Environmental Extremes Are Associated with Dietary Patterns in Arabian Gulf Reef Fishes

Abstract

Climate change is affecting the trophic ecology of reef fishes through changes in reef-associated food availability and fish feeding behavior. The southern Arabian Gulf is a thermally extreme environment, providing an opportunity to study fish diets on reefs with summer temperatures representative of next-century conditions elsewhere. Using 18S metagenomic analyses of stomach contents, we provide the first description of the dietary composition of three abundant reef fishes (Pomacanthus maculosus, Pomacentrus aquilus, and Pomacentrus trichrourus) from the thermally extreme southern Arabian Gulf, with five sampling periods across 1 year used to assess seasonal variation in diet. In total, 146 stomach content samples were sequenced, resulting in 9.6 million filtered reads that aligned to 17 classes in 14 phyla. Corals (Cnidaria, Anthozoa) dominated stomach contents of all three fishes (overall mean: 74.6, 40.6, and 21.2% of stomach reads, respectively), suggesting coral consumption to be characteristic of reef fish diet in the region. Sanger sequencing validated the presence of corals in the stomach contents and identified two common genera in the region, Porites and Platygyra, as part of the diet. Other common phyla included sponges and annelid worms (P. maculosus: 14.9%, 4.1%; P. aquilus: 5.9%, 16.7%; P. trichrourus: 8.2%, 14.7%, respectively), with the remainder comprised of 11 other phyla. Algae were virtually absent in diets of all three species. The P. maculosus diet was consistently coral/sponge dominated across the year, but there was substantial seasonal variation in the damselfishes, with diets dominated by coral in the hottest month (August; P. aquilus: 89.4%, P. trichrourus: 51.5%) but broadest in spring (March, May) when corals became less common (<19.8% each) and bivalves, free living ascidians, and various arthropods increased; parasitic cestodes were also abundant in damselfish stomachs in spring (mean: >16.4%). These results suggest that these fishes have developed a feeding ecology responsive to the fluctuating and extreme environmental conditions of their region. These results broaden our understanding of the diets of these three species and document the nature, complexity and temporal dynamics of reef fish diets in the most thermally extreme coral reef environment on earth.

The influence of thermal extremes on coral reef fish behaviour in the Persian Gulf

“…Although increasing variance in global SSTs may directly impact coral reef fish community biodiversity (Pratchett et al 2015; Pecl et al 2017; Hughes et al 2018), coral reef fish populations might be able to mitigate the effect of rapidly changing environments through behavioural plasticity (Nagelkerken and Munday 2016; Scott et al 2017; Shraim et al 2017; Chase et al 2018). We examined the impact of seasonal changes in biotic and abiotic conditions on distance from refugia, activity and feeding ecology of the pale-tail damselfish P. trichrourus within the southern Gulf.…”

“…Many studies on temperate fishes have highlighted the ability to compensate energetic and growth losses during periods of adverse temperatures or food scarcity through increased feeding rate and feeding activity when conditions become favourable again (Sevgili et al 2013; Armstrong and Bond 2013; Furey et al 2016; Peng et al 2017). For P. trichrourus such periods of recovery, where it can access highly nutritious food resources (Shraim et al 2017) under optimal environmental temperatures (Kaschner et al 2016), may be vital for mitigating energy loss during winter and summer, and hence ultimately permit the persistence of abundant populations within the southern Gulf throughout the year.…”

“…reduced distance from refugia) and feeding rate (Dill & Fraser 1984; Beck et al 2016; Catano et al 2016), potentially leading to the shift to mixed planktonic and benthic diet observed in summer, when P. trichrourus may have to rely more on safer benthic food resources (i.e. live corals), despite the loss of nutritional value (Shraim et al 2017). On the contrary, we did not observe any correlation between changes in primary productivity and changes in feeding activity, suggesting that shifts in diet may not be related to primary productivity (measured as chlorophyll-a concentration) (Rueda et al 2015; Zhou et al 2016) but the result of temperature-related differences in food preference (Shraim et al 2017).…”

“…live corals), despite the loss of nutritional value (Shraim et al 2017). On the contrary, we did not observe any correlation between changes in primary productivity and changes in feeding activity, suggesting that shifts in diet may not be related to primary productivity (measured as chlorophyll-a concentration) (Rueda et al 2015; Zhou et al 2016) but the result of temperature-related differences in food preference (Shraim et al 2017). Ultimately, we would need manipulative experiments to confirm the potential for predators or other drivers to produce similar behavioural changes to those seen in our temperature manipulation.…”

“…The pale-tail damselfish is a small omnivorous damselfish common in southern Gulf coral communities, often living in association with a single ‘home’ coral head (Allen 1991; Shraim et al 2017). Within the Gulf this species shows high abundance, a benthic life style with diurnal behaviour, a strong association with the reef, and high territoriality to a small area [territory size of 0.5 to 1.5 m 2 ]).…”