Effects of coral bleaching on the obligate coral-dwelling crab Trapezia cymodoce more

Coral Reefs (2011) 30:719–727 DOI 10.1007/s00338-011-0748-0 REPORT Effects of coral bleaching on the obligate coral-dwelling crab Trapezia cymodoce J. S. Stella • P. L. Munday • G. P. Jones Received: 24 January 2011 / Accepted: 19 March 2011 / Published online: 11 April 2011 Ó Springer-Verlag 2011 Abstract Corals are an essential and threatened habitat for a diverse range of reef-associated animals. Episodes of coral bleaching are predicted to increase in frequency and intensity over coming decades, yet the effects of coral-host bleaching on the associated animal communities remain poorly understood. The present study investigated the effects of host-colony bleaching on the obligate coraldwelling crab, Trapezia cymodoce, during a natural bleaching event in the lagoon of Lizard Island, Australia. Branching corals, which harbour the highest diversity of coral associates, comprised 13% of live coral cover at the study site, with 83% affected by bleaching. Crabs on healthy and bleached colonies of Pocillopora damicornis were monitored over a 5-week period to determine whether coral bleaching affected crab density and movement patterns. All coral colonies initially contained one breeding pair of crabs. There was a significant decline in crab density on bleached corals after 5 weeks, with many corals losing one or both crabs, yet all healthy colonies retained a mating pair. Fecundity of crabs collected from bleached and healthy colonies of P. damicornis was also compared. The size of egg clutches of crabs collected from bleached hosts was 40% smaller than those from healthy hosts, indicating a significant reduction in fecundity. A laboratory experiment on movement patterns found that host-colony bleaching also prompted crabs to emigrate in search of more suitable colonies. Emigrant crabs engaged in aggressive interactions with occupants of healthy hosts, with larger crabs always usurping occupants of a smaller size. Decreased densities and clutch sizes, along with increased competitive interactions, could potentially result in a population decline of these important coral associates with cascading effects on coral health. Keywords Climate change Á Coral-associated invertebrates Á Coral bleaching Á Competition Á Habitat degradation Á Habitat specialisation Introduction The high biodiversity of coral reefs is facilitated by the extraordinary diversity of habitats and topographic complexity provided by scleractinian corals (Luckhurst and ¨ Luckhurst 1978; Jennings et al. 1996; Ohman and Rajasuriya 1998; Lindahl et al. 2001). The close association between small mobile animals and corals has resulted in the evolution of numerous symbiotic associations (Castro 1988; Stella et al. 2011). Although coral reefs experience natural disturbances (e.g. storms) that help maintain local diversity (Abele 1976; Connell 1978; Karlson and Hurd 1993), an escalation of anthropogenic disturbances is having serious negative effects on reef diversity (Hughes et al. 2003; Bellwood et al. 2004) and may disrupt these symbiotic relationships (Caley et al. 2001). Coral bleaching is one such disturbance that is predicted to become more frequent and intense over coming decades due to anthropogenic climate change (Hoegh-Guldberg 1999; Sheppard 2003; Donner et al. 2005). Bleaching events cause Communicated by Ecology Editor Prof. Mark Hay J. S. Stella Á P. L. Munday Á G. P. Jones ARC Centre of Excellence for Coral Reef Studies, and School of Marine and Tropical Biology, James Cook University, Townsville, QLD 4811, Australia J. S. Stella (&) Climate Adaptation Flagship, CSIRO, Hobart, Tasmania 7001, Australia e-mail: Jessica.Stella@my.jcu.edu.au 123 720 Coral Reefs (2011) 30:719–727 significant coral mortality and consequently alter the abundance and community composition of animals that are symbiotic or closely associated with coral (Glynn 1983a; Munday 2004; Bellwood et al. 2006; Pratchett et al. 2008). However, many coral colonies recover from bleaching and may retain their symbiotic animal communities throughout the bleaching event. Even though corals may recover, such non-lethal bleaching may still have negative impacts on the populations of symbiotic species. Many symbioses are formed between tightly branching corals and other reef invertebrates, such as crustaceans and molluscs (Patton 1966, 1994; Abele and Patton 1976; Austin et al. 1980; Coles 1980; Castro 1988; Stella et al. 2010, 2011). Branching corals provide symbiotic animals with a range of resources including a large surface area on which to live, a complex architecture that provides a refuges from predation, food in the form of coral tissue, mucus and its associated detritus, and a hard skeleton used as a substratum by specialised burrowers and gall-forming animals (Castro 1988). In turn, many branching corals are reliant upon certain invertebrates for protection from predators and cleaning (Glynn 1983c; Stewart et al. 2006), thus forming recognisable mutually beneficial partnerships. There is often a differential response among coral species to bleaching, with branching corals consistently being the most susceptible to bleaching and consequent colony mortality (Brown and Suharsono 1990; Gleason 1993; Marshall and Baird 2000; Loya et al. 2001; McClanahan et al. 2004). This differential response can lead to marked shifts in the community composition of coral reefs, with branching corals slowly being replaced by bleachingresistant corals, such as massive and encrusting forms, which offer little structural complexity (Marshall and Baird 2000; Loya et al. 2001; McClanahan et al. 2004, 2007). As live coral is an important resource for a large diversity of reef organisms and branching corals are the most preferred (Pratchett et al. 2009; Stella et al. 2011), any reduction in branching coral cover could have severe implications for reef biodiversity and vital ecological processes. A high degree of dependence on branching corals has been documented for some coral-reef fish, with consequent effects of coral loss on reef fish abundance and diversity (Jones et al. 2004; Garpe et al. 2006; Wilson et al. 2006; Pratchett et al. 2008) with the most coral-reliant species exhibiting the greatest declines (Munday 2004; Wilson et al. 2008). However, measures of abundance do not always provide a clear picture of the full effects of coral loss on coral-dependent species. Coral bleaching and habitat degradation can also affect the individual fitness of coraldependent animals (Kokita and Nakazono 2001; Munday 2001; Pratchett et al. 2004). For example, Kokita and Nakazono (2001) documented a dramatic decrease in survival, growth and reproduction of the obligate corallivorous filefish, Oxymonacanthus longirostris, within a month of coral bleaching. A few months after the bleaching event, the local population had entirely disappeared. The corallivorous butterflyfish Chaetodon lunulatus responded to a mass bleaching event by switching to a more abundant coral prey that was less affected by bleaching. Total abundance was not affected; however, the physiological condition of the fish declined (Pratchett et al. 2004), with possible long-term consequences for reproductive success. Although coralassociated invertebrates may be more dependent on coral than many reef fish, their response to coral loss is almost completely unknown. As a large proportion of coral-associated invertebrates demonstrate a high reliance on live coral hosts in conjunction with a preference for coral hosts that are most susceptible to coral bleaching and mortality (Pratchett et al. 2009; Stella et al. 2011), these animals will likely be predisposed to increased rates of extinction via a decline in fitness and subsequent population declines if reef degradation continues unabated. Coral crabs of the genus Trapezia are perhaps some of the most coral-reliant reef animals, specialised to certain coral hosts upon which they depend for habitat, food in the form of coral mucus, polyps and eggs, and as a breeding site (Knudsen 1967; Patton 1974; Castro 1988; Stimson 1990). The relationship between trapeziids and corals appears to have been established by the Eocene (Schweitzer 2005) and there is evidence to support co-evolution (Glynn 1983b). Trapeziids are ecologically important to their coral hosts. Occurring in excess of 90% on pocilloporid corals (Huber and Coles 1986; Stella et al. 2010), Trapezia crabs have been shown to enhance coral skeletal growth (Glynn 1983c), clean coral hosts of sediments (Stewart et al. 2006) and mucus nets of the vermetid gastropods (Stier et al. 2010) that would otherwise be detrimental to coral growth and survival (Shima et al. 2010), and actively defend their hosts from coral predators such as the starfish, Acanthaster planci (Weber and Woodhead 1970; Glynn 1980; Pratchett 2001). Indeed, the relationship between coral host and Trapezia crabs is such that the crabs are only found in association with a coral host and the corals undergo high rates of colony mortality if the crabs are removed (Glynn 1983c; Stewart et al. 2006). The abundance of pocilloporid colonies, coral colony size and living space within branches are all limiting factors to Trapezia (Castro 1978). Therefore, competition for space may increase as coral cover declines (Glynn 1976). Trapeziids are territorial and naturally occur in strict mating pairs among colonies (Patton 1974; Castro 1978). They are aggressive towards other associates, including conspecifics of the same sex (Castro 1978), and rely solely on their relatively large chelipeds for defence (Glynn 1980; Pratchett et al. 2000). As species of Trapezia are known to move among colonies at night with the possible aim of securing a 123 Coral Reefs (2011) 30:719–727 721 35 34 33 32 31 30 29 28 27 26 25 Jan-10 Feb-10 Mar-10 Apr-10 May-10 larger colony or mate (Castro 1978), conspecific interactions can occur frequently. Interactions between conspecifics of the same sex usually elicit a strong aggressive response and fights can result in the loss of limbs (Vannini 1985). The outcome of these interactions appears to relate to body size, with larger crabs successfully expelling smaller intruding crabs or taking over colonies from smaller crabs (Tsuchiya and Yonaha 1992). Due to the crabs’ aggressive nature and healthy colony numbers acting as a limiting factor, an acute reduction in healthy coral hosts due to coral bleaching could increase competitive interactions among the crab population as suitable resources dwindle. The aim of this study was to examine the immediate effects of coral bleaching on the persistence, reproduction and competitive interactions of the obligate coral-associated crab, Trapezia cymodoce. We document the consequences for crabs of a prolonged bleaching event in the lagoon of Lizard Island (Great Barrier Reef, Australia). Coral bleaching was first documented in order to describe the severity and extent of bleaching and also to distinguish which coral growth forms were most affected. Individual corals were then monitored along with the persistence and social organisation of the crabs in bleached and healthy corals. Fecundity was compared among crabs inhabiting bleached and healthy corals to assess the effects of bleaching on reproductive success. Finally, competition for healthy hosts was experimentally tested, in order to assess how the crabs’ behaviour during a bleaching event might further affect their fitness. Sea surface temperature (ºC) Average Max Date Fig. 1 Average and maximum 2010 summer sea-surface (depth of 2 m) temperatures for Lizard Island (data courtesy of the Australian Institute of Marine Science) determined by conducting 4 replicate 25-m line-intercept transects at each of the sites, and benthic substratum was identified under 50 random points along each transect. Where live corals corresponded with a random point, the growth form and genus were recorded. Corals were also categorised as either healthy (e.g. normal pigmentation) or affected by bleaching (pale or white). Per cent hard coral cover, branching coral cover, and per cent bleaching at each site were calculated from the transect data. The total number of bleached colonies was also compared with the total number of colonies in order to estimate the proportion of bleaching at the whole colony level. Effects of host bleaching on crab density and persistence To assess the effects of host-colony bleaching on the persistence of the obligate coral-associate Trapezia cymodoce, 20 unbleached and 20 bleached colonies of Pocillopora damicornis that hosted a mating pair of crabs were tagged in the lagoon and monitored over a 5-week period. Pocillopora damicornis was chosen because both healthy and bleached colonies were approximately equally abundant, making it ideal for this type of study. Bleaching was categorised using the 4-point scale developed by Marshall and Baird (2000) where (1) healthy = no visible loss of colour, (2) moderately bleached = 1–50% of colony affected or entire colony pale, (3) severely bleached = 51–100% of colony with strong pigmentation loss (colony appears white), (4) dead = 80–100% of colony covered by light algal overgrowth. Tagged colonies were censused once per week by visually inspecting the interbranch spaces for the presence of the crabs. Recovery from bleaching, bleaching progress or mortality of the host colony was monitored by Materials and methods Study site This study was conducted during a natural coral bleaching event in the lagoon of Lizard Island, Australia, from April to May 2010, at a depth range of 2–5 m. A temperature anomaly was recorded from 6 March 2010–10 March 2010 at a depth of 2 m, with maximum daily temperatures ranging from 32 to 32.9°C (Fig. 1). This temperature anomaly coincided with the onset of coral bleaching around mid-March (L. Vail pers. comm.). The maximum temperatures sustained over the 5-day period were *3–4°C higher than the long-term average summer temperature of 29°C for Lizard Island (Lough 1999). Extent of bleaching Coral bleaching was most prominent in shallow depths (1–5 m) and nearly constrained within the lagoon. Therefore, 2 sites were chosen in the lagoon to document coral cover and the extent of bleaching. Coral cover was 123 722 Coral Reefs (2011) 30:719–727 reassigning a score using the 4-point scale and proportional mortality was estimated to the nearest 5%. As bleaching severity did not differ among bleached coral hosts over the census period, host colony health was then categorised as either ‘healthy’ or ‘bleached’ for crab density comparisons. Changes in the number of crabs on healthy and bleached colonies of P. damicornis were examined using the Freeman–Halton extension (Freeman and Halton 1951) to Fisher’s exact test in which the frequency of all possible combinations (0 crabs, 1 crab or 2 crabs) was compared between healthy and bleached colonies at the start and end of the monitoring period. Effects of host bleaching on crab fecundity To determine the effects of host-colony bleaching on the fecundity of T. cymodoce, the number and size of eggs were measured for crabs collected from 30 bleached and 30 unbleached colonies of P. damicornis of approximately equal diameters (*20 cm). Because fecundity is likely to be affected by crab body size, we selected a similar size range of crabs from both healthy (5.5–17 mm carapace width) and bleached (6.9–16 mm) coral hosts to help control for this. Coral colonies were removed from the reef and carefully transported back to the laboratory in bins full of seawater. The crabs were removed from their coral host by gently nudging them to the outer perimeter of the colony with a blunt probe. All crabs were weighed to the nearest 0.001 g and carapace width measured to the nearest 0.1 mm. Body condition was noted if the crabs were missing any claws. Female crabs were anesthetised using a mild solution of clove oil (*1–2 drops of clove oil per 250 mL of seawater). The egg clutches were then gently scraped out of the abdomen using tweezers, added to a petri dish with seawater, photographed under a dissecting microscope and counted using UTHSCSA ImageTool (IT). The diameter of eggs from a subset of each clutch was also measured using ImageTool. The crabs were then returned to their original coral host and the colony cemented back onto the substratum. ANCOVA was used to determine the effect of coral health on clutch size. Crab size was included as a covariate because female size can have a significant effect on fecundity (Gotelli et al. 1985; Tsuchiya and Yonaha 1992). Carapace width was used as the measure of crab size. The assumption of homogeneity of slopes between the covariate (crab size) and main effect (coral health) was confirmed prior to running the ANCOVA. As the relationship between fecundity and body size for decapod crustaceans usually takes the form of a power function (Somers 1991), data were log-transformed for the analyses. Egg diameter was measured for 10 eggs per clutch. The mean diameter of each clutch was calculated and ANOVA was then used to determine if group means differed between crabs from healthy or bleached coral hosts. Effects of host bleaching on crab emigration and competitive interactions To ascertain whether host bleaching prompts T. cymodoce to seek an alternate host and whether crab size is a factor in emigration success, movement of crabs from bleached to unbleached colonies of P. damicornis was observed in a manipulative experiment. In the laboratory, crab pairs were removed from 44 colonies (22 healthy and 22 bleached) of P. damicornis and the carapace of each individual measured to the nearest 0.1 mm with vernier callipers. Crab pairs were then returned to a host colony of either (1) the same quality (i.e. from bleached to bleached or healthy to healthy) or (2) a different quality (i.e. from bleached to healthy). To account for possible colony fidelity, no crabs were returned to, nor offered in the experiment, their original coral host. Coral colonies were then paired based on nearest size and similar interbranch space and having crab occupants with at least a 2-mm difference in carapace size to the occupants of the paired colony. Of the 44 colonies, 14 healthy colonies were paired, 14 bleached colonies were paired and 16 colonies of differing health were paired (8 bleached and 8 healthy). The larger pair of crabs was placed on the bleached colonies in the latter treatment. Each pair of colonies was then placed into an aquarium measuring 40 9 30 9 30 cm, with a continuous flow of sea water (approximately 2 L min-1). Corals were placed approximately 5 cm apart. After 2 days, all crabs were removed from the corals and re-measured in order to detect movement among colonies, as crab size was used to identify the original occupants of the colony. To determine whether degraded host colony health would cause crabs to seek out a new host, the number of crabs that moved to an alternate host of the same quality (either from healthy to healthy or bleached to bleached) was compared with the number that moved to an alternate host of improved quality (from bleached to healthy). The frequencies were compared using a 2-tailed Fisher’s exact test. Results Extent of coral bleaching Mean hard coral cover pooled among sites was 21% ± 2.7% (mean ± SE) of the benthos. Branching coral constituted 64.7% (±5.7%) of total hard coral cover. The mean proportion of hard corals affected by bleaching pooled was 60.4% (±4.8%). Of the hard corals that exhibited bleaching, 86.8% (±4.7%) were branching corals. 123 Coral Reefs (2011) 30:719–727 723 y = 2.1029x + 0.9395 R² = 0.4654 Proportion of coral colonies (%) 100 2 80 60 2 2 2 2 0 1 2 0 1 2 2 0 1 2 0 1 3.75 Healthy Bleached Log (number of eggs) 2 2 3.25 y = 3.6487x - 0.9965 R² = 0.2537 2 40 20 0 H B H B H B H B H B H 2.75 2.25 1.75 B 0.7 0.8 0.9 1 1.1 1.2 1.3 0 1 2 3 4 5 Log (carapace width in mm) Weeks after initial census Fig. 2 Proportion of colonies of Pocillopora damicornis with 2 Trapezia cymodoce crabs, 1 crab or no crabs on healthy (H) and bleached (B) colonies Fig. 3 Relationship between the carapace width (mm) and fecundity (number of eggs) of Trapezia cymodoce females collected from either healthy or bleached colonies of Pocillopora damicornis Effects of host bleaching on crab density and persistence Of the 20 healthy colonies tagged at the start of the census period, 75% remained unaffected by bleaching or mortality. Four colonies were affected by mild bleaching on the branch tips. Two colonies experienced partial mortality of 20 and 10%; however, the remaining tissue was healthy. Of the bleached colonies initially tagged, 70% remained bleached, 10% experienced mortality of more than 50% of the colony and 20% showed some signs of recovery. Crab density remained at a constant of 2 per colony for all tagged colonies during the first 2 weeks after the initial census (Fig. 2). However, 3 weeks after the initial census, crab density began to decline on the bleached colonies (Fig. 2). Fisher’s exact tests revealed that crab densities found on bleached colonies differed significantly from that found on healthy colonies after 5 weeks (P = 0.004). Of the 20 bleached colonies, seven colonies lost one or both crabs. While crab densities remained constant on healthy colonies, there was some fluctuation on the bleached colonies between census weeks, with both emigration and immigration occurring (Fig. 2). Effects of host bleaching on crab fecundity As a similar size range of crabs from both healthy (5.5–17 mm carapace width) and bleached (6.9–16 mm) coral hosts was selected to help control for effects of crab size on fecundity, mean carapace size of females collected from healthy coral hosts (10.5 mm ± 0.43) did not differ significantly from those collected from bleached coral hosts (10.67 mm ± 0.39). There was a positive significant relationship between female carapace size and clutch size living on both healthy (F1,28 = 24.37, r2 = 0.46, P \ 0.001) and bleached corals (F1,28 = 9.52, r2 = 0.25, P = 0.004) (Fig. 3). After adjusting the group means for carapace size, there was a significant effect of coral health on mean clutch size (ANCOVA: F1,57 = 11.02, P = 0.001). The average clutch size of T. cymodoce collected from bleached colonies of P. damicornis was 876 eggs (±128.7), 40% less than clutch size of crabs collected from healthy colonies (1,410 eggs per clutch ± 165). Sampling a subset of each clutch revealed that mean size of eggs from healthy corals was 0.358 mm ± 0.008 and eggs from bleached corals were 0.343 mm ± 0.009; however, this was not significant (ANOVA: F1,56 = 2.167, P = 0.14). Observations made on body condition of both female and male crabs noted that 10 of the 60 crabs (4 females and 6 males) from healthy corals were missing one claw. Of the 60 crabs collected from bleached corals, 9 were missing one claw (5 females and 4 males) and 1 female was missing both. Effects of host bleaching on crab emigration The frequency of movement of crabs from bleached host colonies to healthy host colonies was significantly different from movement among colonies of the same quality (2-tailed Fisher’s exact: P \ 0.001). In the 8 trials where coral health differed, all larger crabs moved from bleached colonies to healthy colonies and usurped the smaller occupants, which moved onto the bleached colonies. In the trials where the two corals were of the same quality, only 3 individuals out of 28 moved to an alternate host (Fig. 4). Discussion Coral-bleaching events are occurring more frequently and can result in a severe decline of live coral cover (Glynn 1983a; Hoegh-Guldberg 1999), and impacts on fishes have been widely reported (Jones et al. 2004; Munday 2004; 123 724 Did not switch host corals Switched host corals Coral Reefs (2011) 30:719–727 100 80 60 40 20 0 Different quality host Same quality host Fig. 4 Proportion of Trapezia cymodoce crabs that moved to an alternate coral host of Pocillopora damicornis of either the same quality (i.e. from healthy to healthy or bleached to bleached) or different quality (from bleached to healthy) Wilson et al. 2006; Pratchett et al. 2008). This study is one of the first to directly assess the effects of a natural bleaching event on an obligate coral-associated invertebrate. The bleaching event that took place was relatively moderate, with a low incidence of coral mortality following the onset of bleaching. However, branching corals comprised the majority of affected corals and most corals remained bleached for an extensive period (at least 5 weeks). The coral crabs, Trapezia cymodoce, that are obligate associates of the branching coral Pocillopora damicornis were, in turn, detrimentally affected by hostcolony bleaching. There was both a reduction in the density and a reduction in the fecundity of crabs associated with bleached colonies and evidence for increased movement of crabs occupying bleached corals. As these crab associates have been shown to be vital to coral health, bleached corals with fewer or less fit trapeziid crabs may be more susceptible to further disturbance and predation. Host-colony bleaching affected the normal pattern of occurrence of T. cymodoce, with bleached colonies losing one or both crabs in a breeding pair within a few weeks. Crab numbers remained constant on the healthy colonies, but the densities fluctuated among colonies of bleached P. damicornis, indicating that crabs were both emigrating and immigrating, perhaps in search of more suitable hosts. As only the few predators morphologically equipped to penetrate the matrix of coral branches are capable of picking crabs out of their coral host (such as the bird wrasse Gomphosus varius with its protractile snout and the moray eel Gymnothorax buroensis with its flexible body) (Hiatt and Strasburg 1960), predation of Trapezia by other fish may occur opportunistically as the crabs move among coral hosts at night (Castro 1978). The reduction of suitable hosts, therefore, could increase the exposure of these animals to predation due to increased movement between coral colonies (Preston 1973). As Trapezia crabs are specialised on live coral and have not been recorded from other habitats, it is extremely unlikely that these crabs would persist without a coral host. The decrease in the density of Trapezia on bleached coral hosts could also have implications for the coral host. These crabs help protect the coral hosts from predators (Weber and Woodhead 1970; Glynn 1980; Pratchett 2001), enhance coral growth (Glynn 1983c) and prevent smothering of the colony by sedimentation (Stewart et al. 2006). Consequently, a decline in abundance of crabs could further debilitate bleached corals, making them more susceptible to further disturbance and reducing their recovery potential. The marked difference in clutch size of crabs associated with healthy or bleached corals indicates that coral health, either directly via a change in nutritional quality or indirectly via a change in energy expenditure on competition over less abundant suitable hosts, has a strong influence on the health of obligate associates. If it is assumed that clutch size is a direct function of reproductive ability, female crabs with a larger clutch size would generate more viable offspring than ones with a smaller clutch size (Childress 1972). There was a 40% reduction in fecundity relative to crabs on healthy corals, which could potentially have an effect on the fitness of these individuals. The significant increase in movement from bleached corals observed in the experiment supports the notion that residing in a healthy coral has a significant fitness advantage. In one of the only other studies to investigate the effects of coral bleaching on the fecundity of coral associates, Glynn et al. (1985) found only 1 in 8 females collected from bleached corals was ˜ ovigerous during an El Nino warming event that caused ´ coral bleaching in Panama. A decline in lipid levels in the coral Pocillopora damicornis spurred a simultaneous decline of lipids in trapeziids, with consequences on crab reproductive output (Glynn et al. 1985). A considerable amount of energy is assumed to be allocated for reproductive output in trapeziids, as females usually produce a new clutch 1–2 days after each clutch hatches (Huber and Coles 1986). Living on a healthy coral host, with an adequate food supply in the form of coral mucus, may allow such a high investment of energy into reproduction. An abundance of suitable hosts may also reduce the frequency of intraspecific agnostic interactions, allowing more energy to be allocated to reproduction rather than competition. The manipulative experiment showed the crabs on bleached corals will attempt to move and occupy a healthy coral if their host coral bleaches. This is supported by the evidence for increased movement by crabs occupying bleached corals in the field. To gain access to a healthy coral, crabs must first defeat and evict the current occupants. The smaller individuals will inevitably be forced to leave the coral in search of another. Although crabs usually 123 Proportion of crabs (%) Coral Reefs (2011) 30:719–727 725 of Marine and Tropical Biology at James Cook University and the ARC Centre of Excellence for Coral Reef Studies. move between colonies at night (Castro 1978), the search for suitable coral hosts will likely enhance susceptibility to predation (Preston 1973). Bleaching events and a decline in suitable habitat could therefore affect crab population structure by increasing the mortality rate of small crabs, because they are less likely to gain access to a healthy coral and more likely to be evicted by larger crabs if they already occupy a healthy coral. The strict pair forming social organisation of Trapezia is thought to be the result of strong intraspecific competition for habitat space (Huber 1987). Intraspecific competitive interactions among crustaceans are for the most part limited to displays and do not usually result in injury or limb autonomy (Hyatt and Salmon 1978). For trapeziids, however, nearly all encounters between conspecifics of the same sex result in long, violent fights with injury and/or cheliped autonomy a common occurrence (Huber 1987). Irrespective of sex or host-colony condition, many crabs in this study were missing one or both claws, indicative of previous agonistic encounters. Elevated agonistic interactions caused by more frequent movements to healthy corals would likely increase the occurrence of cheliped loss among crabs. Limb loss is likely to affect the reproductive success of crabs as it involves a significant energy cost for regrowth (Norman and Jones 1993) and could reduce the ability of crabs to defend their hosts from coral predators. Consequently, increased movement of crabs caused by coral bleaching could influence both the condition and fitness of the crabs and their coral hosts. With bleaching events predicted to be more frequent and severe in the future due to continued global warming, the fate of bleaching susceptible branching corals is of considerable concern. The loss of even just a few branching coral species could dramatically impact reef biodiversity, potentially causing the extirpation of other species that are reliant on live coral, such as coral-associated crabs and gobies. As coral health declines, the fecundity of coral associates will decline which could ultimately affect recruitment and population persistence. Reduced health of symbiotic associates could potentially impair their ability to perform important functional roles, such as cleaning and protecting corals from predators. Further research is required to determine how persistent and severe bleaching events will affect the population dynamics of coral associates and ultimately, what feedbacks would occur to coral populations as a result of a reduction in the abundance or physical condition of their associated faunal communities. Acknowledgments We thank B. Gordon, F. DeFaria, T. Z. Ang, C. Holland and the personnel of Lizard Island Research Station for their assistance in the field and Ray Berkelmans and the Australian Institute of Marine Science for sea surface temperature data. 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