This study describes an unusually delayed production during the night of mimicries of sounds related to salient events. The fact that these mimicries are produced when the dolphins are resting or sleeping and never when they were active is intriguing, especially as these sounds were only broadcast in the context of daytime shows. Hooper et al. (
2006) show that mimicries are enhanced by association of sounds with objects or events, and that dolphins tend to produce these sounds in the corresponding contexts/activities. Therefore this raises the question of whether these night productions correspond to a form of “rehearsal” of daily shows. None of these vocalizations had ever been recorded before this broadcast was performed and information of the dolphins’ life history clearly established that these animals had never had the opportunity to hear whale sounds previously. These mimicries occurred neither in direct association with the event, nor during interactions with humans and other dolphins. Data concerning both objective measurements of sound parameters and evaluations by humans converge to show that these atypical vocalizations were mimicries of the whale sounds broadcast during shows. Dolphins transposed frequencies as do killer whales (Foote et al.,
2006) and a variety of mimicking birds (songbirds: Hausberger et al.,
1991; parrots: Cruickshank et al.,
1993). There may be some physical constraints, as the preferred range of frequencies for dolphin copying seems to be between 5 and 10
kHz (Richards et al.,
1984). Other authors give examples of low-pitched vocalizations emitted by dolphins (dos Santos et al.,
1995; Connor and Smolker,
1996; van der Woude,
2009) and the question of whether these sounds correspond to mimicries has been raised (van der Woude,
2009). The sounds produced here clearly differ from these examples in their acoustic structure: WLPs are longer in duration and present more frequency modulations than do “brays” (dos Santos et al.,
1995) and “pops” (Connor and Smolker,
1996), and their minimum and maximum frequencies are higher than those of “moans” (van der Woude,
2009). They also differ from other parts of the dolphin’s species specific repertoire (reviewed in Janik,
2009).
These mimicries are a further proof that dolphins can learn when adult, as they heard this tape only when adult. The most remarkable aspect though is the delayed production of these mimicries in a quiet context. The “salience” of the event/interaction may have been crucial (Tyack and Sayigh,
1997; Hooper et al.,
2006). These atypical vocalizations might be episodes of “vocal play” while at rest (Pepperberg,
2002; Kuczaj and Makecha,
2008), or, given the context, a potential part of a global rehearsal of these salient daytime events. The mimicries occurred only at quiet times, mostly during the night (0 to 3 a.m.), and outside any kind of social interactions, while obviously resting or sleeping. In captivity, show periods are salient events associated with multisensory stimulations (food reinforcement, vocal orders, public responses…). In addition to the general background (crowd, noise,…) that may be emotionally salient, food reinforcement used by trainers may increase excitation (Innes and McBride,
2008) and long term memories (Sankey et al.,
2010); positive as well as negative-emotional valences could potentially induce increased mimicry and strong memories (Armstrong,
1960).
This is to our knowledge the first time that a long separation between hearing an auditory model and copying it has been observed in a marine mammal. One hypothesis predicts that dolphins, like parrots or songbirds, “practice” outside the “model’s” presence (Hausberger et al.,
1991). Another hypothesis predicts that these events correspond to rehearsals of a more global memory, as for example in the form of dreams during sleep or “day dreaming” in humans and animals (Cipolli et al.,
2004). Reports of potential “dreaming” remain anecdotal in species other than laboratory animals. A pilot study by Lubrano Lavadera (
2005) reported that young horses produced adult vocalizations (that they never produced during the day) during REM (i.e., rapid eye movement) sleep. This question is especially intriguing as cetaceans seem to lack typical REM sleep, or may have very short bouts of it (Mukhametov,
1995; Shpak et al.,
2009). Nevertheless periods of sleep, mostly between 0 and 3 a.m., but also at times during the day, have been described, when the animals are floating or swimming slowly (Sekiguchi and Kohshima,
2003; Lyamin et al.,
2008). Resting periods are associated with lower whistle production rates (Sekiguchi and Kohshima,
2003). Muscle jerks recalling REM sleep have been observed (Lyamin et al.,
2008). Whether or not dolphins experience any kind of rehearsal of daytime events during their sleep therefore remains a mystery, although anecdotal reports by trainers suggest that dolphins perform a trained task better in the morning. Improvement of performance is a proved consequence of the rehearsal of memories in human dreams (Aly and Moscovitch,
2010).
As individuals and precise behavior could not be identified in this study, only further investigations associating EEG (electroencephalography) recordings, could confirm or infirm our hypothesis that these productions reflect rehearsal of daytime events by dolphins during rest or sleep. Their rarity (1.1% of total production) and timing (mostly at night) may explain that this constitutes the first report of mimicries of sounds heard during special events produced by dolphins in a resting/sleeping context. This finding opens very large perspectives for future investigations on dolphin learning processes and “mental representations.”
