A comprehensive continuous five-year dataset was used to investigate group size variation in a highly social mammal, the bottlenose dolphin, in a highly impacted coastal area. This study reveals that both social and oceanographic conditions – both on a small-scale (water oxygenation and thermal stratification) and large-scale (NAO index) are related to the spatio-temporal aggregation patterns of bottlenose dolphins. It is well established that environmental changes can condition the phenology and demography of animals, but few studies have recorded such an influence on marine top predators. The current study therefore contributes to the growing body of literature on how environmental change, occurring at different spatio-temporal scales, is indirectly related to the social behavior of a marine top predator by influencing the abundance of its prey.
Findings of this study highlight the importance of year-round monitoring to identify possible environmental changes affecting bottlenose dolphin group dynamics over differing spatial and temporal scales. Modeling analysis reveals that bottlenose dolphin group dynamics were linked to both small-scale oceanographic variation and large-scale climatic variation. The observed link between these variables and dolphin group size is likely associated to changes in the availability of dolphin food resources (Lusseau et al. 2004). Bottlenose dolphins are known to feed on a variety of schooling fish species such as blue whiting (Micromesistius poutassou), European pilchard (Sardina pilchardus), common grey mullet (Mugil cephalus), Atlantic horse mackerel (Trachurus trachurus), and European seabass (Dicentrarchus labrax) (Díaz López 2009; Santos et al. 2007), whose availability in the study area varies both in space and time (Banon et al. 2010). When environmental conditions in specific zones lead to a low availability of schooling prey, bottlenose dolphins could therefore form smaller groups while foraging to reduce inter-individual competition (Methion and Díaz López 2020). Smaller groups may also be advantageous when prey items occur singly, and cooperative or coordinated foraging is inefficient (e.g., Heithaus and Dill, 2002; Mann and Sargeant 2003). In contrast, dolphins could increase prey-finding and capture abilities by forming large groups when the environmental conditions (well-oxygenated waters with high thermal stratification) facilitated a higher availability of schooling fish.
Water temperature stratification and concentration of dissolved oxygen indeed play a fundamental role in fish dynamics in coastal ecosystems, impacting the ecology of fish species (Ware and Thomson 2005; Stevens et al. 2006). Dissolved oxygen is an important factor affecting the distribution and abundance of both demersal and pelagic fish communities (Howell and Simpson, 1994), with fish diversity and abundance increasing in well-oxygenated waters (Mas-Riera et al. 1990; Howell and Simpson 1994). Similarly, thermal stratification affects the vertical distribution and horizontal movement of marine fish by acting as a barrier to vertical migration (Birtwell et al. 2003). The combination of well-oxygenated waters (found close to the sea surface) and a high thermal stratification (Álvarez-Salgado et al. 1993) could induce the presence of large schools of fish close to the sea surface which might also lead to the occurrence of large bottlenose dolphin groups. Direct behavioral observations during this study (S.M. and B.D.L., personal observations) confirm the presence of large fish schools often concentrated in the first meters of the water column (characteristic of the distribution of schooling fish) during feeding events of large groups of bottlenose dolphin.
The significant relationship between the NAO index and bottlenose dolphin group size provides further support to the relationship between large-scale climate indices and variation in grouping patterns in marine top predators. The NAO is a dominant mode of climate variability over the North Atlantic which can exert a strong influence on numerous marine organisms through changes in ocean temperature and salinity as well on vertical mixing and circulation patterns (Drinkwater et al. 2003; Hurrell and Deser 2009). Here, bottlenose dolphin group size was largest with neutral NAO values and this relationship is likely associated to changes in bottlenose dolphin resources availability. The NAO index has indeed been linked to variation in assemblage composition, abundance and growth of marine fish (Attrill and Power 2002; Baez et al. 2011). In Galicia (NW Spain), the NAO has mainly been linked to precipitation, river flow and water resources (Lorenzo and Toboada 2005). Particularly, positive trends in NAO values correspond to cold and dry winters, therefore contributing to a significant decrease in freshwater discharge in the rias in winter (Trigo et al. 2004). On the contrary, a negative trend in the NAO values corresponds to warm and wet winters, contributing to a significant increase in freshwater discharge (Trigo et al. 2004). Significant variation in freshwater discharge in the study area could lead to a decrease in bottlenose dolphin prey availability and/or a change in prey type, which may in turn drive bottlenose dolphins to form smaller aggregations to reduce inter-individual competition. In Scotland and in Canada, cetacean group size also varied from year to year in relation to large-scale climate variation, and local indices of prey abundance were linked to both climate indices and dolphin group size (Lusseau et al. 2004). These similar effects of climate variation on the aggregation patterns of coastal cetaceans provide further evidence that the effects of climate variation can filter up to higher trophic levels by altering the social structure of top predators.
If environmental drivers of prey availability are related to bottlenose dolphin group size, these variables would be linked to the decision individuals have to make to stay or leave the group therefore guiding the structure of dolphin social community and inducing changes in their dispersal rate, survival or reproduction (Lusseau et al. 2003). The observed aggregations of this study (mean = 10.7 ± SE 0.3) are larger than the average group size in other coastal bottlenose dolphin populations (e.g., California, US = 8.8, Bearzi 2004; Shannon Estuary, Ireland = 8.5, Berrow et al. 2012; Kvarneric bay, Croatia = 6.8, Bearzi et al. 1997; Sarasota, US = 4.8, Irvine et al. 1981; Golfo Aranci, Italy = 4.4, Díaz López 2019; but see Moray Firth, Scotland = 14.2, Robinson et al. 2017 and Doubtful Sound, New-Zealand = 17.2, Lusseau et al. 2003), which might be due to differences in food availability and predation risk. In the coastal waters of North-West Spain, bottlenose dolphins are not known to have natural predators (Methion and Díaz López 2018) and the area is highly productive because of upwelling enrichment and land runoff, contributing to a significant abundance of bottlenose dolphin prey species (i.e., European pilchard, blue-whiting, and Atlantic horse mackerel) (Giralt Paradell et al. 2021; Santos et al. 2007; Tenore et al. 1995). This large food availability likely minimizes competition between individuals to access resources, and facilitates prey capture through cooperation, therefore helping bottlenose dolphins to maximize their energy intake. Previous studies in the study area in fact indicated that these bottlenose dolphins use different foraging techniques, including cooperative feeding, which involve a high degree of social organization and behavioral adaptation (Methion and Díaz López 2019, 2020).
In this study, we did not find a direct relationship between monitored anthropogenic activities (marine traffic, fisheries and aquaculture) and the size of bottlenose dolphin aggregations. This could be explained by the fact that these human activities, despite causing changes in the surrounding environment, do not directly condition the availability (both in type and quantity) of dolphin prey as much as oceanographic variables (i.e., oxygenation and thermal stratification of the water).
Bottlenose dolphin group dynamics are likely driven by multiple factors, and other variables such as behavior, parental care, and protection from predators and conspecifics (Gowans et al., 2008) may act synergistically with environmental parameters. The observed link between dependent calves (new-born and immature dolphins) and bottlenose dolphin group dynamics is in concordance with previous studies reporting larger groups in the presence of dependent calves (Gibson and Mann 2008; Kerr et al. 2005; Bearzi et al. 1997; Díaz López 2012). As several cases of infanticide have been reported in this area (Díaz López et al. 2018b), the formation of large groups likely increase calf protection from conspecifics by reducing the probability that a calf be attacked by other conspecifics (through both the dilution effect and the detection effect). On the other hand, forming large groups may also allow mothers to spend a greater proportion of time foraging to maintain the increased energy required for lactation by being assisted by other females in caring for their calves. In addition, by being part of larger groups, nursing females may benefit from an increased ability to search for and catch fish that aggregate in large schools thanks to cooperation with other group members, therefore ensuring sufficient energy intake for nursing. Further studies about parental care, alloparental care and cooperation could help develop a better understanding on grouping patterns in bottlenose dolphins.
This study identifies a link between environmental changes and social behavior in a top marine predator and illustrates the importance of using multiple variables at different scales to explore the factors that shape animal societies. The findings provide valuable information on how bottlenose dolphin grouping patterns are linked to both fine-scale and large-scale environmental changes and suggest that dolphin group size could act as a useful indicator of environmental change in coastal ecosystems. As with previous studies using regression techniques, this study has, however, the limitation of not being able to demonstrate causal links between environmental variation and dolphin grouping behavior. The observed fluctuation in dolphin group size could also be driven by unmeasured oceanographic events occurring at different temporal and spatial scales than the ones monitored in this study (e.g., outside the Ría de Arousa and in periods of time previous to the research). Further studies with larger temporal and spatial scales would therefore allow a better understanding of dolphin grouping patterns associated with broader environmental changes.