1. Introduction
Social behavior is a fundamental feature of many animal species, assuming an important role in the development of their behavior and fitness outcomes [
1,
2]). Among the distinctive characteristics of animal social groups there are complex, dynamic and nonrandom patterns of social interactions and relationships among members of society [
3,
4], resulting in a population’s social structure. Studying the social structure of a population is one way to obtain useful information on its behavior and ecology and how that population will react to internal and external stimuli. It may affect population growth, genetic make-up, the way diseases spreads, pathways of information transfer and the way animals exploit their environment and move around [
5,
6,
7,
8]. Otherwise, the social structure can itself be influenced by intrinsic factors, such as the presence or absence of preferred associates, or by extrinsic habitat characteristics, such as prey availability, landscape complexity and anthropogenic disturbances [
9,
10,
11,
12]. Thus, incorporating social structure information results is a key determinant in population dynamics and may help to define management units of conservation of endangered species [
13,
14,
15].
Since the 19th century the study of social structures has become widely diffused among the scientific community and behavioral researchers have begun to incorporate this aspect into robust models, developing tools and novel methodologies in order to better understand and describe animal societies [
16,
17,
18,
19,
20,
21,
22,
23]. Initially, this approach was principally applied to primates (i.e.,
Pan paniscus [
24],
Pan troglodytes [
25]) and then spread to other vertebrate species with high levels of social complexity, such as bat (i.e.,
Thyroptera tricolor [
26]), giraffes (i.e.,
Giraffa camelopardalis [
27]), elephants (i.e.,
Loxodonta africana [
28]) and cetaceans (i.e.,
Stenella frontalis [
29],
Sousa chinensis [
30] and
Grampus griseus [
31]). Concerning the methodologies applied over time to study social aspects it has developed from relationship-based approaches [
32,
33,
34] to social-network analysis [
16,
35,
36].
Among cetacean species, the common bottlenose dolphin
Tursiops truncatus (Montagu, 1821) is the most studied species concerning aspects of their social structure [
15] due to its wide distribution [
37,
38,
39] especially in coastal areas that are relatively easy to access and monitor. In the Mediterranean Sea, the species is regularly present and is usually distributed within the limits of the continental shelf (<200 m) [
40,
41]. Common bottlenose dolphins have even been found above the shelf-break in the western Mediterranean Sea and in the Northern Ionian Sea, suggesting the possible occurrence of an offshore ecotype [
42,
43,
44]. Due to its coastal habits, the common bottlenose dolphin is affected by several anthropogenic pressures [
45,
46]. Historical intentional killing, bycatch, habitat loss and degradation, prey depletion marine traffic and marine pollution are the main contributors to the decline in the Mediterranean sub-population of common bottlenose dolphins, resulting in a reduction of more than 30% over the last 60 years [
47]. Even though the Mediterranean sub-population of the common bottlenose dolphin was assessed by the IUCN as Vulnerable in 2012, on the basis of the criterion A2cde, with evidence of a declining trend in its population [
48], more recently its status has been downgraded to Least Concern [
49,
50]. Nevertheless, this evidence bodes well; however, many aspects need to be considered to assess an actual improvement in the welfare of this population, especially in a closed and strongly anthropized basin, such as the Mediterranean Sea. The occurrence of a genetically differentiated Mediterranean sub-population (i.e., the critically endangered common bottlenose dolphin found in the Ambracian Gulf and Greece [
51]) shows the need to deepen the knowledge of the culture and the social tendencies of local units, which may not only lead to a differentiation into ecotypes but also into a haplotypic separation of putative metapopulations [
41,
52].
This study provides insight into both the social structure and the temporal distribution of the common bottlenose dolphin living in the Gulf of Taranto (Northern Ionian Sea and Central Mediterranean Sea), combining a social-network analysis (made with some of the most novel tools, such as the social network analysis [
16,
35,
53]) with a more exhaustive analysis of site fidelity and residency patterns in the study area, in order to provide effective indications supporting the future management actions for the species and the mitigation of human impacts on the marine ecosystem. The characterization of bottlenose dolphin populations living in the Gulf of Taranto could prove to be highly relevant for the area, which is characterized by high levels of urbanization, intense fishing activity, commercial and cruise shipping traffic as well as the occurrence of heavy industries, naval exercises and offshore wind farm areas [
54,
55]. Over the past 15 years, common bottlenose dolphins were the focus of various studies in the Gulf of Taranto regarding their abundance and distribution [
56,
57,
58], photo-identification [
44,
59], bioacoustics [
60], evidence of interaction with sharks [
61] and dolphin-fishery competition [
54,
62,
63]. However, little is known about the social structures of the species in this area or its movement variability over space and time.
3. Results
3.1. Data Collection
From July 2013 to September 2021, a survey effort of 1055 h of observation and 7385 nm of navigation was performed providing 216 sightings of bottlenose dolphin (details of effort distribution over the years are reported in
Table 1). Surveys were carried out during the whole year but the effort was differently distributed over the seasons: 65% of surveys in summer, 19.5% in spring, 14% in autumn and 1.5% in winter. The sightings occurred in a depth range from 2 to 900 m with a mean value of 125 ± 147 m, and the group size ranged between 2 to 25 individuals with a mean group size value of 8 ± 5 specimens. Moreover, twelve sightings of a single individual occurred during the study period.
3.2. Photo-Identification
Photo-ID data were collected in 130 daily surveys. The number of sightings with photo-ID data increased during the year as shown in
Table 1, allowing for the identification of more than 60% of the encountered animals in each sighting from 2016. The cumulative number of identified individuals from 2013 to 2021 is shown in
Figure 2. The curve obtained grows sharply over the study period without reaching a plateau.
Once the quality and distinctiveness criteria were applied, it was possible to identify and catalog 141 specimens thanks to the natural marks and cuts or deformities on the edges of the dorsal fin. Among them, 34 individuals were sighted only once and 107 were re-sighted from 2 up to 31 times, with a mean value of re-sightings of 5 ± 5 times. In detail, 25 bottlenose dolphins were re-sighted in one year, 31 were observed in two or more consecutive years and 51 in two or more non-consecutive years. Sixteen dolphins were unequivocally sexed as female and none as male.
3.3. Site Fidelity
The monthly sighting rate of bottlenose dolphins varied between 0.026 (sighted only in 1 month) and 0.410 (sighted up to 39 months), with a mean value of 0.087 ± 0.078. The yearly sighting rate varied between 0.111 (sighted in 1 year) and 0.778 (sighted up to 9 years), with a mean value of 0.247 ± 0.161. The seasonal rate ranged from 0.048 (sighted during 1 season) to 0.476 (sighted in up to 21 seasons), with a mean value of 0.138 ± 0.107. Values of the relative span time index ranged from 0.000 (sighted only once) and 0.990, with a mean value of 0.254 ± 0.279.
The Elbow method identified three as the optimal number of clusters in which to group individuals (
Figure 3). The dendrogram provided by the application of the agglomerative hierarchical cluster analysis clearly highlighted three well defined clusters, including 59, 20 and 62 individuals, respectively (
Figure 4,
Table 2). Cluster 1 included dolphins never re-sighted, or only re-sighted in one year with a low mean value of monthly (0.032 ± 0.012), yearly (0.111 ± 0.000) and seasonal (0.055 ± 0.017) rate and a low mean value of the relative span time index (0.003 ± 0.006), resulting in transient individuals. Cluster 2 included dolphins re-sighted from one year up to 9 years, with relatively high mean values of monthly (0.242 ± 0.066), yearly (0.556 ± 0.088) and seasonal (0.359 ± 0.057) rate and a high mean value of relative span time index (0.634 ± 0.160), resulting in seasonal resident individuals. Cluster 3 included all dolphins with intermediate mean values of monthly (0.088 ± 0.037), yearly (0.278 ± 0.077) and seasonal rate (0.145 ± 0.047) and an intermediate mean value of relative span time index (0.370 ± 0.220), resulting in visitor individuals
3.4. Residency Pattern
For the residency-pattern analysis, only individuals re-sighted at least three times were considered, resulting in 114 sampling periods out of 130 and 55 identified individuals out of 141. The lagged identification rates began to fall within 10 days, suggesting that the common bottlenose dolphin population of the Gulf of Taranto is characterized by some emigration or mortality events (
Figure 5). Following the fall, LIR started to level off again and stabilize after 100 days, indicating emigration from and re-immigration events into the study area. Indeed, the most parsimonious model representing the population, according to QAIC, is the emigration + reimmigration model (
Table 3). This result suggested a mixed population of resident and transient individuals.
3.5. Association Pattern and Social Structure
For the association pattern and the social-structure analysis, only surveys with more than 50% of identified individuals out of the total number of sighted individuals were considered, resulting in 95 sampling periods out of 130 and 133 identified individuals out of 141. The second selection criteria applied (i.e., number of re-sightings > 3) resulted in 89 sampling periods and 48 individuals used for this analysis. The mean value of half-weight association index ranged from 0.06 to 0.21, with an overall mean value of 0.11 ± 0.04. The individual labeled as Tt 41 showed the highest mean value of the HWI (mean HWI = 0.21), followed by Tt 113 (mean HWI = 0.19), Tt 117 (mean HWI = 0.18) and Tt 118 (mean HWI = 0.17). The estimate of social differentiation suggested a differentiated society (S = 1.030) and the correlation coefficient between the real and the estimated association was 0.641, indicating a good power of the analysis. The results of the permutation tests on possible preferred or avoided associations in the population show a significantly higher value of SD (SD 0.18231, random SD 0.00018, p > 0.9999) and CV of association indices (CV 1.6060, random CV 0.00161, p > 0.9999), indicating that occurrence of long-term preferred companionship is present in the population.
The hierarchical cluster analysis highlighted the occurrence of four clusters consisting, respectively, of 3 (cluster 1), 16 (cluster 2), 21 (cluster 3) and 8 individuals (cluster 4) (
Figure 6). The mean values of HWI within each cluster are shown in
Table 4. Within clusters 1, 2 and 3 a certain degree of association was shown, whereas cluster 4 was completely independent from the others, as highlighted by the estimation of mean value of HWI between different clusters (
Figure 6,
Table 4). The maximum modularity was 0.489 at HWI 0.158 and the cophenetic correlation coefficient was 0.897, indicating a good representation of bottlenose dolphin society in clusters.
The SLAR indicated that the most parsimonious model was that of preferred companions plus casual acquaintances among dolphins (
Figure 7,
Table 5). Indeed, the SLAR falls but stabilizes above the null association rate over the period, suggesting a situation in which units have a permanent core membership but there are also floaters who move between units.
The social network analysis highlighted the occurrence of 4 clusters (
Figure 8,
Table 6). Clusters 2 and 3 showed high values of strength, reach, eigenvector centrality and affinity, highlighting how well individuals within these clusters are connected with the others, playing a key role in the society. In Cluster 4, the eigenvector centrality was zero, confirming the poor connection of individuals in this cluster with the others. In particular, the social network graph clearly shows two different social groups in which the strength is represented by the size of each node. Tt 41 was the individual with the highest strength (9.73) and reach (63.35), followed by Tt 1139.09 and 62.51, respectively, Tt 117 8.39 and 58.21, respectively and Tt 118 8.13 and 57.52, respectively. Tt 113 was the individual with the highest eigenvector centrality, Tt57 had the highest clustering coefficient, and finally Tt 119 was the one with the highest affinity. Moreover, in
Figure 8 each individual is characterized by a different shape according to the site fidelity group division, showing the key role of Tt41 as a resident of the area and of Tt 113, Tt 117 and Tt 118 as visitors.
4. Discussion
This study provides valuable information about the temporal ranging pattern of the common bottlenose dolphin occurring in the Gulf of Taranto and its social structure, which is investigated through an integrated approach that includes the analysis of site fidelity indexes and the analysis of the social structure. In detail, this study tries to integrate the information obtained from individual analyzes to increase our knowledge on their use of habitats and their habits in the Gulf; enabling a better understanding into whether individuals sighted in the surveyed area live there permanently, or if they have selected the area as a habitat to return to assiduously over time, during one or more specific seasons. Moreover, social-structure analysis allows us to better understand the occurrence of social units and how they interact with each other. This information is crucial to address specific measures for their protection, especially in a basin affected by several anthropogenic pressures [
54,
55].
The sightings of the common bottlenose dolphin in the study area were distributed over a depth range from 2 to 900 m. According to [
40], the Mediterranean population of bottlenose dolphins is often considered as a ‘coastal’ species, mostly encountered in the continental shelf and shallower waters. However, in some areas of the Mediterranean Sea, such as the Alboran and Balearic seas or the Strait of Gibraltar, they can occur on the continental slope and in productive waters ranging from 200 to 600 m deep, i.e., [
113,
114]. In the Gulf of Taranto, as already reported by Santacesaria et al. [
44], common bottlenose dolphins are also found over the steep slope in the deep waters of the ‘Taranto valley’. Moreover, photo-identification data previously analyzed (until 2018 by Santacesaria et al. [
44] and here updated, suggested the presence of two groups of bottlenose dolphins geographically separated: A “coastal” group distributed in a depth range from 2 to 277 m, and a “pelagic” group in a depth range from 375 to 900 m. In particular, these two groups are separated not only geographically but also socially, as highlighted by the social-network analysis, enforcing the assumption of a different ecotype, even if specific genetic analysis have to be performed to make this assumption official. Some studies have reported cases of spatial or temporal segregation of bottlenose dolphin populations within the Mediterranean Sea, suggesting ecological specialization as one of the main drivers in the foraging activity, possibly including opportunistic feeding on the discards from different fishing activities [
41,
115]. Other factors, such as habitat productivity, predation risk and human activities could also be considered responsible for the differences seen in the social segregation and the organization of bottlenose dolphins [
30,
115,
116]. In the Gulf of Taranto, one of the main drivers of this separation could be the presence of several maritime and land-based human activities. For instance, the intense fishing exploitation recorded within this area, from the coastal waters to about 800 m in depth, could influence the occurrence and the distribution of common bottlenose dolphins; when considering that this species shows a consistent food resource overlap with passive nets and longlines that are used to catch sparids, mullet, European hake, red mullet and small pelagic fishes [
62]. However, results of several studies carried out to assess dolphins-fishery interactions indicate a condition of low competition in the Gulf of Taranto [
54,
63]. Thus, further, and specific studies are needed in order to evaluate the diverse factors of this separation.
Concerning the photo-ID data, a total of 141 individuals were uniquely identified and cataloged thanks to the presence of natural marks, cuts or deformities on the edges of their dorsal fin. About 76% of the identified individuals were re-sighted from 2 up to 31 times and among them about 77% were re-sighted in different years, suggesting a certain degree of stability in the use of this habitat. According to the site fidelity analysis, 20 individuals are seasonal residents within the study area. Despite these individuals showing the highest value of monthly and seasonal sighting rates, they never reach the maximum value of 1 due to the reduction in the survey effort during the colder months. Therefore, these individuals are considered seasonal residents. However, the presence of individuals who reside for part of the year and return in this area confirms that the Gulf of Taranto is a critical habitat for the species, as already suggested for other cetacean species, such as striped dolphin
Stenella coeruleoalba (Mayen, 1833), Risso’s dolphin
Grampus griseus (Cuvier, 1812) and sperm whale
Physeter macrocephalus (Linnaeus, 1758) [
54]. The presence of 121 individuals, including transients and visitors as well as the results obtained from the residency-pattern analysis, suggest classifying the local population as an open population this is characterized by emigration and reimmigration events. In addition, the presence of visitors and transient dolphins also highlights that the Northern part of the Gulf of Taranto might only be part of their distributional range.
For the social-structure analysis, only 48 individuals were used in order to ensure its robustness. Despite the relatively low value of the overall mean half-weight association index (0.11 ± 0.04), the rejection of the null hypothesis, indicating non-random associations and the temporal analysis made with SLAR suggest the presence of both extremely fluid and stable associations between individuals. This outcome is in accordance with the results of the residency-pattern analysis, which suggests a mixed population of resident and transient individuals. In fact, longer-lasting associations can also be explained by the distribution pattern of individuals. According to [
116], all populations of bottlenose dolphin have a fission-fusion grouping pattern in which individuals are associated in small groups that change in composition on a daily basis. Our findings confirm that the Gulf of Taranto bottlenose dolphin population is also represented by a fission–fusion social structure and, as reported for other areas within the Mediterranean Sea [
12,
111,
117,
118,
119,
120], a certain degree of social organization based on sex-specific bonds should be considered
The association pattern and the social-network analysis highlight the occurrence of 4 social units, of which three (clusters 1, 2 and 3) are connected to each other in different degrees and one (cluster 4) that is completely separated. In particular, clusters 1 and 3 are characterized mostly by visitors (3/3 individuals and 11/21 individuals, respectively). Cluster 2 is characterized mostly by resident individuals (11/16) (
Figure 6). These three clusters include individuals distributed at a mean depth of 81 m, suggesting a coastal habitus, whereas eight visitor individuals belonging to cluster 4 were sighted at a mean depth of 450 m, suggesting a preference for the pelagic group. In addition, Tt57, a member of the ‘pelagic group’, is the individual with the highest clustering coefficient, suggesting its membership to a tight, closed and homogeneous social unit. These data highlighted a separation of the ‘pelagic’ group not only from a geographical but also a social point of view.
Among individuals belonging to the connected social units, Tt 41 and Tt 117 with its juvenile Tt 118, have the highest values of mean half-weight association index, strength, eigenvector centrality and reach. The tendency of these two females and of the juvenile to form several and/or stronger associations with other individuals emphasizes their role as bridge nodes between three social units, which interact with each other thanks to a few individuals, both of which are seasonal residents and visitors. According to Connor et al. [
116], all populations of bottlenose dolphin have a fission-fusion society where individuals join and leave groups in a flexible manner, such that group size and composition change frequently on small spatial and temporal scales to rapidly respond to the interaction with ecological variables. These findings confirm that bottlenose dolphins occurring in the Gulf of Taranto is also represented by a fission–fusion social structure, but further study must be conducted in order to investigate whether there is a certain degree of social organization based on sex-specific bonds.
5. Conclusions
According to the Habitats Directive, for species listed in Annex II, such as the bottlenose dolphin, it is required to create SAC (Special Areas of Conservation), sites of Community importance that ‘contribute significantly to the maintenance or restoration at a favorable conservation status, of the habitats or populations of the species for which the site is designated’. Considering our results, the Northern part of the Gulf of Taranto, in both coastal and pelagic areas, should be considered as a critical habitat for this species and therefore a SAC should be designed. However, the institution of a SAC only in the study area could be insufficient for the conservation of the species. Indeed, the population studied is characterized by several emigration and immigration events and the waters within the study area seem to represent only a portion of a wider range used by these animals. Moreover, since data suggest a fission-fusion social structure, the local population of the bottlenose dolphin is not isolated or socially segregated, thus the potential gene flow from individuals entering the area is pivotal to maintaining variation and enhancing its conservation.
Thus, more investigations are needed and the development of a specific conservation plan for the species in the whole Gulf of Taranto is required as well as further studies aimed to better characterize two geographically and socially segregated units.