Ghost crab populations respond to changing morphodynamic and habitat properties on sandy beaches

Acta Oecologica 62 (2015) 18e31

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Original article

Ghost crab populations respond to changing morphodynamic and habitat properties on sandy beaches Serena Lucrezi TREES e Tourism Research in Economic Environs and Society, North-West University, Private Bag X6001, Potchefstroom, 2531 North-West, South Africa

a r t i c l e i n f o

a b s t r a c t

Article history: Received 6 May 2014 Received in revised form 6 November 2014 Accepted 20 November 2014 Available online

The morphodynamic state and habitat properties of microtidal sandy beaches largely account for variations in macrofauna structure. In ecological theory, the habitat harshness hypothesis and the habitat safety hypothesis explain variations in macrofauna populations of the intertidal and supratidal zones of sandy beaches. The former hypothesis states that intertidal macrofauna should increase from reflective to dissipative beaches. The latter hypothesis supports the idea that supratidal species are more successful on reflective beaches, given their relative independence from the swash. However, trends in abundance of supratidal species, particularly crustaceans, have been unclear and further investigation is therefore needed. This study tested the two hypotheses on the largest invertebrate intertidal-to-supratidal crustacean on sandy beaches, namely the ghost crab (genus Ocypode). Variations in ghost crab burrow density, abundance, size and across-shore distribution were measured on four warm-temperate microtidal sandy beaches in KwaZulu-Natal, South Africa. Burrow numbers increased with beach morphodynamic state, while average burrow size decreased. The steepest, narrowest and most inundationprone beach represented the least hospitable environment for the ghost crabs. The results that are reported here tend to support the habitat harshness hypothesis. However, the relevance of i) individual physical variables, ii) tidal action, and iii) the ecology of various species, in shaping ghost crab population dynamics, is also discussed. The results contribute to the knowledge regarding population dynamics of intertidal and supratidal crustaceans across beach types. © 2014 Elsevier Masson SAS. All rights reserved.

Keywords: Sandy beach Ghost crab Burrow density Abundance Size Distribution Morphodynamic state

1. Introduction Sandy beaches are unique ecotones, as they represent the most prominent partitioning environment between the continents and the ocean, constituting 70% of the world's coastlines (Bascom, 1980; Schlacher and Thompson, 2013b). They offer essential extractive and non-extractive ecosystem services (e.g. food, habitat, water storage, nutrient cycling, coastal protection, recreation), aside from having intrinsic values (Defeo et al., 2009; Everard et al., 2010; Schlacher et al., 2014). Sandy beaches are unstable and mobile environments; the habitat is the result of a combination of abiotic factors, from climate to sea conditions and tides. The morphology and dynamics of sandy beaches are ultimately determined by sediment particle size, wave height and period, and topography (Short and Wright, 1983; Short, 1996). The result of the interplay of these features is a range of beach morphodynamic types, from reflective to dissipative.

E-mail address: [email protected]. http://dx.doi.org/10.1016/j.actao.2014.11.004 1146-609X/© 2014 Elsevier Masson SAS. All rights reserved.

Reflective beaches are narrow and steep with coarse sand, and have a dynamic and turbulent swash with short wave periods. Dissipative beaches are wider, flatter, have finer sand particles and gentle swashes, with waves of longer period that dissipate in the surf zone. Between these extremes sit a range of intermediate beach
mez, 2005; Defeo and McLachlan, 2005). types (Defeo and Go Beach morphodynamic types are defined by a compound index of beach state, namely the dimensionless fall velocity or Dean's parameter U (Short, 1996). Dean's parameter U, which is essentially a measure of the ability of the predominant wave energy to erode sand (Defeo and McLachlan, 2005), is calculated as jHb÷(Ws$T)j, where Hb ¼ wave breaker height (m), Ws ¼ sediment fall velocity (m s1) and T ¼ wave period (s). On microtidal beaches (tide range <2 m), a value of U ¼ 1 typically marks the threshold from the reflective to the intermediate state, while a value of U ¼ 6 marks the transition from the intermediate to the dissipative state (Wright and Short, 1984); in a study by Harris et al. (2011a) on microtidal beaches in South Africa, reflective beaches were classified as <27.49 m wide, reflective-intermediate beaches between 27.49 m

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and 47.03 m wide, intermediate-dissipative beaches between 47.04 m and 64.10 m wide, and dissipative beaches >64.10 m wide. When classifying all open coast beach systems (e.g. macrotidal, embayed), Short (1996) determined that values of U < 2 denote a reflective beach; 2 < U < 5 denotes a beach of intermediate state, and U > 5 indicates a dissipative beach. Wright and Short (1984, 1996) established that while beaches can be categorized into reflective, intermediate, and dissipative morphodynamic states, considerable variability still occurs within each category. For example, despite the small range of U values, beaches of the intermediate group exhibit the greatest variation; also, dissipative beaches are largely dynamic spatially and temporally, with U values going up to 30 (Wright and Short, 1984). The diversity of beach types, characterized by the interaction of tides, waves and sand, can account for and explain variations in macrofauna structure on sandy beaches, including species richness, abundance, and morphological and life history traits. Therefore, understanding the spatial variation of sandy beach macrofauna, from the micro-scale to the macro-scale, has always been a pivotal theme in sandy beach and coastal ecology (Defeo and McLachlan, 2005; McLachlan and Dorvlo, 2007a; Schlacher et al., 2008; Defeo and McLachlan, 2013; Dugan et al., 2013; Schlacher and Thompson, 2013a; Veas et al., 2014). The large interest in determining the structure of macrofauna species on sandy beaches and its relation to external drivers has been increasing over the recent years, due to i) the overall importance of sandy beach macrofauna in ecosystem food webs and in the equilibrium of sandy beach ecosystems; and ii) the importance of many key species as ‘signals’ of natural and anthropogenic ecosystem changes (Scapini and Morgan, 2002; McLachlan and Brown, 2006; Harris et al., 2011b; Gonçalves et al., 2013). Over the last 25 years, a number of ecological theories regarding macrofauna structure on sandy beaches have been proposed. The autecological hypothesis was applied to sandy beaches by McLachlan (1990), asserting that the structure of macrofauna communities on sandy beaches is determined by independent responses of each species to physical drivers in the environment. McLachlan (1990) also proposed the swash control hypothesis, asserting that the distribution of sandy beach macrofauna along a morphodynamic gradient is limited by the swash climate. McArdle and McLachlan (1991, 1992) and McLachlan et al. (1993) refined this hypothesis into the swash exclusion hypothesis (reviewed by Defeo and McLachlan, 2005), pertinent to intertidal communities (e.g. Defeo et al., 2001). The claim of this hypothesis is that species richness, abundance and biomass increase from reflective to dissipative beaches; the harshness of the swash climate (predominantly characterized by an increase in the frequency of swashes crossing the effluent line, the line separating saturated and unsaturated sands) on reflective beaches precludes the establishment of species in the intertidal zone. McLachlan et al. (1995) added that at the extreme reflective beach state, supratidal species would be the only ones capable of surviving the harsh conditions of the habitat. Brazeiro (2001) criticized the exclusive role that the swash exclusion hypothesis gives to the hydrodynamic aspect of the beach environment, emphasizing the importance of other factors, including sediment texture, the availability of organic matter, and erosion-accretion dynamics. Acknowledging the interspecific variability of ecological and life history traits that characterizes sandy beach macrofauna, Brazeiro (2001) introduced a hypothesis of multicausal environmental severity, accounting for the possibility of different factors affecting species differently. Shifting focus from the community to the population level of species in the swash zone and landward of this zone, the habitat

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harshness hypothesis (Defeo et al., 2003; Defeo and Martínez, 2003) affirms that not only species richness, but also characteristics of populations, from abundance to reproductive rates, improve along a continuum from reflective to dissipative beaches. The harsh conditions of reflective beaches force organisms to spend more energy on maintenance, thus limiting energy expenditure on reproduction, resulting in greater mortalities in the population. After testing the habitat harshness hypothesis, a number of studies concluded that beach morphodynamic state alone is an insufficient predictor of species abundances; this conclusion was based on results being either unclear or opposite to what was originally predicted, particularly on abundances of supratidal species (Defeo
nez and Yannicelli, 1997; Defeo et al., 2003; et al., 1997; Gime
mez, 2005; McLachlan Defeo and Martínez, 2003; Defeo and Go
mez and Defeo, 2012; and Dorvlo, 2005; Caetano et al., 2006; Go Barboza et al., 2013). In order to explain the newly observed patterns concerning
mez (2005) supratidal species on sandy beaches, Defeo and Go introduced the habitat safety hypothesis, which takes into account swash climate, sediment effects and life history traits of species. According to this hypothesis, supratidal species exhibit greater fitness indicators on reflective beaches, as opposed to intertidal species. This is the result of the relative independence of supratidal species from the swash and independent active movement of these species across the shore. Furthermore, the hypothesis claims that, thanks to their steep slope and relatively inundationfree backshores, reflective beaches provide a safer habitat (Short, 1996) to supratidal forms than dissipative beaches. Supratidal crustaceans in particular have been found to be most abundant on reflective beaches, also thanks to good burrowing abilities and to the tough exoskeleton, providing protection against abrasion from coarse sediment (Defeo and McLachlan, 2011); additional advantage has been attributed to scavenger and predator crustaceans living on the supratidal zone of sandy beaches of all morphodynamic states (Defeo and McLachlan, 2005, 2011). Notwithstanding the large amount of data that have been produced to test hypotheses concerning the structure of macrofauna communities and populations on sandy beaches in response to beach morphodynamics and other habitat properties, further work
mez, 2005). is still required on supratidal species (Defeo and Go Understanding the population dynamics of these species is particularly sought after, as values denoting fitness (e.g. abundance) are customarily used as a tool to evaluate the health of the ecosystem and assess the impact of human-driven changes to the ecosystem. From tropical to temperate regions around the world, the ghost crab of the genera Ocypode and Hoplocypode is the largest invertebrate predator of exposed sandy beaches (Sakai and Türkay, 2013; Lucrezi and Schlacher, 2014). Being adapted to semi-terrestrial habitats, this burrower can cover the entire extent of the beachface, from the swash to the dunes and beyond, also occupying a key locus at the landesea interface, both as predator and prey (Lucrezi and Schlacher, 2014). Ghost crabs respond clearly to a variety of human stressors on sandy beaches, from recreation (e.g. trampling and four-wheel driving; Lucrezi et al., 2009; Schlacher and Lucrezi, 2010) to engineering interventions (armoring and nourishment; Lucrezi et al., 2009; Schlacher et al., 2012), urbanization (Noriega et al., 2012), pollution (Schlacher et al., 2011) and human-induced climatic changes, such as increasing storm intensity (Hobbs et al., 2008; Lucrezi et al., 2010). Despite the wide use of population dynamics and the structure of ghost crab species to measure the effect of human impact on sandy beaches, research exploring the variation in ghost crab populations across beaches with different morphodynamic states

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and habitat properties has yielded contrasting results; these iden
n tified either no clear response of populations to beach type (Quijo et al., 2001; Souza et al., 2008), or a clearly opposite response to the one suggested by the habitat harshness hypothesis, thus supporting the habitat safety hypothesis (Defeo and McLachlan, 2011). Two principal sources of contrast in these results can be traced in the high mobility characterizing ghost crabs and the substantial variation in distribution across the shore occurring between species (either sympatric or allopatric) and geographic populations (Lucrezi and Schlacher, 2014). The objective of this study was to further test the validity of the habitat harshness hypothesis and the habitat safety hypothesis, by investigating the variation in the population structure of ghost crab species inhabiting the lower supratidal region of four warmtemperate sandy beaches with different morphodynamic index and habitat properties. Ghost crab burrow density, abundance, size and distribution across the shore were used as the key assessment metrics in this investigation. The results that are reported here should contribute to building the body of knowledge regarding the population dynamics and the structure of intertidal and supratidal crustaceans across beach types.

2. Materials and methods 2.1. Study area The study took place in the Margate and Southbroom Municipalities, south of Durban in KwaZulu-Natal, South Africa (Fig. 1). Four beaches were selected for sampling: Shelly beach (30 480 2400 S/30 240 4400 E), Lucien beach (30 5102100 S/30 220 4400 E), Margate beach (30 5103500 S/30 220 2600 E) and Marina beach (30 560 2900 S/30180 1600 E; Fig. 1). The total distance between the northernmost beach (Shelly) and the southernmost beach (Marina) is approximately 20 km (Fig. 1). All beaches are developed to various degrees, although a vegetated dune belt is always present (Fig. 1). This is relevant in that studies have demonstrated that severe urbanization characterized by the lack of a vegetated dune belt can cause significant shifts in ghost crab densities, sizes, and distribution (Barros, 2001; Lucrezi et al., 2009, 2010; Noriega et al., 2012). In this study, the absence of a dune belt would have represented a potential source of bias in determining ghost crab population structure, so sites not backed by dunes were carefully avoided.

Fig. 1. Study area located along a 22 km stretch of coast in KwaZulu-Natal, South Africa. For each of the four sites in the study (Marina beach, Shelly beach, Lucien beach, and Margate beach), a 100 m wide section of the beach was chosen for sampling. Each section was divided into four contiguous 5 m wide belt transects, distanced at 20 m from each other. Each transect was characterized by 5  5 m quadrats, arranged sequentially from the base of the dunes to the swash. Photo credits: Google Earth; S Lucrezi.

S. Lucrezi / Acta Oecologica 62 (2015) 18e31

2.2. Study design The study began on 29 March 2013 and ended on 2 April 2013. At each of the selected locations, a 100 m stretch of beach was chosen for sampling (Fig. 1). Ghost crab densities and sizes are usually dependent on the distance from the low water spring tide (LWST) (Lucrezi and Schlacher, 2014), thus excluding the possibility of simple random sampling across the shore (Quinn and Keough, 2002). In this case, belt transects (continuous strips perpendicular to the shore, starting at the base of the dunes and ending at the LWST; Fig. 1) allow an appropriate determination of ghost crab population structure across the shore; this is usually done via measurements of ‘active’ (i.e. not obstructed) burrow openings, which provide an estimate of the population while temporarily sedentary (Barros, 2001; Moss and McPhee, 2006; Schlacher et al., 2007; Valero-Pacheco et al., 2007; Lucrezi et al., 2009, 2010, 2014; Noriega et al., 2012). Therefore, each 100 m stretch was divided into four nested belt transects (Fig. 1). The transects, 5 m wide and at a distance of 20 m from each other, were divided into sequential quadrats of 5 m length (the basic sampling unit was 25 m2; Fig. 1). As a result of variations in beach width, the number of quadrats in each transect varied from transect to transect and from beach to beach; generally, there were never less than four or more than 16 quadrats in each transect. Within each quadrat, all ‘active’ ghost crab burrow openings were counted and their diameter measured (in mm) (Lucrezi et al., 2009). Burrow densities were expressed as ind. m2. Although the sandy beaches in KwaZulu-Natal are reported to be inhabited by up to three different species of ghost crab, namely Ocypode ceratophthalma, Ocypode madagascariensis, and Ocypode ryderii (Day, 1969; McLachlan, 1980), the burrow openings for each species cannot be distinguished with confidence; therefore, burrow counts had to be reported at the genus level. Burrow counts were temporally replicated at each site over a total of four days, specifically on 29 and 30 March, and 1 and 2 April 2013. Due to heavy rain, sampling did not take place on 31 March. Surveys began at 06:00 and ended no later than 11:00; the sampling was carried out by two trained field workers, who spent approximately an hour at each beach. Due to the potential of bias in ghost crab population estimates that could be caused by raising morning temperatures, leading to erosion, collapse and obstruction of burrow entrances, each site was sampled once first, once second, once third and once last during the study. However, the selection of beaches to sample first, second, third and fourth on each day was random. Once a site was randomly selected to be sampled first, second, third or fourth on a given day, it was not given an opportunity to be sampled at the same position on any other day. All study sites were subject to human trampling during the study (this was likely to be the case at the later hours of sampling). However, the beach stretches that were chosen for sampling (Fig. 1) were located away from areas of disturbance, such as the beach juxtaposing the swimming flags, or the area of the beach near lifesaving facilities and infrastructure. Therefore, the potential that burrow counts were biased by burrow-opening obstruction from pedestrians passing was excluded; so was the possibility that food scraps were made available to the ghost crabs by pedestrians, thus increasing densities. 2.3. Environmental variables An account of the weather and tides during the study period at the selected sites was obtained from the South African Weather Services (www.weathersa.co.za) and the South African Navy Hydrographic Office (www.sanho.co.za). All measurements of environmental variables at the study sites were taken according to the

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macrofauna sampling station protocol as prescribed by Schlacher et al. (2008). For each transect in every beach section, standard theodolite surveys of the beachface, from the base of the dunes to the LWST, were used to obtain values of beach width and dumpy readings. These were later used to compute formulas for key morphological properties of the beach, including height above LWST, horizontal distance from LWST, and slope. Height (m) was calculated by using the formula j(y  x)e(n  x)j, where x ¼ dumpy reading at the base of the dunes (m), y ¼ dumpy reading at the LWST (m) and n ¼ dumpy reading at any given point between x and y (m). Horizontal distance (m) was calculated by using the formula j((W2)(H2))0.5j, where W ¼ beach width (m) and H ¼ height (m). Slope ( ) was calculated by using the formula jdegrees (arc tangent (H÷D))j, where H ¼ height (m) and D ¼ horizontal distance (m). In each transect, the position of the high tide line (m) with respect to the dunes was also recorded. Within each quadrat along the belt transects, measurements of sediment shear strength (Humboldt H-4212MH Pocket Shear Vane Tester with standard vane-stress range up to 1 kg cm2), penetration force (Pocket Soil Penetrometer with 6 mm diameter tip-stress range up to 4.5 kg cm2) and sediment cores (30 mm diameter, 100 mm deep) were taken at three random positions. In the laboratory, sediment moisture was calculated by subtracting the dry weight of sand samples (after 48 h in the oven at 70  C) from their wet weight. Sediment granulometry was analyzed by dry-sieving samples through a nested series of seven sieves, arranged in decreasing mesh aperture size (3350 mm, 2000 mm, 1000 mm, 500 mm, 250 mm, 212 mm, 53 mm, and pan); this phi set either equals or approximates those of previous research focusing on ghost crab population estimates on sandy beaches (e.g. Lucrezi et al., 2009, 2014; Noriega et al., 2012; Schlacher et al., 2012). Sediment grain size (mm) was calculated with the GRADISTAT software according to the Folk and Ward method (Blott and Pye, 2001), and was later used to calculate sediment fall velocity or settling velocity (m s1) according to the formula prescribed by Gibbs et al. (1971). Wave breaker height (m), wave period (s) and sediment fall velocity (m s1) were used to estimate the beach morphodynamic state, defined by the Dean's parameter U (Short, 1996). Although the beaches studied are microtidal (tide range <2 m), the same threshold values of U used for all open coast beach systems were employed here, whereby U < 2 denotes a reflective beach; 2 < U < 5 denotes a beach of intermediate state, and U > 5 indicates a dissipative beach (Short, 1996). 2.4. Data analysis All univariate and multivariate statistics were calculated by using StatSoft STATISTICA (Version 12, 2013) and GraphPad Prism (Version 5, 2007). Results from Cochran's C-tests for normality and homoscedasticity confirmed no need to transform the raw data. Spearman (rs) correlation analysis was used to investigate relationships between environmental variables (weather, sea conditions and tides, beach properties, and sediment properties) and ghost crab burrow densities and abundance, either pooled from the whole study or at each specific site. Morphological properties of the beach (slope, Dean's parameter U, beach width and beach elevation above LWST) were contrasted by using a generalized linear mixed model (GLMM), which accounts for the data exhibiting correlation and non-constant variability (McCulloch and Neuhaus, 2013; Hancock and Mueller, 2010). In the model, the beaches (Margate, Shelly, Lucien and Marina) constituted the spatial fixed factor, while the quadrats (between four and 16) that were contained in each transect (four transects per beach) were treated as a spatial random factor; the surveys (29

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March, 30 March, 1 April, 2 April) were treated as a fixed temporal factor. The GLMM was also adopted to partition the total variance in i) physical habitat properties of the beach (sediment moisture, shear strength, penetration force, and grain size), and ii) ghost crab burrow densities and sizes. In the design, the beaches and the days of the survey again represented the fixed spatial and temporal components of variation, respectively, while the quadrats in each transect were treated as a random spatial term. However, three covariates were introduced in this design to account for fluctuations in beach morphology across time and space: elevation above LWST (m), burrow distance upshore from LWST (m), and beach width (m). In order to establish variations in ghost crab burrow densities and sizes across the beach between sites, graphic representations of beach profiles were used to appropriately divide the beachface into distinct zones; these turned out to be as follows: the upper beach, or the first 20 m of the beachface, from the base of the dunes

towards the swash; the berm area, between 20 and 45 m from the base of the dunes; and the lower flat beach, from 45 m to the LWST. For each zone, the variation in ghost crab burrow densities and sizes was partitioned by means of a GLMM, with beach and survey being the fixed spatial and temporal factors, respectively, and the quadrats in each transect being the random spatial factor. Significant main effects or interaction terms in the GLMM were followed by Fisher's least significant difference (LSD) post-hoc tests, contrasting the dependent variables between beaches for each individual survey. 3. Results 3.1. Weather, sea conditions and tides The study period was characterized by humid days (66e94%) with prevailingly north-easterly winds, ranging from 6 to 33 km h1 (Fig. 2a), and air temperatures between 22 and 28  C

Fig. 2. Temporal variation in weather conditions (aec), and comparison of different habitat properties between study sites throughout the study period (deg). The segmented lines denote the days when sampling was carried out during the study period.

S. Lucrezi / Acta Oecologica 62 (2015) 18e31

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(Fig. 2b). Rainfall was minimal (0e13%) during the first and last parts of the study (28e29 March and 1e2 April 2013), but increased to 41e96% during a brief storm surge (30e31 March 2013; Fig. 2c. The winds gave rise to 1e1.2 m high waves, breaking at intervals of 13e20 s. Tidal amplitude was 1.6 m in average (se ¼ 0.02), decreasing from 2 m to 0.97 m throughout the study.

Therefore, the narrowest portion of dry sand out of all sampled sites was at Shelly (Fig. 3b). Sediment moisture content was the greatest (5%), while average shear strength and penetration force values were the lowest (0.15 kg cm2, se ¼ 0.01 and 0.24 kg cm2, se ¼ 0.01, respectively); the sediment was coarse sand (0.6 mm, se ¼ 0.004).

3.2. Habitat properties

3.2.3. Lucien beach Lucien beach was a moderately sloping (4.82 , se ¼ 0.22; Fig. 3c), microtidal reflective (Dean's parameter U ¼ 1.37, se ¼ 0.01) beach; the morphodynamic state index for Lucien beach was second lowest after Shelly. The berm area extended from 20 m from the base of the dunes down to the swash zone (Fig. 3c). The beach was 43.07 m (se ¼ 0.50) wide on average, having a minimal width of 35 m and not extending beyond 50 m from the dunes. Although Lucien was the second narrowest beach after Shelly, the average position of the high tide line was quite far from the dunes (24.43 m, se ¼ 0.26), leaving approximately half of the beachface dry and the other half exposed to submersion by the tides (Fig. 3c). Average sediment moisture was 2.5%, sediment shear strength was 0.21 kg cm2 (se ¼ 0.01) and penetration force was 0.28 kg cm2 (se ¼ 0.01); the sediment was medium-coarse sand (0.5 mm, se ¼ 0.003).

3.2.1. Margate beach Margate beach was characterized by a gently sloping (mean ¼ 2.99 , se ¼ 0.16) beach of microtidal reflective state (Dean's parameter U ¼ 1.42, se ¼ 0.01), with a defined berm area, extending from 20 to 45 m from the dunes (Fig. 3a). Margate was the flattest and widest beach: although beach width had a wide range (25e80 m; Fig. 3a), the median beach width was 55 m with an average of 55.95 m (se ¼ 1.17). The mean position of the high tide line with respect to the dunes was 31.25 m (se ¼ 0.83); this made Margate the site with the widest dry portion of beachface compared with the remaining sites (Fig. 3a). Beach sediment contained 3% water in average, with shear strength and penetration force values of 0.20 kg cm2 (se ¼ 0.01) and 0.29 kg cm2 (se ¼ 0.01), respectively. The beach sediment was medium-coarse sand (0.5 mm, se ¼ 0.002). 3.2.2. Shelly beach Shelly beach was the steepest beach (Fig. 3b), with an average slope of 6.38 (se ¼ 0.03); this microtidal reflective beach presented the lowest Dean's parameter U (1.08, se ¼ 0.01). The beach had a narrow berm area, starting at approximately 20 m from the dunes and ending into the swash zone (Fig. 3b). Shelly beach was also the narrowest beach, with an average width of 30.63 m (se ¼ 0.57). The beach here was never narrower than 20 m or wider than 35 m during sampling. The average distance between the dunes and the high tide line was 9.42 m (se ¼ 1.08); however, there were instances where the tides submerged the beach entirely at night, with the high tide line reaching the base of the dunes the next day (Fig. 3b).

3.2.4. Marina beach Marina beach was characterized by a gently sloping (3.33 , se ¼ 0.10; Fig. 3d), microtidal beach with the greatest average value of Dean's Parameter U, which made it the only beach of intermediate state (U ¼ 2.14, se ¼ 0.01). The berm area extended from approximately 20 to 45 m from the base of the dunes towards the swash (Fig. 3d). Marina beach was the second widest beach (between 35 and 65 m wide) after Margate, with an average width of 49.06 m (se ¼ 0.83) and a median of 50 m. The position of the high tide line with respect to the dunes varied from 8 to 40 m (Fig. 3d); since the average position of the high tide line was 21.38 m (se ¼ 0.63) from the dunes and the median was 20 m, approximately 40% of the beachface at Marina was composed of dry beach,

Fig. 3. Distribution of ghost crab burrows across the beachface (shown as beach profiles) at Margate beach (a), Shelly beach (b), Lucien beach (c), and Marina beach (d). The segmented lines denote the transition from the upper beach to the berm area and from the berm area to the lower flat beach (where present), while the horizontal line at the top of each panel denotes the average position of the high tide line plus the upper and lower limits of its occurrence across the shore.

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while the remaining 60% of beach was exposed to the tides (Fig. 3d). Marina beach had the lowest average value of water content in the sediment (2%), and the greatest values of shear strength and penetration force (0.22 kg cm2, se ¼ 0.01 and 0.36 kg cm2, se ¼ 0.02, respectively). Sediment at Marina was medium sand (0.4 mm, se ¼ 0.002), the finest out of all sampled sites.

3.3. Spatial and temporal variations in habitat properties The morphological properties of the beach, including beach slope, beach morphodynamic state index (U), beach width, and elevation above LWST, varied substantially between sites throughout the study (Table 1; Fig. 2deg). Shelly and Lucien were the narrowest, steepest and highest beaches with the lowest morphodynamic state index values, as opposed to Margate and Marina, which were the widest, flattest beaches with the lowest elevation above LWST, and the highest morphodynamic state indices (Fig. 2deg). Fisher's LSD post-hoc tests results confirmed the following: beach slope was significantly different across all beaches (n ¼ 80e153 quadrats; P < 0.001) except between Margate and Marina (Fig. 2d); Dean's parameter U and beach width were significantly different across all beaches (n ¼ 96e168 quadrats; P < 0.001; Fig. 2e,f); beach elevation above LWST differed significantly between Lucien and Margate (n ¼ 140e169 quadrats; P ¼ 0.03) and between Lucien and Marina (n ¼ 140e155 quadrats; P ¼ 0.005; Fig. 2g). Temporal variations were also notable in the study (Table 1), with the beaches becoming steeper, narrower and higher in coincidence with the storm surge (between 30 and 31 March 2013), first at Marina, then at Lucien and Margate (Fig. 2deg). Shelly beach became narrower, although slope remained unchanged throughout the study (6.3 e6.5 ; Fig. 2d). Fisher's LSD post-hoc tests results confirmed that both beach slope (n ¼ 101e140 quadrats) and Dean's parameter U (n ¼ 117e156 quadrats) were significantly different on the third sampling day (immediately after the storm event) in comparison with all other days in the survey (P < 0.001; Fig. 2d,e). The maximum temporal variation in beach slope was 0.93 , while that in U did not exceed 0.10, with all the beaches retaining their morphodynamic state. While average beach width did not vary significantly between the first and second day of sampling, it did following the storm surge, being reduced by 12 m (n ¼ 117e156 quadrats; P < 0.001; Fig. 2f); beach elevation above LWST reached its greatest value during the storm, but three days after the storm it was substantially lower compared with the previous days (0.44 cm; n ¼ 117e156 quadrats; P ¼ 0.006eP < 0.001; Fig. 2g).

Significant spatial differences occurred for all the sediment properties that were measured during the study (Table 2; Fig. 4aed). Sediment moisture was greatest at Shelly beach (Fig. 4a), which was the narrowest beach with the most exposure to the tides (Fig. 3b); sediment moisture was not significantly different between Lucien and Marina (n ¼ 140e155 quadrats; Fisher's LSD post-hoc test P ¼ 0.70). Shelly also presented significantly lower values of sediment shear strength (n ¼ 93e165 quadrats) and penetration force (n ¼ 93e165 quadrats), and coarser sand (n ¼ 96e168 quadrats) compared with the remaining sites (Fisher's LSD post-hoc test P < 0.001; Table 2; Fig. 4bed). Marina beach presented the finest (n ¼ 96e168 quadrats), most compact (n ¼ 93e165 quadrats) and least penetrable (n ¼ 93e165 quadrats) sand in comparison with the other sites (Fisher's LSD post-hoc test P ¼ 0.02 e P < 0.001; Fig. 4bed). Sediment properties were obviously subject to significant temporal variations (Table 2). Sediment moisture decreased after the storm surge in comparison with the previous days (n ¼ 117e156 quadrats; Fisher's LSD post-hoc test P ¼ 0.01 e P < 0.001; Fig. 4a), possibly due to the strong winds characterizing the second part of the study (Fig. 2a). Sediment shear strength and penetration force also decreased over time, although by a magnitude not exceeding 0.06 kg cm2 in the case of the former and 0.09 kg cm2 in the case of the latter (n ¼ 117e156 quadrats; Fisher's LSD post-hoc test P ¼ 0.047 e P < 0.001; Fig. 4b,c). 3.4. Spatial and temporal variations in ghost crab burrow densities and sizes A total of 1879 ghost crab burrows were counted during the study, with an average burrow density of 0.14 m2 (se ¼ 0.01). There were significant negative correlations between burrow density and sea conditions and tides, including wave period (rs ¼ 0.094, P < 0.05) and tidal amplitude (rs ¼ 0.103, P < 0.05). Ghost crab populations responded to variations in morphodynamic state values and habitat dimensions. Greater values of Dean's parameter U positively influenced ghost crab burrow density (m2) and abundance per transect (rs ¼ 0.125 and 0.244, P < 0.05). The narrowing of the beach caused burrow densities to increase

Table 2 Summary of the GLMM analysis, contrasting sediment properties, ghost crab burrow density, and ghost crab burrow opening diameter between the beaches of Margate, Shelly, Lucien, and Marina during the study (surveys 1e4). The following co-variates were included in the analysis: elevation above low water spring tide (LWST); distance (m) upshore from LWST; and beach width (m).*P < 0.05,***P < 0.001. df

Table 1 Summary of the generalized linear mixed model (GLMM) analysis, contrasting morphological properties of the beach between the beaches of Margate, Shelly, Lucien, and Marina during the study (surveys 1e4).*P < 0.05,**P < 0.01,***P < 0.001. df

MS

F

Beach slope 3 216.85 91.69

Beach (Margate, Shelly, Lucien, Marina) Survey (29 March-02 April) 3 29.04 12.28 Beach  survey 9 35.36 14.95 Error 480 2.37 Beach width Beach (Margate, Shelly, Lucien, Marina) Survey (29 March-02 April) Beach  survey Error

3

Sig. df

MS

F

Sig.

Dean's parameter (U) *** 3 26.500 2393.2 ***

*** 3 0.004 0.3 *** 9 0.004 0.4 543 0.011 Beach elevation above LWST 11785.5 323.41 *** 3 3.01 3.09 *

3 4503.1 9 3279.5 544 36.4

123.57 *** 3 5.25 89.99 *** 9 1.11 544 0.97

5.39 1.14

**

MS

F

Sig. df

MS

F

Sig.

Sediment moisture Sediment shear strength 3 124.39 22.68 *** 3 0.08 13.06 ***

Beach (Margate, Shelly, Lucien, Marina) Survey (29 March-02 April) 3 51.28 9.35 *** Beach  survey 9 21.11 3.85 *** Error 540 5.49 Sediment penetration force Beach (Margate, Shelly, 3 0.36 23.59 *** Lucien, Marina) Survey (29 March-02 April) 3 0.16 10.34 *** Beach  survey 9 0.03 1.91 * Error 526 0.02 Burrow density Beach (Margate, Shelly, 3 0.29 8.34 *** Lucien, Marina) Survey (29 March-02 April) 3 0.36 10.45 *** Beach  survey 9 0.33 9.75 *** Error 540 0.03

3 0.06 9.58 *** 9 0.04 5.85 *** 526 0.01 Sediment mean grain size 3

0.338

337.25 ***

3 0.001 0.69 9 0.001 0.66 540 0.001 Burrow diameter 3 1061.20 12.49 3 1338.24 15.75 9 273.98 3.22 1860 84.97

*** *** ***

S. Lucrezi / Acta Oecologica 62 (2015) 18e31

25

Fig. 4. Comparison of sediment properties (aed), ghost crab burrow density (e), and ghost crab burrow opening diameter (f) between sites throughout the study. The segmented lines denote the days when sampling was carried out during the study period.

(rs ¼ 0.226, P < 0.05), and due to the strong inverse relationship between beach width and slope (rs ¼ 0.700, P < 0.05), burrow density also tended to increase with beach slope; nevertheless, steeper slopes reduced ghost crab burrow abundance per transect (rs ¼ 0.155, P < 0.05), and so did beach width, although weakly (rs ¼ 0.076, P ¼ ns). Burrow densities were affected by sediment properties, being positively associated with high values of sediment shear strength (rs ¼ 0.200, P < 0.05) and penetration force (rs ¼ 0.166, P < 0.05), and negatively associated with increasing sediment moisture (rs ¼ 0.089, P < 0.05) and grain size (rs ¼ 0.114, P < 0.05). Of all the burrows that were counted during the study, 35% were located at Marina beach, 29% at Lucien beach, 24% at Margate beach, and 12% at Shelly beach (Table 3). Ghost crab burrow density was greatest at Marina beach (0.17 m2, se ¼ 0.02), closely followed by Lucien beach (0.16 m2, se ¼ 0.02), while it was the smallest at Shelly beach (0.10 m2, se ¼ 0.01) and Margate beach (0.11 m2, se ¼ 0.01). Fisher's LSD post-hoc tests revealed that average burrow density was neither significantly different between Lucien and Marina (n ¼ 140e155 quadrats; P ¼ 0.60) nor between Shelly and Margate (n ¼ 96e168 quadrats; P ¼ 0.69). Ghost crab burrow densities also underwent substantial variations over time (Table 2; Fig. 4e). Burrow densities increased with the narrowing of the beach at each site (rs beach width vs. burrow density ¼ between 0.161 and 0.587, P < 0.05; Fig. 2f). During the third sampling day, there was a strikingly significant (99.5%) reduction in burrow density at Marina beach (only 12 burrows

were counted), possibly resulting from the negative influence of wind speed, which reached its peak on that day (rs ¼ 0.592, P < 0.05; Fig. 2a). By the following (and last) day of sampling, the burrow number at this location had resumed and increased by over twice the original value (Fig. 4e). Fisher's LSD post-hoc tests results confirmed the significant increase in ghost crab burrow densities over time in correspondence with the effects of the storm surge (n ¼ 117e156 quadrats; P ¼ 0.046 e P < 0.001). The opening diameter of ghost crab burrows ranged from 7 to 50 mm (Table 4), with an average value of 15.44 mm (se ¼ 0.22). Significant variations in averages occurred at both the spatial and temporal scales (Table 2), although these did not exceed 10 mm between sites and throughout the study (Fig. 4f). The largest burrows (50 mm) were found at Marina and Lucien, while burrow opening diameter did not exceed 40 mm at Shelly and Margate (Table 4). However, pooling all surveys, the greatest value of average burrow size was reported at Shelly beach (17.99 mm, se ¼ 0.65, median of 15 mm) and the smallest at Marina beach (14.62 mm, se ¼ 0.35, median of 10 mm; Table 4). Fisher's LSD posthoc tests showed that the average burrow size was similar between all beaches, excluding Shelly, where it was significantly greater than at all other sites (n ¼ 233e662 burrows; P < 0.01). Ghost crab burrows also tended to become larger with the narrowing of the beach (rs burrow opening diameter vs. beach width ¼ 0.067, P < 0.05). The greatest values of burrow size were reached at all sites on the third sampling day (Fig. 4f), following the storm surge; on that day, only 12 burrows were counted at Marina, although

26

S. Lucrezi / Acta Oecologica 62 (2015) 18e31

Table 3 Distribution of burrows (ind. m2) over the entire survey (N ¼ 1879), and summary of the GLMM analysis, contrasting ghost crab burrow densities between the beaches of Margate, Shelly, Lucien, and Marina, and surveys (1e4). All contrasts are done separately for three levels across the dune-swash gradient, including the upper beach which abutted the dunes, the berm area, and the lower flat beach.*P < 0.05,***P < 0.001. Margate 2

Upper beach: 0e20 m Berm area: 20e45 m Lower flat beach: > 45 m Entire beachface

Shelly

All beaches 2

Ind. m

se

Burrow number

(%)

Ind. m

se

Burrow number

(%)

Ind. m2

se

Burrow number

(%)

0.05 0.15 0.12 0.11

0.01 0.02 0.03 0.01

88 257 101 446

(20) (57) (23) (24)

0.14 0.003

0.02 0.01

231 2

(99) (1)

0.10

0.01

233

(12)

0.11 0.18 0.07 0.14

0.01 0.02 0.02 0.01

713 1063 103 1879

(38) (57) (5) (100)

Lucien

Upper beach: 0e20 m Berm area: 20e45 m Lower flat beach: > 45 m Entire beachface

Marina

Ind. m2

se

Burrow number

(%)

Ind. m2

se

Burrow number

(%)

0.10 0.22

0.02 0.02

159 379

(30) (70)

0.16

0.02

538

0.15 0.23 0.004 0.17

0.02 0.04 0.01 0.02

235 425 2 662

(35.5) (64.2) (0.3) (35)

Upper beach: 0e20 m

Beach Survey Beach  survey Error

(29)

Lower beach: > 45 m

Middle beach: 20e45 m

df

MS

F

Sig.

df

MS

F

Sig.

df

MS

F

Sig.

3 3 9 240

0.13 0.03 0.12 0.02

6.61 1.43 6.39

***

3 3 9 230

0.39 0.27 0.31 0.05

8.61 5.98 6.74

*** *** ***

1 3 2 47

0.03 0.09 0.01 0.02

1.28 4.14 0.61

*

***

these yielded the greatest average opening diameter in the study (22.17 mm, se ¼ 4.10, median of 22.5 mm). 3.5. Across-shore variations in ghost crab burrow densities and sizes Variations in ghost crab burrow densities were considerable across the beachface (Table 3; Fig. 3aed). Pooling all beaches, over half of the burrows were counted in the berm region between 20 and 45 m from the base of the dunes (Table 3). The upper beach (from the base of the dunes to 20 m towards the sea) hosted about 40% of the burrows, while only 5% were located on the lower flat beach, which did not exist at Shelly and Lucien (Table 3; Fig. 3b,c). Average burrow density across the beach was particularly high just below the average high tide mark at all sampled sites (Fig. 3a,c,d), with the exception of Shelly beach, where densities were greater above the average position of the high tide line (Fig. 3b). Burrow densities and distributions across the shore also varied according to the habitat properties of each site (Fig. 3aed), and variations across the shore were significantly different between beaches (Table 3). At Margate beach, which was the widest beach sampled, burrow density increased progressively from the base of the dunes to the berm region, reaching its greatest value at the interface between the berm region and the lower flat beach, and then decreased towards the sea (Table 3; Fig. 3a). Burrow density was here negatively correlated with both elevation and distance upshore from the LWST in a significant way (rs ¼ 0.166 and 0.257, P < 0.05). Ghost crab distribution followed the opposite trend at the narrowest beach (Shelly), where 99% of burrows were located on the upper beach, and only two burrows were counted on the narrow berm region immediately downshore (Table 3; Fig. 3b). Burrow density had a significant positive correlation with both elevation (rs ¼ 0.500, P < 0.05) and distance upshore from the LWST (rs ¼ 0.515, P < 0.05), and a strong negative correlation with sand moisture (rs ¼ 0.692, P < 0.05). Fisher's LSD post-hoc tests confirmed that on the upper beach, ghost crab burrow densities were significantly lower at Margate compared with Shelly and Marina (n ¼ 64e64 quadrats; P < 0.001). At Lucien and Marina, the berm region hosted the majority (70%) of the ghost crab burrows, with the highest density occurring

between 25 and 35 m from the base of the dunes (Table 3; Fig. 3c,d). In the berm, the average density of ghost crab burrows was not significantly different between these two beaches (n ¼ 64e64 quadrats; Fisher's LSD post-hoc test P ¼ 0.73), while it was between them and the remaining two sites (n ¼ 64e64 quadrats; Fisher's LSD post-hoc test P ¼ 0.02 e P < 0.001). Only two burrows were counted on the lower flat beach at Marina, as opposed to 101 burrows that were counted at Margate (n ¼ 19e35 quadrats; Fisher's LSD post-hoc test P ¼ 0.01; Table 3; Fig. 3a,d). Generally, the average ghost crab burrow size did not vary by more than 0.44 mm between the upper beach, the berm area, and the lower flat beach (Table 4). Trends across the shore were still notable at all sites: burrows became smaller with increasing proximity to the water, to less than 10 mm at the lowest limit of burrow occurrence (Table 4; Fig. 5aed); there was also a significant positive correlation between ghost crab burrow opening diameter and beach elevation above LWST (rs ¼ 0.079, P < 0.05). Fisher's LSD post-hoc tests showed that average burrow size on the upper beach was significantly greater at Shelly compared with the other sites (n ¼ 88e235 burrows; Fisher's LSD post-hoc test P < 0.01; Fig. 5aed); at the berm region on the other hand, burrow size was substantially smaller at Shelly beach (8 mm, se ¼ 1.00) compared with the remaining sites (between 15 and 16 mm; Table 4; Fig. 5aed).

4. Discussion The objective of this study was to quantify the effects of changing morphodynamic characteristics and habitat properties of sandy beaches on populations of an apex invertebrate predator, namely the ghost crab Ocypode. Densities, abundance, size and distribution of ghost crab burrows were compared across four warm-temperate, micro-tidal sandy beaches along the east coast of South Africa. Results show that ghost crabs display distinct variations in densities, abundance, size and distribution, based on a series of external environmental factors, including sea conditions and tides (wave period, tidal amplitude), habitat dimensions (beach slope, width, elevation, and distance from LWST), beach morphodynamic state index (Dean's parameter U), and sediment properties (shear strength, penetration force, moisture, and size).

S. Lucrezi / Acta Oecologica 62 (2015) 18e31

27

Table 4 Distribution of burrow opening diameters (mean, mm) over the entire survey (N ¼ 1879), and summary of the GLMM analysis, contrasting the ghost crab burrow opening diameter between the beaches of Margate, Shelly, Lucien, Marina, and surveys (1e4). All contrasts are done separately for three levels across the dune-swash gradient, including the upper beach which abutted the dunes, the berm area, and the lower flat beach.*P < 0.05,***P < 0.001. Margate

Upper beach: 0e20 m Berm area: 20e45 m Lower flat beach: > 45 m Entire beachface

Shelly

All beaches

mm

se

Max

Min

mm

se

Max

Min

mm

se

Max

Min

14.94 15.99 15.28 15.62

1.07 0.63 0.89 0.47

40 45 45 45

7 7 8 7

18.08 8.00

0.65 1.00

40 9

7 7

17.99

0.65

40

7

15.57 15.39 15.13 15.44

0.36 0.29 0.88 0.22

50 50 45 50

7 7 7 7

Lucien

Upper beach: 0e20 m Berm area: 20e45 m Lower flat beach: > 45 m Entire beachface

Marina

mm

se

Max

Min

mm

se

Max

Min

14.24 15.60

0.73 0.49

50 45

7 7

15.20

0.41

50

7

14.24 14.86 7.50 14.62

0.58 0.44 0.50 0.35

40 50 8 50

7 7 7 7

Upper beach: 0e20 m

Beach Survey Beach  survey Error a

Lower beach: > 45 m

Middle beach: 20e45 m

df

MS

F

3 3 9 697

161.17 253.18 205.00 88.17

1.83 2.87 2.32

Sig. * *

df

MS

F

Sig.

df

MS

F

3

241.49 1632.73 144.61 80.71

2.99 20.22 1.79

* ***

0 2 0 99

a 95.92

a 1.22

a

a

3 7 1049

Sig.

78.76

Due to limited data at Marina Beach, analysis was not computable.

Fig. 5. Distribution of ghost crab burrow opening diameters across the beachface (shown as beach profiles) at Margate beach (a), Shelly beach (b), Lucien beach (c), and Marina beach (d). The segmented lines denote the transition from the upper beach to the berm area and from the berm area to the lower flat beach (where present), while the horizontal line at the top of each panel denotes the average position of the high tide line plus the upper and lower limits of its occurrence across the shore.

Ghost crab burrow numbers were smallest at Shelly beach, a reflective beach which, at the time of the study, was also the narrowest and steepest beach, presenting the coarsest, wettest, least compact and most penetrable sediment. Marina beach, a wide beach of intermediate morphodynamic state with the finest, most compact and least penetrable sediment, hosted the largest ghost crab population (three times larger than that of Shelly beach). Expected distributions of ghost crabs across the shore were disrupted under hazardous conditions, mainly imposed by inundation and unfavorable sediment properties; at Shelly beach, ghost crabs were distributed largely on the uppermost portion of the beach, while the remaining beaches presented a more similar distribution,

centered in the berm area and just under the average position of the high tide line. As opposed to ghost crab burrow densities, burrow size increased as the conditions of the beach became less favorable. The average burrow opening diameter tended to be greater at Shelly beach compared with the remaining sites. Based on the results of this particular study, it can be concluded that the narrow, sloping and inundation-prone Shelly beach represented the least hospitable environment for the ghost crabs, in comparison with the wider beaches sampled. Sandy beach macrofauna has been established to be affected mainly by three factors, which are sediment texture (e.g. grain size) and movement (e.g. accretion and erosion dynamics), swash climate (e.g. wave period,

28

S. Lucrezi / Acta Oecologica 62 (2015) 18e31

water turbulence and movement over and in the beach surface), and aerial exposure and shifting moisture content on the beach surface (McLachlan and Brown, 2006). Research that summarizes the global patterns of macrofauna distributions on sandy beaches has demonstrated that the abundance of species has a significant inverse relation with beach slope and sand particle size, increasing from microtidal reflective to microtidal dissipative conditions (Defeo and McLachlan, 2013). Although this study focused on the variations in ghost crab population dynamics across a narrow range of morphodynamic states (between U ¼ 1 and U ¼ 2.5), within this range ghost crabs followed a similar pattern to the one described by Defeo and McLachlan (2013) for sandy beach macrofauna across the whole gradient of beach morphodynamic states. However, results from this study partially contradict those of previous research on the population dynamics of ghost crabs and other supratidal to mid-intertidal crustaceans in response to changing beach morphodynamic states; such research identified either no clear response of populations to beach type (e.g. Defeo
n et al., 2001; Contreras et al., 2003; Defeo et al., et al., 1997; Quijo 2003; Defeo and Martínez, 2003; Caetano et al., 2006; Souza et al., 2008) or a clearly opposite response to that suggested by
mez, 2005; Defeo the habitat harshness hypothesis (Defeo and Go
mez and Defeo, 2012; Barboza et al., and McLachlan, 2011; Go
n et al. (2001), who studied the distribution and 2013). Quijo habitat structure of Ocypode gaudichaudii along the western coast of South America, found that spatial variability of ghost crabs across beaches was unrelated to beach morphodynamic state. They suggested that the generalization that beach types explain spatial variation of macrobenthic populations is typically applicable to species of the middle and lower intertidal zones, and not to Ocypode gaudichaudii, which is principally distributed above the high
n et al. (2001), Souza et al. (2008) tide mark. Similarly to Quijo discovered no significant relationship between ghost crab (Ocypode quadrata) abundance and beach morphodynamic state, suggesting that other factors, such as waves and food availability, are likely to influence ghost crab distributions. Research by Schoeman et al. (2003) on the supratidal amphipod Talorchestia capensis in South Africa revealed that species abundance was greater on a pebbly beach than on an exposed dissipative beach. Similarly, research by Veloso and Cardoso (2001), Cardoso
mez (2005), Go
mez and and Defeo (2003, 2004), Defeo and Go Defeo (2012), and Barboza et al. (2013), on the population dynamics of the supratidal amphipod Atlantorchestoidea brasiliensis and the supratidal isopod Excirolana braziliensis on the Atlantic coast of South America, identified a trend of species abundance, increasing from dissipative to reflective beaches, as opposed to other truly intertidal crustacean species. A recent study by Defeo and McLachlan (2011), aimed to explain macrofauna community structure according to beach type on sandy beaches of the eastern coast of South America, confirmed a similar trend for Ocypode quadrata, a mainly supratidal species of ghost crab, thus refuting the applicability of the habitat harshness hypothesis to ghost crabs and other supratidal crustaceans like Atlantorchestoidea brasiliensis. Defeo and McLachlan (2011) justified this general trend by a mixture of behavioral and life history traits that are typical of crustaceans, including high mobility (particularly of scavengers/ predators), great burrowing abilities, the ability to cope with dynamic swash, and the tough exoskeleton. These factors were identified as being key to the success of crustaceans (as in this case Ocypode) at overcoming the harsh conditions of reflective beaches.
mez (2005) argued that both the swash exclusion Defeo and Go hypothesis and the habitat harshness hypothesis are uncritically accepted under two circumstances, namely where characteristics defining communities are related to morphodynamics, and where only truly intertidal species that are directly affected by the swash

climate are being analyzed. These hypotheses do not hold for supratidal and upper intertidal species, which show relative independence from the swash climate and beach morphodynamics.
mez (2005) also explained the Defeo et al. (2003) and Defeo and Go exhibition of greater fitness indicators by supratidal species on reflective beaches by means of life history traits, including larval development. On the one hand, supratidal species tend to show direct development (small reproductive effort, aplanktonic larval phase, and parental care of eggs and embryos) which is independent from the swash climate. On the other hand, truly intertidal species are either broadcast spawners with planktonic larvae (e.g. clams) or have brooding females and planktonic larvae (e.g. crabs); this group is likely to depend on swash climate throughout the life span. Ghost crabs sit astride these two groups, having brooding females with planktonic larvae, but not being strictly confined to the intertidal; they can show different patterns of distribution depending on species, geographic location, and sympatry with other species. While ghost crabs are principally reported as being supratidal semi-terrestrial brachyurans, they also show a strong intertidal component and, to some extent, dependence on the swash (particularly juveniles; Lucrezi and Schlacher, 2014). A key step in the life cycle of ghost crabs, and also one that determines subsequent population structure, is the passage from the pelagic larval phase to the recruitment of megalopae (a changeover phase between the last larval phase and the first crab stage) onto the beach, transported by the swash and deposited on the sand by the receding tides (Lucrezi and Schlacher, 2014). Although megalopae possess anatomical features that allow them to withstand the harsh transition from the sea to the beach, recruitment remains a vulnerable stage in the life cycle, since it is marked by the moulting of megalopae into the first crab stage, which takes place at the surfebeach interface and in the intertidal zone. Therefore, it may be assumed that ghost crab populations are particularly affected on reflective beaches, resulting in shifts in population structure. Nevertheless, it remains difficult to have a universal and clearcut explanation of the response of ghost crab populations to the physical environment, as the ecology of various species needs to be taken into account. Recent work by Dugan et al. (2013) also highlighted the importance of accounting for tidal, daily, semi-lunar, seasonal, annual, and episodic patterns of distribution across the shore that are typical of macrofauna, including ghost crab species. Further, there can be indirect effects of harsher habitat conditions on ghost crab populations, such as reductions in food availability and supply resulting from low productivity on reflective beaches (McLachlan and Brown, 2006). Such low productivity is likely to affect all levels within a population (from juveniles to adults) and various, if not all, levels within the catholic diet of ghost crabs, which ranges from stranded seaweed to animal carcasses, live vertebrate and invertebrate prey, and cannibalism (Lucrezi and Schlacher, 2014). The larger average size of ghost crabs (inferred from measurements of ghost crab burrow opening diameters) at Shelly beach in comparison with the other sites, and the increase in average burrow opening diameter with decreasing beach width, support the inverse relationship between macrofauna abundance and body size depicted in studies of macrofauna distributions on sandy beaches that have been carried out in the last 15 years (Veloso and Cardoso, 2001; Cardoso and Defeo, 2003, 2004; Defeo and Cardoso,
mez, 2005; McLachlan and Dorvlo, 2007b; 2004; Defeo and Go Defeo and McLachlan, 2011, 2013). Although some of these studies have dealt with average individual body size from pooled macrofauna species, much of the research has also included surveys that were based on a single species such as the mole crab Emerita brasiliensis, the amphipod Atlantorchestoidea brasiliensis, and the

S. Lucrezi / Acta Oecologica 62 (2015) 18e31

isopod Excirolana braziliensis (Veloso and Cardoso, 2001; Cardoso and Defeo, 2003, 2004; Defeo and Cardoso, 2004; Defeo and
mez, 2005). In the case of intertidal species, researchers have Go concluded that smaller individuals are more sensitive to the harsher living conditions that are provided by reflective beaches, where species abundance is also low, as opposed to more dissipative beaches, which generally have a greater abundance of individuals and where individual size is smaller (Defeo and Cardoso, 2004). In the case of supratidal species, however, abundance and size tend to increase together from dissipative to reflective beaches
mez, 2005). (Defeo and Go Ghost crab populations occurring on reflective beaches that are characterized by frequent swash, submersion by the tides, coarse sand, and steep slope can be weakened by the susceptible distribution of juveniles on the lower beach, which is a recurring pattern in the genus; such distribution is dictated primarily by lower tolerance of dry conditions on the upper beach, accompanied by territoriality of adults and cannibalism (Lucrezi and Schlacher, 2014). The forced exposure of younger crabs to the harsher limits of distribution (see also the habitat favorability hypothesis; Defeo and McLachlan, 2005) can reduce survival rates among juveniles, thus increasing the average size (yet reducing density) of individuals in the population. In this study, unexpected values of ghost crab burrow densities, abundance and distribution were reported for Lucien beach and Margate beach. Lucien beach, morphologically closer to Shelly beach, hosted the second largest population of ghost crabs; the distribution of ghost crabs across the shore was dissimilar between Shelly and Lucien, with the latter beach presenting a similar distribution to that at Marina and Margate. Margate, morphologically close to Marina and also the widest and flattest beach that was sampled in this study, was the site yielding the second lowest values of ghost crab burrow density and abundance. Trends in density and abundance of ghost crabs across beach types have been unclear in other instances (Defeo and McLachlan, 2011), and while the relationship between species abundance and beach morphodynamic state can be significant (as in the case of this study), individual physical variables may be more useful predictors of density and abundance than compound indices (Nel, 2001; Defeo and
mez, 2005; McLachlan and Dorvlo, 2005). Based on the findGo ings of the present study, individual physical components may have played a key role in explaining ghost crab population dynamics. Aside from the strong influence of the Dean's parameter U on burrow densities and abundance, important predictors of ghost crab burrow abundance were, in decreasing order, sediment moisture, sediment size, sediment shear strength, beach slope, and sediment penetration force. However, there are two additional main factors that need to be considered in the context of this study, namely i) the average position of the high tide mark across the beachface, which is regarded as an indication of the degree of exposure of the beach to the tides; and ii) the ecology of the various species of ghost crab inhabiting the beaches that were studied, in particular the distribution of individuals across the beachface. Although the generalization is that ocypodid crabs are supratidal species, occurring around or above the driftline of tropical, subtropical and warm-temperate sandy beaches worldwide (e.g. Barros, 2001; Defeo and McLachlan, 2005, 2011; Moss and McPhee, 2006; Lucrezi et al., 2009), the spacing of individuals of Ocypode from the surf to the dunes and beyond varies substantially between species across space (populations and geographic locations) and time (tidal, daily, semi-lunar, seasonal, annual, and episodic movements) (Dugan et al., 2013; Lucrezi and Schlacher, 2014). Species occurring on the beaches that were examined here are mainly intertidal and lower supratidal, showing peaks of abundance around the mean tide level and frequently feeding on

29

stranded material; these species tend not to occupy the upper portion of the dry beach (Grubb, 1971; Jones, 1972; Hartnoll, 1975; Berry, 1976; Dye et al., 1981; Haig, 1984). Brazeiro and Defeo (1996) described how microtidal sandy beaches are wave-dominated and can be subject to strong and unpredictable increases in tidal ranges over short time, for example
mez and Defeo (1999) later argued that through storm surges; Go steep slopes on the lower shore of microtidal reflective sandy beaches can alleviate the effects of wave-dominated tides, thus providing a more stable and safer environment for supratidal species, compared with dissipative beaches (habitat safety hy
mez, 2005). The significant positive correpothesis; Defeo and Go lation between ghost crab burrow density and abundance and Dean's parameter U points to the opposite scenario in the case of this particular survey. However, the present study considered a narrow span of beach morphodynamic states. Of the beaches that were examined, three were microtidal reflective and one intermediate, and all beaches presented notable differences and similarities in habitat features, which may have played a critical role in shaping variations in ghost crab populations. For example, while the steep slope at Shelly beach (reflective) did not preclude oncoming tides from inundating the beach, the dry and inundationfree backshore at Margate beach (also reflective) did not support a high abundance of ghost crab burrows as it would have been expected. Regardless of beach morphodynamic state, Marina beach (intermediate) and Lucien beach (reflective) may have offered an ideal 50:50 dry beach:wet beach ration; Shelly beach (reflective) and Margate beach (reflective), on the other hand, represented the lower and upper boundaries of the dry beach:wet beach ration, with Shelly beach being almost entirely exposed to inundation by the tides, and Margate being the driest of all the beaches that were sampled. Although possible, this explanation may still be too simplistic, given the importance of multiple factors in explaining the way ghost crab populations are regulated. 5. Conclusions and study limitations The results from this study demonstrate that, even at a very small geographical scale, great variability exists in the density and distribution of macrofauna, in this case ghost crabs, between sandy beaches with different habitat properties and morphodynamic index. The author recognizes the limitations of this study and urges future research to avoid them. The choice of temporal and spatial aspects in the study design (i.e. low temporal and spatial replication) may have been inadequate, given the limited sampling dates (instantaneous sampling) and the comparison of only four beaches
mez, 2005; Defeo and McLachlan, 2005). This choice (Defeo and Go may have affected accuracy and precision in defining true densities, abundance and distribution of ghost crab populations across the beaches that were studied (Haynes and Quinn, 1995; Defeo and
mez, 2005; Defeo and McLachlan, 2005; Schlacher and Go Thompson, 2013b). Therefore, the interpretation of the results and the inferences made need to be considered with caution. The chief purpose of appropriate temporal replication in the case of studies such as this is to identify environmental factors influencing burrow density (Lucrezi et al., 2009). For sampling designs aimed to determine the spatial structure of sandy beach macrofauna at the community level, low temporal replication is merely unacceptable, due to the highly variable zonation of communities (Schlacher and Thompson, 2013b). However, low temporal replication has been accepted for rapid assessment schemes using a single species or genus, including ghost crabs (Barros, 2001; Lucrezi et al., 2009). Therefore, the results reported here can still represent valuable short timescale information, also given the variable nature of sandy

30

S. Lucrezi / Acta Oecologica 62 (2015) 18e31

beach populations down to fine (e.g. diel) temporal scales (Schlacher et al., 2008). The span of beach morphodynamic state indices that were considered in this study was limited (three reflective beaches and one intermediate beach), particularly in the light of the overall aim. Stretching sampling to cover a wider array of beaches, and thus of Dean's parameter values U between the lower and higher extremes, would have yielded more exhaustive results, perhaps leading the author to draw different conclusions from the ones reported here. Nevertheless, research carried over a limited spatial scale (two to five sites) has demonstrated that small variations in beach morphodynamic index (as small as 0.1) can cause significant variation in macrofauna community structure and phenotype (Harris et al., 2011b; Veas et al., 2014). The study was affected by a storm event, which changed the habitat properties of the beach during sampling, possibly compromising the inferences of the results presented here. Episodic environmental events such as storm surges are well documented to alter the spatial and temporal patterns of abundance and richness of macrofauna species, including ghost crabs, on sandy beaches (Defeo et al., 2003; Hobbs et al., 2008; Lucrezi et al., 2010; Harris et al., 2011b). In the case of ghost crabs, harsh conditions on the beach generated by the occurrence of storms are usually avoided by migration into the vegetated dunes (where present) for shelter (Hobbs et al., 2008). Coupled with limited temporal scales of analysis, such unpredictable events as storms are likely to render the interpretation of the physical and biological variations typical of sandy beaches more difficult (Defeo et al., 2003). Storm events typically erode beaches, thus causing an increase in slope and height and a decrease in width, making the beaches more reflective while still retaining their main morphodynamic state (Lucrezi et al., 2010; Harris et al., 2011b; this study). According to Harris et al. (2011b), the tendency of beaches to become more reflective during storm events is one of the principal causes of variations in macrofauna community structure. The results from this study seem to support this finding, since ghost crab populations at Marina, the only intermediate beach within the small range of morphodynamic indices investigated here, was the only beach where ghost crab densities were not immediately affected during the storm (second sampling day). The author discussed the difficulty in defining clear-cut responses of ghost crab populations to physical drivers, based on the recognition that ghost crabs are not strictly supratidal, and that distribution across the entire beachface and beyond is variable according to species and populations. This study has only dealt with three of the known species of Ocypode; these species are known to be intertidal to lower supratidal. Future research would benefit from comparisons between more intertidal and supratidal populations and species of ghost crabs across beach types. Recent work by Gonçalves et al. (2013) on the population dynamics of tylid isopods and talitrid amphipods in Portugal and Tunisia has highlighted the importance of studying the distribution and bioecology of sandy beach macrobenthos at various levels within a genus (e.g. comparing distinct populations within a species, and comparing species between beaches or geographic regions). The conclusions drawn from this study are merely based on observations of changes in ghost crab population density, abundance, size and distribution across the shore, but there are a number of key life history traits in the genus that are worth exploring, and can be used to assess the variability of population structure across beaches with different morphodynamic and habitat characteristics. These include, for example, larval dispersal into pelagic zones and recruitment back on beaches (Defeo and
mez, 2005; Defeo and McLachlan, 2005; Gonçalves et al., 2013; Go McDermott, 2013). Furthermore, while environmental tolerances

(e.g. salinity tolerance ranges) are not known for a large proportion of macroinvertebrate species (Schlacher and Thompson, 2013b), these are accessible for a number of ghost crab species from various geographic locations, and should be employed to make interpretations about the response of ghost crab species to environmental gradients more appropriate (Lucrezi and Schlacher, 2014). Although most of the limitations of this study were acknowledged before sampling, logistical and financial constraints simply impeded the actuation of a more appropriate sampling strategy. Therefore, the author would like to consider this study as a ‘launching platform’, with the hope to stimulate further research on the issues discussed here.

Acknowledgments Gratitude is extended to Prof Melville Saayman and Prof Peet Van der Merwe at TREES for giving their full support to the project, Dr Marco Scholtz at TREES for fieldwork, Prof Piet Van Deventer at the Faculty of Natural Sciences of the North-West University for supplying monitoring gear, Dr Suria Ellis at the Statistical Consultation Services of the North-West University for statistical advice, and the staff of TREES and the North-West University for assisting with logistics and minor matters. This project was funded by TREES and by the National Research Foundation (NRF).

References
mez, J., Lercari, D., Defeo, O., 2013. Disentangling diversity patterns Barboza, F.R., Go in sandy beaches along environmental gradients. PloS One 7 (7), e40468. http:// dx.doi.org/10.1371/journal.pone.0040468. Barros, F., 2001. Ghost crabs as a tool for rapid assessment of human impacts on exposed sandy beaches. Biol. Conserv. 97, 399e404. Bascom, W., 1980. Waves and Beaches: the Dynamics of the Ocean Surface. Anchor Press, Garden City, NY, p. 366. Berry, P.P., 1976. Natal's ghost crabs. Victims of the Middle East conflict? Afr. Wildl. 30, 35e37. Blott, S.J., Pye, K., 2001. GRADISTAT: a grain size distribution and statistics package for the analysis of unconsolidated sediments. Earth Surf. Process. Landforms 26, 1237e1248. Brazeiro, A., 2001. Relationship between species richness and morphodynamics in sandy beaches: what are the underlying factors? Mar. Ecol. Prog. Ser. 224, 35e44. Brazeiro, A., Defeo, O., 1996. Macroinfauna zonation in microtidal sandy beaches: is it possible to identify patterns in such variable environments? Estuar. Coast. Shelf Sci. 42, 523e536. Caetano, C.H.S., Cardoso, R.S., Veloso, V.G., Silva, E.S., 2006. Population biology and secondary production of Excirolana braziliensis (Isopoda: Cirolanidae) in two sandy beaches of Southeastern Brazil. J. Coast. Res. 22 (4), 825e835. Cardoso, R.S., Defeo, O., 2003. Geographical patterns in reproductive biology of the pan-American sandy beach isopod Excirolana braziliensis. Mar. Biol. 143, 573e581. Cardoso, R.S., Defeo, O., 2004. Biogeographic patterns in life history traits of the pan-American sandy beach isopod Excirolana braziliensis. Estuar. Coast. Shelf Sci. 61, 559e568. Contreras, H., Jaramillo, E., Duarte, C., McLachlan, A., 2003. Population abundances, growth and natural mortality of the crustacean macroinfauna at two sandy beach morphodynamic types in Southern Chile. Rev. Chileana Hist. Nat. 76, 543e561. Day, J.H., 1969. A Guide to Marine Life on South African Shores. AA Balkema, Cape Town, South Africa, p. 300. Defeo, O., Brazeiro, A., de Alava, A., Riestra, G., 1997. Is sandy beach macroinfauna only physically controlled? Role of substrate and competition in isopods. Estuar. Coast. Shelf Sci. 45, 453e462. Defeo, O., Cardoso, R., 2004. Latitudinal patterns in abundance and life-history traits of the mole crab Emerita brasiliensis on South American sandy beaches. Divers. Distributions 10, 89e98.
mez, J., 2005. Morphodynamics and habitat safety in sandy beaches: Defeo, O., Go life-history adaptations in a supralittoral amphipod. Mar. Ecol. Prog. Ser. 293, 143e153.
mez, J., Lercari, D., 2001. Testing the swash exclusion hypothesis in Defeo, O., Go sandy beach populations: the mole crab Emerita brasiliensis in Uruguay. Mar. Ecol. Prog. Ser. 212, 159e170.
mez, J., 2003. The role of morphodynamics in structuring Defeo, O., Lercari, D., Go sandy beach populations and communities: what should be expected? J. Coast. Res. 35 (Special Issue), 352e362.

S. Lucrezi / Acta Oecologica 62 (2015) 18e31 Defeo, O., Martínez, G., 2003. The habitat harshness hypothesis revisited: life history of the isopod Excirolana braziliensis in sandy beaches with contrasting morphodynamics. J. Mar. Biological Assoc. U. K. 83, 331e340. Defeo, O., McLachlan, A., 2005. Patterns, processes and regulatory mechanisms in sandy beach macrofauna: a multi-scale analysis. Mar. Ecol. Prog. Ser. 295, 1e20. Defeo, O., McLachlan, A., 2011. Coupling between macrofauna community structure and beach type: a deconstructive meta-analysis. Mar. Ecol. Prog. Ser. 433, 29e41. Defeo, O., McLachlan, A., 2013. Global patterns in sandy beach macrofauna: species richness, abundance, biomass and body size. Geomorphology. http://dx.doi.org/ 10.1016/j.geomorph.2013.04.013. Defeo, O., McLachlan, A., Schoeman, D.S., Schlacher, T.A., Dugan, J., Jones, A., Lastra, M., Scapini, F., 2009. Threats to sandy beach ecosystems: a review. Estuarine. Coast. Shelf Sci. 81, 1e12. Dugan, J.E., Hubbard, D.M., Quigley, B.J., 2013. Beyond beach width: steps toward identifying ecological envelopes with geomorphic features and datums for sandy beach ecosystems. Geomorphology 199, 95e105. Dye, A.H., McLachlan, A., Wooldridge, T., 1981. The ecology of sandy beaches in Natal. South Afr. J. Zoology 16, 200e209. Everard, M., Jones, L., Watts, B., 2010. Have we neglected the societal importance of sand dunes? An ecosystem services perspective. Aquatic Conservation: Mar. Freshw. Ecosyst. 20, 476e487. Gibbs, R.J., Matthews, M.D., Link, D.A., 1971. The relationship between sphere size and settling velocity. J. Sediment. Petrol. 41, 7e18.
nez, L., Yannicelli, B., 1997. Variability of zonation patterns in temperate Gime microtidal Uruguayan beaches with different morphodynamic types. Mar. Ecol. Prog. Ser. 160, 197e207.
mez, J., Defeo, O., 1999. Life history of the sandhopper Pseudorchestoidea brasiGo liensis (Amphipoda) in sandy beaches with contrasting morphodynamics. Mar. Ecol. Prog. Ser. 182, 209e220.
mez, J., Defeo, O., 2012. Predictive distribution modeling of the sandy-beach Go supralittoral amphipod Atlantorchestoidea brasiliensis along a macroscale estuarine gradient. Estuarine. Coast. Shelf Sci. 98, 84e93.
cio, P.M., Marques, J.C., 2013. Talitrid and Tylid crustaceans Gonçalves, S.C., Anasta bioecology as a tool to monitor and assess sandy beaches' ecological quality condition. Ecol. Indic. 29, 549e557. Grubb, P., 1971. Ecology of terrestrial decapods crustaceans on Aldabra. Philosophical Trans. R. Soc. Lond. 260, 411e416. Haig, J., 1984. Land and freshwater crabs of the Seychelles and neighbouring islands. In: Stoddart, D.R. (Ed.), Biogeography and Ecology of the Seychelles Islands. Dr W Junk Publishers, The Hague, pp. 123e139. Hancock, G.R., Mueller, R.O., 2010. The Reviewer's Guide to Quantitative Methods in the Social Sciences. Routledge, New York. Harris, L.R., Nel, R., Schoeman, D.S., 2011a. Mapping beach morphodynamics remotely: a novel application tested on South African sandy shores. Estuar. Coast. Shelf Sci. 92, 78e89. Harris, L.R., Nel, R., Smale, M., Schoeman, D.S., 2011b. Swashed away? Storm impacts on sandy beach macrofaunal communities. Estuar. Coast. Shelf Sci. 94, 210e221. Hartnoll, R.G., 1975. The Grapsidae and Ocypodidae (Decapoda: Brachyura) of Tanzania. J. Zool. 177, 305e328. Haynes, D., Quinn, G.P., 1995. Temporal and spatial variability in community structure of a sandy intertidal beach, Cape Paterson, Victoria, Australia. Mar. Freshw. Res. 46, 931e942. Hobbs, C.H., Landry, C.B., Perry, J.E., 2008. Assessing anthropogenic and natural impacts on ghost crabs (Ocypode quadrata) at Cape Hatteras National Seashore, North Carolina. J. Coast. Res. 24, 1450e1458. Jones, D.A., 1972. Aspects of the ecology and behaviour of Ocypode ceratophthalmus (Pallas) and O. kuhlii de Haan (Crustacea: Ocypodidae). J. Exp. Mar. Biol. Ecol. 8, 31e43. Lucrezi, S., Saayman, M., Van der Merwe, P., 2014. Impact of off-road vehicles (ORVs) on ghost crabs of sandy beaches with traffic regulations: a case study of Sodwana Bay, South Africa. Environ. Manage. 53, 520e533. Lucrezi, S., Schlacher, T.A., 2014. The ecology of ghost crabs. Oceanogr. Mar. Biol. An Annu. Rev. 52, 201e256. Lucrezi, S., Schlacher, T.A., Robinson, W., 2010. Can storms and shore armouring exert additive effects on sandy-beach habitats and biota? Mar. Freshw. Res. 61, 951e962. Lucrezi, S., Schlacher, T.A., Walker, S.J., 2009. Monitoring human impacts on sandy shore ecosystems: a test of ghost crabs (Ocypode spp.) as biological indicators on an urban beach. Environ. Monit. Assess. 152, 413e424. McArdle, S., McLachlan, A., 1991. Dynamics of the swash zone and effluent line on sandy beaches. Mar. Ecol. Prog. Ser. 76, 91e99. McArdle, S., McLachlan, A., 1992. Sandy beach ecology: swash features relevant to the macrofauna. J. Coast. Res. 8, 398e407. McCulloch, C.E., Neuhaus, J.M., 2013. Generalized linear mixed models. In: ElShaarawi, A.H., Piegorsch, W.W. (Eds.), Encyclopedia of Environmetrics, second ed. John Wiley and Sons Ltd, Hoboken, NJ. http://dx.doi.org/10.1002/ 9780470057339.vag009.pub2. McDermott, J.J., 2013. The distribution of Ocypode quadrata, Atlantic ghost crab (Decapoda: Brachyura: Ocypodidae) megalopae, beyond the presumptive northern boundary of adult populations in the northwest Atlantic. Northeast. Nat. 20 (4), 578e586. McLachlan, A., 1980. Occurrence of ghost crabs Ocypode spp. in the Eastern Cape. South Afr. J. Zoology 15, 57e58.

31

McLachlan, A., 1990. Dissipative beaches and macrofauna communities on exposed intertidal sands. J. Coast. Res. 6, 57e71. McLachlan, A., Brown, A.C., 2006. The Ecology of Sandy Shores. Academic Press, Burlington, p. 392. McLachlan, A., Dorvlo, A., 2005. Global patterns in sandy macrobenthic communities. J. Coast. Res. 21, 674e687. McLachlan, A., Dorvlo, A., 2007a. Global patterns in sandy beach macrobenthic communities: biological factors. J. Coast. Res. 23, 1081e1087. McLachlan, A., Dorvlo, A., 2007b. Species d area relationships for sandy beach macrobenthos in the context of intertidal width. Oceanologia 49, 91e98. McLachlan, A., Jaramillo, E., Defeo, O., Dugan, J., De Ruyck, A., Coetzee, P., 1995. Adaptations of bivalves to different beach types. J. Exp. Mar. Biol. Ecol. 187, 147e160. McLachlan, A., Jaramillo, E., Donn, T.E., Wessels, F., 1993. Sandy beach macrofauna communities and their control by the physical environment: a geographical comparison. J. Coast. Res. 15, 27e38. Moss, D., McPhee, D.P., 2006. The impacts of recreational four-wheel driving on the abundance of the ghost crab (Ocypode cordimanus) on subtropical sandy beaches in SE Queensland. Coast. Manag. 34, 133e140. Nel, P., 2001. Physical and Biological Factors Structuring Sandy Beach Macrofauna Communities. PhD Thesis. University of Cape Town. Noriega, R., Schlacher, T.A., Smeuninx, B., 2012. Reductions in ghost crab populations reflect urbanization of beaches and dunes. J. Coast. Res. 28, 123e131.
n, P., Jaramillo, E., Contreras, H., 2001. Distribution and habitat structure of Quijo Ocypode gaudichaudii H. Milne Edwards and Lucas, 1843, in sandy beaches of northern Chile. Crustaceana 74, 91e103. Quinn, G.P., Keough, M.J., 2002. Experimental Design and Data Analysis for Biologists. Cambridge University Press, Cambridge, UK, p. 537. Sakai, K., Türkay, M., 2013. Revision of the genus Ocypode with the description of a new genus, Hoplocypode (Crustacea: Decapoda: Brachyura). Memoirs Qld. MuseumeNature 56, 665e793. Scapini, F., Morgan, E., 2002. Bioassays for estimation of beach stability and ecosystem quality. In: Scapini, F. (Ed.), Baseline Research for the Integrated Sustainable Management of Mediterranean Sensitive Coastal Ecosystems: a Manual for Coastal Managers, Scientists and All Those Studying Coastal Processes and Management in the Mediterranean. Istituto Agronomico per l’Oltremare, Florence, pp. 120e122. Schlacher, T.A., Holzheimer, A., Stevens, T., Rissik, D., 2011. Impacts of the ‘Pacific Adventurer’ oil spill on the macrobenthos of subtropical sandy beaches. Estuaries Coasts 34, 937e949. Schlacher, T.A., Lucrezi, S., 2010. Compression of home ranges in ghost crabs on sandy beaches impacted by vehicle traffic. Mar. Biol. 157, 2467e2474. Schlacher, T.A., Noriega, R., Jones, A., Dye, T., 2012. The effects of beach nourishment on benthic invertebrates in eastern Australia: impacts and variable recovery. Sci. Total Environ. 435e436, 411e417. Schlacher, T.A., Schoeman, D.S., Dugan, J., Lastra, M., Jones, A., Scapini, F., McLachlan, A., 2008. Sandy beach ecosystems: key features, sampling issues, management challenges and climate change impacts. Mar. Ecol. 29, 70e90. Schlacher, T.A., Schoeman, D.S., Jones, A., Dugan, J.E., Hubbard, D., Defeo, O., Peterson, C.H., Weston, M., Maslo, B., Olds, A., Scapini, F., Nel, R., Harris, L., Lucrezi, S., Lastra, M., Huijbers, C., Connolly, R., 2014. Metrics to assess ecological condition, change, and impacts in sandy beach ecosystems. J. Environ. Manag. 144C, 322e335. Schlacher, T.A., Thompson, L.M.C., 2013a. Environmental control of community organisation on ocean-exposed sandy beaches. Mar. Freshw. Res. 64 (2), 119e129. Schlacher, T.A., Thompson, L.M.C., 2013b. Spatial structure on ocean-exposed sandy beaches: faunal zonation metrics and their variability. Mar. Ecol. Prog. Ser. 478, 43e55. Schlacher, T.A., Thompson, L.M.C., Price, S., 2007. Vehicles versus conservation of invertebrates on sandy beaches: mortalities inflicted by off-road vehicles on ghost crabs. Mar. EcologyeAn Evol. Perspect. 28, 354e367. Schoeman, D.S., Wheeler, M., Wait, M., 2003. The relative accuracy of standard estimators for macrofaunal abundance and species richness derived from selected intertidal transect designs used to sample exposed sandy beaches. Estuar. Coast. Shelf Sci. 58 (Suppl.), 5e16. Short, A.D., 1996. The role of wave height, period, slope, tide range and embaymentisation in beach classifications: a review. Rev. Chileana Hist. Nat. 69, 589e604. Short, A.D., Wright, L.D., 1983. Physical variability of sandy beaches. In: McLachlan, A., Erasmus, T. (Eds.), Sandy Beaches as Ecosystems. Dr W Junk Publishers, The Hague, pp. 133e144. cio, P.H., da Rocha, C.M.C., 2008. Distribution of Souza, J.R.B., Lavoie, N., Bonifa Ocypode quadrata (Fabricius, 1787) on sandy beaches of northeastern Brazil. Atl^ antica, Rio Gd. 30, 139e145. Valero-Pacheco, E., Alvarez, F., Abarca-Arenas, L.G., Escobar, M., 2007. Population density and activity pattern of the ghost crab, Ocypode quadrata, in Veracruz, Mexico. Crustaceana 80, 313e325.
ndez-Miranda, E., Quin ~ ones, R.A., 2014. Body shape and burial Veas, R., Herna behavior of the sand crab Emerita analoga (Stimpson 1857) in a reflective to intermediate morphodynamic range of sandy beaches. Mar. Biol. http:// dx.doi.org/10.1007/s00227-014-2510-y. Veloso, V.G., Cardoso, R.S., 2001. The effect of morphodynamics on the spatial and temporal variation of the macrofauna of three sandy beaches on the Rio de Janeiro state, Brazil. J. Mar. Biological Assoc. U. K. 81, 369e375. Wright, L.D., Short, A.D., 1984. Morphodynamic variability of surf zones and beaches: a synthesis. Mar. Geol. 56, 93e118.