A bioturbation classification of European marine infaunal invertebrates

Bioturbation, the biogenic modification of sediments through particle reworking and burrow ventilation, is a key mediator of many important geochemical processes in marine systems. In situ quantification of bioturbation can be achieved in a myriad of ways, requiring expert knowledge, technology, and resources not always available, and not feasible in some settings. Where dedicated research programmes do not exist, a practical alternative is the adoption of a trait-based approach to estimate community bioturbation potential (BPc). This index can be calculated from inventories of species, abundance and biomass data (routinely available for many systems), and a functional classification of organism traits associated with sediment mixing (less available). Presently, however, there is no agreed standard categorization for the reworking mode and mobility of benthic species. Based on information from the literature and expert opinion, we provide a functional classification for 1033 benthic invertebrate species from the northwest European continental shelf, as a tool to enable the standardized calculation of BPc in the region. Future uses of this classification table will increase the comparability and utility of large-scale assessments of ecosystem processes and functioning influenced by bioturbation (e.g., to support legislation). The key strengths, assumptions, and limitations of BPc as a metric are critically reviewed, offering guidelines for its calculation and application.


Introduction
Marine soft-sediment habitats represent some of the most functionally important ecosystems on Earth, being charac-terized by a high biomass and diversity of invertebrate organisms that are fundamental to the mediation of a wealth of goods and services (Lotze et al. 2006;White et al. 2010;Widdicombe and Somerfield 2012). Infaunal inverte-brates exhibit significant influence over benthic sedimentary geochemical environments in soft sediments through bioturbation, that is, the mixing of sediment and particulate materials carried out during foraging, feeding and burrow maintenance activities, and the enhancement of pore water and solute advection during burrow ventilation (Richter 1936;Rhoads 1974;Volkenborn et al. 2010). These processes influence oxygen, pH and redox gradients (Stahl et al. 2006;Pischedda et al. 2008;Queir os et al. 2011), metal cycling (Teal et al. 2009), sediment granulometry (Montserrat et al. 2009), pollutant release (Gilbert et al. 1994), macrofauna diversity (Volkenborn et al. 2007), bacterial activity and composition (Mermillod-Blondin and Rosenberg 2006;Gilbertson et al. 2012), and ultimately carbon (Kristensen 2001) and nitrogen cycling (Bertics et al. 2010). Hence, in light of anticipated changes to marine systems associated with human activity (Halpern et al. 2008;Hoegh-Guldberg and Bruno 2010), large-scale assessments of bioturbation can contribute to a better understanding of how of ecosystem functioning is mediated by biological activity.
Community bioturbation potential (BP c ) is a metric first described by Solan et al. (2004a), which combines abundance and biomass data with information about the life traits of individual species or taxonomic groups. This information describes modes of sediment reworking (R i ) and mobility (M i ) of taxa in a dataset, two traits known to regulate biological sediment mixing, a key component of bioturbation (Solan 2000; and refereces therein; Solan et al. 2004b). BP c is thus not a direct measure of the process of bioturbation. Rather, BP c provides an estimate of the potential of a community to bioturbate. Hence, where macrofauna abundance and biomass data are available, BP c provides a means to estimate the extent to which benthic communities are likely to affect important ecosystem properties that underpin ecosystem functioning. The consequences of environmentally driven changes in biodiversity to BP c , and its relation to ecosystem functioning, have been explored in this way in terrestrial (Bunker et al. 2005) and marine habitats (Solan et al. 2004a,b); at the local (Lohrer et al. 2010;Teal et al. 2013) and regional scales (Queir os et al. 2011;Birchenough et al. 2012;Solan et al. 2012); for different contexts (e.g., habitat structure and hypoxia, Queir os et al. 2011;Van Colen et al. 2012;Villn€ as et al. 2012); and for a variety of ecosystem functions including productivity , nutrient cycling (Solan et al. 2004a), carbon storage (Bunker et al. 2005;Solan et al. 2012), and decomposition (Josefson et al. 2012). By calculating BP c over time, or for different locations or scenarios, changes in the efficiency of the organism-sediment couple can be monitored for compliance in support of management and policy objectives (Painting et al. 2012;Van Hoey et al. 2013). For example, the effects of simulated changes in benthic com-munity structure have previously been used to explore possible changes in ecosystem properties like sediment organic carbon at the North Sea scale, based on empirically derived relationships between BP c and sediment organic carbon (Fig. 1). Similar uses of BP c could invaluably contribute to an increased understanding of the role of ecosystem structure in the sustenance of marine functioning and its resilience to human activities, an urgent need under current European legislation (Marine Strategy Framework Directive, 2008/56/EC).
A significant obstacle in the widespread application of BP c , however, is the need for a standard classification scheme that is supported by the benthic research community. As a first step in fulfilling this research gap, we present the findings of the Study Group on Climate Related Benthic Processes in the North Sea, an expert group appointed by the International Council for the Exploration of the Sea (ICES SGCBNS). We present the conclusions of a series of dedicated workshops tasked with deriving a functional classification of northwest European marine invertebrate species to facilitate the calculation of BP c in different regions of the North Atlantic.

Methods
The classification of marine invertebrate infauna into bioturbation groups was carried out using 18 datasets compiled from northwest European waters (n = 1033 species). Following Swift (1993) and Solan et al. (2004a), each taxon (1) was scored on categorical scales that reflect increasing mobility (M i ) from 1 (living in a fixed tube) to 4 (free three dimensional movement via burrow system), and increasing sediment reworking (R i ) from 1 (epifauna that bioturbate at the sediment-water interface) to 5 (regenerators that excavate holes, transferring sediment at depth to the surface).
B i and A i are the biomass and abundance of species/taxon i in a sample. Trait scores were derived from an extensive review of published material and expert knowledge (consensus of 12 authors), and details of the scoring system are provided below. Species for which no published information was available were scored based on descriptions of species behavior and information on closely related species at the nearest taxonomic level. As BP c captures information about sediment particle reworking, pelagic species and those living on hard substrates were not included. Sediment reworking functional types were also defined (Ft i ), according to Franc ßois et al. (1997), Solan (2000), and G erino et al. (2003). Taxonomic information and Aphia ID (a unique species database identifier) were extracted from the World Register of Marine Species (2012). Results Table 1 provides the classifications for mobility (M i ) and sediment particle reworking (R i ) assigned to the 1033 marine invertebrate species (and other taxa) from northwest European waters, and the associated sediment reworking functional types (Ft i ). Please refer to the table for details of the scoring criteria.

Discussion
As with any functional classification that on which BP c is calculated relies on three main assumptions. Understanding these assumptions, and the need to correct for them where information is available, is key steps in the adequate use of BP c as a metric: 1 If body size is constant, the BP c of a species/taxon (BP i ) is transferable across space and time. BP c accounts for two "fixed" traits (R i and M i ) that are assumed to be directly related to life-history traits and activity levels of each species, that are not altered by context or spatiotemporal variation. Where information to the contrary is available about the alteration of species behavior in response to external stimuli, context-specific adjustments to reworking and mobility trait scores should be made accordingly: for example, thermal stress (Ouellette et al. 2004;Przeslawski et al. 2009); habitat structure (Godbold et al. 2011); ocean acidification (Godbold and Solan 2013); or presence of a predator (Maire et al. 2010). For instance, sediment type has been observed to be influential when determining the classification of a particular species into one of two specific functional groups (Needham et al. 2011), but this has not been documented for the vast majority of bioturbators. Incorporation of this type of information could be achieved using more sophisticated routines, such as fuzzy coding, to capture the influence of intraspecific variability in reworking and mobility traits (Maire et al. 2007;Bremner 2008;Godbold et al. 2011) across known sources of variation (habitat, season, food availability, etc.). The paucity of such information present for the majority of marine species (Tyler et al. 2012) is a source of concern and will be needed to project potential changes in BP c under future policy or environmental scenarios. Typical body size is a "flexible" trait in the metric, which will vary in response to environmental variation, seasonality, stress, and disturbance (Queir os et al. 2006;Macdonald et al. 2012). BP c captures this information through changes in the biomass/abundance ratio on which typical body size is calculated. 2 An organism's reworking (R i ) and mobility (M i ) modes remain the same across the life span of each individual. Percentage of sediment organic carbon (circles, diameter scaled to %) at each of 109 sites sampled during the North sea benthos Survey conducted by the Benthos Ecology Working Group of the International Council for the Exploration of the Sea in 1986 (left column, "100%"), and following the implementation of simulated trait based extinction scenarios (right column, "50%"). By combining measurements of ecosystem functions with information on relevant species traits (abundance, biomass, functional group and behaviour), empirically derived relationships between specific ecosystem functions and BP c can be derived. In this case, the relationship between BP c and sediment % of organic carbon. Species extinction scenarios can be simulated and the consequential changes in ecosystem functioning recalculated based on changes in community composition and/or structure following implementation of each scenario. In this example, the predicted levels of sediment organic carbon content are presented for a 50% reduction in species richness (right column, "50%") following sequential local expiration of species ordered by the most abundant species within a site (top row), those with the largest biomass (second row from top), or by the most abundant species across the region (bottom row). The consequences for ecosystem functioning (here, sediment organic carbon content) following these ordered extinction scenarios contrast to a scenario where species are extirpated in a random order (third row from top). Implementing various trait-based extinction scenarios in this way provides insights on possible outcomes following, for example, changes in management or as a result of anthropogenic forcing. Modified from Solan et al. (2012).                    Thus far, variation in burrowing behavior across life stages has been poorly documented in the literature. However, in some species, juveniles and adults are known to exhibit different burial behavior, which can also be modified during reproductive stages (Aguzzi and Sard a 2007;Schwalb and Pusch 2009). If such changes in behavior are known to occur, different trait scores should be attributed as appropriate to different genders or life stages. 3 Where no species level information exists, taxa are assumed to have a similar bioturbation mode to others, which are closely related taxonomically. The paucity of information on many bioturbators (Teal et al. 2008) necessitates matching some species with the closest possible species or taxonomic group (e.g., genus or family). Regardless of whether taxonomic relatedness is a good indicator of the ecological characteristics of a species (Bevilacqua et al. 2012), the table presented here does not account for changes in taxonomic classification over time. Such changes in taxonomy could alter an organism's taxonomic relatedness to other taxa and therefore its assumed bioturbation classification. For example, Alitta virens (Sars 1835) and Hediste diversicolor (M€ uller 1776) may have been classified as being functionally similar, as both these species were formerly classified under the genus Nereis (Linnaeus 1758). Recent changes to their taxonomic classification now better reflect fundamental differences in bioturbation modes (i.e., gallery diffusor and conveyor, respectively, Franc ßois et al. 2002). Nevertheless, in the absence of specific information, we consider it likely that genetically and physically similar taxa are likely to be functionally similar. As BP c is a biomass-weighted sum of traits from many species, we consider it unlikely that small changes to trait assignments of individual species would greatly influence large-scale assessments. The current structure of the table reflects the taxonomic classification of the species at the time of analysis and will need updating as taxonomic inventories are refined. Accepting the limitations imposed by the assumptions underpinning BP c , the classification list we have assembled will facilitate the calculation of BP c across most temperate coast and shelf benthic environments in the North Atlantic. This aspects makes a strong case for a wider implementation of BP c as a standardized indicator: the ability to build on existing data (abundance and biomass) to fill gaps about bioturbation patterns where direct assessments are not, or cannot, been routinely carried out. Further efforts will need to take place for other regions of the world or particular circumstances. There is also tremendous potential for application to historical datasets, to estimate bioturbation rates in the past, providing insight into how this process has helped to shape sedimentary ecosystems over time . Finally, the Marine Strategy Framework Directive (2008/56/EC) now requires an integrated understanding and management of regional scale patterns of marine ecosystem functioning, based on the use of inexpensive, rapid indicators. Few functional indicators currently exist for European waters, and initial tests of the suitability and applicability of BP c suggest that it holds promise as a tool for informing management and policy (Van Hoey et al. 2010;Birchenough et al. 2012).