Tropical Fishes Dominate Temperate Reef Fish Communities within Western Japan

Climate change is resulting in rapid poleward shifts in the geographical distribution of tropical and subtropical fish species. We can expect that such range shifts are likely to be limited by species-specific resource requirements, with temperate rocky reefs potentially lacking a range of settlement substrates or specific dietary components important in structuring the settlement and success of tropical and subtropical fish species. We examined the importance of resource use in structuring the distribution patterns of range shifting tropical and subtropical fishes, comparing this with resident temperate fish species within western Japan (Tosa Bay); the abundance, diversity, size class, functional structure and latitudinal range of reef fishes utilizing both coral reef and adjacent rocky reef habitat were quantified over a 2 year period (2008–2010). This region has undergone rapid poleward expansion of reef-building corals in response to increasing coastal water temperatures, and forms one of the global hotspots for rapid coastal changes. Despite the temperate latitude surveyed (33°N, 133°E) the fish assemblage was both numerically, and in terms of richness, dominated by tropical fishes. Such tropical faunal dominance was apparent within both coral, and rocky reef habitats. The size structure of the assemblage suggested that a relatively large number of tropical species are overwintering within both coral and rocky habitats, with a subset of these species being potentially reproductively active. The relatively high abundance and richness of tropical species with obligate associations with live coral resources (i.e., obligate corallivores) shows that this region holds the most well developed temperate-located tropical fish fauna globally. We argue that future tropicalisation of the fish fauna in western Japan, associated with increasing coral habitat development and reported increasing shifts in coastal water temperatures, may have considerable positive economic impacts to the local tourism industry and bring qualitative changes to both local and regional fisheries resources.     

Small invertebrate consumers produce consistent size spectra across reef habitats and climatic zones

Changes in invertebrate body size-distributions that follow loss of habitat-forming species can potentially affect a range of ecological processes, including predation and competition. In the marine environment, small crustaceans and other mobile invertebrates (‘epifauna') represent a basal component in reef food webs, with a pivotal secondary production role that is strongly influenced by their body size-distribution. Ongoing degradation of reef habitats that affect invertebrate size-distributions, particularly transformation of coral and kelp habitat to algal turf, may thus fundamentally affect secondary production. Here we explored variation in size spectra of shallow epifaunal assemblages (i.e. the slope and intercept of the linear relationship between log abundance and body size at the assemblage level) across 21 reef microhabitats distributed along an extensive eastern Australian climatic gradient from the tropical northern Great Barrier Reef to cool temperate Tasmania. When aggregated across microhabitats at the site scale, invertebrate body size spectra (0.125–8 mm range) were consistently log-linear (R² ranging 0.87–0.98). Size spectra differed between, but not within, major groups of microhabitats, and exhibited little variability between tropical and temperate biomes. Nevertheless, size spectra showed significant tropical/temperate differences in slopes for epifauna sampled on macroalgal habitats, and in elevation for soft coral and sponge habitats. Our results reveal epifaunal size spectra to be a highly predictable macro-ecological feature. Given that variation in epifaunal size spectra among groups of microhabitats was greater than variation between tropical and temperate biomes, we postulate that ocean warming will not greatly alter epifaunal size spectra directly. However, transformation of tropical coral and temperate macroalgal habitats to algal turfs due to warming will alter reef food web dynamics through redistribution of the size of prey available to fishes.     

‘Stick with your own kind,or hang with the locals?’ Implications of shoaling strategy for tropical reef fish on a range‐expansion frontline

Range shifts of tropical marine species to temperate latitudes are predicted to increase as a consequence of climate change. To date, the research focus on climate‐mediated range shifts has been predominately dealt with the physiological capacity of tropical species to cope with the thermal challenges imposed by temperate latitudes. Behavioural traits of individuals in the novel temperate environment have not previously been investigated, however, they are also likely to play a key role in determining the establishment success of individual species at the range‐expansion forefront. The aim of this study was to investigate the effect of shoaling strategy on the performance of juvenile tropical reef fishes that recruit annually to temperate waters off the south east coast of Australia. Specifically, we compared body‐size distributions and the seasonal decline in abundance through time of juvenile tropical fishes that shoaled with native temperate species (‘mixed’ shoals) to those that shoaled only with conspecifics (as would be the case in their tropical range). We found that shoaling with temperate native species benefitted juvenile tropical reef fishes, with individuals in ‘mixed’ shoals attaining larger body‐sizes over the season than those in ‘tropical‐only’ shoals. This benefit in terms of population body‐size distributions was accompanied by greater social cohesion of ‘mixed’ shoals across the season. Our results highlight the impact that sociality and behavioural plasticity are likely to play in determining the impact on native fish communities of climate‐induced range expansion of coral reef fishes.     

Ontogenetic changes in foraging tactics of the piscivorous cornetfish <Emphasis Type="Italic">Fistularia commersonii</Emphasis>

Foraging behaviors of the piscivorous cornetfish Fistularia commersonii were observed at shallow reefs in Kuchierabu-jima Island, southern Japan. This fish foraged on two types of prey fishes: one was reef fish that typically dwell on or near substrata (e.g., Tripterygiidae and Labridae), and the other was pelagic fish that shoal in the water column (e.g., Clupeidae and Carangidae). The prey sizes, prey types and foraging behaviors changed as the predator size increased. Prey sizes were largely limited by gape size of the cornetfish, and small predators consumed small prey. The small cornetfish (10–30 cm in total length) fed only on reef fish captured after stalking (where the fish slowly approaches the prey and then suddenly attacks). The stalking was done either solitarily or in foraging association with conspecifics. Large fish (30–120 cm) fed on both types of fishes by stalking and/or chasing (where the fish chases the prey using its high mobility and attacks), either solitarily or in foraging association with con- or heterospecifics. Thus, chasing was only performed by the large cornetfish against pelagic prey fish in associative foraging with other con- and heterospecific predators. As their body sizes increased, F. commersonii began to show a diversification of foraging behaviors, which was strongly related not only to the habitat types and anti-predatory behaviors of the prey fishes but also to associative foraging with con- or heterospecifics, which improves their foraging success.     

Latitudinal gradients in Atlantic reef fish communities: trophic structure and spatial use patterns

Trophic strategies and spatial use habits were investigated in reef fish communities. The results supported the hypothesis of differential use of food resources among tropical and higher latitude reef fishes, i.e . the number of species and relative abundance of fishes relying on relatively low‐quality food significantly decreased from tropical to temperate latitudes. The species : genus ratio of low‐quality food consumers increased toward the tropics, and was higher than the overall ratio considering all fishes in the assemblages. This supports the view that higher speciation rates occurred among this guild of fishes in warm waters. It was also demonstrated that density of herbivorous fishes (the dominant group relying on low‐quality food resources) in the western Atlantic decreased from tropical to temperate latitudes. Spatial use and mobility varied with latitude and consequently reef type and complexity. Fishes with small‐size home ranges predominated on tropical coral reefs.     

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.     

Temperate macroalgae impacts tropical fish recruitment at forefronts of range expansion

Warming waters and changing ocean currents are increasing the supply of tropical fish larvae to temperature regions where they are exposed to novel habitats, namely temperate macroalgae and barren reefs. Here, we use underwater surveys on the temperate reefs of south-eastern (SE) Australia and western Japan (~33.5°N and S, respectively) to investigate how temperate macroalgal and non-macroalgal habitats influence recruitment success of a range of tropical fishes. We show that temperate macroalgae strongly affected recruitment of many tropical fish species in both regions and across three recruitment seasons in SE Australia. Densities and richness of recruiting tropical fishes, primarily planktivores and herbivores, were over seven times greater in non-macroalgal than macroalgal reef habitat. Species and trophic diversity (K-dominance) were also greater in non-macroalgal habitat. Temperate macroalgal cover was a stronger predictor of tropical fish assemblages than temperate fish assemblages, reef rugosities or wave exposure. Tropical fish richness, diversity and density were greater on barren reef than on reef dominated by turfing algae. One common species, the neon damselfish (Pomacentrus coelestis), chose non-macroalgal habitat over temperate macroalgae for settlement in an aquarium experiment. This study highlights that temperate macroalgae may partly account for spatial variation in recruitment success of many tropical fishes into higher latitudes. Hence, habitat composition of temperate reefs may need to be considered to accurately predict the geographic responses of many tropical fishes to climate change.

     

The tropicalization of temperate marine ecosystems: climate-mediated changes in herbivory and community phase shifts

Climate-driven changes in biotic interactions can profoundly alter ecological communities, particularly when they impact foundation species. In marine systems, changes in herbivory and the consequent loss of dominant habitat forming species can result in dramatic community phase shifts, such as from coral to macroalgal dominance when tropical fish herbivory decreases, and from algal forests to ‘barrens’ when temperate urchin grazing increases. Here, we propose a novel phase-shift away from macroalgal dominance caused by tropical herbivores extending their range into temperate regions. We argue that this phase shift is facilitated by poleward-flowing boundary currents that are creating ocean warming hotspots around the globe, enabling the range expansion of tropical species and increasing their grazing rates in temperate areas. Overgrazing of temperate macroalgae by tropical herbivorous fishes has already occurred in Japan and the Mediterranean. Emerging evidence suggests similar phenomena are occurring in other temperate regions, with increasing occurrence of tropical fishes on temperate reefs.     

Multiple disturbances and the global degradation of coral reefs: are reef fishes at risk or resilient?

Increased frequency of disturbances and anthropogenic activities are predicted to have a devastating impact on coral reefs that will ultimately change the composition of reef associated fish communities. We reviewed and analysed studies that document the effects of disturbance‐mediated coral loss on coral reef fishes. Meta‐analysis of 17 independent studies revealed that 62% of fish species declined in abundance within 3 years of disturbances that resulted in >10% decline in coral cover. Abundances of species reliant on live coral for food and shelter consistently declined during this time frame, while abundance of some species that feed on invertebrates, algae and/or detritus increased. The response of species, particularly those expected to benefit from the immediate loss of coral, is, however, variable and is attributed to erratic replenishment of stocks, ecological versatility of species and sublethal responses, such as changes in growth, body condition and feeding rates. The diversity of fish communities was found to be negatively and linearly correlated to disturbance‐mediated coral loss. Coral loss >20% typically resulted in a decline in species richness of fish communities, although diversity may initially increase following small declines in coral cover from high coverage. Disturbances that result in an immediate loss of habitat complexity (e.g. severe tropical storms), have a greater impact on fishes from all trophic levels, compared with disturbances that kill corals, but leave the reef framework intact (e.g. coral bleaching and outbreaks of Acanthaster planci). This is most evident among small bodied species and suggests the long‐term consequences of coral loss through coral bleaching and crown‐of‐thorn starfish outbreaks may be much more substantial than the short‐term effects currently documented.     

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.     

Intentional partial beaching in a coral reef fish: a newly recorded hunting behaviour of titan triggerfish,Balistoides viridescens

Coral reef fishes use a multitude of diverse feeding behaviours to increase their ability to successfully capture a wide range of prey. Here, this study reports a novel hunting behaviour in a coral reef fish, the titan triggerfish, Balistoides viridescens, where an individual was seen partially beaching itself while attempting to catch a Red Sea ghost crab, Ocypode saratan. This is the first report of this behaviour in the order Tetraodontiformes and represents an astonishing capability of this species to exploit food resources outside their typical assumed ecological niche.     

Tool use by a temperate wrasse,California sheephead Semicossyphus pulcher

Multiple individuals of a temperate reef fish species (California sheephead Semicossyphus pulcher) were observed using an anvil to crush hard‐bodied invertebrate prey. Potential implications for this behaviour extend from individuals, which may experience reduced likelihood of injury and increased reproduction, to communities, which could see changes in prey abundance and size‐distribution, with particularly important consequences for communities regulated by top‐down processes. Until relatively recently, the use of simple tools by fishes was overlooked compared with observations of tool use by primates and birds; however, observations of tool use, and interesting foraging behaviours in general, by aquatic organisms should increase with improved underwater monitoring technology.     

Environmental drivers of diurnal visits by transient predatory fishes to Caribbean patch reefs

Video cameras recorded the diurnal visitation rates of transient (large home range) piscivorous fishes to coral patch reefs in The Bahamas and identified 11 species. Visits by bar jack Caranx ruber, mutton snapper Lutjanus analis, yellowtail snapper Ocyurus chrysurus, barracuda Sphyraena barracuda and cero Scomberomorus regalis were sufficiently frequent to correlate with a range of biophysical factors. Patch‐reef visitation rates and fish abundances varied with distance from shore and all species except S. regalis were seen more frequently inshore. This pattern is likely to be caused by factors including close proximity to additional foraging areas in mangroves and on fore‐reefs and higher abundances close to inshore nursery habitats. Visitation rates and abundances of C. ruber, L. analis, O. chrysurus and S. regalis also varied seasonally (spring v. winter), possibly as fishes responded to temperature changes or undertook spawning migrations. The abundance of each transient predator species on the patch reefs generally exhibited limited diurnal variability, but L. analis was seen more frequently towards dusk. This study demonstrates that the distribution of transient predators is correlated spatially and temporally with a range of factors, even within a single lagoon, and these drivers are species specific. Transient predators are considered an important source of mortality shaping reef‐fish assemblages and their abundance, in combination with the biomass of resident predators, was negatively correlated with the density of prey fishes. Furthermore, transient predators are often targeted by fishers and understanding how they utilize seascapes is critical for protecting them within reserves.     

Predator density and competition modify the benefits of group formation in a shoaling reef fish

Synthesis Predation risk experienced by individuals living in groups depends on the balance between predator dilution, competition for refuges, and predator interference or synergy. These interactions operate between prey species as well: the benefits of group living decline in the presence of an alternative prey species. We apply a novel model‐fitting approach to data from field experiments to distinguish among competing hypotheses about shifts in predator foraging behavior across a range of predator and prey densities. Our study provides novel analytical tools for analyzing predator foraging behavior and offers insight into the processes driving the dynamics of coral reef fish. Studies of predator foraging behavior typically focus on single prey species and fixed predator densities, ignoring the potential importance of complexities such as predator dilution; predator‐mediated effects of alternative prey; heterospecific competition; or predator–predator interactions. Neglecting the effects of prey density is particularly problematic for prey species that live in mixed species groups, where the beneficial effects of predator dilution may swamp the negative effects of heterospecific competition. Here we use field experiments to investigate how the mortality rates of a shoaling coral reef fish (a wrasse: Thalassoma amblycephalum), change as a result of variation in: 1) conspecific density, 2) density of a predator (a hawkfish: Paracirrhites arcatus), and 3) presence of an alternative prey species that competes for space (a damselfish: Pomacentrus pavo). We quantify changes in prey mortality rates from the predator's perspective, examining the effects of added predators or a second prey species on the predator's functional response. Our analysis highlights a model‐fitting approach that discriminates amongst multiple hypotheses about predator foraging in a community context. Wrasse mortality decreased with increasing conspecific density (i.e. mortality was inversely density‐dependent). The addition of a second predator doubled prey mortality rates, without significantly changing attack rate or handling time – i.e. there was no evidence for predator interference. The presence of a second prey species increased wrasse mortality by 95%; we attribute this increase either to short‐term apparent competition (predator aggregation) or to a decrease in handling time of the predator (e.g. through decreased wrasse vigilance). In this system, 1) prey benefit from intraspecific group living though a reduced predation risk, and 2) the benefit of group living is reduced in the presence of an alternative prey species.     

Tropical herbivores provide resilience to a climate‐mediated phase shift on temperate reefs

Climate‐mediated changes to biotic interactions have the potential to fundamentally alter global ecosystems. However, the capacity for novel interactions to drive or maintain transitions in ecosystem states remains unresolved. We examined temperate reefs that recently underwent complete seaweed canopy loss and tested whether a concurrent increase in tropical herbivores could be maintaining the current canopy‐free state. Turf‐grazing herbivorous fishes increased in biomass and diversity, and displayed feeding rates comparable to global coral reefs. Canopy‐browsing herbivores displayed high (~ 10 000 g 100 m^?2) and stable biomass between 2006 and 2013. Tropical browsers had the highest abundance in 2013 and displayed feeding rates approximately three times higher than previously observed on coral reefs. These observations suggest that tropical herbivores are maintaining previously kelp‐dominated temperate reefs in an alternate canopy‐free state by grazing turfs and preventing kelp reestablishment. This remarkable ecosystem highlights the sensitivity of biotic interactions and ecosystem stability to warming and extreme disturbance events.     

Foraging in corallivorous butterflyfish varies with wave exposure

Understanding the foraging patterns of reef fishes is crucial for determining patterns of resource use and the sensitivity of species to environmental change. While changes in prey availability and interspecific competition have been linked to patterns of prey selection, body condition, and survival in coral reef fishes, rarely has the influence of abiotic environmental conditions on foraging been considered. We used underwater digital video to explore how prey availability and wave exposure influence the behavioural time budgets and prey selectivity of four species of obligate coral-feeding butterflyfishes. All four species displayed high selectivity towards live hard corals, both in terms of time invested and frequency of searching and feeding events. However, our novel analysis revealed that such selectivity was sensitive to wave exposure in some species, despite there being no significant differences in the availability of each prey category across exposures. In most cases, these obligate corallivores increased their selectivity towards their most favoured prey types at sites of high wave exposure. This suggests there are costs to foraging under different wave environments that can shape the foraging patterns of butterflyfishes in concert with other conditions such as prey availability, interspecific competition, and territoriality. Given that energy acquisition is crucial to the survival and fitness of fishes, we highlight how such environmental forcing of foraging behaviour may influence the ecological response of species to the ubiquitous and highly variable wave climates of shallow coral reefs.     

Predation avoidance and foraging efficiency contribute to mixed-species shoaling by tropical and temperate fishes

The formation of mixed-species social groups, whereby heterospecifics form and maintain either transient or stable groups with each other, can confer substantial fitness benefits to individuals. Such benefits may arise via multiple mechanisms associated with both predation avoidance and foraging efficiency. In fishes, mixed-species shoaling reportedly occurs where displaced tropical species (known as “vagrants”) interact with resident temperate species, although little is known about the nature and frequency of such interactions. To investigate this phenomenon, we used displaced tropical Indo-pacific Sergeant Abudefduf vaigiensis settling in temperate south-eastern Australia as a model system. Underwater visual surveys revealed shoal composition and size differed significantly between open-water and reef habitats, with shoals in open habitats being larger and more speciose. Shoals containing A. vaigiensis were mainly mixed-species, and larger and more speciose in open habitats than nearer to reef. Since both foraging efficiency (via access to plankton) and predation threat likely increase with increasing distance from reef habitat, we suggest that mixed-species shoaling mitigates predation risk whilst allowing increased foraging opportunities for A. vaigiensis in open areas. These findings provide support for the importance of mixed-species shoaling to the persistence of tropical reef fishes in temperate regions.     

Growth-related changes in diet and foraging behavior of the yellow wrasseThalassoma lutescens at Kuchierabu Island

Ontogenetic changes in diet and foraging behavior ofThalassoma lutescens were examined in shallow reef habitats around Kuchierabu Island, southern Japan. This species mainly took small benthic invertebrates, including gammarids, polychaetes, sipunculids, chitons, crabs, gastropods, pelecypods and urchins from algal mats. Larger fish consumed correspondingly larger prey, although most of the latter were armored with hard exoskeletons, shells or body plates (e.g., crabs, gastropods, pelecypods and urchins). Such hard parts were crushed with the molar-like, pharyngeal teeth which develop with fish growth, allowing exploitation of such larger, hard-bodied prey. Because the densities of larger prey species were relatively low in the initial habitats foraged, larger fish shifted their foraging attention to rock and coral crevices, where the prey species dwelt in greater numbers, as well as foraging over larger areas. Such behavioral changes maintained high foraging efficiency in larger fish.     

永兴岛附近海域珊瑚礁鱼类群落结构特征

为更好地保护和管理西沙永兴岛附近海域珊瑚礁鱼类,于2020—2021年对永兴岛上岸渔获物进行了调查研究,分析了鱼类群落结构组成及其变化和演替特征。结果表明:调查共发现永兴岛附近海域珊瑚礁鱼类101种,隶属于5目21科,以鲈形目鱼类最多,占总种类的84.16%,生物量超总渔获物的90%;科级水平鹦嘴鱼科鱼类最多,达21种,生物量超总渔获物的45%。28种珊瑚礁鱼类是永兴岛附近海域主要捕捞对象,占总渔获物的80%以上。永兴岛附近海域珊瑚礁鱼类呈现过度捕捞,一是主要渔获物中的中大型鱼类均重偏小;二是本海域个体体型最大的鱼类出现较多消亡;三是肉食性鱼类大量消亡;四是植食性鱼类生物量占比超过了肉食性鱼类。永兴岛附近海域珊瑚礁鱼类已经演替到以植食性鱼类为主导的生态系统;大量海胆的出现,表明了这一珊瑚礁生态系统在进一步衰退,向以海胆为主导的生态系统演变。保护西沙永兴岛附近海域珊瑚礁鱼类已经刻不容缓,需要严格地控制本海域的捕捞强度。     

Orientation behavior of butterflyfishes (family Chaetodontidae) on coral reefs: spatial learning of route specific landmarks and cognitive maps

Synopsis Foraging butterflyfishes follow predictable paths as they swim from one food patch to another within their territories and home ranges. The pattern is repeated throughout the day. The behavior is described in species belonging to the coral feeding guild. Habit formation and spatial learning are implicated. Foraging paths are based on learned locations of route specific landmarks. When a coral head is removed the fish look for it in its former location. If pairs of foraging fish are deflected from the path, they resume their routine pattern at the first landmark they encounter. Periodically, fish make excursions of 30 m or more to distant parts of the reef. Usually they follow different paths on the outbound and homeward legs of these excursions. The critical question is: Are the paths novel? If they are, it is evidence for the use of cognitive maps. Certainly fishes living in the highly structured coral reef environment are prime candidates to use cognitive maps in their orientation behavior.