Persistent thermally driven shift in the functional trait structure of herbivorous fishes: Evidence of top-down control on the rebound potential of temperate seaweed forests?

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.

Maximization of fitness by phenological and phenotypic plasticity in range expanding rabbitfishes (Siganidae).

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.

Overwintering tropical herbivores accelerate detritus production on temperate reefs.

The tropicalization of temperate marine ecosystems can lead to increased herbivory rates, reducing the standing stock of seaweeds and potentially causing increases in detritus production. However, long-term studies analysing these processes associated with the persistence of tropical herbivores in temperate reefs are lacking. We assessed the seasonal variation in abundances, macrophyte consumption, feeding modes and defecation rates of the range-extending tropical rabbitfish Siganus fuscescens and the temperate silver drummer Kyphosus sydneyanus and herring cale Olisthops cyanomelas on tropicalized reefs of Western Australia. Rabbitfish overwintered in temperate reefs, consumed more kelp and other macrophytes in all feeding modes, and defecated more during both summer and winter than the temperate herbivores. Herbivory and defecation increased with rabbitfish abundance, but this was dependent on temperature, with higher rates attained by big schools during summer and lower rates in winter. Still, rabbitfish surpassed temperate herbivores, leading to a fivefold acceleration in the transformation of macrophyte standing stock to detritus, a function usually attributed to sea urchins in kelp forests. Our results suggest that further warming and tropicalization will not only increase primary consumption and affect the habitat structure of temperate reefs but also increase detritus production, with the potential to modify energy pathways.

Biogeographical diet variation within and between the rabbitfishes Siganus corallinus, Siganus doliatus, Siganus trispilos and Siganus virgatus.

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.

Intergrading reef communities across discrete seaweed habitats in a temperate-tropical transition zone: Lessons for species reshuffling in a warming ocean.

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.

Feeding preferences of range-shifting and native herbivorous fishes in temperate ecosystems.

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.

Remote underwater video reveals higher fish diversity and abundance in seagrass meadows, and habitat differences in trophic interactions.

Seagrass meadows play a key ecological role as nursery and feeding grounds for multiple fish species. Underwater Visual Census (UVC) has been historically used as the non-extractive method to characterize seagrass fish communities, however, less intrusive methodologies such as Remote Underwater Video (RUV) are gaining interest and could be particularly useful for seagrass habitats, where juvenile fish camouflage among the vegetation and could easily hide or flee from divers. Here we compared the performance of UVC and RUV methodologies in assessing the fish communities of two seagrass meadows with low and high canopy density. We found that RUV detected more species and fish individuals than UVC, particularly on the habitat with higher seagrass density, which sheltered more juveniles, especially herbivorous, and adult piscivorous of commercial importance, evidencing significant differences in energy flow from macrophytes to predators between seagrass habitats, and also differences in the ecosystem services they can provide. Considering the ongoing worldwide degradation of seagrass ecosystems, our results strongly suggest that fish surveys using RUV in ecologic and fisheries programs would render more accurate information and would be more adequate to inform the conservation planning of seagrass meadows around the world.

Ordinary kriging vs inverse distance weighting: spatial interpolation of the sessile community of Madagascar reef, Gulf of Mexico.

Information about the distribution and abundance of the habitat-forming sessile organisms in marine ecosystems is of great importance for conservation and natural resource managers. Spatial interpolation methodologies can be useful to generate this information from in situ sampling points, especially in circumstances where remote sensing methodologies cannot be applied due to small-scale spatial variability of the natural communities and low light penetration in the water column. Interpolation methods are widely used in environmental sciences; however, published studies using these methodologies in coral reef science are scarce. We compared the accuracy of the two most commonly used interpolation methods in all disciplines, inverse distance weighting (IDW) and ordinary kriging (OK), to predict the distribution and abundance of hard corals, octocorals, macroalgae, sponges and zoantharians and identify hotspots of these habitat-forming organisms using data sampled at three different spatial scales (5, 10 and 20 m) in Madagascar reef, Gulf of Mexico. The deeper sandy environments of the leeward and windward regions of Madagascar reef were dominated by macroalgae and seconded by octocorals. However, the shallow rocky environments of the reef crest had the highest richness of habitat-forming groups of organisms; here, we registered high abundances of octocorals and macroalgae, with sponges, Millepora alcicornis and zoantharians dominating in some patches, creating high levels of habitat heterogeneity. IDW and OK generated similar maps of distribution for all the taxa; however, cross-validation tests showed that IDW outperformed OK in the prediction of their abundances. When the sampling distance was at 20 m, both interpolation techniques performed poorly, but as the sampling was done at shorter distances prediction accuracies increased, especially for IDW. OK had higher mean prediction errors and failed to correctly interpolate the highest abundance values measured in situ, except for macroalgae, whereas IDW had lower mean prediction errors and high correlations between predicted and measured values in all cases when sampling was every 5 m. The accurate spatial interpolations created using IDW allowed us to see the spatial variability of each taxa at a biological and spatial resolution that remote sensing would not have been able to produce. Our study sets the basis for further research projects and conservation management in Madagascar reef and encourages similar studies in the region and other parts of the world where remote sensing technologies are not suitable for use.

Tropicalization strengthens consumer pressure on habitat-forming seaweeds.

Ocean warming is driving species poleward, causing a 'tropicalization' of temperate ecosystems around the world. Increasing abundances of tropical herbivores on temperate reefs could accelerate declines in habitat-forming seaweeds with devastating consequences for these important marine ecosystems. Here we document an expansion of rabbitfish (Siganus fuscescens), a tropical herbivore, on temperate reefs in Western Australia following a marine heatwave and demonstrate their impact on local kelp forests (Ecklonia radiata). Before the heatwave there were no rabbitfish and low rates of kelp herbivory but after the heatwave rabbitfish were common at most reefs and consumption of kelp was high. Herbivory increased 30-fold and kelp abundance decreased by 70% at reefs where rabbitfish had established. In contrast, where rabbitfish were absent, kelp abundance and herbivory did not change. Video-analysis confirmed that rabbitfish were the main consumers of kelp, followed by silver drummers (Kyphosus sydneyanus), a temperate herbivore. These results represent a likely indirect effect of the heatwave beyond its acute impacts, and they provide evidence that range-shifting tropical herbivores can contribute to declines in habitat-forming seaweeds within a few years of their establishment.

Checklist of fishes from madagascar reef, campeche bank, méxico.

This study presents the first list of fish species from Madagascar Reef, Campeche Bank, Gulf of México. Field surveys and literature review identified 54 species belonging to 8 orders, 30 families and 43 genera, comprising both conspicuous and cryptic fishes. Species richness was lower at this reef site compared to reefs in the Mexican Caribbean, Veracruz or Tuxpan, but was similar to other reefs in the same region. Species composition was a mixture of species present in all the reef systems of the Mexican Atlantic. Hypoplectrusecosur was recorded here for the first time in the Gulf of Mexico, Mycteropercamicrolepis, Equetuslanceolatus and Chaetodipterusfaber were new records for the reefs of the Campeche Bank, Elacatinusxanthiprora was recorded for the second time in Mexico and expanded its known distribution westwards from Alacranes Reef and Sanopusreticulatus, endemic of the Yucatan state, was recorded here for the first time on a reef.