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  • Biodiversity of intertidal food webs in response to warming across latitudes
    Publication . Gauzens, Benoit; Rall, Bjoern C.; Mendonca, Vanessa; Vinagre, Catarina; Brose, Ulrich
    Global warming will affect food-web structure and species persistence, and real world data is needed for better prediction. Combining species counts and temperature data from rock pools with dynamic modelling predicts biodiversity increases in arctic to temperate regions and declines in the tropics. Global warming threatens community stability and biodiversity around the globe. Knowledge of the mechanisms underlying the responses to rising temperatures depends heavily on generic food-web models that do not account for changes in network structure along latitudes and temperature gradients. Using 124 marine rock-pool food webs sampled across four continents, we show that despite substantial variation in ambient temperature (mean 11.5-28.4 degrees C), similar empirical food-web and body-mass structures emerge. We have used dynamic modelling to test whether communities from warmer regions are more sensitive to warming and found a general hump-shaped relationship between simulated biodiversity and temperature (gradient from 0-50 degrees C). This implies that an expected anthropogenic global warming of 4 degrees C should increase biodiversity in arctic to temperate regions while biodiversity in tropical regions should decrease. Interestingly, simulations of synthetic networks did not yield similar results, which stresses the importance of considering the specificities of natural food webs for predicting community responses to environmental changes.
  • Different sensitivity to heatwaves across the life cycle of fish reflects phenotypic adaptation to environmental niche
    Publication . Madeira, Diana; Madeira, Carolina; Costa, Pedro M.; Vinagre, Catarina; Portner, Hans-Otto; Diniz, Mario S.
    Predicting responses of marine organisms to global change requires eco-physiological assessments across the complex life cycles of species. Here, we experimentally tested the vulnerability of a demersal temperate fish (Sparus aurata) to long-lasting heatwaves, on larval , juvenile and adult life-stages. Fish were exposed to simulated coastal (18 degrees C), estuarine (24 degrees C) summer temperatures, and heatwave conditions (30 degrees C) and their physiological responses were assessed based on cellular stress response biomarkers (heat shock protein 70 kDa, ubiquitin, antioxidant enzymes, lipid peroxidation) and phenotypic measures (histopathology, condition and mortality). Life-stage vulnerability can be ranked as larvae > adults > juveniles, based on mortality , tissue pathology and the capacity to employ cellular stress responses, reflecting the different environmental niches of each life stage. While larvae lacked acclimation capacity, which resulted in damage to tissues and elevated mortality, juveniles coped well with elevated temperature. the rapid induction of cytoprotective proteins maintained the integrity of vital organs in juveniles, suggesting adaptive phenotypic plasticity in coastal and estuarine waters. Adults displayed lower plasticity to heatwaves as they transition to deeper habitats for maturation, showing tissue damage in brain, liver and muscle. Life cycle closure of sea breams in coastal habitats will therefore be determined by larval and adult stages.
  • Differential effects of food restriction and warming in the two-spotted goby: impaired reproductive performance and stressed offspring
    Publication . Lopes, Ana F.; Murdoch, Robyn; Martins-Cardoso, Sara; Madeira, Carolina; Costa, Pedro M.; Félix, Ana S.; Oliveira, Rui F.; Bandarra, Narcisa M.; Vinagre, Catarina; Lopes, Ana R.; Gonçalves, Emanuel J.; Faria, Ana Margarida
    Climate change is a growing threat to marine organisms and ecosystems, and it is already modifying ocean properties by, for example, increasing temperature and decreasing pH. Increasing water temperature may also lead to an impairment of primary productivity and an overall depletion of available zooplankton. Understanding how the crossover between warming and zooplankton availability impacts fish populations has paramount implications for conservation and mitigation strategies. Through a cross factorial design to test the effects of ocean temperature and food availability in a temperate marine teleost, Pomatochistus flavescens, we showed that hindered feeding impacted sheltering and avoidance behaviour. Also, low food availability impaired fish reproduction, particularly male reproduction, as the expression of cyp11b1, a gene with a pivotal role in the synthesis of the most important fish androgen, 11-ketotestosterone, was significantly reduced under a low food regime. In contrast, temperature alone did not affect reproductive success, but offspring showed increased saturated fatty acid content (embryos) and increased lipid peroxidation (larvae). Altogether, food availability had a stronger effect on fitness, showing that coping with elevated temperatures, an ability that may be expected in shallow-water fish, can be indirectly impacted, or even overwhelmed, by the effects of ocean warming on primary productivity and downstream ecological processes.
  • Conserved fatty acid profiles and lipid metabolic pathways in a tropical reef fish exposed to ocean warming – An adaptation mechanism of tolerant species?
    Publication . Madeira, Carolina; Madeira, Diana; Ladd, Nemiah; Schubert, Carsten J.; Diniz, Mário S.; Vinagre, Catarina; Leal, Miguel C.
    Climate warming is causing rapid spatial expansion of ocean warm pools from equatorial latitudes towards the subtropics. Sedentary coral reef inhabitants in affected areas will thus be trapped in high temperature regimes, which may become the "new normal". In this study, we used clownfish Amphiprion ocellaris as model organism to study reef fish mechanisms of thermal adaptation and determine how high temperature affects multiple lipid aspects that influence physiology and thermal tolerance. We exposed juvenile fish to two different experimental conditions, implemented over 28 days: average tropical water temperatures (26 °C, control) or average warm pool temperatures (30 °C). We then performed several analyses on fish muscle and liver tissues: i) total lipid content (%), ii) lipid peroxides, iii) fatty acid profiles, iv) lipid metabolic pathways, and v) weight as body condition metric. Results showed that lipid storage capacity in A. ocellaris was not affected by elevated temperature, even in the presence of lipid peroxides in both tissues assessed. Additionally, fatty acid profiles were unresponsive to elevated temperature, and lipid metabolic networks were consequently well conserved. Consistent with these results, we did not observe changes in fish weight at elevated temperature. There were, however, differences in fatty acid profiles between tissue types and over time. Liver showed enhanced α-linolenic and linoleic acid metabolism, which is an important pathway in stress response signaling and modulation on environmental changes. Temporal oscillations in fatty acid profiles are most likely related to intrinsic factors such as growth, which leads to the mobilization of energetic reserves between different tissues throughout time according to organism needs. Based on these results, we propose that the stability of fatty acid profiles and lipid metabolic pathways may be an important thermal adaptation feature of fish exposed to warming environments.
  • Changing webs—Variation of complex networks over a tidal cycle in an intertidal rocky reef
    Publication . Vinagre, Catarina; Mendonça, Vanessa
    Incorporating temporal variation in models is one of the most important challenges in food web research. One of the environments where time causes profound changes is the intertidal zone, where the immersion-emersion cycle drastically changes the abiotic and biotic conditions. Intertidal rocky shores have been intensively studied, however the variation in the complex food web network that occurs during a tidal cycle remains undescribed. Highly resolved food web networks were assembled for an intertidal reef depicting the food web during low and high tide, and with and without tide pools. It was concluded that high tide adds new species to the web, but it does not add complexity since network connectance was not changed. This occurs because incoming species are mostly highly generalist fish, which add many new links to the web. Tide pools, however, add not only diversity but also complexity. Webs were dominated by intermediate species, with the proportion of top consumers fluctuating throughout the tidal cycle, being lowest during low tide and highest at high tide, due to the incoming larger vertebrate predators. Consumer taxa outnumbered resource taxa, except at low tide when pools are present. Mean trophic level was lowest at low tide (2.3) and highest at high tide with pools (2.6). Omnivory was high and showed little change. "Chain", the number of links connecting top to basal species, was stable but low. This implies that disturbance can rapidly travel bottom-up or top-down through predator-prey links. The increased connectance given by the addition of tide pools likely increases robustness to disturbances, an important feature in coastal areas so often impacted by human action.
  • Patterns of rock pool molluscs in differing shore exposures
    Publication . Gonçalves, Inês; Vinagre, Catarina; Silva, Ana
    Rock pools are understudied systems of extreme importance due to their proven vulnerability to climate change. Rock pool molluscs play essential ecological roles therein, directly by acting both as prey and predator and, indirectly by influencing the macroalgal canopy/vegetation topography via grazing. However, the environmental factors driving their rock pool occupation remain largely unknown. Our study is one of the few to focus on community patterns in rock pool molluscs, particularly at a large scale between shores of differing exposure to wave action, being the first focused assessment of rock pool molluscs in Portugal. Overall, 32 intertidal rock pools on four rocky shores were studied during the summer spring tide of 2015. We used multivariate analysis to evaluate the potential impact of sheltered versus exposed wave action, physical pool structure (length, width, and depth), and relationships within the pool community on the abundance and diversity of molluscs. Wave exposure significantly influenced mollusc abundance and diversity. The majority of the 37 different taxa identified were grazing gastropods (62.2%), followed by bivalves (27.0%) and chitons (10.8%). We suggest that mollusc taxa may have preferences for particular rock pool habitats depending on the type of algae present rather than pool size. We also suggest that species-specific mollusc presence in rock pools can be related to their shell size, aperture, and foot size due to corresponding variation in musculature needed to hold the snail to the substrate in hydrodynamic conditions. Further investigation would benefit from disentangling the potential role of algal pool coverage as a refuge for molluscs.
  • Consistent predator-prey biomass scaling in complex food webs
    Publication . Perkins, Daniel M.; Hatton, Ian A.; Gauzens, Benoit; Barnes, Andrew D.; Ott, David; Rosenbaum, Benjamin; Vinagre, Catarina; Brose, Ulrich
    The ratio of predator-to-prey biomass is a key element in food webs. Here, the authors report a unified analysis of predator-prey biomass scaling in complex food webs, finding general patterns of sub-linear scaling across ecosystems and levels of organization. The ratio of predator-to-prey biomass is a key element of trophic structure that is typically investigated from a food chain perspective, ignoring channels of energy transfer (e.g. omnivory) that may govern community structure. Here, we address this shortcoming by characterising the biomass structure of 141 freshwater, marine and terrestrial food webs, spanning a broad gradient in community biomass. We test whether sub-linear scaling between predator and prey biomass (a potential signal of density-dependent processes) emerges within ecosystem types and across levels of biological organisation. We find a consistent, sub-linear scaling pattern whereby predator biomass scales with the total biomass of their prey with a near 3/4-power exponent within food webs - i.e. more prey biomass supports proportionally less predator biomass. Across food webs, a similar sub-linear scaling pattern emerges between total predator biomass and the combined biomass of all prey within a food web. These general patterns in trophic structure are compatible with a systematic form of density dependence that holds among complex feeding interactions across levels of organization, irrespective of ecosystem type.
  • Thermal plasticity over a marine-estuarine ecocline can buffer a tropical fish from warming
    Publication . de Souza, Joice Silva; Vinagre, Catarina; dos Santos, Luciano Neves
    Intraspecific variation in thermal tolerance can favor species persistence in a warmer ocean, but is often over-looked in fine-scale studies. Nonetheless, local drivers (e.g. salinity) interact with temperature to shape species' thermal response. Here, we acclimated juveniles of Brazilian silversides Atherinella brasiliensis captured at the limits of a marine-estuarine ecocline under reciprocal-cross conditions, to test for phenotypic plasticity in heat tolerance. We also tested whether silversides acclimated to temperatures predicted for 2100 (+3-4.5 degrees C). Fish in warm-brackish waters showed higher CTMax (Critical Thermal Maximum) than those in cold-marine conditions, regardless of their origin. Silversides' CTMax reached up to 40.6 degrees C, but it did not increase after exposure to temperatures predicted for 2100. Lack of acclimation response suggests that silversides heat tolerance has reached a "ceiling", despite thermal plasticity. Our findings show that fine-scale environmental heterogeneity can promote phenotypic plasticity for tropical species, reducing the risk of short-term extirpation.
  • Unknown facts of the biology of Polybius henslowii - Effect of gender on claw morphology and diet
    Publication . Cereja, Rui; Vinagre, Catarina; Silva, Ana
    Polybius henslowii is known for both its unusual swimming behaviour and for forming large shoals during its pelagic phase. Although being a common species, many aspects of its biology remain unknown. In this work, P. henslowif s sexual dimorphism was examined in both dietary composition and morphologies of carapace and claw. Males were generally larger than females both on carapace and claw sizes. Claw morphology differed between males and females. Diet was similar between genders. Hence, we suggest that the sexual dimorphism in claw morphology results from gender-specific behaviours instead of diet. The most common dietary items were sand (51.2%), squid (34.1%) and crustaceans (26.8%). The same items were also the most important in volume, but with squids being more important than sand. The diet composition of P. henslowii was consistent with previous studies but also presenting sediment as an important item.
  • Priority effects, environmental filtering and neutral coexistence explain large- to small-scale distribution of invasive sun corals in the SW Atlantic
    Publication . Barbosa, A. C.C.; Vinagre, Catarina; Kitahara, MV; Flores, A. A. V.
    Two sun coral species, Tubastraea tagusensis and T. coccinea, have successfully colonized reef habitats along the Southwest Atlantic. However, their invasive biology has been largely addressed without considering species-specific distribution patterns. Here, we assessed the distribution and abundance of Tubastraea spp. at vertical rocky reef sites within a number of islands along 120 km of coastline off the northern coast of Sao Paulo State, Brazil, to (1) investigate possible mechanisms underlying the invasion dynamics in the region, (2) test species-specific distributions according to a key environmental filter (depth), and (3) examine within-patch patterns to assess whether competition, niche-based or neutral processes are best candidates to modulate local species coexistence. Sun corals were found in the great majority of the studied locations, and the probability of finding them at any given reef site was estimated to be 0.54. There was substantial species segregation across locations, consistent with primary priority effects. Within locations, results suggest environmental filtering, with T. coccinea apparently advantaged in more hydrodynamic environments just below the surf zone. At sun coral patches with extensive co-occurrence of T. tagusensis and T. coccinea, the presence of each species can be, remarkably, modeled as an independent event, suggesting neutral coexistence. The spread of sun corals is an ongoing and increasingly invasive process that may be explained by the enemy-release hypothesis and the lack of negative interactions between Tubastraea species. The stochastic nature of small-scale distributions sets an additional challenge to predict (and thus control) sun coral invasion.