Acoustic behaviour of bottlenose dolphins under human care while performing synchronous aerial jumps

Highlights

• Three bottlenose dolphins were asked to perform synchronised jumps in tandem.

• While jumping in tandem, click trains were emitted by only one individual 98% of times.

• The dolphins that do not vocalize are probably synchronising their jumps by eavesdropping the clicking dolphin.

Abstract

Synchronous behaviours occur when two or more animals display the same behaviour at the same time. However, the mechanisms underlying this synchrony are not well understood. In this study, we carried out an experiment to determine whether or not Bottlenose dolphins use acoustic cues when performing a known synchronised exercise. For this, we recorded three dolphins while they performed requested aerial jumps both individually or synchronously in pairs, with a hydrophone array and a 360° underwater video camera allowing the identification of the subject emitting vocalisations. Results indicated that in pairs, dolphins synchronised their jumps 100% of the time. Whether they jumped alone or in pairs, they produced click trains before and after 92% of jumps. No whistles or burst-pulsed sounds were emitted by the animals during the exercise. The acoustic localisation process allowed the successful identification of the vocalising subject in 19.8% of all cases (N = 141). Our study showed that in all (n = 28) but one successful localisations, the click trains were produced by the same individual. It is worth noting that this individual was the oldest female of the group. This paper provides evidence suggesting that during synchronous behaviours, dolphins use acoustic cues, and more particularly click trains, to coordinate their movements; possibly by eavesdropping on the clicks or echoes produced by one individual leading the navigation.

Introduction

Synchrony is defined as the precise coincidence of events in time (Ravignani, 2017). Thus, synchronous behaviours occur when two or more animals perform the same behaviour at the same time (Connor et al., 2006), and have been described for several animal species in different sensory modalities (e.g., visual, acoustic) (reviewed in Herzing, 2015). The degree of synchronisation varies from time intervals of less than one second, to several minutes (Sakai et al., 2010). For example, visual synchrony occurs between fireflies (Pteroptyx spp.) that synchronise their bioluminescent flashing at night (Buck, 1988), and between male fiddler crabs (Uca annulipes) that wave their major claws in synchrony in order to attract females (Backwell et al., 1999). Examples of acoustic synchrony have been described in the courtship vocalisations of male long-tailed manakins (Chiroxiphia linearis) (Trainer and McDonald, 1993) and male frogs (Kassina kuvangensis) (Grafe, 2003). Many synchronous animal displays, such as those mentioned above, are driven by competition (Ravignani et al., 2014). Some species, however, perform synchronous behaviours linked to cooperation. This is the case for humans during sports and musical activities (Launay et al., 2016), as it is for dolphins (Tursiops truncatus) when allied males synchronise their vocal behaviour to coerce females (Moore et al., 2020).

In dolphins, the term “synchrony” has been used in two different ways. First, to describe group members that perform non-random grouping behaviours, such as swimming and breathing in synchrony (Hastie et al., 2003; Fellner et al., 2013); and second, to describe behaviours that are performed ‘simultaneously’ or ‘in unison’ (Mann and Smuts, 1999; Connor et al., 2006). Simultaneous behaviour has been described in several dolphin species. Pantropical spotted dolphins (Stenella attenuata) synchronise their movements as a defensive response while being herded in tuna nets (Pryor and Kang-Shallenberger, 1991). Synchronous behaviour has been reported in Atlantic spotted dolphins (Stenella frontalis) as a means of dominating larger sized opponents (i.e., Bottlenose dolphins (Tursiops truncatus)) during aggressive interspecific interactions (Cusick and Herzing, 2014). Male Indo-Pacific Bottlenose dolphins (Tursiops aduncus) have been observed to synchronise their surfacing behaviour during social interactions with female consorts (Connor et al., 2006; Sakai et al., 2010) and whilst herding females (Connor et al., 1992; Connor and Smolker, 1996), but also as a signal of alliance unity and a means to maintain and strengthen social bonds (McCue et al., 2020).

Vocal synchrony has also been described in a number of species: Spinner dolphins (Stenella longirostris) synchronise their vocalisations when dispersing from bays (Brownlee and Norris, 1994) and during cooperative prey herding (Benoit-Bird and Au, 2009). Offshore populations of Bottlenose dolphins (Tursiops truncatus) have shown evidence of vocal synchrony in order to maintain contact in a large home range (Janik et al., 2011). Finally, simultaneous vocal and visual signals have been reported for this same species during intraspecific aggressions (Herzing, 2015).

Sounds emitted by dolphins are classified into three structural categories and two functional classes. Structurally, sound production is thus categorised into whistles or tonal sounds (reviewed in Janik, 2009), clicks or pulsed sounds (Au et al., 1974), and burst-pulsed sounds (Diaz-Lopez and Bernal-Shirai, 2009). Functionally, whistles and burst-pulsed sounds play a role in communication and social interactions (reviewed in Herzing, 2000). Clicks, however, are used for echolocation, which can be defined as the acoustic representation of one’s surroundings, obtained by the production and emission of clicks and the subsequent nervous integration of the perceived echoes (Au, 1993).

Vocalisations associated with cooperative behaviours have been described in Bottlenose dolphins (Eskelinen et al., 2016) and killer whales (van Opzeeland et al., 2005). Such cooperative behaviours do not necessarily involve the expression of the same movement or behaviour in a fully synchronised manner. However, the fact that there is a communicative process during cooperation in these experiments, leads us to believe that when two or more dolphins engage in a synchronous behaviour, information may be flowing between them. This flow of information can involve a communication process (Johnson, 2015) and may occur by use of one of several sensory channels. Underwater, visibility can be limited (i.e., turbidity, depth, light), in contrast, sound travels well (Tyack and Clark, 2000). Therefore, the expression of acoustic cues to synchronise behaviours is a plausible assumption.

The use of acoustic cues to perform simultaneous movements is difficult to investigate in free-ranging dolphins for two main reasons: First, low visibility underwater in most of their habitats (Würsig and Pearson, 2015) (with the exception of a few locations such as the Bahamas (Herzing, 1996) or Fernando de Noronha in Brazil (Silva Jr. et al., 2005)) allow neither clear determination of the degree of synchronicity, nor the localisation of the individual emitting the sound. Second, even with good visibility, the occurrence of synchronous behaviours, the identification of the individuals performing them and the replication of tests cannot be controlled by the experimenter.

Management of dolphins under professional care provides a favourable opportunity to study the mechanisms underlying synchronisation due to the fact that a synchronous behaviour can be requested from the target animals and be replicated several times. The clarity of the water and the proximity for observations allows for direct recording of behavioural sequences as well as the identification of the individual emitting a vocalisation by use of a hydrophone array.

Dolphins in human care facilities regularly engage in behaviours simultaneously (e.g., jumps) and, through positive reinforcement, can be trained to display these synchronous behaviours upon request (Brando, 2010). However, it is unknown how dolphins manage to synchronise their actions and whether or not they use acoustic cues to coordinate their simultaneous behaviours. The first aim of this study was to explore the potential involvement of acoustic cues during a simultaneous exercise requested by a caregiver (or trainer). Thus, if synchronisation relies on the emission of acoustic signals, one might assume that acoustic signals will be emitted during the exercise and that acoustic cues will be different depending on whether the individuals perform the exercise alone or in synchronisation with another individual. The second aim of the study was to identify the category of sounds emitted during such an exercise, as well as the identity of the emitters.