Targeting fin whale conservation in the North-Western Mediterranean Sea: insights on movements and behaviour from biologging and habitat modelling.

Biologging and habitat modelling are key tools supporting the development of conservation measures and mitigating the effects of anthropogenic pressures on marine species. Here, we analysed satellite telemetry data and foraging habitat preferences in relation to chlorophyll-a productivity fronts to understand the movements and behaviour of endangered Mediterranean fin whales (Balaenoptera physalus) during their spring-summer feeding aggregation in the North-Western Mediterranean Sea. Eleven individuals were equipped with Argos satellite transmitters across 3 years, with transmissions averaging 23.5 ± 11.3 days. Hidden Markov Models were used to identify foraging behaviour, revealing how individuals showed consistency in their use of seasonal core feeding grounds; this was supported by the distribution of potential foraging habitat. Importantly, tracked whales spent most of their time in areas with no explicit protected status within the study region. This highlights the need for enhanced time- and place-based conservation actions to mitigate the effects of anthropogenic impacts for this species, notably ship strike risk and noise disturbance in an area of exceptionally high maritime traffic levels. These findings strengthen the need to further assess critical habitats and Important Marine Mammal Areas that are crucial for focused conservation, management and mitigation efforts.

Isotopic composition of the eastern gray whale epidermis indicates contribution of prey outside Arctic feeding grounds.

Eastern gray whales' distribution range and plasticity in feeding behavior complicates the understanding of critical life-history such as pregnancy and lactation. Our goal was to determine if females who experienced gestation, gave birth, and lactated their calves, assimilated a high proportion of benthic amphipods from the Bering Sea, which are considered the species' main prey. We used Bayesian stable isotope mixing models to estimate the probability of contribution of food items sampled along the species' distributional range, using isotopic data on amphipods from the Bering Sea, mysids from Vancouver Island, and amphipods and polychaetes from Ojo de Liebre Lagoon. We sampled epidermal tissue from lactating females (n = 25) and calves (n = 34) and analyzed their carbon and nitrogen isotopic composition. Model outcome indicated that benthic amphipods from the Bering Sea were not the primary food for the eastern gray whale. Each mother performed a different feeding strategy, and prey from Vancouver Island were generally as important as that from the Bering Sea. Moreover, model results indicate a constant use of Ojo de Liebre Lagoon as a feeding ground. Our results appear to agree with previous studies that report continuous feeding by females to satisfy certain physiological requirements (e.g., fatty acids omega-6) during migration and breeding time. Future investigations of the isotopic composition of all those prey items that could be assimilated by the eastern gray whale emerge as critical. Both historical and recent information, that would provide insights in the species feeding ecology under past and present environmental conditions, should be considered as equally important to establish conservation and management plans.

Fin whale (Balaenoptera physalus) mitogenomics: A cautionary tale of defining sub-species from mitochondrial sequence monophyly.

The advent of massive parallel sequencing technologies has resulted in an increase of studies based upon complete mitochondrial genome DNA sequences that revisit the taxonomic status within and among species. Spatially distinct monophyly in such mitogenomic genealogies, i.e., the sharing of a recent common ancestor among con-specific samples collected in the same region has been viewed as evidence for subspecies. Several recent studies in cetaceans have employed this criterion to suggest subsequent intraspecific taxonomic revisions. We reason that employing intra-specific, spatially distinct monophyly at non-recombining, clonally inherited genomes is an unsatisfactory criterion for defining subspecies based upon theoretical (genetic drift) and practical (sampling effort) arguments. This point was illustrated by a re-analysis of a global mitogenomic assessment of fin whales, Balaenoptera physalus spp., published by Archer et al. (2013), which proposed to further subdivide the Northern Hemisphere fin whale subspecies, B. p. physalus. The proposed revision was based upon the detection of spatially distinct monophyly among North Atlantic and North Pacific fin whales in a genealogy based upon complete mitochondrial genome DNA sequences. The extended analysis conducted in this study (1676 mitochondrial control region, 162 complete mitochondrial genome DNA sequences and 20 microsatellite loci genotyped in 380 samples) revealed that the apparent monophyly among North Atlantic fin whales reported by Archer et al. (2013) to be due to low sample sizes. In conclusion, defining sub-species from monophyly (i.e., the absence of para- or polyphyly) can lead to erroneous conclusions due to relatively "trivial" aspects, such as sampling. Basic population genetic processes (i.e., genetic drift and migration) also affect the time to the most recent common ancestor and hence the probability that individuals in a sample are monophyletic.

Assessing cetacean surveys throughout the Mediterranean Sea: a gap analysis in environmental space.

Heterogeneous data collection in the marine environment has led to large gaps in our knowledge of marine species distributions. To fill these gaps, models calibrated on existing data may be used to predict species distributions in unsampled areas, given that available data are sufficiently representative. Our objective was to evaluate the feasibility of mapping cetacean densities across the entire Mediterranean Sea using models calibrated on available survey data and various environmental covariates. We aggregated 302,481 km of line transect survey effort conducted in the Mediterranean Sea within the past 20 years by many organisations. Survey coverage was highly heterogeneous geographically and seasonally: large data gaps were present in the eastern and southern Mediterranean and in non-summer months. We mapped the extent of interpolation versus extrapolation and the proportion of data nearby in environmental space when models calibrated on existing survey data were used for prediction across the entire Mediterranean Sea. Using model predictions to map cetacean densities in the eastern and southern Mediterranean, characterised by warmer, less productive waters, and more intense eddy activity, would lead to potentially unreliable extrapolations. We stress the need for systematic surveys of cetaceans in these environmentally unique Mediterranean waters, particularly in non-summer months.

Satellite tagging of Mediterranean fin whales: working towards the identification of critical habitats and the focussing of mitigation measures.

Mediterranean fin whales comprise a genetically distinct population, listed as Vulnerable (VU) in the IUCN Red List. Collisions with vessels are believed to represent the main cause of human-induced mortality. The identification of critical habitats (including migration routes) incorporating satellite telemetry data is therefore crucial to develop focussed conservation efforts. Between 2012 and 2015 thirteen fin whales were equipped with satellite transmitters, 8 in the Pelagos Sanctuary (although two ceased within two days) and 5 in the Strait of Sicily, to evaluate movements and habitat use. A hierarchical switching state-space model was used to identify transiting and area-restricted search (ARS) behaviours, believed to indicate foraging activities. All whales undertook mid- to long-distance migrations, crossing some of the world's busiest maritime routes. Areas where the animals predominantly engaged in ARS behaviour were identified in both study areas. The telemetry data were compared with results from ecosystem niche modelling, and showed that 80% of tagged whale positions was near (<7 km) the closest suitable habitat. The results contribute to the view that precautionary management should include establishment of a coordinated and dynamic basin-wide management scheme; if appropriate, this may include the establishment of protected areas by specific regional Conventions.

Fin whales and microplastics: The Mediterranean Sea and the Sea of Cortez scenarios.

The impact that microplastics have on baleen whales is a question that remains largely unexplored. This study examined the interaction between free-ranging fin whales (Balaenoptera physalus) and microplastics by comparing populations living in two semi-enclosed basins, the Mediterranean Sea and the Sea of Cortez (Gulf of California, Mexico). The results indicate that a considerable abundance of microplastics and plastic additives exists in the neustonic samples from Pelagos Sanctuary of the Mediterranean Sea, and that pelagic areas containing high densities of microplastics overlap with whale feeding grounds, suggesting that whales are exposed to microplastics during foraging; this was confirmed by the observation of a temporal increase in toxicological stress in whales. Given the abundance of microplastics in the Mediterranean environment, along with the high concentrations of Persistent Bioaccumulative and Toxic (PBT) chemicals, plastic additives and biomarker responses detected in the biopsies of Mediterranean whales as compared to those in whales inhabiting the Sea of Cortez, we believe that exposure to microplastics because of direct ingestion and consumption of contaminated prey poses a major threat to the health of fin whales in the Mediterranean Sea.

The Devil We Don't Know: Investigating Habitat and Abundance of Endangered Giant Devil Rays in the North-Western Mediterranean Sea.

The giant devil ray Mobula mobular, the only Mediterranean mobulid, is subject to mortality caused by directed and accidental captures in fisheries throughout the region. Whilst the combination of human impacts, limited range and a low reproductive potential is not inconsistent with its endangered listing, there are insufficient data to enable a quantitative assessment of trends. Without this, it is difficult to assess and prioritise threats and develop effective conservation actions. Using results from aerial surveys conducted between 2009 and 2014 over the Ligurian, Corsican, Sardinian, northern and central Tyrrhenian seas (626,228 km2), this study provides the first quantitative information on giant devil ray abundance and habitat choice in the western Mediterranean. Devil rays were observed in all seasons except winter, with their estimated abundance in the study area peaking in summer. The overall uncorrected mean density in the study area during summer was estimated at 0.0257 individuals km-2 (range: 0.017-0.044), resulting in a total abundance estimate of 6,092 (12.7%CV) individuals at the surface; once corrected for availability bias, this estimate indicates a summer presence of >12,700 devil rays in the study area. Rays were mostly observed alone even if occasionally, larger aggregations up to a maximum of 18 individuals were observed. Although observed throughout the study area, spatial modelling identified their preferred habitat to be over a broad strip connecting the Tuscan Archipelago to Eastern Sardinia, over a wide range of water depths ranging from 10 to 2000m. The observed seasonal changes in giant devil ray distribution in this study, combined with similar evidence from other areas in the Mediterranean, support the hypothesis that the species undertakes latitudinal migrations across the region, taking advantage of highly productive waters in the north during summer, and warmer southern waters during winter.

An index based on the biodiversity of cetacean species to assess the environmental status of marine ecosystems.

The Marine Strategy Framework Directive (MSFD) requires the assessment of the environmental status in relation to human pressures. In this study the biodiversity of the cetacean community is proposed as MSFD descriptor of the environmental status and its link with anthropogenic pressures is investigated. Functional groups are generally favoured over indicator species since they are thought to better reflect to anthropogenic stressors. Cetaceans are in many situations the most well known component of pelagic ecosystems. Their habitat requirements are known and can be used to evaluate the theoretical biodiversity that should be expected in a certain area. The deviations between the theoretical biodiversity and the actual biodiversity may be used to detect the impacts of human activities. Based on this analysis fishery resulted to be by far the most significant of the existing pressures. Among all the species, bottlenose dolphin was found the most correlated with the fishery sector dynamics.

Abundance and distribution of Tursiops truncatus in the Western Mediterranean Sea: an assessment towards the Marine Strategy Framework Directive requirements.

The Mediterranean Sea common bottlenose dolphin population has been assessed as Vulnerable according to the IUCN Red List Criteria. The species is also included in several International Agreements, European Union Regulations and Directives. Amongst them, a strict protection and identification of special conservation areas are requested by the EU Habitats Directive. Despite direct takes, by-catch, chemical and acoustic pollution, and prey depletion, general habitat degradation and fragmentation have been indicated as detrimental for the species, the degree to which these threats pose population risk is still largely unknown. At present it is thus not possible to depict the actual status of the population and to assess prospective trends. To address this gap in the current knowledge, line transect distance sampling aerial surveys were conducted in a wide portion of the Western Mediterranean Sea between the summer of 2010 and winter 2011. A total of 165 parallel transects equally spaced at 15 km were designed providing homogeneous coverage probability. Overall, 21,090 km were flown on effort and 16 bottlenose dolphin sightings were recorded and used for the analysis. The surface abundance and density estimates resulted in 1676 animals (CV = 38.25; 95% CI = 804-3492) with a density of 0.005 (CV = 38.25%). These results represent the first ever estimates for the common bottlenose dolphin over a wide portion of the Western Mediterranean Sea Subregion, with the potential to be useful baseline data to inform conservation. Specifically, they could be used as indicators under the Marine Strategy Framework Directive requirements, in conjunction with other study methods.

Demography and conservation of the Mediterranean fin whale (Balaenoptera physalus): what clues can be obtained from photo-identification data.

Long-lived and slow reproducing species, such as cetaceans, are among the most critical conservation units: a demographic approach can be very useful for their management and conservation. In the present work, we examined, by demographic tools, the most exhaustive photo-identification database available for the Mediterranean fin whale (Balaenoptera physalus) population, recorded by Tethys Research Institute between 1990 and 2007 in the Western Ligurian Sea. A total of 31,782 km were covered and 548 fin whale sightings were recorded. The occurrence of the target species was uneven across the years and months: an anomalous reduction of sightings occurred between 2001 and 2004. Moreover, the target species is likely to concentrate in the study area in the summer months and probably moves to other areas in the early autumn. Using the photo-identification technique, 431 different individuals were photo-identified, but only 318 of them were sized: 6 calves (≤ 10 meters), 33 immature (10-15 m), 261 adolescent-adult (> 15 m) and 18 olds (≥ 20 m). For the first time the site of the fin whale sub-population in the Pelagos Sanctuary was obtained by photo-identification and mark-recapture techniques. These techniques were used to estimate the site of the sub-population composed by individuals > 15 meters as 539 fin whales (95% confidence interval = 345-732) over the period 1990-1999. The number of calves was likely underestimated, as the sighting period (late spring-summer) was shifted with respect to the peak of births (late autumn). To fill this gap of knowledge we propose a simple mathematical model for the yearly dynamics of calves. After correcting the number of calves, a static life history table for the period 1990-2007 was set out. Our results highlight the highest survival proportions between calf and immature (61.1%) and the minimum between adolescent-adult and old (2.5%) vital stages. The overall life expectancy is estimated to be 6.3 years while the life expectancy of individuals entering the adolescent-adult stage is 14.3 years. This paper aims at providing a contribution for improving the conservation efforts and the demographic knowledge on fin whales in the Pelagos Sanctuary.

Mitogenomic phylogenetics of fin whales (Balaenoptera physalus spp.): genetic evidence for revision of subspecies.

There are three described subspecies of fin whales (Balaenoptera physalus): B. p. physalus Linnaeus, 1758 in the Northern Hemisphere, B. p. quoyi Fischer, 1829 in the Southern Hemisphere, and a recently described pygmy form, B. p. patachonica Burmeister, 1865. The discrete distribution in the North Pacific and North Atlantic raises the question of whether a single Northern Hemisphere subspecies is valid. We assess phylogenetic patterns using ~16 K base pairs of the complete mitogenome for 154 fin whales from the North Pacific, North Atlantic--including the Mediterranean Sea--and Southern Hemisphere. A Bayesian tree of the resulting 136 haplotypes revealed several well-supported clades representing each ocean basin, with no haplotypes shared among ocean basins. The North Atlantic haplotypes (n = 12) form a sister clade to those from the Southern Hemisphere (n = 42). The estimated time to most recent common ancestor (TMRCA) for this Atlantic/Southern Hemisphere clade and 81 of the 97 samples from the North Pacific was approximately 2 Ma. 14 of the remaining North Pacific samples formed a well-supported clade within the Southern Hemisphere. The TMRCA for this node suggests that at least one female from the Southern Hemisphere immigrated to the North Pacific approximately 0.37 Ma. These results provide strong evidence that North Pacific and North Atlantic fin whales should not be considered the same subspecies, and suggest the need for revision of the global taxonomy of the species.

Monitoring winter and summer abundance of cetaceans in the Pelagos Sanctuary (northwestern Mediterranean Sea) through aerial surveys.

Systematic long-term monitoring of abundance is essential to inform conservation measures and evaluate their effectiveness. To instigate such work in the Pelagos Sanctuary in the Mediterranean, two aerial surveys were conducted in winter and summer 2009. A total of 467 (131 in winter, 336 in summer) sightings of 7 species was made. Sample sizes were sufficient to estimate abundance of fin whales in summer (148; 95% CI = 87-254) and striped dolphins in winter (19,462; 95% CI = 12 939-29 273) and in summer (38 488; 95% CI = 27 447-53 968). Numbers of animals within the Sanctuary are significantly higher in summer, when human activities and thus potential population level impacts are highest. Comparisons with data from past shipboard surveys suggest an appreciable decrease in fin whales within the Sanctuary area and an appreciable increase in striped dolphins. Aerial surveys proved to be more efficient than ship surveys, allowing more robust estimates, with smaller CIs and CVs. These results provide essential baseline data for this marine protected area and continued regular surveys will allow the effectiveness of the MPA in terms of cetacean conservation to be evaluated and inform future management measures. The collected data may also be crucial in assessing whether ship strikes, one of the main causes of death for fin whales in the Mediterranean, are affecting the Mediterranean population.

A multi-trial diagnostic tool in fin whale (Balaenoptera physalus) skin biopsies of the Pelagos Sanctuary (Mediterranean Sea) and the Gulf of California (Mexico).

The main objective of this study was to apply a set of sensitive non-lethal biomarkers in skin biopsies of fin whales (Balaenoptera physalus) to evaluate the toxicological status of this mysticete in the Pelagos Sanctuary (Mediterranean Sea) and in the Gulf of California (Sea of Cortez-Mexico). We developed a "multi-trial diagnostic tool" (based on field and in vitro studies), combining molecular biomarkers (western blot of CYP1A1, CYP2B) and gene expression (qRT-PCR of HSP70, ERα, AHR, E2F-1) with the analysis of OCs, PAHs and PBDEs. The study revealed a higher level of toxicological stress in the Mediterranean fin whales.

Mediterranean fin whales at risk from fatal ship strikes.

This paper reviews and analyzes ship collision records for the relatively isolated population of fin whales in the Mediterranean Sea from 1972 to 2001. Out of 287 carcasses, 46 individuals (16.0%) were certainly killed by boats. The minimum mean annual fatal collision rate increased from 1 to 1.7 whales/year from the 1970s to the 1990s. Fatal strike events (82.2%) were reported in or adjacent to the Pelagos Sanctuary, characterized by high levels of traffic and whale concentrations. Among 383 photo-identified whales, 9 (2.4%) had marks that were attributed to a ship impact. The reported rates are unusually high for baleen whales. The high likelihood of unreported fatal strikes combined with other anthropogenic threats suggests an urgent need for a comprehensive, basin-wide conservation strategy, including ship strike mitigation requirements, like real-time monitoring of whale presence and distribution to re-locate ferry routes to areas of lower cetacean density, and reducing ship speed in high cetacean density areas.

The use of a non-lethal tool for evaluating toxicological hazard of organochlorine contaminants in Mediterranean cetaceans: new data 10 years after the first paper published in MPB.

In the Mediterranean Sea, top predators, and particularly cetacean odontocetes, accumulate high concentrations of organochlorine contaminants and toxic metals, incurring high toxicological risk. In this paper we investigate the use of the skin biopsies as a non-lethal tool for evaluating toxicological hazard of organochlorines in Mediterranean cetaceans, presenting new data 10 years after the paper published by Fossi and co-workers [Mar. Poll. Bull. 24 (9) (1992) 459] in which this new methodology was first presented. Some organochlorine compounds, now with worldwide distribution, are known as endocrine disrupting chemicals (EDCs). Here the unexplored hypothesis that Mediterranean cetaceans are potentially at risk due to organochlorines with endocrine disrupting capacity is investigated. High concentrations of DDT metabolites and PCB congeners (known as EDCs) were found in the different Mediterranean species (Stenella coeruleoalba, Delphinus delphis, Tursiops truncatus and Balaenoptera physalus). In this paper we also propose benzo(a)pyrene monooxygenase (BPMO) activity in marine mammal skin biopsies (non-lethal biomarker) as a potential indicator of exposure to organochlorines, with special reference to the compounds with endocrine disrupting capacity. A statistically significant correlation was found between BPMO activity and organochlorine levels (DDTs, pp(')DDT, op(')DDT, PCBs and PCB99) in skin biopsies of males of B. physalus. Moreover a statistical correlation was also found between BPMO activity and DDT levels in skin biopsies of the endangered Mediterranean population of D. delphis. These results suggest that BPMO induction may be an early sign of exposure to organochlorine EDCs and can be used for periodic monitoring of Mediterranean marine mammal toxicological status.