From ecological functions to ecosystem services: linking coastal lagoons biodiversity with human well-being.

In this review we highlight the relevance of biodiversity that inhabit coastal lagoons, emphasizing how species functions foster processes and services associated with this ecosystem. We identified 26 ecosystem services underpinned by ecological functions performed by bacteria and other microbial organisms, zooplankton, polychaetae worms, mollusks, macro-crustaceans, fishes, birds, and aquatic mammals. These groups present high functional redundancy but perform complementary functions that result in distinct ecosystem processes. Because coastal lagoons are located in the interface between freshwater, marine and terrestrial ecosystems, the ecosystem services provided by the biodiversity surpass the lagoon itself and benefit society in a wider spatial and historical context. The species loss in coastal lagoons due to multiple human-driven impacts affects the ecosystem functioning, influencing negatively the provision of all categories of services (i.e., supporting, regulating, provisioning and cultural). Because animals' assemblages have unequal spatial and temporal distribution in coastal lagoons, it is necessary to adopt ecosystem-level management plans to protect habitat heterogeneity and its biodiversity, ensuring the provision of services for human well-being to multi-actors in the coastal zone.

Effect of kelp gull harassment on southern right whale calf survival: a long-term capture-recapture analysis.

Kelp gulls (Larus dominicanus) commonly feed on the skin and blubber of surfacing southern right whales (SRW, Eubalaena australis) in the near shore waters of Península Valdés (PV), Argentina. Mothers and especially calves respond to gull attacks by changing their swimming speeds, resting postures and overall behaviour. Gull-inflicted wounds per calf have increased markedly since the mid-1990s. Unusually high mortality of young calves occurred locally after 2003, and increasing evidence points to gull harassment as a factor contributing to the excess deaths. After leaving PV, calves undertake a long migration with their mothers to summer feeding areas; their health during this strenuous exertion is likely to affect their probabilities of first-year survival. To explore the effects of gull-inflicted wounds on calf survival, we analysed 44 capture-recapture observations between 1974 and 2017, for 597 whales photo-identified in their years of birth between 1974 and 2011. We found a marked decrease in first-year survival associated with an increase in wound severity over time. Our analysis supports recent studies indicating that gull harassment at PV may impact SRW population dynamics.

Foraging synchrony drives resilience in human-dolphin mutualism.

Interactions between humans and nature have profound consequences, which rarely are mutually beneficial. Further, behavioral and environmental changes can turn human-wildlife cooperative interactions into conflicts, threatening their continued existence. By tracking fine-scale behavioral interactions between artisanal fishers and wild dolphins targeting migratory mullets, we reveal that foraging synchrony is key to benefiting both predators. Dolphins herd mullet schools toward the coast, increasing prey availability within the reach of the net-casting fishers, who gain higher foraging success-but only when matching the casting behavior with the dolphins' foraging cues. In turn, when dolphins approach the fishers' nets closely and cue fishers in, they dive for longer and modify their active foraging echolocation to match the time it takes for nets to sink and close over mullets-but only when fishers respond to their foraging cues appropriately. Using long-term demographic surveys, we show that cooperative foraging generates socioeconomic benefits for net-casting fishers and ca. 13% survival benefits for cooperative dolphins by minimizing spatial overlap with bycatch-prone fisheries. However, recent declines in mullet availability are threatening these short- and long-term benefits by reducing the foraging success of net-casting fishers and increasing the exposure of dolphins to bycatch in the alternative fisheries. Using a numerical model parametrized with our empirical data, we predict that environmental and behavioral changes are pushing this traditional human-dolphin cooperation toward extinction. We propose two possible conservation actions targeting fishers' behavior that could prevent the erosion of this century-old fishery, thereby safeguarding one of the last remaining cases of human-wildlife cooperation.

Safeguarding human-wildlife cooperation.

Human-wildlife cooperation occurs when humans and free-living wild animals actively coordinate their behavior to achieve a mutually beneficial outcome. These interactions provide important benefits to both the human and wildlife communities involved, have wider impacts on the local ecosystem, and represent a unique intersection of human and animal cultures. The remaining active forms are human-honeyguide and human-dolphin cooperation, but these are at risk of joining several inactive forms (including human-wolf and human-orca cooperation). Human-wildlife cooperation faces a unique set of conservation challenges, as it requires multiple components-a motivated human and wildlife partner, a suitable environment, and compatible interspecies knowledge-which face threats from ecological and cultural changes. To safeguard human-wildlife cooperation, we recommend: (i) establishing ethically sound conservation strategies together with the participating human communities; (ii) conserving opportunities for human and wildlife participation; (iii) protecting suitable environments; (iv) facilitating cultural transmission of traditional knowledge; (v) accessibly archiving Indigenous and scientific knowledge; and (vi) conducting long-term empirical studies to better understand these interactions and identify threats. Tailored safeguarding plans are therefore necessary to protect these diverse and irreplaceable interactions. Broadly, our review highlights that efforts to conserve biological and cultural diversity should carefully consider interactions between human and animal cultures. Please see AfricanHoneyguides.com/abstract-translations for Kiswahili and Portuguese translations of the abstract.

Ocean warming threatens southern right whale population recovery.

Whales contribute to marine ecosystem functioning, and they may play a role in mitigating climate change and supporting the Antarctic krill (Euphausia superba) population, a keystone prey species that sustains the entire Southern Ocean (SO) ecosystem. By analyzing a five-decade (1971­2017) data series of individual southern right whales (SRWs; Eubalaena australis) photo-identified at Península Valdés, Argentina, we found a marked increase in whale mortality rates following El Niño events. By modeling how the population responds to changes in the frequency and intensity of El Niño events, we found that such events are likely to impede SRW population recovery and could even cause population decline. Such outcomes have the potential to disrupt food-web interactions in the SO, weakening that ecosystem's contribution to the mitigation of climate change at a global scale.

Low-frequency sampling rates are effective to record bottlenose dolphins.

Acoustic monitoring in cetacean studies is an effective but expensive approach. This is partly because of the high sampling rate required by acoustic devices when recording high-frequency echolocation clicks. However, the proportion of echolocation clicks recorded at different frequencies is unknown for many species, including bottlenose dolphins. Here, we investigated the echolocation clicks of two subspecies of bottlenose dolphins in the western South Atlantic Ocean. The possibility of recording echolocation clicks at 24 and 48 kHz was assessed by two approaches. First, we considered the clicks in the frequency range up to 96 kHz. We found a loss of 0.95-13.90% of echolocation clicks in the frequency range below 24 kHz, and 0.01-0.42% below 48 kHz, to each subspecies. Then, we evaluated these recordings downsampled at 48 and 96 kHz and confirmed that echolocation clicks are recorded at these lower frequencies, with some loss. Therefore, despite reaching high frequencies, the clicks can also be recorded at lower frequencies because echolocation clicks from bottlenose dolphins are broadband. We concluded that ecological studies based on the presence-absence data are still effective for bottlenose dolphins when acoustic devices with a limited sampling rate are used.

Ecological divergence and speciation in common bottlenose dolphins in the western South Atlantic.

Coastal and offshore ecotypes of common bottlenose dolphins have been recognized in the western South Atlantic, and it is possible that trophic niche divergence associated with social interactions is leading them to genetic and phenotypic differentiation. The significant morphological differentiation observed between these ecotypes suggests they represent two different subspecies. However, there is still a need to investigate whether there is congruence between morphological and genetic data to rule out the possibility of ecophenotypic variation accompanied by gene flow. Mitochondrial DNA (mtDNA) control region sequence data and 10 microsatellite loci collected from stranded and biopsied dolphins sampled in coastal and offshore waters of Brazil as well as 106 skulls for morphological analyses were used to determine whether the morphological differentiation was supported by genetic differentiation. There was congruence among the data sets, reinforcing the presence of two distinct ecotypes. The divergence may be relatively recent, however, given the moderate values of mtDNA nucleotide divergence (dA = 0.008), presence of one shared mtDNA haplotype and possibly low levels of gene flow (around 1% of migrants per generation). Results suggest the ecotypes may be in the process of speciation and reinforce they are best described as two different subspecies until the degree of nuclear genetic divergence is thoroughly evaluated: Tursiops truncatus gephyreus (coastal ecotype) and T. t. truncatus (offshore ecotype). The endemic distribution of T. t. gephyreus in the western South Atlantic and number of anthropogenic threats in the area reinforces the importance of protecting this ecotype and its habitat.

Risk tolerance and control perception in a game-theoretic bioeconomic model for small-scale fisheries.

Cooperation is generally the most advantageous strategy for the group; however, on an individual level, cheating is frequently more attractive. In a fishery, one can choose to cooperate by fishing only the regulated amount or not to cooperate, by fishing to maximize profits. Top-down management can help to emulate a cooperative result in fisheries, but it is costly and not always a viable alternative for development states. Here, we investigate elements of a fishing system that can be strategically managed to encourage a cooperative behaviour. Using bioeconomic data, we modelled an evolutionary game between two populations of fishers that differ if they cooperate or do not cooperate with a fishing restriction. We penalized players including risk tolerance and control perception, two social parameters that might favour cooperation. We assessed the degrees to which risk tolerance and control perception affect the cooperative behaviours of fishers in a restricted fishing effort small-scale fishery (RSSF) in southern Brazil. We also assessed the likelihood of a scenario wherein a cooperative strategy can evolve and dominate the system. We identified dominance and coexistence outcomes for the RSSF. Sensitivity analyses suggested that both control perception and risk tolerance could facilitate a cooperative outcome for the fishery.

The ability of artisanal fishers to recognize the dolphins they cooperate with.

BACKGROUND: Human-animal interactions with mutual benefits in the wild are rare. Such positive interactions seem to require an intricate knowledge from the human side on the animals' behavior and their habitat. In southern Brazil, dolphins and human net-casting fishers have specialized in a cooperative foraging, in which fishers report being able to identify and name dolphins. Here, we evaluate the consensus in their ability to recognize the individual dolphins they interact with. By investigating the reliability of this recognition process, we assess the pros and cons of relying on the fishers' traditional knowledge to further understand the behavior and ecology of dolphins at the individual level. We also assess the potential role of traditional knowledge for the maintenance of this unusual interaction. METHODS: We interviewed 38 fishers using a semi-structured questionnaire. During each interview, we evaluate their recognition ability of dolphins by showing high-quality photos of dorsal fins of different dolphins, asking questions about the dolphins' behavior and traits, and about how fishers recognize each dolphin. We also evaluated information about the fishers. Different indices were used to measure the fishers' ability to recognize dolphins via photos, and their consensus on individual identification. These indices were modeled as functions of traits of both dolphins and fishers to investigate which ones influence the recognition process. RESULTS: We found that fishers can primarily recognize dolphins by natural marks in the dorsal fin but there was little consensus in recognition. Fishers also tend to repeat the name of the most "popular" dolphins for different photos, indicating low reliability in individual recognition. We also found that fishers who learned from relatives (vertical learning) how to interact with dolphins tend to be more accurate and have higher consensus in dolphin recognition than those fishers who learned from friends (horizontal learning) or individually. CONCLUSION: Artisanal fishers have a deep understanding of the dolphins and the system they are inserted in. However, the lack of consensus in identifying individual dolphins herein reported indicates that using their traditional knowledge to further understand dolphin behavior and ecology at the individual level requires caution. Our study also suggests that the transmission of this tradition from parents to sons can be crucial to preserve such a unique human-animal positive interaction in its original form.

Molecular identification and microscopic characterization of poxvirus in a Guiana dolphin and a common bottlenose dolphin, Brazil.

The poxviruses identified in cetaceans are associated with characteristic tattoo or ring skin lesions. However, little is known regarding the prevalence and progression of these lesions and the molecular characterization of cetacean poxviruses in the Southern Hemisphere. This manuscript describes the progression of poxvirus-like skin lesions in 5 free-ranging Guiana dolphins Sotalia guianensis. Additionally, 151 skin samples from 113 free-ranging cetaceans from Brazil, including 4 animals with tattoo skin lesions, were selected for poxvirus testing. Poxviral DNA polymerase gene PCR amplification was used to detect the virus in ß-actin-positive samples (145/151). DNA topoisomerase I gene PCR was then used in Cetaceanpoxvirus (CePV)-positive cases (n = 2), which were further evaluated by histopathology and electron microscopy. Based on photo-identification, adult Guiana dolphins presented regressing or healed poxvirus-like lesions (2/2), while juveniles presented persistent (2/3) or healed and progressive lesions (1/3). CePV DNA was amplified in a common bottlenose dolphin Tursiops truncatus and in a Guiana dolphin. Intracytoplasmic inclusion bodies and viral particles consistent with poxvirus were identified by histology and electron microscopy, respectively. CePV-specific amino acid motifs were identified through phylogenetic analysis. Our findings corroborate previous studies that suggest the placement of poxviruses from cetaceans within the novel CePV genus. This is the first molecular identification of poxvirus in South American odontocetes.

Nestedness across biological scales.

Biological networks pervade nature. They describe systems throughout all levels of biological organization, from molecules regulating metabolism to species interactions that shape ecosystem dynamics. The network thinking revealed recurrent organizational patterns in complex biological systems, such as the formation of semi-independent groups of connected elements (modularity) and non-random distributions of interactions among elements. Other structural patterns, such as nestedness, have been primarily assessed in ecological networks formed by two non-overlapping sets of elements; information on its occurrence on other levels of organization is lacking. Nestedness occurs when interactions of less connected elements form proper subsets of the interactions of more connected elements. Only recently these properties began to be appreciated in one-mode networks (where all elements can interact) which describe a much wider variety of biological phenomena. Here, we compute nestedness in a diverse collection of one-mode networked systems from six different levels of biological organization depicting gene and protein interactions, complex phenotypes, animal societies, metapopulations, food webs and vertebrate metacommunities. Our findings suggest that nestedness emerge independently of interaction type or biological scale and reveal that disparate systems can share nested organization features characterized by inclusive subsets of interacting elements with decreasing connectedness. We primarily explore the implications of a nested structure for each of these studied systems, then theorize on how nested networks are assembled. We hypothesize that nestedness emerges across scales due to processes that, although system-dependent, may share a general compromise between two features: specificity (the number of interactions the elements of the system can have) and affinity (how these elements can be connected to each other). Our findings suggesting occurrence of nestedness throughout biological scales can stimulate the debate on how pervasive nestedness may be in nature, while the theoretical emergent principles can aid further research on commonalities of biological networks.

Estimating population parameters of longsnout seahorses, Hippocampus reidi (Teleostei: Syngnathidae) through mark-recapture

Estimating population parameters is essential for understanding the ecology of species, which ultimately helps to assess their conservation status. The seahorse Hippocampus reidi is directly exposed to anthropogenic threats along the Brazilian coast, but the species still figures as Data Deficient (DD) at IUCN's Red List. To provide better information on the ecology of this species, we studied how population parameters vary over time in a natural subtropical environment. By combing mark-recapture models for open and closed populations, we estimated abundance, survival rate, emigration probability, and capture probability. We marked 111 individuals, which showed a 1:1 sex ratio, and an average size of 10.5 cm. The population showed high survival rate, low temporary emigration probability and variable capture probability and abundance. Our models considering relevant biological criteria illuminate the relatively poorly known population ecology and life history of seahorses. It is our hope that this study inspires the use of mark-recapture methods in other populations of H. reidi in a collective effort to properly assess their conservation status.(AU)

Parâmetros populacionais são essenciais para compreender a ecologia das espécies, além de auxiliar a avalição do seu status de conservação. Dentre as espécies de cavalo-marinho que ocorrem no Brasil, Hippocampus reidi é a mais abundante, o que expõe suas populações a frequentes ameaças antropogênicas. Entretanto, esta espécie ainda consta como Deficiente em Dados (DD) na lista vermelha da IUCN. Considerando esta falta de informações sobre populações de H. reidi, utilizamos métodos de marcação e recaptura para avaliar como parâmetros de uma população de ambiente subtropical variam ao longo do tempo. Baseado em históricos de captura individuais, combinamos modelos de populações abertas e fechadas para estimar abundância, taxa de sobrevivência, probabilidade de emigração e probabilidade de captura. Ao todo, marcamos 111 indivíduos, em proporção sexual de 1:1, e tamanho médio de 10,5 cm. Esta população relativamente pequena apresentou alta taxa de sobrevivência, baixa probabilidade de emigração temporária e probabilidade de captura e abundância variáveis. A partir dos nossos modelos que consideraram critérios biológicos relevantes, fornecemos estimativas de parâmetros chave que auxiliarão a compreensão da ecologia e da história de vida de cavalos-marinhos. Nossa expectativa é que este método passe a ser amplamente utilizado em outras populações, em um esforço coletivo para avaliar o estado de conservação desta espécie.(AU)

Epidemiology of lobomycosis-like disease in bottlenose dolphins Tursiops spp. from South America and southern Africa.

We report on the epidemiology of lobomycosis-like disease (LLD), a cutaneous disorder evoking lobomycosis, in 658 common bottlenose dolphins Tursiops truncatus from South America and 94 Indo-Pacific bottlenose dolphins T. aduncus from southern Africa. Photographs and stranding records of 387 inshore residents, 60 inshore non-residents and 305 specimens of undetermined origin (inshore and offshore) were examined for the presence of LLD lesions from 2004 to 2015. Seventeen residents, 3 non-residents and 1 inshore dolphin of unknown residence status were positive. LLD lesions appeared as single or multiple, light grey to whitish nodules and plaques that may ulcerate and increase in size over time. Among resident dolphins, prevalence varied significantly among 4 communities, being low in Posorja (2.35%, n = 85), Ecuador, and high in Salinas, Ecuador (16.7%, n = 18), and Laguna, Brazil (14.3%, n = 42). LLD prevalence increased in 36 T. truncatus from Laguna from 5.6% in 2007-2009 to 13.9% in 2013-2014, albeit not significantly. The disease has persisted for years in dolphins from Mayotte, Laguna, Salinas, the Sanquianga National Park and Bahía Málaga (Colombia) but vanished from the Tramandaí Estuary and the Mampituba River (Brazil). The geographical range of LLD has expanded in Brazil, South Africa and Ecuador, in areas that have been regularly surveyed for 10 to 35 yr. Two of the 21 LLD-affected dolphins were found dead with extensive lesions in southern Brazil, and 2 others disappeared, and presumably died, in Ecuador. These observations stress the need for targeted epidemiological, histological and molecular studies of LLD in dolphins, especially in the Southern Hemisphere.

Biochemical biomarkers and hydrocarbons concentrations in the mangrove oyster Crassostrea brasiliana following exposure to diesel fuel water-accommodated fraction.

Understanding the toxic mechanisms by which organisms cope to environmental stressful conditions is a fundamental question for ecotoxicology. In this study, we evaluated biochemical responses and hydrocarbons bioaccumulation of the mangrove oyster Crassostrea brasiliana exposed for 96 h to four sublethal concentrations of diesel fuel water-accommodated fraction (WAF). For that purpose, enzymatic activities (SOD, CAT, GPx, GR, G6PDH, GST and GGT), HSP60 and HSP90 immunocontent and lipid peroxidation (LPO) levels were determined in the gill and digestive gland of oysters and related to the hydrocarbons accumulated in the whole soft tissues. The results of this study revealed clear biochemical responses to diesel fuel WAF exposure in both tissues of the oyster. The capacity of C. brasiliana to bioaccumulate aliphatic and aromatic hydrocarbons in a dose-dependent manner is a strong indication of its suitability as a model in biomonitoring programs along the Brazilian coast, which was also validated by the response of the antioxidant defenses, phase II biotransformation and chaperones. HSP60 levels and GGT activity were the most promising biomarkers in the gill, while GST and GR activities stood out as suitable biomarkers for the detection of diesel toxicity in the digestive gland. The decrease of SOD activity and HSP90 levels may also reflect a negative effect of diesel exposure regardless the tissue. The present results provide a sound preliminary report on the biochemical responses of C. brasiliana challenged with a petroleum by-product and should be carefully considered for use in the monitoring of oil and gas activities in Brazil.

Lobomycosis-like disease in wild bottlenose dolphins Tursiops truncatus of Laguna, southern Brazil: monitoring of a progressive case.

Lobomycosis is a chronic dermal infection affecting humans and small cetaceans. In 1993, a study identified the presence of the etiologic agent of lobomycosis in a resident population of Tursiops truncatus (bottlenose dolphin) in Laguna, Brazil. Until now, no additional information relating to the persistence or prevalence of this pathogen in this population has been available. Numbering less than 60 animals, the residency of these dolphins in an impacted lagoon system has raised concerns about the health and viability of this small population. Using photo-identification data collected between September 2007 and September 2009, this study evaluated the occurrence of lobomycosis-like disease (LLD) throughout this population. Of 47 adult dolphins and 10 calves identified, 7 (12%) presented some form of epidermal lesion and 5 (9%) had evidence of LLD. The lesions were stable in all but 2 cases, in which a progressive development was recorded in a presumed adult female and her calf (referred to here as the LLD pair). During the first few months of observation, the lesion grew slowly and at a constant rate on the adult. However, in the fourteenth month, the growth rate increased rapidly and the first lesions appeared on the calf. Compared to the rest of the population, the LLD pair also presented a different spatial ranging pattern, suggesting a possible social or geographic factor. Current and previous records of LLD or lobomycosis indicate that the disease is endemic in this population. These findings highlight the importance of monitoring both the health of these cetaceans and the quality of their habitat.