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.     

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.     

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.     

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.     

The influence of habitat characteristics and conspecifics on attraction and survival of coral reef fish juveniles

In marine species with a pelagic larval stage, search behavior and selection of a suitable reef habitat can maximize the settlement success of recently settled juveniles and their subsequent performance (growth and survival of juveniles). Our objective was to test this hypothesis for a single target coral reef fish species (Chromis viridis) at Moorea Island. C. viridis settle on living coral colonies of Porites rus already populated with conspecifics. In the present study (conducted in experimental cages), we found that: 1) mortality rate of recently settled juveniles of C. viridis was lower in the settlement habitat (living coral colonies of P. rus) than in other habitats having physical structure different from those of P. rus colonies; 2) C. viridis juveniles preferentially colonized coral heads of P. rus with conspecifics present rather than uninhabited coral heads and they also preferentially colonized uninhabited coral heads rather than coral heads with heterospecifics; 3) mortality rate of C. viridis juveniles did not vary with the presence or absence of conspecifics or heterospecifics on P. rus colonies. Overall, the study allows us to highlight that site selection by juveniles for habitat containing conspecifics does not benefit their short term mortality rates, suggesting that in the short term at least, site selection has little importance.     

Post-larval French grunts (Haemulon flavolineatum) distinguish between seagrass, mangrove and coral reef water: Implications for recognition of potential nursery habitats

Environmental cues like sound, magnetic field, oceanic currents, water chemistry or habitat structure are believed to play an important role in the orientation of reef fish towards their settlement habitat. Some species of coral reef fish are known to use seagrass beds and mangroves as juvenile habitats. Once oceanic larvae of these fish have located a coral reef from the open ocean, they still have to find embayments or lagoons harbouring these juvenile habitats. The sensory mechanisms that are used for this are still unknown. In the present study, experiments were conducted to investigate if recruits of the French grunt (Haemulon flavolineatum) respond to habitat differences in water type, as mangrove/seagrass water may differ in biotic and abiotic compounds from coral reef water. Our results show that post-larvae of a reef fish that is highly associated with mangroves and seagrass beds during its juvenile life stage, choose significantly more often for water from mangroves and seagrass beds than for water from the coral reef. These results provide a more detailed insight in the mechanisms that play a role in the detection of these juvenile habitats.     

Experimental study on the sensory capabilities of coral-reef fish larvae for the recognition of their settlement location

Some experiments in aquarium and in situ have been carried out to investigate the sensory abilities of coral reef fish larvae in the recognition of their settlement location. Ten out 12 species studied detected their settlement location due to the presence of conspecifics and not by habitat characteristics. Larvae use three senses in this detection: sight, smell and vibratory sense.     

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.     

Coral larvae settle at a higher frequency on red surfaces

Although chemical cues serve as the primary determinants of larval settlement and metamorphosis, light is also known to influence the behavior and the settlement of coral planulae. For example, Porites astreoides planulae settle preferentially on unconditioned red substrata. In order to test whether this behavior was a response to color and whether other species also demonstrate color preference, settlement choice experiments were conducted with P. astreoides and Acropora palmata. In these experiments, larvae were offered various types of plastic substrata representing three to seven different color choices. Both species consistently settled on red (or red and orange) substrata at a higher frequency than other colors. In one experiment, P. astreoides settled on 100% of red, plastic cable ties but failed to settle on green or white substrata. In a second experiment, 24% of larvae settled on red buttons, more than settled on six other colors combined. A. palmata settled on 80% of red and of orange cables ties but failed to settle on blue in one experiment and settled on a greater proportion of red acrylic squares than on four other colors or limestone controls in a second experiment. The consistency of the response across a variety of plastic materials suggests the response is related to long-wavelength photosensitivity. Fluorescence and reflectance spectra of experimental substrata demonstrated that the preferred substrata had spectra dominated by wavelengths greater than 550 nm with little or no reflection or emission of shorter wavelengths. These results suggest that some species of coral larvae may use spectral cues for fine-scale habitat selection during settlement. This behavior may be an adaptation to promote settlement in crustose coralline algae (CCA)-dominated habitats facilitating juvenile survival.     

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.     

Habitat selection, facilitation, and biotic settlement cues affect distribution and performance of coral recruits in French Polynesia

Habitat selection can determine the distribution and performance of individuals if the precision with which sites are chosen corresponds with exposure to risks or resources. Contrastingly, facilitation can allow persistence of individuals arriving by chance and potentially maladapted to local abiotic conditions. For marine organisms, selection of a permanent attachment site at the end of their larval stage or the presence of a facilitator can be a critical determinant of recruitment success. In coral reef ecosystems, it is well known that settling planula larvae of reef-building corals use coarse environmental cues (i.e., light) for habitat selection. Although laboratory studies suggest that larvae can also use precise biotic cues produced by crustose coralline algae (CCA) to select attachment sites, the ecological consequences of biotic cues for corals are poorly understood in situ. In a field experiment exploring the relative importance of biotic cues and variability in habitat quality to recruitment of hard corals, pocilloporid and acroporid corals recruited more frequently to one species of CCA, Titanoderma prototypum, and significantly less so to other species of CCA; these results are consistent with laboratory assays from other studies. The provision of the biotic cue accurately predicted coral recruitment rates across habitats of varying quality. At the scale of CCA, corals attached to the “preferred” CCA experienced increased survivorship while recruits attached elsewhere had lower colony growth and survivorship. For reef-building corals, the behavioral selection of habitat using chemical cues both reduces the risk of incidental mortality and indicates the presence of a facilitator.     

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.     

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.     

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.     

Recognition of individual,sex and species odours by salamanders of the Plethodon glutinosus-P. Jordani complex

Salamanders of the Plethodon glutinosus-P. jordani complex were tested for the ability to distinguish conspecific, sex-specific, and heterospecific chemical cues. Male and female P. glutinosus preferred substrates previously occupied by conspecifics over their own, but randomly chose between substrates marked by male or female conspecifics. This suggests that while these salamanders are able to distinguish between their own and conspecific substrate odours, they are unable to identify sex by means of substrate odours. Experiments using an olfactometer showed that male P. jordani, male and female P. glutinosus, and an electrophoretically distinct and non-hybridizing sympatric phenotype in the P. glutinosus complex (here called species A), all preferred female airborne odours over male airborne odours. This demonstrates that these salamanders can identify sex by means of airborne odours. Male P. glutinosus and species A both preferred conspecific female odours over heterospecific female odours in olfactometer experiments. These results suggest an important role for olfaction in the sexual and social behaviour of these salamanders, particularly as a pre-mating isolating mechanism.     

Habitat differentiation in the early life stages of simultaneously mass-spawning corals

The settlement process of coral larvae following simultaneous mass-spawning remains poorly understood, particularly in terms of population and community parameters. Here, the larval settlement patterns of Acropora corals, which are the most diverse genera of scleractinian corals at the species (haplotype) level, were investigated within a single subtropical reef. Across a 4-year period (2007–2010), the mitochondrial and nuclear molecular markers of 1,073 larval settlers were analyzed. Of the 11 dominant haplotypes of recruited populations, nine exhibited non-random patterns of settlement distribution. This result suggests that the actual habitat segregation starts during the early swimming larval stages of their life history, rather than by natural selection after random settlement. In addition, the presence of a depth-related settlement pattern supports that species-specific vertical zonation of coral larvae may play a role in the establishment of habitat segregation. Moreover, in some species that showed a preference toward the shoreward area of the bay, the settlement pattern was consistent with that of the adult distribution. This result indicates that the gametes were not mixed between fore and back reefs in the period from fertilization to settlement during the mass-spawning event, even within a single small reef. Another compatible hypothesis of this pattern is that the larvae are able to recognize various types of environmental information, facilitating the selection of optimal micro-habitats. Overall, Acropora coral larvae that are produced from a simultaneous mass-spawning event may have adapted to complex reef topography by means of multi-step habitat selection at settlement, corresponding to different spatial scales.     

The settlement behaviour of planulae larvae of the hermatypic coral Favia fragum (Esper)

Experiments on the settlement behaviour of planulae larvae of the reef coral Favia fragum (Esper) are described. The larvae are positively phototaxic upon release but reverse this and become attracted to dark surfaces, corners, crevices, and the undersides of objects on the bottom. Clean glass surfaces were preferred to surfaces covered with biological slime but there was no preference for rough against smooth surfaces. There was clear evidence of gregarious settlement behaviour, the planulae being able to recognize both adult colonies and previously settled juveniles. A distinction was made between crawling and swimming larvae, and the consequences of their differences in behaviour on the spatial distribution of Favia on reef are discussed. Settlement behaviour of Favia is similar in many respects to that of the Pacific reef coral Pocillopora damicornis (Dana) but is distinguished by gregarious settlement and by a preference for clean surfaces over surfaces covered with biological slime.     

Importance of visual cues of conspecifics and predators during the habitat selection of coral reef fish larvae

The study investigated visual recognition of conspecifics and predators by settlement-stage coral reef fish larvae in a set of three experiments using a dual-choice aquarium (Moorea Island). Experiments 1 and 2 were conducted under artificial light conditions. Experiment 3 was conducted under natural light during new and full moon nights. In experiment 1, five out of six species preferred conspecifics rather than heterospecifics (Acanthurus triostegus, Chromis viridis, Ostorhinchus angustatus, Stegastes fasciolatus, Valenciaenna strigata). In experiment 2, three out of six species were repulsed by predators (Mulloidichtys flavolineatus, O. angustatus, V. strigata). In experiment 3 (conducted on one species), A. triostegus was attracted to conspecifics during bright nights, but did not show such behavior during dark nights. Our study raises the question of trade-off for fish larvae to settle during the night with high light intensities to favor the visual recognition of conspecifics and predators, or during darker nights to reduce reef predation.     

Effects of substratum and conspecific adults on the metamorphosis of Chasmagnathus granulata (Dana) (Decapoda: Grapsidae) megalopae

The ability of marine invertebrate larvae to delay their metamorphosis in the absence of adequate environmental cues has been reported for numerous sedentary and sessile species. In the present study, the effect of various substrata and the presence of conspecific adults on the metamorphosis of a mobile species, the crab Chasmagnathus granulata, was evaluated. The duration of the megalopa stage in experiments with six different substrata and in the presence or absence of conspecific adults was compared in a laboratory study. In addition, the influence of natural substrata was compared with that of artificial substrata of similar grain size or texture. In a further experiment, the two most effective cues (natural mud and conspecific adults) were tested as single vs. combined factors. Natural mud and unidentified chemical cues from conspecific adults had the strongest accelerating effects on development duration to metamorphosis. With the exception of nylon threads (artificial filamentous substratum), none of the artificial substrata had a significant effect on the duration of the megalopa stage. Simultaneous exposure to natural mud and water containing chemical cues from conspecific adults accelerated metamorphosis more than each of these factors separately. Megalopae that were reared without a substratum (control) delayed their metamorphosis by 29% (about 3 days) compared with those in simultaneous contact with natural mud and rearing water of adult conspecifics. The results indicate that the metamorphosis of the megalopa of C. granulata is influenced by the presence or absence of environmental stimuli that are associated with the preferred adult habitat.     

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.