Acoustic communication in Australian fur seals

ce of a neighbour-stranger vocal discrimination in male Australian fur seals. It also demonstrated that there was an increase in response from males when they heard more bark units from stranger seals, indicating that the number of units was important for eliciting a response from males. Furthermore, altering the inter-unit spaces of neighbouring male calls did not affect the response of male subjects, which was surprising as this result is not consistent with other studies and further experimental playbacks are suggested to examine this further. Playback experiments also indicated that the whole frequency spectrums of calls are important to recognition. Finally, investigations reveal that males may only need to hear between 25 - 75% of each bark unit for recognition to occur. Further research examining the importance of behavioural posturing to the recognition process and examining the location of callers on territories would provide useful insights into the importance of these factors to vocal recognition in male Australian fur seals. 122 CHAPTER 7 GENERAL DISCUSSION The Australian fur seal is a highly vocal marine mammal, breeding in dense social groups on only ten islands in the Bass Strait. As with other pinnipeds, vocalisations in this species are pivotal to reproductive exchanges and are important on a number of different levels in social organisation, including mother- offspring interactions and male territorial defence. However, while the importance of understanding the acoustic behaviour of pinnipeds is clear, this behaviour in Australian fur seals has received very little attention in the literature, with only one previous study providing descriptive evidence of vocalisations (Stirling and Warneke 1971). The present study investigated the acoustic behaviour of Australian fur seals by examining wild seals at the remote breeding colony on Kanowna Island, with the aim of describing the physical structure and behavioural context of the animals’ calls. The study examined the individuality of vocalisations and the acoustic characteristics that are important in separating callers. These identified characteristics may be used in vocal recognition. It also examined the call structure of pup vocalisations and how these change through the maternal dependency period, then tested vocal recognition in territorial males thus the present study expands the understanding of the acoustic behaviour and vocal recognition abilities of this species and provides information of broader relevance to other colonial breeding species. 7.1 Functionality of vocalisations Species recognition is important as it allows individuals to recognise other animals as conspecifics, thereby deterring them from interbreeding. By conducting baseline studies on the vocalisations produced by Australian fur seals, the study was able to compare acoustic characteristics between species. Results indicate the PAC, FAC and bark that are produced by Australian fur seal 123 females, pups and males, respectively, are structurally similar in their gross morphology and function to the vocalisations of other otariid species (Fernández- Juricic et al. 1999; Phillips and Stirling 2000; Page et al. 2002 a and b). However, the species are clearly distinguishable in their acoustic characteristics. In particular, the PAC (females), FAC (pups) and bark (males) produced by Australian fur seals, have a lower fundamental frequency (Phillips and Stirling 2000; Page et al. 2002a; Roux 1986). In male Australian fur seals, the fundamental frequency is much lower than in other fur seals, being at least 250 Hz lower than the barks of the subantarctic fur seals (Roux 1986). In general, a direct relationship exists between the size of an animal and the frequency it can produce, with larger animals capable of producing lower frequency calls (Morton 1977). These species differences may function in keeping species discrete, this aspect being particularly important with respect to sympatrically occurring species, such as Australian and New Zealand fur seals. A number of vocalisations are employed by both males and females in territorial defence. These are aggressive vocalisations that are structurally low in frequency and pulsed. In male Australian fur seals, the calls used in the defence of territories include the bark and the guttural threat, whereas the full threat call and growl that are reported in other fur seals is missing in this species. In female Australian fur seals, the aggressive vocalisations include the bark, guttural threat and growl. Aggressive vocalisations in females have received little attention in the literature, with the main focus being on mother-offspring vocalisations. However, in resource defence polygyny, evidence suggests that females defend resources within the male’s territory, and this in turn may limit the number of mates available to the territorial male and reduce his mating success (Carey 1992). On the basis of descriptive evidence it has been suggested that the bark produced by male Australian fur seals is important to vocal recognition (Stirling and Warneke 1971). In the dear-enemy effect, territorial individuals which compete to defend a resource area typically respond more to strangers (i.e. unfamiliar individuals) than to neighbouring animals (Fisher 1954). This variation 124 in response may be based on the perceived level of threat posed by the different individuals (Temeles 1994). In the present study, the call structure of the male bark was analysed to determine if the vocalisations of Australian fur seals fit this theory. Using traditional analytical techniques only, evidence was sought to establish that bark calls were individually distinct. The more novel technique (i.e. CART) was not deemed necessary as most call features could be incorporated into the traditional techniques (i.e. PIC and DFA). Both frequency and temporal parameters were reported as necessary in separating individual callers. The neighbour-stranger recognition system in males was tested in Australian fur seals using playback experiments and the results indicate that territorial males respond more to the calls of strangers than to the calls of their neighbours, supporting neighbour-stranger recognition in this species. Acoustic modifications of the bark call parameters were used to assess their importance to vocal recognition. The whole frequency spectrum was found to be important to recognition. Furthermore, recognition occurred when males heard between 25- 75% of each bark unit from seals indicating that the whole duration of each bark unit is not necessary for recognition to occur. This may have particular advantages for communication in acoustically complex breeding areas, where calls may be degraded by the environment. Other acoustic manipulations where the inter-unit spaces were increased and decreased by 25%, did not elicit changes in the response of males. This result was surprising as the outcome from the individual variation study indicated that the inter-unit duration would be important. A substantial proportion of male barks, including those associated with nuzzling and mating, were directed to females during the breeding season. This suggests that these calls are important in inter-sexual relations and mate attraction. In South American sea lions, there is a high degree of association between male vocal behaviour and the factors that influence male mating success, with vocal rates increasing as males monopolize larger numbers of females (Fernández-Juricic et al. 2001). 125 Vocalisations in infant animals are typically high frequency and tonal, vocal characteristics that are adapted for eliciting parental care (Morton 1977). To date, descriptive and qualitative evidence in otariids suggests that calls used by mothers and pups during the reunion process contain unique properties that enable vocal recognition (Insley et al. 2003b). In Australian fur seals, similar to other otariids, mothers and pups experience repeated separations and reunions over an extended lactation period. A mechanism for mutual recognition is vital for both mother and pup as both benefit from a successful reunion. This reunion process may be facilitated through a multi-modal sensory system using a combination of vocal, olfactory and spatial cues. In a crowded breeding colony acoustic communication is considered more efficient, as it is less constrained by environmental factors. The present study investigated call individuality in Australian fur seal mother-pup vocalisations. Results indicated that the PAC (females) and FAC (pups) contain enough information to permit the discrimination of individual mothers and offspring. Using a combination of traditional and non-traditional techniques, several acoustic parameters were suggested to be important for recognition. Investigations into the call structure changes of newborn pups to 11 months of age indicate that calls increase in duration, lower in both the number of parts per call and the harmonic band containing the maximum frequency. These call modifications may be related to the growth and weight changes (Arnould and Hindell 2002), as well as lengthening of the vocal cords and increases in lung capacity, as reported in other vertebrate species (Snowdown and Elowson 1992). This study, together with others, support the hypothesis that long term maternal recognition of offspring may be facilitated through mothers learning new versions of pup vocalisations as these modify throughout postnatal development and maturation (Charrier et al. 2003c). In general the individuality studies of males, females and pups produced some parallels in the call parameters that were important in separating callers. The fundamental frequency and duration were valuable in separating callers in all categories (i.e. females, pups and males). In addition, the maximum peak 126 frequency was essential in separating pup and male callers, and the inter-unit duration was important in separating male callers only. The PAC (females), FAC (pups) and bark (males) of Australian fur seals are all moderately stereotyped, when compared to other fur seal studies. This may imply that other sensory signals such as vision and olfaction may be used in the recognition process by this species. 7.2 Factors influencing the vocal behaviour of Otariids The present study examined characteristics that relate to the breeding biology of otariids that are likely to influence their acoustic behaviour. There are large gaps in the literature in these areas amongst the otariid species and this lack of knowledge needs to be addressed before the results of the present study can be analysed in detail. There are also differences in sample size, and differences in the replicates per individual which may account for some of the variances in results between species. Nevertheless, comparisons were made using results from the literature and some preliminary trends are reported. Species breeding at low densities have more calls in their repertoire as opposed to species breeding in higher female densities, which have in general, lower repertoire sizes (Table 7.1). This pattern is also known to occur in birds, where smaller repertoire sizes are used by males that have access to more females (Catchpole 1980). Vocalisations of polygynous species have evolved primarily through intra-sexual selection where calls are simpler, shorter and stereotyped in structure used in male-male interactions, while vocalisations used in monogamous species, have evolved for use in sexual attraction, where songs are more elaborate, long and complex (Catchpole 1980). Although all otariids are polygynous, this argument may be applied in part to these seals. The selective pressures on species where female congregations on breeding areas are dense may be different to those breeding on areas where there are fewer females. Where females are more densely spaced, calls in males may function primarily in male-male interactions and may need to be simple and repetitive. On the other hand males holding territories in which females are more widely 127 dispersed may need to defend their territories, but may also attract females to some degree. The requirement to attract females may account for the larger repertoire sizes for these species. There is a general trend toward greater vocal repertoire in those species breeding on boulder and jumbled rock areas as opposed to those breeding on more open areas (some exceptions e.g., Antarctic fur seal). Roux and Jouventin (1987) suggested that species inhabiting boulder type areas may need to use more call types for communication as other sensory modes, such as vision in relation to behavioural displays, may be constrained by the physical environment. In contrast, species such Australian fur seals that breed in more open areas, might be able to utilise both calls in combination with other sensory modalities for communication, thereby reducing the need for larger call repertoires. It is suggested that this feature, in association with others, may influence the vocal behaviour of otariids. The degree of call stereotypy is fairly high in all species investigated, implying vocal recognition can be used by all species. In females the greatest difference in call stereotypy was between South American fur seals (70%) and South American sea lions (90%). This may be related to female density where the need to be more stereotyped, (i.e. more recognisable) to pups may be greater in more crowded areas, such as those in South American sea lions. Similarly, in pup vocalisations, the call stereotypy is lowest in Antarctic and South American fur seals and highest in South American sea lions. This may be a reflection of similar selective pressures for this behaviour which has led to more stereotyped calls, where the acoustic features in South American sea lion pup calls are more distinctive, allowing mothers to recognise their offspring. There is also a notable difference in the fundamental frequency amongst otariid species in all categories compared (i.e. males, females and pups), being lower in Australian fur seals compared with other fur seal species (Table 7.1). This difference may be related to body size where larger body size of Australian fur seals enables them to produce lower frequency vocalisations (Morton 1977). This aspect was also reported as an influential factor in shaping the acoustic 128 behaviour of male phocids (Rogers 2003). The degree of polygyny and length of lactation (Rogers et al. 2003) did not appear to be influence the acoustic behaviour of both otariids and phocids. In summary female density, body size and breeding environment all appear to influence the vocal behaviour of otariids, while duration of lactation and degree of polygyny do not appear to be influential. 1 2 9 T a b le 7 .1 L if e h is to ry c h a ra c te ri s ti c s a n d c a ll fe a tu re s o f O ta ri id s . S P E C IE S D u ra ti o n o f la c ta ti o n (m o n th s ) 1 ,2 D e g re e o f p o ly g y n y 3 F e m a le d e n s it y (f /m 2 ) 4 S o c ia l o rg a n iz a ti o n 3 H a b it a t 4 , 5 , 6 M a le w e ig h t (k g ) 7 F e m a le w e ig h t (k g ) 7 N o rt h e rn f u r s e a ls , C a llo rh in u s U rs in u s 3 -4 E x tr e m e p o ly g y n y 0 .2 -0 .6 E x tr e m e ly l a rg e g ro u p s ; fe m a le s d e n s e ly s p a c e d Is la n d , b ro k e n b a s a lt ; b o u ld e r b e a c h e s 2 2 7 .0 4 4 .8 S u b a n ta rc ti c f u r s e a ls , A . tr o p ic a lis 1 0 -1 1 M o d e ra te t o e x tr e m e p o ly g y n y 0 .1 S m a ll to l a rg e g ro u p s ; fe m a le s w e ll s p a c e d Is la n d ; ju m b le d r o c k y c o a s tl in e 1 5 2 .5 5 0 .0 N e w Z e a la n d f u r s e a ls , A . fo rs te ri 9 -1 2 P o ly g y n y 0 .1 S m a ll to l a rg e g ro u p s ; fe m a le s w e ll s p a c e d Is la n d ; j u m b le d r o c k y c o a s tl in e 1 6 4 .4 5 5 .0 A n ta rc ti c f u r s e a l, A . g a z e lle 4 M o d e ra te t o e x tr e m e p o ly g y n y 0 .4 -1 .1 S m a ll to l a rg e g ro u p s ; fe m a le s p a c in g v a ri a b le Is la n d , a n d o p e n b e a c h e s 1 5 5 .0 3 8 .2 S o u th A m e ri c a n f u r s e a ls , A . A u s tr a lis 7 -3 6 P o ly g y n y 0 .5 -1 .0 S m a ll g ro u p s ; fe m a le s w e ll s p a c e d Is la n d a n d c o a s ta l; ro c k s h e lv e s 1 5 9 .0 4 8 .5 G a la p a g o s f u r s e a l, A . G a la p a g o e n s is 2 4 P o ly g y n y 0 .0 4 S m a ll g ro u p s ; fe m a le s w e ll s p a c e d Is la n d ; ro c k s h e lv e s ; b o u ld e r b e a c h e s 6 4 .5 2 7 .4 S o u th A fr ic a n f u r s e a l, A . p u s ill u s . p u s ill u s 6 -1 2 M o d e ra te t o e x tr e m e p o ly g y n y 1 .4 -1 .9 M o d e ra te -s iz e d t o e x tr e m e ly l a rg e g ro u p s ; fe m a le s d e n s e ly s p a c e d Is la n d a n d c o a s ta l, ro c k s h e lv e s 2 7 8 .0 7 1 .0 A u s tr a lia n f u r s e a ls , A . p . D o ri fe ru s 1 1 -1 2 M o d e ra te t o e x tr e m e p o ly g y n y 0 .2 S m a ll to l a rg e g ro u p s ; fe m a le s d e n s e ly s p a c e d Is la n d a n d c o a s ta l, ro c k s h e lv e s , o p e n te rr a in 3 0 7 .0 0 8 4 .0 C a lif o rn ia n s e a l io n , Z a lo p h u s c a lif o rn ia n u s 4 -8 (u p t o 1 2 ) M o d e ra te t o e x tr e m e p o ly g y n y 0 .1 -0 .2 M o d e ra te -s iz e d t o l a rg e g ro u p s ; fe m a le s d e n s e ly s p a c e d Is la n d ; s a n d b e a c h e s , ro c k s h e lv e s 2 8 9 .0 8 6 .0 S o u th A m e ri c a n s e a l io n s , O ta ri a f la v e s c e n s 5 -1 2 M o d e ra te p o ly g y n y - M o d e ra te -s iz e d t o l a rg e g ro u p s ; fe m a le s d e n s e ly s p a c e d Is la n d a n d c o a s ta l; ro c k s h e lv e s , s h in g le b e a c h e s 3 0 0 .0 1 4 4 .0 1 3 0 1 = A tk in s o n 1 9 9 7 ; 2 = B o w e n 1 9 9 1 ; 3 = R ie d m a n 1 9 9 0 ; 4 = B o n e s s = 1 9 9 1 ; 5 = G o ld s w o rt h y e t a l. 1 9 9 9 ; 6 = P a g e e t a l. 2 0 0 2 (a ); 7 = L in d e n fo rs e t a l 2 0 0 2 ; 8 = P h ill ip s a n d S ti rl in g 2 0 0 1 ; 9 = S ti rl in g a n d W a rn e k e 1 9 7 1 ; 1 0 = T ri p o v ic h e t a l. 2 0 0 5 ; 1 1 = F e rn a n d e z -J u ri c ic e t a l. , 1 9 9 9 ; 1 2 = P e te rs o n a n d B a rt h o lo m e w 1 9 6 9 ; 1 3 = R o u x 1 9 8 6 ; 1 4 = T ri p o v ic h e t a l. 2 0 0 6 , 1 5 = I n s le y 1 9 9 2 ; 1 6 = c u rr e n t s tu d y . S P E C IE S N o o f c a lls in m a le re p e rt o ir e 8 , 9 , 1 0 , 1 1 , 1 2 % c o rr e c t D F A m a le b a rk 1 0 , 1 1 , 1 3 M a le F o 1 0 , 1 3 % c o rr e c t D F A fe m a le P A C 6 , 8 , 1 1 , 1 4 , 1 5 F e m a le F o 6 , 8 , 1 4 % c o rr e c t D F A p u p F A C 6 , 8 , 1 1 , 1 5 , 1 6 P u p F o 6 , 8 , 1 6 N o rt h e rn f u r s e a ls , C a llo rh in u s U rs in u s ? - - 8 2 - 7 9 x S u b a n ta rc ti c f u r s e a ls , A . tr o p ic a lis 3 -7 x 3 9 1 ( 5 5 ) 8 4 5 0 6 ( 1 4 ) 8 3 5 2 0 ( 1 9 ) N e w Z e a la n d f u r s e a ls , A . fo rs te ri 5 -7 x x 8 8 5 3 0 ( 6 1 ) 7 9 7 2 9 ( 6 3 ) A n ta rc ti c f u r s e a l, A . g a z e lle 5 x X 7 4 7 6 0 ( 1 4 ) 5 2 6 6 6 ( 1 2 ) S o u th A m e ri c a n f u r s e a ls , A . A u s tr a lis 7 x x 7 0 9 0 5 ( 1 1 .4 ) 6 0 1 0 3 0 (1 8 .5 ) G a la p a g o s f u r s e a l, A . G a la p a g o e n s is 7 x x x x x x S o u th A fr ic a n f u r s e a l, A . p u s ill u s . p u s ill u s 3 -7 x x x x x x A u s tr a lia n f u r s e a ls , A . p . D o ri fe ru s 3 8 3 1 4 0 .3 ( 2 4 .1 ) 7 6 2 6 2 ( 3 4 .6 ) 7 5 3 4 2 ( 6 2 ) C a lif o rn ia n s e a l io n , Z a lo p h u s c a lif o rn ia n u s 2 x x x x x x S o u th A m e ri c a n s e a l io n s , O ta ri a f la v e s c e n s 4 7 6 x 9 0 x 9 0 x 131 7.3 Are Australian fur seals vocalisations more like sea lions? Previously, it has been suggested that the behaviour and vocalisations of Australian fur seals resemble more of sea lions rather than those of fur seals (Warneke and Shaughnessy 1985). Throughout the study it was apparent that differences existed in the vocal characteristics between Australian fur seals and other fur seal species but due to the lack of sufficient data, detailed comparisons were not possible. However what was evident was that the fundamental frequency characteristic of Australian fur seal vocalisations was more similar to sea lions than to those of fur seals. The opinion of the author is that both the larger body size and breeding environment may influence and shape the vocalisations of seals. Firstly, Australian fur seals are the largest of all fur seals (Table 7.1) and are comparative in size to other sea lions, and in general, larger animals are capable of producing lower frequency calls (Morton 1977) which may account for the lower frequency (particularly in barks produced by males) reported for Australian fur seals and sea lions compared with other fur seals. And secondly, the differences in the vocalisations may be related to the variation in breeding environments. In general, Australian fur seals and sea lions (from available data to date) produce lower frequency bark calls and breed in more open areas, while fur seals produce higher frequency barks and breed on more jumbled rocky areas (Table 7.1). The potential for scattering of vocalisations is greater in jumbled rocky areas and so having higher frequency calls that are more directional would be advantageous in those environments, which may explain for the differences in frequencies between the Australian fur seals and sea lions compared with all other fur seals (Wiley and Richards 1978). 7.4 Future research Acoustic signals play a very important role in the breeding success of a wide variety of species. The current study described the calls produced by males, females, yearlings and pups throughout the breeding season, providing valuable information on the vocal behaviour of a species that has not been studied in great detail. This information provided by this study allows the opportunity for researchers to compare this species with other pinnipeds and the results may elucidate general evolutionary patterns. 132 Future research could extend the playback studies to investigate the recognition abilities of mothers and offspring. Artificial modification of the calls would be advised in order to determine the call features that are required for the individual identification process. The choice of variables for modification could be based on the results of the individual call variability studies, which highlight the call parameters most likely to be important to the recognition process. Behavioural development studies involve examination of the changes that occur as the young grows and matures (Martin and Bateson 1993). The present study investigated changes in pup vocalisations utilising a cross- sectional sampling approach. An alternative method of analysis known as longitudinal analysis, involves sampling the same individuals through time. It would be ideal if seal pups could be sampled using longitudinal in addition to cross-sectional techniques and results compared. In the present study the recognition abilities of male Australian fur seals was investigated. Future experiments testing a male’s ability to recognise individual neighbours would prove interesting as it can reveal whether male vocal recognition is based on males recognising individuals or recognising a group of animals as ether familiar or unfamiliar. Furthermore while the present study reports valuable information on a colonial male seal species, it would be interesting to conduct playback studies on male seals that utilise other breeding strategies such as those that of solitary species (e.g., leopard seals, Hydrurga leptonyx) or those having harems (e.g., southern elephant seals, Mirounga leonina). This may provide further insights into the evolutionary patterns or environmental constraints affecting social communication in pinnipeds. Vocal communication and recognition between mothers and offspring and between males may involve other features (e.g. amplitude modulation, sound pressure levels, and others) not measured in the present study. These call features may improve the percent correct classification scores. Other features such vision, spatial orientation and smell may also play a role in the recognition process and investigations on these factors could help reveal 133 important information on the recognition process in seals and in understanding the reproductive success in fur seals. Lastly, vocalisations emitted by Australian fur seals are not produced in isolation. It appears that different call types are used in combination during certain behavioural contexts. Other studies on primates have indicated that these call combinations are not produced randomly and that the order of the combinations may have meaning (Crockford and Boesch 2005). This study has provided the necessary baseline descriptions of single call units, which can then be utilised to investigate the importance of call combinations in the communicative process. Sexual reproduction creates a social environment of conflict and competition among individuals as each attempt to maximise its genetic contribution to subsequent generations (Alcock 1993). Vocalisations are a major component in the breeding communication of Australian fur seals. Consequently, investigations made by this study broaden our understanding on the acoustic behaviour of Australian fur seals and the influences shaping vocalisations, all of which may ultimately impact the breeding success of an individual. 134 LIST OF REFERENCES Alcock, J., 1993. Animal Behaviour: an evolutionary approach. Fifth Edition. 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