISTURBANCE, PRODUCTIVITY, AND DIVERSITY 833 TABLE 1. Abundance (mean percent cover 6 SE) of sessile invertebrate and algal species present in the experimental communities from both sites after 24 weeks, averaged over nutrient treatment for all levels of disturbance (D0–D6). Taxon D0 D1 D2 D3 D4 D5 D6 0 0 0.17 6 0.14 0 Chlorophyceae Ulva intestinalis Ulva lactuca 0.09 6 0.04 0.10 6 0.06 0.10 6 0.06 0.39 6 0.19 0.06 6 0.04 0 0 0 0.04 6 0.04 0 Phaeophyceae Ectocarpus siliculosus 0.45 6 0.26 0.03 6 0.03 0.59 6 0.29 0.11 6 0.06 0.11 6 0.05 0.18 6 0.16 0.20 6 0.15 Rhodophyceae Bonnemaisonia hamifera Ceramium rubrum Ceramium strictum Dasya baillouviana Osmundea truncata Polysiphonia fucoides Polysiphonia urceolata Spermothamnion repens 0 1.98 6 0.57 2.62 0.07 6 0.04 0.07 0.04 6 0.03 0.03 0 0.03 0.83 6 0.49 0.17 0 0.20 6 0.12 0.07 Porifera Leucosolenia botryoides 0.78 6 0.28 1.28 6 0.50 1.10 6 0.43 1.21 6 0.53 1.40 6 0.49 1.36 6 0.43 0.74 6 0.24 Cnidaria Clytia hemispherica Laomedea flexuosa Metridium senile Sargatiogeton undatus 0 12.8 6 2.30 18.9 0.11 6 0.05 0.14 0.07 6 0.04 0.14 Annelida Pomatoceros triqueter 0.11 6 0.05 0.21 6 0.08 0.38 6 0.09 0.54 6 0.10 0.51 6 0.09 0.61 6 0.08 0.49 6 0.09 Crustacea Balanus crenatus 0 Mollusca Mytilus edulis Podesmus sp. 0 6 6 6 6 6 0 6 0 4.21 6 1.06 3.39 0.03 6 0.03 0.07 0.03 6 0.03 0.04 0 0.38 6 0.18 0.61 0.03 6 0.03 0.21 0.05 0.03 6 0.03 0.25 0.53 0.05 0.03 0.03 0.07 0 6 6 6 0 6 6 6 0 0 0.04 6 6 3.09 19.7 6 3.07 23.9 6 6 0.06 0.31 6 0.18 0.39 6 6 0.06 0.03 6 0.03 0.18 6 0.03 6 0.03 0 0 0 1.07 2.23 6 0.55 0.05 0.03 6 0.03 0.04 0.03 6 0.03 0.06 6 0.04 0.36 1.46 6 1.15 0.18 0 0.18 0.23 6 0.15 0.04 0.64 0.14 0.04 6 6 6 6 0 0.21 6 0 0.38 6 0.03 0 0.17 2.09 6 1.07 0.06 0.03 6 0.03 0.03 0.17 6 0.14 0.03 6 0.03 0.07 0.40 6 0.29 0 0.17 0.09 6 0.05 0.04 0 0 0 4.30 19.9 6 3.04 30.7 6 3.44 24.4 6 2.44 0.36 0.14 6 0.06 0.14 6 0.06 0.37 6 0.20 0.07 0.11 6 0.05 0.14 6 0.06 0.06 6 0.04 0.06 6 0.04 0 0 0.35 6 0.12 0.52 6 0.18 0.59 6 0.24 0.64 6 0.25 0.63 6 0.24 1.00 6 0.37 0.57 6 0.29 0 0.17 6 0.17 0 0 0 0.04 6 0.03 0 Bryozoa Cryptosula pallasiana 0.39 6 0.19 0.28 6 0.18 0.03 6 0.03 0.04 6 0.04 0.23 6 0.15 0.29 6 0.16 0.06 6 0.04 Electra pilosa 0.91 6 0.29 1.34 6 0.46 0.76 6 0.28 0.93 6 0.33 0.46 6 0.20 1.36 6 0.34 0.49 6 0.20 Membranipora membranacea 0.33 6 0.19 0.03 6 0.03 0 0.71 6 0.42 0.14 6 0.14 0.18 6 0.16 0 Hemichordata Ascidiella aspersa Botryllus schlosseri Botrylloides leachi Ciona intestinalis 11.9 6 2.38 12.3 0 0 84.0 6 3.50 75.3 6 2.74 12.5 6 2.27 8.32 6 2.13 8.94 6 1.81 8.82 6 1.60 5.03 6 1.17 0 0 0.04 6 0.04 0 0 0 0 0.17 6 0.17 0 0 0 0 6 5.15 64.3 6 5.17 71.4 6 4.82 68.0 6 4.69 53.6 6 4.04 17.3 6 2.25 among levels of enrichment were tested using undisturbed panels (D0) after eight weeks. Data were analyzed using ANOVA: Xijk ¼ l þ Si þ Nj þ SNij þ RðSNÞkðijÞ þ eijk RESULTS General observations During the experiment a total of 15 species of algae and 17 species of sessile invertebrates were observed. The most abundant organisms, occupying large areas of the panels, were the tunicates Ciona intestinalis and Ascidiella aspersa and the hydroid Laomedea flexuosa. At the end of the experiment, ephemeral algae, bryozoans, and sea anemones were frequent in the communities, although usually low in cover (Table 1). Studies of the development of undisturbed communities showed that richness was highest after 8 weeks at site 1 and after 16 weeks at site 2 (Fig. 1A). The decrease in richness at later stages suggests that some species were excluded as a result of competition. This is consistent with the observation of an earlier peak in richness at site 1, following the establishment of a dense cover of C. intestinalis at this site (Fig. 1B). The ascidians occupied .95% of the space on control panels after 24 weeks at site 1, suggesting that C. intestinalis is a competitive dominant in this system, capable of excluding both other invertebrates as well as most species of macroalgae (Fig. 1B). Assessment of productivity The analysis of algal cover in undisturbed communities after 8 weeks showed that there was a statistically significant response to increased nutrient availability (F2,44 ¼ 10.74, P , 0.001). Inspection of means (mean [6SE] cover of algae for N0, Nþ, and Nþþ were 54.5 6 834 J. ROBIN SVENSSON ET AL. Ecology, Vol. 88, No. 4 Testing predictions from the IDH and DEM FIG. 1. Temporal patterns of (A) species richness and (B) percent cover of C. intestinalis in fouling communities at sites 1 and 2. Data are presented as mean 6 SE. 5.13%, 82.5 6 4.41%, and 71.1 6 3.55%, respectively) and the SNK test revealed that there were significant differences between unfertilized panels (N0) and those fertilized (Nþ and Nþþ). Furthermore, there was no significant interaction term between the two factors, site (S) and nutrient enrichment (N) (F2,42 ¼ 1.45, P ¼ 0.25), suggesting that nutrient availability had a general effect on productivity and that useful tests of the DEM were in fact possible. However, no significant difference in algal cover was observed between Nþ and Nþþ, which could be due to a saturation of nutrients already at the Nþ level. Analysis of species richness at the end of the experiment showed that there was a significant effect of disturbance, but no interactive effect of disturbance and nutrients (Table 2a). In all levels of nutrients, there was a tendency for maximum richness at intermediate levels of disturbance (Fig. 2). Initially it might appear that maximum diversity occurred at different levels of disturbance, but the variability among and within levels of disturbance was large and the predicted shift toward more frequent disturbances was not observed (maximum richness was observed at D5, D5, and D2 for N0, Nþ, and Nþþ, respectively). Considering the fact that the hypothesis about simple effects of disturbance and that of interactive effects involving disturbance and nutrients were both tested using the same pooled mean square as the error term (with 189 df ), conclusions about lack of interactive effects appear robust and not caused by a lack of statistical power. This view is supported by calculation of effect-sizes from estimated mean squares, which reveal that the effect of disturbance was ;20 times larger than that of the interaction (kD2 ¼ 1.82 and k2N3D ¼ 0.10). There was no significant interaction involving disturbance and any of the spatial scales, i.e., sites and rings (Table 2a). This indicates that the effect of disturbance was consistent among places. Nevertheless, significant variability among rings indicates that there was small-scale variability in richness within sites. Further analysis showed that, not only were there differences among levels of disturbance, but there was also a significant quadratic component in the polynomial regression (Table 2b), i.e., maximum richness at intermediate disturbances (Fig. 3A). Consistent with the IDH, these results suggest that sessile species are removed at low and high frequencies of disturbance. Inspection of the mean cover of the most abundant taxa suggests that they differ in their responses to disturbance TABLE 2. (a) ANOVA on species richness at the end of the experiment and (b) regression analysis. Source df MS F P Error term a) ANOVA on species richness Site, S Nutrients, N Disturbance, D S3N S3D N3D Ring, R(S 3 N) S3N3D D 3 R(S 3 N) Residual Pooled 1 2 6 2 6 12 17 12 102 69 189 7.47 2.66 7.98 3.88 3.01 2.58 7.90 0.90 2.75 2.44 2.53 0.94 0.69 3.16 0.49 1.10 1.03 3.24 0.33 1.13 0.34 0.59 0.01 0.62 0.37 0.43 0.00 0.98 0.30 R(S 3 N) S3N pooled R(S 3 N) D 3 R(S 3 N) pooled residual D 3 R(S 3 N) residual 2 4 0.44 0.04 10.04 0.03 b) Regression analysis Regression Residual R2 0.83 Notes: (a) Hypotheses about effects of disturbance (consistent with predictions from IDH) and interactions between disturbance and nutrients (consistent with predictions from DEM) were tested using a pooled error term following nonsignificant tests (P . 0.25) of D 3 R(S 3 N), S 3 N 3 D, and S 3 D. (b) Regression analysis for effects of disturbance on species richness. Coefficients for the regression analysis are as follows. For the intercept, b ¼ 5.25, t ¼ 29.12, P ¼ 0.00; for D (disturbance), b ¼ 3.73, t ¼ 3.96, P ¼ 0.02; for D2, b ¼ 3.77, t ¼ 4.39, P ¼ 0.01. April 2007 DISTURBANCE, PRODUCTIVITY, AND DIVERSITY FIG. 2. Effects of disturbance on species richness at different nutrient levels (see Materials and Methods: Experimental design). Data are presented as mean 6 SE. (Fig. 3B). Thus there is a strong negative effect on the cover of the dominant tunicates Ciona intestinalis and Ascidiella aspersa, while a rapid colonizer such as the hydroid Laomedea flexuosa is positively affected by disturbance. DISCUSSION In this study we found empirical evidence supporting the IDH, but not the DEM. Species richness was highest at an intermediate frequency of disturbance, and this pattern was not significantly affected by different levels of nutrient enrichment. This was in spite of the fact that the nutrient treatment had a significant effect increasing percentage cover of macroalgae, which is closely linked to productivity (Death 2002). In contrast to the IDH, the empirical support for the DEM is scarce. So far support has come from observational studies of flooding in riparian wetlands (Pollock et al. 1998), a mesocosm study of sediment movement and organic enrichment in deep-sea benthos (Widdicombe and Austen 2001), laboratory experiments of energy availability and mortality in microcosms (Rashit and Bazin 1987), and in the only two experiments that have manipulated disturbance and productivity simultaneously in the field (Worm et al. 2002, Jara et al. 2006). The conclusions from our experiment differ from the few previous studies testing the DEM. Because productivity was manipulated using the same procedures as in Worm et al. (2002) and Jara et al. (2006), the nutrient treatment cannot explain the different results. Instead, it is more likely that the divergent outcomes were caused by differences in (1) the composition of the experimental communities, and/or (2) the way the communities were disturbed. The communities in this study were not only rich in species, but also in terms of higher taxa and functional groups. During the experiment .30 different species were observed in the communities, 15 species of macroalgae and 17 species from such different taxonomic groups as tunicates, mussels, hydroids, bryozoans, barnacles, annelids, and sea anemones. Other experi- 835 ments on the DEM have used more restricted taxon sampling and studied communities composed mainly of algae (Worm et al. 2002), polychaetes (Widdicombe and Austen 2001), protist bacterivores (Scholes et al. 2005), and bacteria, flagellates, and ciliates (Rashit and Bazin 1987). Experiments conducted in more diverse systems can be advantageous due to the possibility of recognizing patterns among more distantly related taxa. In this experiment tunicates occupied most of the space on control panels, and were thus capable of excluding a variety of both invertebrate and macroalgal species. Had the hypotheses been tested in assemblages of solely macroalgae or invertebrates, this dominance of one taxon over several taxa from distant groups might not have been revealed, and patterns among, for instance, only macroalgae (cf. Worm et al. 2002) might have been different and not representative for the natural diversity of hard-substratum assemblages of temperate marine waters. Because the DEM and the IDH are general ecological models intended to explain gradients of diversity in nature, their generality and explanatory power should be assessed using natural communities. The diversity and composition of communities can influence the outcome of an experiment, because different species and functional groups respond differently to experimental treatments. It is therefore impor- FIG. 3. (A) Species richness on the experimental panels, and (B) percent cover of Ascidiella aspersa, Laomedea flexuosa, and Ciona intestinalis, as functions of relative disturbance frequency (see Materials and Methods: Experimental design). Data are presented as mean 6 SE. 836 J. ROBIN SVENSSON ET AL. tant also to consider the composition of communities, and not only the design of experimental treatments, when comparing results and conclusions from experiments on effects of disturbance and productivity on diversity. Another potential explanation of the difference in results and conclusions between this study and previous studies on the DEM is based on the application and the definition of disturbance. In this study we used controlled levels of mechanical scraping. This type of disturbance shares important properties with natural disturbances, such as ice-scouring (Åberg 1992), drifting logs (Dayton 1971), and wave action (Dudgeon et al. 1999), in the sense that it makes free space available for settling (i.e., the limiting resource). This is a central component in definitions of disturbance (Sousa 1984, 2001), which is not always considered in experimental manipulations (e.g., Rashit and Bazin 1987, Scholes et al. 2005). Another potentially complicating issue is the selectivity of agents of disturbance in manipulative experiments. Worm et al. (2002) used mesoherbivores as agents of disturbance in communities composed largely of macroalgae. In this case it is possible that interactions, not predicted by the DEM, occurred between grazing and nutrient enrichment of algae. Grazers have been shown to prefer plants (Onuf et al. 1977) and macroalgae (Cruz-Rivera and Hay 2000) with higher nutrient content, whereas physical disturbance has no such selectivity. Grazing has previously been argued as an unsuitable agent of disturbance in studies on the IDH (e.g., McGuinness 1987, Sousa 2001). Due to selective preference for nutrient-rich individuals, grazing might be an even less appropriate agent of disturbance in studies on the DEM. Despite its conceptual appeal, the scarcity of manipulative studies suggests that empirical testing of the DEM may not be straightforward. One important issue that has to be considered in experimental tests of the DEM is that the extensive discussion about agents and definitions of disturbance (Grime 1977, Pickett and White 1985, Sousa 2001) has no equivalence for productivity. Experimental manipulation of productivity is often done indirectly, i.e., by adding nutrients. This has two fundamental implications for the interpretation of manipulative experiments. First, it becomes necessary to test not only for effects of the experimental treatment on diversity, but also to test independently whether the actual experimental treatment (the adding of nutrients) has an effect on productivity. Without evidence for an actual increase in productivity, it is not clear whether the experiment is testing the DEM or not. Unfortunately, this is not always made clear (e.g., Widdicombe and Austen 2001, Scholes et al. 2005, Jara et al. 2006). Another problematic issue is the fact that productivity of an assemblage is determined both by external factors (i.e., light, temperature, energy transport, and nutrients) and internal processes (i.e., differences in usage of resources, resource capture ability, and energy conver- Ecology, Vol. 88, No. 4 sion ability within and among species [Tilman 1980, Tilman and Pacala 1993]). In a field experiment on natural assemblages, energy conversion ability is usually not amenable to manipulation. One consequence is that there may be a lack of independence between the response variable and the levels of the experimental factor. This is because the productivity of an assemblage may influence diversity (e.g., Connell and Orias 1964, Abrams 1995) at the same time as the diversity influences the productivity (e.g., Tilman et al. 1996). Therefore, in an experiment where productivity is manipulated indirectly, the response variable (i.e., some measure of diversity) may modify the effect of the experimental treatment. This relationship may lead to confusion about cause and effect in otherwise carefully planned experiments. Nevertheless, if predictions about effects of productivity on diversity are to be tested in field experiments, indirect manipulations may be the only conceivable solution. In this system, addition of nutrients, which are often a limiting resource, is probably the most effective way to increase productivity in a field experiment (e.g., Widdicombe and Austen 2001, Worm et al. 2002, Jara et al. 2006). In a manner similar to manipulations of disturbance, the experimental manipulations of productivity in natural communities are often selective. The matter of selectivity is probably of greater concern in experimental manipulations of productivity, because designing a nonselective agent of productivity is more complicated then designing a nonselective agent of disturbance. If all organisms are affected equally by the productivity treatment, or if the dominant organisms are affected relatively more strongly, it would require a stronger disturbance to prevent competitive exclusion, as predicted by the DEM. However, if the inferior competitors are more strongly affected by the productivity treatment, this could instead slow down the process of competitive exclusion, which would cause diversity to peak at lower intensities of disturbance, rather than at the predicted higher intensities. In this experiment, the dominant tunicates, unlike the ephemeral macroalgae, did not noticeably increase their growth rates in response to the nutrient treatment. This result could explain why an interaction between disturbance and productivity was not found. Jara et al. (2006) also discussed the nutrient treatment as a possible cause for their weak support for the DEM, because the nutrients may only have affected the autotrophic part of the community. Studies that have found the predicted interaction between disturbance and productivity have predominantly been made in plant communities (Pollock et al. 1998, Death 2002) or algae (Worm et al. 2002). In such experiments, the species in the communities would be more equally affected, even though individual species of plants and algae differ in their ability to utilize available resources. In this study, we found maximum richness at intermediate frequencies of disturbance, which is in April 2007 DISTURBANCE, PRODUCTIVITY, AND DIVERSITY accordance with the IDH. A literature review showed that this is not a universal pattern in experimental tests of effects of disturbance on diversity (Mackey and Currie 2001). Less than 20% of the published studies on disturbance–diversity relations supported the IDH. As an extended theory, the DEM may explain some of the results that are inconsistent with the IDH; and it has therefore been suggested that it is preferable to the IDH (Stallins 2003). In their review, Mackey and Currie (2001) found that .50% of all experiments on disturbance showed either monotonically positive or negative patterns with increasing disturbance. These patterns could in principle be explained by the DEM, if it could be shown that productivity was high in cases where diversity increased with disturbance, and low when diversity decreased with disturbance. The explanatory power of the DEM is therefore potentially large. Nevertheless, many alternative explanations may be proposed for results that are inconsistent with the IDH. Several authors have suggested that the predictions of the IDH rely on a number of prerequisites, such as competitive exclusion (Connell 1978), large regional species pool (Osman 1977), multiple stages in succession (Collins and Glenn 1997), and trade-off between competition and tolerance (Dial and Roughgarden 1998) and between competition and colonization (Petraitis et al. 1989). Menge and Sutherland (1987) argued that the effects of disturbance depend on the amount of environmental stress in the system. Accordingly, experiments in systems where these prerequisites are not fulfilled seldom find support for the IDH. For instance Cowie et al. (2000) and Huxham et al. (2000) did not observe maximum diversity at intermediate levels of disturbance, because settling propagules and a small regional species pool were lacking. Studies testing the DEM have also explained lack of support for the model with the failure of fulfilment of these requirements. Scholes et al. (2005) suggested that the absence of recolonization of bacteria and ciliates could explain lack of support in the closed microcosms, while Death (2002) found that the DEM could not predict patterns of diversity in forest streams because such systems are not driven by competition. These results imply that models incorporating productivity is only one of several possibilities for improving our understanding of mechanisms behind patterns of diversity. 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An introduction to model selection. Journal of Mathematical Psychology 44:41–61. Paper I Paper II PAPER Paper III II Paper IV Paper V “You tried your best and you failed miserably. The lesson is 'never try'.“ -Homer J. Simpson Paper VI Ecology, 90(2), 2009, pp. 496–505 Ó 2009 by the Ecological Society of America Equal rates of disturbance cause different patterns of diversity J. ROBIN SVENSSON,1 MATS LINDEGARTH, AND HENRIK PAVIA Department of Marine Ecology–Tjärnö, University of Gothenburg, 452 96 Strömstad, Sweden Abstract. Empirical evidence suggests that disturbance has profound effects on the species diversity of aquatic and terrestrial assemblages. Conceptual ecological theories, such as the intermediate disturbance hypothesis (IDH), predict maximum diversity at intermediate levels of disturbance. Tests of the predictive power and generality of these models are, however, hampered by the fact that the meaning and units of ‘‘disturbance’’ are not clearly defined. For example, it is seldom recognized that the rate of disturbance is the product of both frequency and extent (e.g., area or volume) of disturbance events. This has important consequences for the design and interpretation of experiments on disturbance. Here we present, for the first time, an experimental design that allows for unconfounded testing of combinations of area and frequency (i.e., regimes) for a given rate of disturbance. We tested the prediction that species richness responds differently to equal rates of disturbance, depending on the specific combination of frequency and area, on marine hard-substratum assemblages. Five different rates of disturbance and two regimes (small frequent or large infrequent disturbances) were applied at three sites. The results showed that the effect of a certain rate of disturbance (1) varies strongly among assemblages and (2) also depends on the specific combination of frequency and area of disturbance events. Maximum species richness was observed at intermediate rates of disturbance at site 1 (i.e., support for the IDH), whereas there was a monotonic decline at site 2 and there was no evident pattern at site 3. The variable responses among sites were explained by differences in degree of competitive exclusion and rates of recruitment. At the site where the IDH was supported, the regime with a large proportion of the area disturbed infrequently showed higher richness, compared to the regime with a small proportion disturbed frequently. This was likely due to a stronger decrease of dominants, which allowed for the recruitment of new colonizing species. In summary, we conclude that tests and general syntheses of models of disturbance–diversity patterns would benefit from more explicit definitions of the components of disturbance, as well as a stronger focus on the importance of variation in inherent properties of natural assemblages. Key words: competitive exclusion; diversity; marine assemblages; rate of disturbance; regime; species richness. INTRODUCTION Disturbance is an important factor explaining patterns of biodiversity in many terrestrial (e.g., Eggeling 1947, Grime 1977, Molino and Sabatier 2001) and aquatic environments (e.g., Sousa 1979, Patricio et al. 2006). One of the most influential formulations of the effects of disturbance on biological diversity is the intermediate disturbance hypothesis (IDH; Connell 1978). The IDH predicts low diversity at low levels of disturbance due to competitive exclusion and also at high levels as a result of local extinction. At intermediate levels of disturbance, diversity is higher due to coexistence of rapid colonizers and competitive dominants. The IDH has been supported in laboratory experiments (e.g., Widdicombe and Austen 1999, Buckling et al. 2000, Cowie et al. 2000) as well as field experiments in terrestrial (e.g., Armesto and Pickett 1985, Collins 1987, Manuscript received 4 October 2007; revised 4 June 2008; accepted 12 June 2008. Corresponding Editor: H. Hillebrand. 1 E-mail: [email protected] 496 Molino and Sabatier 2001), freshwater (e.g., Padisak 1993, Reynolds 1995, Flöder and Sommer 1999) and marine communities (e.g., Osman 1977, Sousa 1979, Valdivia et al. 2005). Nevertheless, a literature review revealed that only 20% of the studies on effects of disturbance on diversity showed the unimodal pattern predicted by the IDH (Mackey and Currie 2001). Thus, despite its conceptual appeal, it appears that the predictive value of the IDH is often limited. This has led to the development of more complex models, e.g., by incorporating effects of productivity (the dynamic equilibrium model [DEM]; Huston 1979, 1994), which could potentially account for a wider range of patterns. One important focus for research in general is to understand the limitations of a theory and to unravel causes of variable predictive power. A fundamental difficulty with the IDH and the DEM is that they are largely conceptual and verbal models based on relatively scaled variables (Schoener 1972, Peters 1991). Therefore the units and meaning of disturbance is sometimes unclear and often different among studies (Pickett and White 1985, Sousa 2001; Table 1). Conceptual terms, such February 2009 DISTURBANCE RATE AND COMMUNITY DYNAMICS 497 TABLE 1. Conceptual and operational terms used to define the magnitude of disturbance in ecological literature. Term Conceptual Level Severity Intensity Regime Operational Frequency Time Extent Size Rate Meaning Quantity general description of overall magnitude of disturbance general description often used as ‘‘strength’’ of the disturbing force general description sometimes used synonymously to severity generic term for the types and components of disturbance currently acting in a given area number of disturbance events per unit time period of time since last disturbance event total two- or three-dimensional space disturbed size of an individual disturbance event product of area and frequency as ‘‘intensity’’ and ‘‘severity,’’ are not explicitly defined, and are therefore not easily generalized among studies. For example, ‘‘intensity’’ has been used to describe a variety of experimental manipulations and variables, such as penetration depth per bite by limpets (Steneck et al. 1991), type of mechanical scrubbing (McCabe and Gotelli 2000), and degree of oscillation in sediment (Garstecki and Wickham 2003). Clearly, there is a need for systemspecific concepts, but in order to evaluate general ecological theories, such as the IDH, it is important that concepts are commensurable among studies. Disturbance can be operationally defined as a rate, i.e., the sum of the size of all disturbance events in a given area per unit time (Miller 1982). The rate is the only measure, which accounts for the combined effects of area and frequency, and thus the total amount of disturbance actually inflicted upon the community under study. This is important because information about one of these components makes no sense without the context of the other. For instance, the information that a defined biological community was disturbed once a week is completely uninformative if we do not know the extent of the disturbance. Surely, we would predict massive differences in effects on diversity if the area disturbed each week was 0.5% of the total area compared to if it was 20%. This is a fundamental fact that is always considered in the process of defining appropriate treatment levels in ecological experiments, but it is later also commonly disregarded in the interpretation and discussion of the study. Consequently, the combined effects of frequency and area are always implicit in experimental studies on the effects of disturbance, but in order to put any experimental result into a wider context, and to allow for direct and meaningful comparisons among studies, it is always necessary to transform the measure of disturbance into a rate. From this it does, however, not follow that the rate of disturbance is always the most accurate predictor of diversity. Several theoretical arguments can be made, which suggest that the effect of a given rate of disturbance may differ depending on the way the specific time1 time area or volume area area/time rate is obtained, i.e., the regime. For instance, Miller (1982) suggested that small, frequent disturbances favor species with rapid vegetative growth (‘‘competitive’’ species), whereas large, less frequent disturbances favor species with high capacity for dispersal (‘‘colonizers’’) due to the differences in perimeter to area ratios among patches. Although the area of disturbance have been the predominant focus for models of rates of disturbance (i.e., Miller 1982), the other component of the rate, frequency, is equally important. Differences in frequency and timing of disturbance will, similarly to variations in area, influence the abundance and composition of natural communities (Sousa 2001), because species are likely to increase in abundance when the disturbance regime matches their preferred recruitment time (Underwood and Anderson 1994, Crawley 2004). The large variation in temporal distribution of propagules among species (Roughgarden et al. 1988, Underwood and Anderson 1994) will also have the consequence that a single large disturbance cannot be colonized by all species in the regional species pool, but only by the propagules that are available at the specific time when space is made free. Thus, it is evident that variations in both area and frequency of a disturbance rate are likely to influence the outcome of studies on effects of disturbance on diversity. However, despite that area and frequency have well known distinct effects on diversity, no study, to our knowledge, has performed unconfounded testing of these factors for a given rate of disturbance. Testing of differences among regimes at equal rates of disturbance is not straightforward because experimental manipulations of the frequency or the extent of disturbance are inevitably associated with a change in the rate of disturbance. Previous experiments, simultaneously testing hypotheses about effects of frequency and extent, have done this using orthogonal designs (e.g., Collins 1987, McCabe and Gotelli 2000). The interpretation of such experiments is problematic because tests of the effects of one factor, within one level of the other factor, are confounded by changes in 498 J. ROBIN SVENSSON ET AL. TABLE 2. Explanation of each combination of experimental factors, regime (Re1, small, frequent disturbances; Re2, large, infrequent disturbances), and frequency and rate of disturbance. Regime Area (cm2) Frequency (no./week) Rate (cm2/week) Re1 Re1 Re1 Re1 Re1 45 45 45 45 45 0 2/16 4/16 8/16 16/16 0 5.63 11.25 22.5 45 Re2 Re2 Re2 Re2 Re2 90 90 90 90 90 0 1/16 2/16 4/16 8/16 0 5.63 11.25 22.5 45 the rate. In order to test for differences among regimes, specific analytical contrasts need to be extracted and parts of the experiment become redundant. Furthermore, in a direct analogy to generalizations among studies, any significant interaction resulting from such an experiment can only be sensibly interpreted if the rate of disturbance is considered. Here we present, for the first time, a field experiment with an experimental design that allows for unconfounded testing of combinations of area and frequency (i.e., regimes) for a given rate of disturbance. In a previous manipulative experiment in marine hardsubstratum communities on the west coast of Sweden, we found that maximum species richness was attained at intermediate frequencies of disturbance (Svensson et al. 2007). Following from this work, our aim was to use hard-substratum assemblages to test the hypothesis that, in these assemblages, the effect of a certain rate of disturbance depends on the specific combination of area and frequency. In order to do this mechanical disturbance was applied at five distinct rates of disturbance under two different regimes (disturbing either a small proportion of the assemblage, frequently, or a large proportion, infrequently) at three sites. MATERIALS AND METHODS Study site The field experiment was conducted on the west coast of Sweden in the vicinity of Tjärnö Marine Biological Laboratory. The experimental sites were three bays located approximately 1 km apart (58852 0 92 00 N, 1188 0 3100 E; 58852 0 2000 N, 1188 0 7000 E; and 58852 0 7600 N, 1188 0 1500 E for sites 1, 2, and 3, respectively). Site 1 had an average depth of 8 m and was surrounded by muddy and rocky shores inhabited by red, green and brown macroalgae as well as mussels and tunicates. Site 2 had an average depth of 6 m and was surrounded by sandy beaches and boulder fields. This site also had an extensive seagrass (Zostera marina) meadow and the boulders were commonly overgrown by fucoids, barnacles, and mussels. Site 3 had an average depth of 10 m Ecology, Vol. 90, No. 2 and was surrounded exclusively by rocky shores with a steep declining sandy bottom. The nearby rocks were predominantly occupied by breadcrumb sponge (Halichondria panicea), ephemeral red algae, and fucoids. Experimental design Experimental units, made from 2100 3 250 3 4 mm PVC strips folded into a ring, were placed hanging from a buoy approximately 0.5 m below the water surface (Svensson et al. 2007). Ten quadratic PVC panels (150 3 150 3 3 mm), roughened with emery paper, were attached with cable ties on each of the 24 rings. Eight rings were deployed at each site on 25 April to allow settling and establishment of communities before the experimental manipulation started on 25 May. The experimental manipulation had a duration of 17 weeks and was terminated 28 September 2005. The panels were disturbed by either of five different rates of disturbance (Ra0Ra4), under two different disturbance regimes (Re1 and Re2; Table 2). Under the first regime two randomly selected areas were scraped, each covering 10% of the panel area, with frequencies ranging from every week to every eighth week. Under the second regime, four randomly selected areas, each covering 10% of the panel area, were scraped at frequencies ranging from every second week to 16th week (Table 2). In addition to killing or damaging individuals, the disturbance treatment also facilitated recruitment by freeing substratum and is therefore coherent with the definition of disturbance by Sousa (1984). All rates were present in all rings with two replicate panels and either of the two regimes was randomly assigned to rings. Thus, four rings of regime 1 and four rings of regime 2 was present at each of the three sites, allowing eight rings with all five rates replicated per site. Sampling The composition and abundance of assemblages were sampled at the end of the experiment after 17 weeks of manipulation. Panels were detached and brought into the laboratory submerged in seawater and then kept under running seawater in the laboratory during the entire sampling procedure. Wet weight was measured and the edges and reverse side of all panels were scraped clean before sampling. Percent cover of bare space and sessile species was then estimated in 5% intervals using a 15 3 15 cm plastic grid. A 1-cm margin to all edges of the panels was not assessed in order to avoid confounding edge effects. The percentage cover of species with a small holdfast and wide thallus was estimated from the two dimensional projection of the organism on the panel. Cover of epibionts was also estimated, thus, total cover could exceed 100%. Statistical analyses The data obtained from the experiment was analysed with analysis of variance (ANOVA) using Statistica 6.0 (Statsoft, Tulsa, Oklahoma, USA). Hypotheses about February 2009 DISTURBANCE RATE AND COMMUNITY DYNAMICS 499 FIG. 1. Abundance of species in undisturbed communities (rate 0) averaged over regime at sites 1, 2, and 3. Different letters indicate significant difference in community composition (ANOSIM; R . 0.6, P ¼ 0.001). effects of main factors and interactions were tested using the following general linear model: Xijklm ¼ l þ Si þ Rej þ SReij þ Rak þ SRaik þ ReRajk þ SReRaijk þ RiðSReÞlðijÞ þ RaRiðSReÞklðijÞ þ eijklm where l is the overall mean, site (Si) is a random factor with three levels, disturbance regime (Rej) is a fixed factor with two levels, disturbance rate (Rak) is a fixed factor with five levels, ring (Ri[SRe]l(ij)) is a nested random factor with four levels and eijklm is a random deviation. Support for the hypothesis that equivalent rates of disturbance may cause different effects depending on the specific combination of frequency and area of disturbance, would be shown by a significant interaction (Ra 3 Re). More specifically the hypothesis is supported if a difference in species richness is found at equivalent rates of disturbance for regimes with the larger area (regime 2), compared to regimes with the smaller area (regime 1). Support for the alternative, i.e., that the effect of rate of disturbance does not depend on the particular combination of frequency and area, is obtained from a significant effect of rate of disturbance (Ra) if there is a nonsignificant interaction (Ra 3 Re). Furthermore, to evaluate whether the response of disturbance is consistent with the predictions from the IDH, two additional tests are necessary. First, if there is a significant negative quadratic component in a polynomial regression this indicates that the response is non-linear and that the rate of increase declines at larger rates of disturbance. Second, in order to test whether the maximum species richness occurs at a rate of disturbance that is different from the two extreme rates of disturbance in our study, we performed a Mitchell-Olds and Shaw’s test (MOS test [Mitchell-Olds and Shaw 1987]). This method has previously been used to investigate patterns of curvilinear relationships between diversity and productivity, where significant results of the MOS test shows support for hump-shaped or U-shaped patterns (Mittelbach et al. 2001, Chase and Leibold 2002, Fukami and Morin 2003). Initial tests of differences among sites in undisturbed assemblages (Ra0) were made using analysis of similarity (ANOSIM) using the PRIMER software package (PRIMER-E, Plymouth, UK). The abundance data was transformed to the fourth root, in order to avoid bias by the greater influence of abundant species, following the recommendations by Clarke and Warwick (1994). These analyses revealed whether differences were solely related to the number of species or also dependent on the particular species present and their relative abundance. The individual contributions of different species to the observed differences among sites were evaluated using SIMPER. A graphical comparison among sites was obtained using non-metric multidimensional scaling (nMDS). RESULTS Structure of assemblages A total of 19 species of algae and 16 species of sessile invertebrates were observed in the experimental communities at the time of sampling. The most abundant organisms, occupying large areas of the panels, were the tunicate Ciona intestinalis, the common blue mussel Mytilus edulis, the red algae Ceramium rubrum, and the hydroid Laomedea flexuosa, whereas sea anemones, bryozoans, barnacles, and most ephemeral algae were found at low cover (Fig. 1). The composition of species in undisturbed assemblages differed among all three sites (ANOSIM; global R . 0.6, P , 0.005 for all pairwise tests; Fig. 2). Difference in cover of C. intestinalis explained most of the dissimilarity among all sites (SIMPER; 77%, 54%, and 35%, sites 1 vs. 2, 1 vs. 3, and 2 vs. 3, respectively). The total area covered of sessile species in the undisturbed assemblages exceeded 100% at site 1, whereas assemblages at sites 2 and 3 had less than full coverage of available space, indicating that the 500 J. ROBIN SVENSSON ET AL. FIG. 2. Multidimensional scaling (MDS) of species composition for all sites averaged over disturbance regime. strength of competition for space differed substantially among sites (Fig. 1). The ascidian C. intestinalis covered over 95% of the space in the undisturbed assemblages at site 1, and was also the most abundant species at site 2 occupying 33% of the panel. At site 3 no single species occupied more than 15% of the available space in the assemblage. Responses to rates of disturbance There was no overall effect of the rate of disturbance on species richness and thus there was no general support for the IDH (Table 3). Instead, the effects of the rate of disturbance differed significantly among sites (P , 0.05 for S 3 Ra; Table 3, Figs. 3 and 4). A graphical examination of the nature of this interaction suggested that there was maximum richness at intermediate rates of disturbance at site 1, a decrease in richness with increasing rate of disturbance at site 2, while no clear pattern was distinguishable at site 3 (Fig. 4). Additional analyses using polynomial regression showed that there were significant linear and quadratic components at site 1, a significant decreasing linear trend at site 2, and no significant pattern at site 3 (Table 4). Because significant quadratic components do not automatically show evidence for internal maxima in polynomial regressions, a Mitchell-Olds and Shaw’s test was performed for assemblages at site 1. This test showed that maximum richness occurs at an intermediate rate of disturbance Ecology, Vol. 90, No. 2 (b1/2b2 ¼ 32.8, P , 0.01 for Mitchell-Olds and Shaw’s test), and comparisons of adjusted R2 showed that the hump-shaped model had a better fit to our data compared to the linear model (adjusted R2 ¼ 0.213 and 0.156, respectively). Thus, although the IDH was not globally supported, the patterns observed at site 1 were not only statistically significant but precisely those predicted by the IDH (Table 4). Analyses of individual species also showed that these differed in their response to rate of disturbance (Fig. 5). Inspection of mean cover showed that the highly abundant tunicate C. intestinalis was negatively affected by the disturbance treatment, whereas rapid colonizers, such as the ephemeral algae Enteromorpha intestinalis and Ectocarpus siliquosis, increased in cover with increasing disturbance rate. Although disturbance rate had a negative effect on richness on many panels it is still noteworthy that assemblages subjected to the highest rate, which constituted of scraping 320% of the panel area over a period of 16 weeks, still had between 5 and 11 species at the termination of the experiment. Responses to regimes of disturbance Analysis of species richness at the end of the experiment also showed that there was a significant interaction among factors site, regime and disturbance rate (Table 3). Although calculations of variance components showed that this component was only half as large as that of the two-way interaction (for S 3 Re 3 Ra, r2 ¼ 0.46, and for S 3 Ra, r2 ¼ 0.98), this interaction suggests that the effects of the rate of disturbance differ between regimes, at least at some sites. In order to test for differences among regimes in assemblages where maximum richness was observed at intermediate rates (Fig. 3), post hoc tests for differences between regimes within rates were done at site 1. SNK test showed that regime 2 (large and infrequent disturbances), had significantly greater species richness than regime 1 (small and frequent disturbances) at rate 2. In order to further investigate the underlying cause for this difference in richness we compared the abundance of species among regimes (Table 5). Assemblages in regime 2 had more species of ephemeral algae (i.e., ‘‘colonizers’’) and most algal species had higher coverage, whereas the ascidian C. intestinalis and the blue TABLE 3. Analysis of variance on species richness. Source df MS F P Error term Site, S Regime, Re Rate, Ra S 3 Re S 3 Ra Re 3 Ra S 3 Re 3 Ra Ring, Ri(S 3 Re) Ra 3 Ri(S 3 Re) Residual 2 1 4 2 8 4 8 17 68 115 89.26 2.03 5.31 7.77 18.26 4.60 6.26 10.71 2.58 2.17 8.34 0.26 0.29 0.73 7.09 0.74 2.43 4.95 1.19 0.003 0.660 0.876 0.499 0.000 0.593 0.023 0.000 0.205 Ri(S 3 Re) S 3 Re S 3 Ra Ri(S 3 R) Ra 3 Ri(S 3 Re) S 3 Re 3 Ra Ra 3 Ri(S 3 Re) residual residual February 2009 DISTURBANCE RATE AND COMMUNITY DYNAMICS 501 FIG. 3. Effects of rate of disturbance on species richness at different sites and disturbance regimes. Data are presented as mean þ SE. Disturbance rates and regimes are described in Table 2. mussel M. edulis (i.e., ‘‘competitors’’) had higher cover in regime 1. Furthermore, inspection of means showed that maximum richness was attained at lower rates of disturbance for regimes involving larger areas at site 1 (Fig. 3). Thus, in addition to significantly affecting the number of species, the specific combination of area and frequency of disturbance also determines what kind of species that will be present in assemblages. DISCUSSION This experiment was designed to test the hypothesis that species richness in a hard-substratum assemblage respond in specific ways to different rates of disturbance and that this response depends on the particular combination of area and frequency of the disturbance events. We found that the rate of disturbance affects species richness in a hard-substratum assemblage in different ways at different sites. At one site richness responded in accordance with the predictions from the IDH, while at the other sites there was a monotonic negative effect on richness or richness was not affected at all. Furthermore, at the site where patterns were consistent with the IDH, maximum species richness was observed at lower rates of disturbance when large areas were scraped less frequently, compared to when small areas were scraped more frequently. Because the experiment allows comparisons among regimes at comparable rates of disturbance, our study provide the first unconfounded test and empirical evidence for the hypothesis that different combinations of area and frequency at equal rates have different effects on diversity. TABLE 4. Regressions of species richness on linear and quadratic rates at individual sites. FIG. 4. Species richness, averaged over disturbance regime, as a function of the rate of disturbance at sites 1, 2, and 3. Data are presented as mean 6 SE. See Table 2 for specific details of how each rate can be obtained through two different regimes. Source df MS F P Site 1 Rate Rate2 Residual 1 1 67 61.78 24.78 4.19 14.74 5.91 ,0.001 0.018 Site 2 Rate Rate2 Residual 1 1 77 46.76 0.32 2.87 11.16 0.08 0.001 0.783 Site 3 Rate Rate2 Residual 1 1 77 2.89 1.03 2.85 0.69 0.25 0.409 0.621 502 J. ROBIN SVENSSON ET AL. Ecology, Vol. 90, No. 2 FIG. 5. Effects of rate of disturbance on cover of C. intestinalis, E. silicuosus, and E. intestinalis at site 1, averaged over regime. Data are presented as mean 6 SE. Miller (1982) argued that the underlying cause for observing higher diversity in assemblages under regimes composed of larger, compared to smaller, areas at lower rates, was that larger disturbances would favor species with high capacity for dispersal (i.e., ‘‘colonizers’’) due to the longer persistence of free space. Smaller disturbances should benefit ‘‘competitive’’ species because the larger ratio of perimeter to area allows more rapid reoccupation of space by vegetative growth. In our experiment we investigated the effects of regimes with different area and frequency with similar size and shape of disturbance events at equivalent rates of disturbance. This allowed testing for differences among regimes that are not based on differences in perimeter area ratios. Nevertheless, similar to the predictions in the model by Miller (1982), we observed a larger number of species of ephemeral algae (i.e., Ceramium rubrum, Cystoclonium purpureum, and Ectocarpus siliquosis) in assemblages under the regime composed of larger area at site 1, for rates where this regime showed maximum richness. We also found that the ephemeral algae and the hydroid Laomedea flexuosa (i.e., colonizers [Svensson et al. 2007]) had higher percent cover in regimes with larger area, while the ascidian Ciona intestinalis and the blue mussel Mytilus edulis, which are strong competitors for space (Lenz et al. 2004, Svensson et al. 2007), were more abundant in the regime composed of smaller areas at this site. This means that colonizing species may not only be facilitated by larger ratios of perimeter to area, as predicted by Miller (1982), but also by removing a larger part of the assemblage where their propagules settle. It has previously been shown that post-settlement survivability of propagules is greatly affected by larval– adult interactions, such as competition for food (Osman et al. 1989) and space (Connell 1961), and also that the survivability of propagules is more sensitive during the first few days (Gosselin and Qian 1997). A possible explanation for the difference among regimes in this study may, therefore, be that post-settlement survivability among colonizers is higher where 40% of an assemblage is removed, compared to 20%, due to lower levels of larval–adult competition at the time following the disturbance events. Although the underlying mechanisms for this pattern need to be unraveled by further experiments, our results demonstrate that the disturbance regime will affect the outcome of studies investigating effects of disturbance on diversity. One striking result of this experiment was that the assemblages at the three sites all differed substantially in their response to disturbance. A likely explanation to the variability among sites in their response to disturbance is the natural variation in abundance and composition of assemblages. The total cover in undisturbed assemblages exceeded 100% at site 1, and the ascidian C. intestinalis covered more than 95% of the area. At the other sites, the total cover was less dense and no single taxa covered more than 35%. The high percentage of total cover and TABLE 5. Qualitative differences in cover between regime 1 (small area and frequent disturbances) and regime 2 (large area and infrequent disturbances) at site 1 and rate 2. Species Difference Algae Cystoclonium purpureum Dasya baillouviana Ceramium rubrum Cladophora rupestris Ectocarpus siliquosus Enteromorpha intestinalis Spermotamnion repens Osmondea truncata Polysiphonia fucoides Ceramium strictum þþ þþ þ þ þ þ þ Invertebrates Electra pilosa Membranipora membranacea Ascidiella aspersa Laomeda flexuosa Ciona intestinalis Mytilus edulis Cryptosula pallasiana þþ þþ þ þ Note: Symbols are as follows: þ, larger cover in regime 2; , smaller cover in large areas; , species occurs exclusively in regime 1; and þþ, species occurs only in regime 2. February 2009 DISTURBANCE RATE AND COMMUNITY DYNAMICS 503 FIG. 6. Effects of rate of disturbance on species richness in a study by Svensson et al. 2007 (experiment 1) and this study (experiment 2) expressed as (a) relative disturbance and (b) absolute rate. Data are presented as mean 6 SE. the dominance of the ascidians at site 1, suggests that C. intestinalis is a strong competitor for space, excluding other invertebrates and many species of macroalgae. Such competitive exclusion is a fundamental premise for observing higher diversity at intermediate levels of disturbance in natural communities (e.g., Fuentes and Jaksic 1988, Collins and Glenn 1997). Accordingly, the lack of support for the IDH at the other sites is most likely explained by the absence of clear dominance of strong competitors. By reducing the cover of the strong dominant C. intestinalis, and thereby preventing or disrupting competitive exclusion, disturbance can have a positive effect on diversity in assemblages with intense competition. This mechanism has previously been implied in field experiments in Sweden (Svensson et al. 2007) and Chile (Valdivia et al. 2005), where reduction in cover of the dominant ascidians C. intestinalis and Pyura chilensis both resulted an increase in diversity at intermediate frequencies of disturbance. Additional evidence for the importance of disrupting competitive exclusion comes from several studies involving dominant organisms, such as mussels (Paine 1966), bryozoans (Jara et al. 2006), trees (Molino and Sabatier 2001), and grasses (Collins 1987). An important factor with potentially large effects on the outcome of disturbance experiments is the availability of propagules, which is not easily controlled or measured in field experiments. The availability of propagules and a large regional species pool, is of great importance in order for disturbance to have a positive effect on richness (Osman 1977). In a study on tallgrass prairie vegetation Collins et al. (1995) pointed out that it is settlement by propagules, and not disturbance per se, which increases species richness. If no new species settle in the cleared space, richness will obviously not increase. This was clearly shown in an experiment on soft-bottom intertidal assemblages by Huxham et al. (2000), where the species settling in areas cleared by disturbance were the same species that already inhabited the patch. The different responses to disturbance among experimental sites in this study, and the large difference in total cover of undisturbed assemblages among the sites, suggests that there is large spatial variation in propagule supply. Jonsson et al. (2004) showed that local hydrodynamics strongly influenced the settling of planktonic barnacle larvae and caused highly variable recruitment on panels at different sites in the archipelago where this study was conducted. This could possibly explain the surprisingly low cover (;35%) of substratum in the undisturbed assemblages at site 3. However, the highly disturbed panels at this site still did not show a large reduction in diversity compared to the controls. This suggests that some propagules were capable of settlement, and that the amount of propagules that settled successfully could compensate for the loss in species by the disturbance treatment. One important theme of this paper is the distinction between conceptual and operational terms and its consequences for the interpretation and synthesis of empirical results. Comparisons of the result from site 1 in this study and the one by Svensson et al. (2007), which both provide support for the IDH in the same system, serves to illustrate some of these consequences (Fig. 6). If disturbance is not consistently defined (e.g., frequency the first study and rate in this study) and subsequently compared on a relative scale, the outcomes of the experiments appear similar in some respects but different in others. Maximum diversity was predicted at similar levels of disturbance (0.5 and 0.7) by both models. The parameters of the fitted model were consistent with respect to the intercept, which represents the diversity in the absence of disturbance, while the linear (the rate of increase in the absence of disturbance) and the quadratic components (the curvature) were 504 J. ROBIN SVENSSON ET AL. roughly doubled in this study, compared to the previous (Fig. 6a). When levels of disturbance are transformed into rates, however, it becomes obvious that maximum diversity was obtained at rates approximately three times larger in this compared to the previous study (Fig. 6b). Furthermore, an analysis of the parameters of the fitted model show that the intercept and initial increase were consistent between studies, but that the curvature, i.e., the tendency to decline at higher levels of disturbance, was less pronounced in this study compared to the previous (Fig. 6b). These detailed analyses have important consequences not only for the interpretation of differences in patterns among studies, but also for the hypotheses about the processes that were causing these differences. In a relative perspective it appears that the effect of competitive exclusion at low levels of disturbance was stronger in this compared to the previous study (Fig. 6a). On an absolute scale, however, the effects of competitive exclusion were similar in both experiments, while lack of recruitment of new species in the first experiment was responsible for the rapid decline at higher rates of disturbance. Although this analysis does not provide conclusive evidence about the importance of different processes it is clear that results may be interpreted in very different ways depending on how disturbance is represented. Conclusions This study provides the first unconfounded experimental design for testing the hypothesis that equal rates cause different patterns of diversity. Because the experiment was designed to test effects of regimes at equivalent rates of disturbance, we were able to show that effects on species richness depended on the specific combination of frequency and area and not only on the rate. Furthermore, the effects of a certain rate of disturbance differed substantially among sites. At one site maximum richness was observed at intermediate rates (i.e., support for the IDH), at another site richness of assemblages declined with increasing rates of disturbance and at the third site there was no effect of disturbance. The variable responses among sites were likely due to differences in degree of competitive exclusion and rates of recruitment. In summary, the results suggest that the general understanding of the magnitude and nature of effects of disturbance would benefit from more explicit definitions of the components of disturbance and a stronger focus on the importance of the inherent properties of natural assemblages. ACKNOWLEDGMENTS This study was financially supported by MARICE (an interdisciplinary research platform at the Faculty of Sciences, University of Gothenburg) and by the Swedish Research Council through contract no. 621-2004-2658 to H. Pavia, as well as by Formas through contracts 21.0/2004-0550 to H. Pavia and 217-2006-357 to M. Lindegarth. We thank Malin Karlsson for performing a large part of the fieldwork and Elisabet Brock for assistance with identification of macroalgal species. Ecology, Vol. 90, No. 2 LITERATURE CITED Armesto, J. J., and S. T. A. Pickett. 1985. 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Paper I Paper II Paper III III PAPER Paper IV Paper V On drawing conclusions from observations: “Sir Bedevere: What makes you think she's a witch? Paper VI Peasant: Well, she turned me into a newt! Sir Bedevere: A newt? Peasant: [meekly after a long pause] ... I got better. Crowd: [shouts] Burn her anyway!” -the quest for the Holy Grail, Monty Python Ecology, 91(10), 2010, pp. 3069–3080 Ó 2010 by the Ecological Society of America Physical and biological disturbances interact differently with productivity: effects on floral and faunal richness J. ROBIN SVENSSON,1 MATS LINDEGARTH, AND HENRIK PAVIA Department of Marine Ecology, University of Gothenburg, Tjärnö Marine Biological Laboratory, Strömstad 452 96 Sweden Abstract. Physical and biological disturbances are ecological processes affecting patterns in biodiversity at a range of scales in a variety of terrestrial and aquatic systems. Theoretical and empirical evidence suggest that effects of disturbance on diversity differ qualitatively and quantitatively, depending on levels of productivity (e.g., the dynamic equilibrium model). In this study we contrasted the interactive effects between physical disturbance and productivity to those between biological disturbance and productivity. Furthermore, to evaluate how these effects varied among different components of marine hard-substratum assemblages, analyses were done separately on algal and invertebrate richness, as well as richness of the whole assemblage. Physical disturbance (wave action) was simulated at five distinct frequencies, while biological disturbance (grazing periwinkles) was manipulated as present or absent, and productivity was manipulated as high or ambient. Uni- and multivariate analyses both showed significant effects of physical disturbance and interactive effects between biological disturbance and productivity on the composition of assemblages and total species richness. Algal richness was significantly affected by productivity and biological disturbance, whereas invertebrate richness was affected by physical disturbance only. Thus, we show, for the first time, that biological disturbance and physical disturbance interact differently with productivity, because these two types of disturbances affect different components of assemblages. These patterns might be explained by differences in the distribution (i.e., press vs. pulse) and degree of selectivity between disturbances. Because different types of disturbance can affect different components of assemblages, general ecological models will benefit from using natural diverse communities, and studies concerned with particular subsets of assemblages may be misleading. In conclusion, this study shows that the outcome of experiments on effects of disturbance and productivity on diversity is greatly influenced by the composition of the assemblage under study, as well as on the type of disturbance that is used as an experimental treatment. Key words: disturbance; diversity; dynamic equilibrium model (DEM); intermediate disturbance hypothesis (IDH); marine assemblages; species richness; Tjärnö, Sweden. INTRODUCTION Disturbance has long been recognized as an important structuring force in ecological communities (Darwin 1859). In the mid-1920s Cooper (1926) initiated a discussion on possible effects of disturbance on succession and biodiversity, a discussion that is still ongoing and has given rise to several hypotheses and models. Among the most prominent is the intermediate disturbance hypothesis (IDH; Connell 1978), which predicts that diversity will be high at intermediate levels of disturbance and low at both extremes of a disturbance continuum. Disturbance does, however, not only have documented effects on the diversity of biological communities, but also on evolutionary processes (Benmayor et al. 2008), biological invasions (Davis et al. 2000), and ecosystem functions (Cardinale and Palmer Manuscript received 17 April 2009; revised 27 January 2010; accepted 10 February 2010. Corresponding Editor: B. J. Cardinale. 1 E-mail: [email protected] 2002). The ecological literature contains many examples of agents and definitions of disturbance. One potentially important distinction is that between agents of physical and biological disturbance (McGuinness 1987, Sousa 2001, Svensson et al. 2007). Agents of physical disturbance in previous studies include fire (Eggeling 1947), wind (Molino and Sabatier 2001), wave action (McGuinness 1987), ice-scouring (Gutt and Piepenburg 2003), drifting logs (Dayton 1971), floods (Lake et al. 1989), sediment movement (Cowie et al. 2000), temperature (Flöder and Sommer 1999), desiccation (Lenz et al. 2004), trawling (Tuck et al. 1998), pollution (Benedetti-Cecchi et al. 2001), and even warfare (Rapport et al. 1985). Biological disturbances are mainly predation (Talbot et al. 1978) and grazing (Collins 1987), although some authors add trampling (Eggeling 1947) and burrowing (Guo 1996). Because of the rich variety of agents of disturbance, a number of definitions of disturbance have been proposed to make experiments commensurable (Sousa 2001). The definitions range from Grime’s (1977) 3069 3070 J. ROBIN SVENSSON ET AL. straightforward partial or total destruction of biomass to the more explicit definition of Pickett and White (1985:356) in which disturbance is ‘‘. . . any relative discrete event in time that disrupts ecosystems, community, or population structure and changes resources, substrate availability, or the physical environment.’’ Among the more operational, and therefore more commonly used definitions, is that of Sousa (1984:7), in which disturbance not only kills or damages individuals, but also ‘‘directly or indirectly creates an opportunity for new individuals (or colonies) to become established.’’ The recognition that disturbance creates opportunities for recruitment is crucial, because without new species recruiting into the freed space, disturbance cannot increase diversity (Osman 1977, Collins et al. 1995, Huxham et al. 2000). Disturbance has also been recognized as an important component in multifactorial models in which interactions among community structuring processes are used to predict diversity in natural communities. The dynamic equilibrium model (DEM; Huston 1979, Kondoh 2001) predicts high diversity at high levels of disturbance when productivity is high, because a stronger disturbance is then required to prevent competitive exclusion. Similarly, diversity will be high at low levels of disturbance when productivity is low, because exclusion is then disrupted already by disturbances that are less frequent. The DEM has been tested using either biological or physical agents of disturbance in several experiments in aquatic as well as terrestrial systems (e.g.,Turkington et al. 1993, Worm et al. 2002, Jara et al. 2006, Svensson et al. 2007). The DEM and the IDH have, however, received criticism from both empirical and theoretical studies for being too simplistic and based on weak theoretical grounds (Pacala and Rees 1998, Huxham et al. 2000, Shea et al. 2004). For example, Chesson and Huntley (1997) showed that disturbance may not diminish the importance of competition, as predicted by Huston (1979), and that indirect benefits of disturbance may fall short of the direct negative effects. As a consequence of the elucidation of the models’ weaknesses, their predictions have been suggested, by empirical studies, to rely on a number of prerequisites: competitive exclusion (Fuentes and Jaksic 1988), a large regional species pool (Osman 1977), multiple stages in succession (Collins and Glenn 1997), and trade-offs between competition and colonization (Wilson 1994). These prerequisites, or assumptions, are in essence very similar to the flaws pointed out in theoretical studies, i.e., that disturbance alone cannot stabilize coexistence (Chesson and Huntly 1997) and the underlying mechanisms for coexistence are in fact nonlinear responses caused by trade-offs in life history attributes (Amarasekare et al. 2004) and spatiotemporal niches (Pacala and Rees 1998). In order to benefit from this critique in a constructive way, Shea et al. (2004) proposed that combining the suggestions of improvement from both empirical and theoretical studies will Ecology, Vol. 91, No. 10 lead beyond mere descriptions of the hump-shaped pattern. However, despite the many studies suggesting critique against or improvements of the IDH and DEM, few studies recognize the potentially large source of variation caused by differences in the way an assemblage is disturbed. The manner in which a disturbance inflicts damage is important because disturbances that are equal in extent can nonetheless have significantly different effects on diversity, depending on how the disturbance is distributed (Bertocci et al. 2005, Svensson et al. 2009). In a theoretical study, Bender et al. (1984) identified two different types of disturbance, pulse and press, and evaluated their different effects on species’ interactions. This distinction may also be useful for predictions of patterns of diversity. Instantaneous alteration of species number (pulse) and the sustained alteration of species densities (press) are two clearly different mechanisms that may still fall under the same general definition of disturbance. Consequently, inconsistencies in outcomes may occur if disturbances with dissimilar distributions are treated without distinction in manipulative experiments (Svensson et al. 2009). Furthermore, it may be important to make a general distinction between biological and physical agents, because they commonly differ in the degree of selectiveness (McGuinness 1987, Sousa 2001). Such selectivity may be increasingly complex under interactions with productivity, because consumers often prefer prey with higher nutrient content (Emlen 1966, Onuf et al. 1977, Pavia and Brock 2000). There are many studies from various environments that show interactive effects between biological disturbance and productivity (see Proulx and Mazumder 1998), while tests of the DEM using physical disturbance have more variable outcomes (e.g., Turkington et al. 1993, Jara et al. 2006, Svensson et al. 2007). No study, to our knowledge, has explicitly contrasted differences between biological and physical disturbances and their interactions with productivity. The only study to apply all three factors simultaneously found a significant interaction between biological, but not physical, disturbance and productivity (Kneitel and Chase 2004). These findings suggest that the choice of disturbance agent may influence the outcome of experiments on interactive effects of disturbance and productivity. In this study we contrast the interactive effects between a physical disturbance (i.e., wave action) and productivity to those between a biological disturbance (i.e., grazing) and productivity, in natural marine benthic communities placed in mesocosms. We predict that: (1) the biological disturbance will have a stronger impact on macroalgal species and the physical disturbance will have a stronger impact on invertebrate species and (2) the biological and the physical disturbances therefore will interact differently with productivity. Furthermore, we attempt to identify underlying mechanisms by investigating changes in composition of assemblages among levels of biological and physical October 2010 DISTURBANCES AND PRODUCTIVITY disturbance and productivity, as well as evaluating differences in species’ trade-offs in life history attributes (sensu Pacala and Rees 1998, Shea et al. 2004). Hardsubstratum communities, such as the epilithic assemblages in this study, are generally considered to be suitable for studies on disturbance, because sessile species compete for the limiting resource space (e.g., Sousa 1984). More specifically, manipulative experiments conducted in this system have previously observed the pattern predicted by the IDH, as well as strong competition for space among macroalgae and invertebrates within one season (Svensson et al. 2007, 2009). MATERIALS AND METHODS Experimental assemblages The marine hard-substratum assemblages that were used to study the effects of physical and biological disturbance and productivity were collected from semiexposed boulder fields in the Tjärnö archipelago at depths of 0.5–1.5 m (58852.17 0 N, 1188.82 0 E). The epilithic assemblages were composed exclusively of sessile species, and the collected boulders, on which the assemblages resided, were all of similar size (;20 cm diameter). Common species in this system include red, green, and brown macroalgae, as well as mussels, tunicates, bryozoes, and sea anemones (Svensson et al. 2007, 2009; see Plate 1). The 43 different species present in the experimental assemblages are listed in Table 1. Associated mobile invertebrates (i.e., amphipods and isopods) were not collected and included in the experiment, since our aim was to add grazers of similar density in assemblages subjected to the biological disturbance treatment. Natural conditions of assemblages were maintained to a high extent by a constant supply of unfiltered seawater from the Tjärnö bay, allowing natural conditions of salinity, temperature, food for filter feeders, nutrient availability, and propagules for colonization. Experimental design The experiment was carried out in the Ecotrone mesocosm facility at Tjärnö Marine Biological Laboratory (TMBL), Strömstad, Sweden. One hundred boulders with epilithic assemblages were placed separately in 10-L plastic containers filled with seawater and covered with mosquito nets (mesh size ¼ 1 mm) to prevent grazers from escaping and/or entering. Water volume in the containers was maintained using a constant flow seawater supply, drawn from the bay adjacent to TMBL at 0.5 m depth. The experimental manipulation started on 5 June, had a duration of 17 weeks, and was terminated on 10 October 2005. The physical disturbance treatment was replicated five times in each treatment combination, and the boulders were subjected to one of five different frequencies: twice per week (DP1), once per week (DP2), once every second (DP3) or every fourth week (DP4), or left undisturbed (DP0). The physical disturbance was caused 3071 by rolling each boulder by hand for one minute with equal force in a tub filled with seawater and clean boulders, in order to mimic effects of wave action in boulder fields, at each disturbance event. In addition to killing or damaging individuals, the rolling also facilitates recruitment by freeing substratum, and the disturbance is therefore coherent with the definition by Sousa (1984). The productivity treatment consisted of two levels: ambient (PR0) and increased (PR1). Bags with 100 g slow-release fertilizer were attached to 50 containers with boulders subjected to the increased productivity treatment (PR1), while boulders of the ambient treatment (PR0) were not experiencing increased nutrient availability. Fertilizer bags were changed every eighth week in order to have constant nutrient release throughout the experiment. Plantacote Depot 6-M (5.7% NO3, 8.3% NH4, 9% P2O5, and 15% K2O; AGLUKON, Düsseldorf, Germany) was used as fertilizer due to its steady release rate (Worm et al. 2000). The common periwinkle, Littorina littorea, is a very abundant and important grazer in the Tjärnö archipelago (Wikström et al. 2006, Toth et al. 2007) where the boulders were collected and was therefore used in the grazing treatment. Littorina littorea periwinkles were collected from the same areas as the boulders. In order to achieve an ecologically relevant grazing pressure we conducted a pilot study that suggested that ;10 periwinkles would be appropriate for the size of the boulders in this experiment. Accordingly, 10 L. littorea of similar size were added to each of the 50 boulders subjected to the biological disturbance treatment (DB1), and no periwinkles were added to the remaining 50 boulders, which were not experiencing grazing (DB0). Sampling Sampling of abundance and composition of the communities was done at the end of the experiment after 17 weeks of manipulation. Boulders were brought into the laboratory submerged in seawater and also kept under running seawater in the laboratory during the entire sampling procedure. An area of 100 cm2 was randomly chosen on each boulder for sampling, in order to sample an equal area from all boulders regardless of differences in actual area and size. Percent cover of bare space and sessile species was then estimated at 5% intervals using a 10 3 10 cm plastic grid, and a dissecting microscope (magnification 123) was used for species identification. Percent cover of species with a small holdfast and wide thallus was estimated from the twodimensional projection of the organism on the panel. Sessile epibionts were also accounted for. Thus, total cover was allowed to exceed 100%. Statistical analyses The data obtained from the experiment were analyzed with a three-way factorial ANOVA using Statistica 6.0 3072 J. ROBIN SVENSSON ET AL. Ecology, Vol. 91, No. 10 TABLE 1. Abundance (percent cover, mean 6 SE) of sessile invertebrate and algal species present in the experimental communities after 24 weeks, averaged over nutrient treatment for all levels of physical disturbance (DP0–DP4). Species Chlorophyceae Chaetomorpha melagonium Cladophora albido Cladophora rupestris Codium fragile Enteromorpha prolifera Enteromorpha intestinalis Ulva lactuca Phaeophyceae Ahnfeltia plicata Dumontia incrassata Ectocarpus siliculosus Fucus serratus Fucus vesiculosus Ralfsia tenuis Sargassum muticum Sphacelaria cirrosa Sphacelaria plumosa Rhodophyceae Bonnemaisonia hamifera Ceramium rubrum Ceramium strictum Chondrus crispus Corallina officinalis Cystoclonium purpureum Furcellaria lumbricalis Hildenbrandia rubra Lithothamnion sp. Osmundea truncata Polysiphonia nigrescens Polysiphonia urceolata Polysiphonia violacea Spermothamnion repens DP0 0.5 6 0 0.9 6 0 0.4 6 1.4 6 1.65 6 DP1 0.11 0.54 0.26 0.67 1.09 0.4 6 0.26 1.3 6 1.25 0 1.0 6 1.0 21.55 6 7.59 0 0.5 6 0.50 7.35 6 3.38 0.25 6 0.25 1.6 0.1 0.1 19.6 0.05 2.75 1.25 4.1 15.6 1.5 1 2.45 0.15 6 6 6 6 6 6 6 6 6 6 6 6 6 0 1.50 0.07 0.07 7.04 0.05 1.56 1.25 2.52 3.97 1.50 0.78 1.99 0.08 DP2 DP3 0.6 6 0.11 0.1 6 0.07 1.2 6 0.57 0 0.45 6 0.26 3.7 6 3.24 1.45 6 0.60 0.85 0.3 0.55 0.25 1.75 2.8 0.75 0.24 0.25 0.26 0.25 1.25 1.54 0.34 0.8 0.05 0.3 0.05 1.45 5.4 1.1 2.5 0.05 0.05 1.55 0.75 0.05 0.1 6 0.07 0.25 6 0.10 0.1 6 0.07 0 0 0 0 1.75 6 0.71 0 0.8 0.55 0.05 0.05 6 6 6 6 6 6 0 5.1 6 0 1.38 0.05 0.05 1.03 0.55 0.05 2.61 0.25 6 0.25 0.1 6 0.07 0 17.1 6 8.03 0 1.35 6 1.25 0.25 6 0.25 2.6 6 1.11 8.15 6 2.25 0 0.05 6 0.05 1.75 6 1.22 0.25 6 0.25 0 7.25 0.05 2.85 7.65 0.05 0.1 0.05 6 6 6 6 6 6 6 0 0 0 6 0 6 0 6 6 0 6 6 6 0 3.46 0.05 1.11 2.23 0.05 0.05 0.05 DP4 6 6 6 6 6 6 6 0.25 0.05 0.11 0.05 0.60 3.18 0.45 1.6 6 0.54 0.25 6 0.10 0.5 6 0.26 0 0.9 6 0.33 4.15 6 1.59 1.9 6 0.70 6 6 6 6 0 0 0 1.2 6 0 0.55 0.26 0.05 0.05 0.05 6 0.05 0.05 6 0.05 0 0 0 0 0 0.9 6 0.33 0 0.57 0.05 6 0.05 0.1 6 0.07 0 7.35 6 2.94 0 0 0 4.25 6 1.59 8.9 6 3.63 0 0 0 0 0.05 6 0.05 0 0.1 6 0 2.0 6 0 0 0 3.05 6 3.7 6 0 0.1 6 0.1 6 0.05 6 0 0.07 0.58 1.04 1.18 0.07 0.07 0.05 Porifera Leucosolenia botryides 0.05 6 0.05 0 0.05 6 0.05 0 0 Cnidaria Dynamena pumila Laomedea flexuosa Metridium senile 0.05 6 0.05 0.05 6 0.05 0.5 6 0.26 0 0.05 6 0.05 0 0.05 6 0.05 0.1 6 0.07 0 0 0.25 6 0.10 0.05 6 0.05 0 0.65 6 0.34 0 Annelida Pomatoceros triqueter Spirorbis spirorbis 0.2 6 0.09 0.75 6 0.50 0.4 6 0.26 0.05 6 0.05 0.05 6 0.05 0.4 6 0.26 0.1 6 0.07 0.15 6 0.08 0.35 6 0.25 0.15 6 0.08 Crustacea Balanus crenatus Semibalanus balanoides 0.05 6 0.05 0.05 6 0.05 0.1 6 0.07 0 0.1 6 0.07 0 0.05 6 0.05 0 0.15 6 0.08 0 Mollusca Acanthocardia sp. Leptochiton sp. Mytilus edulis 0.05 6 0.05 0.25 6 0.10 0.4 6 0.26 0 0 0.05 6 0.05 0 0 0 0 0 0 0 0 0 2.4 6 0.75 1.45 6 0.79 0.6 6 0.34 0.45 6 0.26 0.55 6 0.26 Bryozoa Cryptosula pallasiana Hemichordata Ciona intestinalis Total coverage 0.6 6 0.05 0 0 0 0 90.1 6 8.86 49.8 6 9.52 29.2 6 4.98 31.6 6 6.25 21.3 6 3.13 Note: The marine hard-substratum assemblages that were used to study the effects of physical and biological disturbance and productivity were collected from semi-exposed boulder fields in the Tjärnö archipelago, Sweden. (Statsoft, Tulsa, Oklahoma, USA) and with permutational multivariate analysis of variance (PERMANOVA) using the Permanova software (Anderson 2001). The multivariate analyses were performed to reveal whether differences were solely related to the number of species or also dependent upon the particular species present and their relative abundance. Hypotheses about effects of main factors and interactions were tested using October 2010 DISTURBANCES AND PRODUCTIVITY 3073 TABLE 2. ANOVA on total species richness, algal richness, and invertebrate richness. Total richness Algal richness Invertebrate richness Source df MS P MS P MS P PR DB DP PR 3 DB PR 3 DP DB 3 DP PR 3 DB 3 DP Residual 1 1 4 1 4 4 4 80 171.28 61.76 16.82 16.74 0.79 8.54 3.26 3.83 0.000 0.000 0.003 0.040 0.935 0.073 0.496 132.49 99.34 2.41 8.88 1.31 4.55 1.44 3.15 0.000 0.000 0.552 0.097 0.797 0.228 0.767 2.49 4.44 7.30 1.24 1.94 1.07 1.75 1.20 0.154 0.058 0.000 0.313 0.178 0.473 0.223 Notes: Values in boldface indicate significance. Abbreviations are: PR, productivity; DB, biological disturbance; DP, physical disturbance. the following general linear model: Xijkl ¼ l þ PRi þ DBj þ PRDBij þ DPk þ PRDPik þ DBDPjk þ PRDBDPijk þ eijkl where l is the overall mean, PRi is the ith level of productivity, DBj is the jth level of biological disturbance, DPk is the kth level of physical disturbance, and eijkl is a random deviation. Productivity, biological disturbance, and physical disturbance are fixed factors with two, two, and five levels, respectively. For the univariate analysis post hoc tests of differences among means were analyzed using the Student-Newman-Keuls test (SNK), and t tests were used for the multivariate analysis following the recommendations by Anderson (2001). For all analyses data were tested for meeting the assumptions of the statistical methods. The hypothesis that physical and biological disturbance will interact differently with productivity is supported if there is an interaction between productivity and either biological disturbance or physical disturbance exclusively or if a three-way interaction reveals different patterns for different factorial combinations. Support for the hypothesis that physical and biological disturbance will have different effects on different components of assemblages is found if algal and invertebrate richness are affected by either type of disturbance exclusively or if the effects of the treatments show different patterns (e.g., increase vs. decline) for algal compared to invertebrate richness. In order to visualize patterns of the multivariate tests and identify differences in species’ life history trade-offs, canonical analysis of principal coordinates (CAP; Anderson and Willis 2003) was used as a constrained ordination procedure on appropriate terms found to be significant using PERMANOVA. RESULTS General observations During the experiment a total of 13 sessile invertebrates and 31 algal species were observed in the experimental communities. The macroalgae were not only numerous in species, they also covered most of the area in the experimental assemblages, and the most abundant organisms were the red alga Chondrus crispus, the brown alga Fucus vesiculosus, and the green algae Enteromorpha intestinalis and Chaetomorpha melagonium. Unlike the algae, the ascidians, bryozoans, crustaceans, molluscs, and sea anemones were usually infrequent and had low percent cover in the assemblages (Table 1). Efficiency of the productivity treatment In order to detect effects on productivity as a consequence of the nutrient addition, differences in percent cover among levels of nutrient availability were tested. The ANOVA showed that there was a significant effect of nutrient availability on total cover (F1,80 ¼ 26.9, P , 0.001). Inspection of means (total cover for PR0 and PR1 were 29.4 6 4.0 and 58.7 6 4.0 [mean 6 SE], respectively) showed that the total percent cover in assemblages experiencing increased nutrient availability was significantly higher than total cover under ambient nutrient availability. This large difference in coverage was mainly caused by increases in percent cover of algal species (cover of algae for PR0 and PR1 were 27.9 6 4.0 and 56 6 4.0, respectively). Effects of frequency of physical disturbance Analysis of total species richness and community composition at the end of the experiment showed that there were significant effects of physical disturbance (Tables 2 and 3 and Figs. 1a and 2), but no interactive effects with productivity (Tables 2 and 3). A tendency TABLE 3. Permutation multivariate analysis of variance (PERMANOVA) with data transformed to presence/absence. Source df MS P PR DB DP PR 3 DB PR 3 DP DB 3 DP PR 3 DB 3 DP Residual 1 1 4 1 4 4 4 80 14 240 39 085 2899 4044 972 2313 1237 1746 0.001 0.001 0.034 0.028 0.944 0.159 0.829 Notes: Values in boldface indicate significance. Abbreviations are: PR, productivity; DB, biological disturbance; DP, physical disturbance. 3074 J. ROBIN SVENSSON ET AL. Ecology, Vol. 91, No. 10 FIG. 1. (a) Effects of frequency of physical disturbance on total species richness, algal richness, and invertebrate richness (mean 6 SE). (b) Effects of frequency of physical disturbance on mean cover of Chaetomorpha melagonium, Chondrus crispus, Enteromorpha intestinalis, and Fucus vesiculosus averaged over nutrient and grazing treatments (mean 6 SE). The marine hardsubstratum assemblages that were used to study the effects of physical and biological disturbance and productivity were collected from semi-exposed boulder fields in the Tjärnö archipelago, Sweden. for an interaction between physical and biological disturbance was found in the univariate analysis (P ¼ 0.07; Table 2), indicating that the effects of biological disturbance on richness were stronger in the presence of physical disturbance (i.e., grazers had no impact on undisturbed assemblages: richness for DP0DB0 and DP0DB1 were 8.1 6 0.50 and 8.1 6 0.71, respectively). Post hoc analysis on the multivariate test showed that undisturbed assemblages were significantly different from those experiencing higher levels of physical disturbance (post hoc, DP0 ¼ DP1 6¼ DP2 6¼ DP3 6¼ DP4, at a ¼ 0.05) and in the univariate test all levels of disturbance had lower species richness compared to the undisturbed treatments (post hoc, DP0 . DP1 ¼ DP2 ¼ DP3 ¼ DP4, at a ¼ 0.05). Graphical examination of the multivariate test using CAP revealed that undisturbed assemblages and assemblages experiencing high levels of physical disturbance were distributed at opposite sides along the first axis with overlap around the origo (Fig. 2). Inspection of the mean cover of the most abundant species suggested that there was a strong negative effect on the cover of the perennial red alga Chondrus crispus and the brown alga Fucus vesiculosus, whereas the ephemeral green alga Enteromorpha intestinalis and Chaetomorpha melagonium, capable of rapid growth and colonization, were positively affected by disturbance (Fig. 1b). Investigation of the effects of physical disturbance on richness of algal and invertebrate species showed that only the invertebrate species were significantly affected (Table 2). Graphical analysis also showed that the number of invertebrate species was higher in assemblages that were not subjected to physical disturbance compared to assemblages that experienced physical disturbance, whereas the algal richness remained fairly constant over the disturbance continuum (Fig. 1a). October 2010 DISTURBANCES AND PRODUCTIVITY 3075 FIG. 2. Constrained canonical analysis of principal coordinates (CAP) plot on Bray-Curtis similarity comparing assemblages among levels of physical disturbance (twice per week [DP1], once per week [DP2], once every second [DP3] or every fourth week [DP4], or left undisturbed [DP0]). Values shown for d2 are the squared canonical correlation coefficients. Effects of biological disturbance There was a significant interaction between biological disturbance and productivity for total species richness, whereas algal richness was significantly altered by biological disturbance and productivity independently and the invertebrate species was not affected by either factor (Table 2 and Fig. 3a–c). Inspection of means showed that the effect of biological disturbance on total richness was greater in assemblages in which nutrients were not added (Fig. 3a). Thus richness was significantly higher in assemblages with both grazers and nutrient additions than in assemblages with only grazers (post hoc; PR0, DB0 . DB 1; PR1, DB0 ¼ DB1; DB0, PR0 , PR1; DB1, PR0 , PR1; at a ¼ 0.05), which suggested that the productivity treatment counteracted the effects of biological disturbance on richness. The interaction between biological disturbance and productivity was also significant in the multivariate analysis (Table 3) and post hoc analysis showed that all factor combinations differed significantly (post hoc; PR0, DB0 6¼ DB1; PR1, DB0 6¼ DB1; DB0, PR0 6¼ PR1; DB1, PR0 6¼ PR1; at a ¼ 0.05). Further graphical examination using CAP revealed that, similar to the univariate analysis, there was a more distinct separation between communities with high compared to low productivity when grazers were present (Fig. 4). Inspection of mean cover at the species level showed that the green alga Chaetomorpha melagonium was positively affected by biological disturbance, whereas Sphacelaria cirrosa and Enteromorpha intestinalis decreased in the presence of grazers, and that Hildenbrandia rubra was more frequent at high levels of productivity (Fig. 4). Thus, in addition to significantly affecting the number of species, the levels of biological disturbance and productivity interactively determine what species will be present in the assemblages. DISCUSSION In accordance with the first hypothesis, biological and physical disturbances had different effects on the marcoalgal and invertebrate species in the assemblages. Biological disturbance significantly reduced only macroalgal richness, whereas physical disturbance exclusively reduced invertebrate richness. Our second prediction, that interactive effects of biological disturbance and productivity on species richness were different from those of physical disturbance and productivity, was also supported. Increased productivity had a positive effect on the number of algal, but not invertebrate, species. Total species richness was negatively affected by biological disturbance under ambient productivity, but richness was generally larger and not affected by biological disturbance when productivity was increased. Physical disturbance, on the other hand, had a negative effect on richness irrespective of whether productivity was high or ambient. Similarly, the multivariate analyses showed that increased productivity affected species composition interactively with biological disturbance but not with physical disturbance. Furthermore, evalu- 3076 J. ROBIN SVENSSON ET AL. ation of responses of individual species to both types of disturbance and productivity indicate that differences in assemblage composition may be attributed to differences in species’ trade-offs in life history characteristics. The results of this study are consistent with those of Kneitel and Chase (2004) and Svensson et al. (2007), who found that the effect of physical disturbance on richness was not affected by levels of productivity. Svensson et al. (2007) suggested that their results could be explained by the lack of a positive effect of the productivity treatment on the dominant invertebrate species. However, this cannot explain the lack of an interactive effect in our experiment, since the dominant organisms were macroalgae, which benefit directly from increased nutrient availability (e.g., Worm et al. 2002). The outcome is instead more likely explained by the different effects of treatments on different components of the assemblages. Physical disturbance affected the number of invertebrate species, but not algal richness. The invertebrate species were not affected by either productivity or biological disturbance. Thus, the decimation of invertebrate species by physical disturbance could not be counteracted by productivity, and, consequently, there were no interactive effects between the two treatments. There was, however, a tendency for interactive effects between physical and biological disturbance, although physical disturbance did not show the quadratic function predicted by the IDH, which has previously been observed in this environment (Svensson et al. 2007, 2009). The lack of support for the IDH is likely explained by the low rate of competitive exclusion, despite the presence of competitive species, and the tendency for interactive effects is possibly caused by consumers inhibiting recolonization of free substratum (e.g., Underwood 1980, Robles 1982). Unlike physical disturbance, biological disturbance had interactive effects with productivity on total species richness, which is in accordance with previous studies from many different environments (Proulx and Mazumder 1998). The number of algal species was higher in assemblages subjected to both grazing and productivity than in assemblages subjected only to grazing. This indicates that the positive effect of the productivity treatment counteracted the negative effects of the biological disturbance. Thus, it would appear that productivity, rather than biological or physical disturbance, was the factor promoting diversity in this experiment, in contrast to previous manipulative experiments in the same system (Svensson et al. 2007, 2009). It has been shown in both theory (Chesson and Huntly 1997) and practice (Huxham et al. 2000) that disturbance, by either physical or biological agents, is not in itself a diversity-promoting mechanism. Advancements have, however, been made in response to this criticism by the suggestions of specific prerequisites that are necessary for disturbance-mediated coexistence (e.g., Collins and Glenn 1997) and alternative theoretical models, such as the ‘‘storage effect’’ (Roxburgh et al. Ecology, Vol. 91, No. 10 FIG. 3. Interactive effects of productivity (PR0, PR1) and biological disturbance, averaged over levels of physical disturbance, on (a) total species richness, (b) algal richness, and (c) invertebrate richness (mean 6 SE). Productivity 0 is ambient productivity, and PR1 is increased productivity (increased growth rates in the experimental assemblages through the addition of nutrients: 100 g of slow-release fertilizer per experimental assemblage). 2004) and ‘‘successional niche’’ (Pacala and Rees 1998). The common ground in both the suggested prerequisites and the alternative models is that disturbance can promote coexistence in spatially homogeneous competitive environments with large species pools if the species show differences in life history trade-offs. Coexistence may then occur through creation of spatiotemporal niches by disturbance, which may allow inferior species competitive advantages over dominants in different niches. Interpretation of results from multivariate analyses within this framework may allow identification of underlying mechanisms of disturbance–diversity patterns through investigation of changes in community October 2010 DISTURBANCES AND PRODUCTIVITY 3077 FIG. 4. Constrained canonical analysis of principal coordinates (CAP) plot on Bray-Curtis similarity comparing assemblages among levels of productivity (high [PR1] or ambient [PR0]) and biological disturbance (present [DB1] or absent [DB0]). Treatment combinations plotted are: productivity and biological disturbance (PR1DB1), solely biological disturbance (PR0DB1) or productivity (PR1DB0), and controls (PR0DB0). Values shown for d2 are the squared canonical correlation coefficients. composition and life history trade-offs (Shea et al. 2004). In this study, there were significant differences in composition of species in the assemblages among levels of physical disturbance. Biological disturbance and productivity interactively affected the composition of assemblages to form four distinct groups based on the treatment combination (PR0DB0, PR0DB1, PR1DB0, and PR1DB1). Although these four groups were all significantly different, there were larger differences among levels of productivity in the presence of grazers, which is in accordance with the results from the univariate analyses. Evaluation of responses of individual species allows for speculations on whether differences in species’ trade-offs in life history characteristics may be the underlying cause for differences in assemblage composition. For instance, the green alga Chaetomorpha melagonium was positively affected by both physical and biological disturbance, but not by productivity, possibly suggesting life history attributes toward environmental tolerance rather than competition or fast growth (Dial and Roughgarden 1998). Conversely, Enteromorpha intestinalis, another green alga, was positively affected by physical disturbance and productivity, but not by biological disturbance, thus indicating a trade-off for fast growth compared to grazer tolerance or competitive capacity (Petraitis et al. 1989). Two algal species, Fucus vesiculosus and Chondrus crispus, had coverage of up to 100% in individual undisturbed assemblages and were negatively affected by physical disturbance, while not benefiting from either productivity or biological disturbance. This shows that there were species present in the assemblages that have characteristics of competitive dominants, even though the strong competitive exclusion seen in this system in previous experiments (Svensson et al. 2007, 2009) was not apparent here. In accordance with the theories of Pacala and Rees (1998), trade-offs in species’ life history attributes allowed assemblages to differ in composition, depending on the levels and treatment combinations of biological and physical disturbance and productivity. Thus, it would appear that combinations of different regimes of disturbances and productivity enable different species to thrive under different conditions, ultimately maintaining regional and/or local coexistence. The underlying mechanisms of the interaction between biological, but not physical, disturbance and productivity, is most likely a combination of differences in growth rates of species among levels of productivity and mechanical differences in the way the damage is inflicted on the assemblages. In addition, productivity interacted with biological but not physical disturbance, reflecting qualitative differences between the damage exerted by the two types of disturbance. It has previously been shown that similar disturbances can 3078 J. ROBIN SVENSSON ET AL. Ecology, Vol. 91, No. 10 PLATE 1. (Main image) A typical boulder field on the west coast of Sweden. (Inset) Submerged boulders with benthic assemblages composed of green, brown, and red macroalgae, as well as bryozoans, hydroids, mussels, tunicates, polychaetes, and sea anemones. A color version of this plate is available in the Appendix. Photo credits: J. R. Svensson. have different effects on diversity, depending on the way the damage is distributed (Bertocci et al. 2005, Svensson et al. 2009). In a theoretical study, Bender et al. (1984) have described differences between two kinds of mechanical disturbances, pulse and press. The herbivorous periwinkles in our experiment could be characterized as a press disturbance because they exert a continuous small-scale reduction of biomass in algal species. When biomass is slowly reduced, this effect can more easily be counteracted by increased growth of the affected organisms (Huston 1979, Kondoh 2001). The productivity treatment probably had such a positive effect, since diversity was higher in assemblages that experienced grazing and nutrient addition compared to assemblages subjected solely to grazing. The frequency of physical disturbance shows characteristics similar to pulse disturbance, which instantaneously kills, or removes, a fraction of the community (Bender et al. 1984, Sousa 1984). Increased individual growth rate cannot easily compensate for instantaneous loss of individuals, which could explain the lack of interactive effects between productivity and physical disturbance in this experiment. In accordance with these arguments and our results, Kneitel and Chase (2004), in the only previous study that has tested for interactions of all three factors, also found that biological disturbance (predation), but not physical disturbance (drying), and productivity interactively affected species richness. Although Kneitel and Chase (2004) did not discuss their treatments in terms of press and pulse disturbances, the predatory mosquito larvae in their study could be characterized as a press disturbance, whereas drying every third or eighth day is similar to a pulse disturbance. Thus, not only the selectivity, but also the way that the damage caused by disturbance is applied, may differ between agents of biological and physical disturbance and determine the outcome of multifactorial experiments. In this study we have shown that the outcome of experiments on disturbance and productivity is greatly influenced by the type of disturbance that is used as a treatment and also on the composition of the assemblage upon which the disturbance is inflicted. Previous studies testing the DEM have commonly looked at specific parts of natural communities, such as annelids (Widdicombe and Austen 2001), macroalgae (Worm et October 2010 DISTURBANCES AND PRODUCTIVITY al. 2002), or periphytes (Cardinale et al. 2006), or used artificial assemblages composed of bacteria and protozoans (Rashit and Bazin 1987), protozoans and rotifers (Kneitel and Chase 2004), or bacteria and ciliates (Scholes et al. 2005). The effects of treatments in such experiments may be overestimated if the specific group of species in the study are strongly affected or, conversely, underestimated if species strongly affected by the process in nature are not present in the experimental assemblages. We have also shown, for the first time, that an agent of biological disturbance and an agent of physical disturbance interacted differently with productivity due to their different effects on different components of assemblages. Differences in community composition and in responses of individual species also indicate that the underlying mechanism for the observed effects of both types of disturbance and productivity may be traced back to species’ trade-offs in life history attributes. In conclusion, our findings suggest that experiments testing hypotheses on interactive effects between disturbance and productivity, such as the DEM, benefit from working with natural diverse communities and should consider the ecological relevance of manipulative treatments in relation to both the explanatory model and the system under study. ACKNOWLEDGMENTS This study was financially supported by MARICE (an interdisciplinary research platform at the Faculty of Sciences, Göteborg University) and by the Swedish Research Council through contract number 621-2007-5779 to H. Pavia, as well as by Formas through contracts 21.0/2004-0550 to H. Pavia and 217-2006-357 to M. Lindegarth. We thank Malin Karlsson for performing a large part of the fieldwork and Anneli Lindgren for assistance with identification of macroalgal species. We also thank two anonymous reviewers, whose comments greatly improved an earlier version of the manuscript. LITERATURE CITED Amarasekare, P., M. F. Hoopes, N. 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The intermediate disturbance hypothesis of species coexistence is based on patch dynamics. New Zealand Journal of Ecology 18:176–181. Worm, B., H. K. Lotze, H. Hillebrand, and U. Sommer. 2002. Consumer versus resource control of species diversity and ecosystem functioning. Nature 417:848–851. Worm, B., T. B. H. Reusch, and H. K. Lotze. 2000. In situ nutrient enrichment: methods for marine benthic ecology. International Review of Hydrobiology 85:359–375. APPENDIX A color version of Plate 1 showing a typical boulder field on the west coast of Sweden (Ecological Archives E091-213-A1). Paper I Paper II PAPER Paper III IV Paper IV Paper V ”Du utför ditt slitgöra, match efter match, och håller käften. Då kommer du dit du vill.” - Håkan Mild Paper VI An Epic Journal 1(1), 2010, pp. 1-8 © 2010 by the El Grande Society The Intermediate Disturbance Hypothesis predicts different effects on species richness and evenness J. Robin Svensson1, Mats Lindegarth, Per R. Jonsson, and Henrik Pavia Department of Marine Ecology - Tjärnö, University of Gothenburg, SE-452 96 Strömstad, Sweden Abstract. The Intermediate Disturbance Hypothesis (IDH) is among the most influential theories in ecology. Yet, the aspect of biodiversity predicted to peak at intermediate disturbance is not explicitly defined, or even discussed, in the literature. An issue that reaches beyond the scientific community, since the IDH also influences management of national parks and reserves. As a consequence of this apparent lapse in disturbance theory, tests of the IDH and later extensions are often based on unclear hypotheses and ambiguous measures of biodiversity. We used one established model and one new, spatially explicit model to compare the responses to disturbance between the two major aspects of biodiversity: species richness and the evenness of species abundance. Both models support the IDH when biodiversity is measured as species richness, but predict that evenness instead increases monotonically with increasing levels of disturbance. In order to investigate the generality of this discrepancy, we performed an extensive meta-analysis of studies that use more than one measure of diversity and support the IDH. In accordance with the predictions of the models, two-thirds of the published studies in the survey present different results for different diversity measures. More specifically, comparisons between richness and evenness showed an even higher degree of dissimilarity. Hence, based on the logic behind the underlying mechanism of the IDH, the predictions of our two models and the meta-analysis, we argue that species richness is the most straightforward and appropriate response variable in tests of the IDH and its associated models. Key words: disturbance; diversity indices; evenness; ecological models; IDH; species richness. INTRODUCTION the last five years. The IDH, and the related dynamic equilibrium model (DEM; Huston 1979, Kondoh 2001), have received criticism in both empirical and theoretical studies (Pacala and Rees 1998, Huxham et al. 2000, Shea et al. 2004). Variable outcomes of empirical tests have led to the awareness that the models rely on a number of assumptions: competitive exclusion (Fuentes and Jaksic 1988), large regional species pool (Osman 1977), multiple stages in succession (Collins and Glenn 1997) and tradeoffs between competition and colonization (Wilson 1994). Similarly, theoretical studies argue that the underlying mechanisms for coexistence are nonlinear responses to competition (Amarasekare et al. 2004) and spatiotemporal differences in niches (Pacala and Rees 1998). This critique has, thus, led to a more thorough understanding of the underlying coexistence mechanisms (Shea et al. 2004). However, regardless of these improvements of the models, tests of the IDH will inevitably also depend on the choice of diversity measure and this has not yet received attention. Arguably, the most fundamental steps in science are the formulation and testing of hypotheses (Popper 1959, Underwood 1997, Quinn and Keough 2002). This involves the logical linking of results from observations or experiments to the hypothesis under test. Without clear and explicit definitions of response variables, empirical studies cannot unambiguously test the predictions of the model. In ecological sciences, a central concept with such an elusive definition is biodiversity (e.g. CBD Rio 1992). Because of the great inconsistency in the way scientists define and measure biodiversity (e.g. Hurlbert 1971), hypotheses aiming to predict patterns of diversity, and the subsequent tests, can be unclear. The well-known intermediate disturbance hypothesis (IDH; Connell 1978) constitute, together with its related models (Huston 1979, Miller 1982, Kondoh 2001), a keystone in ecological theory, but it is also a case where many tests are based on unclear predictions and ambiguous measures of biodiversity. The original formulation of IDH predicts maximum biodiversity to occur at an intermediate level of disturbance due to coexistence of competitive dominants and rapid colonizers, while diversity will be low at both extremes due to competitive exclusion and local extinction. The IDH is one of few well established ecological theories and has influenced management and conservation of nature reserves (Wootton 1998) as well as grass- and pasture-land (Olff and Ritchie 1998). The original work by Connell has received more than 3000 citations and continues to generate scientific papers at an increasing rate, with over one third of all articles published 1 Considering the large body of literature on the IDH and its later extensions it is surprising that it is still unclear what aspects of species diversity that are predicted or measured. This is even more remarkable, given that many other aspects of the IDH have received ample attention, such as alternative mechanisms underlying coexistence (Pacala and Rees 1998), influence of characteristics of communities (Fuentes and Jaksic 1988), interactive effects of disturbances (Collins 1987), specific traits of individual species (Haddad et al. 2008), temporal variation of disturbance (Bertocci et al. 2005), how disturbance is applied (Svensson et al. 2009) as well as the important Corresponding author: J. Robin Svensson Email: [email protected] 1 J. ROBIN SVENSSON ET AL. apparent and unrecognized lapse in the tests of IDH and related hypotheses/models jeopardizes the applicability of disturbance-diversity theory in both basic and applied ecology. discussion on definitions of ecological disturbance (Pickett and White 1985). In contrast, explicit discussions of how to measure species diversity for appropriate tests of the IDH is lacking in even the most extensive and influential reviews on disturbance (cf. Sousa 1984, Mackey and Currie 2001, Sousa 2001, Shea et al. 2004). Hence, it is not surprising that there is no consensus on which measure of diversity to use. A consequence of the lack of such a consensus is that the IDH is tested with a plethora of measures and indices of diversity, such as, Margalef’s Richness, Simpson’s D, clonal diversity, functional diversity, 1-lambda, and the more well known Shannon index H’ (a.k.a the Shannon-Wiener or Shannon-Weaver index, eqn 3; Shannon 1948, Shannon and Weaver 1963), Pielou’s Evenness (eqn 4; Pielou 1966), and Species Richness (i.e. number of species). It is likely that much of the confusion about how to measure diversity stems from the lack of clarity in the original formulations of IDH and related models. The confusion about what aspects of biodiversity that are predicted by IDH led us to explore in detail the logical link between IDH and biodiversity. We first show that models of the IDH generate qualitatively different predictions for different biodiversity measures. Secondly, we apply a meta-analysis of the published tests of IDH to show that support of IDH indeed depends on how diversity is measured. Finally, we discuss the need for hypotheses about mechanisms explaining the relationship between disturbance intensity and specific measures of biodiversity. METHODS Model predictions of how disturbance affects species richness and evenness In the original article by Connell (1978), the word diversity is frequently used without being defined in the text, while species richness is the only specific measure of diversity used in graphs and tables. This indicates that the IDH primarily was intended to predict changes in the number of species. The dynamic equilibrium hypothesis (DEM; (Huston 1979, Kondoh 2001), an extension of the IDH, predicts that the level of disturbance where maximum diversity is observed will depend on the level of productivity. Huston (1979) defines diversity as only richness and evenness, rejecting various diversity indices, but makes no distinction in predictions between effects of disturbance on richness and evenness. Kondoh (2001) discusses only species richness and does not consider specific effects of productivity and disturbance on evenness. In yet another extension of the IDH, on differences in effects depending on distribution of disturbance, Miller (1982) stated that the highest diversity will occur at an intermediate rate of disturbance “…if diversity is a measure of both species abundance and number”. The addition of species abundance to the hypothesis is, however, not explained or motivated in the article. The only articles to our knowledge that discuss the relevance of different diversity measures in tests of the IDH, are those by Sommer (1995) and Weithoff et al. (2001). Both articles mainly concern phytoplankton communities, but while Weithoff et al. (2001) argues that functional diversity, rather than species diversity, is the most suitable response variable, Sommer (1995) maintains that theories about coexistence principally predict changes in species number, not abundances or diversity indices. In their review, Shea et al. (2004) argue that the IDH cannot be tested by studies using only one species, because the IDH does not make predictions about abundances of species. If the IDH does not predict differences in abundance, not only single species studies but also tests using compound diversity indices or the evenness of species distributions as response variables are inappropriate. The lack of an explicit definition of diversity in the original presentation of the models has, together with the variety of response variables that have been used in subsequent experimental tests, made the status of the IDH and related models unclear. This The two models, spatially implicit and explicit, both involve one-sided competition, occupancy as a function of colonization ability, competitive strength and local extinction, which increases with disturbance. A pool of 20 species was used in all modeling runs and colonization rates of the ith species, ci, were modeled as ci=0.1/0.9i: (Kondoh 2001). The first model (A) is a spatially implicit patch-occupancy model proposed by Kondoh (2001) and later used by Worm et al. (2002). The model was solved using an ordinary differential equation solver in Matlab® 7.6 (MathWorks Inc) and colonization rates of the ith species, ci, was modeled as ci=0.1/0.9i: (Kondoh 2001). For more details see Kondoh (2001). Since spatial relationships are well-known to affect population- and community dynamics (e.g. Hassell et al. 1991, Molofsky 1994), the second modeling approach (B) Table 1. a) Number of studies supporting the IDH and the measures used in tests; Species richness (S), ShannonWiener index (H') and Pielous Evenness (J). b) Number of studies where different measures of diversity differed in their support of the IDH. a) Measure of diversity Supported Tested Species richness (S) 109 123 Shannon index (H') 49 56 Pielous Evenness (J) 16 38 Other measures/indices 27 32 Total number of studies 160 Dissimilarity among b) measures Studies testing >1 diversity measure Studies testing both richness and evenness 2 Total Dissimilar 60 42 (70%) 33 25 (76%) THE IDH PREDICTS; RICHNESS ≠ EVENNESS Fig. 1 Quadratic components for Species richness and Evenness, calculated through regression analyses after z-transformation of data extracted from studies in the meta-analysis that used both measures (see methods), a) plotted together for each study for comparisons within studies and b) plotted separately for general comparisons among measures. Support for the IDH, i.e. a humpshaped relationship, is indicated by high negative values of quadratic components for each measure of diversity. For the examination of dissimilarities in outcomes of tests of the IDH using more than one measure of diversity, we specifically contrasted the number of species (i.e. species richness) to the evenness of species distributions (i.e. Pilou’s Evenness). This was done because (i) these two measures are the key components in all indices of diversity, and (ii) they represent two very different components of the concept of diversity. In order to compare differences in outcomes between species richness and evenness we calculated the quadratic coefficient in regression models describing the relationship between disturbance and richness. The quadratic components were calculated through regression analyses after ztransformation of data extracted from publications using the graph digitizer GrabIt!© (Datatrend Software, Raleigh, North Carolina, USA). The z-transformations were done in order to allow comparisons between component values for richness and evenness. Disturbance levels were normalized between 0 and 1. Data extraction was possible in 28 studies from the articles reviewed (Fig. 1, Appendix S1). The strength and polarity of the quadratic coefficient was then plotted with species richness on the x-axis and evenness on the y-axis. A high negative quadratic coefficient indicates a strong hump-shaped relationship between disturbance and diversity, thus supporting the IDH. was spatially explicit using a cellular automaton model (e.g. Silvertown et al. 1992, Ermentrout and Edelsteinkeshet 1993). The model was set up as a onedimensional universe with 100 cells. At each time step, a proportion of the cells were subjected to a random, local extinction. Thereafter, transition of each cell was achieved either by competition or by recruitment. In the event of competition, the state (i.e. the occupying species), a, of the jth cell at time t+1, was determined by the state of neighboring cells by: (1) a tj+1 = max([a tj−1 a tj a tj +1]) Recruitment occurred with a probability of 0.1 in unoccupied cells. The probability of recruitment of the ith species was modeled as: (2) pi = ci 20 ∑c i i=1 Meta-analysis of diversity measures and support for IDH In the meta-analysis of previous tests of IDH and choice of diversity measure we followed Shea et al. (2004), only included studies reporting support for proceeded from the list of papers provided in Shea et al. (2004) and complemented it by searching in ISI Web of Science for recent articles (2003-2010)citing Connell’s original paper (Connell 1978). Of the over one thousand articles initially reviewed, 143 studies in 132 publication were found which reported support for the IDH (Table 1, Appendix S1). Among these, 60 studies included more than one measure of diversity (Table 1b, Appendix S1), mainly species richness, Shannon’s index H’ (eqn 3; Shannon 1948, Shannon and Weaver 1963), and evenness (eqn 4; Pielou 1966). S (3) ' H max = −∑ (4) H' E= ' H max i =1 RESULTS Model predictions of how disturbance affects species richness and evenness We applied a modeling approach to explore how disturbance affects different measures of biodiversity. Here we report effects on species richness and Pielou’s evenness since these measures extract the two main components of species-abundance distributions. Other compound indices (e.g. Shannon’s H’) yielded intermediate results. The response of species richness and evenness to different rates of disturbance was explored with two different models, one well-established (Kondoh 2001, Worm et al. 2002) spatially implicit (model A) and one spatially explicit (model B). Both models involve one-sided competition, and occupancy of a particular species is a function of colonization ability, competitive strength and local 1 1 ln s s 3 J. ROBIN SVENSSON ET AL. Fig. 2 Species richness (solid line) and Evenness (dashed line) as functions of magnitude of disturbance predicted by a) the spatially implicit model A and b) the spatially explicit model B. Parameters in A are: productivity level=2, extinction rate=0.05, threshold for local extinction=0.01, time steps=500. Data are presented as mean ± SE consistent with the model predictions as species richness yielded stronger hump-shaped relationships between disturbance and diversity, than did evenness. This also corresponds with our finding that two-thirds of the published studies supporting the IDH present different results for different diversity measures. Specifically, when both species richness and evenness were used the relationship between disturbance and diversity showed an even higher degree of dissimilarity. It is surprising that the use of different diversity measures and implications for how to interpret tests of the IDH has not received any previous attention. Mackey and Currie (2001) reviewed tests of IDH and they found a hump-shaped relationship for species richness, the Shannon index H’ and evenness with disturbance in 19, 10 and 3 out of 85 analyzed articles, respectively. They did not, however, discuss possible causes of the different outcomes based on the selected measure of diversity. This potentially confounding factor in tests of the IDH is also neglected in the otherwise excellent review by Shea et al. (2004), where they focus on the mechanisms of coexistence underlying the humpshaped pattern. extinction, which increases with disturbance (see Methods). In both model A and model B richness shows a unimodal hump-shaped pattern, whereas evenness is asymptotically increasing with increasing disturbance levels (Figs. 1a and b). Thus, both mathematical models of the IDH predict qualitatively different effects on species richness and evenness. Meta-analysis of diversity measures and support for IDH Of the over one thousand articles initially reviewed, 143 studies in 132 publications reported support for the IDH and 60 of these studies included more than one measure of diversity (Table 1). In studies including more than one measure of diversity the support for the IDH was often inconsistent between different diversity measures. When outcomes among all measures are compared they show dissimilar support in 70% of the cases (Table 1b). In comparisons specifically contrasting outcomes among tests using both richness and evenness, these two measures differed in their support in over 75 % of the cases. The support for the IDH in 28 previous studies using both species richness and evenness as biodiversity measures is shown in Fig. 2. Negative values of the quadratic component in the statistical model of the effect of disturbance on diversity indicate a hump-shaped (unimodal peak) relationship and thus support for the IDH. Only when diversity is measured as species richness is there a consistent hump-shaped relation supporting IDH (Fig. 2a), and the cumulative distributions in Fig. 2b show that the range of the quadratic coefficients is narrower for the tests using species richness compared to when evenness is used. Why then do different measures of diversity differ in response to disturbance? According to the original formulation of the IDH by Connell (1978), it is the number of species that will increase when disturbance prevents competitive exclusion to occur and allows new species to colonize, up to a certain point when disturbance becomes too severe for species to persist (Eggeling 1947, Osman 1977, Connell 1978). Thus, the prediction that the number of species should show a hump-shaped response to disturbance rests on logic arguments, and the hypothesis is easily tested with species richness as the most evident response variable. It is, however, less logical that this prediction should automatically also apply to various diversity indices, such as Shannon’s H’ and evenness, that also consider how abundance is distributed among species. Species do not need to be more evenly distributed at intermediate disturbance just because the number of species is large. If the predictions are logical for the number of species, but not for species-abundance Discussion We here show that an established model as well as a new, spatially explicit model only support IDH when biodiversity is measured as species richness. Both models predict that evenness instead increases monotonically with increasing levels of disturbance. Our extensive metaanalysis of published empirical tests of the IDH is also 4 THE IDH PREDICTS; RICHNESS ≠ EVENNESS contaminated with mine tailings (Gregory and Bradshaw 1965). However, because of the general lack of discussion of what is predicted about evenness, we recommend that studies choosing evenness as the response variable in tests of the IDH and DEM should present logical arguments, a priori, to why the predicted pattern can be observed in natural communities. distributions (Shea et al. 2004), there is no clear reason for H’ to be a preferable index in disturbance studies, as has previously been suggested (Worm et al. 2002). On a more general level, Stirling and Wilsey (2001) argued that H’ was the best measure of diversity because it considers both the separate effects of richness and evenness and also their interrelations. Although this may be advantageous under certain circumstances, it may be less so in efforts to unravel specific changes in diversity, because the underlying ecological process or mechanism causing changes in H’ can be traced back to effects on either richness or evenness (Hurlbert 1971). Thus, a more interesting and challenging question is why patterns of richness and evenness differ, and if a logical pattern between evenness and disturbance can be conceived within the framework of the IDH. In conclusion, we argue that the logic behind the underlying mechanism of the IDH, the predictions of our two models and the meta-analysis, all suggest that species richness is the most straightforward and appropriate response variable in tests of the IDH and its associated models. Furthermore, since the IDH is also utilized in management of marine and terrestrial national reserves and parks (e.g. Yellowstone National Park, USA), a consensus on appropriate response variables will have benefits reaching beyond the scientific community. The IDH relies on the assumption that one or a few species will dominate the community in the absence of disturbance (Fuentes and Jaksic 1988, Collins and Glenn 1997, Svensson et al. 2007). An uneven distribution of species is therefore to be expected at low levels of disturbance, which is also commonly observed in marine and terrestrial field experiments (Eggeling 1947, Molis et al. 2003, Lenz et al. 2004b, a). According to the compensatory mortality hypothesis(Janzen 1970), mortality from causes unrelated to the competitive interactions falls heaviest on whichever species that ranks highest in competitive ability. The reduction of a highly abundant basal species (i.e. dominant) by disturbance may lead to colonization of new species in the free space (e.g. Connell 1978). Consequently, both the number of species and the evenness of species distributions are likely to initially increase following a disturbance in an already uneven community. In accordance with this, the presented mathematical models (Figs. 2a and b), as well as previous field experiments from both marine and terrestrial systems (Vujnovic 2002, Kimbro and Grosholz 2006), support these patterns. Acknowledgements This study was financially supported by MARICE (an interdisciplinary research platform at the Faculty of Sciences, Göteborg University), by the Swedish Research Council through contract no. 621-2007-5779 to HP and 621-2008-5456 to PRJ, and by Formas through contracts 21.0/2004-0550 to HP and 217-2006-357 to ML. References Amarasekare, P., M. F. Hoopes, N. Mouquet, and M. Holyoak. 2004. 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