Current use of and future needs for soil invertebrate functional traits in community ecology

Abstract

Soil invertebrates are assumed to play a major role in ecosystem dynamics, since they are involved in soil functioning. Functional traits represent one of the main opportunities to bring new insights into the understanding of soil invertebrate responses to environmental changes. They are properties of individuals which govern their responses to their environment. As no clear conceptual overview of soil invertebrate trait definitions is available, we first stress that previously-described concepts of trait are applicable to soil invertebrate ecology after minor modification, as for instance the inclusion of behavioural traits. A decade of literature on the use of traits for assessing the effects of the environment on soil invertebrates is then reviewed. Trait-based approaches may improve the understanding of soil invertebrate responses to environmental changes as they help to establish relationships between environmental changes and soil invertebrates. Very many of the articles are dedicated to the effect of one kind of stress at limited spatial scales. Underlying mechanisms of assembly rules were sometimes assessed. The patterns described seemed to be similar to those described for other research fields (e.g. plants). The literature suggests that trait-based approaches have not been reliable over eco-regions. Nevertheless, current work gives some insights into which traits might be more useful than others to respond to a particular kind of environmental change. This paper also highlights methodological advantages and drawbacks. First, trait-based approaches provide complementary information to taxonomic ones. However the literature does not allow us to differentiate between trait-based approaches and the use of a priori functional groups. It also reveals methodological shortcomings. For instance, the ambiguity of the trait names can impede data gathering, or the use of traits at a species level, which can hinder scientific interpretation as intra-specific variability is not taken into account and may lead to some biases. To overcome these shortcomings, the last part aims at proposing some solutions and prospects. It concerns notably the development of a trait database and a thesaurus to improve data management.

Zusammenfassung

Man nimmt an, dass wirbellose Bodentiere eine wichtige Rolle bei der Ökosystemdynamik spielen, da sie am Funktionieren der Böden beteiligt sind. Funktionelle Merkmale bilden eine der wichtigsten Möglichkeiten für ein neues Verständnis der Reaktion von Bodenwirbellosen auf Umweltänderungen. Es handelt sich um Eigenschaften von Individuen, die deren Reaktion auf die Umwelt bestimmen. Da es keinen klaren konzeptionellen Überblick über die Merkmalsdefinitionen für Bodenwirbellose gibt, betonen wir zunächst, dass existierende Konzepte nach geringen Modifikationen auf die Ökologie von Bodenwirbellosen anwendbar sind, wie z.B. das Einbeziehen von Verhaltensmerkmalen. Anschließend betrachten wir ein Jahrzehnt der Literatur zum Gebrauch von Merkmalen bei der Abschätzung der Effekte der Umwelt auf Bodenwirbellose. Merkmalsbasierte Ansätze können unser Verständnis der Reaktionen von Bodenwirbellosen auf Umweltänderungen verbessern, da sie helfen, Beziehungen zwischen Umweltänderungen und Bodenwirbellosen zu etablieren. Sehr viele der Artikel widmen sich dem Effekt eines Stressfaktors auf begrenzten räumlichen Skalen. Die zugrundeliegenden Mechanismen von Vergemeinschaftungsregeln wurden manchmal bestimmt. Die beschriebenen Muster scheinen denen von anderen Forschungsgebieten (z.B. Pflanzen) ähnlich zu sein. Die Literatur legt nahe, dass merkmalsbasierte Ansätze über Ökoregionen hinweg nicht zuverlässig sind. Nichtsdestotrotz lassen aktuelle Arbeiten erkennen, welche Merkmale nützlicher als andere sein könnten, um auf spezielle Umweltveränderungen zu reagieren. Diese Arbeit stellt auch methodische Vor- und Nachteile heraus. Zuerst liefern merkmalsbasierte Ansätze Informationen, die taxonomische ergänzen. Indessen erlaubt uns die Literatur nicht, zwischen merkmalsbasierten Ansätzen und dem Gebrauch von a-priori definierten funktionellen Gruppen zu unterscheiden. Sie zeigt auch methodische Unzulänglichkeiten. So kann z.B. die Mehrdeutigkeit von Merkmalsbezeichungen das Sammeln von Daten behindern, oder der Gebrauch von Merkmalen auf der Artebene, der die wissenschaftliche Interpretation erschweren kann, da die intraspezifische Variabilität nicht berücksichtigt wird und zu gewissen Verzerrungen führen kann. Um diese Unzulänglichkeiten zu überwinden, hat der letzte Teil zum Ziel, einige Lösungen und Ausblicke vorzuschlagen. Dies betrifft namentlich die Entwicklung einer Merkmalsdatenbank und eines Thesaurus’ um die Datenverwaltung zu verbessern.

Introduction

The current biodiversity estimation of soil fauna assumes that soil is the third biotic frontier after tropical forest canopies and ocean abysses (André et al., 1994, Giller, 1996, Swift et al., 1979, Wolters, 2001). The soil fauna encompasses both the obligate and facultative inhabitants of soil and soil annexes (Wolters 2001). Soil annexes are simple structures which diversify the soil surface (e.g. tree stumps) (Gobat, Aragno, & Matthey 1998). The soil includes a variety of animals from almost all major taxa that compose the terrestrial animal communities and may represent as one quarter of all currently described biodiversity (Decaëns, Jimenez, Gioia, Measey, & Lavelle 2006). Soil invertebrates are assumed to play a major role in ecosystem dynamics, since they are involved in soil functioning (e.g. carbon transformation and sequestration, regulation of microbial activity or community structure, nutrient turnover, aggregation). Consequently, soil invertebrates contribute to the provision of many ecosystem services such as nutrient cycling or soil structure maintenance (Barrios, 2007, Kibblewhite et al., 2008, Lavelle et al., 2006).

Studying soil invertebrate responses to environmental changes is of great interest. In various research fields (e.g. plant ecology), functional components of communities have revealed valuable insights into the understanding of organisms’ responses to the environment (Garnier and Navas, 2012, McGill et al., 2006). Originally, taxa were grouped into a priori functional groups based on certain “characteristics” which they shared. The classification into such functional groups is based on subjective expert judgement. For instance, several plant functional types existed, based on their life form or growth form (Lavorel, McIntyre, Landsberg, & Forbes 1997). Conclusions were drawn from these a priori functional groups’ richness (Villéger, Mason, & Mouillot 2008). However these approaches led to several limitations (Villéger et al. 2008) such as (i) a loss of information by imposing a discrete structure on functional differences between taxa, which are usually continuous (Fonseca and Ganade, 2001, Gitay and Noble, 1997), (ii) a non-robust way of obtaining results depending on the choice of the functional group types in the analysis (Wright et al. 2006) and sometimes (iii) a failure to take account of abundance (Díaz & Cabido 2001). As an alternative to the taxonomic and a priori functional group approaches, trait-based approaches have been developed (Lavorel and Garnier, 2002, McGill et al., 2006). Traits can be divided into response and effect traits. An effect trait is an individual property which affects an upper level of organization (e.g. ecosystem processes). Response traits, also called functional traits, are properties of individuals which govern their responses to their environment (Statzner et al., 2001, Violle et al., 2007). In the following, traits will mean response traits. Unlike a priori functional groups, trait-based approaches are based on objective relations between individual properties (= traits) and the environment. In other research fields, notably for plants, trait-based approaches have brought several new insights to the understanding of organisms’ responses to environmental changes, by improving predictability and reducing context dependence (Garnier and Navas, 2012, Webb et al., 2010). Prediction involves that a relationship must be found between soil invertebrates and environmental changes through their traits. It has been demonstrated that community assembly mechanisms are governed by rules. The literature tends to support the existence of environmental filters which filter a sub-set of individuals of the regional pool to form local communities (Keddy, 1992, McGill et al., 2006). Furthermore, environmental filters can be categorized according to the scale on which they work. From larger scales to smaller ones, filters are (i) dispersal filters which select individuals according to their dispersal capacity, (ii) abiotic filters which select individuals according to their capacity to live under certain abiotic conditions and (iii) biotic filters which represent the selection resulting from the interactions between individuals (Belyea and Lancaster, 1999, Garnier and Navas, 2012). Reducing context dependency implies that trait-based approaches have to be: (i) generic over eco-regions and (ii) reliable whatever kind of environmental change is considered. Enough trait-based approach studies have been made on plants to associate one or more traits with one or more environmental changes in any eco-region (Garnier & Navas 2012). For instance, “leaf area” responds gradually to complex environmental change such as climate change over eco-regions (Moles et al., 2009, Thuiller et al., 2004).

To our knowledge, attempts to relate terrestrial invertebrate responses in terms of their “characteristics” to environmental stress began at the end of the ninetieth century (Statzner et al. 2001). In 1880, Semper (in Statzner et al. 2001) assessed the temperature-induced switch from parthenogenetic to sexual reproduction in aphids. During the following years, authors were convinced that environmental stress and “characteristics” of terrestrial insects were linked (Buxton, 1923, Hesse, 1924, Pearse, 1926, Shelford, 1913 – all in Statzner et al. 2001). For instance, Buxton (1923 – in Statzner et al. 2001) related “characteristics” of terrestrial insects such as the presence of wings or the tolerance of larvae to a lack of food and water to harsh environmental conditions of deserts (e.g. drought, torrential rain, whirlwinds).

Despite this early interest, no clear conceptual and methodological overview has been made for such “characteristics” of soil invertebrates, which are now called traits. Originally, as for plants, most previous studies assessed soil invertebrate responses to their environment using taxonomic structure and/or composition of communities. As soil invertebrate taxonomic diversity is huge, authors tried to simplify it by grouping together individuals by shared properties. The grouping also dealt with the lack of knowledge of taxonomy. For instance, eco-morphological groups, such as epigeic, anecic and endogeic groups of earthworms (Bouché 1972), epiedaphic, hemiedaphic and euedaphic groups of springtails (Gisin 1943) or terrestrial isopods (Schmallfuss 1984) and functional guilds such as the distinction between ecosystem engineers, litter transformers and micropredators (Lavelle & Spain 2001) were used. For instance, eco-morphological groups bring together individuals based on subjective expert judgments of some of the ecological or biological “characteristics” they share. For instance, epigeic earthworms are pigmented and live near the soil surface, whereas endogeic earthworms are unpigmented and live deep in the soil. As for plants, all of these groupings have been used as a priori functional groups and should present the same disadvantages (see above). Experience in other research fields led us to think that using functional trait-based approaches for soil invertebrates represents one of the main opportunities to bring new insights into the understanding of soil invertebrate responses to the environment.

To our knowledge, no attempt has been made to clearly define functional trait concepts for soil invertebrates. The concept already existed but was used in other research fields. As a consequence, we first determine whether the actual definitions around the notion of traits are applicable to soil invertebrates. Second, to summarize the current advances in the understanding of soil invertebrate responses to the environment through their traits, a one-decade literature review was made. It also aimed to focus on current methodological advantages and drawbacks of soil invertebrate trait-based approaches. The last part envisages solutions and prospects for overcoming current conceptual and methodological drawbacks. It notably deals with the development of eco-informatics tools.