Coexistence of Juvenile with Adult Ocypode gaudichaudii at Culebra Beach, Panama: A Temporal-spatial Partitioning Compromise

© 2022 Academia Sinica, Taiwan Open Access Coexistence of Juvenile with Adult Ocypode gaudichaudii at Culebra Beach, Panama: A Temporal-spatial Partitioning Compromise Adeline Y.P. Yong1 and Shirley S.L. Lim1,* 1Ecology Lab, Natural Sciences and Science Education, NIE, Nanyang Technological University, 1 Nanyang Walk, Singapore 637616, Republic of Singapore. *Correspondence: E-mail: shirley[email protected]; shirley[email protected] (Lim). E-mail: [email protected] (Yong) Received 29 May 2021 / Accepted 28 January 2022 / Published 5 May 2022 Communicated by Benny K.K. Chan The temporal-spatial resource use patterns of juvenile and adult Ocypode gaudichaudii were studied by comparing the zonation patterns and activity budgets of the two life stages at Culebra Beach, Panama. Burrow distribution of the crabs during the day and at night was studied over six months. Diurnal activity budgets of 46 crabs (22 juveniles and 24 adults) were determined by observing seven predominant behaviors upon emergence from their respective burrows when the burrow zone is uncovered after the tide recedes. The behaviors comprise three foraging-related activities (i.e., deposit-feeding, scavenging, and probing for food), the maintenance of burrow, walking, staying within the burrow, and resting at the burrow entrance. Juvenile crabs occupied a higher intertidal zone than the adults and had a higher emergence rate at night. This temporal-spatial habitat partitioning could possibly reduce intraspecific competition between the two life stages, thereby enabling their coexistence in the habitat as well as increasing the survival rate of the juveniles, potentially raising the carrying capacity of the population at Culebra Beach. All 46 crabs—regardless of life stage—spent the highest mean proportion of time on foraging-related activities. Out of the three feeding-related behaviors, adults spent most time on deposit-feeding while juveniles spent most time probing. Only juveniles scavenged. In both life stages, a similar proportion of time was spent maintaining the burrow and staying within the burrow. Key words: Diel activity pattern, Habitat selection, Intraspecific competition, Niche partitioning, Resource use. Citation: Yong AYP, Lim SSL. 2022. Coexistence of juvenile with adult Ocypode gaudichaudii at Culebra Beach, Panama: a temporal-spatial partitioning compromise. Zool Stud 61:8. doi:10.6620/ZS.2022.61-08. BACKGROUND In the field of community ecology, it is well established that no two interacting species can occupy similar niches, compete for the same resources, and coexist in the long term—this is known as the Competitive Exclusion Principle (see Gause 1934). However, MacArthur and Levins (1967) stated that stable coexistence is possible, up to a certain threshold of niche similarity; this was termed the ‘limiting similarity theory’. To achieve coexistence, competing species must segregate in one or more dimensions of their ecological niche, a process known as niche partitioning (see Schoener 1974a). In his classic work on seven sympatric congeneric species of lizards in the Western Australian desert, Pianka (1969) provided evidence that resource division can be classified into three dimensions: food type, habitat, and time. Niche differentiation, thus, can be achieved through trophic, spatial, or temporal partitioning, or a combination of them, to avoid intense competition. Species may be distinctive in their resource selection (trophic differences) or in the places (spatial differences) or time (temporal differences) when shared resources are exploited. Zoological Studies 61: 8 (2022) doi:10.6620/ZS.2022.61-08 1 © 2022 Academia Sinica, Taiwan Food resource partitioning has been extensively studied, especially in vertebrate communities (e.g., fish, birds, mammals). Most of the research has involved comparative studies of diets, e.g., prey/food type and size, through stomach content analyses (see Pianka 1969; Su and Lim 2016); food preference/selection observations (see Sushma and Singh 2006); or scat analyses (see Chillo et al. 2010). Diet data are often linked with the morphometrics of the individuals, or the species, with conclusions on food partitioning being drawn based on constraints/advantages of various morphological structures such as gape size (see Su and Lim 2016) and head proportions (see Pianka 1969). Spatial resource partitioning occurs when two or more competing species reduce competition by occupying different areas/microhabitats within the range of occurrence of a common resource. Time is a resource axis that can be partitioned both on diel and seasonal scales. In a review on resource partitioning, Schoener (1974a) observed that temporal partitioning was markedly less common than food-type or habitat partitioning. Schoener (1974b) subsequently developed a theoretical model that predicts that temporal partitioning at the diel scale should be relatively rare as only in situations whereby there is a severe depletion of resources would it be no longer optimal to forage during the same period as competitors. Notably, there are many more papers published on seasonal temporal partitioning than diel partitioning (Schoener 1974a). However rare, temporal differences in activity patterns of competitors occur in nature, and these are discussed in a more recent review by Kronfeld-Schor and Dayan (2003). Although niche differentiation of coexisting species is important in studies on community dynamics, there are increasing empirical studies on intraspecific resource use (see Bolnick et al. 2011). Some researchers referred to the different age-classes of a few animal taxa (e.g., crocodiles, desert scorpions, spiders) as ‘ecological species’ because the variation in resource use among the age classes were equivalent or more than that between different species (Enders 1976; Maiorana 1978; Polis 1984). For example, the different intraspecific resource use patterns in desert scorpions (Polis 1984), snakes (Shine and Wall 2007) and fishes (Marrin 1983) suggest intraspecific niche partitioning and explain the coexistence of conspecifics at different life stages (see Quevedo et al. 2009). Different resource use patterns are also evident in brachyuran crabs. Habitat shifts (e.g., Hultgren and Stachowicz 2010) and diet shifts (e.g., Rosas et al. 1994) with the maturation of juvenile brachyuran crabs into adults have been reported, but the existing literature centres on the niche shifts in temperate sub-tidal brachyurans (e.g., Callinectes sp., blue crab). To date there are only three studies on the diet shifts in semi-terrestrial brachyurans from the genera Helice (see Mia et al. 2001) and Ocypode (see Crane 1941; Lim et al. 2016), commonly known as ghost crabs. Moreover, only these two studies on ghost crabs (Ocypode) have been conducted in tropical regions. Ghost crabs (genus Ocypode) can be good model organisms with which to study resource partitioning as their burrows are distinct (see Yong and Lim 2009) on sandy beaches (indicating habitat-use). As large beach macrofauna, their dietary preferences can be easily ascertained through behavioral observations and stomach analyses (indicating food resource use) (Crane 1941; Hughes 1966; Jones 1972), and they have been known to be diurnally and nocturnally active (indicating diel partitioning) (Barrass 1963). In addition, adult O. ceratophthalmus cannibalize juveniles, and the relationship between these two life stages is that of a predator-prey system (Hughes 1966). Hence, ghost crabs are excellent models for intraspecific niche partitioning investigations. Ocypode gaudichaudii is the only ghost crab species that predominantly deposit-feeds and undergoes an ontogenetic change in claw morphology—the pointed claw tips of juvenile crabs become chisel-shaped or ‘truncated’ in the adults (see Crane 1941). Analyses of foregut contents and claw morphometrics of juvenile and adult O. gaudichaudii suggested that the juvenile crabs switched from a diet of small invertebrates (i.e., insects, worms, isopods) to diatoms with the onset of claw truncation as adults (see Crane 1941; Lim et al. 2016). However, field observations of the adult and juvenile O. gaudichaudii at Culebra Beach—a resourcerich sandy beach in Panama—by Yong and Lim (2021) indicated no diet differentiation between the life stages, suggesting that the crabs rely on the partitioning of other resources to reduce the competition between the two life stages. How do adult and juvenile O. gaudichaudii differ in their utilization of resources to decrease intraspecific competition? We hypothesized that O. gaudichaudii show spatial and temporal variation in the resource use patterns to reduce intraspecific competition. In this study, we ascertained the diel zonation patterns and the diurnal activity budgets of juvenile and adult O. gaudichaudii to determine if there is intraspecific niche partitioning that could decrease competition between the two life stages. MATERIALS AND METHODS The study was conducted from July 2012 to October 2013 at Culebra Beach (8°54'45"N, page 2 of 13Zoological Studies 61: 8 (2022) © 2022 Academia Sinica, Taiwan 79°31'48"W) along the Pacific Coast of Panama. Culebra Beach (CB) is a sheltered sandy beach on the eastern side of the Pacific entrance to the Panama Canal. The burrow zone was demarcated into six 5 m wide zones across the shore and parallel to the shoreline (Fig. 1). The tidal heights of the demarcated zones at CB ranged from -0.6 m to 4.6 m, and various abiotic and biotic factors across the six zones of the two beaches were determined. According to Yong and Lim (2021), the concentration of total organic content, chlorophyll a and prey types (i.e., isopods and rove beetles) across the burrow zones were similar. Sediment grain size distribution in the burrow and foraging zones of Ocypode gaudichaudii Granulometry of the substrate collected from the burrow and foraging zones at CB was conducted to test for sediment particle size differences across the zones. This was carried out using the methods outlined in Buchanan (1984). Data obtained from dry and wet sieving were analyzed using GRADISTAT 8 (see Blott and Pye 2001). Abundance and distribution of juvenile and adult Ocypode gaudichaudii The abundance and distribution of juvenile and adult O. gaudichaudii were determined from June to November 2012. Regression of the variable ‘Carapace width’ (CW) against ‘Burrow diameter’ (BD) of 86 crabs was determined following the method outlined in Lim and Yong (2015). This crab population exhibited high burrow fidelity and the smaller crabs did not colonize abandoned burrows constructed by larger conspecifics (personal observation by AYPY). The CW-BD relationship was established so that the CW, and hence the life stage of the crab occupant could be ascertained with just the BD measurement, with minimal disturbance to the crab occupant during the sampling sessions. A total of 215 juvenile crabs were collected by examining their pleopods as described by Lim et al. (2016). The cut-off BD for juvenile crabs was based on the CW (14.3 mm) of the largest juvenile crabs collected. Extrapolation of the cut-off BD for juvenile crabs was carried out using the regression equation CW = 1.01BD + 0.78 (r2 = 0.94) and the cut-off CW of 14.3 mm. The extrapolated BD of 13 mm indicated that adult O. gaudichaudii excavated burrows with BD > 13 mm. A 30 × 30 m plot across the six burrow zones was marked out as the sampling area, and the area was divided into 36 (5 × 5 m) quadrats (Fig. 2) with six replicates at each zone. Day and night sampling sessions were conducted at low tide when the intertidal zone was exposed by the ebbing tide. During each sampling session, the burrows with crab occupants in each quadrat were identified. For each burrow, the zone in which it was located was recorded and the diameter was measured before the CW of the crab occupant was extrapolated. The burrow was then categorized as one that was excavated by a juvenile or an adult crab according to the cut-off BD of 13 mm. A boxplot was used to compare the size range of the crabs that emerged during the day and night. All the juvenile and adult crabs in each quadrat were counted, and the percentage composition of each life-history stage was determined for each sampling session. A Chi-square test was performed to test if the mean proportions of juvenile and adult crabs that emerged during the day and night were different. The burrow density within the sampling session was calculated, and a t-test was used to compare the mean burrow densities at Culebra Beach during the day and night. Due to heteroscedasticity and a non-normal distribution, two separate non-parametric KruskalWallis tests were performed to compare the median of the zonal burrow densities at different times of the day. A Kruskal-Wallis test was used to compare the median burrow densities between the zones. Scatterplots of the burrow densities of the juvenile and adult crabs in each sampling session were plotted against the highest high tide level and lowest low tide level for the day at Fig. 1. Beach profile showing the burrow zones of Ocypode gaudichaudii at Culebra Beach. page 3 of 13Zoological Studies 61: 8 (2022) © 2022 Academia Sinica, Taiwan each site. These two tide levels determine the upper and lower limits of the intertidal zone for each day and could influence the burrow densities at the site. The zonal burrow densities of the juvenile and adult crabs during each sampling day were also related to the highest high tide and lowest low tide levels during the study. Behavioral observations of Ocypode gaudichaudii Ad libitum sampling and ethogram construction Field observations for an ethogram were conducted from June to August 2013. During the day, crabs were observed from 5 m away with a pair of binoculars (Steiner Safari 10 × 26) and a handheld video camera (Sony Handycam DCR-SR62) to minimize the influence of human disturbance on the behavior of the animals. Night observations of the crabs were made in total darkness using a pair of night vision goggles (ATN NVG-7 CGT) within 2 m from the crabs. Preliminary observations showed that the crabs were only active at the intertidal zone for about 6 h after emergence during the day. Ad libitum sampling was carried out to identify the common behaviors of O. gaudichaudii after emergence during the day. An ethogram based on the types of behavior observed in the field was constructed. Activity budget of Ocypode gaudichaudii The diurnal activity budgets of 46 crabs (22 juveniles, 24 adults) were determined from August to December 2013. During the day, most crabs emerged from their burrows approximately half an hour after the receding tide uncovered the burrow zone. Freshlyemerged juvenile and adult crabs were randomly selected from each zone for observation. The crabs usually rested at the burrow entrance for approximately an hour upon emergence. Recording of a crab’s behavior started once it moved away from the burrow entrance. The activity in which the observed crab was engaged was recorded at five-minute intervals. Every crab was observed for a minimum of an hour and for as long as possible until it was out of sight for more than 15 min. The mean total activity time between the juveniles and adults from each site were compared with t-tests. The Fig. 2. Location of Culebra Beach with the inset showing a 30 × 30 m plot marked out as the sampling area across six five-metre zones (zone 1 to zone 6). The area was divided into 36 (5 × 5 m) quadrats. N page 4 of 13Zoological Studies 61: 8 (2022) © 2022 Academia Sinica, Taiwan mean proportion of time in which the juvenile and adult crabs were engaged in each activity was calculated and compared separately. No field observations were carried out on rainy days as the crabs did not emerge. We used statistical methods similar to those used by Baladrón et al. (2016) to compare the activity budgets of the two life stages by first constructing a BrayCurtis similarity/dissimilarity matrix, then performing a similarity percentage (SIMPER) procedure to examine the contribution of each behavior to the similarity within each life stage and average dissimilarity between the life stages. Non-metric multidimensional scaling based on the Bray-Curtis similarity matrix was then applied to visualize the ordination distribution between the juvenile and adult crabs. The crabs with similar activity budgets will cluster closer in the ordination plot and vice versa for the crabs with different activity budgets. In addition, a cluster analysis based on the same similarity matrix was performed to determine the occurrence of behavioral heterogeneity of the crabs at the life stages. The ordination plot was superimposed with the results of the cluster analysis at 80% similarity indicated the heterogeneity in crab behavior. A Oneway Analysis of Similarities (ANOSIM) was performed to verify the behavioral heterogeneity between the juvenile and adult crabs. All multivariate statistical analyses were carried out using the PRIMER software (PRIMER-E Ltd., Version 6.1.2, 2005; see Clarke and Gorley 2001). RESULTS Sediment grain size distribution The sediment had approximately 98.7% sand and 1.3% of silt and clay. Results from the analysis showed that the sediment across the zones had uniform particle grain size (well-sorted). The mean sediment grain size was 98.7 ± 0.3 μm. Abundance and distribution of Ocypode gaudichaudii All extrapolated CW > 37.0 mm and < 4.0 mm were discarded as the CW of the crabs observed throughout the study ranged from 4.0 mm to 36.9 mm. The size range of the crabs that emerged during the day and night was similar to the CW: 5.1 to 35.6 mm (Fig. 3). However, the mean CW of the crabs that emerged during the day was significantly larger than those that emerged at night (t = 12.92, d.f. = 769, p < 0.05; 18.8 ± 0.1 mm > 14.5 ± 0.3 mm; mean ± S.E., respectively). The mean proportion of juvenile and adult O. gaudichaudii that emerged during the day and night were significantly different (χ2 = 16.592, d.f. = 1, p < 0.05). During the day, 32% of the crabs that emerged were juveniles, but the mean proportion increased to 58% at night. There was no significant difference in the mean burrow densities between day and night (t = 1.23, d.f. = 185, p = 0.221; 0.18 ± 0.01 burrows m-2 ≈ 0.14 ± 0.03 burrows m-2; mean ± S.E., respectively). Results of the Kruskal-Wallis tests showed a significant difference in the median burrow densities between the zones during the day (H = 241.70, d.f. = 5, p < 0.05) and night (H = 83.13, d.f. = 5, p < 0.05). The burrow densities of the adult crabs were consistently higher than the juveniles during the day except on six out of the 21 days of sampling. There was no clear trend in the fluctuation of burrow densities throughout the tidal cycles. Scatterplots of the burrow densities at each burrow zone (Fig. 4) showed the highest burrow densities of the adults mainly (16 out of the 21 sampling days) occurred between zones 3 and 4. In comparison, the highest burrow densities of the juveniles generally (15 out of the 21 sampling days) occurred between zones 1 and 2. However, on 27 September, and 9 November, 2012, the burrow densities of the juveniles at zone 3 were the highest. There is no clear trend in the results with respect to the tidal cycle. The scatterplot of zone 6 of the burrow zone was excluded due to negligible burrow densities throughout the study. Generally, the burrow densities of the adults and juveniles were the highest in zone 2 at night (Fig. 5). The only exception was on 27 September, 2012 when the burrow densities of the Fig. 3. Boxplots of the median carapace width and interquartile range of Ocypode gaudichaudii during the day and night at Culebra Beach. Dark bands represent medians, boxes represent interquartile range and whiskers represent 1.5 times the interquartile range. page 5 of 13 Zoological Studies 61: 8 (2022) © 2022 Academia Sinica, Taiwan Fig. 4. Burrow densities of the juvenile and adult Ocypode gaudichaudii at zones 1 to 5 of Culebra Beach during the day with respect to the high and low tide levels from 9 June to 29 November, 2012. page 6 of 13Zoological Studies 61: 8 (2022) © 2022 Academia Sinica, Taiwan adults and juveniles in zone 3 were the highest, which is similar to the trend observed during the day. Behavioral observations of Ocypode gaudichaudii Ad libitum sampling and ethogram construction Seven distinct behaviors in juvenile and adult O. gaudichaudii were observed over the month-long period of ad libitum sampling (Table 1). Ocypode gaudichaudii spent a large proportion of time foraging when the intertidal zone was exposed at low tide. Three out of the seven common behaviors—deposit-feeding, probing, and scavenging/predation—observed in the crabs were related to foraging (Table 1). Activity budget of Ocypode gaudichaudii Juvenile crabs usually emerged before the adults when the tide receded. As a result, all the juvenile crabs that were observed were engaged in the observed activities before the adult crabs. The juveniles spent a significantly lower mean total activity time than the Fig. 5. Burrow densities of the juvenile and adult Ocypode gaudichaudii in zones 1 to 3 of Culebra Beach during the night with respect to the high and low tide levels from 9 June to 29 November, 2012. page 7 of 13Zoological Studies 61: 8 (2022) © 2022 Academia Sinica, Taiwan adults engaged in the seven behaviors after burrow emergence (t = 4.75, d.f. = 39, p < 0.05; 146 ± 12 min < 216 ± 9 min; mean ± S.E., respectively). All 46 crabs spent the highest mean proportion of time on foraging-related activities upon emergence. Out of the three feeding-related behaviors (i.e., depositfeeding, scavenging/predation, and probing), the adult crabs spent the most time deposit-feeding (Fig. 6). Scavenging/predation was not observed in the adults during the day, and the juveniles spent more time on probing than the adults. Both stages of crabs spent a similar amount of time on burrow maintenance (Fig. 6). Adult crabs spent similar amount of time in the burrows as the juveniles, but the juveniles spent more time resting at the burrow entrance than the adults (Fig. 6). Results of SIMPER indicated that there was limited overlap in the activity budget of the juvenile and adult crabs (Table 2). Among the six behaviors, depositfeeding contributed the most and walking contributed the least to the difference in activity budgets of the two life stages. The nMDS plot superimposed with the Bray-Curtis cluster analysis using 60% similarity showed five clusters for the activity budgets of all 46 crabs: three clusters comprising solely juvenile crabs on the left, a cluster of only adult crabs on the right, and one cluster of mixed juveniles (9 individuals) and adults (13 individuals) in the middle of the plot (Fig. 7). When 80% similarity was used to differentiate the activity budgets of this middle cluster, only one of the nine groups had mixed life stages. Results of the oneway ANOSIM showed a significant difference between the activity budgets of the juveniles and adults (Global R = 0.45, p < 0.05). The evidence indicated behavioral heterogeneity between the juvenile and adults. DISCUSSION Schober and Christy (1993) studied the abundance and distribution of O. gaudichaudii at Culebra Beach. Table 1. Ethogram for Ocypode gaudichaudii based on field observations Behavior Definition Deposit-feeding Scooping up portions of surficial sediment into the buccal cavity with chela and producing pseudofecal pellets Probing Inserting chela into the substrate repeatedly Scavenging/predation Picking up living or dead plant or animal matter from the substrate and placing food into the buccal cavity Burrow maintenance Excavation and cleaning of burrows and moving of sand away from the burrows Walking Lateral movements across the substrate surface Resting Standing motionless In burrow Staying in the burrow Fig. 6. Mean proportion of time (± S.E.) that Ocypode gaudichaudii from Culebra Beach were engaged in seven behaviors after burrow emergence. ScF, scavenging; DepF, deposit-feeding; Probe, probing for food; BurM, burrow maintenance; Walk, walking; In bur, staying within the burrow; Rest, resting at the burrow entrance. page 8 of 13Zoological Studies 61: 8 (2022) © 2022 Academia Sinica, Taiwan The highest mean burrow density that they observed was higher than the mean diurnal burrow density in the current study (0.78 burrows m-2 > 0.18 ± 0.01 burrows m-2). In addition, Schober and Christy (1993) reported that the burrow densities varied with the tidal regime and lunar cycle; the height of the high tide immediately before the sampling period was significantly positively correlated with the burrow density within one to five days later. In comparison, the tidal cycles, did not affect the burrow densities of the crabs in the current study. Although the size range of O. gaudichaudii reported by Schober and Christy (1993) is different from that of the current study (the largest mean CW: 37.3 ± 0.78 mm cf. 35.6 mm, respectively), the zonation patterns of O. gaudichaudii of both studies are comparable with the highest burrow densities at zone 1 to zone 3 (Fig. 4). Burrow densities and zonation patterns of the juvenile and adult crabs varied throughout the study, but the burrow densities of adult crabs were generally higher. Although the adult crabs had a wider distribution Table 2. Contribution of each behavior to the dissimilarities between the activity budgets of adult and juvenile Ocypode gaudichaudii, according to SIMPER analysis. Behaviors were arranged in decreasing order according to their contribution to the average dissimilarity Behavior % Similarity (Average ± SD) % Dissimilarity adult vs juvenile Adult Juvenile Contribution Cumulative Deposit-feeding 27.72 ± 1.45 2.93 ± 0.49 32.06 32.06 In burrow 16.72 ± 1.17 22.48 ± 2.05 18.94 51.00 Probing 0 11.40 ± 1.18 16.75 67.75 Resting 10.50 ± 2.04 13.64 ± 1.33 12.66 80.40 Burrow maintenance 6.01 ± 1.71 3.96 ± 0.72 8.53 88.94 Walking 0 0 8.52 97.46 Average similarity 62.58 57.54 Average dissimilarity 54.42 Fig. 7. Non-metric Multidimensional Scaling plot of the activity budget of the juvenile and adult Ocypode gaudichaudii from Culebra Beach superimposed with Bray-Curtis cluster analysis using 60% and 80% similarity. 2D stress = 0.15. page 9 of 13Zoological Studies 61: 8 (2022)