Influence of habitat degradation on fish replenishment

Temperature-induced coral bleaching is a major threat to the biodiversity of coral reef ecosystems. While reductions in species diversity and abundance of fish communities have been documented following coral bleaching, the mechanisms that underlie these changes are poorly understood. The present study examined the impacts of coral bleaching on the early life-history processes of coral reef fishes. Daily monitoring of fish settlement patterns found that ten times as many fish settled to healthy coral than sub-lethally bleached coral. Species diversity of settling fishes was least on bleached coral and greatest on dead coral, with healthy coral having intermediate levels of diversity. Laboratory experiments using light-trap caught juveniles showed that different damselfish species chose among healthy, bleached and dead coral habitats using different combinations of visual and olfactory cues. The live coral specialist, Pomacentrus moluccensis, preferred live coral and avoided bleached and dead coral, using mostly visual cues to inform their habitat choice. The habitat generalist, Pomacentrus amboinensis, also preferred live coral and avoided bleached and dead coral but selected these habitats using both visual and olfactory cues. Trials with another habitat generalist, Dischistodus sp., suggested that vision played a significant role. A 20 days field experiment that manipulated densities of P. moluccensis on healthy and bleached coral heads found an influence of fish density on juvenile weight and growth, but no significant influence of habitat quality. These results suggests that coral bleaching will affect settlement patterns and species distributions by influencing the visual and olfactory cues that reef fish larvae use to make settlement choices. Furthermore, increased fish density within the remaining healthy coral habitats could play an important role in influencing population dynamics.     

Ocean acidification alters temperature and salinity preferences in larval fish

Ocean acidification alters the way in which animals perceive and respond to their world by affecting a variety of senses such as audition, olfaction, vision and pH sensing. Marine species rely on other senses as well, but we know little of how these might be affected by ocean acidification. We tested whether ocean acidification can alter the preference for physicochemical cues used for dispersal between ocean and estuarine environments. We experimentally assessed the behavioural response of a larval fish (Lates calcarifer) to elevated temperature and reduced salinity, including estuarine water of multiple cues for detecting settlement habitat. Larval fish raised under elevated CO₂ concentrations were attracted by warmer water, but temperature had no effect on fish raised in contemporary CO₂ concentrations. In contrast, contemporary larvae were deterred by lower salinity water, where CO₂-treated fish showed no such response. Natural estuarine water—of higher temperature, lower salinity, and containing estuarine olfactory cues—was only preferred by fish treated under forecasted high CO₂ conditions. We show for the first time that attraction by larval fish towards physicochemical cues can be altered by ocean acidification. Such alterations to perception and evaluation of environmental cues during the critical process of dispersal can potentially have implications for ensuing recruitment and population replenishment. Our study not only shows that freshwater species that spend part of their life cycle in the ocean might also be affected by ocean acidification, but that behavioural responses towards key physicochemical cues can also be negated through elevated CO₂ from human emissions.     

Characteristics of Settling Coral Reef Fish Are Related to Recruitment Timing and Success

Many marine populations exhibit high variability in the recruitment of young into the population. While environmental cycles and oceanography explain some patterns of replenishment, the role of other growth-related processes in influencing settlement and recruitment is less clear. Examination of a 65-mo. time series of recruitment of a common coral reef fish, Stegastes partitus, to the reefs of the upper Florida Keys revealed that during peak recruitment months, settlement stage larvae arriving during dark lunar phases grew faster as larvae and were larger at settlement compared to those settling during the light lunar phases. However, the strength and direction of early trait-mediated selective mortality also varied by settlement lunar phase such that the early life history traits of 2–4 week old recruit survivors that settled across the lunar cycle converged to more similar values. Similarly, within peak settlement periods, early life history traits of settling larvae and selective mortality of recruits varied by the magnitude of the settlement event: larvae settling in larger events had longer PLDs and consequently were larger at settlement than those settling in smaller pulses. Traits also varied by recruitment habitat: recruits surviving in live coral habitat (vs rubble) or areas with higher densities of adult conspecifics were those that were larger at settlement. Reef habitats, especially those with high densities of territorial conspecifics, are more challenging habitats for young fish to occupy and small settlers (due to lower larval growth and/or shorter PLDs) to these habitats have a lower chance of survival than they do in rubble habitats. Settling reef fish are not all equal and the time and location of settlement influences the likelihood that individuals will survive to contribute to the population.     

Ocean acidification boosts larval fish development but reduces the window of opportunity for successful settlement

Locating appropriate settlement habitat is a crucial step in the life cycle of most benthic marine animals. In marine fish, this step involves the use of multiple senses, including audition, olfaction and vision. To date, most investigations of larval fish audition focus on the hearing thresholds to various frequencies of sounds without testing an ecological response to such sounds. Identifying responses to biologically relevant sounds at the development stage in which orientation is most relevant is fundamental. We tested for the existence of ontogenetic windows of reception to sounds that could act as orientation cues with a focus on vulnerability to alteration by human impacts. Here we show that larvae of a catadromous fish species (barramundi, Lates calcarifer) were attracted towards sounds from settlement habitat during a surprisingly short ontogenetic window of approximately 3 days. Yet, this auditory preference was reversed in larvae reared under end-of-century levels of elevated CO₂, such that larvae are repelled from cues of settlement habitat. These future conditions also reduced the swimming speeds and heightened the anxiety levels of barramundi. Unexpectedly, an acceleration of development and onset of metamorphosis caused by elevated CO₂ were not accompanied by the earlier onset of attraction towards habitat sounds. This mismatch between ontogenetic development and the timing of orientation behaviour may reduce the ability of larvae to locate habitat or lead to settlement in unsuitable habitats. The misinterpretation of key orientation cues can have implications for population replenishment, which are only exacerbated when ontogenetic development decouples from the specific behaviours required for location of settlement habitats.     

Adding coral rubble to substrata enhances settlement of Pocillopora?damicornis larvae

Settlement preferences of Pocillopora damicornis larvae were examined on artificial substrata. Planulation of P. damicornis followed a lunar cycle and the release of larvae occurred after new moon. P. damicornis larvae had the highest rates of settlement within 3 days of being presented settlement substrata. Cumulative settlement gradually increased from 3 to 8 days, and post-settlement mortality was most frequent after 8 days. Settlement experiments showed greatest settlement preference to cement tiles containing 10% coral rubble. This study suggests that physical cues are important in the settlement process, which may be useful for coral reef rehabilitation projects.     

Growth history and intrinsic factors influence risk assessment at a critical life transition for a fish

Making the appropriate decision in the face of predation risk dictates the fate of prey, and predation risk is highest at life history boundaries such as settlement. At the end of the larval phase, most coral reef fishes enter patches of reef containing novel predators. Since vision is often obscured in the complex surroundings, chemical information released from damaged conspecific is used to forewarn prey of an active predator. However, larvae enter the reef environment with their own feeding and growth histories, which will influence their motivation to feed and take risks. The present study explored the link between recent growth, feeding history, current performance and behavioural risk taking in newly settling stages of a coral reef damselfish (Pomacentrus amboinensis). Older and larger juveniles in good body condition had a stronger response to chemical alarm cues of injured conspecifics; these fish spent a longer time in shelter and displayed a more dramatic decrease in foraging behaviour than fish in lower body condition. Feeding experiments supported these findings and emphasized the importance of body condition in affecting risk assessment. Evidently, larval growth history and body condition influences the likelihood of taking risks under the threat of predation immediately after settlement, thereby affecting the probability of survival in P. amboinensis.     

Larval Settlement: The Role of Surface Topography for Sessile Coral Reef Invertebrates

For sessile marine invertebrates with complex life cycles, habitat choice is directed by the larval phase. Defining which habitat-linked cues are implicated in sessile invertebrate larval settlement has largely concentrated on chemical cues which are thought to signal optimal habitat. There has been less effort establishing physical settlement cues, including the role of surface microtopography. This laboratory based study tested whether surface microtopography alone (without chemical cues) plays an important contributing role in the settlement of larvae of coral reef sessile invertebrates. We measured settlement to tiles, engineered with surface microtopography (holes) that closely matched the sizes (width) of larvae of a range of corals and sponges, in addition to surfaces with holes that were markedly larger than larvae. Larvae from two species of scleractinian corals (Acropora millepora and Ctenactis crassa) and three species of coral reef sponges (Luffariella variabilis, Carteriospongia foliascens and Ircinia sp.,) were used in experiments. L. variabilis, A. millepora and C. crassa showed markedly higher settlement to surface microtopography that closely matched their larval width. C. foliascens and Ircinia sp., showed no specificity to surface microtopography, settling just as often to microtopography as to flat surfaces. The findings of this study question the sole reliance on chemical based larval settlement cues, previously established for some coral and sponge species, and demonstrate that specific physical cues (surface complexity) can also play an important role in larval settlement of coral reef sessile invertebrates.     

Ontogenetic changes in responses to settlement cues by Anemonefish

Population connectivity for most marine species is dictated by dispersal during the pelagic larval stage. Although reef fish larvae are known to display behavioral adaptations that influence settlement site selection, little is known about the development of behavioral preferences throughout the larval phase. Whether larvae are attracted to the same sensory cues throughout their larval phase, or exhibit distinct ontogenetic shifts in sensory preference is unknown. Here, we demonstrate an ontogenetic shift in olfactory cue preferences for two species of anemonefish, a process that could aid in understanding both patterns of dispersal and settlement. Aquarium-bred na?ve Amphiprion percula and A. melanopus larvae were tested for olfactory preference of relevant reef-associated chemical cues throughout the 11-day pelagic larval stage. Age posthatching had a significant effect on the preference for olfactory cues from host anemones and live corals for both species. Preferences of olfactory cues from tropical plants of A. percula, increased by approximately ninefold between hatching and settlement, with A. percula larvae showing a fivefold increase in preference for the olfactory cue produced by the grass species. Larval age had no effect on the olfactory preference for untreated seawater over the swamp-based tree Melaleuca nervosa, which was always avoided compared with blank seawater. These results indicate that reef fish larvae are capable of utilizing olfactory cues early in the larval stage and may be predisposed to disperse away from reefs, with innate olfactory preferences drawing newly hatched larvae into the pelagic environment. Toward the end of the larval phase, larvae become attracted to the olfactory cues of appropriate habitats, which may assist them in identification of and navigation toward suitable settlement sites.     

Early life history and settlement of the slender filefish, <Emphasis Type="Italic">Monacanthus tuckeri</Emphasis> (Monacanthidae), at Calabash Caye,Turneffe Atoll,Belize

Synopsis We examined early life history traits and patterns of settlement of the slender filefish, Monacanthus tuckeri, at Calabash Caye, Turneffe Atoll, Belize. A settlement peak was evident at the new moon, and no settlement occurred at the full moon. However, settlement rates at the quarter moons could not be estimated due to sampling gaps. Many reef fishes show new moon settlement peaks, so M. tuckeri shares some characteristics with the primarily perciform species on coral reefs. Pelagic larval duration was long (mean = 42 days) and variable, suggesting that dispersal patterns might be diverse. Size at settlement was large (mean = 32 mm total length) and also variable. Larval duration and size at settlement were outside of the average values exhibited by reef fishes, but are not beyond the extreme end of the range, and might be explained by association with pelagic debris prior to settlement. There were no differences in overall settlement rates on reef and seagrass habitats, and fish settling to either habitat did not differ in larval duration, size at settlement, or larval growth rate. This suggests that settlement to alternative habitats may be random, or driven by availability of suitable microhabitat, rather than habitat quality or individual traits.     

Coral settlement onto Halimeda opuntia: a fatal attraction to an ephemeral substrate?

Degraded reefs with a high abundance of macroalgae usually also have low densities of coral recruits. Few studies, however, have examined whether these algae affect coral larval settlement. This study demonstrates, experimentally, that larvae of the Caribbean coral Favia fragrum can settle on the green alga Halimeda opuntia even when another substrate more suitable for settlement is present. Larval settlement onto experimental substrates was quantified under three treatments: rubble only, rubble plus plastic algal mimic, and rubble plus live H. opuntia. Similar total larval settlement was observed in all treatments. No larvae settled on the algal mimic, but total settlement was similar on the rubble in the first two treatments, showing that the rubble alone offered sufficient substrate for high settlement success. About half the larvae in the live algal treatment settled on H. opuntia instead of on the rubble, showing that larvae did not reject this substrate as they did the algal mimic. This result raises the possibility that corals will settle on some macroalgae when their abundance is high. Most macroalgae, including H. opuntia, are ephemeral substrates unsuitable for post-settlement survival. Such unexpected settlement may therefore have significant consequences for coral recruitment success on algal-dominated reefs.     

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.     

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.     

Intrageneric variation in antipredator responses of coral reef fishes affected by ocean acidification: implications for climate change projections on marine communities

Our planet is experiencing an increase in the concentration of atmospheric carbon dioxide (CO₂) unprecedented in the past 800 000 years. About 30% of excess atmospheric CO₂ is absorbed by the oceans, thus increasing the concentration of carbonic acid and reducing the ocean's pH. Species able to survive the physiological stress imposed by ocean acidification may still suffer strong indirect negative consequences. Comparing the tolerance of different species to dissolved CO₂ is a necessary first step towards predicting the ecological impacts of rising CO₂ levels on marine communities. While it is intuitive that not all aquatic species will be affected the same way by CO₂, one could predict that closely related species, sharing similar life histories and ecology, may show similar tolerance levels to CO₂. Our ability to create functional groups of species according to their CO₂ tolerance may be crucial in our ability to predict community change in the future. Here, we tested the effects of CO₂ exposure on the antipredator responses of four damselfish species (Pomacentrus chrysurus, Pomacentrus moluccensis, Pomacentrus amboinensis and Pomacentrus nagasakiensis). Although being sympatric and sharing the same ecology and life history, the four congeneric species showed striking and unexpected variation in CO₂ tolerance, with CO₂‐induced loss of response to predation risk ranging from 30% to 95%. Using P. chrysurus as a model species, we further tested if these behavioural differences translated into differential ability to survive predators under natural conditions. Our results indicate that P. chrysurus larvae raised under CO₂ levels predicted by 2070 and 2100 showed decreased antipredator responses to risk, leading to a five‐ to sevenfold increase in predation‐related mortality in the first few hours of settlement. Examining ocean acidification, along with other environmental variables, will be a critical step in further evaluating ecological responses to predicted climatic change.     

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.     

The effects of age and size on habitat selection during settlement of a damselfish

The adults of many coral reef fish species are site-attached, and their habitat is selected at the time of settlement by their larvae. The length of the planktonic larval period varies both intra- and interspecifically, and it is unknown how the age and size of larvae may affect their selection of habitat. To investigate the influence of age and size on habitat selection, I collected newly settled Hawaiian domino damselfish, Dascyllus albisella, daily from grids containing three coral species at four locations in Kaneohe Bay, Oahu, Hawaii. I recorded the coral species each fish was collected on, and measured and aged (by otoliths) the collected fish. The results indicate that the coral Pocillopora meandrina was selected by settling fish significantly more than the other two coral species. Younger and smaller larvae selected this coral species more frequently than older/larger larvae. In addition, younger/smaller individuals were found more commonly inside the bay than older/larger settling larvae. Differences in the choice of coral species and location of settlement may be partly due to ontogenetic differences in the sensory capacities of larvae to detect corals, conspecifics, and predators, or to a larval competency period. This revised version was published online in July 2006 with corrections to the Cover Date.     

Visual and chemical cues in habitat selection of sepioid larvae

The present study explored, by experiments in aquaria, the modality of senses used by sepioid larvae (Euprymna scolopes) when searching for their species’ settlement habitat (Rangiroa, French Polynesia). Our results showed that E. scolopes larvae made active choices among the four habitats tested (living coral, dead coral, macroalgae and sand), and that their selective choice was influenced by presence or absence of conspecifics on the habitat. Sensory experiments showed that E. scolopes larvae differentiated between conspecifics and heterospecifics (and not between their preferred habitat versus the least preferred habitat) using both visual and olfactory cues. Overall, our results suggest species-specific cues may play a vital role in establishment spatial patterns at settlement.     

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.     

The morphology and ultrastructure of the peripheral olfactory organ in newly metamorphosed coral-dwelling gobies, Paragobiodon xanthosomus Bleeker (Gobiidae, Teleostei)

We examined the peripheral olfactory organ in newly metamorphosed coral-dwelling gobies, Paragobiodon xanthosomus (SL=5.8mm+/-0.8mm, N=15), by the aid of electron microscopy (scanning and transmission) and light microscopy. Two bilateral olfactory placodes were present in each fish. They were oval-shaped and located medio-ventrally, one in each of the olfactory chambers. Each placode had a continuous cover of cilia. The placode epithelium contained three different types of olfactory receptor neurons: ciliated, microvillous and crypt cells. The latter type was rare. Following a pelagic larval phase, P. xanthosomus settle to the reef and form an obligate association with one species of coral, Seriatopora hystrix. Their well-developed olfactory organs likely enable larvae of P. xanthosomus to detect chemical cues that assist in navigating towards and selecting appropriate coral habitat at settlement. Our findings support past studies showing that the peripheral olfactory organ develops early in coral reef fishes.     

Evidence of density-independent mortality in a settling coral reef damselfish, Chromis viridis

To know if the variation in the number of settling fish larvae can be dampened by density-dependent postsettlement mortality, we investigated the relationship between settler density and predator-induced mortality of a coral reef damselfish, Chromis viridis. Totals of 2, 3, 5, 8, 10, 12, 14, 16, 18, and 20 fish of 10 or 20 mm total length were released in experimental cages enclosing a coral head of Porites rus (to provide settlement habitat) and five predators. The results showed that the mortality rate of both 10- and 20-mm fish was density independent.     

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.