The bottlenose dolphin (Tursiops truncatus
; henceforth ‘dolphin’) is a social species that lives in fission–fusion societies [1
] and can develop long-term associations between individuals [3
]. Under professional care, dolphins engage in a variety of social and solitary activities, which vary due to factors including, but not limited to, the time of day, the composition of the group, and age [9
]. However, less is known about the relationships between adult female dolphins as well as the maternal care and behavior of dependent juveniles. Observing behavioral and association patterns can be used to inform management decisions regarding the animals’ environments, social groups, health, and husbandry practices [13
Various factors must be considered when evaluating these patterns, including temporal oscillations in behavior changes. Specifically, dolphins engage in more social, sexual, and play behaviors in the mornings and early afternoons when compared with the late afternoons [16
]. In addition, dolphins under professional care are more active during the day than at night [12
]. During the day, dolphins spend the majority of their time engaging in low intensity swimming, low intensity playing, and social play [12
]. In cetaceans, affiliative behaviors, such as social play, rubbing, and synchronous swimming, are considered behaviors indicative of positive welfare [9
]. In addition, social play behaviors are inversely related to agonistic behaviors [18
], which are reported to occur at relatively low rates under professional care [25
Group composition is another important factor that may influence association patterns and activity levels. Dolphin calves and juveniles may influence both the social activities and behavioral patterns not only of their mother but of the entire social group. Dolphins have prolonged nursing and association periods, which can last up to three to six years [1
] and generally follow a pattern of very high levels of care at birth with a slow decline in maternal care over several years as the offspring gain independence [29
]. Similarly, the rate of nursing decreases as calves age [29
Despite the extended association and nursing period, research examining the influence of juveniles on social groups under professional care is limited. Mother–calf dyads spend between 24.67 and 65.28% of their time together during the calves’ first year of life [30
] and the association between dyads remains at a lower yet stable rate in years two and three of life [34
]. During the first year of life, affiliative behaviors are reported between the calf and adult females, often in the form of allomaternal care, as well as with adult males [25
]. Calf play behavior also becomes increasingly social during the first year of life [10
]. Initially, the calf’s mother is their primary play partner, followed by calves of a similar age. Towards the end of their first year of life, age appears to become less relevant in selecting a play partner. Thus, it is possible that dolphin calves diversify the behavior of the adults similarly to the way in which beluga calves increase play behavior in adults [24
Regardless of the extensive knowledge of general activity patterns and the maternal care of calves, little research has focused on the impact juveniles have on the overarching social relationships and activity throughout the day over an extended period of time. The aim of the current study was to examine the activity, relationship strength, and maternal care in an established group of dolphins. Specifically, this study examined: (1) the temporality of social and solitary activities of social groups with and without dependent juveniles; (2) the association patterns relative to group composition; and (3) age-related changes in mother–calf interactions over time. The results from this study provided valuable insights for animal care professionals to make informed decisions on group housing management that can optimize the welfare of all group members based on their individual needs.
2. Materials and Methods
Data were collected from eight dolphins living at Brookfield Zoo in Brookfield, IL, USA. Behavioral observations of this group were collected over a ten-month period. The group consisted of two adult females and their dependent juveniles (mother–calf dyads were D7/D5 and D8/D6), one adult female (D4), two sub-adult females (D2 and D3), and one juvenile (D1) (Table 1
). The habitat consisted of four interconnected areas that could be cordoned off. This allowed the dolphins either to have access to all other individuals while in one large group or to be cared for in subgroups while the dolphins only had direct access to a subset of the other individuals. During the present study, dolphins were regularly maintained in two subgroups with fixed members. One subgroup consisted of the two mother–calf dyads and the other subgroup was comprised of the remaining four dolphins. As other social configurations were rare, those data were excluded from the analysis because there was too little data to analyze.
Although the offspring are classified as juveniles [36
], the term mother–calf dyad will be used to denote their dependent status and continued nursing. Figure 1
depicts the timeline for dolphins entering and being born into the focal group. D8 gave birth to D3 (13 years), D2 (11 years), and D6 (two and a half years), prior to the data collection. D4, an unrelated female, was introduced to D2, D3, and D8 six years prior to the data collection period. D7 was introduced to the group three and a half years before data collection. D1 was born to D4 two and a half years prior to the data collection period. At that time, D4 failed to engage in maternal behaviors and D1 was hand-raised by the animal care staff at Brookfield Zoo. Therefore, D4 and D1 were not considered a mother–calf dyad in the current study. Finally, D7 gave birth to D5 one and a half years before the data collection period.
Both D5 and D6 were nursing and receiving fish as part of their diet at the onset of data collection. The dolphin’s habitat consisted of four interconnected areas: an oblong front area (33.5 × 12.2 × 6.7 m; length × width × depth), two circular rear areas (10.7 × 4.3 m; diameter × depth), and a medical area (7.6 × 2.4 m; diameter × depth).
Behavioral observations were recorded 18 h per week on a randomized, counterbalanced schedule. Direct observations were collected five days a week between 0630 and 1800 h local time from underwater viewing windows. Data were not collected during formal presentations or training sessions. Behavioral data were gathered in 15 min focal follows using the iOS mobile application Animal Behaviour Pro. Behavioral events were recorded using continuous sampling, and swim state was recorded using instantaneous sampling at 60 s intervals. The identification of each dolphin in the group swim was recorded at social swim state sample points. To be classified as a member of a social swim, the individual was required to be swimming synchronously with or interacting with at least one other dolphin (i.e., not in brief proximity). Behavior events, swim states and locations are operationally defined and categorized in Table S1 (Supplementary Materials)
. Operational definitions were adapted, in part, from Dudzinski [37
], Harvey [38
], and Hill and colleagues [23
Reliability was calculated using a combination of live observations and video recordings. Inter-observer agreement was evaluated for 16 live observations (4 h). Intra-observer reliability was evaluated through scoring three one-hour video observations three times over the data collection periods. Reliability was calculated with Pearson’s correlation coefficient and Cohen’s kappa for continuous and instantaneous data [39
]. At least 80% reliability was achieved for inter- and intra-reliability. All behavioral data were collected by the first author.
Data were analyzed and graphed using IBM SPSS Statistics 21, Microsoft Excel (version 16), and Gephi (version 0.9.2). Non-parametric statistics were used due to the small sample size, and differences were considered significant at p
< 0.05. Data were partitioned into groups of nine consecutive observations in order to create blocks of data. In total, there were 42 blocks of data (collected over 10 months) grouped into three phases based on availability of a novel enrichment device. The novel enrichment device was a submerged clear box with a shelf that lowered to release a food reward when a specific amount of weight was added (see Lauderdale and Miller [40
] and Lauderdale & Miller [41
] for details). Phase 1 included the 12 blocks of data collected prior to the introduction of the novel enrichment device. Phase 2 included the subsequent 18 blocks of data during which the dolphins had access to the novel enrichment device once per day, five days per week between 1200 and 1300 h, when observations were not being collected. Phase 3 included the following 12 blocks of data when the dolphins no longer had access to the novel enrichment device. To assess swim types from the instantaneous samples, the average amount of time spent in each swim state (solo swim and social swim) for each block was calculated by summing the number of occurrences in each category and dividing by the total number of visible scans for each dolphin. To assess behavior events from the continuous samples, the rates of behavior in each category (i.e., social active, social agonistic, social sexual, and solitary active) were calculated by summing the number of events by the total number of minutes visible.
The rate for each behavior and swim type was averaged in the early morning (0600–0829 h), late morning (0830–1145 h), and afternoon (1315–1630 h) and then plotted based on time of day. Generalized estimating equations were used to determine if swim type and behavior categories were affected by time of day. These predictive models allowed for the individual dolphin to be the unit of analysis and the repeated measurement on an individual. Univariate regression models were built with an independent correlation structure for solo swim, social swim, social active, social agonistic, social sexual, and solitary active behaviors.
The simple ratio index [42
] was used to calculate association rates for all dyads in the group. High association indices indicate a stronger tie between the two individuals. To illustrate social structure within the group and each subgroup, dyadic relationships were displayed visually. Changes in association indices over time were examined using chronological randomization tests [43
]. Data were parsed into three time periods, which aligned with the implementation of a complex environmental enrichment device (see [40
] for details).
The rate of nursing for mother–calf pairs was calculated by summing the number of nursing occurrences by the number of minutes visible and was plotted over time. The percentage of time mother–calf dyads spent together was calculated by summing the number of events in a pair or social swim by the number of minutes visible and was plotted over time.
Affiliative behaviors were the dominant behavior class in this social group. All behavior and swim states differed based on the time of day. The time of day affected both sociality and behavior. Preferred associates remained the same for some individuals in the subgroup as in the larger group, while they differed for other individuals. However, no large reductions in associations were recorded suggesting dyads with strong relationships in the subgroups continued to associate when other individuals were accessible. Bonds between mother and calf in dyads remained very strong in both the subgroup and the larger group. However, differences in maternal style also may have moderated the strength of other social relationships. Positive social relationships can enhance the welfare of dolphins under professional care [50
]. Social behaviors, such as synchronous swimming, are associated with positive affective states [64
]. Therefore, measuring dolphin’s social behavior and defining the strengths of relationships may provide insight into an individual’s welfare state as social behaviors appear to be related to sex, environmental enrichment factors (i.e., enrichment schedule and frequency of new enrichment), and social grouping [19
This type of information can be incorporated into the daily management of the dolphins. The present study acts as a baseline for rates of social and solitary swimming for these individuals and could be used as one component of their continuous welfare monitoring program. These data could be used to assess the effectiveness of enrichment designed to promote social behaviors. In addition, data on pair swimming and agonistic behavior could speak to the cohesiveness of the group and influence the composition of subgroups. For example, two animals with high association values could be managed in the same subgroup more often. Finally, the information on maternal care could be valuable to monitoring the dependence and social development of juveniles. Examining key aspects of sociality over time (i.e., strength of relationships and rates of play, pair swimming, and agonistic behavior) and activity levels may be important predictors of welfare. Sociality and activity appear to be related to the composition of the social group and the time of day. Therefore, they may be a useful tool in monitoring and continuing to improve welfare.