The role of visual cues in mother–pup reunions in a colonially breeding mammal

Abstract

Parental care is an important factor influencing offspring survival and adult reproductive success in many vertebrates. Parent–offspring recognition ensures care is only directed to filial young, avoiding the costs of misallocated resource transfer. It is essential in colonial mammal species, such as otariids (fur seals and sea lions), in which repeated mother–offspring separations increase the risk of misdirecting maternal effort. Identification of otariid pups by mothers is known to be multi-modal, yet the role of visual cues in this process remains uncertain. We used three-dimensional visual models to investigate the importance of visual cues in maternal recognition of pups in Australian sea lions (Neophoca cinerea). We showed that the colour pattern of pup pelage in the absence of any other sensory cues served to attract the attention of females and prompt investigation. Furthermore, females were capable of accurately distinguishing between models imitating the age-class of their own pup and those resembling older or younger age-classes. Our results suggest that visual cues facilitate age-class discrimination of pups by females and so are likely to play an important role in mother–pup reunions and recognition in otariid species.

1. Introduction

Parental care is an important component of the life history of many animals, influencing offspring survival and consequently adult reproductive success [1]. To reduce costs, parents should direct care only towards filial young. Consequently, recognition of filial offspring is an essential element of parental care for many species [1]. Information about offspring identity may be conveyed through various modalities [2,3]. While the roles of acoustic and olfactory cues have been well investigated for many mammals, there is considerably less information about the role and accuracy of visual cues in the parent–offspring recognition process. Visual cues appear important in mother–offspring reunions of ungulates and primates [4–6], and are likely to be particularly important for gregarious, colonial species, in which mother–offspring separations are frequent [1].

Otariid females and pups face extremely high selection pressures for successful recognition. Throughout lactation, females leave their pups on land while they forage at sea [7]. Following each return, they must find and identify their pup in a colony. Furthermore, females are aggressive towards non-filial pups [8] and allosuckling is rare [9], making successful reunion necessary for pup survival. Otariid mothers and pups use vocal and olfactory cues to both localize and recognize individuals [10,11], but while the ability to use visual cues to discriminate appears to be present [10], its role and precision in reunions remain uncertain.

Australian sea lions (Neophoca cinerea; ASL) have a 17–18-month long breeding cycle [12] with a prolonged pupping season lasting up to eight months [12]. Consequently, pups of different ages co-occur in the colony. Over their first four months, ASL pups undergo significant morphological changes in pelage colour pattern and size. There are three visually distinct age-classes: A1—pups under two months of age, small and black; A2—pups two to four months old, larger with brown to cinnamon colour; A3—post-moult pups, over four months old, very large with silver-beige pelage (electronic supplementary material, figure S1; [13]), enabling investigation of their role as visual cues in mother–pup recognition and in reunions.

2. Material and methods

We investigate the role of visual cues in mother–pup reunions with two experiments. The first experiment, natural versus unnatural (N/UN), tested the response of females to pup models with a natural or an unnatural pelage colour pattern. The second, age-classes (AC), tested the ability of females to distinguish pup models using age-class-specific pelage patterns. Data were collected on Beagle Island (N/UN) and Olive Island (AC), Australia in 2010 and 2016. For N/UN, we tested 15 adult ASL females with A1 pups. For AC, we used 28 ASL females, 15 with A1 filial pups and 13 with A2 pups.

We constructed three-dimensional visual models of ASL pups. Models used in N/UN were the size and shape of A1 pups and were either black (natural) or white (unnatural brightness). For AC, model pups were constructed to approximate the size, shape and colour brightness of the three visually distinct age-classes (A1, A2 and A3; electronic supplementary material, figure S1). Sea lion pup models have been previously used in similar studies and shown to successfully imitate pups [11]. During presentations, we simultaneously placed two models on the ground, approximately 1 m apart, and 2–4 m in front of a targeted female (electronic supplementary material, videos S1 and S2). This distance range is well known to elicit a response from females [11]. For N/UN, a black (congruent) and a white (incongruent) model were presented to each female. For AC, each female was presented with one model imitating her pup's age-class (congruent model) and one imitating a different age-class pup (incongruent model), thereby providing four possible combinations of models: A1 (congruent) versus A2 (incongruent), n = 8; A1 (congruent) versus A3 (incongruent), n = 7; A2 (congruent) versus A1 (incongruent), n = 7; A2 (congruent) versus A3 (incongruent), n = 6. All models were randomly allocated to left or right.

We expected the mothers to act aggressively towards incongruent models, and not aggressively (displaying investigatory behaviour) towards congruent models. To ensure that the principal focus was the females' response to visual cues, we recorded which model was approached first and whether the female was aggressive upon approach. Based on this, we classified each response as appropriate or inappropriate. Appropriate was defined as the female (i) approaching the congruent model first in a non-aggressive manner or (ii) approaching the incongruent model first and exhibiting aggressive behaviour. Inappropriate was defined when the female (i) approached the congruent model first and exhibited aggressive behaviour or (ii) approached the incongruent model first and was not aggressive. An approach was considered as the female moving directly towards a model in a linear manner, stopping before it and exhibiting either an appropriate or an inappropriate response. We defined aggression as the female presenting an open mouth display, producing ‘puffs’ (i.e. air expulsion through nostrils) and/or biting the model. We tested for significant differences between appropriate and inappropriate responses with an exact binomial test. We later implemented a Fisher's exact test to assess whether differences in success ratios occur between the different combinations of presented models for AC.

Furthermore, for AC following data centring and scaling, we performed a principal component analysis (PCA) that included the number of sniffs, puffs and bites exhibited by the female within 90 s of approach and used a Wilcoxon signed-rank test to determine the differences in principal components (PC) between female response to congruent and incongruent models. For N/UN, we compared only the number of sniffs (as no aggression occurred) with a Wilcoxon signed-rank test. All statistical analyses were performed in R v. 3.2.2 [14].

3. Results

(a). Natural versus unnatural

Females showed a significant preference for black over white pup models (p > 0.001; table 1) demonstrating that visual cues influence female reunion behaviour. Fourteen out of 15 females investigated the black model first and none displayed aggression towards the model they approached first. Females sniffed the congruent model significantly more times than the incongruent (p = 0.001; figure 1a).

Table 1.

Number of appropriate and inappropriate responses of ASL females towards congruent and incongruent pup models based on visual cues. Notations: A1/2/3, age-class of pup model; AC, age-classes experiment; N/UN, natural versus unnatural experiment. The p-value is the statistic of an exact binomial test for experiments N/UN and AC, and Fisher's exact test for comparison of different treatments for AC experiment.

experiment	N appropriate	N inappropriate	N total	congruent model	incongruent model	p-value
N/UN	14	1	15	natural	unnatural	0.001
AC	21	7	28	congruent age-class	incongruent age-class	0.013
AC	5	3	8	A1	A2	0.705
AC	6	1	7	A1	A3
AC	6	1	7	A2	A1
AC	4	2	6	A2	A3

Figure 1.

Differences in ASL female response towards congruent and incongruent models. Notations: (a) experiment N/UN, (b) experiment AC. *Statistical significance (p < 0.05) determined by a Wilcoxon signed-rank test. (Online version in colour.)

(b). Age-classes

Significantly more ASL females behaved appropriately towards models representing different pup age-classes (i.e. ‘appropriate’ defined in §2; p = 0.01; table 1), confirming that they accurately distinguished the current age-class of their pup based solely on visual cues. Twelve females approached the congruent model first and behaved non-aggressively, while nine females approached the incongruent model first, but showed aggression. All inappropriate responses (n = 7) were when females approached the incongruent model first but did not exhibit aggressive behaviours. We did not find any significant differences across the various combinations of presented models (p = 0.7; table 1; figure 2), indicating equivalent accuracy of female visual discrimination of pup age-classes, irrespective of filial pup age or level of difference between the age-classes of presented models.

Figure 2.

Number of appropriate (solid) and inappropriate (dashed) responses of ASL females towards pup models representing visually distinctive age-classes. Notations: A1/2/3, age-class represented by pup model. *Congruent model. (Online version in colour.)

The PCA compiled three PCs, with only PC1 having an eigenvalue >1, explaining 57% of the variance in female response (table 2). Aggressive behaviours were correlated with PC1 (puffs = 0.68; bites = 0.70). There was a higher number of aggressive behaviours exhibited by the females towards incongruent models than congruent models (p = 0.006; figure 1b).

Table 2.

Results of a PCA including the number of sniffs, puffs and bites exhibited by ASL females towards pup models representing different age-classes. The PCA compiled three PC, with only PC1 scoring an eigenvalue >1. PC1 was positively correlated with aggressive behaviours and explained 57% of the variance in female response.

	PC1	PC2	PC3
rotation
sniff	−0.22	−0.96	0.18
puff	0.68	−0.29	−0.68
bite	0.70	−0.03	0.71
eigenvalue	1.71	0.99	0.30
proportion of variance	0.57	0.33	0.10
cumulative proportion	0.57	0.90	1.00

4. Discussion

ASL mothers were more attracted to natural than to unnatural pup pelage, and could accurately differentiate pup age-class visual characteristics in favour of those resembling their own pup, suggesting that visual cues may play an important role in mother–pup reunions and recognition in wild otariids.

Females showed a clear preference towards congruent pup models and most ignored pup models with unnatural pelage colour patterns. While model size and shape were held constant, a change in the pelage completely changed maternal behaviour, indicating that it is used in distinguishing pups and is important in attracting the attention of females during mother–pup reunion. Females also clearly recognized their own pup's age-class regardless of which other age-class it was compared against. This suggests that females are aware of the current morphological characteristics of their pup (size and pelage). Given that this will change through the lactation period, females must also have to adjust their recognition of their pup's appearance. The revision of the pup visual template by the female seems to be extremely accurate. Six of seven tested females with A2 pups successfully recognized the correct model when presented simultaneously with A1 models, yet their pup would have presented with A1 visual characteristics only a few weeks prior to the experiment. The ability to distinguish pup age-classes based on visual cues is likely to facilitate mother–pup reunions to the benefit of both. When many pups are present within the same area and aggression by non-mother females is common, the ability to quickly distinguish pups of the appropriate age and appearance not only increases the accuracy and speed of reunion, but also reduces potential harm to pups by non-mother females.

This study builds on earlier research which showed that both acoustic and olfactory cues reliably convey individual identity information of ASL pups [11,15]. Here, we have demonstrated that visual cues also play a role in the recognition process with age-class discrimination. Visual cues thus create an additional tier of recognition, complementing the longer-range vocal and shorter-range olfactory individual recognition. While the exact contribution and relative importance of each sensory modality are still to be determined, it is likely that visual cues form part of a multi-modal communication system in conjunction with vocal and olfactory cues and interact with them [16].

Our study demonstrates behaviourally that ASL mothers can use visual cues derived from the pelage of their pups to discriminate between age-classes. Examination of pinniped visual systems indicate that despite being monochromatic, they might be capable of obtaining some colour information in mesopic light conditions or potentially use differences in brightness or contrast [17]. While it is not possible from our study to determine which particular aspects of visual information ASL mothers are using, we have shown that differences in pelage facilitate differentiation. Further research is needed to identify the parameters used by ASL in these contexts.

Our findings illustrate that visual cues function to attract the attention of females during mother–pup reunions and refine the ability of a female to search for her pup. Their role in individual recognition and their interactions with olfactory and acoustic cues in the recognition process await further investigation.

Ethics

This research was carried out under the permission of the South Australian Wildlife Ethics Committee (Approval 61/2005 and 30/2015). All experimental procedures followed the Australian code of practice for the care and use of animals for scientific purposes.

Data accessibility

The raw data used for analysis are available from the Dryad Digital Repository (http://dx.doi.org/10.5061/dryad.qq435) [18].

Authors' contributions

K.W., B.J.P., R.H. and I.C. participated in the design of the study and drafted the manuscript. K.W. processed the data and conducted statistical analysis. All authors gave final approval for publication and agree to be held accountable for the work performed.

Competing interests

We declare we have no competing interests.

Funding

The project was funded by the Centre National de la Recherche Scientifique (CNRS) LIA ‘Multimodal Communication in Marine Mammals’ (McoMM) granted to I.C. K.W. was funded by an International Macquarie University Research Excellence Scholarship. B.J.P. was funded by a Macquarie University Research Excellence Scholarship and a Macquarie University Research Fellowship.