Strandings of cetaceans and sea turtles in the Alboran Sea and Strait of Gibraltar : a long – term glimpse at the north coast ( Spain ) and the south coast ( Morocco )

A total of 13 species of cetaceans and three species of marine turtles were found in this study. Data were collected by eight independent and self-regulated stranding networks, providing information about 1,198 marine mammal (10 odontocetii, three mysticetii and one phocidae) and 574 sea turtle stranding events between 1991 and 2008. Trends in the strandings were analysed in relation to species composition and abundance, and their geographic and seasonal distribution. The most abundant species recorded were the striped dolphin and the loggerhead turtle. Some of the strandings, such as the humpback whale, harbour porpoise, hooded seal and olive ridley turtle, were considered ‘rare’ because their distribution did not match the pattern of the study. When the north and south coasts in the study area were compared, pilot whales stranded more frequently in the north, while delphinid species stranded more in the south coast, and loggerhead turtles stranded more frequently in the north while leatherback turtles stranded more in south coast.


Introduction
Andalucía is a region in the south of Spain where two geographic systems meet: the Gulf of Cádiz (Atlantic Ocean) and the Alboran Sea (Mediterranean Sea).Andalucian coastal waters (south of Spain) are characterized by high biodiversity and productive habitats for commercial species; the area is characterized by nutrient inputs due to upwelling processes in the Gulf of Cadiz (García Lafuente & Ruiz, 2007), the Alboran Sea (Reul et al., 2005), and the water bodies mixing processes at the Strait of Gibraltar (Echevarria et al., 2002).In the Mediterranean Sea, 20 species of cetaceans (Notarbartolo di Sciara, 2002), and three species of marine turtles (Jerez et al., 2010) have been recorded.
Small and large species of cetaceans are distributed in this area not only as migrators (fin whale, Balaenoptera physalus, L. 1758; Jonsgård, 1966), but also as resident populations (short-beaked common dolphin, Delphinus delphis, L. 1758; Cañadas et al., 2002).Cetaceans are particularly vulnerable to threats deriving from human activities.The Mediterranean Sea supports a high human density in the coastal zone.Chemical pollution, marine debris, climate change, land-based changes (agriculture, industry, tourism, etc.), depletion of marine resources and acoustic contamination may all contribute to the degradation and loss of cetacean habitat.As a result, the natural factors causing cetacean mortality have intensified, such as the morbillivirus epizootic that affected the striped dolphin (Stenella coeruleoalba, M. 1833) in 1990 (Aguilar & Borrell, 1994).In addition, collisions with ships and incidental captures by fisheries are sources of direct mortality (Notarbartolo di Sciara, 2002).Cetaceans may also be affected by oil spills by causes such as contamination of their prey items (Moore & Clarke, 2002).
Three of the seven species of marine turtles can still be found in the Mediterranean Sea: the loggerhead sea turtle (Caretta caretta, L. 1758), the green turtle (Chelonia mydas, L. 1758) and the leatherback turtle (Dermochelys coriacea, V. 1761).All of them are currently classified as 'endangered' species (IUCN, 2007).Bycatch in drifting longlines has often been considered to be the main threat for immature loggerhead sea turtles, C. caretta, throughout the Mediterranean (Aguilar et al., 1995;Margaritoulis et al., 2003;Lewison et al., 2004;Deflorio et al., 2005;Camiñas et al., 2006).
To be effective, conservation actions require basic biological information about the species.Obtaining abundant estimates is a priority to assess the status of the cetacean species in the Mediterranean Sea and to evaluate the impact that human threats may have on the populations (Gómez de Segura et al., 2006).The information collected could contribute to the development of conservation plans by identifying coastal areas of high importance to cetaceans (Pierce et al., 2010).
To promote the maintenance of biodiversity, most species of cetaceans and marine turtles are protected under the European Union Habitats and Species Directive (92/43/EEC).The Spanish Law on Conservation of Wild areas and Species (4/1989) recognizes the need to protect cetaceans and marine turtles, and establishes the legal basis for their conservation, providing a national catalogue of threatened species.The Law on Conservation of Nature (9/2001) sets out rules for protection, and the Law on Natural Heritage and Biodiversity (42/2007) includes the incorporation of the Habitats Directive into Spanish Law.Royal decree 1727/2007 completes this legislation, establishing measures for the protection of cetacean species in Spanish waters (Pierce et al., 2010).
The monitoring of cetacean strandings in the south of Spain and north of Morocco has been undertaken since 1990 by several non-governmental volunteer organizations through the Marine Animal Stranding Network.Stranding networks are made up of volunteers based at local environmental NGOs, academic associations, and veterinary clinics and also by independent people who respond to or provide professional advice on handling stranding events.Data gathered from stranding events can facilitate management in several ways.It provides an overview of distribution and stranding trends usually observed in the region, it helps monitor stranding patterns (spatial and temporal) by identifying unusual mortality events, and it adds to existing knowledge on distribution of cetaceans already obtained from terrestrial sightings and aerial and shipboard surveys.Furthermore, stranded animals provide information on population movement patterns or residency of a given species (Norman et al., 2004).It may also be possible to draw correlations between beached species and their parent populations in the region (Woodhouse, 1991).
This work links data from eight independent and self-regulated stranding networks in Spain and Morocco, providing information about 1198 cetacean and 574 sea turtle stranding events from both sides of the Gibraltar Strait and the Alboran Sea.Trends in stranding reports are analysed in relation to species composition and abundance, geographic and seasonal distribution and size of stranded animals and gender.No attempts have been made to explain the cause of strandings except in general terms.

Material and methods
Records of marine mammals and turtles stranded on beaches in the study area were collected from several sources; mainly comprised by volunteers from universities and from the NGO Ecologistas en Acción.Data of this study were recorded from 1991 to 2008.Only some punctual data were recorded before that period.The volunteer network is distributed along the coast forming a marine mammal and turtle stranding network, and allowing performance of an effective stranding time-response in the whole area (fig.1).
The stranding network receives alerts from diverse sources such as state agencies like the police corps and coast guards, an emergency phone number, and also from local residents and tourists who may encounter a dead or injured marine mammal (or turtle).
In case of a stranding event, the network immediately sends the closest volunteer (team) out to confirm the report, investigate the animal, collect data about location, beach morphology, weather conditions, sea conditions and physical condition of the animal (alive or dead), to decide the suitable response.
If the animal is still alive, qualified personnel such as veterinarians and staff members from the rescue centres go to the site to assist the animal with medical care and, if necessary, to transport it to the nearest rehabilitation centre.Some of the work teams do not have qualified personnel at all times.However, all the volunteers are trained in marine mammal health assessment and supportive care, so they are able to proceed with keeping the animal in situ, checking vital signs, informing general public about the situation and waiting for the authorised personnel to arrive (DELPHIS, 2005).
When the stranded animal is dead on the beach (the most frequent case), data are collected according to established protocols (Geraci & Lounsbury, 1993): species identification, general measurements (standard length, head height, body width), body state and body condition.If the body is still in a fresh stage, the authorised team personnel proceed to do a necropsy and collect the samples (tissues, teeth, etc.).Samples are stored and/or delivered to university research groups who are carrying out studies on cetacean and marine turtles (i.e.teeth for age studies, muscle for isotope analyses for trophic research, etc.).

Species
This paper contains data from thirteen cetacean species, one phocid species, and four marine turtle species: D.d.   T. truncatus S. coeruleoalba The eigenvalues of the PCs are the measure of their associated variance; the participation of the original variables in the PCs is given by loadings, and the individual transformed observations are called scores.
A varimax rotation (VF) allows to 'clean up' the PCs by increasing the participation of the variables with higher contribution, while simultaneously reducing the variables with less contribution.Therefore, the number of original variables contributing to each VF is reduced at the cost of a loss of orthogonality.Cluster analysis is an unsupervised pattern recognition technique that uncovers intrinsic structure or underlying behaviour of a data set without making prior assumptions about the data.The objective is to classify the variables, or cases (sampling stations) of the system into categories or clusters based on their proximity or similarity.Hierarchical agglomerative cluster analysis was carried out on the standardised data by means of the Wards method of linkage, using Euclidean distances as a measure of similarity (Massart & Kaufman, 1983).

Cetacea
Table 1 and 2 show the data of strandings obtained from 1991 to 2008 (with some punctual data of strandings occurring before this period) in six areas on the coast of the Alboran Sea and Strait of Gibraltar.A total

Study area
The Alboran Sea is the most western area in the Mediterranean Sea.The western boundary is the Strait of Gibraltar, and the Eastern end is a line drawn from the Gata Cape (Almería) to the African coastline.In the Alboran Sea, upwellings take place, providing nutrient enrichment of the surface waters (Reul et al., 2005), and thus making this area one of the most productive regions in the Mediterranean Sea (Cañadas et al., 2002).Furthermore, it is an important route for migratory species (such as cetaceans and marine turtles) between the Atlantic Ocean and the Mediterranean Sea (DELPHIS, 2009).This makes the Alboran Sea region rich in cetacean and turtle diversity, with stable (Gómez de Segura et al., 2006) and migratory populations (Castellote et al., 2010).The study area is shown in figure 1.

Statistical analysis
Principal component analysis and cluster multivariate analysis were performed using the software Statistica 6.0 (StatSoft ® ).Principal component analysis (PCA) enabled ascertainment of associations between variables, thus reducing the dimensionality of the data table.This reduction is accomplished by diagonalisation of the correlation matrix data, which transforms the 'n' standardised original variables into 'n' uncorrelated (orthogonal) ones (weighed linear combinations of the original variables) called principal components (PCs).  .This is the widest compilation of stranding data to date in the study area.These data may also be used as an approximation to which species are present in the study area, but never as an approximation to a size of population, because the number of beached animals depends on several factors, such as habitat (more or less close to the platform), feeding behaviour, impact factors, etc., and they are not only linked to number of members.

Spatial distribution
Figure 2A shows the percentages of stranding of each species.The data have been standardised with respect to the total number of strandings to avoid errors in comparisons.The species that stranded most frequently were dolphins (striped and common), followed by the pilot whales (Risso's dolphin and long-finned pilot whale).
The striped dolphin was the most abundantly stranded (34.3%) cetacean species in the western Mediterranean.Common dolphins were common two decades ago, but the continuous incidental killings of common dolphins in some areas such as the Alboran Sea and the Strait of Gibraltar may have caused a significant decline even when the population was still abundant (Forcada & Hammond, 1998).In the Andalucian coast, the striped dolphin is catalogued as a 'vulnerable' species, and the common dolphin is catalogued to be at 'critical risk' (Libro Rojo de los Vertebrados Amenazados de Andalucía, 2001); this indicates that the high number of deaths may be important for the conservation of the species.
Other species are uncommonly stranded; however, some strandings were maintained over the years (e.g.Balaenoptera physalus).A significant point to highlight in this study is the first stranding record of the species Sowerby's beaked whale in the Gulf of Cadiz, according to the authors' knowledge and bibliography.
There was a remarkably high occurrence of stranding of pilot whales in Almeria in 2007 (seven cases).According to Fernández et al. (2008) this was due to a morbillivirus epizootic.The increase in strandings of Cuvier's beaked whales in Almeria since 2005 is also interesting.
In 2003, in Morocco, a program was carried out to monitor the dolphins captured in fishing nets.These data are accounted together with the normal data of strandings for that year.
Figures 3a shows a comparison between the strandings that occurred in the north coast, Alboran Sea and Strait of Gibraltar (Andalucian coast), and the south coast (Ceuta and Melilla).The data have been standardized with respect to the total number of strandings on each coast (where total stranding cases on each coast were equal to 100).It was found that for the species with a high number of strandings (dolphins and pilot whales) there was a difference in frequency on the beached animals; dolphins stranded more on the south coast (although the difference was not significant, 89% vs. 86%), and pilot whales stranded more on the north coast (8.2% vs. 4.3%).This could be due to the distribution patterns in the study area and/or the oceanographic water circulation.
Table 3 shows the results of the factorial analysis (PCA) to establish the determinant factors for location and species variables of the strandings.In the case of locations, there were two principal factors that were related with the north and south coasts.In the case of species, there were two principal factors: one of them related with the two species that stranded more frequently (common and striped dolphin), and the other related to the remaining species.
Figure 4A shows cluster analysis results for the associations between the strandings of the different species.For this analysis, the results of factorial analysis by species (table 4) were taken into consideration.The most important factor in this analysis was the delphinid species, possibly due to their representative number of cases.Two well-differentiated groups were found in the cluster analysis: one of them with the common dolphin, striped dolphin and unidentified dolphin (because it is one of the precedent species), and the other group included the rest of the delphinid species.These two groups were representative of the stranding frequency.
Figure 4B shows the zoning of the study area according to the strandings that occurred.Cluster analysis was carried out using the components of the two factors by species.Figure 4 shows that south zones were highly related and constituted a group.Northern areas did not make a differentiated group, but certain trend in strandings may be noticed.Further studies would be necessary to corroborate that trend.

Temporal trends
Figure 5 shows the temporal trends of strandings of different species (the data have been standardized with respect to the total strandings of each species).These temporal trends were only made for those species with more than 10 recorded animals.
During the study period, most of the strandings occurred in spring; however, data were not analysed by season.Future analysis would be necessary to show whether different seasonal trend patterns exist.

Turtles
Table 2 shows the data obtained for the period from 1991 to 2008 (with some punctual data recorded before this period) in six locations on the coasts of the Alboran Sea and the Strait of Gibraltar.Four species      were found stranded in the study area.Data were grouped by location (table 2).A total of 574 animals were recorded and this is also the widest compilation recorded in the area to date.These data may also be used as an approximation of knowledge of the species present in the study area, but not as an approximation of population abundance.Loggerhead sea turtle and leatherback turtle were the most frequent and abundant species in the Western Mediterranean (92.9% and 7.8% respectively).Two other species were found on the beaches, C. mydas and L. olivacea.These strandings were considered 'rare' in this area; the first one because the population was located in the Eastern Mediterranean, and the second was an extremely rare stranding because in the Mediterranean Sea it is considered neither a migration nor resident species in the area.Both species only occurred once in the study period.

Spatial distribution
Figure 2B shows the percentages of strandings for each species (data are standardized for comparisons).The species that beached most frequently (more than 90%) was the loggerhead sea turtle, followed by the leatherback turtle.
Figure 3B shows a comparison between the strandings occurring on the north coast and the south coast of the Alboran Sea and the Strait of Gibraltar.Data have been standardized with respect to the total strandings on each coast (total strandings on each coast is equal 100).The results for the most abundant and representative species (loggerhead sea turtle and leatherback turtle) revealed slight spatial difference in frequency of the beached animals: the loggerhead sea turtle stranded more on the north coast (although the difference was not significant, 93.3% vs. 82.5)and the leatherback turtle stranded more on the south coast (5.4 vs. 17.4%).The reasons for this could be due to the distribution patterns of each species in the study area and/or by the oceanographic characteristics.
In this case, the factorial analysis was not used because there were only two factors (the two main species).Cluster analysis was used to zone the study area according to stranding occurrence (fig.4C).Cluster analysis was carried out using the two main species.Figure 4C shows how southern areas were highly related and formed a group (including one of the northern areas).The north area did not make a differentiated group, but as found in the cetacean analysis, the cluster analysis showed a certain trend.Further studies would be necessary to contrast that trend.

Temporal trends
Figure 5B shows the temporal trends of the two main species.Data were standardised with respect to the total stranding of each species.These temporal trends were only obtained for those species with more than 10 stranding events.Over the years, most of the strandings occurred in summer; however, data for this study were not analysed by seasons.Future analysis will show whether there are patterns in these trends.
Although little information is available to determine the causes of these deaths, the reason appears to be mainly human induced for the marine turtles, but cetacean deaths were less clear.This paper does not attempt, however, to explain the causes of mortalities.

Conclusions
This study is the widest compilation made to date of cetacean and sea turtles stranded in the Strait of Gibraltar-Alboran Sea: 1,198 strandings of cetaceans and 574 strandings of sea turtles were recorded.Thirteen species of cetaceans, one species of pinnipeds and four species of sea turtle were identified.Two of these species were recorded for the first time in the area of Cadiz (Mesoplodon bidens and Lepidochelys olivacea).A trend can be observed in the strandings for cetaceans and sea turtles.There are two differentiated areas: the north coast and south coast of the study area.This zoning could be due to the distribution patterns of the species in the study area and/or to oceanographic characteristics.Further studies with future data will provide information to ascertain whether the observed variations were isolated events or part of a defined zoning.For cetaceans, specifically in the case of delphinids, two groups can be defined according to stranding occurrence; one of them is formed of common and striped dolphins, and the other group consists of the remaining delphinids.The first group was by far the most important group of cetaceans that stranded in the study area.

Fig. 1 .
Fig. 1.Study area indicating the location of volunteer groups.

Fig. 3 .
Fig. 3. Comparison between strandings recorded on the north and south coasts.(Species codes are indicated in Material and methods section.)Fig. 3. Comparación entre varamientos registrados en la costa norte y en la costa sur de la zona de estudio.(Los códigos de las especies se encuentran indicados en la sección Material and methods.)

Fig. 4 .
Fig. 4. Cluster analysis results by cetacean species (A); by location, taking cetacean species into consideration (B); and by location, taking turtle species into consideration (C).