Lethal effects of habitat degradation on fishes through changing competitive advantage

Coral bleaching has caused catastrophic changes to coral reef ecosystems around the world with profound ecological, social and economic repercussions. While its occurrence is predicted to increase in the future, we have little understanding of mechanisms that underlie changes in the fish community associated with coral degradation. The present study uses a field-based experiment to examine how the intensity of interference competition between juveniles of two species of damselfish changes as healthy corals degrade through thermal bleaching. The mortality of a damselfish that is a live coral specialist (Pomacentrus moluccensis) increased on bleached and dead coral in the presence of the habitat generalist (Pomacentrus amboinensis). Increased mortality of the specialist was indirectly owing to enhanced aggression by the generalist forcing the specialist higher up and further away from shelter on bleached and dead coral. Evidence from this study stresses the importance of changing interspecific interactions to community dynamics as habitats change.     

Rising CO2 concentrations affect settlement behaviour of larval damselfishes

Reef fish larvae actively select preferred benthic habitat, relying on olfactory, visual and acoustic cues to discriminate between microhabitats at settlement. Recent studies show exposure to elevated carbon dioxide (CO₂) impairs olfactory cue recognition in larval reef fishes. However, whether this alters the behaviour of settling fish or disrupts habitat selection is unknown. Here, the effect of elevated CO₂ on larval behaviour and habitat selection at settlement was tested in three species of damselfishes (family Pomacentridae) that differ in their pattern of habitat use: Pomacentrus amboinensis (a habitat generalist), Pomacentrus chrysurus (a rubble specialist) and Pomacentrus moluccensis (a live coral specialist). Settlement-stage larvae were exposed to current-day CO₂ levels or CO₂ concentrations that could occur by 2100 (700 and 850 ppm) based on IPCC emission scenarios. First, pair-wise choice tests were performed using a two-channel flume chamber to test olfactory discrimination between hard coral, soft coral and coral rubble habitats. The habitat selected by settling fish was then compared among treatments using a multi-choice settlement experiment conducted overnight. Finally, settlement timing between treatments was compared across two lunar cycles for one of the species, P. chrysurus. Exposure to elevated CO₂ disrupted the ability of larvae to discriminate between habitat odours in olfactory trials. However, this had no effect on the habitats selected at settlement when all sensory cues were available. The timing of settlement was dramatically altered by CO₂ exposure, with control fish exhibiting peak settlement around the new moon, whereas fish exposed to 850 ppm CO₂ displaying highest settlement rates around the full moon. These results suggest larvae can rely on other sensory information, such as visual cues, to compensate for impaired olfactory ability when selecting settlement habitat at small spatial scales. However, rising CO₂ could cause larvae to settle at unfavourable times, with potential consequences for larval survival and population replenishment.     

Degraded Environments Alter Prey Risk Assessment

Elevated water temperatures, a decrease in ocean pH, and an increasing prevalence of severe storms have lead to bleaching and death of the hard corals that underpin coral reef ecosystems. As coral cover declines, fish diversity and abundance declines. How degradation of coral reefs affects behavior of reef inhabitants is unknown. Here, we demonstrate that risk assessment behaviors of prey are severely affected by coral degradation. Juvenile damselfish were exposed to visual and olfactory indicators of predation risk in healthy live, thermally bleached, and dead coral in a series of laboratory and field experiments. While fish still responded to visual cues in all habitats, they did not respond to olfactory indicators of risk in dead coral habitats, likely as a result of alteration or degradation of chemical cues. These cues are critical for learning and avoiding predators, and a failure to respond can have dramatic repercussions for survival and recruitment.     

Suspended sediment impairs habitat choice and chemosensory discrimination in two coral reef fishes

Increasing sediment onto coral reefs has been identified as a major source of habitat degradation, and yet little is known about how it affects reef fishes. In this study, we tested the hypothesis that sediment-enriched water impairs the ability of larval damselfish to find suitable settlement sites. At three different experimental concentrations of suspended sediment (45, 90, and 180 mg l⁻¹), pre-settlement individuals of two species (Pomacentrus amboinensis and P. moluccensis) were not able to select their preferred habitat. In a clear water environment (no suspended sediment), both species exhibit a strong preference for live coral over partially dead and dead coral, choosing live coral 70 and 80% of the time, respectively. However, when exposed to suspended sediment, no habitat choice was observed, with individuals of both species settling on live coral, partially dead, and dead coral, at the same frequency. To determine a potential mechanism underlying these results, we tested chemosensory discrimination in sediment-enriched water. We demonstrated that sediment disrupts the ability of this species to respond to chemical cues from different substrata. That is, individuals of P. moluccensis prefer live coral to dead coral in clear water, but in sediment-enriched water, chemical cues from live and dead coral were not distinguished. These results suggest that increasing suspended sediment in coral reef environments may reduce settlement success or survival of coral reef fishes. A sediment-induced disruption of habitat choice may compound the effects of habitat loss on coral reefs.     

Behaviourally Mediated Phenotypic Selection in a Disturbed Coral Reef Environment

Natural and anthropogenic disturbances are leading to changes in the nature of many habitats globally, and the magnitude and frequency of these perturbations are predicted to increase under climate change. Globally coral reefs are one of the most vulnerable ecosystems to climate change. Fishes often show relatively rapid declines in abundance when corals become stressed and die, but the processes responsible are largely unknown. This study explored the mechanism by which coral bleaching may influence the levels and selective nature of mortality on a juvenile damselfish, Pomacentrus amboinensis, which associates with hard coral. Recently settled fish had a low propensity to migrate small distances (40 cm) between habitat patches, even when densities were elevated to their natural maximum. Intraspecific interactions and space use differ among three habitats: live hard coral, bleached coral and dead algal-covered coral. Large fish pushed smaller fish further from the shelter of bleached and dead coral thereby exposing smaller fish to higher mortality than experienced on healthy coral. Small recruits suffered higher mortality than large recruits on bleached and dead coral. Mortality was not size selective on live coral. Survival was 3 times as high on live coral as on either bleached or dead coral. Subtle behavioural interactions between fish and their habitats influence the fundamental link between life history stages, the distribution of phenotypic traits in the local population and potentially the evolution of life history strategies.     

Temperature influences habitat preference of coral reef fishes: Will generalists become more specialised in a warming ocean?

Climate change is expected to pose a significant risk to species that exhibit strong behavioural preferences for specific habitat types, with generalist species assumed to be less vulnerable. In this study, we conducted habitat choice experiments to determine how water temperature influences habitat preference for three common species of coral reef damselfish (Pomacentridae) that differ in their levels of habitat specialisation. The lemon damselfish Pomacentrus moluccensis, a habitat specialist, consistently selected complex coral habitat across all temperature treatments (selected based on local average seasonal temperatures naturally experienced in situ: ambient winter 22°C; ambient summer 28°C; and elevated 31°C). Unexpectedly, the neon damselfish Pomacentrus coelestis and scissortail sergeant Abudefduf sexfasciatus, both of which have more generalist habitat associations, developed strong habitat preferences (for complex coral and boulder habitat, respectively) at the elevated temperature treatment (31°C) compared to no single preferred habitat at 22°C or 28°C. The observed shifts in habitat preference with temperature suggest that we may be currently underestimating the vulnerability of some habitat generalists to climate change and highlight that the ongoing loss of complex live coral through coral bleaching could further exacerbate resource overlap and species competition in ways not currently considered in climate change models.     

Terrestrial chemical cues help coral reef fish larvae locate settlement habitat surrounding islands

Understanding the degree of connectivity between coastal and island landscapes and nearby coral reefs is vital to the integrated management of terrestrial and marine environments in the tropics. Coral reef fish are capable of navigating appropriate settlement habitats following their pelagic larval phase, but the mechanisms by which they do this are unclear. The importance of olfactory cues in settlement site selection has been demonstrated, and there is increasing evidence that chemical cues from terrestrial sources may be important for some species. Here, we test the olfactory preferences of eight island-associated coral reef fish recruits and one generalist species to discern the capacity for terrestrial cue recognition that may aid in settlement site selection. A series of pairwise choice experiments were used to evaluate the potential role that terrestrial, water-borne olfactory cues play in island-reef recognition. Olfactory stimuli tested included near-shore water, terrestrial rainforest leaf litter, and olfactory cues collected from different reef types (reefs surrounding vegetated islands, and reefs with no islands present). All eight island-associated species demonstrated high levels of olfactory discrimination and responded positively toward olfactory cues indicating the presence of a vegetated island. We hypothesize that although these fish use a suite of cues for settlement site recognition, one mechanism in locating their island/reef habitat is through the olfactory cues produced by vegetated islands. This research highlights the role terrestrial olfactory cues play in large-scale settlement site selection and suggests a high degree of ecosystem connectivity.     

Habitat degradation drives increased gnathiid isopod ectoparasite infection rate on juvenile but not adult fish

Widespread coral mortality is leading to coral reef degradation worldwide. Many juvenile reef fishes settle on live coral, and their predator-avoidance behaviour is disrupted in seawater exposed to dead corals, ultimately increasing predation risk. Gnathiid isopods are micropredatory fish ectoparasites that occur in higher abundances in dead coral. However, the effect of seawater associated with dead coral on the susceptibility of fish to micropredators has never been investigated. We tested whether the infection rate of cultured gnathiid ectoparasites on individual damselfish, Pomacentrus amboinensis Bleeker 1868, from two different ontogenetic stages (juveniles and adults) was influenced by seawater exposed to three different treatments: dead coral, live coral, or no coral. Seawater treatments were presumed to contain different chemical properties and are meant to represent environmental changes associated with habitat degradation on coral reefs. Gnathiid infection of juvenile fish in seawater exposed to dead coral was twice as high as that of fish in live coral or no coral. Infection rates did not significantly differ between live coral and no coral treatments. In contrast to juveniles, the susceptibility of adults to gnathiids was not affected by seawater treatment. During experiments, juvenile fish mortality was relatively low, but was higher for infected fish (9.7%), compared to fish held without exposure to gnathiids (1.7%). No mortality occurred in adult fish that became infected with gnathiids. Our results suggest that chemical cues released from dead corals and/or dead coral colonisers affect the ability of juvenile, but not adult fish to avoid parasite infection. Considering increased habitat degradation on coral reefs and that gnathiids are more abundant in dead coral substrate, it is possible that wild juvenile fish may experience increased susceptibility to parasitic infection and reduced survival rate. This highlights the importance of including parasitism in ecological studies of global environmental change.

     

Habitat choice and recruitment of tropical fishes on temperate coasts of Japan

Tropical reef corals are expanding on Japanese temperate coasts in response to rising sea surface temperatures, and many tropical fish juveniles have been observed routinely in these coral habitats. The present study explored how offshore tropical fish larvae locate coral habitat on the temperate coasts of Japan. Settlement-stage larvae were sampled between July and October 2009–2011 with light traps anchored on coral-replete and coral-free habitats (rocky habitats) at two-level distance (distance between each habitat type was 6 km and 500 m, respectively). Larval abundance was significantly higher on the coral-dominated habitat than that on the rocky habitat at both short and long distance sites, suggesting that coral habitats attract offshore tropical fish larvae. In underwater visual survey, Chaetodontidae and Pomacentridae juveniles were more abundant in coral habitats than in rocky habitats at both the sites, and a laboratory habitat choice experiment demonstrated that these larvae showed a preference for corals rather than rocks. In contrast, densities of juvenile Mullidae did not differ between the coral and rocky habitats, and the larvae did not show a substrate preference in the habitat choice experiment. These observations suggest that habitat choice at settlement possibly accounts for the differences in settlement patterns of tropical fishes between the two habitats. Taken together, our results showed that most tropical fish larvae colonize their settlement coast at a scale of ~0.5 km, and that they may locate coral habitats after reaching a reef. Moreover, the results suggest that coral habitat expansion on temperate coasts will lead to an increase in coral-associated tropical fishes and will change assemblage structures of fishes on temperate coasts.     

Habitat associations of juvenile fish at Ningaloo Reef, Western Australia: the importance of coral and algae

Habitat specificity plays a pivotal role in forming community patterns in coral reef fishes, yet considerable uncertainty remains as to the extent of this selectivity, particularly among newly settled recruits. Here we quantified habitat specificity of juvenile coral reef fish at three ecological levels; algal meadows vs. coral reefs, live vs. dead coral and among different coral morphologies. In total, 6979 individuals from 11 families and 56 species were censused along Ningaloo Reef, Western Australia. Juvenile fishes exhibited divergence in habitat use and specialization among species and at all study scales. Despite the close proximity of coral reef and algal meadows (10's of metres) 25 species were unique to coral reef habitats, and seven to algal meadows. Of the seven unique to algal meadows, several species are known to occupy coral reef habitat as adults, suggesting possible ontogenetic shifts in habitat use. Selectivity between live and dead coral was found to be species-specific. In particular, juvenile scarids were found predominantly on the skeletons of dead coral whereas many damsel and butterfly fishes were closely associated with live coral habitat. Among the coral dependent species, coral morphology played a key role in juvenile distribution. Corymbose corals supported a disproportionate number of coral species and individuals relative to their availability, whereas less complex shapes (i.e. massive & encrusting) were rarely used by juvenile fish. Habitat specialisation by juvenile species of ecological and fisheries importance, for a variety of habitat types, argues strongly for the careful conservation and management of multiple habitat types within marine parks, and indicates that the current emphasis on planning conservation using representative habitat areas is warranted. Furthermore, the close association of many juvenile fish with corals susceptible to climate change related disturbances suggests that identifying and protecting reefs resilient to this should be a conservation priority.     

Specialization in habitat use by coral reef damselfishes and their susceptibility to habitat loss

While it is generally assumed that specialist species are more vulnerable to disturbance compared with generalist counterparts, this has rarely been tested in coastal marine ecosystems, which are increasingly subject to a wide range of natural and anthropogenic disturbances. Habitat specialists are expected to be more vulnerable to habitat loss because habitat availability exerts a greater limitation on population size, but it is also possible that specialist species may escape effects of disturbance if they use habitats that are generally resilient to disturbance. This study quantified specificity in use of different coral species by six coral‐dwelling damselfishes (Chromis viridis, C. atripectoralis, Dascyllus aruanus, D. reticulatus, Pomacentrus moluccensis, and P. amboinensis) and related habitat specialization to proportional declines in their abundance following habitat degradation caused by outbreaks of the coral eating starfish, Acanthaster planci. The coral species preferred by most coral‐dwelling damselfishes (e.g., Pocillopora damicornis) were frequently consumed by coral eating crown‐of‐thorns starfish, such that highly specialized damselfishes were disproportionately affected by coral depletion, despite using a narrower range of different coral species. Vulnerability of damselfishes to this disturbance was strongly correlated with both their reliance on corals and their degree of habitat specialization. Ongoing disturbances to coral reef ecosystems are expected, therefore, to lead to fundamental shifts in the community structure of fish communities where generalists are favored over highly specialist species.     

Habitat degradation disrupts neophobia in juvenile coral reef fish

Habitat degradation not only disrupts habitat‐forming species, but alters the sensory landscape within which most species must balance behavioural activities against predation risk. Rapidly developing a cautious behavioural phenotype, a condition known as neophobia, is advantageous when entering a novel risky habitat. Many aquatic organisms rely on damage‐released conspecific cues (i.e. alarm cues) as an indicator of impending danger and use them to assess general risk and develop neophobia. This study tested whether settlement‐stage damselfish associated with degraded coral reef habitats were able to use alarm cues as an indicator of risk and, in turn, develop a neophobic response at the end of their larval phase. Our results indicate that fish in live coral habitats that were exposed to alarm cues developed neophobia, and, in situ, were found to be more cautious, more closely associated with their coral shelters and survived four‐times better than non‐neophobic control fish. In contrast, fish that settled onto degraded coral habitats did not exhibit neophobia and consequently suffered much greater mortality on the reef, regardless of their history of exposure to alarm cues. Our results show that habitat degradation alters the efficacy of alarm cues with phenotypic and survival consequences for newly settled recruits.     

Importance of live coral habitat for reef fishes

Live corals are the key habitat forming organisms on coral reefs, contributing to both biological and physical structure. Understanding the importance of corals for reef fishes is, however, restricted to a few key families of fishes, whereas it is likely that a vast number of fish species will be adversely affected by the loss of live corals. This study used data from published literature together with independent field based surveys to quantify the range of reef fish species that use live coral habitats. A total of 320 species from 39 families use live coral habitats, accounting for approximately 8 % of all reef fishes. Many of the fishes reported to use live corals are from the families Pomacentridae (68 spp.) and Gobiidae (44 spp.) and most (66 %) are either planktivores or omnivores. 126 species of fish associate with corals as juveniles, although many of these fishes have no apparent affiliation with coral as adults, suggesting an ontogenetic shift in coral reliance. Collectively, reef fishes have been reported to use at least 93 species of coral, mainly from the genus Acropora and Porities and associate predominantly with branching growth forms. Some fish associate with a single coral species, whilst others can be found on more than 20 different species of coral indicating there is considerable variation in habitat specialisation among coral associated fish species. The large number of fishes that rely on coral highlights that habitat degradation and coral loss will have significant consequences for biodiversity and productivity of reef fish assemblages.     

Trawl fishery resources in the “southern waters” of Japan

Settlement-stage larvae of the coral reef fishes Ostorhinchus doederleini (Apogonidae) and Pomacentrus coelestis (Pomacentridae) prefer the odor of their settlement reef to that of other nearby reefs. It was unknown whether these olfactory preferences are temporally stable or the result of recent olfactory experience. Ostorhinchus doederleini and P. coelestis larvae were held in aquaria and exposed to water from either their settlement reef or a neighboring reef for 5–9 days and their olfactory preference was tested. We show that exposure to water from another reef did not influence olfactory preference. Ostorhinchus doederleini olfactory preference declined slightly over time whereas P. coelestis preference was gradually lost after 2–3 days in captivity. Neither species switched their preference to the new reef odor. While we cannot determine conclusively the time window of odor learning, imprinting at or shortly after birth is logical and has been demonstrated in other fish species.     

Habitat associations of juvenile versus adult butterflyfishes

Many coral reef fishes exhibit distinct ontogenetic shifts in habitat use while some species settle directly in adult habitats, but there is not any general explanation to account for these differences in settlement strategies among coral reef fishes. This study compared distribution patterns and habitat associations of juvenile (young of the year) butterflyfishes to those of adult conspecifics. Three species, Chaetodon auriga, Chaetodon melannotus, and Chaetodon vagabundus, all of which have limited reliance on coral for food, exhibited marked differences in habitat association of juvenile versus adult individuals. Juveniles of these species were consistently found in shallow-water habitats, whereas adult conspecifics were widely distributed throughout a range of habitats. Juveniles of seven other species (Chaetodon aureofasciatus, Chaetodon baronessa, Chaetodon citrinellus, Chaetodon lunulatus, Chaetodon plebeius, Chaetodon rainfordi, and Chaetodon trifascialis), all of which feed predominantly on live corals, settled directly into habitat occupied by adult conspecifics. Butterflyfishes with strong reliance on corals appear to be constrained to settle in habitats that provide access to essential prey resources, precluding their use of distinct juvenile habitats. More generalist butterflyfishes, however, appear to utilize distinct juvenile habitats and exhibit marked differences in the distribution of juveniles versus adults.     

Consumption of coral propagules represents a significant trophic link between corals and reef fish

Mass spawning of corals provides a large seasonal pulse of high-energy prey that potentially benefits reef fish that are capable of capturing and digesting coral propagules. This study examines the range of fish species that consume coral propagules and also tests whether reef fish experience a significant increase in physiological condition when feeding on coral propagules. Thirty-six species of diurnal reef fish were seen to consume coral propagules released during mass coral spawning. Stomach content analyses of three reef fish species (Pomacentrus moluccensis, Abudefduf whitleyi, and Caesio cunning) revealed that both P. moluccensis and A. whitleyi feed almost exclusively on coral propagules during mass coral spawning. Fish feeding extensively on coral propagules also amassed considerable lipid stores, which could greatly improve the quality and survivorship of their progeny. In contrast, C. cunning consumed only very small quantities of coral propagules, and showed no detectable change in lipid stores during the course of the study. This study provides the first direct evidence that reef fish benefit from mass coral spawning, and reveals a potentially significant trophic link between scleractinian corals and reef fish. Accepted: 9 June 2000     

Population Dynamics and Spatial Distribution of Coral Reef Fishes: Comparison Between Continuous and Isolated Habitats

Recent studies have shown that there are high degrees of spatial and temporal stability in coral reef fish assemblage structures in a continuous habitat, in contrast to results of observations in isolated habitats. In order to determine the reason for the difference in temporal stability of fish assemblage structures in a continuous habitat site and an isolated habitat site, population dynamics and spatial distributions of coral reef fishes (six species of pomacentrids and two species of apogonids) in the two habitat site were investigated over a 2-year period in an Okinawan coral reef. The population densities of pomacentrid and apogonid species increased in juvenile settlement periods at both sites, but the magnitude of seasonal fluctuation in population density was significantly greater at the isolated habitat site, indicating that the rate of juvenile settlement and mortality rate in the isolated habitat were greater than those in the continuous habitat. The magnitude of aggregation of fishes, which affects density-dependent biological interactions that modify population density such as competition and predation, was also significantly greater at the isolated habitat site, especially in the juvenile settlement season. Most of the fishes at the isolated habitat site exhibited more generalized patterns of microhabitat selection because of less coral coverage and diversity. The seasonal stability in the species composition of fishes was greater at the continuous habitat site than that at the isolated habitat. Our findings suggest that the relative importance of various ecological factors responsible for regulation of the population density of coral reef fishes (e.g., competition, predation, microhabitat selection and post-settlement movement) in a continuous habitat site and the isolated habitat site are different.     

Ontogenetic changes in habitat selection during settlement in a coral reef fish: ecological determinants and sensory mechanisms

The behavior of marine larvae during and after settlement can help shape the distribution and abundance of benthic juveniles and therefore the intensity of ecological interactions on reefs. Several laboratory choice-chamber experiments were conducted to explore sensory capabilities and behavioral responses to ecological stimuli to better understand habitat selection by “pre-metamorphic” (larval) and “post-metamorphic” (juvenile) stages of a coral reef fish (Thalassoma hardwicke). T. hardwicke larvae were attracted to benthic macroalgae (Turbinaria ornata and Sargassum mangarevasae), while slightly older post-metamorphosed juveniles chose to occupy live coral colonies (Pocillopora damicornis). Habitat choices of larvae were primarily based upon visual cues and were not influenced by the presence of older conspecifics. In contrast, juveniles selected live coral colonies and preferred those occupied by older conspecifics; choices made by juveniles were based upon both visual and olfactory cues from conspecifics. Overall, the laboratory experiments suggest that early life-history stages of T. hardwicke use a range of sensory modalities that vary through ontogeny, to effectively detect and possibly discriminate among different microhabitats for settlement and later occupation. Habitat selection, based upon cues provided by environmental features and/or by conspecifics, might have important consequences for subsequent competitive interactions.     

Habitat use patterns of fishes across the mangrove-seagrass-coral reef seascape at Ishigaki Island,southern Japan

To clarify seascape-scale habitat use patterns of fishes in the Ryukyu Islands (southern Japan), visual censuses were conducted in the mangrove estuary, sand area, seagrass bed, coral rubble area, branching coral area on the reef flat, and tabular coral area on the outer reef slope at Ishigaki Island in August and November 2004, and May, August and November 2005. During the study period a total of 319 species were observed. Species richness and abundance were highest in the branching and tabular coral areas, followed in order by the seagrass bed and mangrove estuary, and coral rubble and sand areas, in each month. Cluster analysis resulted in a clear grouping of assemblage structures by habitat type rather than by census month. SIMPER analysis showed that fish assemblages in the tabular coral area were mainly characterized by Acanthurus nigrofuscus, Pomacentrus lepidogenys, P. philippinus and P. vaiuli, the branching coral area by Chromis viridis and Pomacentrus moluccensis, the coral rubble area by Amblyeleotris steinitzi and Ctenogobiops pomastictus, the seagrass bed by Cheilio inermis, Lethrinus atkinsoni and Stethojulis strigiventer, the sand area by Valenciennea longipinnis, and the mangrove estuary by Gerres oyena, Lutjanus fulvus and Yongeichthys criniger. Moreover, fishes exhibited two habitat use strategies, inhabiting either a single or several specific habitats throughout their benthic life history stages, or having a possible ontogenetic habitat shift from the mangrove estuary or seagrass bed to coral-dominated habitats (e.g., Lethrinus atkinsoni, Lethrinus obsoletus, Lutjanus fulviflamma, Lutjanus fulvus, Lutjanus gibbus, Lutjanus monostigma and Parupeneus barberinus), suggesting that the mangrove estuary and seagrass bed have a nursery function.