- Email: [email protected]
Human threats to sandy beaches: A meta-analysis of ghost crabs illustrates global anthropogenic impacts.
Accepted Manuscript Human threats to sandy beaches: A meta-analysis of ghost crabs illustrates global anthropogenic impacts. Thomas A. Schlacher, Serena Lucrezi, Rod M. Connolly, Charles H. Peterson, Ben L. Gilby, Brooke Maslo, Andrew D. Olds, Simon J. Walker, Javier X. Leon, Chantal M. Huijbers, Michael A. Weston, Alexander Turra, Glenn A. Hyndes, Rebecca A. Holt, David S. Schoeman PII:
S0272-7714(15)30147-5
DOI:
10.1016/j.ecss.2015.11.025
Reference:
YECSS 4964
To appear in:
Estuarine, Coastal and Shelf Science
Received Date: 23 October 2015 Revised Date:
20 November 2015
Accepted Date: 28 November 2015
Please cite this article as: Schlacher, T.A., Lucrezi, S., Connolly, R.M., Peterson, C.H., Gilby, B.L., Maslo, B., Olds, A.D., Walker, S.J., Leon, J.X., Huijbers, C.M., Weston, M.A., Turra, A., Hyndes, G.A., Holt, R.A., Schoeman, D.S., Human threats to sandy beaches: A meta-analysis of ghost crabs illustrates global anthropogenic impacts., Estuarine, Coastal and Shelf Science (2015), doi: 10.1016/ j.ecss.2015.11.025. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
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* SCHLACHER, Thomas A. School of Science and Engineering, The University of the Sunshine Coast, Q-4558 Maroochydore, Australia; [email protected]
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LUCREZI, Serena TREES—Tourism Research in Economic Environs and Society, North-West University, Potchefstroom, South Africa; [email protected]
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CONNOLLY, Rod M. Australian Rivers Institute - Coast & Estuaries, and School of Environment, Gold Coast Campus, Griffith University, Queensland, 4222, Australia; [email protected]
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PETERSON, Charles H. Institute of Marine Sciences, University of North Carolina, Chapel Hill, Morehead City, NC 28557, USA; [email protected]
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GILBY, Ben L. School of Science and Engineering, The University of the Sunshine Coast, Q-4558 Maroochydore, Australia; [email protected]
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MASLO, Brooke Department of Ecology, Evolution and Natural Resources Rutgers, The State University of New Jersey; [email protected]
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OLDS, Andrew D. School of Science and Engineering, The University of the Sunshine Coast, Q-4558 Maroochydore, Australia; [email protected]
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WALKER Simon J. School of Science and Engineering, The University of the Sunshine Coast, Q-4558 Maroochydore, Australia; [email protected]
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LEON, Javier X. School of Science and Engineering, The University of the Sunshine Coast, Q-4558 Maroochydore, Australia; [email protected]
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HUIJBERS, Chantal M. School of Science and Engineering, The University of the Sunshine Coast, Q-4558 Maroochydore, Australia; [email protected]
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WESTON, Michael A. Centre for Integrative Ecology, School of Life and Environmental Sciences, Deakin University, Burwood, VIC 3125, Australia; [email protected]
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TURRA, Alexander Departamento de Oceanografia Biológica, Instituto Oceanográfico, Universidade de São Paulo, Praça do Oceanográfico, 191, CEP 05508-120 São Paulo, SP, Brasil; [email protected]
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HYNDES, Glenn A. Centre for Marine Ecosystems Research, Edith Cowan University, WA, Australia; [email protected]
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HOLT, Rebecca A. Australian Rivers Institute - Coast & Estuaries, and School of Environment, Gold Coast Campus, Griffith University, Queensland, 4222, Australia; [email protected]
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SCHOEMAN, David S. School of Science and Engineering, The University of the Sunshine Coast, Q-4558 Maroochydore, Australia; [email protected]
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* corresponding author: [email protected]
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Human threats to sandy beaches: A meta-analysis of ghost crabs illustrates global anthropogenic impacts.
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Abstract
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1.
Human Beach Impacts
Beach and coastal dune systems are increasingly subjected to a broad range of anthropogenic pressures that on many shorelines require significant conservation and mitigation
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interventions. But these interventions require reliable data on the severity and frequency of
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adverse ecological impacts. Such evidence is often obtained by measuring the response of
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‘indicator species’.
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Ghost crabs are the largest invertebrates inhabiting tropical and sub-tropical sandy shores and are frequently used to assess human impacts on ocean beaches. Here we present the first
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global meta-analysis of these impacts, and analyse the design properties and metrics of
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studies using ghost-crabs in their assessment. This was complemented by a gap analysis to
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identify thematic areas of anthropogenic pressures on sandy beach ecosystems that are
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under-represented in the published literature. 3.
Our meta-analysis demonstrates a broad geographic reach, encompassing studies on shores
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of the Pacific, Indian, and Atlantic Oceans, as well as the South China Sea. It also reveals what
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are, arguably, two major limitations: i) the near-universal use of proxies (i.e. burrow counts to
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estimate abundance) at the cost of directly measuring biological traits and bio-markers in the
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organism itself; and ii) descriptive or correlative study designs that rarely extend beyond a
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simple ‘compare and contrast approach’, and hence fail to identify the mechanistic cause(s) of
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observed contrasts.
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Evidence for a historically narrow range of assessed pressures (i.e., chiefly urbanisation, vehicles, beach nourishment, and recreation) is juxtaposed with rich opportunities for the
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broader integration of ghost crabs as a model taxon in studies of disturbance and impact
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assessments on ocean beaches. Tangible advances will most likely occur where ghost crabs
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provide foci for experiments that test specific hypotheses associated with effects of chemical,
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light and acoustic pollution, as well as the consequences of climate change (e.g. species range
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shifts).
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Key-words: meta-analysis; ecological indicator species; sandy shores; coastal dunes; impact
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assessments; Hoplocypode; Ocypode.
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1. Introduction
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“I'll try you on the shore”
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William Shakespeare: Antony and Cleopatra (1606) Accelerating environmental impacts on ocean beaches and coastal dunes call for effective
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environmental planning and biological conservation. These interventions should meet two cardinal
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criteria: 1.) environmental values and conservation goals must be clearly identified for broad and
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inclusive segments of the population (Harris et al., 2014; Vivian and Schlacher, 2015); and 2.)
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management decisions must be based on impact assessments that produce defensible and
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biologically relevant information (Harris et al., 2015).
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A sizeable part of this information comes from documenting the response of organisms (at various
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levels of ecological organisation ranging from individuals to ecosystems) to human activities or
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anthropogenic habitat change (Defeo et al., 2009; Schlacher et al., 2007a). On ocean shores, a broad
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range of animals (e.g. benthic invertebrates, birds, marine turtles) has been used to detect biological
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effects attributed to an equally diverse spectrum of anthropogenic pressures, ranging from vehicle
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impacts to urbanisation (e.g. Huijbers et al., 2015b; Marshall et al., 2014; Reyes-Martínez et al., 2015;
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Walker and Schlacher 2011).
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Ghost crabs (Genera Ocypode and Hoplocypode) are perhaps the most widely-studied invertebrate
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indicator species on ocean-beaches (e.g. Barros, 2001). Ghost crabs are attractive as ecological indicators for a number of reasons: i) they are widespread in the subtropics and tropics; ii) they occur
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on both the non-vegetated beaches and in the dunes backing beaches; iii) they are relatively large,
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often locally abundant, arguably charismatic, and require no specialised tools to sample; iv) their
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taxonomy is well known and identification not overly difficult; and v) they construct semi-permanent
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burrows with clearly visible openings at the beach surface (Lucrezi and Schlacher, 2014; Schoeman et
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al., 2015). It is the fossorial habits of ghost crabs, in particular, that has led to their widespread
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adoption as ecological indicators, chiefly because estimates of abundance and body size can be made
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from counts and measurements of burrow sizes without the need to physically collect the organisms
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(Barros, 2001).
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Given the extensive use of ghost crabs as ecological indicators on ocean beaches, a formal review and
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meta-analysis of this practice is warranted. To this end, here we synthesise the literature and address
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five broad questions:
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1) What are the types of human pressures acting on beach-dune systems that have been assessed with
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ghost crabs?
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2.) What is the magnitude of reported ecological effect sizes for different stressors?
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3.) Which metrics (response variables) have been used?
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4.) What are the gaps in terms of human pressures currently not adequately assessed using ghost
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crabs?
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5.) What opportunities exist to advance the use of ghost crabs as ecological indicators on ocean
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beaches?
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2. Methods
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Studies that examined the response of ghost crabs to anthropogenic activities (sensu lato) were
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obtained by first searching the Web of Science, Scopus, and Google Scholar using “ghost crabs” OR
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“Ocypode OR Hoplocypode ” as key words. From this pool we identified studies reporting on human
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impact assessments by reading the original documents. Sources from literature searches were
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supplemented by examining the cited reference lists of publications in hand; this yielded several
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additional reports from government agencies (e.g. U.S. Fish & Wildlife Service, Natal Parks Board). No
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filter was applied with respect to the types of impacts. Nevertheless, all studies were required to meet
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two minimum criteria for inclusion in the meta-analysis: peer-review or an equivalent quality control
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was likely to have been completed, and quantitative data on changes / differences of at least one
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response variable could be extracted from a publication (e.g. contrasts in burrow counts between
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beach sections with and without vehicle traffic). In all cases, we classified the intensity of human use or
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habitat modification by following the original descriptions provided by the authors of each study,
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usually representing a ‘high impact/use treatment’ condition that was compared with a ‘low
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use/reference/control’ condition. In most cases it was not possible to quantify or rank the intensity or
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level of pressure from the original descriptions; hence, all analyses here are performed using a binary
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classification of ‘impact’ vs. ‘reference’, irrespective of differences in impact intensity that may have
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existed among studies.
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We quantified the magnitude of effects on measured ghost crab biological metrics by using the log-
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response ratio, lnR, which is a common statistic of ecological effect sizes in meta-analyses:
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lnR = ln(mean impact / mean control)(Borenstein et al., 2009). ‘Impact’ refers to sites or beaches that were
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categorised by authors as being evidently more influenced by a particular human stressor of interest
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and hence usually represent values from ‘impact’ groups or ‘treatments’. Conversely, ‘control’ values
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usually represent localities where the stressor of interest was judged (by the original study authors) to
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be substantially less influential or absent and hence represent ‘reference conditions’ in the context of
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individual studies. Half of the studies in our database did not report sufficient details on samples sizes,
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variances, statistical tests used, or P-values; in other papers these statistics could not be reliably
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extracted or inferred from graphs or tables. These omissions precluded the calculation of standardised
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effect-size statistics such as Cohen’s d and Hedges’ g (Harrison, 2011) for the majority of studies. For
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these reasons, we limit our analysis to unweighted one-sample t-tests of the hypothesis that the mean
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log-response ratio is 0 (i.e., that there is, on average, no effect; raw response ratio = 1).
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The term ‘indicator species’ has multiple meanings in ecology and environmental science, with little or
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no consistency of usage amongst authors. Broadly, five main types of usage can be identified to: 1.)
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measure the biological responses to anthropogenic stressors, pollutants, human activities,
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management actions, or restoration efforts (i.e. ‘indicator species’ are used as biological monitors that
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are thought to react in predictable ways to changes in the environment) (Carignan and Villard, 2002; Page | 4
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Diekmann and Dupré, 1997; Jonsell and Nordlander, 2002; Krmpotić et al., 2015; Siddig et al., 2016); 2.)
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characterize assemblages or habitats (i.e. ‘indicator species’ are those that are viewed as 'typical'
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species, showing consistent fidelity to a set of biological or environmental attributes) (Antonelli et al.,
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2015; De Cáceres et al., 2010; Dufrêne and Legendre, 1997; Hogle et al., 2015; Hwang et al., 2015;
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Peterken, 1974; Ricotta et al., 2015; Sarrazin et al., 2015); 3.) reflect more than one process, condition,
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or biological attribute that may or may not be linked to human interventions (i.e. ‘indicator species’
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serve as multiple proxies, the specific meaning being often dependent on the study context)
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(Lindenmayer, 1999; Niemi et al., 1997; Regehr and Montevecchi, 1997); 4.) act as surrogates for
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species that are difficult to detect or sample or to reflect specific environmental conditions (i.e.
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‘indicator species’ are functionally closely associated with other species or environmental attributes
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required by those species) (Pérez-García et al., 2015; Schaefer and Hocking, 2015; Turner and McGraw,
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2015; Weaver, 1995); and 5.) serve as surrogates for biodiversity at the assemblage or ecosystem level
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(i.e. ‘indicator species’ are surrogates for biological diversity at higher levels of ecological organisation)
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(Morelli, 2015). Historically, indicator species were often used in the context of biodiversity surrogates
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or being other proxies, whereas modern studies predominantly use indicator species to describe
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habitats or assemblages, or to assess biological effects of environmental change, generally linked to
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human stressors (Siddig et al., 2016). In this paper the term ‘indicator species’, as applied to ghost
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crabs, represents usage to assess anthropogenic threats and environmental change.
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3. Results
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3.1 Coverage, Variables, Replication, Scale
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In terms of geographic provenance, just over half (53%) of studies are from Atlantic beaches, nearly a
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third from the Pacific (32%), with the remainder coming from the Indian Ocean (13%), and the South
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China Sea (3%; Table 1, Fig. 1). Papers from Australia (34%) and the USA (32%) make up the bulk of
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publications examining human impacts on ghost crabs, complemented by significant contributions
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from Brazil (13%) and South Africa (8%; Table 1). All studies reviewed here were conducted in the
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tropics (74%) and subtropics (26%), with the average latitude being 26.1º (s = 9.35º; Fig. 1). With
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respect to usage as an ecological indicator, Ocypode quadrata was most often studied (18 studies),
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followed by O. cordimanus (13) and O. ceratophthalma (10); other species, including Hoplocypode
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occidentalis, the single species in this genus, are rarely used. Low coverage of species in the literature
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should, however, not be interpreted as inferring that certain under-sampled species perform more
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poorly as ecological indicators.
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The number of response variables measured per study is limited. Most authors measured only one
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(47%) or two (29%) variables, usually abundance and diameter of burrow openings (Table 1). We also
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found a surprisingly narrow range of the type of variables measured by authors and a dominance of
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indirect proxies. Indeed, only four of the 38 studies reviewed by us have measured the response of
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ghost crabs to human disturbance directly, rather than extrapolating from proxies related to burrow
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metrics. Schlacher and Lucrezi (2010a) tracked crabs to test whether disturbance by vehicles affected
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home-range size and habitat use. Body condition of individuals was used to predict the availability
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and quality of food resources, as this metric indicates altered trophic conditions for ghost crabs, as
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occurs where food scraps are discarded by campers in coastal dunes abutting beaches (Schlacher et
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al., 2011a). Wolcott and Wolcott (1984) and Schlacher et al. (2007c) used an experimental approach to
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measure the rate at which vehicles driven on beaches injure and crush individuals, both whilst crabs
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were inside burrows at various depths and whilst they were active on the beach surface at night.
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All study designs contained some element of spatial replication. On average, five sites were sampled
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(se = 0.67), ranging up to a maximum of 21 sites (Schlacher et al., 2011a). However, half of the studies
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sampled fewer than four sites, with ten studies (26 %) having sampled two sites only (mostly a classic
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unreplicated 'compare and contrast' approach), and eight studies (21 %) having examined three sites.
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The mean spatial extent over which sites were dispersed was relatively large at 39 km (se = 11). This
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statistic is, however, attributable to three studies that had sites extending over 200 km or farther: i)
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Barros (2001) assessed the effects of seawalls on urban beaches in south-eastern Australia, measuring
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burrow densities on three beaches dispersed along ca. 310 km of coast; ii) Ocaña et al. (2012)
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estimated the consequences of coastal development for ghost crabs at eight beaches along 200 km of
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the NE coast of Cuba; iii) Fisher and Tevesz (1979) worked over a similar spatial range, surveying the
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response of O. quadrata to urbanisation and trampling at 13 sites ranging over 200 km from Cape
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Henry, Virginia to Cape Hatteras, North Carolina. Notwithstanding a few relatively large-scale designs,
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half of the studies were completed over less than 15 km. Small-scale (<10 km) studies are not
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uncommon in the ghost crab literature: 7 papers (18 %) sampled sites covering less than 1 km and
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15 papers (39 %) surveyed sites over less than 10 km.
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Ten studies (26 %) were ‘spot measurements’, lacking temporal replication in their design. In studies
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that made repeated estimates of ghost crab responses, the average number of temporal replicates
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was 8.89 (se = 1.28), ranging up to 27 temporal replicates (Lucrezi et al., 2010). Studies that were
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particularly well replicated in time include: Moss and McPhee (2006) assessed vehicle effects on ghost
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crabs in Eastern Australia (n = 20); Peterson et al. (2014) quantified the consequences of beach
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nourishment in North Carolina (n = 20); and Irlandi and Arnold (2008) report on nourishment effects
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in Florida (n = 22). The average duration of temporally replicated impact studies was 180 days
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(se = 53), and only four studies spanned less than a week. By contrast, the duration of four studies was
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close to a year or longer: Robertson and Kruger (1995) who gauged the effects of artisanal fisheries on
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ghost crabs in South Africa (330 days), and Christoffers’ (1986) work on the effects of recreational
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activities at Assateague Island (488 days). The two papers with the longest duration both dealt with
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nourishment impacts: Irlandi and Arnold (2008) spanning 640 days, and Peterson et al. (2014) lasting
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1370 days.
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3.2 Effect Sizes
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The reported responses of ghost crabs to human activities and associated habitat changes on beaches
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generally show consistently negative impacts of human pressures on the number of burrow openings
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(a proxy for abundance), but highly variable or non-significant effects on burrow diameter (a proxy for
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body size; Table 2; Fig. 2).
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Response ratios of abundance denote a significant (t = 6.32, df = 36, P < 0.001) mean density
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decrease (lnR = -1.35 ± 0.21se),at impacted locations for all stressors combined (Table 2; Fig. 2); mean
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response ratios significantly smaller than unity are evident for the effects of vehicles (lnR = -
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1.42 ± 0.45se, P <0.01), nourishment (R = -1.27 ± 0.36se, P = 0.038), and urbanisation (R = -
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1.52 ± 0.30, P <0.001). Fewer individuals associated with more intense human use (e.g. more vehicles
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or trampling) or greater habitat conversions (e.g. seawalls, development, nourishment) were reported
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in 35 of the 37 papers that measured abundance (via burrow counts). Of the 26 studies (70%) that
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undertook some form of statistical test, or adequately described the results of such tests between
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control and impact conditions, 23 (88%) report significant differences in burrow counts between
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'impact' and ‘control’ sites, 21 studies (81%) reported fewer burrows, whilst only two studies (8%)
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reported more burrows associated with putative human pressures.
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In contrast to the largely significant and negative effects on crab abundance (assessed by proxy using
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burrow counts), responses of the diameter of burrow openings (a proxy for crab size) are inconsistent,
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both in terms of the direction and magnitude of responses to tested pressures (Table 2, Fig. 2).
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Although sample size was limited, the mean response ratio (lnR = -0.15 ± 0.09) suggests that burrows
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tended to be slightly smaller at impacted sites. This effect was, however, not consistent among
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studies. Thirteen out of 38 (34%) studies measured changes in burrow size, which allowed calculation
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of response ratios. Of these, 12 (92%) tested for differences between mean diameter, with eight
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reporting significant differences in burrow diameter: two studies document smaller diameter burrows,
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whilst six document larger ones at impact sites (Table 2, Fig. 2).
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Limited (one or two papers depending on the type of pressure) information is available on abundance
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changes attributable to stressors other than vehicles, nourishment, or urbanisation. Notwithstanding
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this limitation, lower burrow counts appear to be associated with oil spills (lnR = -4.61), invasive plants
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(lnR = -2.81), subsistence harvesting (lnR = -0.42), mining (lnR = -0.97), and trampling (lnR = -0.14).
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Conversely, a greater number of burrows have been reported from dune areas frequented by campers
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(lnR = 0.44) and following human controls on the crabs’ predators (i.e. culling of racoons to protect
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turtle eggs and hatchlings; lnR = 0.38) (Barton and Roth, 2008).
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The three papers that measured variables other than the number and diameter of burrow openings
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report decreases in the extent of daily home range (lnR = -0.80), trail length (lnR = -0.31), burrow
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depth (lnR = -0.20), burrow volume (lnR = -0.11), and burrow angle (lnR = -0.36). A single paper
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describes a 50 % increase in body condition of crabs collected from camp grounds in dunes relative to
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reference sites without camping (Schlacher et al., 2011a).
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3.3Addressing Pressures: Gaps and Opportunities
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In terms of how ghost crabs can be used to assess ecological effects arising from the main types of
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human stressors acting on sandy beaches, six clusters emerge based on the degree of missing
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information (‘data deficiency’) and the likely reliability of ghost-crabs as indicator species to deliver
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these data (‘suitability’) in the future (Table 3, Fig. 3).
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1.) Pressures that both lack data regarding their ecological impacts and can be readily addressed
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using ghost crabs as suitable indicators in future studies: five aspects of pollution (artificial night light,
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chemical pollutants, marine debris, noise, and sewage) and warming of the atmosphere and oceans
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associated with climate change.
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2.) Pressures that lack data and can be gauged with ghost-crabs, albeit at slightly lower confidence or
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scope than those in the first cluster: altered current regimes and upwelling under climate change, the
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effects of invasive algae, and thermal-discharge impacts.
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3.) A broad suite of pressures for which some data on their ecological effects do exist (i.e. moderate
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data deficiency) and for which ghost crabs would be good ecological indicators for future
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assessments: urbanisation stressors (armouring, urbanisation, grooming), invasive carnivores and dune
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plants, fisheries and mining impacts, and the consequences of sea-level rise and altered storm
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regimes.
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4.) Three pressures that have both moderate data availability and can be measured with ghost crabs at
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moderate levels of indicator performance: dune camping, recreational fishing, and trampling.
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5.) Ghost crabs are very well suited to assess the biological effects of vehicles and sand nourishment
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on beaches and this is reflected by an adequate level of available information for these two pressures.
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6.) Few or no data currently exist for the biological effects of ocean acidification, altered precipitation,
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and motorised watercraft in beach systems; however, ghost crabs will rarely be the indicator taxon of
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first choice in impact assessments targeting these specific stressors (Table 3, Fig. 3).
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4. Discussion
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4.1 Time for New Directions?
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A sizeable body of evidence is now available that strengthens arguments for the use of ghost crabs as
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indicator species to assess the biological and ecological consequences of human activities and habitat
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changes on sandy beaches (Table 1, Fig. 2). In addition, there is a reasonably broad geographic
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distribution of published studies (Fig. 1) and coverage of issues (Fig. 2), suggesting that the use of Page | 8
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ghost crabs as ecological indicator species is widely applicable and versatile. Much of this reach stems
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from the ease with which population estimates can be made by counting burrow entrances. However,
312
what is – in a technical sense – a fortuitous trait of ghost crabs, has also led to a prevalence of simple
313
‘compare and contrast designs’ that usually fail to measure response variables of the organisms
314
directly, instead relying overwhelmingly on burrow numbers and sizes as proxies (Table 1).
315 Notwithstanding the broad usage of the technique, there are, in our opinion, five new directions that
317
future environmental studies using ghost crabs should take. 1.) Establishing the mechanistic links that
318
account for observed spatial contrasts (‘processes’). 2.) Adopting more diverse designs, especially
319
those that encompass experiments aimed at discerning causality in the relationship between
320
functional responses and the intensity and nature of putative stressors on one hand, and the resulting
321
biological effects on the other (‘dose-response studies’). 3.) Separating individual causative agents
322
among suites of putative predictors (‘specificity and un-confounding’). 4.) Including modern genetic,
323
bio-chemical and physiological biomarkers and assays that reflect the state of the art in ecotoxicology
324
and behavioural ecology. 5.) Broadening the scope of environmental pressures that are addressed in
325
future impact assessments using ghost-crabs as “canaries in the mine” (‘scope and thematic ambit’).
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Resolving the first four issues above will essentially be a question of aligning ghost-crab studies with
328
modern statistical and eco-toxicological design principles that will yield more robust and reliable
329
attribution and inference. Expanding the thematic ambit to be truly reflective of the diverse nature of
330
anthropogenic stressors acting on sandy beach and dune systems is potentially a very large
331
undertaking, but offers, in our opinion, rich opportunities - we sketch these prospects and their
332
rationale in the following sections.
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4.2 Addressing Significant Anthropogenic Beach Stressors Using Ghost Crabs as
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Indicators
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4.2.1 Climate-Change-Associated Effects: Sea-level rise, Warming, Current and Rainfall
338
Changes, Ocean Acidification
339
Beaches are malleable and dynamic landscapes, responding readily to changes in external physical
340
forcing (Schlacher et al., 2015b). The key physical beach controls that are modified by climate change
341
are accelerated sea-level rise (IPCC, 2013), altered wave and large-scale weather regimes (Barnard et
342
al., 2015; Hemer et al., 2013; Johnson et al., 2015), possibly augmented by storminess (Emanuel, 2013).
343
These can have dramatic impacts on beach and dune geomorphology, resulting in greater erosion and
344
shoreline retreat, and more widespread and frequent coastal flooding during storms (Johnson et al.,
345
2015; Woodruff et al., 2013).
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Changes to the beach and coastal morphology attributable to global change can be accurately
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consequences of these habitat alterations are less well understood; in this context, ghost crabs can be
350
useful indicators to gauge these consequences. For example, it is possible that local populations of
351
ghost crabs will become extinct in extreme cases of beach or dune erosion, especially where the upper
352
beach habitat near the strandline is lost and where high and persistent beach scarps are formed that
353
block movement of crabs between the non-vegetated beach and the dunes. Local extirpations of
354
invertebrates inhabiting the upper beach and lower dunes have already been reported for Californian
355
beaches under high urbanisation pressure (Hubbard et al., 2014). Ghost crabs may respond in a similar
356
fashion on sub-tropical and tropical beaches that have undergone recent extreme or repeated erosion
357
events: such effects may be exacerbated by delayed recovery on beaches with seawalls or similar
358
structures on the landward margin (Lucrezi et al., 2010).
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Rising temperatures associated with climate change are predicted to cause a broad range of biological
361
and ecological responses in marine organisms, including altered physiology, phenology, demography,
362
behaviour, and shifts in distributions and species ranges (Burrows et al., 2014; García Molinos et al.,
363
2015; Poloczanska et al., 2013; Sunday et al., 2015). We predict that several of the temperature effects
364
recorded in other marine species at the land-ocean interface will be detectable in ghost crabs, and
365
these can be tested experimentally. In fact, ghost crabs are good model organisms for such tests
366
because they are abundant, widespread, usually not of significant or legal conservation concern, and
367
relatively large bodied. These traits particularly favour their use in physiological studies (laboratory
368
and field-based) and in investigations examining geographic range shifts of beach species (Schoeman
369
et al., 2015). Interestingly, temperature will likely also affect larvae by increasing metabolic and
370
therefore development rates – earlier metamorphsis is likely to result, potentially reducing time in the
371
plankton, and therefore dispersal (Gerber et al., 2014; O'Connor et al., 2009).
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Altered oceanographic current regimes and greater variability or intensity in oceanographic forcing,
374
such as upwelling (Black et al., 2014; Sydeman et al., 2014), may affect the dispersal and survivorship
375
of larvae, and are predicted to modify the geographic patterns and magnitude of ghost-crab
376
recruitment onto beaches. It is certainly feasible to measure recruitment dynamics in relation to
377
changes in oceanographic forcing, and this can be combined with genetic work to examine changes in
378
connectivity amongst populations and beaches (e.g. Austin et al., 2015). Effects associated with altered
379
primary productivity, upwelling intensity, or the availability of marine carrion deposited on the shore
380
may be more varied, but some expectations are plausible. Ocean currents, and their nearshore
381
compensatory counter-currents, are more important in terms of dispersal of recruits, whereas storms
382
are more likely to generate wrack and carrion. One interesting exception here is the eastern boundary
383
current upwelling systems, with evidence suggesting upwelling might intensify, and perhaps shift
384
poleward (Sydeman et al., 2014; Wang et al., 2015). Ghost crabs currently do not occur in sizeable
385
numbers on beaches bordering some of the strongest and most persistent eastern boundary
386
upwelling areas, except in the Humboldt (Lucrezi and Schlacher, 2014). Thus, shifts in ghost crab
387
distributions may be a sensitive indicator to gauge the broader ecological impacts of altered
388
upwelling for sedimentary shore ecosystems.
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Notwithstanding uncertainties and large geographic variation in response, higher rainfall is possible in
391
response to climate change (Thorpe and Andrews, 2014). Plausible consequences for beach and dune
392
systems are altered dune vegetation (e.g. increased cover, shifts in species composition) and changes
393
in aquifers underlying dunes and beaches (e.g. increased height of water table, wider low-salinity
394
zones in the intertidal, increased discharge of groundwater to surf-zones) (Feagin et al., 2005; Werner
395
et al., 2013). Both are expected to affect ghosts crabs, and several predictive hypotheses can be tested
396
in the future: i) moderate increases in vegetation cover may enhance habitat stability of dunes, leading
397
to increased population abundance of crabs; ii) very dense vegetation, especially species with
398
extensive root networks, will impede burrowing and lead to lower crab abundance; iii) because crabs
399
avoid constructing burrows that reach the water table, higher ground-water levels might limit crab
400
populations (this effect is hypothesized to be strongest at the poleward edge of the range where deep
401
burrows are thought to provide a thermal refuge during winter; Schoeman et al., 2015).
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Ocean acidification has profound and varied impacts at multiple levels of biological and ecological
404
organisation; it affects organismal physiology, health, growth, survivorship, and abundance, and these
405
effects can propagate to changes at the assemblage and system scale (Byrne and Przeslawski, 2013;
406
Gaylord et al., 2015; Kroeker et al., 2013; Nagelkerken and Connell, 2015). Acidification is predicted to
407
affect ghost crabs during their larval phase, which could depress recruitment to beaches if growth
408
and/or survivorship are impaired. Recruitment could be monitored, but it is unlikely that this would be
409
considered an efficient variable to measure to assess the effects of ocean acidification in beach
410
ecosystems.
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4.2.2 Recreation Effects: Vehicles, Trampling, Camping, Motorised Watercraft,
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Recreational Fishing & Bait Collecting
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The environmental impacts of vehicles on beach-dune ecosystems are mostly well documented. A
415
solid body of evidence clearly demonstrates widespread, and often massive, environmental harm
416
caused by vehicles driven on beaches and in dunes, including adverse impacts on ghost crabs (Groom
417
et al., 2007; Moss and McPhee, 2006; Schlacher et al., 2013c; Walker and Schlacher 2011). Vehicle
418
effects are also among the few stressors for which the mechanisms of impacts (i.e. crushing, collisions
419
with wildlife) have been identified or quantified (Schlacher and Lucrezi, 2010b; Schlacher et al., 2007c;
420
Schlacher et al., 2008b). What is generally not known, but of great importance to management and
421
conservation, are the thresholds of use (e.g. traffic volumes, allowed vehicle types, distribution across
422
shores) above which negative biological effects rise steeply or become irreversible (Schlacher et al.,
423
2008b). In this context, more and better-designed impact studies that determine the ‘dose-response
424
curves’ for ghost crabs and other beach species (including charismatic flagship species such as turtles
425
and birds provided that ethical and permitting issues can be overcome for these vertebrates) for a
426
variety of stressors are a critical information gap to inform ecologically responsible management
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actions.
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Trampling is a near-ubiquitous disturbance agent in sandy shore systems, having multiple effects on
430
biota. These effects have been documented for species and assemblages in both the dunes (Brunbjerg
431
et al., 2014) and the non-vegetated beach seawards of the dunes (Reyes-Martínez et al., 2015;
432
Schlacher and Thompson, 2012). Surprisingly, given how common trampling is on many shores
433
worldwide, only a single paper has examined the short-term changes to ghost-crab burrow density
434
and size distribution following intense trampling by people on an urban beach (Lucrezi et al., 2009a).
435
Effects were small and crabs do not appear to be strongly affected by intense trampling over a period
436
of three days (Lucrezi et al., 2009a). Effects may well be stronger if trampling is particularly extreme at
437
small scales (~100m ; e.g. beach volleyball games) or sustained over much of the year (Turra et al.,
438
2005). Several papers have ostensibly measured the effects of 'trampling', but tests are invariably
439
confounded with other stressors superimposed at the same site, most often shore armouring and
440
urbanisation of the supratidal and the dunes. Thus, carefully designed studies are needed that
441
separate the impacts caused by trampling from other human pressures.
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Camping in coastal dunes close to beaches is a popular leisure activity. Whilst the environmental
444
impacts of ‘beach-camping’ are likely to be diverse, significant clearing of vegetation and vehicle-
445
associated impacts (e.g. tracks, erosion) are the most prominent and frequent adverse effects. Food
446
discarded by campers can provide additional resources for ghost crabs and other scavengers
447
(Schlacher et al., 2011a); whether this is a benign, positive, or negative practice is debatable and will
448
largely depend on the population of scavengers that is ‘subsidised’ (i.e. larger numbers of crows,
449
foxes, or racoons attracted to campground are predicted to increase predation pressure on ground-
450
nesting shorebirds and possibly also on ghost crabs). Populations of ghost crabs in dunes are
451
negatively impacted by vehicle tracks (Schlacher et al., 2011a), whilst benefiting – in terms of better
452
body condition - from food subsidies (Schlacher et al., 2011a). This illustrates that applications of
453
ghost crabs in environmental assessments can fruitfully extend beyond simple burrow counts. For
454
example, they may encompass tissue stable isotope measurements to test for the uptake of fecal
455
matter deposited by beach campers or the tissue analysis of hydrocarbons typical of off-road vehicle
456
emissions (Schlacher pers. obs.).
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The use of personal motorised watercraft (e.g. jet skis, water scooters, inflatable boats) in the surf-
459
zone is a popular leisure activity globally. However, there are numerous, often severe, environmental
460
consequences arising from this practice, poignantly summarised by Josephson (2007): “These
461
machines cannot be operated without loss of life or habitat”. Broad types of environmental impacts
462
encompass direct strikes on wildlife, bioacoustic impacts on fauna, chemical pollution (fuel spillages,
463
exhaust emissions, antifouling paints), and alterations to wave climates and turbidity (Erbe, 2013;
464
Whitfield and Becker, 2014). Ghost crabs generally enter the surf-zone only when gravid females
465
release eggs in the swash. Thus, impacts of watercraft on ghost crabs are expected to be much smaller
466
than for truly marine species (e.g. mammals, fish, and seabirds). However, chemical pollution arising
467
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468
beach erosion, crushing of crabs during launching and retrieval of boats and jet skis, and bioacoustic
469
impacts.
470 Beaches, especially their surf-zones, are important sites for coastal fisheries (Gutiérrez et al., 2011;
472
McLachlan et al., 1996). Many beach fisheries are small-scale (artisanal, subsistence), particularly in
473
less-developed countries, but recreational angling is widespread irrespective of socio-economic
474
conditions (Sowman, 2006). Where ghost crabs are harvested as part of subsistence fisheries, they are
475
susceptible to population impacts that can be measured using standard fishery-assessment
476
techniques (Kyle et al., 1997). On beaches without direct harvests of ghost crabs, ecological impacts
477
caused by fishing may still be detectable. Because a large fraction (on some beaches the vast majority)
478
of beach vehicle traffic is attributable to recreational fishers, impacts on ghost crabs often arise
479
indirectly from shore-based angling via vehicles. Discards of bait, by-catch, and fish frames are readily
480
consumed by birds on beaches (Rees et al., 2014). Consequently, it is possible that carrion subsidies
481
provided by fisherman enhance food intake in ghost crabs in similar ways. Arguably, this may be a
482
positive effect. Conversely, discarded fishing line may kill individuals that become entangled in it.
483
Hypotheses concerning impacts of carrion subsidy or fishing-line mortality have not been tested for
484
ghost crabs to date.
485
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4.2.3 Pollution: Sewage and Storm-water, Debris, Thermal discharges, Chemicals,
487
Noise, Artificial Night Light
488
Contamination of beaches with sewage and storm-water is a worldwide problem. The issue is regularly
489
managed for human health risks (Brownell et al., 2007; Sabino et al., 2014), but very rarely in the
490
context of its biological impacts (Mearns et al., 2014; Schlacher et al., 2006). Disregarding the broader
491
environmental consequences of sewage inputs to dunes and beaches ignores, however, the facts that
492
transfers of sewage-derived matter to beach invertebrates has been demonstrated on ocean shores
493
(Schlacher and Connolly, 2009), and that wastewater can have numerous detrimental impacts on the
494
health of organisms (Ings et al., 2012; Schlacher et al., 2007b). Ghost crabs are likely to be exposed to
495
human waste material via direct contact with solid waste and via water-borne material contained in
496
the aquifer and, to a small degree, the swash. Because pathogens (viruses, bacteria, fungi) and
497
xenobiotics are not restricted to the water, but are also found in beach sands (Sabino et al., 2014), the
498
intense contact of crabs with the sediment during burrow construction and maintenance and feeding,
499
increases the likelihood of exposure, uptake, and detrimental effects. A broad arsenal of biomarkers
500
(e.g. genetic, hormonal, immunological, cytological, enzymatic, histological) is available to assess such
501
health effects (e.g. Gillis et al., 2014), but surprisingly, biomarkers in ghost crabs have not been used
502
for ecological assessments; this line of enquiry thus offers multiple opportunities to better assess the
503
status of dune and beach systems in biologically more meaningful ways using a suite of different
504
biomarkers.
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Man-made debris, mostly plastics, is now one of the most common, widespread and persistent
507
pollutants in marine waters and beaches worldwide (Moore, 2008). The last decade has seen an
508
exponential rise in the number of scientific papers examining the biological impacts of marine debris,
509
reflecting a growing recognition of severe environmental harm arising mostly from plastics (Gall and
510
Thompson, 2015). Detrimental effects of larger marine debris on marine wildlife are often dramatic
511
(e.g. whales entangled in fishing nets, turtles succumbing from ingested plastic bags, seabirds
512
ingesting large volumes of floating plastics) (Vegter et al., 2014). Evidence is also rapidly accumulating
513
that smaller debris, microplastics (< 5 mm), has equally deleterious effects in a broad range of marine
514
organisms, ranging from toxicant magnification to incorporation of microspheres into consumers’
515
tissues (Ivar Do Sul and Costa, 2014; Law and Thompson, 2014). Beaches are deposition sites for
516
floating marine debris, accumulating both larger litter items and high concentrations of microplastics
517
up to 2 m deep into the sediments (Fisner et al., 2013; Turra et al., 2014). Alarmingly, beach deposits
518
can contain the toxic break-down products of styrofoam in large quantities (Kwon et al., 2015).
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Accurately measuring and predicting the environmental risks that marine debris poses for wildlife is a
521
research priority for beaches and beyond (Brennecke et al., 2015; Vegter et al., 2014). Because beaches
522
are prime sites for accumulation of debris, they are ideal model sites to test the ecological effects of
523
debris. These effects are likely to differ between larger litter items and microplastics (Law and
524
Thompson, 2014). Hypothetically, large debris may add habitat complexity and heterogeneity to
525
beach environments and increase sediment stability at small, patchy scales; these habitat
526
modifications may propagate to greater abundance and/or longevity of crab burrows and other
527
invertebrates. Conversely, ingestion and tissue transfer of microplastics and associated toxicants by
528
ghost crabs is possible (Brennecke et al., 2015), with potential knock-on effects on the health and
529
fitness of organisms that may propagate to impacts (untested) at the assemblage and system level
530
(Brennecke et al., 2015; Browne et al., 2015).
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The few available studies on the ecological effects of marine debris are often correlational or lack
533
empirical data on mechanisms, making the interpretation of reported conclusions somewhat
534
problematic (Browne et al., 2015). We propose that ghost crabs are suitable organisms to undertake
535
such experiments on biological debris effects, given that their distribution overlaps with the stranding
536
zone of most marine debris and that they can be relatively easily manipulated and enumerated in
537
experiments (e.g. Schlacher et al., 2007c).
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In addition to the global effects of climate change, localised human modifications to the thermal
540
environment in coastal areas arise mainly from discharges of cooling water required in power plants,
541
typically at temperatures 8–12.5 °C above the intake water (Wither et al., 2012). Altered temperature
542
affects the behaviour, phenology, distribution, reproduction and movement of many marine
543
organisms subjected to thermal effluents (Mazik et al., 2013; Wither et al., 2012). On beaches, patterns
544
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localised density effect may be possible (Hussain et al., 2010), but attribution was highly uncertain, and
546
impacts on high-energy coasts are likely to be limited to 100s of metres (Cardoso-Mohedano et al.,
547
2015). Because ghost crabs rarely enter the swash post settlement they are not routinely exposed for
548
significant periods to thermal discharges where these occur in the surf-zone of beaches. Hence ghost
549
crabs are unlikely to show strong and persistent temperature responses to this particular stressor. It is
550
possible, however, that thermal plumes may modify larval behaviour, dispersal and recruitment to
551
beaches. Also, traces of biocides (added to cooling water to prevent bio-fouling) may have broader
552
effects on the condition of exposed individuals close to discharge points (Mazik et al., 2013).
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Chemical contaminants, toxicants, and xenobiotics are a major class of anthropogenic stressor in
555
marine ecosystems. The biological effects, and their ecological ramifications, of chemical contaminants
556
are as diverse as their sources, and new threats are continually being identified (Mearns et al., 2014).
557
The issue of chemical pollution in dune-beach systems is treated very cursorily (Defeo et al., 2009; Nel
558
et al., 2014); however, there is no reason to suspect that species and dune-beach ecosystems are less
559
susceptible to inputs of toxic chemicals than other marine ecosystems. The one exception to the
560
dearth of data on chemical pollution effects in beach systems is crude oil spills. Probably due to the
561
high public profile of spill events, short-term ecological changes in beach systems following shipping
562
accidents and well failures have been reported for several incidents globally (de la Huz et al., 2005;
563
Engel and Gupta, 2014; Schlacher et al., 2011b; Stevens et al., 2012), although questions about
564
recovery remain mostly unanswered (Peterson et al., 2003). The biological impacts of many chemicals
565
are truly global, but they are often most evident near cities in developed countries. Ghost crabs occur
566
regularly in dunes and beaches in and near coastal cities, making them appropriate sentinel species to
567
monitor ecological effects in these settings. Also, ghost crabs are the apex invertebrate predators on
568
sandy shores, creating opportunities to measure chemical contaminant transfers through food webs.
569
How oil spills affect ghost crabs has also not been quantified, representing an obvious opportunity to
570
include them in future spill assessments. Furthermore, ghost crabs may directly consume toxic flakes
571
of antifouling paint where small boats are scrapped and re-painted directly on the beach.
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Humans emit a range of chemical and physical stimuli that disturb animals and interfere with the
574
perceptual processing of important signals and cues, creating sensory pollution in many ecosystems
575
(Halfwerk and Slabbekoorn, 2015). Man-made noises have become near ubiquitous (Radford et al.,
576
2014), creating an acoustic environment that presents novel challenges to many animal species
577
(Morley et al., 2014; Shannon et al., 2015). Whilst the biological effects arising in this altered acoustic
578
landscape are manifold, they most often encompass shifts in physiology (e.g. impaired hearing,
579
elevated stress hormone levels), changes to key behaviours (e.g. foraging, mating, vigilance,
580
movement), interference with the ability to detect important natural sounds (e.g. vocalisations of
581
conspecifics, acoustic signals of prey or predators), and direct fitness consequences (e.g. survival,
582
reproduction)(Morley et al., 2014; Shannon et al., 2015). Vertebrates (especially birds, mammals and
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583
fish) are by the far most-studied group in terms of noise pollution, but impacts are equally detectable
584
– and arguably of comparable biological significance – in invertebrates (Morley et al., 2014).
585 Hearing and sound production in brachyuran crabs provides essential environmental information
587
(Hughes et al., 2014) and facilitates channels for communication, which can be in the form of
588
elaborate audio-visual displays in ghost crabs (Clayton, 2008). Crabs are also sensitive to noise
589
pollution, detectable as physiological stress (Wale et al., 2013b), altered development (Pine et al.,
590
2012), shifts in foraging behaviour (Wale et al., 2013a), or impaired predator avoidance (Chan et al.,
591
2010). Contemporary beach and dune habitats present strongly altered acoustic landscapes for ghost
592
crabs and other species, so the potential exists for biological and ecological impacts arising from man-
593
made noise in sandy shore systems.
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Two aspects of ghost crab biology appear particularly intriguing to us in the context of assessing
596
noise pollution on beaches: behavioural shifts in responses to predation risks as a result of altered
597
acoustic landscapes and distorted acoustic settlement cues. Man-made noise can reduce an animal’s
598
fitness by impairing its ability to respond normally to a potential predator; such altered risk
599
assessment to predation has been experimentally demonstrated for hermit crabs exposed to boat
600
noise (Chan et al., 2010). Significantly, hermit crabs share several traits with ghost crabs, most notably
601
being conspicuous, semi-terrestrial animals displaying a distinct predator avoidance behaviour that
602
relies on hiding (hermit crabs retreat into their shells whilst ghost crabs flee into their burrows). This
603
offers the intriguing possibility of assessing noise pollution in beach animals using ‘behavioural
604
acoustic bio-assays’ in ghost crabs. Because brachyuran shore crabs use habitat-specific acoustic cues
605
for settlement, acoustic sensory pollution may impact on recruitment intensity and patterns, as
606
suggested for estuarine crabs based on limited lab experiments (Pine et al., 2012). It is possible, but
607
untested, that noise from personal watercraft may interfere with settlement cues important for late-
608
stage larvae of ghost crabs in the surf-zone off beaches. Anthropogenic noise may also mask the
609
acoustic signals produced by prey that predators use during foraging (Halfwerk and Slabbekoorn,
610
2015). Ghost crabs are omnivorous predators and scavengers of catholic tastes (Lucrezi and Schlacher,
611
2014), and it is thus possible, but untested, that prey detection and foraging efficiency in ghost crabs
612
in altered acoustic landscapes changes - this offers intriguing possibilities for acoustic bio-assays.
613
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Global light regimes have changed profoundly in intensity, spectral signatures, spatial patterns, and
615
periodicity (Kyba et al., 2015). Such changes to the light environment experienced by organisms are
616
amplified in the coastal fringe where a growing part of the human population is concentrated in
617
expanding coastal cities (Davies et al., 2014). How organisms respond to these new illumination
618
domains created by artificial night light, and the ecological ramifications of their responses, are
619
equally profound; they include changes to gene expression, physiology, behaviour, distributions, and
620
the composition of communities (Davies et al., 2015; Gaston et al., 2013; Gaston et al., 2014).
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The adverse effects of artificial night light on beach biota are well publicised for marine turtles: fewer
623
nests generally occur on more brightly lit sections of sandy coasts where hatchlings become
624
disorientated by shore-based lights (Kamrowski et al., 2014; Mazor et al., 2013; Verutes et al., 2014).
625
With the exception of a single study on beach mice, impacts of artificial night light on other beach
626
species, including ghost crabs remain untested, but are certainly plausible. For example, navigation in
627
mobile beach invertebrates (e.g. amphipods, isopods) can be complex and relies on multiple cues that
628
can include moonlight. It follows that artificial night light has the potential to disrupt orientation and
629
movement in sandy-shore animals (Scapini, 2014); it is not known whether ghost crabs also use light
630
cues to orient (e.g. homing behaviour), but effects of light pollution on movement and orientation
631
cannot be precluded and hence could be measured using behavioural assays.
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Moonlight is important in determining activity in many animal species, mainly related to changes in
634
predation risk and reproductive cycles (Kronfeld-Schor et al., 2013). Many beaches are artificially
635
illuminated at night (in addition to the more diffuse but widespread skyglow) potentially interfering
636
with natural cycles of lunar signals that are particularly important in nocturnally-foraging species. In
637
beach mice, nocturnal movement is modulated by moon phases, presumably in response to higher
638
predation risk during full-moon nights (Wilkinson et al., 2013). Consequently, beach mice exposed to
639
artificial light feed significantly less and exploit fewer food patches (Bird et al., 2004). Ghost crabs have
640
a functionally similar foraging behaviour (i.e. regular nocturnal excursion from burrows). Their foraging
641
behaviour and activity rhythms may therefore be equally sensitive to artificial light at night and could
642
possibly have fitness implications (e.g. body condition, fertility etc.). Artificial light may also extend the
643
foraging window of visually-orientated predators into the nocturnal activity period of ghost crabs, and
644
facilitate prey detection by both native consumers (e.g. shorebirds) and feral or invasive carnivores
645
(e.g. foxes, cats). Thus, changes to foraging behaviour and predation risk in ghost crabs that are
646
associated with artificial night light could be used to gauge the biological implications of light
647
pollution in sandy shore species.
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4.2.4 ‘URBANISATION’: Buildings, Grooming, Armouring, Nourishment
650
At least half of the global human population lives in cities, and these urban populations will grow
651
exponentially in the coming decades, fuelling an escalating expansion of cities globally, many of which
652
border the ocean (Seto et al., 2012; Strauss et al., 2015). Coastal cities are hotspots of current and
653
future urbanisation, including in Australia, where most (> 80%) of the population is concentrated in
654
urban centres, which are mostly located near beaches (Hallegatte et al., 2013). Pervasive ecological
655
changes in cities commonly include biotic homogenisation, biodiversity declines, altered population
656
dynamics of species, and shifts in the species composition of assemblages (Aronson et al., 2014; Sol et
657
al., 2014).
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Because beaches represent highly attractive and valuable nodes for coastal development, coastal
660
urbanisation is frequently intense along sandy coastlines (Mills et al., in press; Nordstrom et al., 2000). Page | 17
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The ecological ramifications of this ‘beach urbanisation’ span a broad ambit of reported impacts,
662
ranging from impediments to turtle nesting to local extirpations of invertebrates and functional losses
663
of key vertebrate groups (Hubbard et al., 2014; Huijbers et al., 2015b; Huijbers et al., 2013; Schlacher et
664
al., 2015a). ‘Urbanisation effects’ have also been reported for ghost crabs in several urban beach
665
studies (e.g. Barros, 2001). Except for a few isolated cases (e.g. habitat loss caused by urban seawall
666
construction; Dugan et al., 2008), the underlying causes and mechanisms that produce the observed
667
biological responses to urbanisation remain, however, largely unresolved. Failures to isolate, and
668
mechanistically explain, the causative stressors in urban beach studies arise either from employing
669
inadequate study designs, or from simply reflecting the multiple nature of man-made pressures in
670
these environments where noise pollution, artificial night light, shore-defences, trampling, grooming,
671
and nourishment often coincide in space and time (Acuña and Jaramillo, 2015). From a conservation
672
perspective it is, however, critical to resolve which of the putative factors causes the most
673
environmental harm as this will guide prioritisation of management interventions. It is also unknown
674
how, and to which degree, these urban pressures interact to produce the observed ecological effects
675
on urban beaches (but see Lucrezi et al., 2010).
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Many urban beaches are regularly cleaned (‘groomed’ or ‘raked’) to remove beach-cast algae and
678
seagrass (‘wrack’) and litter, mainly for aesthetic and public-health reasons. Wrack constitutes,
679
however, an important habitat and food resource in beach ecosystems (Colombini and Chelazzi, 2003).
680
Consequently, beach cleaning operations have multiple ecological flow-on effects: loss of upper beach
681
habitat and strandline vegetation (Dugan and Hubbard, 2010); reduced abundance and diversity of
682
invertebrates reliant on wrack (Gilburn, 2012; Llewellyn and Shackley, 1996); and diminished
683
abundance, density, and fitness of beach-nesting birds and beach-spawning fishes (Dugan et al., 2003;
684
Martin et al., 2006; Pietrelli and Biondi, 2012).
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Beach cleaning targets mainly the upper shore, which is the main habitat of ghost crabs. Expectations
687
are therefore that cleaning will adversely impact ghost crabs, but this has not been explicitly tested.
688
From a management perspective, it will be important to develop best practices for beach cleaning
689
operations (assuming a continued public mandate to clean beaches) that reduce ecological impacts; in
690
this context, ‘dose-response’ type studies using ghost crabs, combined with experiments that compare
691
techniques and procedures (e.g. manual removal, different equipment, depth of raking, etc.) in terms
692
of their ecological impacts will be useful. Since abundance estimates for ghost crabs via counts of
693
burrows are less costly than sampling other beach invertebrate, they provide an advantage by
694
allowing more treatment types and replication levels.
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Shoreline recession is a major risk to public and private assets located on eroding sedimentary
697
coastlines (Johnson et al., 2015). Conventional approaches to combat beach erosion are to replace the
698
lost sand volumes (‘dredge-and-fill’, ‘nourishment’) or to stabilise shore position with fixed, hard
699
structures (‘seawalls’, ‘shore armouring’). With respect to adverse environmental impacts, nourishment Page | 18
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has traditionally been viewed as a less harmful option than armouring, but adverse ecological
701
outcomes of beach filling are not uncommon. These include significant reductions in the abundance
702
of infaunal organisms, resulting from a combination of limited recruitment, unsuitable new sediment,
703
and direct mortality from crushing and burial (Manning et al., 2014; Peterson et al., 2006). Impacts of
704
nourishment on invertebrates propagate upwards to shorebirds and fishes through loss of prey
705
organisms and deteriorating feeding conditions on nourished beaches (Manning et al., 2013; Peterson
706
et al., 2006). These effects can be long-lasting, with recovery from nourishment impacts taking several
707
years or longer (Peterson et al., 2014; Schlacher et al., 2012).
708
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Nourishment impacts are well documented for ghost crabs in a few locations, where significant
710
declines in population density have been detected following sand placement, and reduced
711
recruitment has been recorded at nourished sites (Peterson and Bishop, 2005; Peterson et al., 2000).
712
There remains, however, considerable scope to use ghost crabs in targeted experiments that establish
713
threshold levels of nourishment procedures that are less damaging than current practices (e.g.
714
acceptable depth of burial, frequency of application, spatial extent of single sand placement, etc.).
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Engineered structures aimed at stabilising shorelines are widely constructed to protect human assets
717
on soft, sedimentary shorelines, particularly in response to beach erosion (Nordstrom, 2014). Whilst
718
the practice of ‘shore armouring’ with seawalls and similar structures has occurred for millennia, its
719
ecological impacts have been recognised only in the last two decades (Dugan et al., 2011). In brief,
720
shore armouring significantly diminishes habitat extent and quality, resulting in severe reductions and
721
local extirpations of animal and plant species inhabiting the interface between the dunes and the
722
beach on armoured beaches (Dugan et al., 2008; Hubbard et al., 2014); these impacts propagate to
723
shorebirds and are publicly well recognised for turtles where seawalls create significant barriers to
724
nesting (Witherington et al., 2011).
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Although the adverse effects of shore armouring have been relatively well documented for ghost
727
crabs (e.g. Barros, 2001; Lucrezi et al., 2010), there remains a great potential for studies that identify
728
the biological returns from creative alternatives to traditional shore defence (e.g. structures that are
729
smaller, or below ground, or constructed from materials that improves habitat values, etc.; Nordstrom,
730
2014) and biological returns from restoration of habitats by removing armouring structures (Toft et al.,
731
2014). Biota can respond relatively quickly to habitat restoration on beaches (Toft et al., 2014), but
732
wider uptake of environmentally less destructive practices will require broad political and public
733
acceptance (Nordstrom, 2014). Demonstrating positive biological responses of key biota is imporant
734
to achieve better acceptance, and species of public appeal are central in this process (Huijbers et al.,
735
2015b). Arguably, amongst the beach invertebrates, ghost crabs (as a taxonomic group) are a prime
736
candidate to be used in this context, particularly as the basic patterns of their response to traditional
737
shore armouring is already known (e.g. Barros, 2001; Lucrezi et al., 2010).
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4.2.5 Invasive Species: Non-native Carnivores, Dune Plants and Seaweeds
740
Invasive, predominantly non-native, species have the potential to significantly alter the architecture
741
and function of ecosystems (Ehrenfeld, 2010). Traditional views concerning the effects of invasive
742
species have emphasised major adverse impacts (Courchamp et al., 2003; Norton, 2009), but a more
743
nuanced view is emerging (Davis et al., 2011; Pysek et al., 2012; Strayer, 2012). Whilst invasive species
744
effects are highly topical in the broader ecological literature (Moran and Alexander, 2014; Yelenik and
745
D'Antonio, 2013), beach ecology is somewhat lagging in this respect.
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Information on the effects of non-native species in coastal dune and beach systems is largely
748
restricted to: i) trophic impacts of exotic mammalian carnivores (Brown et al., 2015; Huijbers et al.,
749
2015a; Huijbers et al., 2015b; Huijbers et al., 2013; Maslo and Lockwood, 2009; Schlacher et al., 2013a;
750
Schlacher et al., 2013b); ii) how exotic vegetation modifies dune geomorphology and habitat quality
751
for dune-associated species (Johnson and De León, 2015; Nordstrom et al., 2011; Zarnetske et al.,
752
2012); and iii) the implications of fire ants for nesting success in marine turtles (Allen et al., 2001).
753
Much less is known about the effects of invasive species on the non-vegetated part of the beach and
754
in the surf-zone. However, non-native species of macroalgae that are invading the nearshore zone off
755
beaches alter wrack composition and quality, resulting in changes to animal use of wrack and possible
756
flow-on effects on feeding and fitness of wrack-associated consumers (Lastra et al., 2008; Rodil et al.,
757
2015; Rodil et al., 2008).
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Effects of invasive species on ghost crabs have been documented in only a single study reporting
760
lower density of O. cordimanus in areas dominated by exotic vegetation (Brook et al., 2009). Other
761
effects are, however, plausible, involving any of the mechanisms above (e.g. top-down control by
762
exotic and feral carnivores, infestation with fire ants) and hence can be fruitfully measured.
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4.2.6 Fishing and Mining
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A pivotal ecosystem service provided by sandy beaches on many shorelines globally is the provision of
766
harvestable species for human consumption. These ‘beach fisheries’ target both vertebrates (i.e. bony
767
fishes, sharks, rays) and invertebrates, mostly benthic bivalves (McLachlan et al., 1996). The economic
768
nature of beach fisheries ranges from the occasional collection of individuals for subsistence to true
769
commercial operations (Castilla and Defeo, 2001), and are subject to the same problems (e.g. over-
770
harvesting, social conflicts, socio-economic cohesion) as are often evident in open-water finfish
771
operations (Gutiérrez et al., 2011). Species in both the intertidal and the surf-zone are harvested (Turra
772
et al., 2015), and such harvests are not limited to ‘less developed’ economies but occur globally (Gray
773
et al., 2014; Gutiérrez et al., 2011).
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There exist very few data on ghost crab harvesting with respect to species targeted, geographic
776
distribution, frequency and population impacts. The single ghost crab fishery for which published data Page | 20
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are available (e.g. eastern KwaZulu-Natal, South Africa) appears to have, historically, had few adverse
778
population-level effects under low intensities of subsistence collecting (Beckley et al., 1996; Kyle et al.,
779
1997; Robertson and Kruger, 1995). However, these are historical estimates and human population
780
growth, coupled with changing economic conditions, may have increased harvesting pressures
781
considerably. It is also very plausible that ghost crabs are harvested for subsistence purposes in many
782
other small-scale artisanal fisheries (A. Turra pers. comm.); whether these artisanal harvests constitute
783
significant ecological impacts is unknown.
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Sand and gravel (aggregates) are among the globe’s most valuable mineral resources, being mined
786
world-wide and account for the largest volume of solid material extracted (Peduzzi, 2014). Most of the
787
mined aggregates are used for construction and land reclamation, complemented by applications in
788
road embankments, asphalt pavements, and manufacturing (glass, electronics; (Peduzzi, 2014). Two
789
developments in aggregate extractions have particularly dramatic repercussions for sandy beaches: i)
790
the volumes of mined marine sand exceed the volumes of sand delivered by rivers to the ocean; and
791
ii) as inland sources of aggregates are becoming exhausted, mining has increasingly shifted to
792
shorelines (Peduzzi, 2014).
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Not surprisingly, removing often large volumes of sand from beaches can lead to significant changes
795
in landforms and sediment properties, and can accelerate erosion (Jonah et al., 2015) to the point
796
where mining on sandy-shores has been labelled as effectively constituting “active destruction” of
797
beaches (Pilkey and Cooper, 2014). Further geo-morphological impacts arise from the disposal of
798
tailings or slurries on the beach or into the nearshore zone (Castilla, 1983). Habitat alterations caused
799
by mining operations on beaches and in dunes translate into significant ecological harm, generally
800
manifested as reductions in abundance, biomass, and diversity of beach-associated species, local
801
extirpations, and major shifts in the species composition of assemblages exposed to mining (Pulfrich
802
and Branch, 2014; Simmons, 2005). Ghost crabs can respond in a similar pattern to habitat changes
803
arising from sand extraction, but the generalisations about biological impacts are impossible to make
804
from a single study (Jonah et al., 2015). Thus, ecological cause-and-effect studies of beach and dune
805
mining using ghost crabs as ecological indicator species in more locations, and using more response
806
variables, have future potential.
807
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808
5. Conclusions
809
Notwithstanding the sizeable number of studies that have examined ‘urbanisation effects’ on ghost
810
crabs, generalisations that can be developed into credible conservation actions in this domain remain
811
largely very unsatisfactory, chiefly because knowledge about mechanistic links are poorly known.
812
Whilst this situation is not unique to beach science, bedevilling urban ecology more widely
813
(McDonnell and Hahs, 2013), we contend that it presents an opportunity rather than a malaise: future
814
urban beach studies can build on the considerable knowledge about ghost crab biology and use the Page | 21
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815
design principles established for ecological experiments to employ logically consistent and powerful
816
designs that will yield stronger inference and attribution about urban effects; such experiments will
817
also need to draw upon more refined predictor and response variables that better match the
818
hypotheses tested (Browne et al., 2015; McDonnell and Hahs, 2013).
819 Whereas ghost crabs have proven to serve well to monitor conditions of sandy beaches throughout
821
the tropical and subtropical latitudes, standard assessment metrics currently involve inferring
822
abundances from numbers of burrows and sizes from burrow diameters. The failure to observe and
823
make direct measurements on the crabs themselves, including modern biomarkers, inhibits strong
824
inference about the mechanistic process or processes that cause differences in burrow counts or in
825
burrow diameters. It also limits our ability to identify critical biological harm where it may occur.
826
Nevertheless, sampling of individual ghost crabs and using them in experiments that test explicit
827
hypotheses is feasible and could expand the range of process-oriented inferences about specific
828
drivers of observed burrow abundance differences. While some manipulative experiments could be
829
piggybacked on field studies of real-world coastal impacts, especially if these studies can be initiated
830
in advance of the putative impact, much could also be learned by fundamental experimental work in
831
the laboratory. Thus, further progress is contingent on a better mechanistic understanding of what
832
drives observed responses in ghost crabs, from the individual to the population levels, and more
833
rigorous attribution to specific anthropogenic stressors.
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In any respect, ghost crabs lend themselves almost ideally to such studies, therefore representing a
836
powerful model organism for detection of ecological impacts in warm-temperate to tropical coastal
837
systems. The scope of anthropogenic impacts on ocean beach ecosystems promises more and
838
growing needs for impact evaluations. Ghost crabs can continue to provide a strong indicator of
839
impact from studies of counting and/or sizing burrows. However, these widespread dune dominants
840
may be used to provide even more specific indicators of process and causation as they are further
841
used in future experiments.
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Allen, C.R., Forys, E.A., Rice, K.G., Wojcik, D.P., 2001. Effects of fire ants (Hymenoptera: Formicidae) on hatching turtles and prevalence of fire ants on sea turtle nesting beaches in Florida. Florida Entomologist 84, 250-253.
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Austin, J.D., Gore, J.A., Greene, D.U., Gotteland, C., 2015. Conspicuous genetic structure belies recent dispersal in an endangered beach mouse (Peromyscus polionotus trissyllepsis). Conservation Genetics 16, 915-928.
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Black, B.A., Sydeman, W.J., Frank, D.C., Griffin, D., Stahle, D.W., García-Reyes, M., Rykaczewski, R.R., Bograd, S.J., Peterson, W.T., 2014. Six centuries of variability and extremes in a coupled marine-terrestrial ecosystem. Science 345, 1498-1502.
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Borenstein, M., Hedges, L.V., Higgins, J.P.T., Rothstein, H.R., 2009. Introduction to Meta-Analysis. John Wiley & Sons, Chichester, United Kingdom.
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Brennecke, D., Ferreira, E.C., Costa, T.M.M., Appel, D., da Gama, B.A.P., Lenz, M., 2015. Ingested microplastics (>100μm) are translocated to organs of the tropical fiddler crab Uca rapax. Marine Pollution Bulletin 96, 491-495.
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Burrows, M.T., Schoeman, D.S., Richardson, A.J., Molinos, J.G., Hoffmann, A., Buckley, L.B., Moore, P.J., Brown, C.J., Bruno, J.F., Duarte, C.M., Halpern, B.S., Hoegh-Guldberg, O., Kappel, C.V., Kiessling, W., O'Connor, M.I., Pandolfi, J.M., Parmesan, C., Sydeman, W.J., Ferrier, S., Williams, K.J., Poloczanska, E.S., 2014. Geographical limits to speciesrange shifts are suggested by climate velocity. Nature 507, 492-495.
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Byrne, M., Przeslawski, R., 2013. Multistressor impacts of warming and acidification of the ocean on marine invertebrates' life histories. Integrative and Comparative Biology 53, 582-596.
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Castilla, J.C., Defeo, O., 2001. Latin American benthic shellfisheries: emphasis on co-management and experimental practices. Reviews in Fish Biology and Fisheries 11, 1-30.
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7. Figure Captions
Fig. 1 Distribution of studies reporting effects of human pressures on ghost crabs on ocean beaches. Fig. 2 Effect sizes attributed to different types of human pressures on the abundance (left panel) and size (right panel) of ghost crab burrow openings on ocean beaches. Plotted values are response ratios
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ln(R), calculated as the log of the quotient of the mean value recorded for impact sites, divided by the mean value at corresponding reference sites in individual studies: lnR = mean impact / mean control
(Borenstein et al., 2009). Dots represent response ratios from individual studies. Vertical lines are
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means and horizontal lines are the 95% confidence intervals for data groups with n ≥ 3.
Fig. 3 Classification of ecological impact assessment for specific human pressures with respect to the amount of information that is currently available about their effects on ghost crabs (y axis) and how
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sensitive and reliable ghost crabs are likely to be as indicator species in impacts studies targeting a particular pressure (x axis). Pressures in the top right are both information-poor (i.e. high data
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deficiency) and may be best quantified using ghost crabs (i.e. good suitability).
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Table 1 Attributes of reviewed publications that measured the response of ghost crabs to human activities or anthropogenic habitat changes on ocean-exposed sandy beaches. (Details for individual publications are provided in Table 1 of the supplementary material).
1 - Geographic Distribution Ocean Basin / Sea (No. studies) Pacific
Indian
South China Sea
20
12
5
1
Australia
USA
Brazil
13
12
5
min
max
mean
1.30
38.24
26.10
Tropics
Subtropics
28
10
Countries (No. studies)
South Africa
Others#
3
5
sd
9.35
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Latitude (º)
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Atlantic
2 - Species Species
No. Studies
O. quadrata
Species
18
O. cordimanus O ceratophthalma
No. Studies 2
13
O. africana O. madagascariensis
10
O. cursor
1
2
4
3 - Response Metrics
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O ryderi
3.1 No. metrics measured per study min
max
mean
sd
6
1.95
1.27
1 Metric
2 Metrics
3 Metrics
>3 Metrics
18
11
6
3
1
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3.2 No. studies using x metrics
3.3. Types of metrics used
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3.3.1 - Direct (Organism)
No. studies
3.3.2 - Indirect (Burrows)
No. studies
Mortality
2
Abundance
38
Home Range
1
Diameter
19
Body Condition
1
Depth
3
Trail Length
1
Length
3
Turns in Trail
1
Angle
2
Weight
2
Orientation
1
4 - Replication and Scale Spatial min
max
mean
sd
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No. sites (n) 2
21
5.16
4.11
0.05
310
38.69
66.10
min
max
mean
sd
2
27
8.89
6.77
1
1370
158.47
Spatial ambit (km) Temporal
Duration (days)
267.34
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# Ghana: 2, Cuba: 1, Seychelles: 1, Singapore: 1
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No. times measured (n)
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Table 2 Summary statistics of response ratios lnR in ghost crabs, testing the biological effects of human pressures on ocean beaches in terms of changes to the abundance and size of crab burrows. Response ratios, lnR, are the log quotient of the mean value at impact sites divided by the mean at reference sites: lnR = mean impact / mean control (Borenstein et al., 2009). Values of lnR < 0 denote decreases in abundance or size, whilst iR > 0 signifies more or larger burrows at sites classified as ‘impacted’ by authors. (Tabulated lnR values are for stressor
xxx
Abundance (burrow counts)
RI PT
assessed by at least three studies; for all full listing of all studies refer to Table S1 and Fig. 2.).
Size (burrow diameter)
n
mean
(95% CI)
P
n
mean
(95% CI)r
P
All stressors
37
-1.35
(-1.78 - -0.92)
<0.0001
13
-0.15
(-0.35 - 0.05)
0.1327
Vehicles
11
-1.43
(-2.42 - -0.43)
0.0095
5
-0.07
(-0.27 - 0.13)
0.3772
Nourishment
4
-1.27
(-2.41 - -0.13)
0.0378
0
na
na
na
Urbanisation & Recreation
13
-1.52
(-2.16 - -0.87)
-0.19
(-1.23 - 0.84)
0.5064
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3
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0.0003
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1394 1 1395 2 3 1396 4 1397 5 6 1398 7 1399 8 9 1400 10 1401 11 1402 12 13 14 15 16 17 18 19 20 21 22 23 24 25 1403 26 27 1404 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62 63 64 65
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Table 3 Gap analysis of the application of ghost crabs as indicator species to quantify the ecological consequences of human pressures on ocean beaches and coastal dunes. 1
Habitat & Environmental Changes / Effects 1 (predicted)
Expected Response(s) of Ghost Crabs
CLIMATE CHANGE
Suitability of Ghost Crabs as Indicator 2 Species
Data Deficiency (Lack of Published Evidence for 3
Ghost Crabs)
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Main Pressures
Sea-level rise, storms
Erosion, shoreline retreat, elimination of upper beach and frontal dune habitats.
Population decrease(s), local extirpations, delayed recovery from erosion events, limited recruitment in beaches with (seasonal) scarps.
Warming
Temperature (increase).
Altered physiology, phenology, demography, geographic range, behaviour.
(good)
ΔΔΔ (high)
Currents, upwelling
Altered organism dispersal, primary productivity, marine carrion availability, wrack deposition.
Changes to recruitment and geographic distribution, altered nutritional status, condition and physiological performance.
(acceptable)
ΔΔΔ (high)
Altered precipitation
Changes to dune vegetation, height of water table, thermal environment of sand wedge, aquifer outcrops on beach.
Possibly, altered distribution and population size, but direction and magnitude difficult to predict.
(poor)
ΔΔΔ (high)
Diverse biological effects on marine organisms (e.g. decreased survival, calcification, growth, development, abundance in response to acidification and altered life histories).
Multiple detrimental developmental and survivorship effects during larval (fully marine) phase possible, possibly lowering recruitment to beaches.
(poor)
ΔΔΔ (high)
Substantially lower habitat quality, direct kills of individuals, behavioural changes.
Lower abundance, altered habitat use, population structure, and behaviour.
(good)
Δ (low)
(good)
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Acidification
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1405 1 1406 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62 63 64 65
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ΔΔ (moderate)
RECREATION Vehicles
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Lower habitat quality, direct kills of individuals, behavioural changes.
Lower abundance, altered habitat use & behaviour.
(acceptable)
ΔΔ (moderate)
Camping (dunes)
Increased food resources, altered habitat quality, behavioural changes..
Changed abundance, altered habitat use & behaviour
(acceptable)
ΔΔ (moderate)
Motorised Watercrafts
Noise and chemical pollution, wildlife strikes.
Altered behaviour and time budgets, toxicity, kills, etc.
(poor)
ΔΔΔ (high)
Population impacts on target species, bycatch, fauna impacts and habitat changes associated with vehicle-based access by fishers.
Individuals crushed by vehicles; food subsidies from fisheries discards.
(acceptable)
ΔΔ (moderate)
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Recreational fishing & bait collecting
SC
(jet skis, boats)
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Trampling
POLLUTION
Changes to interstitial chemistry, inputs of toxicants, nutrient enrichment.
Uptake of sewagederived nutrients and pollutants via direct exposure and foodweb transfers.
(good)
ΔΔΔ (high)
Debris
Ingestion (microplastics) or entanglement (larger litter), changes to structural attributes of beach habitat.
Physiological and other health impairment from ingestion of microplastics, altered distribution and higher abundance in areas of abundant larger litter items deposited on shore.
(good)
ΔΔΔ (high)
Increased habitat temperature and thermal variability.
Altered recruitment dynamics, possible health effects from anti bio-fouling treatment.
(acceptable)
ΔΔΔ (high)
Chemicals
Toxicity from contaminants; (e.g. crude oil spills).
Multiple and varied consequences of toxicity, from sub-lethal physiological and behavioural effects to impairment of reproduction and population persistence.
(good)
ΔΔΔ (high)
Noise
Acoustic environment (altered intensity and frequency spectrum).
Behavioural changes, altered behavioural time budgets and predation risks,
(good)
ΔΔΔ (high)
Thermal discharges
EP
TE D
Sewage and Stormwater
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1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62 63 64 65
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Artificial Night Light
Light environment (altered intensity and frequency spectrum).
Behavioural changes, altered behavioural time budgets and predation risks, endocrine disruptions.
(good)
ΔΔΔ (high)
Buildings, infrastructure, roads
Conversion or loss of natural habitat, especially the upper shore and dunes.
Smaller population sizes, shifts in distributions and possibly species interactions.
(good)
ΔΔ (moderate)
Grooming (raking, cleaning)
Habitat losses (upper beach), impedes dune formation, lowers beach stability, fewer food resources.
Smaller population sizes, shifts in distributions and possibly species interactions.
(good)
ΔΔ (moderate)
Nourishment
Mortality of fauna (crushing, burial), reduced habitat suitability.
Smaller population sizes, shifts in distributions and possibly species interactions.
(good)
(low)
Armouring (seawalls, groins, revetments, breakwaters)
Loss of habitat, increased rates of beach erosion and habitat instability.
Smaller population sizes, shifts in distributions and possibly species interactions.
(good)
ΔΔ (moderate)
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INVASIVE SPECIES
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URBANISATION'
Predation, possible competition for carrion.
Smaller population sizes, altered pop. structure
(good)
ΔΔ (moderate)
Invasive dune plants
Altered habitat quality and stability.
Altered population sizes and/or structure
(good)
ΔΔ (moderate)
Modified wrack composition and properties.
Unknown, but possibly negative if exotic wrack material lowers habitat use of strandline by ghost crabs.
(acceptable)
ΔΔΔ (high)
Fisheries
Overfishing of target species.
Smaller population sizes, altered pop. structure
(good)
ΔΔ (moderate)
Mining
Contamination and/or loss of habitat, direct mortality, habitat modification through exacerbated erosion.
Smaller population sizes, altered pop. structure, toxic effects
(good)
ΔΔ (moderate)
Exotic algae and seagrass species
EP
Exotic predators and feral animals
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1
Pressures and their environmental effects are adapted from Defeo et al. (2009) and Schlacher et al. (2007a; 2014a; 2008a; 2014b; 2006). Suitability as ecological indicator: – POOR (Responses to specific environmental change(s) or human activities IMPROBABLE because mechanistic links are biologically implausible or unknown); – ACCEPTABLE (Responses to specific environmental change(s) or human activities PLAUSIBLE, but mechanistic links are incompletely known in many cases); – GOOD (Responses to specific environmental change(s) or human activities are PROBABLE IN MOST CASES, consistent with expectations derived from known biological effects or mechanistic links).
3
Data Deficiency (Lack of Published Evidence for Ghost Crabs) ΔΔΔ – High (No published information on response(s) to specific pressures); ΔΔ – Moderate (Few (<3) papers documenting response(s) to specific pressures); Δ – Low (Three or more papers documenting response(s) to specific pressures).
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Electronic Appendix – Supplementary Material Table S1 Publications summarised in this paper that estimated the effects of human stressors on ghost crabs on ocean-exposed sandy beaches. 1
Species
Locality
Main 2 pressure(s)
(Florschuts and Williamson, 1978) (Fisher and Tevesz, 1979) (Wolcott and Wolcott, 1984) (Christoffers, 1986)
O. quadrata
USA, North Carolina
VEH
O. quadrata
URB#
O. quadrata
USA, North Carolina / Virginia USA, North Carolina
O. quadrata
USA, Maryland
URB#
(McGwynne, 1988)
O. ryderi, O. madagascariensis, O. ceratophthalma O. ryderi, O. madagascariensis, O. ceratophthalma O. quadrata
South Africa, KwaZulu Natal, Maputaland
VEH
(Peterson et al., 2000)
O. cordimanus
(Blankensteyn, 2006)
O. quadrata
(Moss and McPhee, 2006) (Neves and Bemvenuti, 2006) (Peterson et al., 2006)
USA, North Carolina
3
RI PT ABU
ABU, DIAM, CRUSH ABU, DIAM, DEPTH ABU
HARV
ABU
NOU
ABU
#
URB
ABU
URB#
ABU
O. cordimanus
Australia, New South Wales Brazil, Santa Catarina Island Australia, Queensland
VEH
ABU
O. quadrata
Brazil, Rio Grande do Sul
URB#
ABU
O. quadrata
USA, North Carolina
NOU
ABU
(Bisson, 2007)
O. quadrata
USA, Virginia
URB#
ABU
(Foster-Smith et al., 2007) (Maccarone and Mathews, 2007) (Schlacher et al., 2007c) (Barton and Roth, 2008) (De Araújo et al., 2008) (Hobbs et al., 2008)
O. spp.
Australia, Western Australia USA, Texas
VEH
ABU
URB#
ABU, DIAM, ORI
O. cordimanus, O. ceratophthalma O. quadrata
Australia, Queensland
VEH
ABU, DIAM, CRUSH
USA, Florida
PRED
ABU, DIAM
O. quadrata
Brazil, Espírito Santo
CLEAN
ABU, DIAM
O. quadrata
USA, Virginia
VEH
ABU, DIAM, LENGTH
O. quadrata
USA, Florida
NOU
ABU
O. cordimanus, O. ceratophthalma O. cordimanus, O. ceratophthalma, O. ryderi O. cordimanus, O. ceratophthalma O. cordimanus, O. ceratophthalma O. quadrata
Australia, Queensland
VEH
ABU, DIAM
Seychelles,
INV
ABU
Australia, Queensland
URB#
ABU, DIAM
Australia, Queensland
TRAMP
ABU, DIAM
Brazil, Bahia
URB#
ABU
O. cordimanus, O. ceratophthalma O. cordimanus, O. ceratophthalma
Australia, Queensland
URB#
ABU, DIAM
Australia, Queensland
VEH
ABU, DIAM, DEPTH, LENGTH, WEIGHT, ANGLE
TE D
(Barros, 2001)
South Africa, KwaZulu Natal
VEH
SC
(Robertson and Kruger, 1995)
Metric(s) ABU
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EP
O. quadrata
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(Irlandi and Arnold, 2008) (Thompson and Schlacher, 2008) (Brook et al., 2009)
(Lucrezi et al., 2009b) (Lucrezi et al., 2009a) (Magalhaes et al., 2009) (Lucrezi et al., 2010) (Lucrezi and Schlacher, 2010)
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O. cordimanus, O. ceratophthalma O. cordimanus, O. ceratophthalma
Australia, Queensland
VEH
Australia, Queensland
VEH
(Aheto et al., 2011)
O. africana, O. cursor
Ghana, Central Ghana
URB#
ABU, TRAIL, AREA, TURN ABU, DIAM, DEPTH, LENGTH, WEIGHT, ANGLE ABU, DIAM
(Schlacher et al., 2011a) (Noriega et al., 2012)
O. cordimanus
Australia, Queensland
CAM
ABU, DIAM, BCI
Australia, Queensland
URB#
ABU, DIAM
(Ocaña et al., 2012)
O. cordimanus, O. ceratophthalma O. quadrata
Cuba, NE Coast
URB#
ABU
(Guilherme, 2013)
O. quadrata
Brazil, Paraná
CLEAN
ABU, DIAM
(Lucrezi et al., 2014)
South Africa, KwaZuluNatal
VEH
ABU, DIAM
(Peterson et al., 2014)
O. ceratophthalma, O. madagascariensis, O. ryderi O. quadrata
USA, North Carolina
NOU
(Jonah et al., 2015)
O. africana, O. cursor
Ghana, Cape Coast
MINE
(Lim and Yong, 2015)
O. ceratophthalma
Singapore,
OIL
SC
1
RI PT
(Schlacher and Lucrezi, 2010a) (Schlacher and Lucrezi, 2010b)
ABU
ABU, DIAM ABU
Criteria for inclusions were that a) some form of peer review was likely to have been in place, and b) that at least means for
2
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controls and reference conditions could be extracted from a publication to estimate effects sizes for at least one variable. - CLEAN - cleaning / grooming (manual and mechanical); HARV - harvesting, subsistence fishing; INV - invasive species
(plants); MINE - mining for beach sand; NOUR - nourishment, re-profiling, beach bulldozing etc.; OIL - oil spill; PRED - predator control (racoon culling); TRAMP - trampling (short-term, intense); URB - 'urbanisation & recreation' (includes shore armouring, trampling, dune conversions, erosion etc.); VEH - vehicles (ORV - off-road vehicles, 4WD - four wheel drives, quad bikes, etc.). 3
- ABU - Abundance (density) of burrow openings at the beach surface; ANGLE - inclination of main shaft of burrow; BCI - Body
Condition Index; CRUSH - mortality caused by vehicles; DEPTH - vertical penetration of burrow into the sediment; DIAM diameter of burrow opening at / close to beach surface; HOME - size of daily home range; LENGTH - dimension of longest axis
TE D
of burrow; ORI - orientation of main shaft / compass direction; TRAIL - length of trails between turns during nocturnal movement; TURN - number of turns in movement path during nocturnal activity; WEIGHT - of burrow cast made with plaster of Paris or similar. #
-‘urbanisation’ is used as a collective term, intended to encompass multiple pressures associated with the intensive human use
EP
of beaches and development of dunes backing beaches. Because in many cases, two or more threats are spatially superimposed (e.g. sections of beach with seawalls are usually more heavily trampled than non-armoured sections) or pressures act sequentially or repeatedly (e.g. beach cleaning activities alternating with recreational use), past study designs failed to identify the effects of individual pressures un-confounded from other.
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ACCEPTED MANUSCRIPT Mitigating threats to sandy beaches requires accurate assessments of condition.
2.
Ghost crabs are widely used as indicator species in ecological beach assessments.
3.
Human impacts detected with ghost crabs are globally evident for sandy shores.
4.
Applied conservation needs experiments that yield defensible cause-effect evidence.
5.
Priority areas are acoustic and light pollution, debris, climate change effects.
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S0272-7714(15)30147-5
DOI:
10.1016/j.ecss.2015.11.025
Reference:
YECSS 4964
To appear in:
Estuarine, Coastal and Shelf Science
Received Date: 23 October 2015 Revised Date:
20 November 2015
Accepted Date: 28 November 2015
Please cite this article as: Schlacher, T.A., Lucrezi, S., Connolly, R.M., Peterson, C.H., Gilby, B.L., Maslo, B., Olds, A.D., Walker, S.J., Leon, J.X., Huijbers, C.M., Weston, M.A., Turra, A., Hyndes, G.A., Holt, R.A., Schoeman, D.S., Human threats to sandy beaches: A meta-analysis of ghost crabs illustrates global anthropogenic impacts., Estuarine, Coastal and Shelf Science (2015), doi: 10.1016/ j.ecss.2015.11.025. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
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3 4 5 6
* SCHLACHER, Thomas A. School of Science and Engineering, The University of the Sunshine Coast, Q-4558 Maroochydore, Australia; [email protected]
7 8 9
LUCREZI, Serena TREES—Tourism Research in Economic Environs and Society, North-West University, Potchefstroom, South Africa; [email protected]
10 11 12
CONNOLLY, Rod M. Australian Rivers Institute - Coast & Estuaries, and School of Environment, Gold Coast Campus, Griffith University, Queensland, 4222, Australia; [email protected]
13 14 15
PETERSON, Charles H. Institute of Marine Sciences, University of North Carolina, Chapel Hill, Morehead City, NC 28557, USA; [email protected]
16 17 18
GILBY, Ben L. School of Science and Engineering, The University of the Sunshine Coast, Q-4558 Maroochydore, Australia; [email protected]
19 20 21
MASLO, Brooke Department of Ecology, Evolution and Natural Resources Rutgers, The State University of New Jersey; [email protected]
22 23 24
OLDS, Andrew D. School of Science and Engineering, The University of the Sunshine Coast, Q-4558 Maroochydore, Australia; [email protected]
25 26 27
WALKER Simon J. School of Science and Engineering, The University of the Sunshine Coast, Q-4558 Maroochydore, Australia; [email protected]
28 29 30
LEON, Javier X. School of Science and Engineering, The University of the Sunshine Coast, Q-4558 Maroochydore, Australia; [email protected]
31 32 33
HUIJBERS, Chantal M. School of Science and Engineering, The University of the Sunshine Coast, Q-4558 Maroochydore, Australia; [email protected]
34 35 36
WESTON, Michael A. Centre for Integrative Ecology, School of Life and Environmental Sciences, Deakin University, Burwood, VIC 3125, Australia; [email protected]
37 38 39
TURRA, Alexander Departamento de Oceanografia Biológica, Instituto Oceanográfico, Universidade de São Paulo, Praça do Oceanográfico, 191, CEP 05508-120 São Paulo, SP, Brasil; [email protected]
40 41
HYNDES, Glenn A. Centre for Marine Ecosystems Research, Edith Cowan University, WA, Australia; [email protected]
42 43 44
HOLT, Rebecca A. Australian Rivers Institute - Coast & Estuaries, and School of Environment, Gold Coast Campus, Griffith University, Queensland, 4222, Australia; [email protected]
45 46 47
SCHOEMAN, David S. School of Science and Engineering, The University of the Sunshine Coast, Q-4558 Maroochydore, Australia; [email protected]
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* corresponding author: [email protected]
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Human threats to sandy beaches: A meta-analysis of ghost crabs illustrates global anthropogenic impacts.
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Abstract
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1.
Human Beach Impacts
Beach and coastal dune systems are increasingly subjected to a broad range of anthropogenic pressures that on many shorelines require significant conservation and mitigation
52
interventions. But these interventions require reliable data on the severity and frequency of
53
adverse ecological impacts. Such evidence is often obtained by measuring the response of
54
‘indicator species’.
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2.
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Ghost crabs are the largest invertebrates inhabiting tropical and sub-tropical sandy shores and are frequently used to assess human impacts on ocean beaches. Here we present the first
57
global meta-analysis of these impacts, and analyse the design properties and metrics of
58
studies using ghost-crabs in their assessment. This was complemented by a gap analysis to
59
identify thematic areas of anthropogenic pressures on sandy beach ecosystems that are
60
under-represented in the published literature. 3.
Our meta-analysis demonstrates a broad geographic reach, encompassing studies on shores
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of the Pacific, Indian, and Atlantic Oceans, as well as the South China Sea. It also reveals what
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are, arguably, two major limitations: i) the near-universal use of proxies (i.e. burrow counts to
64
estimate abundance) at the cost of directly measuring biological traits and bio-markers in the
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organism itself; and ii) descriptive or correlative study designs that rarely extend beyond a
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simple ‘compare and contrast approach’, and hence fail to identify the mechanistic cause(s) of
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observed contrasts.
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Evidence for a historically narrow range of assessed pressures (i.e., chiefly urbanisation, vehicles, beach nourishment, and recreation) is juxtaposed with rich opportunities for the
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broader integration of ghost crabs as a model taxon in studies of disturbance and impact
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assessments on ocean beaches. Tangible advances will most likely occur where ghost crabs
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provide foci for experiments that test specific hypotheses associated with effects of chemical,
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light and acoustic pollution, as well as the consequences of climate change (e.g. species range
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shifts).
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Key-words: meta-analysis; ecological indicator species; sandy shores; coastal dunes; impact
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assessments; Hoplocypode; Ocypode.
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1. Introduction
81
“I'll try you on the shore”
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William Shakespeare: Antony and Cleopatra (1606) Accelerating environmental impacts on ocean beaches and coastal dunes call for effective
84
environmental planning and biological conservation. These interventions should meet two cardinal
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criteria: 1.) environmental values and conservation goals must be clearly identified for broad and
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inclusive segments of the population (Harris et al., 2014; Vivian and Schlacher, 2015); and 2.)
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management decisions must be based on impact assessments that produce defensible and
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biologically relevant information (Harris et al., 2015).
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A sizeable part of this information comes from documenting the response of organisms (at various
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levels of ecological organisation ranging from individuals to ecosystems) to human activities or
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anthropogenic habitat change (Defeo et al., 2009; Schlacher et al., 2007a). On ocean shores, a broad
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range of animals (e.g. benthic invertebrates, birds, marine turtles) has been used to detect biological
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effects attributed to an equally diverse spectrum of anthropogenic pressures, ranging from vehicle
95
impacts to urbanisation (e.g. Huijbers et al., 2015b; Marshall et al., 2014; Reyes-Martínez et al., 2015;
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Walker and Schlacher 2011).
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Ghost crabs (Genera Ocypode and Hoplocypode) are perhaps the most widely-studied invertebrate
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indicator species on ocean-beaches (e.g. Barros, 2001). Ghost crabs are attractive as ecological indicators for a number of reasons: i) they are widespread in the subtropics and tropics; ii) they occur
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on both the non-vegetated beaches and in the dunes backing beaches; iii) they are relatively large,
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often locally abundant, arguably charismatic, and require no specialised tools to sample; iv) their
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taxonomy is well known and identification not overly difficult; and v) they construct semi-permanent
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burrows with clearly visible openings at the beach surface (Lucrezi and Schlacher, 2014; Schoeman et
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al., 2015). It is the fossorial habits of ghost crabs, in particular, that has led to their widespread
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adoption as ecological indicators, chiefly because estimates of abundance and body size can be made
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from counts and measurements of burrow sizes without the need to physically collect the organisms
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(Barros, 2001).
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Given the extensive use of ghost crabs as ecological indicators on ocean beaches, a formal review and
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meta-analysis of this practice is warranted. To this end, here we synthesise the literature and address
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five broad questions:
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1) What are the types of human pressures acting on beach-dune systems that have been assessed with
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ghost crabs?
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2.) What is the magnitude of reported ecological effect sizes for different stressors?
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3.) Which metrics (response variables) have been used?
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4.) What are the gaps in terms of human pressures currently not adequately assessed using ghost
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crabs?
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5.) What opportunities exist to advance the use of ghost crabs as ecological indicators on ocean
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beaches?
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2. Methods
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Studies that examined the response of ghost crabs to anthropogenic activities (sensu lato) were
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obtained by first searching the Web of Science, Scopus, and Google Scholar using “ghost crabs” OR
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“Ocypode OR Hoplocypode ” as key words. From this pool we identified studies reporting on human
125
impact assessments by reading the original documents. Sources from literature searches were
126
supplemented by examining the cited reference lists of publications in hand; this yielded several
127
additional reports from government agencies (e.g. U.S. Fish & Wildlife Service, Natal Parks Board). No
128
filter was applied with respect to the types of impacts. Nevertheless, all studies were required to meet
129
two minimum criteria for inclusion in the meta-analysis: peer-review or an equivalent quality control
130
was likely to have been completed, and quantitative data on changes / differences of at least one
131
response variable could be extracted from a publication (e.g. contrasts in burrow counts between
132
beach sections with and without vehicle traffic). In all cases, we classified the intensity of human use or
133
habitat modification by following the original descriptions provided by the authors of each study,
134
usually representing a ‘high impact/use treatment’ condition that was compared with a ‘low
135
use/reference/control’ condition. In most cases it was not possible to quantify or rank the intensity or
136
level of pressure from the original descriptions; hence, all analyses here are performed using a binary
137
classification of ‘impact’ vs. ‘reference’, irrespective of differences in impact intensity that may have
138
existed among studies.
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We quantified the magnitude of effects on measured ghost crab biological metrics by using the log-
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response ratio, lnR, which is a common statistic of ecological effect sizes in meta-analyses:
142
lnR = ln(mean impact / mean control)(Borenstein et al., 2009). ‘Impact’ refers to sites or beaches that were
143
categorised by authors as being evidently more influenced by a particular human stressor of interest
144
and hence usually represent values from ‘impact’ groups or ‘treatments’. Conversely, ‘control’ values
145
usually represent localities where the stressor of interest was judged (by the original study authors) to
146
be substantially less influential or absent and hence represent ‘reference conditions’ in the context of
147
individual studies. Half of the studies in our database did not report sufficient details on samples sizes,
148
variances, statistical tests used, or P-values; in other papers these statistics could not be reliably
149
extracted or inferred from graphs or tables. These omissions precluded the calculation of standardised
150
effect-size statistics such as Cohen’s d and Hedges’ g (Harrison, 2011) for the majority of studies. For
151
these reasons, we limit our analysis to unweighted one-sample t-tests of the hypothesis that the mean
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log-response ratio is 0 (i.e., that there is, on average, no effect; raw response ratio = 1).
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The term ‘indicator species’ has multiple meanings in ecology and environmental science, with little or
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no consistency of usage amongst authors. Broadly, five main types of usage can be identified to: 1.)
156
measure the biological responses to anthropogenic stressors, pollutants, human activities,
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management actions, or restoration efforts (i.e. ‘indicator species’ are used as biological monitors that
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are thought to react in predictable ways to changes in the environment) (Carignan and Villard, 2002; Page | 4
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Diekmann and Dupré, 1997; Jonsell and Nordlander, 2002; Krmpotić et al., 2015; Siddig et al., 2016); 2.)
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characterize assemblages or habitats (i.e. ‘indicator species’ are those that are viewed as 'typical'
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species, showing consistent fidelity to a set of biological or environmental attributes) (Antonelli et al.,
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2015; De Cáceres et al., 2010; Dufrêne and Legendre, 1997; Hogle et al., 2015; Hwang et al., 2015;
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Peterken, 1974; Ricotta et al., 2015; Sarrazin et al., 2015); 3.) reflect more than one process, condition,
164
or biological attribute that may or may not be linked to human interventions (i.e. ‘indicator species’
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serve as multiple proxies, the specific meaning being often dependent on the study context)
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(Lindenmayer, 1999; Niemi et al., 1997; Regehr and Montevecchi, 1997); 4.) act as surrogates for
167
species that are difficult to detect or sample or to reflect specific environmental conditions (i.e.
168
‘indicator species’ are functionally closely associated with other species or environmental attributes
169
required by those species) (Pérez-García et al., 2015; Schaefer and Hocking, 2015; Turner and McGraw,
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2015; Weaver, 1995); and 5.) serve as surrogates for biodiversity at the assemblage or ecosystem level
171
(i.e. ‘indicator species’ are surrogates for biological diversity at higher levels of ecological organisation)
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(Morelli, 2015). Historically, indicator species were often used in the context of biodiversity surrogates
173
or being other proxies, whereas modern studies predominantly use indicator species to describe
174
habitats or assemblages, or to assess biological effects of environmental change, generally linked to
175
human stressors (Siddig et al., 2016). In this paper the term ‘indicator species’, as applied to ghost
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crabs, represents usage to assess anthropogenic threats and environmental change.
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3. Results
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3.1 Coverage, Variables, Replication, Scale
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In terms of geographic provenance, just over half (53%) of studies are from Atlantic beaches, nearly a
182
third from the Pacific (32%), with the remainder coming from the Indian Ocean (13%), and the South
183
China Sea (3%; Table 1, Fig. 1). Papers from Australia (34%) and the USA (32%) make up the bulk of
184
publications examining human impacts on ghost crabs, complemented by significant contributions
185
from Brazil (13%) and South Africa (8%; Table 1). All studies reviewed here were conducted in the
186
tropics (74%) and subtropics (26%), with the average latitude being 26.1º (s = 9.35º; Fig. 1). With
187
respect to usage as an ecological indicator, Ocypode quadrata was most often studied (18 studies),
188
followed by O. cordimanus (13) and O. ceratophthalma (10); other species, including Hoplocypode
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occidentalis, the single species in this genus, are rarely used. Low coverage of species in the literature
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should, however, not be interpreted as inferring that certain under-sampled species perform more
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poorly as ecological indicators.
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The number of response variables measured per study is limited. Most authors measured only one
194
(47%) or two (29%) variables, usually abundance and diameter of burrow openings (Table 1). We also
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found a surprisingly narrow range of the type of variables measured by authors and a dominance of
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indirect proxies. Indeed, only four of the 38 studies reviewed by us have measured the response of
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ghost crabs to human disturbance directly, rather than extrapolating from proxies related to burrow
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metrics. Schlacher and Lucrezi (2010a) tracked crabs to test whether disturbance by vehicles affected
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home-range size and habitat use. Body condition of individuals was used to predict the availability
200
and quality of food resources, as this metric indicates altered trophic conditions for ghost crabs, as
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occurs where food scraps are discarded by campers in coastal dunes abutting beaches (Schlacher et
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al., 2011a). Wolcott and Wolcott (1984) and Schlacher et al. (2007c) used an experimental approach to
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measure the rate at which vehicles driven on beaches injure and crush individuals, both whilst crabs
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were inside burrows at various depths and whilst they were active on the beach surface at night.
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All study designs contained some element of spatial replication. On average, five sites were sampled
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(se = 0.67), ranging up to a maximum of 21 sites (Schlacher et al., 2011a). However, half of the studies
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sampled fewer than four sites, with ten studies (26 %) having sampled two sites only (mostly a classic
209
unreplicated 'compare and contrast' approach), and eight studies (21 %) having examined three sites.
210
The mean spatial extent over which sites were dispersed was relatively large at 39 km (se = 11). This
211
statistic is, however, attributable to three studies that had sites extending over 200 km or farther: i)
212
Barros (2001) assessed the effects of seawalls on urban beaches in south-eastern Australia, measuring
213
burrow densities on three beaches dispersed along ca. 310 km of coast; ii) Ocaña et al. (2012)
214
estimated the consequences of coastal development for ghost crabs at eight beaches along 200 km of
215
the NE coast of Cuba; iii) Fisher and Tevesz (1979) worked over a similar spatial range, surveying the
216
response of O. quadrata to urbanisation and trampling at 13 sites ranging over 200 km from Cape
217
Henry, Virginia to Cape Hatteras, North Carolina. Notwithstanding a few relatively large-scale designs,
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half of the studies were completed over less than 15 km. Small-scale (<10 km) studies are not
219
uncommon in the ghost crab literature: 7 papers (18 %) sampled sites covering less than 1 km and
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15 papers (39 %) surveyed sites over less than 10 km.
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Ten studies (26 %) were ‘spot measurements’, lacking temporal replication in their design. In studies
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that made repeated estimates of ghost crab responses, the average number of temporal replicates
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was 8.89 (se = 1.28), ranging up to 27 temporal replicates (Lucrezi et al., 2010). Studies that were
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particularly well replicated in time include: Moss and McPhee (2006) assessed vehicle effects on ghost
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crabs in Eastern Australia (n = 20); Peterson et al. (2014) quantified the consequences of beach
227
nourishment in North Carolina (n = 20); and Irlandi and Arnold (2008) report on nourishment effects
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in Florida (n = 22). The average duration of temporally replicated impact studies was 180 days
229
(se = 53), and only four studies spanned less than a week. By contrast, the duration of four studies was
230
close to a year or longer: Robertson and Kruger (1995) who gauged the effects of artisanal fisheries on
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ghost crabs in South Africa (330 days), and Christoffers’ (1986) work on the effects of recreational
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activities at Assateague Island (488 days). The two papers with the longest duration both dealt with
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nourishment impacts: Irlandi and Arnold (2008) spanning 640 days, and Peterson et al. (2014) lasting
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1370 days.
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3.2 Effect Sizes
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The reported responses of ghost crabs to human activities and associated habitat changes on beaches
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generally show consistently negative impacts of human pressures on the number of burrow openings
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(a proxy for abundance), but highly variable or non-significant effects on burrow diameter (a proxy for
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body size; Table 2; Fig. 2).
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Response ratios of abundance denote a significant (t = 6.32, df = 36, P < 0.001) mean density
243
decrease (lnR = -1.35 ± 0.21se),at impacted locations for all stressors combined (Table 2; Fig. 2); mean
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response ratios significantly smaller than unity are evident for the effects of vehicles (lnR = -
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1.42 ± 0.45se, P <0.01), nourishment (R = -1.27 ± 0.36se, P = 0.038), and urbanisation (R = -
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1.52 ± 0.30, P <0.001). Fewer individuals associated with more intense human use (e.g. more vehicles
247
or trampling) or greater habitat conversions (e.g. seawalls, development, nourishment) were reported
248
in 35 of the 37 papers that measured abundance (via burrow counts). Of the 26 studies (70%) that
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undertook some form of statistical test, or adequately described the results of such tests between
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control and impact conditions, 23 (88%) report significant differences in burrow counts between
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'impact' and ‘control’ sites, 21 studies (81%) reported fewer burrows, whilst only two studies (8%)
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reported more burrows associated with putative human pressures.
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In contrast to the largely significant and negative effects on crab abundance (assessed by proxy using
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burrow counts), responses of the diameter of burrow openings (a proxy for crab size) are inconsistent,
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both in terms of the direction and magnitude of responses to tested pressures (Table 2, Fig. 2).
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Although sample size was limited, the mean response ratio (lnR = -0.15 ± 0.09) suggests that burrows
258
tended to be slightly smaller at impacted sites. This effect was, however, not consistent among
259
studies. Thirteen out of 38 (34%) studies measured changes in burrow size, which allowed calculation
260
of response ratios. Of these, 12 (92%) tested for differences between mean diameter, with eight
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reporting significant differences in burrow diameter: two studies document smaller diameter burrows,
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whilst six document larger ones at impact sites (Table 2, Fig. 2).
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Limited (one or two papers depending on the type of pressure) information is available on abundance
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changes attributable to stressors other than vehicles, nourishment, or urbanisation. Notwithstanding
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this limitation, lower burrow counts appear to be associated with oil spills (lnR = -4.61), invasive plants
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(lnR = -2.81), subsistence harvesting (lnR = -0.42), mining (lnR = -0.97), and trampling (lnR = -0.14).
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Conversely, a greater number of burrows have been reported from dune areas frequented by campers
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(lnR = 0.44) and following human controls on the crabs’ predators (i.e. culling of racoons to protect
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turtle eggs and hatchlings; lnR = 0.38) (Barton and Roth, 2008).
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The three papers that measured variables other than the number and diameter of burrow openings
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report decreases in the extent of daily home range (lnR = -0.80), trail length (lnR = -0.31), burrow
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depth (lnR = -0.20), burrow volume (lnR = -0.11), and burrow angle (lnR = -0.36). A single paper
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describes a 50 % increase in body condition of crabs collected from camp grounds in dunes relative to
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reference sites without camping (Schlacher et al., 2011a).
277
3.3Addressing Pressures: Gaps and Opportunities
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In terms of how ghost crabs can be used to assess ecological effects arising from the main types of
280
human stressors acting on sandy beaches, six clusters emerge based on the degree of missing
281
information (‘data deficiency’) and the likely reliability of ghost-crabs as indicator species to deliver
282
these data (‘suitability’) in the future (Table 3, Fig. 3).
283
1.) Pressures that both lack data regarding their ecological impacts and can be readily addressed
284
using ghost crabs as suitable indicators in future studies: five aspects of pollution (artificial night light,
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chemical pollutants, marine debris, noise, and sewage) and warming of the atmosphere and oceans
286
associated with climate change.
287
2.) Pressures that lack data and can be gauged with ghost-crabs, albeit at slightly lower confidence or
288
scope than those in the first cluster: altered current regimes and upwelling under climate change, the
289
effects of invasive algae, and thermal-discharge impacts.
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3.) A broad suite of pressures for which some data on their ecological effects do exist (i.e. moderate
291
data deficiency) and for which ghost crabs would be good ecological indicators for future
292
assessments: urbanisation stressors (armouring, urbanisation, grooming), invasive carnivores and dune
293
plants, fisheries and mining impacts, and the consequences of sea-level rise and altered storm
294
regimes.
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4.) Three pressures that have both moderate data availability and can be measured with ghost crabs at
296
moderate levels of indicator performance: dune camping, recreational fishing, and trampling.
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5.) Ghost crabs are very well suited to assess the biological effects of vehicles and sand nourishment
298
on beaches and this is reflected by an adequate level of available information for these two pressures.
299
6.) Few or no data currently exist for the biological effects of ocean acidification, altered precipitation,
300
and motorised watercraft in beach systems; however, ghost crabs will rarely be the indicator taxon of
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first choice in impact assessments targeting these specific stressors (Table 3, Fig. 3).
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4. Discussion
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4.1 Time for New Directions?
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A sizeable body of evidence is now available that strengthens arguments for the use of ghost crabs as
307
indicator species to assess the biological and ecological consequences of human activities and habitat
308
changes on sandy beaches (Table 1, Fig. 2). In addition, there is a reasonably broad geographic
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distribution of published studies (Fig. 1) and coverage of issues (Fig. 2), suggesting that the use of Page | 8
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ghost crabs as ecological indicator species is widely applicable and versatile. Much of this reach stems
311
from the ease with which population estimates can be made by counting burrow entrances. However,
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what is – in a technical sense – a fortuitous trait of ghost crabs, has also led to a prevalence of simple
313
‘compare and contrast designs’ that usually fail to measure response variables of the organisms
314
directly, instead relying overwhelmingly on burrow numbers and sizes as proxies (Table 1).
315 Notwithstanding the broad usage of the technique, there are, in our opinion, five new directions that
317
future environmental studies using ghost crabs should take. 1.) Establishing the mechanistic links that
318
account for observed spatial contrasts (‘processes’). 2.) Adopting more diverse designs, especially
319
those that encompass experiments aimed at discerning causality in the relationship between
320
functional responses and the intensity and nature of putative stressors on one hand, and the resulting
321
biological effects on the other (‘dose-response studies’). 3.) Separating individual causative agents
322
among suites of putative predictors (‘specificity and un-confounding’). 4.) Including modern genetic,
323
bio-chemical and physiological biomarkers and assays that reflect the state of the art in ecotoxicology
324
and behavioural ecology. 5.) Broadening the scope of environmental pressures that are addressed in
325
future impact assessments using ghost-crabs as “canaries in the mine” (‘scope and thematic ambit’).
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Resolving the first four issues above will essentially be a question of aligning ghost-crab studies with
328
modern statistical and eco-toxicological design principles that will yield more robust and reliable
329
attribution and inference. Expanding the thematic ambit to be truly reflective of the diverse nature of
330
anthropogenic stressors acting on sandy beach and dune systems is potentially a very large
331
undertaking, but offers, in our opinion, rich opportunities - we sketch these prospects and their
332
rationale in the following sections.
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4.2 Addressing Significant Anthropogenic Beach Stressors Using Ghost Crabs as
335
Indicators
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4.2.1 Climate-Change-Associated Effects: Sea-level rise, Warming, Current and Rainfall
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Changes, Ocean Acidification
339
Beaches are malleable and dynamic landscapes, responding readily to changes in external physical
340
forcing (Schlacher et al., 2015b). The key physical beach controls that are modified by climate change
341
are accelerated sea-level rise (IPCC, 2013), altered wave and large-scale weather regimes (Barnard et
342
al., 2015; Hemer et al., 2013; Johnson et al., 2015), possibly augmented by storminess (Emanuel, 2013).
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These can have dramatic impacts on beach and dune geomorphology, resulting in greater erosion and
344
shoreline retreat, and more widespread and frequent coastal flooding during storms (Johnson et al.,
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2015; Woodruff et al., 2013).
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Changes to the beach and coastal morphology attributable to global change can be accurately
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consequences of these habitat alterations are less well understood; in this context, ghost crabs can be
350
useful indicators to gauge these consequences. For example, it is possible that local populations of
351
ghost crabs will become extinct in extreme cases of beach or dune erosion, especially where the upper
352
beach habitat near the strandline is lost and where high and persistent beach scarps are formed that
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block movement of crabs between the non-vegetated beach and the dunes. Local extirpations of
354
invertebrates inhabiting the upper beach and lower dunes have already been reported for Californian
355
beaches under high urbanisation pressure (Hubbard et al., 2014). Ghost crabs may respond in a similar
356
fashion on sub-tropical and tropical beaches that have undergone recent extreme or repeated erosion
357
events: such effects may be exacerbated by delayed recovery on beaches with seawalls or similar
358
structures on the landward margin (Lucrezi et al., 2010).
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Rising temperatures associated with climate change are predicted to cause a broad range of biological
361
and ecological responses in marine organisms, including altered physiology, phenology, demography,
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behaviour, and shifts in distributions and species ranges (Burrows et al., 2014; García Molinos et al.,
363
2015; Poloczanska et al., 2013; Sunday et al., 2015). We predict that several of the temperature effects
364
recorded in other marine species at the land-ocean interface will be detectable in ghost crabs, and
365
these can be tested experimentally. In fact, ghost crabs are good model organisms for such tests
366
because they are abundant, widespread, usually not of significant or legal conservation concern, and
367
relatively large bodied. These traits particularly favour their use in physiological studies (laboratory
368
and field-based) and in investigations examining geographic range shifts of beach species (Schoeman
369
et al., 2015). Interestingly, temperature will likely also affect larvae by increasing metabolic and
370
therefore development rates – earlier metamorphsis is likely to result, potentially reducing time in the
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plankton, and therefore dispersal (Gerber et al., 2014; O'Connor et al., 2009).
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Altered oceanographic current regimes and greater variability or intensity in oceanographic forcing,
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such as upwelling (Black et al., 2014; Sydeman et al., 2014), may affect the dispersal and survivorship
375
of larvae, and are predicted to modify the geographic patterns and magnitude of ghost-crab
376
recruitment onto beaches. It is certainly feasible to measure recruitment dynamics in relation to
377
changes in oceanographic forcing, and this can be combined with genetic work to examine changes in
378
connectivity amongst populations and beaches (e.g. Austin et al., 2015). Effects associated with altered
379
primary productivity, upwelling intensity, or the availability of marine carrion deposited on the shore
380
may be more varied, but some expectations are plausible. Ocean currents, and their nearshore
381
compensatory counter-currents, are more important in terms of dispersal of recruits, whereas storms
382
are more likely to generate wrack and carrion. One interesting exception here is the eastern boundary
383
current upwelling systems, with evidence suggesting upwelling might intensify, and perhaps shift
384
poleward (Sydeman et al., 2014; Wang et al., 2015). Ghost crabs currently do not occur in sizeable
385
numbers on beaches bordering some of the strongest and most persistent eastern boundary
386
upwelling areas, except in the Humboldt (Lucrezi and Schlacher, 2014). Thus, shifts in ghost crab
387
distributions may be a sensitive indicator to gauge the broader ecological impacts of altered
388
upwelling for sedimentary shore ecosystems.
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Notwithstanding uncertainties and large geographic variation in response, higher rainfall is possible in
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response to climate change (Thorpe and Andrews, 2014). Plausible consequences for beach and dune
392
systems are altered dune vegetation (e.g. increased cover, shifts in species composition) and changes
393
in aquifers underlying dunes and beaches (e.g. increased height of water table, wider low-salinity
394
zones in the intertidal, increased discharge of groundwater to surf-zones) (Feagin et al., 2005; Werner
395
et al., 2013). Both are expected to affect ghosts crabs, and several predictive hypotheses can be tested
396
in the future: i) moderate increases in vegetation cover may enhance habitat stability of dunes, leading
397
to increased population abundance of crabs; ii) very dense vegetation, especially species with
398
extensive root networks, will impede burrowing and lead to lower crab abundance; iii) because crabs
399
avoid constructing burrows that reach the water table, higher ground-water levels might limit crab
400
populations (this effect is hypothesized to be strongest at the poleward edge of the range where deep
401
burrows are thought to provide a thermal refuge during winter; Schoeman et al., 2015).
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Ocean acidification has profound and varied impacts at multiple levels of biological and ecological
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organisation; it affects organismal physiology, health, growth, survivorship, and abundance, and these
405
effects can propagate to changes at the assemblage and system scale (Byrne and Przeslawski, 2013;
406
Gaylord et al., 2015; Kroeker et al., 2013; Nagelkerken and Connell, 2015). Acidification is predicted to
407
affect ghost crabs during their larval phase, which could depress recruitment to beaches if growth
408
and/or survivorship are impaired. Recruitment could be monitored, but it is unlikely that this would be
409
considered an efficient variable to measure to assess the effects of ocean acidification in beach
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ecosystems.
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4.2.2 Recreation Effects: Vehicles, Trampling, Camping, Motorised Watercraft,
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Recreational Fishing & Bait Collecting
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The environmental impacts of vehicles on beach-dune ecosystems are mostly well documented. A
415
solid body of evidence clearly demonstrates widespread, and often massive, environmental harm
416
caused by vehicles driven on beaches and in dunes, including adverse impacts on ghost crabs (Groom
417
et al., 2007; Moss and McPhee, 2006; Schlacher et al., 2013c; Walker and Schlacher 2011). Vehicle
418
effects are also among the few stressors for which the mechanisms of impacts (i.e. crushing, collisions
419
with wildlife) have been identified or quantified (Schlacher and Lucrezi, 2010b; Schlacher et al., 2007c;
420
Schlacher et al., 2008b). What is generally not known, but of great importance to management and
421
conservation, are the thresholds of use (e.g. traffic volumes, allowed vehicle types, distribution across
422
shores) above which negative biological effects rise steeply or become irreversible (Schlacher et al.,
423
2008b). In this context, more and better-designed impact studies that determine the ‘dose-response
424
curves’ for ghost crabs and other beach species (including charismatic flagship species such as turtles
425
and birds provided that ethical and permitting issues can be overcome for these vertebrates) for a
426
variety of stressors are a critical information gap to inform ecologically responsible management
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actions.
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Trampling is a near-ubiquitous disturbance agent in sandy shore systems, having multiple effects on
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biota. These effects have been documented for species and assemblages in both the dunes (Brunbjerg
431
et al., 2014) and the non-vegetated beach seawards of the dunes (Reyes-Martínez et al., 2015;
432
Schlacher and Thompson, 2012). Surprisingly, given how common trampling is on many shores
433
worldwide, only a single paper has examined the short-term changes to ghost-crab burrow density
434
and size distribution following intense trampling by people on an urban beach (Lucrezi et al., 2009a).
435
Effects were small and crabs do not appear to be strongly affected by intense trampling over a period
436
of three days (Lucrezi et al., 2009a). Effects may well be stronger if trampling is particularly extreme at
437
small scales (~100m ; e.g. beach volleyball games) or sustained over much of the year (Turra et al.,
438
2005). Several papers have ostensibly measured the effects of 'trampling', but tests are invariably
439
confounded with other stressors superimposed at the same site, most often shore armouring and
440
urbanisation of the supratidal and the dunes. Thus, carefully designed studies are needed that
441
separate the impacts caused by trampling from other human pressures.
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Camping in coastal dunes close to beaches is a popular leisure activity. Whilst the environmental
444
impacts of ‘beach-camping’ are likely to be diverse, significant clearing of vegetation and vehicle-
445
associated impacts (e.g. tracks, erosion) are the most prominent and frequent adverse effects. Food
446
discarded by campers can provide additional resources for ghost crabs and other scavengers
447
(Schlacher et al., 2011a); whether this is a benign, positive, or negative practice is debatable and will
448
largely depend on the population of scavengers that is ‘subsidised’ (i.e. larger numbers of crows,
449
foxes, or racoons attracted to campground are predicted to increase predation pressure on ground-
450
nesting shorebirds and possibly also on ghost crabs). Populations of ghost crabs in dunes are
451
negatively impacted by vehicle tracks (Schlacher et al., 2011a), whilst benefiting – in terms of better
452
body condition - from food subsidies (Schlacher et al., 2011a). This illustrates that applications of
453
ghost crabs in environmental assessments can fruitfully extend beyond simple burrow counts. For
454
example, they may encompass tissue stable isotope measurements to test for the uptake of fecal
455
matter deposited by beach campers or the tissue analysis of hydrocarbons typical of off-road vehicle
456
emissions (Schlacher pers. obs.).
457
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The use of personal motorised watercraft (e.g. jet skis, water scooters, inflatable boats) in the surf-
459
zone is a popular leisure activity globally. However, there are numerous, often severe, environmental
460
consequences arising from this practice, poignantly summarised by Josephson (2007): “These
461
machines cannot be operated without loss of life or habitat”. Broad types of environmental impacts
462
encompass direct strikes on wildlife, bioacoustic impacts on fauna, chemical pollution (fuel spillages,
463
exhaust emissions, antifouling paints), and alterations to wave climates and turbidity (Erbe, 2013;
464
Whitfield and Becker, 2014). Ghost crabs generally enter the surf-zone only when gravid females
465
release eggs in the swash. Thus, impacts of watercraft on ghost crabs are expected to be much smaller
466
than for truly marine species (e.g. mammals, fish, and seabirds). However, chemical pollution arising
467
from motorised watercraft may be evident, as may be habitat changes from enhanced wave-driven Page | 12
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468
beach erosion, crushing of crabs during launching and retrieval of boats and jet skis, and bioacoustic
469
impacts.
470 Beaches, especially their surf-zones, are important sites for coastal fisheries (Gutiérrez et al., 2011;
472
McLachlan et al., 1996). Many beach fisheries are small-scale (artisanal, subsistence), particularly in
473
less-developed countries, but recreational angling is widespread irrespective of socio-economic
474
conditions (Sowman, 2006). Where ghost crabs are harvested as part of subsistence fisheries, they are
475
susceptible to population impacts that can be measured using standard fishery-assessment
476
techniques (Kyle et al., 1997). On beaches without direct harvests of ghost crabs, ecological impacts
477
caused by fishing may still be detectable. Because a large fraction (on some beaches the vast majority)
478
of beach vehicle traffic is attributable to recreational fishers, impacts on ghost crabs often arise
479
indirectly from shore-based angling via vehicles. Discards of bait, by-catch, and fish frames are readily
480
consumed by birds on beaches (Rees et al., 2014). Consequently, it is possible that carrion subsidies
481
provided by fisherman enhance food intake in ghost crabs in similar ways. Arguably, this may be a
482
positive effect. Conversely, discarded fishing line may kill individuals that become entangled in it.
483
Hypotheses concerning impacts of carrion subsidy or fishing-line mortality have not been tested for
484
ghost crabs to date.
485
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4.2.3 Pollution: Sewage and Storm-water, Debris, Thermal discharges, Chemicals,
487
Noise, Artificial Night Light
488
Contamination of beaches with sewage and storm-water is a worldwide problem. The issue is regularly
489
managed for human health risks (Brownell et al., 2007; Sabino et al., 2014), but very rarely in the
490
context of its biological impacts (Mearns et al., 2014; Schlacher et al., 2006). Disregarding the broader
491
environmental consequences of sewage inputs to dunes and beaches ignores, however, the facts that
492
transfers of sewage-derived matter to beach invertebrates has been demonstrated on ocean shores
493
(Schlacher and Connolly, 2009), and that wastewater can have numerous detrimental impacts on the
494
health of organisms (Ings et al., 2012; Schlacher et al., 2007b). Ghost crabs are likely to be exposed to
495
human waste material via direct contact with solid waste and via water-borne material contained in
496
the aquifer and, to a small degree, the swash. Because pathogens (viruses, bacteria, fungi) and
497
xenobiotics are not restricted to the water, but are also found in beach sands (Sabino et al., 2014), the
498
intense contact of crabs with the sediment during burrow construction and maintenance and feeding,
499
increases the likelihood of exposure, uptake, and detrimental effects. A broad arsenal of biomarkers
500
(e.g. genetic, hormonal, immunological, cytological, enzymatic, histological) is available to assess such
501
health effects (e.g. Gillis et al., 2014), but surprisingly, biomarkers in ghost crabs have not been used
502
for ecological assessments; this line of enquiry thus offers multiple opportunities to better assess the
503
status of dune and beach systems in biologically more meaningful ways using a suite of different
504
biomarkers.
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Man-made debris, mostly plastics, is now one of the most common, widespread and persistent
507
pollutants in marine waters and beaches worldwide (Moore, 2008). The last decade has seen an
508
exponential rise in the number of scientific papers examining the biological impacts of marine debris,
509
reflecting a growing recognition of severe environmental harm arising mostly from plastics (Gall and
510
Thompson, 2015). Detrimental effects of larger marine debris on marine wildlife are often dramatic
511
(e.g. whales entangled in fishing nets, turtles succumbing from ingested plastic bags, seabirds
512
ingesting large volumes of floating plastics) (Vegter et al., 2014). Evidence is also rapidly accumulating
513
that smaller debris, microplastics (< 5 mm), has equally deleterious effects in a broad range of marine
514
organisms, ranging from toxicant magnification to incorporation of microspheres into consumers’
515
tissues (Ivar Do Sul and Costa, 2014; Law and Thompson, 2014). Beaches are deposition sites for
516
floating marine debris, accumulating both larger litter items and high concentrations of microplastics
517
up to 2 m deep into the sediments (Fisner et al., 2013; Turra et al., 2014). Alarmingly, beach deposits
518
can contain the toxic break-down products of styrofoam in large quantities (Kwon et al., 2015).
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Accurately measuring and predicting the environmental risks that marine debris poses for wildlife is a
521
research priority for beaches and beyond (Brennecke et al., 2015; Vegter et al., 2014). Because beaches
522
are prime sites for accumulation of debris, they are ideal model sites to test the ecological effects of
523
debris. These effects are likely to differ between larger litter items and microplastics (Law and
524
Thompson, 2014). Hypothetically, large debris may add habitat complexity and heterogeneity to
525
beach environments and increase sediment stability at small, patchy scales; these habitat
526
modifications may propagate to greater abundance and/or longevity of crab burrows and other
527
invertebrates. Conversely, ingestion and tissue transfer of microplastics and associated toxicants by
528
ghost crabs is possible (Brennecke et al., 2015), with potential knock-on effects on the health and
529
fitness of organisms that may propagate to impacts (untested) at the assemblage and system level
530
(Brennecke et al., 2015; Browne et al., 2015).
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The few available studies on the ecological effects of marine debris are often correlational or lack
533
empirical data on mechanisms, making the interpretation of reported conclusions somewhat
534
problematic (Browne et al., 2015). We propose that ghost crabs are suitable organisms to undertake
535
such experiments on biological debris effects, given that their distribution overlaps with the stranding
536
zone of most marine debris and that they can be relatively easily manipulated and enumerated in
537
experiments (e.g. Schlacher et al., 2007c).
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In addition to the global effects of climate change, localised human modifications to the thermal
540
environment in coastal areas arise mainly from discharges of cooling water required in power plants,
541
typically at temperatures 8–12.5 °C above the intake water (Wither et al., 2012). Altered temperature
542
affects the behaviour, phenology, distribution, reproduction and movement of many marine
543
organisms subjected to thermal effluents (Mazik et al., 2013; Wither et al., 2012). On beaches, patterns
544
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localised density effect may be possible (Hussain et al., 2010), but attribution was highly uncertain, and
546
impacts on high-energy coasts are likely to be limited to 100s of metres (Cardoso-Mohedano et al.,
547
2015). Because ghost crabs rarely enter the swash post settlement they are not routinely exposed for
548
significant periods to thermal discharges where these occur in the surf-zone of beaches. Hence ghost
549
crabs are unlikely to show strong and persistent temperature responses to this particular stressor. It is
550
possible, however, that thermal plumes may modify larval behaviour, dispersal and recruitment to
551
beaches. Also, traces of biocides (added to cooling water to prevent bio-fouling) may have broader
552
effects on the condition of exposed individuals close to discharge points (Mazik et al., 2013).
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Chemical contaminants, toxicants, and xenobiotics are a major class of anthropogenic stressor in
555
marine ecosystems. The biological effects, and their ecological ramifications, of chemical contaminants
556
are as diverse as their sources, and new threats are continually being identified (Mearns et al., 2014).
557
The issue of chemical pollution in dune-beach systems is treated very cursorily (Defeo et al., 2009; Nel
558
et al., 2014); however, there is no reason to suspect that species and dune-beach ecosystems are less
559
susceptible to inputs of toxic chemicals than other marine ecosystems. The one exception to the
560
dearth of data on chemical pollution effects in beach systems is crude oil spills. Probably due to the
561
high public profile of spill events, short-term ecological changes in beach systems following shipping
562
accidents and well failures have been reported for several incidents globally (de la Huz et al., 2005;
563
Engel and Gupta, 2014; Schlacher et al., 2011b; Stevens et al., 2012), although questions about
564
recovery remain mostly unanswered (Peterson et al., 2003). The biological impacts of many chemicals
565
are truly global, but they are often most evident near cities in developed countries. Ghost crabs occur
566
regularly in dunes and beaches in and near coastal cities, making them appropriate sentinel species to
567
monitor ecological effects in these settings. Also, ghost crabs are the apex invertebrate predators on
568
sandy shores, creating opportunities to measure chemical contaminant transfers through food webs.
569
How oil spills affect ghost crabs has also not been quantified, representing an obvious opportunity to
570
include them in future spill assessments. Furthermore, ghost crabs may directly consume toxic flakes
571
of antifouling paint where small boats are scrapped and re-painted directly on the beach.
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Humans emit a range of chemical and physical stimuli that disturb animals and interfere with the
574
perceptual processing of important signals and cues, creating sensory pollution in many ecosystems
575
(Halfwerk and Slabbekoorn, 2015). Man-made noises have become near ubiquitous (Radford et al.,
576
2014), creating an acoustic environment that presents novel challenges to many animal species
577
(Morley et al., 2014; Shannon et al., 2015). Whilst the biological effects arising in this altered acoustic
578
landscape are manifold, they most often encompass shifts in physiology (e.g. impaired hearing,
579
elevated stress hormone levels), changes to key behaviours (e.g. foraging, mating, vigilance,
580
movement), interference with the ability to detect important natural sounds (e.g. vocalisations of
581
conspecifics, acoustic signals of prey or predators), and direct fitness consequences (e.g. survival,
582
reproduction)(Morley et al., 2014; Shannon et al., 2015). Vertebrates (especially birds, mammals and
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583
fish) are by the far most-studied group in terms of noise pollution, but impacts are equally detectable
584
– and arguably of comparable biological significance – in invertebrates (Morley et al., 2014).
585 Hearing and sound production in brachyuran crabs provides essential environmental information
587
(Hughes et al., 2014) and facilitates channels for communication, which can be in the form of
588
elaborate audio-visual displays in ghost crabs (Clayton, 2008). Crabs are also sensitive to noise
589
pollution, detectable as physiological stress (Wale et al., 2013b), altered development (Pine et al.,
590
2012), shifts in foraging behaviour (Wale et al., 2013a), or impaired predator avoidance (Chan et al.,
591
2010). Contemporary beach and dune habitats present strongly altered acoustic landscapes for ghost
592
crabs and other species, so the potential exists for biological and ecological impacts arising from man-
593
made noise in sandy shore systems.
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Two aspects of ghost crab biology appear particularly intriguing to us in the context of assessing
596
noise pollution on beaches: behavioural shifts in responses to predation risks as a result of altered
597
acoustic landscapes and distorted acoustic settlement cues. Man-made noise can reduce an animal’s
598
fitness by impairing its ability to respond normally to a potential predator; such altered risk
599
assessment to predation has been experimentally demonstrated for hermit crabs exposed to boat
600
noise (Chan et al., 2010). Significantly, hermit crabs share several traits with ghost crabs, most notably
601
being conspicuous, semi-terrestrial animals displaying a distinct predator avoidance behaviour that
602
relies on hiding (hermit crabs retreat into their shells whilst ghost crabs flee into their burrows). This
603
offers the intriguing possibility of assessing noise pollution in beach animals using ‘behavioural
604
acoustic bio-assays’ in ghost crabs. Because brachyuran shore crabs use habitat-specific acoustic cues
605
for settlement, acoustic sensory pollution may impact on recruitment intensity and patterns, as
606
suggested for estuarine crabs based on limited lab experiments (Pine et al., 2012). It is possible, but
607
untested, that noise from personal watercraft may interfere with settlement cues important for late-
608
stage larvae of ghost crabs in the surf-zone off beaches. Anthropogenic noise may also mask the
609
acoustic signals produced by prey that predators use during foraging (Halfwerk and Slabbekoorn,
610
2015). Ghost crabs are omnivorous predators and scavengers of catholic tastes (Lucrezi and Schlacher,
611
2014), and it is thus possible, but untested, that prey detection and foraging efficiency in ghost crabs
612
in altered acoustic landscapes changes - this offers intriguing possibilities for acoustic bio-assays.
613
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Global light regimes have changed profoundly in intensity, spectral signatures, spatial patterns, and
615
periodicity (Kyba et al., 2015). Such changes to the light environment experienced by organisms are
616
amplified in the coastal fringe where a growing part of the human population is concentrated in
617
expanding coastal cities (Davies et al., 2014). How organisms respond to these new illumination
618
domains created by artificial night light, and the ecological ramifications of their responses, are
619
equally profound; they include changes to gene expression, physiology, behaviour, distributions, and
620
the composition of communities (Davies et al., 2015; Gaston et al., 2013; Gaston et al., 2014).
621 Page | 16
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The adverse effects of artificial night light on beach biota are well publicised for marine turtles: fewer
623
nests generally occur on more brightly lit sections of sandy coasts where hatchlings become
624
disorientated by shore-based lights (Kamrowski et al., 2014; Mazor et al., 2013; Verutes et al., 2014).
625
With the exception of a single study on beach mice, impacts of artificial night light on other beach
626
species, including ghost crabs remain untested, but are certainly plausible. For example, navigation in
627
mobile beach invertebrates (e.g. amphipods, isopods) can be complex and relies on multiple cues that
628
can include moonlight. It follows that artificial night light has the potential to disrupt orientation and
629
movement in sandy-shore animals (Scapini, 2014); it is not known whether ghost crabs also use light
630
cues to orient (e.g. homing behaviour), but effects of light pollution on movement and orientation
631
cannot be precluded and hence could be measured using behavioural assays.
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Moonlight is important in determining activity in many animal species, mainly related to changes in
634
predation risk and reproductive cycles (Kronfeld-Schor et al., 2013). Many beaches are artificially
635
illuminated at night (in addition to the more diffuse but widespread skyglow) potentially interfering
636
with natural cycles of lunar signals that are particularly important in nocturnally-foraging species. In
637
beach mice, nocturnal movement is modulated by moon phases, presumably in response to higher
638
predation risk during full-moon nights (Wilkinson et al., 2013). Consequently, beach mice exposed to
639
artificial light feed significantly less and exploit fewer food patches (Bird et al., 2004). Ghost crabs have
640
a functionally similar foraging behaviour (i.e. regular nocturnal excursion from burrows). Their foraging
641
behaviour and activity rhythms may therefore be equally sensitive to artificial light at night and could
642
possibly have fitness implications (e.g. body condition, fertility etc.). Artificial light may also extend the
643
foraging window of visually-orientated predators into the nocturnal activity period of ghost crabs, and
644
facilitate prey detection by both native consumers (e.g. shorebirds) and feral or invasive carnivores
645
(e.g. foxes, cats). Thus, changes to foraging behaviour and predation risk in ghost crabs that are
646
associated with artificial night light could be used to gauge the biological implications of light
647
pollution in sandy shore species.
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4.2.4 ‘URBANISATION’: Buildings, Grooming, Armouring, Nourishment
650
At least half of the global human population lives in cities, and these urban populations will grow
651
exponentially in the coming decades, fuelling an escalating expansion of cities globally, many of which
652
border the ocean (Seto et al., 2012; Strauss et al., 2015). Coastal cities are hotspots of current and
653
future urbanisation, including in Australia, where most (> 80%) of the population is concentrated in
654
urban centres, which are mostly located near beaches (Hallegatte et al., 2013). Pervasive ecological
655
changes in cities commonly include biotic homogenisation, biodiversity declines, altered population
656
dynamics of species, and shifts in the species composition of assemblages (Aronson et al., 2014; Sol et
657
al., 2014).
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Because beaches represent highly attractive and valuable nodes for coastal development, coastal
660
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The ecological ramifications of this ‘beach urbanisation’ span a broad ambit of reported impacts,
662
ranging from impediments to turtle nesting to local extirpations of invertebrates and functional losses
663
of key vertebrate groups (Hubbard et al., 2014; Huijbers et al., 2015b; Huijbers et al., 2013; Schlacher et
664
al., 2015a). ‘Urbanisation effects’ have also been reported for ghost crabs in several urban beach
665
studies (e.g. Barros, 2001). Except for a few isolated cases (e.g. habitat loss caused by urban seawall
666
construction; Dugan et al., 2008), the underlying causes and mechanisms that produce the observed
667
biological responses to urbanisation remain, however, largely unresolved. Failures to isolate, and
668
mechanistically explain, the causative stressors in urban beach studies arise either from employing
669
inadequate study designs, or from simply reflecting the multiple nature of man-made pressures in
670
these environments where noise pollution, artificial night light, shore-defences, trampling, grooming,
671
and nourishment often coincide in space and time (Acuña and Jaramillo, 2015). From a conservation
672
perspective it is, however, critical to resolve which of the putative factors causes the most
673
environmental harm as this will guide prioritisation of management interventions. It is also unknown
674
how, and to which degree, these urban pressures interact to produce the observed ecological effects
675
on urban beaches (but see Lucrezi et al., 2010).
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Many urban beaches are regularly cleaned (‘groomed’ or ‘raked’) to remove beach-cast algae and
678
seagrass (‘wrack’) and litter, mainly for aesthetic and public-health reasons. Wrack constitutes,
679
however, an important habitat and food resource in beach ecosystems (Colombini and Chelazzi, 2003).
680
Consequently, beach cleaning operations have multiple ecological flow-on effects: loss of upper beach
681
habitat and strandline vegetation (Dugan and Hubbard, 2010); reduced abundance and diversity of
682
invertebrates reliant on wrack (Gilburn, 2012; Llewellyn and Shackley, 1996); and diminished
683
abundance, density, and fitness of beach-nesting birds and beach-spawning fishes (Dugan et al., 2003;
684
Martin et al., 2006; Pietrelli and Biondi, 2012).
685
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Beach cleaning targets mainly the upper shore, which is the main habitat of ghost crabs. Expectations
687
are therefore that cleaning will adversely impact ghost crabs, but this has not been explicitly tested.
688
From a management perspective, it will be important to develop best practices for beach cleaning
689
operations (assuming a continued public mandate to clean beaches) that reduce ecological impacts; in
690
this context, ‘dose-response’ type studies using ghost crabs, combined with experiments that compare
691
techniques and procedures (e.g. manual removal, different equipment, depth of raking, etc.) in terms
692
of their ecological impacts will be useful. Since abundance estimates for ghost crabs via counts of
693
burrows are less costly than sampling other beach invertebrate, they provide an advantage by
694
allowing more treatment types and replication levels.
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Shoreline recession is a major risk to public and private assets located on eroding sedimentary
697
coastlines (Johnson et al., 2015). Conventional approaches to combat beach erosion are to replace the
698
lost sand volumes (‘dredge-and-fill’, ‘nourishment’) or to stabilise shore position with fixed, hard
699
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has traditionally been viewed as a less harmful option than armouring, but adverse ecological
701
outcomes of beach filling are not uncommon. These include significant reductions in the abundance
702
of infaunal organisms, resulting from a combination of limited recruitment, unsuitable new sediment,
703
and direct mortality from crushing and burial (Manning et al., 2014; Peterson et al., 2006). Impacts of
704
nourishment on invertebrates propagate upwards to shorebirds and fishes through loss of prey
705
organisms and deteriorating feeding conditions on nourished beaches (Manning et al., 2013; Peterson
706
et al., 2006). These effects can be long-lasting, with recovery from nourishment impacts taking several
707
years or longer (Peterson et al., 2014; Schlacher et al., 2012).
708
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Nourishment impacts are well documented for ghost crabs in a few locations, where significant
710
declines in population density have been detected following sand placement, and reduced
711
recruitment has been recorded at nourished sites (Peterson and Bishop, 2005; Peterson et al., 2000).
712
There remains, however, considerable scope to use ghost crabs in targeted experiments that establish
713
threshold levels of nourishment procedures that are less damaging than current practices (e.g.
714
acceptable depth of burial, frequency of application, spatial extent of single sand placement, etc.).
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Engineered structures aimed at stabilising shorelines are widely constructed to protect human assets
717
on soft, sedimentary shorelines, particularly in response to beach erosion (Nordstrom, 2014). Whilst
718
the practice of ‘shore armouring’ with seawalls and similar structures has occurred for millennia, its
719
ecological impacts have been recognised only in the last two decades (Dugan et al., 2011). In brief,
720
shore armouring significantly diminishes habitat extent and quality, resulting in severe reductions and
721
local extirpations of animal and plant species inhabiting the interface between the dunes and the
722
beach on armoured beaches (Dugan et al., 2008; Hubbard et al., 2014); these impacts propagate to
723
shorebirds and are publicly well recognised for turtles where seawalls create significant barriers to
724
nesting (Witherington et al., 2011).
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Although the adverse effects of shore armouring have been relatively well documented for ghost
727
crabs (e.g. Barros, 2001; Lucrezi et al., 2010), there remains a great potential for studies that identify
728
the biological returns from creative alternatives to traditional shore defence (e.g. structures that are
729
smaller, or below ground, or constructed from materials that improves habitat values, etc.; Nordstrom,
730
2014) and biological returns from restoration of habitats by removing armouring structures (Toft et al.,
731
2014). Biota can respond relatively quickly to habitat restoration on beaches (Toft et al., 2014), but
732
wider uptake of environmentally less destructive practices will require broad political and public
733
acceptance (Nordstrom, 2014). Demonstrating positive biological responses of key biota is imporant
734
to achieve better acceptance, and species of public appeal are central in this process (Huijbers et al.,
735
2015b). Arguably, amongst the beach invertebrates, ghost crabs (as a taxonomic group) are a prime
736
candidate to be used in this context, particularly as the basic patterns of their response to traditional
737
shore armouring is already known (e.g. Barros, 2001; Lucrezi et al., 2010).
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4.2.5 Invasive Species: Non-native Carnivores, Dune Plants and Seaweeds
740
Invasive, predominantly non-native, species have the potential to significantly alter the architecture
741
and function of ecosystems (Ehrenfeld, 2010). Traditional views concerning the effects of invasive
742
species have emphasised major adverse impacts (Courchamp et al., 2003; Norton, 2009), but a more
743
nuanced view is emerging (Davis et al., 2011; Pysek et al., 2012; Strayer, 2012). Whilst invasive species
744
effects are highly topical in the broader ecological literature (Moran and Alexander, 2014; Yelenik and
745
D'Antonio, 2013), beach ecology is somewhat lagging in this respect.
746
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Information on the effects of non-native species in coastal dune and beach systems is largely
748
restricted to: i) trophic impacts of exotic mammalian carnivores (Brown et al., 2015; Huijbers et al.,
749
2015a; Huijbers et al., 2015b; Huijbers et al., 2013; Maslo and Lockwood, 2009; Schlacher et al., 2013a;
750
Schlacher et al., 2013b); ii) how exotic vegetation modifies dune geomorphology and habitat quality
751
for dune-associated species (Johnson and De León, 2015; Nordstrom et al., 2011; Zarnetske et al.,
752
2012); and iii) the implications of fire ants for nesting success in marine turtles (Allen et al., 2001).
753
Much less is known about the effects of invasive species on the non-vegetated part of the beach and
754
in the surf-zone. However, non-native species of macroalgae that are invading the nearshore zone off
755
beaches alter wrack composition and quality, resulting in changes to animal use of wrack and possible
756
flow-on effects on feeding and fitness of wrack-associated consumers (Lastra et al., 2008; Rodil et al.,
757
2015; Rodil et al., 2008).
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Effects of invasive species on ghost crabs have been documented in only a single study reporting
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lower density of O. cordimanus in areas dominated by exotic vegetation (Brook et al., 2009). Other
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effects are, however, plausible, involving any of the mechanisms above (e.g. top-down control by
762
exotic and feral carnivores, infestation with fire ants) and hence can be fruitfully measured.
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4.2.6 Fishing and Mining
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A pivotal ecosystem service provided by sandy beaches on many shorelines globally is the provision of
766
harvestable species for human consumption. These ‘beach fisheries’ target both vertebrates (i.e. bony
767
fishes, sharks, rays) and invertebrates, mostly benthic bivalves (McLachlan et al., 1996). The economic
768
nature of beach fisheries ranges from the occasional collection of individuals for subsistence to true
769
commercial operations (Castilla and Defeo, 2001), and are subject to the same problems (e.g. over-
770
harvesting, social conflicts, socio-economic cohesion) as are often evident in open-water finfish
771
operations (Gutiérrez et al., 2011). Species in both the intertidal and the surf-zone are harvested (Turra
772
et al., 2015), and such harvests are not limited to ‘less developed’ economies but occur globally (Gray
773
et al., 2014; Gutiérrez et al., 2011).
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There exist very few data on ghost crab harvesting with respect to species targeted, geographic
776
distribution, frequency and population impacts. The single ghost crab fishery for which published data Page | 20
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are available (e.g. eastern KwaZulu-Natal, South Africa) appears to have, historically, had few adverse
778
population-level effects under low intensities of subsistence collecting (Beckley et al., 1996; Kyle et al.,
779
1997; Robertson and Kruger, 1995). However, these are historical estimates and human population
780
growth, coupled with changing economic conditions, may have increased harvesting pressures
781
considerably. It is also very plausible that ghost crabs are harvested for subsistence purposes in many
782
other small-scale artisanal fisheries (A. Turra pers. comm.); whether these artisanal harvests constitute
783
significant ecological impacts is unknown.
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Sand and gravel (aggregates) are among the globe’s most valuable mineral resources, being mined
786
world-wide and account for the largest volume of solid material extracted (Peduzzi, 2014). Most of the
787
mined aggregates are used for construction and land reclamation, complemented by applications in
788
road embankments, asphalt pavements, and manufacturing (glass, electronics; (Peduzzi, 2014). Two
789
developments in aggregate extractions have particularly dramatic repercussions for sandy beaches: i)
790
the volumes of mined marine sand exceed the volumes of sand delivered by rivers to the ocean; and
791
ii) as inland sources of aggregates are becoming exhausted, mining has increasingly shifted to
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shorelines (Peduzzi, 2014).
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Not surprisingly, removing often large volumes of sand from beaches can lead to significant changes
795
in landforms and sediment properties, and can accelerate erosion (Jonah et al., 2015) to the point
796
where mining on sandy-shores has been labelled as effectively constituting “active destruction” of
797
beaches (Pilkey and Cooper, 2014). Further geo-morphological impacts arise from the disposal of
798
tailings or slurries on the beach or into the nearshore zone (Castilla, 1983). Habitat alterations caused
799
by mining operations on beaches and in dunes translate into significant ecological harm, generally
800
manifested as reductions in abundance, biomass, and diversity of beach-associated species, local
801
extirpations, and major shifts in the species composition of assemblages exposed to mining (Pulfrich
802
and Branch, 2014; Simmons, 2005). Ghost crabs can respond in a similar pattern to habitat changes
803
arising from sand extraction, but the generalisations about biological impacts are impossible to make
804
from a single study (Jonah et al., 2015). Thus, ecological cause-and-effect studies of beach and dune
805
mining using ghost crabs as ecological indicator species in more locations, and using more response
806
variables, have future potential.
807
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5. Conclusions
809
Notwithstanding the sizeable number of studies that have examined ‘urbanisation effects’ on ghost
810
crabs, generalisations that can be developed into credible conservation actions in this domain remain
811
largely very unsatisfactory, chiefly because knowledge about mechanistic links are poorly known.
812
Whilst this situation is not unique to beach science, bedevilling urban ecology more widely
813
(McDonnell and Hahs, 2013), we contend that it presents an opportunity rather than a malaise: future
814
urban beach studies can build on the considerable knowledge about ghost crab biology and use the Page | 21
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815
design principles established for ecological experiments to employ logically consistent and powerful
816
designs that will yield stronger inference and attribution about urban effects; such experiments will
817
also need to draw upon more refined predictor and response variables that better match the
818
hypotheses tested (Browne et al., 2015; McDonnell and Hahs, 2013).
819 Whereas ghost crabs have proven to serve well to monitor conditions of sandy beaches throughout
821
the tropical and subtropical latitudes, standard assessment metrics currently involve inferring
822
abundances from numbers of burrows and sizes from burrow diameters. The failure to observe and
823
make direct measurements on the crabs themselves, including modern biomarkers, inhibits strong
824
inference about the mechanistic process or processes that cause differences in burrow counts or in
825
burrow diameters. It also limits our ability to identify critical biological harm where it may occur.
826
Nevertheless, sampling of individual ghost crabs and using them in experiments that test explicit
827
hypotheses is feasible and could expand the range of process-oriented inferences about specific
828
drivers of observed burrow abundance differences. While some manipulative experiments could be
829
piggybacked on field studies of real-world coastal impacts, especially if these studies can be initiated
830
in advance of the putative impact, much could also be learned by fundamental experimental work in
831
the laboratory. Thus, further progress is contingent on a better mechanistic understanding of what
832
drives observed responses in ghost crabs, from the individual to the population levels, and more
833
rigorous attribution to specific anthropogenic stressors.
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In any respect, ghost crabs lend themselves almost ideally to such studies, therefore representing a
836
powerful model organism for detection of ecological impacts in warm-temperate to tropical coastal
837
systems. The scope of anthropogenic impacts on ocean beach ecosystems promises more and
838
growing needs for impact evaluations. Ghost crabs can continue to provide a strong indicator of
839
impact from studies of counting and/or sizing burrows. However, these widespread dune dominants
840
may be used to provide even more specific indicators of process and causation as they are further
841
used in future experiments.
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Schlacher, T.A., Schoeman, D.S., Jones, A.R., Dugan, J.E., Hubbard, D.M., Defeo, O., Peterson, C.H., Weston, M.A., Maslo, B., Olds, A.D., Scapini, F., Nel, R., Harris, L.R., Lucrezi, S., Lastra, M., Huijbers, C.M., Connolly, R.M., 2014b. Metrics to assess ecological condition, change, and impacts in sandy beach ecosystems. Journal of Environmental Management 144, 322-335. Schlacher, T.A., Schoeman, D.S., Lastra, M., Jones, A., Dugan, J., Scapini, F., McLachlan, A., 2006. Neglected ecosystems bear the brunt of change. Ethology, Ecology & Evolution 18, 349-351.
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Schlacher, T.A., Strydom, S., Connolly, R.M., 2013a. Multiple scavengers respond rapidly to pulsed carrion resources at the land–ocean interface. Acta Oecologica 48, 7-12. Schlacher, T.A., Strydom, S., Connolly, R.M., Schoeman, D., 2013b. Donor-Control of Scavenging Food Webs at the Land-Ocean Interface. PLoS ONE 8, e68221. Schlacher, T.A., Thompson, L., 2012. Beach recreation impacts benthic invertebrates on ocean-exposed sandy shores. Biological Conservation 147, 123–132.
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Schlacher, T.A., Thompson, L.M.C., Price, S., 2007c. Vehicles versus conservation of invertebrates on sandy beaches: quantifying direct mortalities inflicted by off-road vehicles (ORVs) on ghost crabs. Marine Ecology 28, 354-367. Schlacher, T.A., Thompson, L.M.C., Walker, S.J., 2008b. Mortalities caused by off-road vehicles (ORVs) to a key member of sandy beach assemblages, the surf clam Donax deltoides. Hydrobiologia 610, 345-350.
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Schlacher, T.A., Weston, M.A., Lynn, D., Schoeman, D.S., Huijbers, C.M., Olds, A.D., Masters, S., Connolly, R.M., 2015a. Conservation gone to the dogs: when canids rule the beach in small coastal reserves. Biodiversity and Conservation 24, 493-509. Schlacher, T.A., Weston, M.A., Lynn, D.D., Connolly, R.M., 2013c. Setback distances as a conservation tool in wildlife-human interactions: testing their efficacy for birds affected by vehicles on open-coast sandy beaches. PLoS ONE 8(9), e71200.
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Schlacher, T.A., Weston, M.A., Schoeman, D.S., Olds, A.D., Huijbers, C.M., Connolly, R.M., 2015b. Golden opportunities: A horizon scan to expand sandy beach ecology. Estuarine, Coastal and Shelf Science 157, 1-6. Schoeman, D.S., Schlacher, T.A., Jones, A.R., Murray, A., Huijbers, C.M., Olds, A.D., Connolly, R.M., 2015. Edging along a warming coast: A range extension for a common sandy beach crab. PLoS ONE 10(11), e0141976. Seto, K.C., Güneralp, B., Hutyra, L.R., 2012. Global forecasts of urban expansion to 2030 and direct impacts on biodiversity and carbon pools. Proceedings of the National Academy of Sciences of the United States of America 109, 16083-16088. Shannon, G., McKenna, M.F., Angeloni, L.M., Crooks, K.R., Fristrup, K.M., Brown, E., Warner, K.A., Nelson, M.D., White, C., Briggs, J., McFarland, S., Wittemyer, G., 2015. A synthesis of two decades of research documenting the effects of noise on wildlife. Biological Reviews, doi: 10.1111/brv.12207.
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7. Figure Captions
Fig. 1 Distribution of studies reporting effects of human pressures on ghost crabs on ocean beaches. Fig. 2 Effect sizes attributed to different types of human pressures on the abundance (left panel) and size (right panel) of ghost crab burrow openings on ocean beaches. Plotted values are response ratios
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ln(R), calculated as the log of the quotient of the mean value recorded for impact sites, divided by the mean value at corresponding reference sites in individual studies: lnR = mean impact / mean control
(Borenstein et al., 2009). Dots represent response ratios from individual studies. Vertical lines are
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means and horizontal lines are the 95% confidence intervals for data groups with n ≥ 3.
Fig. 3 Classification of ecological impact assessment for specific human pressures with respect to the amount of information that is currently available about their effects on ghost crabs (y axis) and how
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sensitive and reliable ghost crabs are likely to be as indicator species in impacts studies targeting a particular pressure (x axis). Pressures in the top right are both information-poor (i.e. high data
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deficiency) and may be best quantified using ghost crabs (i.e. good suitability).
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Table 1 Attributes of reviewed publications that measured the response of ghost crabs to human activities or anthropogenic habitat changes on ocean-exposed sandy beaches. (Details for individual publications are provided in Table 1 of the supplementary material).
1 - Geographic Distribution Ocean Basin / Sea (No. studies) Pacific
Indian
South China Sea
20
12
5
1
Australia
USA
Brazil
13
12
5
min
max
mean
1.30
38.24
26.10
Tropics
Subtropics
28
10
Countries (No. studies)
South Africa
Others#
3
5
sd
9.35
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Latitude (º)
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Atlantic
2 - Species Species
No. Studies
O. quadrata
Species
18
O. cordimanus O ceratophthalma
No. Studies 2
13
O. africana O. madagascariensis
10
O. cursor
1
2
4
3 - Response Metrics
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O ryderi
3.1 No. metrics measured per study min
max
mean
sd
6
1.95
1.27
1 Metric
2 Metrics
3 Metrics
>3 Metrics
18
11
6
3
1
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3.2 No. studies using x metrics
3.3. Types of metrics used
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3.3.1 - Direct (Organism)
No. studies
3.3.2 - Indirect (Burrows)
No. studies
Mortality
2
Abundance
38
Home Range
1
Diameter
19
Body Condition
1
Depth
3
Trail Length
1
Length
3
Turns in Trail
1
Angle
2
Weight
2
Orientation
1
4 - Replication and Scale Spatial min
max
mean
sd
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No. sites (n) 2
21
5.16
4.11
0.05
310
38.69
66.10
min
max
mean
sd
2
27
8.89
6.77
1
1370
158.47
Spatial ambit (km) Temporal
Duration (days)
267.34
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# Ghana: 2, Cuba: 1, Seychelles: 1, Singapore: 1
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No. times measured (n)
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Table 2 Summary statistics of response ratios lnR in ghost crabs, testing the biological effects of human pressures on ocean beaches in terms of changes to the abundance and size of crab burrows. Response ratios, lnR, are the log quotient of the mean value at impact sites divided by the mean at reference sites: lnR = mean impact / mean control (Borenstein et al., 2009). Values of lnR < 0 denote decreases in abundance or size, whilst iR > 0 signifies more or larger burrows at sites classified as ‘impacted’ by authors. (Tabulated lnR values are for stressor
xxx
Abundance (burrow counts)
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assessed by at least three studies; for all full listing of all studies refer to Table S1 and Fig. 2.).
Size (burrow diameter)
n
mean
(95% CI)
P
n
mean
(95% CI)r
P
All stressors
37
-1.35
(-1.78 - -0.92)
<0.0001
13
-0.15
(-0.35 - 0.05)
0.1327
Vehicles
11
-1.43
(-2.42 - -0.43)
0.0095
5
-0.07
(-0.27 - 0.13)
0.3772
Nourishment
4
-1.27
(-2.41 - -0.13)
0.0378
0
na
na
na
Urbanisation & Recreation
13
-1.52
(-2.16 - -0.87)
-0.19
(-1.23 - 0.84)
0.5064
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3
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0.0003
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Table 3 Gap analysis of the application of ghost crabs as indicator species to quantify the ecological consequences of human pressures on ocean beaches and coastal dunes. 1
Habitat & Environmental Changes / Effects 1 (predicted)
Expected Response(s) of Ghost Crabs
CLIMATE CHANGE
Suitability of Ghost Crabs as Indicator 2 Species
Data Deficiency (Lack of Published Evidence for 3
Ghost Crabs)
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Main Pressures
Sea-level rise, storms
Erosion, shoreline retreat, elimination of upper beach and frontal dune habitats.
Population decrease(s), local extirpations, delayed recovery from erosion events, limited recruitment in beaches with (seasonal) scarps.
Warming
Temperature (increase).
Altered physiology, phenology, demography, geographic range, behaviour.
(good)
ΔΔΔ (high)
Currents, upwelling
Altered organism dispersal, primary productivity, marine carrion availability, wrack deposition.
Changes to recruitment and geographic distribution, altered nutritional status, condition and physiological performance.
(acceptable)
ΔΔΔ (high)
Altered precipitation
Changes to dune vegetation, height of water table, thermal environment of sand wedge, aquifer outcrops on beach.
Possibly, altered distribution and population size, but direction and magnitude difficult to predict.
(poor)
ΔΔΔ (high)
Diverse biological effects on marine organisms (e.g. decreased survival, calcification, growth, development, abundance in response to acidification and altered life histories).
Multiple detrimental developmental and survivorship effects during larval (fully marine) phase possible, possibly lowering recruitment to beaches.
(poor)
ΔΔΔ (high)
Substantially lower habitat quality, direct kills of individuals, behavioural changes.
Lower abundance, altered habitat use, population structure, and behaviour.
(good)
Δ (low)
(good)
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Acidification
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ΔΔ (moderate)
RECREATION Vehicles
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Lower habitat quality, direct kills of individuals, behavioural changes.
Lower abundance, altered habitat use & behaviour.
(acceptable)
ΔΔ (moderate)
Camping (dunes)
Increased food resources, altered habitat quality, behavioural changes..
Changed abundance, altered habitat use & behaviour
(acceptable)
ΔΔ (moderate)
Motorised Watercrafts
Noise and chemical pollution, wildlife strikes.
Altered behaviour and time budgets, toxicity, kills, etc.
(poor)
ΔΔΔ (high)
Population impacts on target species, bycatch, fauna impacts and habitat changes associated with vehicle-based access by fishers.
Individuals crushed by vehicles; food subsidies from fisheries discards.
(acceptable)
ΔΔ (moderate)
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Recreational fishing & bait collecting
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(jet skis, boats)
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Trampling
POLLUTION
Changes to interstitial chemistry, inputs of toxicants, nutrient enrichment.
Uptake of sewagederived nutrients and pollutants via direct exposure and foodweb transfers.
(good)
ΔΔΔ (high)
Debris
Ingestion (microplastics) or entanglement (larger litter), changes to structural attributes of beach habitat.
Physiological and other health impairment from ingestion of microplastics, altered distribution and higher abundance in areas of abundant larger litter items deposited on shore.
(good)
ΔΔΔ (high)
Increased habitat temperature and thermal variability.
Altered recruitment dynamics, possible health effects from anti bio-fouling treatment.
(acceptable)
ΔΔΔ (high)
Chemicals
Toxicity from contaminants; (e.g. crude oil spills).
Multiple and varied consequences of toxicity, from sub-lethal physiological and behavioural effects to impairment of reproduction and population persistence.
(good)
ΔΔΔ (high)
Noise
Acoustic environment (altered intensity and frequency spectrum).
Behavioural changes, altered behavioural time budgets and predation risks,
(good)
ΔΔΔ (high)
Thermal discharges
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Sewage and Stormwater
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Artificial Night Light
Light environment (altered intensity and frequency spectrum).
Behavioural changes, altered behavioural time budgets and predation risks, endocrine disruptions.
(good)
ΔΔΔ (high)
Buildings, infrastructure, roads
Conversion or loss of natural habitat, especially the upper shore and dunes.
Smaller population sizes, shifts in distributions and possibly species interactions.
(good)
ΔΔ (moderate)
Grooming (raking, cleaning)
Habitat losses (upper beach), impedes dune formation, lowers beach stability, fewer food resources.
Smaller population sizes, shifts in distributions and possibly species interactions.
(good)
ΔΔ (moderate)
Nourishment
Mortality of fauna (crushing, burial), reduced habitat suitability.
Smaller population sizes, shifts in distributions and possibly species interactions.
(good)
(low)
Armouring (seawalls, groins, revetments, breakwaters)
Loss of habitat, increased rates of beach erosion and habitat instability.
Smaller population sizes, shifts in distributions and possibly species interactions.
(good)
ΔΔ (moderate)
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INVASIVE SPECIES
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URBANISATION'
Predation, possible competition for carrion.
Smaller population sizes, altered pop. structure
(good)
ΔΔ (moderate)
Invasive dune plants
Altered habitat quality and stability.
Altered population sizes and/or structure
(good)
ΔΔ (moderate)
Modified wrack composition and properties.
Unknown, but possibly negative if exotic wrack material lowers habitat use of strandline by ghost crabs.
(acceptable)
ΔΔΔ (high)
Fisheries
Overfishing of target species.
Smaller population sizes, altered pop. structure
(good)
ΔΔ (moderate)
Mining
Contamination and/or loss of habitat, direct mortality, habitat modification through exacerbated erosion.
Smaller population sizes, altered pop. structure, toxic effects
(good)
ΔΔ (moderate)
Exotic algae and seagrass species
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Exotic predators and feral animals
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1
Pressures and their environmental effects are adapted from Defeo et al. (2009) and Schlacher et al. (2007a; 2014a; 2008a; 2014b; 2006). Suitability as ecological indicator: – POOR (Responses to specific environmental change(s) or human activities IMPROBABLE because mechanistic links are biologically implausible or unknown); – ACCEPTABLE (Responses to specific environmental change(s) or human activities PLAUSIBLE, but mechanistic links are incompletely known in many cases); – GOOD (Responses to specific environmental change(s) or human activities are PROBABLE IN MOST CASES, consistent with expectations derived from known biological effects or mechanistic links).
3
Data Deficiency (Lack of Published Evidence for Ghost Crabs) ΔΔΔ – High (No published information on response(s) to specific pressures); ΔΔ – Moderate (Few (<3) papers documenting response(s) to specific pressures); Δ – Low (Three or more papers documenting response(s) to specific pressures).
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2
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Electronic Appendix – Supplementary Material Table S1 Publications summarised in this paper that estimated the effects of human stressors on ghost crabs on ocean-exposed sandy beaches. 1
Species
Locality
Main 2 pressure(s)
(Florschuts and Williamson, 1978) (Fisher and Tevesz, 1979) (Wolcott and Wolcott, 1984) (Christoffers, 1986)
O. quadrata
USA, North Carolina
VEH
O. quadrata
URB#
O. quadrata
USA, North Carolina / Virginia USA, North Carolina
O. quadrata
USA, Maryland
URB#
(McGwynne, 1988)
O. ryderi, O. madagascariensis, O. ceratophthalma O. ryderi, O. madagascariensis, O. ceratophthalma O. quadrata
South Africa, KwaZulu Natal, Maputaland
VEH
(Peterson et al., 2000)
O. cordimanus
(Blankensteyn, 2006)
O. quadrata
(Moss and McPhee, 2006) (Neves and Bemvenuti, 2006) (Peterson et al., 2006)
USA, North Carolina
3
RI PT ABU
ABU, DIAM, CRUSH ABU, DIAM, DEPTH ABU
HARV
ABU
NOU
ABU
#
URB
ABU
URB#
ABU
O. cordimanus
Australia, New South Wales Brazil, Santa Catarina Island Australia, Queensland
VEH
ABU
O. quadrata
Brazil, Rio Grande do Sul
URB#
ABU
O. quadrata
USA, North Carolina
NOU
ABU
(Bisson, 2007)
O. quadrata
USA, Virginia
URB#
ABU
(Foster-Smith et al., 2007) (Maccarone and Mathews, 2007) (Schlacher et al., 2007c) (Barton and Roth, 2008) (De Araújo et al., 2008) (Hobbs et al., 2008)
O. spp.
Australia, Western Australia USA, Texas
VEH
ABU
URB#
ABU, DIAM, ORI
O. cordimanus, O. ceratophthalma O. quadrata
Australia, Queensland
VEH
ABU, DIAM, CRUSH
USA, Florida
PRED
ABU, DIAM
O. quadrata
Brazil, Espírito Santo
CLEAN
ABU, DIAM
O. quadrata
USA, Virginia
VEH
ABU, DIAM, LENGTH
O. quadrata
USA, Florida
NOU
ABU
O. cordimanus, O. ceratophthalma O. cordimanus, O. ceratophthalma, O. ryderi O. cordimanus, O. ceratophthalma O. cordimanus, O. ceratophthalma O. quadrata
Australia, Queensland
VEH
ABU, DIAM
Seychelles,
INV
ABU
Australia, Queensland
URB#
ABU, DIAM
Australia, Queensland
TRAMP
ABU, DIAM
Brazil, Bahia
URB#
ABU
O. cordimanus, O. ceratophthalma O. cordimanus, O. ceratophthalma
Australia, Queensland
URB#
ABU, DIAM
Australia, Queensland
VEH
ABU, DIAM, DEPTH, LENGTH, WEIGHT, ANGLE
TE D
(Barros, 2001)
South Africa, KwaZulu Natal
VEH
SC
(Robertson and Kruger, 1995)
Metric(s) ABU
M AN U
Source
EP
O. quadrata
AC C
1409 1 2 1410 3 1411 4 5 1412 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62 63 64 65
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(Irlandi and Arnold, 2008) (Thompson and Schlacher, 2008) (Brook et al., 2009)
(Lucrezi et al., 2009b) (Lucrezi et al., 2009a) (Magalhaes et al., 2009) (Lucrezi et al., 2010) (Lucrezi and Schlacher, 2010)
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R1 Schlacher et al
Human Beach Impacts
O. cordimanus, O. ceratophthalma O. cordimanus, O. ceratophthalma
Australia, Queensland
VEH
Australia, Queensland
VEH
(Aheto et al., 2011)
O. africana, O. cursor
Ghana, Central Ghana
URB#
ABU, TRAIL, AREA, TURN ABU, DIAM, DEPTH, LENGTH, WEIGHT, ANGLE ABU, DIAM
(Schlacher et al., 2011a) (Noriega et al., 2012)
O. cordimanus
Australia, Queensland
CAM
ABU, DIAM, BCI
Australia, Queensland
URB#
ABU, DIAM
(Ocaña et al., 2012)
O. cordimanus, O. ceratophthalma O. quadrata
Cuba, NE Coast
URB#
ABU
(Guilherme, 2013)
O. quadrata
Brazil, Paraná
CLEAN
ABU, DIAM
(Lucrezi et al., 2014)
South Africa, KwaZuluNatal
VEH
ABU, DIAM
(Peterson et al., 2014)
O. ceratophthalma, O. madagascariensis, O. ryderi O. quadrata
USA, North Carolina
NOU
(Jonah et al., 2015)
O. africana, O. cursor
Ghana, Cape Coast
MINE
(Lim and Yong, 2015)
O. ceratophthalma
Singapore,
OIL
SC
1
RI PT
(Schlacher and Lucrezi, 2010a) (Schlacher and Lucrezi, 2010b)
ABU
ABU, DIAM ABU
Criteria for inclusions were that a) some form of peer review was likely to have been in place, and b) that at least means for
2
M AN U
controls and reference conditions could be extracted from a publication to estimate effects sizes for at least one variable. - CLEAN - cleaning / grooming (manual and mechanical); HARV - harvesting, subsistence fishing; INV - invasive species
(plants); MINE - mining for beach sand; NOUR - nourishment, re-profiling, beach bulldozing etc.; OIL - oil spill; PRED - predator control (racoon culling); TRAMP - trampling (short-term, intense); URB - 'urbanisation & recreation' (includes shore armouring, trampling, dune conversions, erosion etc.); VEH - vehicles (ORV - off-road vehicles, 4WD - four wheel drives, quad bikes, etc.). 3
- ABU - Abundance (density) of burrow openings at the beach surface; ANGLE - inclination of main shaft of burrow; BCI - Body
Condition Index; CRUSH - mortality caused by vehicles; DEPTH - vertical penetration of burrow into the sediment; DIAM diameter of burrow opening at / close to beach surface; HOME - size of daily home range; LENGTH - dimension of longest axis
TE D
of burrow; ORI - orientation of main shaft / compass direction; TRAIL - length of trails between turns during nocturnal movement; TURN - number of turns in movement path during nocturnal activity; WEIGHT - of burrow cast made with plaster of Paris or similar. #
-‘urbanisation’ is used as a collective term, intended to encompass multiple pressures associated with the intensive human use
EP
of beaches and development of dunes backing beaches. Because in many cases, two or more threats are spatially superimposed (e.g. sections of beach with seawalls are usually more heavily trampled than non-armoured sections) or pressures act sequentially or repeatedly (e.g. beach cleaning activities alternating with recreational use), past study designs failed to identify the effects of individual pressures un-confounded from other.
AC C
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 1413 45 1414 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62 63 64 65
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AC C
EP
TE D
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT
AC C
EP
TE D
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT
AC C
EP
TE D
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT
ACCEPTED MANUSCRIPT Mitigating threats to sandy beaches requires accurate assessments of condition.
2.
Ghost crabs are widely used as indicator species in ecological beach assessments.
3.
Human impacts detected with ghost crabs are globally evident for sandy shores.
4.
Applied conservation needs experiments that yield defensible cause-effect evidence.
5.
Priority areas are acoustic and light pollution, debris, climate change effects.
AC C
EP
TE D
M AN U
SC
RI PT
1.