Abundance, Distribution and Ecology of the Tufted Ghost Crab

Home , Ghost crab, Ocypode, Ocypode ceratophthalmus, Ocypode cursor, Ocypodidae

Journal of Sea Research 156 (2020) 101832

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Abundance, distribution and ecology of the tufted ghost crab Ocypode cursor (Linnaeus, 1758) (Crustacea: Ocypodidae) from a recently colonized urban T sandy beach, and new records from Sicily (central Mediterranean Sea) ⁎ Francesco Tiralongoa,b, , Giuseppina Messinaa, Sebastiano Marinob, Sebastiano Bellomob, Antonio Vanadiab, Laura Borzìa, Daniele Tibullob,c, Agata Di Stefanoa, Bianca Maria Lombardoa a Department of Biological, Geological and Environmental Sciences, University of Catania, Catania, Italy b Ente Fauna Marina Mediterranea, Avola (SR), Italy c Department of Biomedical and Biotechnological Sciences, Section of Biochemistry, University of Catania, 95123 Catania, Italy

ARTICLE INFO ABSTRACT

Keywords: The tufted ghost crab, Ocypode cursor, was recorded for the first time on the coast of Sicily mainland in 2009, Protected taxon however no ecological studies were conducted so far. In this study, we provide the first ecological data, based on Beach massive data collection of the ghost crab in Sicily. In particular, we studied the spatio-temporal distribution of Range-expanding species the species in the recently colonized urban beach of Avola. Our results showed that this species' activity is mainly Ionian Sea affected by temperature (crabs were more active during warmer months), while distance from the shoreline Burrows affected size distribution (larger crabs were usually found farther away from the shoreline). Crabs feed on a great variety of food items, and are undergoing northward range expansion.

1. Introduction located at least 1 cm above the water table (Strachan et al., 1999), where they are more protected from storm waves and extreme tides Crabs of the family Ocypodidae are known for their semi-terrestrial (Rodrigues et al., 2016). Furthermore, burrows provide a thermally habits. Within this family, the species belonging to the genus Ocypode stable environment, protecting crabs against temperature extremes Weber, 1795, commonly known as ghost crabs, are found in tropical (Chan et al., 2006). These crabs are opportunistic omnivorous feeders; and subtropical sandy coasts (Barrass, 1963; Sakai and Türkay, 2013). their diet include human food remains, organic detritus stranded on the They are called “ghosts” because their color allows them to camouflage beach, carrions, eggs and hatchlings of Caretta caretta (Trott, 1999). with the color of the sand. In Sicily (central Mediterranean Sea), the species was recorded in Ocypode cursor (Linnaeus, 1758), the only Mediterranean species of Lampedusa (Froglia, 1995), Sampieri (Relini, 2009), Avola (Tiralongo, the family Ocypodidae, is distributed in the west coast of Africa 2016) and Gela (Zafarana and Nardo, 2016). However, since 2016, (Lucrezi et al., 2009b) and in the eastern half of the Mediterranean Sea when it was first recorded from the Ionian coast, the species appears to (Ziese, 1985; Glaubrecht, 1992; Stevcic and Galil, 1993; Kocatas et al., have become quite common on some Sicilian beaches. Recently, the 2004). This crab is a protected species: it is listed as an Endangered or species was recorded at other locations of southern Sicily and in Malta Threatened Species (Annex II) of the Convention for the Protection of (Deidun et al., 2017). the Marine Environment and the Coastal Region of the Mediterranean In this study, we provide the first ecological data on O. cursor from (Barcelona Convention 1995) and among the Strictly Protected Fauna Sicily (central Mediterranean Sea). In particular, we provide the fol- Species (Annex II) of the Convention on the Conservation of European lowing data: (1) distribution and abundance of O. cursor; (2) year-round Wildlife and Natural Habitats (Bern Convention 1996–98). The species data on spatio-temporal distribution pattern of O. cursor in relation to is primarily nocturnal. During daylight hours (or when it feels threa- its size; (3) notes on its behavior and interaction with prey and pre- tened) it shelters in deep burrows on the beach and occupies the coastal dators. Finally, we discuss the newly established population of this crab zone from the low intertidal up to > 30 m inland. Burrows are usually and its spread. L-shaped or J-shaped and reach 80–90 cm in depth. Larger crabs are usually found farther inland from the shoreline and dig deeper burrows

⁎ Corresponding author at: University of Catania, Department of Biological, Geological and Environmental Sciences, Via Androne, n° 81, 95124 Catania, Italy. E-mail address: [email protected] (F. Tiralongo). https://doi.org/10.1016/j.seares.2019.101832 Received 18 September 2019; Received in revised form 10 December 2019; Accepted 16 December 2019 Available online 17 December 2019 1385-1101/ © 2019 Elsevier B.V. All rights reserved. F. Tiralongo, et al. Journal of Sea Research 156 (2020) 101832

Fig. 1. Study area (red rectangle) in the central Mediterranean Sea (Sicily); blue rectangle: study area for data massive collection; red circles: new records of O. cursor in Sicily; green circles: published records of O. cursor in Sicily. (For interpretation of the references to color in this ﬁgure legend, the reader is referred to the web version of this article.)

2. Materials and methods 2.2. Sediment analysis

2.1. Study area and data collection The sample of sand (about 1 kg) was carefully preserved in poly- thene bag and brought to the University of Catania sedimentology lab, The study area was the recently colonized beach of Avola, in where it was placed in an oven at approximately 60 °C and weighed southeastern Sicily (Ionian Sea) (Fig. 1). Data on O. cursor were col- when completely dry. Sediment was then pretreated chemically using lected using non-destructive methods (i.e. burrow counts and mea- hydrogen peroxide to enhance separation or dispersion of aggregates. surements of burrow sizes) from September 2016 to September 2017 Grain size distribution was then carried out by a mechanical sieve with an interval of about 15 days between surveys (two survey per shaker (Giuliani IG/3-EXP). The typical particle-size range for sieving is month), for a total of 26 survey days. At each survey, we counted and 63 μm - 4000 μm. Soil under 63 μm was analyzed by an ELZONE 282 PC measured to the nearest 1 mm with a meter stick each burrow within densimeter. Mean, standard deviation, skewness and kurtosis were each area. Sampling was performed between 7:00 and 09:00 AM and computed (Folk and Ward, 1957). the air temperature during this time was recorded. Burrow counts is a proven approach to estimate ghost crab abundance. Burrow size 2.3. Statistical analysis (opening diameter) is strictly correlated with carapace width, and is therefore a good estimator of crab size (Wolcott, 1978; Warren, 1990; Statistical analysis was performed with the software R (R Valero-Pacheco et al., 2007; Türeli et al., 2009). The selected beach Development Core Team, 2018) and graphics were created using the R extended from side to side for about 600 m and is approximately 30 m package “ggplot2”. The Shapiro-Wilk test was used to determine whe- wide, from the water's edge to upper reaches of the beach. It was lo- ther data were normally distributed in order to use the appropriate cated between 36.88121° N, 15.13763° E and 36.87602° N, 15.13670° tests. A Fligner-Killeen test was used to verify the homogeneity of E. This beach is characterized by the presence of the Asinaro River at variances of burrow sizes between the 3 areas (A, B and C) and the the south end. Transects (black rope) divided the beach into 3 areas, homogeneity of variances of burrow sizes between the seasons. A chi- parallel to water's edge: A (from the intertidal to 5 m inland), B (from 5 squared test was used to determine if the abundance of burrows varied to 15 m inland) and C (from 15 to 30 m inland). between seasons and between areas. The Kruskal-Wallis test was used A sample of sand was collected near the burrows for granulometric to verify whether there was a significant difference in burrow sizes analysis. Additional sampling stations along the entire southern coast of between the 3 areas, to verify whether there were significant seasonal Sicily were explored in order to provide an update on the distribution of changes in burrow sizes, and to verify whether there was a significant the species (Fig. 1, Table 1). Additional, approximately 75 h were spent, seasonal difference in burrows' abundance for each area. A linear re- both during daylight and night hours, on observations of the behavior gression was performed to relate burrows sizes to temperature. of the species: about 3 h per night and per day at Avola for a total of 10 days, and about 5 h per day at Torre Salsa for a total of 3 days. 3. Results

A total of 2673 observations of burrows were recorded in the beach of Avola (Ionian coast of Sicily) (Fig. 1) during the whole study period. Table 1 Abundance of burrows was season dependent (chi-squared test: New records of O. cursor along the Sicilian coasts. Locations are indicated with p < .05), burrows were markedly more abundant (1605 burrows, 60% red circles in Fig. 1. The study area is excluded from the table. of the total recorded) in the summer (Fig. 2, Table 2), with a maximum Location Coordinates Date mean abundance of 4.99 burrows per square decameter (burrows/ dam2) in the area A (Table 3). Abundance of burrows increased with Agnone Bagni 37.42475° N, 15.08972° E 18th September 2018 Siracusa 36.96421° N, 15.20936° E 7th August 2018 proximity to the sea (chi-squared test: p < .05), reaching a maximum Marzamemi 36.74767° N, 15.10996° E 22th June 2017 in the area A, with a total of 1601 burrows recorded (59.9% of the total) Scoglitti 36.89903° N, 14.42503° E 7th November 2016 in the study period (Table 2); while, burrow size increased with the Cannatello 37.24623° N, 13.60927° E 24th August 2017 distance from the sea (Kruskal-Wallis test: p < .05), reaching the Torre Salsa 37.37903° N, 13.30883° E 19th October 2016 maximum average value in the area C (50.51 mm) (Fig. 3A). The Triscina 37.57194° N, 12.73363° E 20th August 2017 Campobello di Mazara 37.57144° N, 12.73194° E 5th July 2017 median of burrows' density during the four seasons was statistically diﬀerent only for the area A (Kruskal-Wallis test: p < .05). In summer,

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Fig. 2. Burrows/dam2 for each area and season at Avola.

Table 2 During field observations, the species was observed feeding on Burrows per area and season recorded during the study period at the beach of beached algae, human food remains and bait abandoned by beach Avola. Areas: A (from the intertidal to 5 m inland), B (from 5 to 15 m inland) fishermen; while birds, stray dogs and foxes (two records at Torre Salsa) and C (from 15 to 30 m inland). were observed preying on the crab. In the beach of Avola, at night, Season AVOLA cannibalism was observed: a large specimen was seen preying on a small individual. We also noticed that during night hours, most crabs A B C Tot. Mean were found very close to the shoreline (at a distance of about 2 m). The granulometric analysis of the beach of Avola showed that the Spring 147 106 83 336 56 Summer 1198 350 57 1605 200.6 sample was well sorted (0.413 s), mean value indicates medium sand Autumn 256 242 204 702 117 (1.462 Mz), skewness shows symmetrical value (0.024 Sk) and kurtosis Winter 0 3 27 30 6 value depicts mesokurtic distribution (0.962 kg). Finally, new records Total 1601 701 371 2673 102.8 of the species showed a westward and northward spread of O. cursor along the Sicilian coast (Fig. 1, Table 1). most of the burrows were concentrated close to the sea (area A), and progressively decrease in number at greater distances (Table 2). A si- 4. Discussion milar situation, but with overall lower abundance, was present in spring; while, in autumn, burrows abundance was similar in all three Seasons, and consequently temperature, are the most important areas, especially between the area A and B, where it was higher than in factors affecting crabs activity. Indeed, the highest number of burrows area C. In winter, when burrows abundance was very low (30 in all) and were observed during the warmer months. In contrast, during the reached its minimum value, burrows were concentrated in the area C, colder months, most of the crabs remain dormant in their burrows, as and no burrows were recorded in the area A. The results of the linear was demonstrated by the low numbers of burrows observed in parti- regression showed that temperature and burrows sizes were correlated cular during winter. Most of the large-sized specimens were con- (p < .05), and the maximum burrows sizes were recorded with lower centrated far from the shoreline, in which some individuals remain temperatures (Figs. 3C, 4, 5). We found a significant difference in the active almost all year and probably reproduce too, and are more pro- variance of burrow size between areas and between seasons (Fligner- tected from storm waves. Indeed, during winter months, the species Killeen test: p < .05) (Figs. 3D, 6, Table 4). The burrows size varied activity was almost exclusively limited to a few large-sized specimens during seasons and reached the maximum mean value in winter inhabiting area C, at the greater distance from the sea. With tempera- (54.80 mm) (Kruskal-Wallis test: p < .05) (Fig. 3B), when most of the tures below about 15 °C, the crabs' activity was reduced or virtually few burrows recorded were concentrated in area C. absent. However, other factors, such as wind, can induce the crab to close the entrance of its burrow, as it was shown for another species of

Table 3 Mean values of burrows per square decameter of beach surface (b/dam2) and burrows' abundance (b) at Avola; SD = Standard deviation. Areas: A (from the intertidal to 5 m inland), B (from 5 to 15 m inland) and C (from 15 to 30 m inland).

Season Burrows' abundance

ABC

b/dam2 SD b SD b/dam2 SD b SD b/dam2 SD b SD

Spring 1.63 1.6 49 48.13 0.59 0.34 35.33 20.5 0.23 0.21 13.83 12.84 Summer 4.99 1.33 149.75 39.91 0.73 0.39 43.75 23.72 0.24 0.19 14.25 11.59 Autumn 1.71 1.47 51.2 44.04 0.67 0.54 40.33 32.24 0.57 0.32 34 19.04 Winter 0 0 0 0 0.02 0.01 1.5 0.71 0.09 0.03 5.4 1.82

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Fig. 3. Burrows' sizes at Avola in relation to areas (A), seasons (B), temperatures (C) and general view of burrows sizes in relation to areas and seasons (D).

Fig. 4. Burrows' sizes in relation to temperature and period at Avola. the genus Ocypode (Alberto and Fontoura, 1999), even though, in our granulometric composition of the beach of Avola appears to be well opinion, the opposite is more likely: burrows entrances can be closed by suited for the species. the sand transported by strong winds. Small and medium-sized speci- The maximum abundance of crab burrows was recorded in the mens are probably more sensitive to low temperature; therefore, almost summer and close to the sea: 4.99 burrows/dam2 in the Area A. In this all of them remain inactive during winter. area, most of the specimens were small and medium-sized. During this Similar results were reported in other studies (Lucrezi et al., 2009b; season, relatively few burrows were recorded in the area C; while, the Dubey et al., 2013; Haque and Choudhury, 2014) that clearly underline great number of burrows recorded in the area A suggests that they find the role of temperature in affecting crabs' activity. Lucrezi et al. (2009b) in this area suitable conditions to prevent desiccation. Conversely, in also underline the importance of strong winds in enhancing crabs' ac- autumn and winter the burrows were concentrated in the area C, and tivity as a consequence of resource availability due to stranded food. during winter crab abundance was very low and reached its minimum However, other factors, such as predation levels, food abundance and value. The great abundance of small and medium-sized burrows in the water content of sand are also relevant in determining crabs' activity area A and B during warm months seem to be related to the high hu- and distribution (Warburg and Shuchman, 1979; Strachan et al., 1999). midity of these areas, that allow to a considerable number of small and The substratum nature can also affect crab abundance and distribution medium-sized crabs to inhabit this zone. Indeed, small specimens of the (Warburg and Shuchman, 1979; Ewa-Oboho, 1993), and the genus Ocypode are less resistant to desiccation and less efficient

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Fig. 5. Linear regression of burrows' sizes against temperature.

Fig. 6. Number of burrows per area (A) and burrows' density in relation to burrows' size per area (B); number of burrows per season (C) and burrows' density in relation to burrows' size per season (D). burrowers than adults (Fisher and Tevesz, 1979; Williams, 1984; Corrêa nesting sites for the loggerhead sea turtle (Caretta caretta)(Casale et al., et al., 2014). Close to the shoreline, they can find the optimal humidity 2012), whose hatchings and eggs are preyed on by O. cursor (Strachan simply digging burrows of few centimeters. Hence the importance of et al., 1999; Marco et al., 2015). Another important factor could be the the area A, in particular during summer, that is directly and continually changes in beach morphodynamics, which altering the availability of affected by the sea water. On the other hand, large-sized crabs dig food can influence size, distribution and abundance of the species deeper and more complex burrows far from the shoreline, reflecting the (Turra et al., 2005; Lucrezi, 2015). increasing depth of the water table (Türeli et al., 2009). However, also In all cases, the low abundance of burrows observed during winter food availability (e. g., food remains of bathers, stranded organic ma- suggests that crabs hibernate in this period. Similar results were ob- terial) can affect crabs' abundance and distribution (Steiner and tained in similar studies for other species of the genus Ocypode (Haley, Leatherman, 1981; Neves and Bemvenuti, 2006). Furthermore, the Si- 1972; Branco et al., 2010; Corrêa et al., 2014). Crabs were abundant in cilian coasts, especially the southern ones, are known to be suitable as almost all the beaches of Avola. After the first record of the species in

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Table 4 Mean values of burrows' size in mm per area and season recorded during the study period at the beach of Avola; SD = Standard deviation. Areas: A (from the intertidal to 5 m inland), B (from 5 to 15 m inland) and C (from 15 to 30 m inland).

Season Burrows' size (mm)

ABC

mean SD min. max mean SD min. max mean SD min. max

Spring 31.99 8.98 11 53 37.01 7.26 13 56 50.82 8.23 35 68 Summer 30.33 9.59 7 57 40.86 8.36 8 61 50.81 10.56 18 71 Autumn 30.99 8.65 9 52 36.19 8.65 9 58 49.67 9.09 9 68 Winter 0 0 0 0 50 4.36 45 53 55.33 7.80 39 67

2016 (Tiralongo, 2016), the crab undergone a rapid population growth, wide, were recorded only 16 burrows. Notwithstanding the minimal indicating as this species is able to rapidly colonize new areas. In Sicily anthropogenic disturbance, the species abundance was low, and this is mainland, O. cursor was recorded for the first time in 2009 at Sampieri probably due, at least in part, to lack of human food remains. Also, the (Relini, 2009), and subsequently undergoing a rapid westward and daily mechanical cleaning of urbanized beaches seems not to cause eastward expansion (Tiralongo, 2016; Zafarana and Nardo, 2016). The great disturbance: mechanical means removal of only a few superficial great abundance of crabs in the crowded beach of Avola could be at centimeters of sand that cover the burrow does not seem to have ap- least in part explained by a greater food availability (e.g. food remains parent effects on crabs. Furthermore, this operation was carried out in of humans, carrions) (Rodrigues et al., 2016), that could be further the early morning, when crabs are usually inside the burrows, several increased by the presence of the River Asinaro. decimeters below the surface. The crabs opened the burrow entrances a The current Atlantic-Mediterranean disjunct distribution of O. cursor few minutes after the beach cleaning or at sunset. However, considering is probably the result of a past wider and continuous Atlantic- the legal status (protected) of the species, the impact of human activ- Mediterranean distribution (Vecchioni et al., 2019). Indeed, the low- ities on O. cursor needs to be explored in more detail. Therefore, data on ering of the sea temperature during the Würm glaciation (Pleistocene) abundance and distribution of the species, such as those provided in (Thiede, 1978) is assumed to be the cause of the fragmentation of the this study, provide base line information useful for policy making and species range, relegating this thermophilous species to the warmer management of the species. For example, in some areas in which the African Atlantic and Levantine Mediterranean coasts as consequence of crabs are particularly abundant, the mechanical cleaning and/or access its local extinction from the temperate Atlantic Ocean and the western may be limited or prohibited. Other protection measures, such as ban of Mediterranean Sea. Currently, as demonstrated by this study, the construction for bathing facilities, or the construction of particular low spread of this species continues northward: along the recently colonized impact structures, should be adopted to achieve protection objectives. Ionian coast and along the west area of Sicily. Furthermore, very recent This study provides the first ecological data of O. cursor in Sicily records from the Salento Peninsula (Italy) and Tunisia emphasize the based on massive data collection, providing useful information for fast spread rate of the species in the Mediterranean Sea (Karaa et al., possible future actions. The species showed a nocturnal activity, from 2019; Mancinelli et al., 2019). sunset to sunrise, when it comes out from its burrow in search of food The ongoing increase in sea temperature can be the main, or one of and prey. During those hours, we observed most of the specimens the main, facilitating factor for the spread of the species (Pastor et al., feeding very close to the shoreline, on wet sand. However, we observed 2017; Sacco et al., 2017). Hence, sea warming could lead to a secondary that in Scoglitti the species can be found out of the burrow also during contact between the Atlantic and Mediterranean subpopulations daylight hours; while it was very rare to observe active crabs during (Bianchi, 2007). However, the habitat discontinuity represented by the daylight hours at Avola. However, several aspects of the biology and long stretches of rocky coast in the northern Sicily could represent a ecology of the species remain unclear (e.g., reproduction, the impact on barrier for the dispersal of the species in other Italian locations, even population of C. caretta, predators and prey, cannibalism frequency) or though marine currents should play an important role to overcome unknown (e.g., larval dispersal, recruitment). Further studies will be these barriers and, consequently, for secondary colonization of other necessary to understand how the species is able to rapidly colonize new beaches, for example through rafting on floating objects (e.g. detached beaches. macroalgae, seagrasses, wood) or through dispersion of the larvae Furthermore, a deeper understanding of the ecology of the species (Peña-Toribio et al., 2017). Furthermore, the use of citizen science is a can help to protect this species from anthropogenic threats, and to suitable method for monitoring the spread of the species in the Medi- better understand how this recent colonizer influence terrestrial and terranean Sea (Tiralongo et al., 2019) and should be implemented at marine food webs and ecosystems. Indeed, the species is an opportu- international level. Indeed, O. cursor is an easily recognizable and de- nistic omnivorous and feeds on a wide variety of food sources (Wolcott, tectable species. 1978; Trott, 1999; Türeli et al., 2009) and is preyed on by several Although anthropogenic impacts are considered to have negative terrestrial and marine species (Lucrezi and Schlacher, 2014; Marco effects on crab abundance, and some authors have used ghost crabs as et al., 2015), including specimens of the same species (cannibalism was ecological indicators (Neves and Bemvenuti, 2006; Lucrezi et al., also recorded by us during filed observations). However, although the 2009b; Lucrezi et al., 2009a; Schlacher et al., 2011; Noriega et al., role usually ascribed to ghost crabs has been that of scavengers (Taylor, 2012; Jonah et al., 2015), the massive presence of O. cursor in several 1971), they are also predators (Wolcott, 1978). Furthermore, their Sicilian urban beaches suggests that the species is rather tolerant to digging behavior enhances oxygenation in the ground soil and facil- human presence, and may even benefit from food supplementation due itates the decomposition of organic materials and nutrient recycling to human presence. This tolerance can be explained by the nocturnal (Dubey et al., 2013). habits of the species. Indeed, during daylight hour, in particular during From our results, the spatial and temporal distribution, as well as the summer months, beaches are typically crowded and crabs remain the size distribution of O. cursor in Sicily appear well defined. The crabs' inside their burrows. Furthermore, on 19th October 2016, at the natural activity decreases from warm to cold seasons, while crab size increases area of the Nature Reserve of Torre Salsa, along a stretch of beach with with distance from the sea. In contrast, during the warmer months, the low human presence that extended for about 300 m and was > 30 m crabs abundance decrease with its distance from the sea. However,

6 F. Tiralongo, et al. Journal of Sea Research 156 (2020) 101832 several factors such as temperature, food availability, predators and ecosystems: a test of ghost crabs (Ocypode spp.) as biological indicators on an urban changes in beach morphodynamics can locally and temporarily alter the beach. Environ. Monit. Assess. 152, 413–424. Mancinelli, G., Belmonte, F., Belmonte, G., 2019. Occurrence of Ocypode cursor (Linnaeus, general pattern of the species abundance and distribution. 1758) (Crustacea, Decapoda) in Salento (southern Italy). Thalassia salentina 41, 47–52. Declaration of Competing Interest Marco, A., da Graça, J., García-Cerdá, R., Abella, E., Freitas, R., 2015. Patterns and in- tensity of ghost crab predation on the nests of an important endangered loggerhead turtle population. J. Exp. Mar. Biol. Ecol. 468, 74–82. We wish to confirm that there are no known conflicts of interest Neves, F.M., Bemvenuti, C.E., 2006. 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