Size-specific recolonization success by coral-dwelling damselfishes moderates resilience to habitat loss

Increasing degradation of coral reef ecosystems and specifically, loss of corals is causing significant and widespread declines in the abundance of coral reef fishes, but the proximate cause(s) of these declines are largely unknown. Here, we examine specific responses to host coral mortality for three species of coral-dwelling damselfishes (Dascyllus aruanus, D. reticulatus, and Pomacentrus moluccensis), explicitly testing whether these fishes can successfully move and recolonize nearby coral hosts. Responses of fishes to localized coral loss was studied during population irruptions of coral feeding crown-of-thorns starfish, where starfish consumed 29 (34%) out of 85 coral colonies, of which 25 (86%) were occupied by coral-dwelling damselfishes. Damselfishes were not tagged or individually recognizable, but changes in the colonization of different coral hosts was assessed by carefully assessing the number and size of fishes on every available coral colony. Most damselfishes (> 90%) vacated dead coral hosts within 5 days, and either disappeared entirely (presumed dead) or relocated to nearby coral hosts. Displaced fishes only ever colonized corals already occupied by other coral-dwelling damselfishes (mostly conspecifics) and colonization success was strongly size-dependent. Despite movement of damselfishes to surviving corals, the local abundance of coral-dependent damselfishes declined in approximate accordance with the proportional loss of coral habitat. These results suggest that even if alternative coral hosts are locally abundant, there are significant biological constraints on movement of coral-dwelling damselfishes and recolonization of alternative coral habitats, such that localized persistence of habitat patches during moderate or patchy disturbances do not necessarily provide resilience against overall habitat loss.

Damselfishes alleviate the impacts of sediments on host corals

Mutualisms play a critical role in ecological communities; however, the importance and prevalence of mutualistic associations can be modified by external stressors. On coral reefs, elevated sediment deposition can be a major stressor reducing the health of corals and reef resilience. Here, we investigated the influence of severe sedimentation on the mutualistic relationship between small damselfishes ( Pomacentrus moluccensis and Dascyllus aruanus ) and their coral host ( Pocillopora damicornis ). In an aquarium experiment, corals were exposed to sedimentation rates of approximately 100 mg cm −2 d −1 , with and without fishes present, to test whether: (i) fishes influence the accumulation of sediments on coral hosts, and (ii) fishes moderate partial colony mortality and/or coral tissue condition. Colonies with fishes accumulated much less sediment compared with colonies without fishes, and this effect was strongest for colonies with D. aruanus (fivefold less sediment than controls) as opposed to P. moluccensis (twofold less sediment than controls). Colonies with symbiont fishes also had up to 10-fold less sediment-induced partial mortality, as well as higher chlorophyll and protein concentrations. These results demonstrate that fish mutualisms vary in the strength of their benefits, and indicate that some mutualistic or facilitative interactions might become more important for species health and resilience at high-stress levels.

Young fishes persist despite coral loss on the Great Barrier Reef

Unprecedented global bleaching events have led to extensive loss of corals. This is expected to lead to extensive losses of obligate coral-dependent fishes. Here, we use a novel, spatially-matched census approach to examine the nature of fish-coral dependency across two mass coral bleaching events. Despite a >40% loss of coral cover, and the ecological extinction of functionally important habitat-providing Acropora corals, we show that populations of obligate coral-dependent fishes, including Pomacentrus moluccensis, persisted and – critically – recruitment was maintained. Fishes used a wide range of alternate reef habitats, including other coral genera and dead coral substrata. Labile habitat associations of ‘obligate’ coral-dependent fishes suggest that recruitment may be sustained on future reefs that lack Acropora, following devastating climatic disturbances. This persistence without Acropora corals offers grounds for cautious optimism; for coral-dwelling fishes, corals may be a preferred habitat, not an obligate requirement.

Influence of nursery microhabitats on the future abundance of a coral reef fish

Species habitat associations are often complex, making it difficult to assess their influence on populations. Among coral reef fishes, habitat requirements vary among species and with ontogeny, but the relative importance of nursery and adult-preferred habitats on future abundances remain unclear. Moreover, adult populations may be influenced by recruitment of juveniles and assessments of habitat importance should consider relative effects of juvenile abundance. We conducted surveys across 16 sites and 200 km of reef to identify the microhabitat preferences of juveniles, sub-adults and adults of the damselfish Pomacentrus moluccensis . Microhabitat preferences at different life-history stages were then combined with 6 years of juvenile abundance and microhabitat availability data to show that the availability of preferred juvenile microhabitat (corymbose corals) at the time of settlement was a strong predictor of future sub-adult and adult abundance. However, the influence of nursery microhabitats on future population size differed spatially and at some locations abundance of juveniles and adult microhabitat (branching corals) were better predictors of local populations. Our results demonstrate that while juvenile microhabitats are important nurseries, the abundance of coral-dependent fishes is not solely dependent on these microhabitats, especially when microhabitats are readily available or following large influxes of juveniles.

Damsel in distress: captured damselfish prey emit chemical cues that attract secondary predators and improve escape chances

In aquatic environments, many prey animals possess damage-released chemical alarm cues that elicit antipredator behaviours in responsive con- and heterospecifics. Despite considerable study, the selective advantage of alarm cues remains unclear. In an attempt to investigate one of the more promising hypotheses concerning the evolution of alarm cues, we examined whether the cue functions in a fashion analogous to the distress vocalizations emitted by many terrestrial animals. Our results suggest that chemical alarm cues in damselfish ( Pomacentridae ) may have evolved to benefit the cue sender by attracting secondary predators who disrupt the predation event, allowing the prey a greater chance to escape. The coral reef piscivore, the dusky dottyback ( Pseudochromis fuscus ), chemically eavesdrops on predation events and uses chemical alarm cues from fish prey (lemon damselfish; Pomacentrus moluccensis ) in an attempt to find and steal prey from primary predators. Field studies showed that Ps. fuscus aggregate at sites where prey alarm cue has been experimentally released. Furthermore, secondary predators attempted to steal captured prey of primary predators in laboratory trials and enhanced prey escape chances by 35–40%. These results are the first, to the best of our knowledge, to demonstrate a mechanism by which marine fish may benefit from the production and release of alarm cues, and highlight the complex and important role that semiochemicals play in marine predator–prey interactions.

Long-term cleaner fish presence affects growth of a coral reef fish

Cleaning behaviour is considered to be a classical example of mutualism. However, no studies, to our knowledge, have measured the benefits to clients in terms of growth. In the longest experimental study of its kind, over an 8 year period, cleaner fish Labroides dimidiatus were consistently removed from seven patch reefs (61–285 m 2 ) and left undisturbed on nine control reefs, and the growth and parasite load of the damselfish Pomacentrus moluccensis determined. After 8 years, growth was reduced and parasitic copepod abundance was higher on fish from removal reefs compared with controls, but only in larger individuals. Behavioural observations revealed that P. moluccensis cleaned by L. dimidiatus were 27 per cent larger than nearby conspecifics. The selective cleaning by L. dimidiatus probably explains why only larger P. moluccensis individuals benefited from cleaning. This is the first demonstration, to our knowledge, that cleaners affect the growth rate of client individuals; a greater size for a given age should result in increased fecundity at a given time. The effect of the removal of so few small fish on the size of another fish species is unprecedented on coral reefs.