Salvador Zarco-Perello

Rabbitfishes (Siganidae) are common members of coastal and estuarine fish assemblages throughout the tropical Indo-Pacific, where they contribute to key ecological processes and ecosystem goods and services. In this review, we summarise current knowledge of the phylogeny, biogeography, life history, habitat associations, feeding ecology, fisheries and aquaculture production of rabbitfishes (Siganidae). Rabbitfishes, which consist of 29-32 species within the single genus Siganus, display remarkable diversity of biological traits that make them unique from other families of herbivorous fishes. Their tolerances to environmental conditions and plastic life history characteristics have allowed them to colonise diverse ecosystems, expand their ranges to higher latitudes, emerge among the most important consumers of macroalgae and seagrass, sustain high intensity fisheries and be very promising for the aquaculture industry. While research on rabbitfishes has started to highlight their importance, further biological and ecological research is needed on more species across different spatial and temporal scales to better understand their relevance for ecosystem functions, their responses to disturbances and the sustainable harvesting of wild populations and aquaculture production.

Climate change is causing poleward expansions of species. Notably, the rabbitfishes (Siganidae) Siganus rivulatus, Siganus luridus and Siganus fuscescens are spearheading the range-expansion of tropical herbivorous fishes into the Mediterranean Sea, Western and Eastern Australia, and Japan. Their range-expansion success is likely due to their plastic biological traits, such as adjustments in phenology, fecundity, habitat associations, and diets, making them highly competitive under a diverse set of environments. Their expansion has led to increased consumption of temperate habitat-forming macrophytes (e.g. Ecklonia spp. and Cystoseira spp.). In Japan, aggregations of rabbitfishes exceeding 500 individuals have been linked to kelp deforestation. Transplantation experiments have shown that rabbitfishes can readily consume solitary adult and juvenile kelps, potentially maintaining canopy-free states. Despite these negative impacts, rabbitfishes have positively influenced local economies, becoming important catches in recreational and commercial fisheries, especially in the eastern Mediterranean Sea, where catches reach hundreds of tonnes valued at millions of euros annually. As climate change progresses, integrating tropical herbivorous fishes in management strategies will become crucial for temperate reefs. Future solutions should include cost-benefit analyses of the ecological and social impacts of range-expansions, particularly considering kelp forests resilience to thermal stress.

Marine fish communities are highly diverse and contribute significantly to ecosystem processes. However, understanding their specific functional roles and the importance of different prey groups for sustaining fish communities has been limited by the historical classification of fishes into a few coarse trophic guilds. Using diet information to perform a high‐resolution trophic classification of 298 temperate reef fish species distributed across south‐western Australia, we built metacommunity and subregional trophic networks to evaluate the most important trophic relationships and energy pathways in temperate reefs. We identified 26 specialized trophic guilds within the groups of herbivores, zoobenthivores, zooplanktivores, piscivores, and cleaners. Zoobenthivorous fishes had the highest species richness and trophic diversity with 191 species in nine guilds. Consumers of crustaceans showed greater species redundancy at the metacommunity level. In contrast, a low redundancy of echinodermivores could represent a risk to local capacity for top‐down control of sea urchins across the region. Finer scale analysis of prey at the family level showed that piscivorous guilds may influence different trophic pathways, with some guilds consuming other piscivorous fishes, while others consume lower trophic levels, particularly crustaceavores. Evidence of predation on herbivorous guilds was only found for turf grazers, suggesting that fish herbivory might not function as a major direct link between primary producers and higher trophic levels. Among the prey consumed by fishes, micro‐crustaceans and decapods accounted for 33% of all diet proportions. The importance of macrophytes to the fish community likely resides indirectly through the trophic pathway of herbivorous and detritivorous invertebrates, particularly crustaceans, which are more consumed by fishes than macrophytes themselves. Comparison of trophic networks in the region showed that warmer locations had higher species redundancy per node and higher strength in trophic interactions. Yet, all networks had structural properties consistent with the meta‐network regarding the importance of prey groups and modularity. Considering high‐resolution predator–prey interactions enhances our understanding of the blue‐print of ecosystem functions in shallow marine systems. Identifying the specific trophic significance of different consumers and prey groups is important for ecological forecasting and the prioritization of conservation and resource management regulations in our current fast‐changing world.

Feeding habits of herbivorous fishes play an important role in shaping form and function of coastal marine ecosystems. Rabbitfishes (Siganidae) are important consumers of macroalgae on Indo-West Pacific coral reefs. However, it is unclear how their diet varies among and within species at biogeographical scales, casting doubt on their precise functional roles across different regions. The present study assessed the inter- and intraspecific diet variation of four rabbitfishes (Siganus trispilos, Siganus coralinus, Siganus virgatus, and Siganus doliatus) factored by morphological relatedness among populations from Ningaloo Reef (western Australia), the Great Barrier Reef (GBR, eastern Australia) and the Yaeyama Islands (Okinawa Prefecture, Japan). Results showed that region had a strong effect on diet, effectively reducing the expected effect of morphologic similitude. While intraspecific differences were only significant when populations inhabited different regions; interspecific differences were not as predicted, with different morphotypes having similar diets when populations inhabited the same regions. Rabbitfishes consumed more corticated and filamentous macroalgae on the GBR, more foliose and membranous macroalgae at the Yaeyama Islands, and more leathery macroalgae at Ningaloo Reef. The findings indicate that rabbitfishes have high diet plasticity, and hence their functional role as mediators of competition between macroalgae and corals can change across biogeographic regions. Local context is therefore important when assessing the diet and functional role of herbivorous fishes. As climate change unfolds, shifts in the distribution, trophic behaviour and function of species are expected, making the study of trophic plasticity more important.

Feeding habits of herbivorous fishes play an important role in shaping the form and function of coastal marine ecosystems. Rabbitfishes (Siganidae) are important consumers of macroalgae on Indo-West Pacific coral reefs. However, it is unclear how their diet varies among and within species at biogeographical scales, casting doubt on their precise functional roles across different regions. The present study assessed the inter- and intra-specific diet variation of four rabbitfishes (Siganus trispilos, Siganus corallinus, Siganus virgatus and Siganus doliatus) factored by morphological relatedness among populations from Ningaloo Reef (western Australia), the Great Barrier Reef (GBR, eastern Australia) and the Yaeyama Islands (Okinawa Prefecture, Japan). Results showed that the region had a strong effect on diet, effectively reducing the expected effect of morphologic similitude. While intra-specific differences were only significant when populations inhabited different regions; interspecific differences were not as predicted, with different morphotypes having similar diets when populations inhabited the same regions. Rabbitfishes consumed more corticated and filamentous macroalgae on the GBR, more foliose and membranous macroalgae at the Yaeyama Islands, and more leathery macroalgae at Ningaloo Reef. The findings indicate that rabbitfishes have high diet plasticity, and hence their functional role as mediators of competition between macroalgae and corals can change across biogeographic regions. Local context is therefore important when assessing the diet and functional role of herbivorous fishes. As climate change unfolds, shifts in the distribution, trophic behaviour and function of species are expected, making the study of trophic plasticity more important.Feeding habits of herbivorous fishes play an important role in shaping the form and function of coastal marine ecosystems. Rabbitfishes (Siganidae) are important consumers of macroalgae on Indo-West Pacific coral reefs. However, it is unclear how their diet varies among and within species at biogeographical scales, casting doubt on their precise functional roles across different regions. The present study assessed the inter- and intra-specific diet variation of four rabbitfishes (Siganus trispilos, Siganus corallinus, Siganus virgatus and Siganus doliatus) factored by morphological relatedness among populations from Ningaloo Reef (western Australia), the Great Barrier Reef (GBR, eastern Australia) and the Yaeyama Islands (Okinawa Prefecture, Japan). Results showed that the region had a strong effect on diet, effectively reducing the expected effect of morphologic similitude. While intra-specific differences were only significant when populations inhabited different regions; interspecific differences were not as predicted, with different morphotypes having similar diets when populations inhabited the same regions. Rabbitfishes consumed more corticated and filamentous macroalgae on the GBR, more foliose and membranous macroalgae at the Yaeyama Islands, and more leathery macroalgae at Ningaloo Reef. The findings indicate that rabbitfishes have high diet plasticity, and hence their functional role as mediators of competition between macroalgae and corals can change across biogeographic regions. Local context is therefore important when assessing the diet and functional role of herbivorous fishes. As climate change unfolds, shifts in the distribution, trophic behaviour and function of species are expected, making the study of trophic plasticity more important.

Global warming is modifying the phenology, life-history traits and biogeography of species around the world. Evidence of these effects have increased over recent decades; however, we still have a poor understanding of the possible outcomes of their interplay across global climatic gradients, hindering our ability to accurately predict the consequences of climate change in populations and ecosystems.

We examined the effect that changes in biogeography can have on the life-history traits of two of the most successful range-extending fish species in the world: the tropical rabbitfishes Siganus fuscescens and Siganus rivulatus. Both species have established abundant populations at higher latitudes in the northern and southern hemispheres and have been identified as important ecological engineers with the potential to alter the community structure of seaweed forests (Laminariales and Fucales) in temperate regions.

Life-history trait information from across their global distribution was compiled from the published literature and meta-analyses were conducted to assess changes in (i) the onset and duration of reproductive periods, (ii) size at maturity, (iii) fecundity, (iv) growth rates, (v) maximum body sizes and (vi) longevity in populations at the leading edge of range expansion in relation to sea surface temperature and primary productivity (a common proxy for nutritional resource levels).

Populations at highest latitudes had shortened their reproductive periods and reduced growth rates, taking longer to reach sexual maturity and maximum sizes, but compensated this with higher fecundity per length class and longer lifespans than populations in warmer environments. Low primary productivity and temperature in the Mediterranean Sea resulted in lower growth rates and body sizes for S. rivulatus, but also lower length at maturity, increasing life-time reproductive output.

The results suggest that plasticity in the phenology and life-history traits of range-expanding species would be important to enhance their fitness in high latitude environments, facilitating their persistence and possible further poleward expansions. Quantifying the magnitude and direction of these responses can improve our understanding and ability to forecast species redistributions and its repercussions in the functioning of temperate ecosystems.

Extreme climatic events can reshape the functional structure of ecological communities, potentially altering ecological interactions and ecosystem functioning. While these shifts have been widely documented, evidence of their persistence and potential flow-on effects on ecosystem structure following relaxation of extreme events remains limited. Here, we investigate changes in the functional trait structure - encompassing dimensions of resource use, thermal affinity, and body size - of herbivorous fishes in a temperate reef system that experienced an extreme marine heatwave (MHW) and subsequent return to cool conditions. We quantify how changes in the trait structure modified the nature and intensity of herbivory-related functions (macroalgae, turf, and sediment removal), and explored the potential flow-on effects on the recovery dynamics of macroalgal foundation species. The trait structure of the herbivorous fish assemblage shifted as a result of the MHW, from dominance of cool-water browsing species to increased evenness in the distribution of abundance among temperate and tropical guilds supporting novel herbivory roles (i.e. scraping, cropping, and sediment sucking). Despite the abundance of tropical herbivorous fishes and intensity of herbivory-related functions declined following a period of cooling after the MHW, the underlying trait structure displayed limited recovery. Concomitantly, algal assemblages displayed a lack of recovery of the formerly dominant foundational species, the kelp Ecklonia radiata, transitioning to an alternative state dominated by turf and Sargassum spp. Our study demonstrates a legacy effect of an extreme MHW and exemplified the value of monitoring phenotypic (trait mediated) changes in the nature of core ecosystem processes to predict and adapt to the future configurations of changing reef ecosystems.

Temperate reefs are increasingly affected by the direct and indirect effects of climate change. At many of their warm range edges, cool-water kelps are decreasing, while seaweeds with warm-water affinities are increasing. These habitat-forming species provide different ecological functions, and shifts to warm-affinity seaweeds are expected to modify the structure of associated communities. Predicting the nature of such shifts at the ecosystem level is, however, challenging, as they often occur gradually over large geographical areas. Here, we take advantage of a climatic transition zone, where cool-affinity (kelp) and warm-affinity (Sargassum) seaweed forests occur adjacently under similar environmental conditions, to test whether these seaweed habitats support different associated seaweed, invertebrate, coral, and fish assemblages. We found clear differences in associated seaweed assemblages between habitats characterized by kelp and Sargassum abundance, with kelp having higher biomass and seaweed diversity and more cool-affinity species than Sargassum habitats. The multivariate invertebrate and fish assemblages were not different between habitats, despite a higher diversity of fish species in the Sargassum habitat. No pattern in temperature affinity of the invertebrate or fish assemblages in each habitat was found, and few fish species were exclusive to one habitat or the other. These findings suggest that, as ocean warming continues to replace kelps with Sargassum, the abundance and diversity of associated seaweeds could decrease, whereas fish could increase. Nevertheless, the more tropicalized seaweed habitats may provide a degree of functional redundancy to associated fauna in temperate seaweed habitats.

1. Global warming is facilitating the range expansion of tropical herbivores, causing a tropicalization of temperate marine ecosystems, where tropical herbivores can suppress habitat-forming macrophytes, supporting the resilience of canopy-free ecosystem states. However, currently we lack a thorough understanding of the mechanisms that, on one hand, support the persistence of tropical herbivores and on the other support the recovery of temperate foundation species in tropicalized ecosystems, a required knowledge to predict potential regime shifts and reversals to the baseline state of the ecosystem.

2. This study tested processes behind the persistence of the tropicalization of temperate reefs which experienced a complete loss of their kelp forests and an influx of tropical herbivores following a marine heatwave in 2011. For this, we assessed the feedback mechanisms that maintain turf-dominated states (recruitment of tropical herbivores, browsing and grazing rates and turf cover) and those that resist it (kelp recruitment, survival and reproductiveness).

3. We found that the reefs remained tropicalized with high abundances of turf and tropical herbivores after 9 years from the regime shift. The rabbitfish Siganus fuscescens and the chub Kyphosus bigibbus were the most important herbivores whose persistence was supported by the adjacent reef lagoon, where seagrass meadows and the backreef habitats hosted juveniles of both species, particularly rabbitfish. Tropical herbivores exerted a strong top–down control on turf seaweed and kelp during herbivory assays, rapidly consuming kelp individuals in open areas. However, in topographical refuges in the reefs, herbivory was low and kelp individuals survived, with some having reproductive tissue.

4. Synthesis. Our findings incorporate the importance of nursery grounds for tropical herbivores and herbivory refugia for kelp individuals into the tropicalization model, where the former increases the resilience of canopy-free states and the latter might facilitate recovering kelp populations. The restoration of abundant warm-resistant kelp populations in shelters could provide local sources of propagules to recolonize open spaces; however, our results suggest that the reduction of herbivory and the provision of turf-free substratum would be necessary to boost the recovery of kelp forests.

Temperate reefs are being tropicalized worldwide. In temperate Western Australia, a marine heatwave led to a regime shift from kelp (Ecklonia radiata) dominated to canopy-free reefs, together with an increase in tropical herbivorous fishes that contribute to keeping low kelp abundances and even prevent kelp reestablishment in northern regions. However, whether tropical herbivorous fishes prefer kelps over other seaweeds and/or whether this preference changes with latitude remains untested. Multiple-choice experiments (young kelp vs. other seaweeds) with tropical, subtropical and temperate herbivorous fishes show shifting species-specific preferences and fish-to-fish interference shifting with latitude (assays replicated in two regions four degrees of latitude apart). Against expectations, only the temperate Kyphosus sydneyanus preferred kelp over other seaweeds, but only in the lower latitude region. Siganus fuscescens, the most abundant tropical herbivore in both regions, preferred grazing on turf, suggesting that tropical fish might reduce kelp recruitment by consuming microscopic sporophytes in turf matrix.