Marine protected areas promote stability of reef fish communities under climate warming.

Protection from direct human impacts can safeguard marine life, yet ocean warming crosses marine protected area boundaries. Here, we test whether protection offers resilience to marine heatwaves from local to network scales. We examine 71,269 timeseries of population abundances for 2269 reef fish species surveyed in 357 protected versus 747 open sites worldwide. We quantify the stability of reef fish abundance from populations to metacommunities, considering responses of species and functional diversity including thermal affinity of different trophic groups. Overall, protection mitigates adverse effects of marine heatwaves on fish abundance, community stability, asynchronous fluctuations and functional richness. We find that local stability is positively related to distance from centers of high human density only in protected areas. We provide evidence that networks of protected areas have persistent reef fish communities in warming oceans by maintaining large populations and promoting stability at different levels of biological organization.

Dense cold-water coral garden of Paragorgia johnsoni suggests the importance of the Mid-Atlantic Ridge for deep-sea biodiversity.

Mid-ocean ridges generate a myriad of physical oceanographic processes that favor the supply of food and nutrients to suspension- and filter-feeding organisms, such as cold-water corals and deep-sea sponges. However, the pioneering work conducted along the Mid-Atlantic Ridge failed to report the presence of large and dense living coral reefs, coral gardens, or sponge aggregations. Here, we describe the densest, near-natural, and novel octocoral garden composed of large red and white colonies of Paragorgia johnsoni Gray, 1862 discovered at 545-595 m depth on the slopes of the Mid-Atlantic Ridge, in the Azores region. This newly discovered octocoral garden is a good candidate for protection since it fits many of the FAO criteria that define what constitutes a Vulnerable Marine Ecosystem. The observations described here corroborate the existence of a close relationship between the octocoral structure and the ambient currents on ridge-like topographies, providing new insights into the functioning of mid-ocean ridges' ecosystems. The ubiquitous presence of biogenic and geological topographies associated with mid-ocean ridges, which could act as climate refugia, suggests their global importance for deep-sea biodiversity. A better understanding of the processes involved is, therefore, required. Our observations may inspire future deep-sea research initiatives to narrow existing knowledge gaps of biophysical connections with benthic fauna at small spatial scales along mid-ocean ridges.

The MPA Guide: A framework to achieve global goals for the ocean.

Marine Protected Areas (MPAs) are conservation tools intended to protect biodiversity, promote healthy and resilient marine ecosystems, and provide societal benefits. Despite codification of MPAs in international agreements, MPA effectiveness is currently undermined by confusion about the many MPA types and consequent wildly differing outcomes. We present a clarifying science-driven framework­The MPA Guide­to aid design and evaluation. The guide categorizes MPAs by stage of establishment and level of protection, specifies the resulting direct and indirect outcomes for biodiversity and human well-being, and describes the key conditions necessary for positive outcomes. Use of this MPA Guide by scientists, managers, policy-makers, and communities can improve effective design, implementation, assessment, and tracking of existing and future MPAs to achieve conservation goals by using scientifically grounded practices.

Soft-bottom fishes and spatial protection: findings from a temperate marine protected area.

Numerous studies over the last decades have focused on marine protected areas (MPAs) and their effects on fish communities. However, there is a knowledge gap regarding how species that live associated with soft-substrates (e.g., sand, mud) respond to spatial protection. We analyzed abundance, biomass and total lengths of the soft-bottom fishes in a multiple-use MPA in the north-eastern Atlantic, the Luiz Saldanha Marine Park (Portugal), during and after the implementation of its management plan. Data were collected by experimental fishing in areas with three different levels of protection, during the implementation period and for three years after full implementation of the MPA. Univariate analysis detected significant biomass increases between the two periods. Fish assemblages were mainly structured by depth and substrate, followed by protection level. Community composition analyses revealed significant differences between protection levels and between the two periods. Species exhibited a broad variation in their response to protection, and we hypothesize that factors such as species habitat preferences, body size and late maturity might be underlying determinants. Overall, this study provides some evidence of protection effectiveness in soft-bottom fish communities, supported by the significant increase in biomass in the protected areas and the positive trends of some species.

Sand smelt ability to cope and recover from ocean's elevated CO2 levels.

Considered a major environmental concern, ocean acidification has induced a recent research boost into effects on marine biodiversity and possible ecological, physiological, and behavioural impacts. Although the majority of literature indicate negative effects of future acidification scenarios, most studies are conducted for just a few days or weeks, which may be insufficient to detect the capacity of an organism to adjust to environmental changes through phenotypic plasticity. Here, the effects and the capacity of sand smelt larvae Atherina presbyter to cope and recover (through a treatment combination strategy) from short (15 days) and long-term exposure (45 days) to increasing pCO2 levels (control: ~515 µatm, pH = 8.07; medium: ~940 µatm, pH = 7.84; high: ~1500 µatm, pH = 7.66) were measured, addressing larval development traits, behavioural lateralization, and biochemical biomarkers related with oxidative stress and damage, and energy metabolism and reserves. Although behavioural lateralization was not affected by high pCO2 exposure, morphometric changes, energetic costs, and oxidative stress damage were impacted differently through different exposures periods. Generally, short-time exposures led to different responses to either medium or high pCO2 levels (e.g. development, cellular metabolism, or damage), while on the long-term the response patterns tend to become similar between them, with both acidification scenarios inducing DNA damage and tending to lower growth rates. Additionally, when organisms were transferred to lower acidified condition, they were not able to recover from the mentioned DNA damage impacts. Overall, results suggest that exposure to future ocean acidification scenarios can induce sublethal effects on early life-stages of fish, but effects are dependent on duration of exposure, and are likely not reversible. Furthermore, to improve our understanding on species sensitivity and adaptation strategies, results reinforce the need to use multiple biological endpoints when assessing the effects of ocean acidification on marine organisms.

Contrasts in the marine ecosystem of two Macaronesian islands: A comparison between the remote Selvagens Reserve and Madeira Island.

The islands of Madeira and Selvagens are less than 300 km apart but offer a clear contrast between a densely populated and highly developed island (Madeira), and a largely uninhabited and remote archipelago (Selvagens) within Macaronesia in the eastern Atlantic. The Madeira Archipelago has ~260,000 inhabitants and receives over six million visitor days annually. The Selvagens Islands Reserve is one of the oldest nature reserves in Portugal and comprises two islands and several islets, including the surrounding shelf to a depth of 200 m. Only reserve rangers and a small unit of the maritime police inhabit these islands. The benthic community around Selvagens was dominated by erect and turf algae, while the community at Madeira was comprised of crustose coralline and turf algae, sessile invertebrates, and sea urchin barrens. The sea urchin Diadema africanum was 65% more abundant at Madeira than at Selvagens. Total fish biomass was 3.2 times larger at Selvagens than at Madeira, and biomass of top predators was more than 10 times larger at Selvagens. Several commercially important species (e.g., groupers, jacks), which have been overfished throughout the region, were more common and of larger size at Selvagens than at Madeira. Important sea urchin predators (e.g., hogfishes, triggerfishes) were also in higher abundance at Selvagens compared to Madeira. The effects of fishing and other anthropogenic influences are evident around Madeira. This is in stark contrast to Selvagens, which harbors healthy benthic communities with diverse algal assemblages and high fish biomass, including an abundance of large commercially important species. The clear differences between these two island groups highlights the importance of expanding and strengthening the protection around Selvagens, which harbors one of the last intact marine ecosystems in the North Atlantic, and the need to increase management and protection around Madeira.

Cryptic effects of biological invasions: Reduction of the aggressive behaviour of a native fish under the influence of an "invasive" biomolecule.

The invasive green alga Caulerpa cylindracea has become an important component of the diet of the Mediterranean white seabream Diplodus sargus. As a consequence of this "exotic diet", the algal bisindolic alkaloid caulerpin accumulates in the fish tissues. Although the compound shows structural similarity to endogenous indolamines that modulate animal behaviour, the potential impact of caulerpin on fish behaviour still remains unexplored. In this report, behavioural experiments both on groups and on single fish responding towards a mirror were performed under different doses of dietary caulerpin. Differences between treated and control groups for each behaviour and for the overall aggressive pattern during the different experimental phases showed that the aggressiveness of D. sargus decreased with the administration of caulerpin. These results call the attention to a still unexplored potential ability of bioactive metabolites from marine invasive species, to alter the behaviour on native species, with putative negative effects on patterns of fish growth and population dynamics.

Painted Goby Larvae under High-CO2 Fail to Recognize Reef Sounds.

Atmospheric CO2 levels have been increasing at an unprecedented rate due to anthropogenic activity. Consequently, ocean pCO2 is increasing and pH decreasing, affecting marine life, including fish. For many coastal marine fishes, selection of the adult habitat occurs at the end of the pelagic larval phase. Fish larvae use a range of sensory cues, including sound, for locating settlement habitat. This study tested the effect of elevated CO2 on the ability of settlement-stage temperate fish to use auditory cues from adult coastal reef habitats. Wild late larval stages of painted goby (Pomatoschistus pictus) were exposed to control pCO2 (532 µatm, pH 8.06) and high pCO2 (1503 µatm, pH 7.66) conditions, likely to occur in nearshore regions subjected to upwelling events by the end of the century, and tested in an auditory choice chamber for their preference or avoidance to nighttime reef recordings. Fish reared in control pCO2 conditions discriminated reef soundscapes and were attracted by reef recordings. This behaviour changed in fish reared in the high CO2 conditions, with settlement-stage larvae strongly avoiding reef recordings. This study provides evidence that ocean acidification might affect the auditory responses of larval stages of temperate reef fish species, with potentially significant impacts on their survival.

High Interannual Variability in Connectivity and Genetic Pool of a Temperate Clingfish Matches Oceanographic Transport Predictions.

Adults of most marine benthic and demersal fish are site-attached, with the dispersal of their larval stages ensuring connectivity among populations. In this study we aimed to infer spatial and temporal variation in population connectivity and dispersal of a marine fish species, using genetic tools and comparing these with oceanographic transport. We focused on an intertidal rocky reef fish species, the shore clingfish Lepadogaster lepadogaster, along the southwest Iberian Peninsula, in 2011 and 2012. We predicted high levels of self-recruitment and distinct populations, due to short pelagic larval duration and because all its developmental stages have previously been found near adult habitats. Genetic analyses based on microsatellites countered our prediction and a biophysical dispersal model showed that oceanographic transport was a good explanation for the patterns observed. Adult sub-populations separated by up to 300 km of coastline displayed no genetic differentiation, revealing a single connected population with larvae potentially dispersing long distances over hundreds of km. Despite this, parentage analysis performed on recruits from one focal site within the Marine Park of Arrábida (Portugal), revealed self-recruitment levels of 2.5% and 7.7% in 2011 and 2012, respectively, suggesting that both long- and short-distance dispersal play an important role in the replenishment of these populations. Population differentiation and patterns of dispersal, which were highly variable between years, could be linked to the variability inherent in local oceanographic processes. Overall, our measures of connectivity based on genetic and oceanographic data highlight the relevance of long-distance dispersal in determining the degree of connectivity, even in species with short pelagic larval durations.

At odds with the group: changes in lateralization and escape performance reveal conformity and conflict in fish schools.

Many vertebrates are known to show behavioural lateralization, whereby they differentially use one side of their body or either of their bilateral organs or limbs. Behavioural lateralization often manifests in a turning bias in fishes, with some individuals showing a left bias and others a right bias. Such biases could be the source of considerable conflict in fish schools given that there may be considerable social pressure to conform to the group to maintain effective group evasion. Here, we show that predation pressure is a major determinant of the degree of lateralization, both in a relative and absolute sense, in yellow-and-blueback fusiliers (Caesio teres), a schooling fish common on coral reefs. Wild-caught fish showed a bias for right turning. When predation pressure was experimentally elevated or relaxed, the strength of lateralization changed. Higher predation pressure resulted in an increase in the strength of lateralization. Individuals that exhibited the same turning bias as the majority of individuals in their group had improved escape performance compared with individuals that were at odds with the group. Moreover, individuals that were right-biased had improved escape performance, compared with left-biased ones. Plasticity in lateralization might be an important evolutionary consequence of the way gregarious species respond to predators owing to the probable costs associated with this behaviour.

Effects of ocean acidification on the swimming ability, development and biochemical responses of sand smelt larvae.

Ocean acidification, recognized as a major threat to marine ecosystems, has developed into one of the fastest growing fields of research in marine sciences. Several studies on fish larval stages point to abnormal behaviours, malformations and increased mortality rates as a result of exposure to increased levels of CO2. However, other studies fail to recognize any consequence, suggesting species-specific sensitivity to increased levels of CO2, highlighting the need of further research. In this study we investigated the effects of exposure to elevated pCO2 on behaviour, development, oxidative stress and energy metabolism of sand smelt larvae, Atherina presbyter. Larvae were caught at Arrábida Marine Park (Portugal) and exposed to different pCO2 levels (control: ~600µatm, pH=8.03; medium: ~1000µatm, pH=7.85; high: ~1800µatm, pH=7.64) up to 15days, after which critical swimming speed (Ucrit), morphometric traits and biochemical biomarkers were determined. Measured biomarkers were related with: 1) oxidative stress - superoxide dismutase and catalase enzyme activities, levels of lipid peroxidation and DNA damage, and levels of superoxide anion production; 2) energy metabolism - total carbohydrate levels, electron transport system activity, lactate dehydrogenase and isocitrate dehydrogenase enzyme activities. Swimming speed was not affected by treatment, but exposure to increasing levels of pCO2 leads to higher energetic costs and morphometric changes, with larger larvae in high pCO2 treatment and smaller larvae in medium pCO2 treatment. The efficient antioxidant response capacity and increase in energetic metabolism only registered at the medium pCO2 treatment may indicate that at higher pCO2 levels the capacity of larvae to restore their internal balance can be impaired. Our findings illustrate the need of using multiple approaches to explore the consequences of future pCO2 levels on organisms.

Fishers' behaviour in response to the implementation of a Marine Protected Area.

Marine Protected Areas (MPAs) have been widely proposed as a fisheries management tool in addition to their conservation purposes. Despite this, few studies have satisfactorily assessed the dynamics of fishers' adaptations to the loss of fishing grounds. Here we used data from before, during and after the implementation of the management plan of a temperate Atlantic multiple-use MPA to examine the factors affecting the spatial and temporal distribution of different gears used by the artisanal fishing fleet. The position of vessels and gear types were obtained by visual surveys and related to spatial features of the marine park. A hotspot analysis was conducted to identify heavily utilized patches for each fishing gear and time period. The contribution of individual vessels to each significant cluster was assessed to better understand fishers' choices. Different fisheries responded differently to the implementation of protection measures, with preferred habitats of target species driving much of the fishers' choices. Within each fishery, individual fishers showed distinct strategies with some operating in a broader area whereas others kept preferred territories. Our findings are based on reliable methods that can easily be applied in coastal multipurpose MPAs to monitor and assess fisheries and fishers responses to different management rules and protection levels. This paper is the first in-depth empirical study where fishers' choices from artisanal fisheries were analysed before, during and after the implementation of a MPA, thereby allowing a clearer understanding of the dynamics of local fisheries and providing significant lessons for marine conservation and management of coastal systems.

Sex differences in the dorsolateral telencephalon correlate with home range size in blenniid fish.

Blenniid fish exhibit a polygynandric mating system with parental care restricted to males. Nest-holder males defend a breeding territory centered on their nest, usually a crevice or hole in a rocky substrate, to which they attract females to spawn. Females, on the other hand, must search for nests in order to spawn and usually are the choosy sex, producing several sequential egg batches and broods during the breeding season. Therefore, male blennies are more site-attached than females. This situation offers an opportunity to investigate potential neural correlates of intraspecific differences in selective pressures for different spatial abilities in these species. Since the dorsolateral telencephalon has been considered a teleost homologue of the mammalian hippocampus, we predicted that the spatial abilities required for females to locate and return accurately to nests of males may have produced a sex difference in the size of the telencephalic nuclei involved in spatial abilities, biased towards females. To test this hypothesis, we assessed the home ranges and measured the size of the dorsolateral telencephalon of both sexes during the breeding season in two blenniid species, the shanny (Lipophrys pholis) and the Azorean rock-pool blenny (Parablennius parvicornis). We chose these two species because they differ in the degree of chemical communication they use, and this could also lead to differences in telencephalic areas. As predicted, in both species females present considerably larger home ranges paralleled by larger dorsolateral ventral telencephalic nuclei (DLv) than males. Other telencephalic nuclei that were measured did not show any sex difference in size. These results suggest that the DLv is involved in spatial abilities in blenniid fish and that sexual selection may be promoting this divergence as already described for mammals and birds.

Monitoring underwater explosions in the habitat of resident bottlenose dolphins.

Maintenance work on the harbor of Setúbal, in Portugal, required the removal of a 14-m deep rocky outcrop at the ship maneuver area, using about 35 kg of Gelamonite, a nitroglycerin-based high-explosive. This important harbor is located in the Sado estuary, a biologically rich environment and an important feeding area for a resident community of bottlenose dolphins. Using different safe range calculation models, a mitigation and monitoring plan was developed that minimized the risks of these underwater explosions for the dolphins. At our monitoring station, at 2 km from the demolition site, acoustic pressure levels in excess of 170 dB re 1 µPa (root-mean-square) were measured. Samples of dead fish collected at the site were indicative of shock trauma from the blasts.