Effect of predation risk on grouping pattern and ...

Acta Theriologica 54 (1): 77–86, 2009. PL ISSN 0001–7051

Effect of predation risk on grouping pattern and whistling behaviour in a wild mouflon Ovis aries population Anna PIPIA, Simone CIUTI*, Stefano GRIGNOLIO, Sara LUCHETTI, Rossana MADAU and Marco APOLLONIO

Pipia A., Ciuti S., Grignolio S., Luchetti S., Madau R. and Apollonio M. 2009. Effect of predation risk on grouping pattern and whistling behaviour in a wild mouflon Ovis aries population. Acta Theriologica 54: 77–86. We studied the effect of predation risk on grouping pattern and whistling behaviour in a free-ranging mouflon Ovis aries Linnaeus, 1758 population in Sardinia. Direct observations were carried out from July 2005 to June 2007 (ngroups = 881, nmouflon = 3477). In our study site, the rut occurred in October and November, when social sexual segregation disappeared, while lambing peaked in April. Groups with lambs (mean ± SE: female groups with lambs 4.98 ± 0.23, mixed groups 6.49 ± 0.29) were larger than male groups (2.01 ± 0.10) and female groups without lambs (2.77 ± 0.11), especially during the lambing season. This reflected the anti-predator tactics adopted by mothers so as to benefit from the dilution effect. Also male aggregations increased in size during the lambing season, as a consequence of the gradual decrease of rutting activities and consequently of male-male aggressiveness. Among the anti-predator tactics adopted by mouflon, whistling behaviour seemed to be a warning signal directed to predators and not to conspecifics. This was because whistling was shown by smaller aggregations only, regardless of group type, presence of lamb and habitat occupied. Smaller groups cannot profit from the dilution effect and therefore may be more motivated to signal the predator that it has been spotted. Department of Zoology and Evolutionary Genetics, University of Sassari, Via Muroni 25 I-07100, Sassari, Italy

Key words: mouflon, group size, predator avoidance, sexual segregation, whistle

and population density (Edmunds 1974, Jarman 1974, Treisman 1975). It should also be noticed that groups may grow larger in open habitats, such as grassland, and smaller in closed forested habitats (Estes 1974, Jarman 1974), being these characterized by physical constraints and poor

Introduction The group pattern preferred by large mammalian herbivores can be associated with anti-predator tactic, energy resource distribution

* Corresponding author – e-mail: [email protected]

[77]

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visual communication. In trying to understand why animals form groups, biologists have focused on the anti-predator benefits related to the increase of group size, including shared vigilance (Lazaurus 1979), dilution of risk (Foster and Treherne 1981, Morgan and Godin 1985), predator swamping (Clark and Robertson 1979), confusion of predators (Neill and Cullen 1974, Milinski 1977) and increased ability to mob predators (Curio 1978). Accordingly, anti-predator behaviour is argued to be a major constraint on behavioural patterns in ungulates (Berger 1978, Risenhoover and Bailey 1985a, b, Festa-Bianchet 1988, Berger 1991, Grignolio et al. 2007), especially when small, vulnerable offspring are present. Pregnant females and females engaged in maternal care are likely to change different aspects of their behaviour, such as aggregation pattern (de Vos et al. 1967, Clutton-Brock and Guinness 1975, Green 1992, Schwede et al. 1993, Boschi and Nievergelt 2003) and anti-predator tactics (Clutton-Brock et al. 1982, Byers and Byers 1983, Bergerud et al. 1984, San José and Braza 1992, Kohlmann et al. 1996, Villaret et al. 1997, Barten et al. 2001). On the other hand, rutting activities reduce the time and energy spent in foraging as well as in looking out for and escaping from predators, and this is especially pronounced in adult males (Dunbar et al. 1990, Lima and Dill 1990, Ciuti et al. 2008). Therefore, variation of group size and aggregation pattern throughout the year may reflect different responses to predation risk by sexes (eg during the lambing and the rutting season). More in general, the different behavioural tactics and foraging strategies shown by males and females throughout the annual biological cycle could be leading factors affecting group type and size of ungulate populations. Accordingly, social segregation between sexes commonly occurs outside the rutting period (Geist 1971, for bighorn Ovis canadensis; Bon and Campan 1989, for mouflon), regardless of proximate and ultimate causations leading to sexual segregation among ungulates (Mooring et al. 2003, Ruckstuhl 2007). Given such a scenario, we studied the effect of predation risk on grouping pattern in a wild

mouflon Ovis aries Linnaeus, 1758 population in Sardinia and focused on such parameters as group size, group type and the degree of social segregation between sexes throughout the annual biological cycle. Specifically, we predicted that, as a consequence of the anti-predator tactics adopted by mouflon: (1) groups with lambs would form larger aggregations than other group types on account of mothers’ need to benefit from the dilution effect to minimize the risk of predation for their lambs; for the same reasons, during the lambing period the number of females would be higher in female groups with lambs than in female groups without lambs; (2) given males’ low aggressiveness outside the rut and assuming the lambs’ need to benefit from the dilution effect during their first weeks of life, all group types would be larger during the lambing period than during the rut; and (3) given the physical constraints and the lack of visual communication which characterize closed forested habitats, groups observed in these habitats would be smaller than those observed in open habitats. Furthermore, beside group size and type, predation risk seems to be able to affect several characteristics of individual behaviours. Specifically, individuals belonging to smaller aggregations could profit from a lower dilution effect against possible attacks by predators (Foster and Treherne 1981, Morgan and Godin 1985) and therefore may try to compensate it by adopting acoustic signals directed towards predators. Indeed, animals show a variety of behaviours when threatened by predators, including acoustic and visual signals, peculiar gaits during flight and specific forms of escape (Hamilton 1971, Edmunds 1974, Sherman 1977, Bertram 1978, Elgar 1989, Caro et al. 2004, Caro 2005). In African bovids, for example, whistling is common in species living in woodland and riverine habitats where visibility is poor, and could thus be used as an alarm signal to conspecifics (Caro 1994). However, Stuart and Stuart (1997) observed that, when disturbed, oribis Ourebia ourebi will give a sharp whistle directed towards the predator and then run off rapidly, possibly to let the predator know that it has been spotted. That whistling behaviour may be a signal to

Anti-predator tactic of Sardinian mouflon

predators, as opposed to conspecifics, was confirmed by Caro et al. (2004) in relation to a large number of ungulate species. Therefore, we further analyzed whistling as a behavioural response to human observers, with reference to group size, group type and habitat type. Specifically, we predicted that: (4) in order to increase the survival of lambs, female aggregations with lambs would show a more frequent occurrence of whistling behaviour; (5) individuals belonging to smaller aggregations would whistle more frequently than those belonging to larger aggregations, given that they benefit from a lower dilution effect; and (6) whistling behaviour would be more frequently exhibited in closed than in open habitats, as a consequence of the lack of visual communication among individuals.

Study area The study was performed in the Montes forest (40°7’N, 9°23’E), Province of Nuoro, a mountainous area located in the centre of Sardinia (Italy). This 4630 ha-wide area (altitude range: 800 to 1401 m a.s.l.) is characterized by a Mediterranean climate with very hot and dry summers, and windy and cold winters. The vegetational cover consists of a mosaic of oaks Quercus ilex, non-native conifer plantations Cedrus atlantica, Pinus nigra, Pinus pinaster, Mediterranean scrubland Arbutus unedo, Erica spp., and meadows mixed with Mediterranean garigue Genista corsica, Cistus incanus, Helicrisum saxatile, Rosmarinus insularis. Large terrestrial predators are absent. The main predator of mouflon in the area is the golden eagle Aquila chrysäetos, which usually preys upon lambs in their first weeks of life (Love and Watson 1990). The area has been protected from any kind of hunting since 1979 and, moreover, mouflon hunting is strictly forbidden everywhere in Sardinia. However, poaching is common in the area and, despite the absence of large predators and the hunting ban, mouflon persist in being elusive and highly suspicious of human presence (Ciuti et al. 2008).

Material and methods Direct observations of mouflon were carried out from July 2005 to June 2007 using eight fixed transects (mean ± SD length of transects: 5.9 ± 1.2 km; total 47.2 km) whose locations were chosen so as to be representative of the available habitat and altitude classes. The transects were walked each month at dawn and dusk by the same four expert observers. Observations were performed using binoculars 10´, telescopes 15–45´, and telemeters 8´. In

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addition to observations carried out along standard transect (n = 541 groups sampled), random observations were collected using the same survey methodology (n = 340 groups). Eventually, 881 groups were sampled over the 24-month monitored period, for a total of 3477 mouflon sightings. Transects in close proximity were covered at the same time by the observers in order to exclude double counts and the following replication of data. Furthermore, 34 collared or ear-tagged mouflon were individually recognizable in the study site, and this helped us to discriminate the mouflon groups which had already been observed in the same transect or in transects in close proximity. Groups were classified following the methodology described by Ciuti et al (2008): male groups (> 1-year-old males), female groups with lambs (³ 1-year-old females, lambs, and 1–2 year-old male yearlings), female groups without lambs (³ 1-year-old females, and 1–2 year-old male yearlings) and mixed groups (³ 1-year-old females, lambs, 1–2 year-old male yearlings, and ³ 2-year-old males). For each observation we collected the following data: age and sex class of each individual, and group type as defined above. Furthermore, we recorded whether a group showed whistling behaviour in response to the human observer. The exact position of each group was assessed with the combined use of a GPS, a topographic map, a compass and a telemeter. Data were digitized and the habitat types used by each observed group were computed in ArcView 3.2. Group sizes were calculated by arithmetic mean (± SE) for comparison with other studies, and by Jarman’s (1974) typical group size (TGS). If compared to the arithmetic mean, TGS is a better representation of the social environment experienced by the average animal in the population, and is defined as: å n12 i=1 TGS = N where n is the group size and N is the total number of animals in all groups. Percentages of sex and age class composition of each group type were also reported. The degree of social sexual segregation was assessed monthly using the sexual segregation and aggregation statistic (SSAS), as recently introduced by Bonenfant et al. (2007). Specifically, SSAS equates to: SSAS = 1 -

X + Y k x i × yi ×å X × Y i=1 x i + yi

where xi is the number of males in the ith group; yi is the number of females in the ith group; k is the number of groups (including solitary animals); X is the total number of males sampled; Y is the total number of females sampled. For a given month, group composition of each year was pooled (Bonenfant et al. 2007). SSAS varies between 0 and 1. This approach provides a general test for the segregation and aggregation patterns observed in our population, also when solitary animals are involved. The major strength of SSAS is its ability to test the null hypothesis of a random association between sexes against two alternatives, segregation or aggregation (see Bonenfant et al. 2007 for more details). In practical terms, SSAS does not assess segregation per se but tests segregation and aggregation in comparison to the random association of males and females. SSAS was computed using the ready-to-use function (Bonenfant et

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al. 2007) in R free software (R Development Core Team 2006). Group sizes were log-transformed and checked for normality (Kolmogorov-Smirnov test) and homoscedasticity (Levene test). In order to test the influence of group type, habitat type and time of the year (on a monthly basis) on each log-transformed group size (dependent variable), we fitted a Linear Mixed Effect (LME) model and considered both the year and the transect as random factors in order to avoid pseudo-replication (Machlis et al. 1985). Specifically, fixed factors in the model were: group type (male groups, female groups with lambs, female groups without lambs, mixed groups), habitat type (pooled into (1) meadows mixed with Mediterranean garigue, (2) Mediterranean scrubland, and (3) woods), and month. As a starting point, we included all main effects and all two-way and three-way interactions in the LME model. Then we removed the non-significant interaction terms and repeated the analysis in a stepwise fashion until all non-significant interaction terms were removed. This procedure enabled us to produce the best model, finally selected following the Akaike Information Criterion (Burnham and Anderson 2002). LME pairwise comparisons with adjustment for multiple comparisons (Bonferroni method) were performed to test differences within each significant fixed factor of the model. In order to test whether mothers joined together to increase the number of group members and to benefit from a higher dilution effect during the lambing period (thus increasing their lamb survival rates), the numbers of females belonging to different group types were compared. Numbers of females belonging to female groups with and without lambs were log-transformed and checked for normality (Kolmogorov-Smirnov test) and homoscedasticity (Levene test). Using the same statistical approach of group size analyses, LME model was fitted for each month in order to test differences between numbers of females in groups with and without lambs.

Male groups (TGS = 3.05) 11%

Female groups without lambs (TGS = 3.55)

In order to investigate the influence of lamb presence, habitat type, group type and group size in evoking whistling behaviour, we fitted a logistic regression. Specifically, we used the logistic regression considering whistle as the binomial dependent variable (0 = no whistling behaviour, 1 = whistling behaviour). We considered log-transformed group size, group type and habitat (both evaluated as categorical data), and number of lambs present in the group as independent variables. A forward stepwise (likelihood ratio) procedure was used in order to detect independent variables that could be successfully included in the model equation. All statistical analyses (excluding SSAS) were performed using the SPSS 13.0 program (SPSS inc., 1989–2004). In all tests significance was set at p < 0.05.

Results Size and pattern of mouflon aggregations and social sexual segregation throughout the year

During the 2-year study, 881 groups and 3477 mouflon were observed. Mean group sizes (± SE) and TGS were as follows: male groups (2.01 ± 0.10, TGS = 3.05, n = 232 groups and 466 mouflon sightings), female groups without lambs (2.77 ± 0.11, TGS = 3.55, n = 180 groups and 483 sightings), female groups with lambs (4.98 ± 0.23, TGS = 6.37, n = 253 groups and 1110 sightings) and mixed groups (6.49 ± 0.29; TGS = 9.44, n = 216 groups and 1418 sightings) (Fig. 1).

Female groups with lambs (TGS = 6.37)

9%

Mixed groups (TGS = 9.44)

3%

6%

28%

40%

52% 89%

91%

57%

14%

Males _ 2 years old) (age >

Females _ 1 year old) (age >

Male yearlings _ age < 2 years old) (1
0.05).

Lambing season

Rutting season

1.0 0.8

SSAS

0.7 0.6 0.5 0.4 0.3 0.2 Jan

Feb

Mar

Apr

May

Jun

Jul

Aug

Sept

Oct

Nov

Dec

Fig. 2. Annual pattern of social sexual segregation/aggregation for mouflon (Montes Forest, Sardinia) tested using the sexual segregation and aggregation statistics (SSAS). SSAS indicates significant sexual segregation or aggregation if the observed value (black point) falls above or below the shaded area (at the 5% error level), respectively. Conversely, SSAS indicates random association between sexes if the observed value falls inside the shaded area. Rutting and lambing seasons are indicated by horizontal lines above the graph.

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Table 1. Linear Mixed Model Analysis of the influence of habitat type, group type and month on mouflon group size (log-transformed) in the Montes Forest, Sardinia. Model selection – Final model including main effects only: AICc = 1483.0, DAICc = 0; discarded model including main effects and two-way interactions: AICc = 1547.8, DAICc = 64.8; discarded model including main effects and both two-way and three-way interactions: AICc = 1595.7, DAICc = 112.7; two-way and three-way interactions: p > 0.05 in all cases.

Variable

df (denominator df = 881)

F

p

Intercept

1

2045.044

< 0.001

Habitat (meadows, Mediterranean scrubland, woods)

2

2.060

0.128

Group type (male groups, female groups with lambs, female groups without lambs, mixed groups)

3

187.419

< 0.001

11

6.740

< 0.001

Month

Lambing season

Rutting season

6

5

Group size (mean + SE)

b, d, f

l

d, f 4 d a d

a

d, f

d

e, a

3

2

LME pairwise comparisons (p < 0.05): b>a d>c f >e Jan

Feb

Mar

Apr

May

Jun

a

a

c, a

Jul

Aug

Sep

Oct

Nov

Dec

Fig. 3. Annual pattern of group size (mean ± SE) recorded for mouflon aggregations in Montes Forest, Sardinia. LME pairwise significant comparisons among natural log-transformed monthly group sizes are reported on the graph. Letters used in LME comparisons refer to abbreviations reported below each error bar. Rutting and lambing seasons are indicated by horizontal lines above the graph.

Anti-predator tactic of Sardinian mouflon

Relationship between whistling behaviour and grouping pattern

The occurrence of whistling was not related to group type (percentages of whistling for each group were: male groups 4.7%, female groups with lambs 7.2%, female groups without lambs 8.2%, mixed groups 5.7%), presence of lamb (whistling groups with lambs 7.2%, without lambs 5.9%) or habitat type (5.2%, 7.6%, 7.9%, whistling groups in meadows mixed with garigue, Mediterranean scrubland, and woods, respectively). According to the forward stepwise procedure group size was the only factor to contribute significantly to whistling occurrence (logistic regression b = –0.466 SE = 0.197, p = 0.018) when group type, habitat, and presence of lambs were excluded. Therefore, only the number of individuals seemed to affect whistling behaviour, given that its occurrence increased when group size decreased.

Discussion Mouflon of the Montes forest formed relatively smaller aggregations than other bovids. For example, Grignolio et al. (2007) recorded larger aggregations (females with offspring TGS = 12.7, females without offspring TGS = 5.1, male groups TGS = 17.7, and mixed groups TGS = 11.6) in Alpine Ibex Capra ibex. The lack of large productive meadows in Sardinia (ie the most attractive habitat for the species, Tsaparis et al. 2008) probably accounts for mouflon smaller aggregations. In a study on mouflon that was performed near Berlin, in Germany, very large aggregations (50–90 individuals) occurred in spring and were all observed in large fields at the time when fresh vegetation was growing (Le Pendu et al. 1995). This dimorphic gregarious species exhibits a high degree of social sexual segregation outside the rut (Pfeffer 1967, Gonzales 1985, Bon and Campan 1989), like other wild (Geist 1971) and feral sheep (Grubb and Jewell 1966). However, Le Pendu et al. (1995) recorded a pronounced social segregation between sexes in mouflon only in summer and opposite values in autumn. The

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use of inadequate methodologies probably accounts for these results. According to our analysis of mixed aggregations appearance as well as to data of Ciuti et al. (2008), mixed groups formed in September (ie during the pre-rutting period) and persisted until late winter, with a peak in October and November. However, the most relevant test in these cases, SSAS (random association vs segregation or aggregation; Bonenfant et al. 2007), provided different results from those provided by either the analysis of mixed group appearance alone or by previous research (eg Le Pendu et al. 1995). Sexual segregation in our study occurred in all months except October and November (ie at the peak of the rutting period). During the rutting period, mouflon rams neither hold harems nor defend territories (Pfeffer 1967), but wander in search of receptive females (following strategy; Gosling 1986). Garel et al. (2005) reported the 22nd of October (± 16 days) to be the median date for the mating season in south France, with most mating occurring between early September and late November. Our data on social sexual segregation showed that the rutting period likely occurred between October and November, ie when sexes did not segregate. In analysing group size variation in relation to group types, we recorded significantly larger sizes in groups with lambs (ie females groups with lambs or mixed aggregations), and this supported our 1st prediction. In fact, groups with lambs were about twice as large as the other group types, and the low female productivity (about 40% of females gave birth to a lamb, Pipia et al., in prep.) could not account for the increase of group sizes. This probably reflects the anti-predator tactics adopted by mothers, which prefer to live in larger aggregations (probably on account of detection and dilution effects; Dehn 1990) and are more susceptible to predators’ presence. In our study, the need to join larger aggregations in order to benefit from a higher dilution effect was stronger in April, ie when newborn lambs are more vulnerable to eagle attacks. In fact, females were more numerous in female groups with lambs than in female groups without lambs in April only, and this supported our 1st prediction. Female groups also showed lon-

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ger flight distances than male aggregations in the presence of human observers (Ciuti et al. 2008). Regardless of habitat type and as a consequence of the annual biological cycle, group sizes showed a significant monthly variation with the highest values occurring during the lambing period and the lowest at the beginning of the rutting season. Indeed, all group types showed a similar pattern in the annual variation of size and this was confirmed by the interaction between group type and time period being not significant. This supported our 2nd prediction, not only in relation to female groups with lambs, but also to other group types. In contrast, our 3rd prediction was not supported by observational data in that habitat type did not affect group size. Our data are consistent with those recorded in a free-ranging mouflon population near Berlin, Germany (Le Pendu et al. 1995), with seasonal variation in group size, and with the lowest values recorded in autumn (mean = 6.1 individuals) and the highest in spring (mean = 9.6 individuals). Pregnant mouflon usually leave their group 5 to 10 days before giving birth (towards the second fortnight of March, Pipia et al., in prep.) in a suitable and isolated place, and stay alone with the newborn for about 5 days after its birth (Briedermann 1993). In total, the isolation period lasts about 14 days in this species (Briedermann 1993) and accounts for the increase of female group sizes recorded from April onwards in our study site, when mothers re-aggregate with other females, thus forming larger groups and decreasing the risk of lambs’ predation (dilution effect: Foster and Treherne 1981, Morgan and Godin 1985). Also male aggregations increased in size during the lambing period. This was due to the decline of rutting activities and the re-aggregation of adult males. In contrast, group sizes were at their smallest in September and increased during the following months. Likewise, Bon et al. (1993) recorded an increasing tendency to aggregate from October to January. In October, animals were sometimes seen alone but most were seen in groups of 2 to 5 individuals (mean = 2.87 ±

0.64) (Bon et al. 1993). In November the proportion of solitary mouflon decreased and the mean group size rose from 4.2 ± 0.91 to 6.8 ± 0.99 (Bon et al. 1993). Probably two simultaneous factors may have determined the tendency of groups to decrease in size during late summer – early autumn. Firstly, males tend to disaggregate, as a consequence of rutting activities. Secondly, the decrease of group sizes proves that a lower attention was paid to predators, in accordance with the reproductive spur that reduces the time and energy spent in foraging as well as in looking out for predators (Dunbar et al. 1990, Lima and Dill 1990). Mixed and female groups including lambs, that is to say the most vulnerable individuals, were larger and could thus profit from the dilution effect against possible attacks by predators (Foster and Treherne 1981, Morgan and Godin 1985). The advantages of living in larger aggregations were further confirmed by the analysis of whistling behaviour. As supposed by Caro et al. (2004), whistling does not seem to be a warning of danger to conspecifics, but rather a signal to predators. As a consequence of the lower dilution effect enjoyed by individuals belonging to smaller groups, it may be reasonably argued that they can compensate it by communicating to the predator that it has been spotted. This was confirmed by the analysis of whistling behaviour as shown by mouflon. Actually whistling behaviour was exhibited by smaller aggregations only, and this was consistent with our 5th prediction. In contrast, our 4th and 6th predictions were not met, given that whistling behaviour was not shown to be related to lamb presence and habitat type, respectively. Had the whistling occurred more frequently in closed habitats, it could have been interpreted as a signal to conspecifics, one prompted by the lack of visual communication among individuals. But this was not the case in our study. Therefore, our results are not in agreement with previous studies asserting that whistling is common in species living in woodland and riverine habitats where visibility is poorer, and could thus serve as an alarm signal to conspecifics (Caro 1994). In fact, our results are in agreement with Caro et al. (2004), who hypothesized that whistling

Anti-predator tactic of Sardinian mouflon

behaviour may be a signal directed to predators, given that in our study this behaviour occurred in smaller and consequently more vulnerable aggregations only. Acknowledgements: We thank the Regione Autonoma della Sardegna for providing funds for this research: in particular we are grateful to P. Onida. We are indebted to the Ente Foreste della Sardegna – Nuoro branch, and to all the people from Orgosolo for their logistical support during our stay in the study area. We also thank F. Ghiandai for his help during data collection. We thank M.W. Hayward, J.-M. Gaillard and two anonymous referees for constructive comments on the first draft of this paper, and C. Bonenfant for useful suggestions about the use of SSAS. During this project, SC and AP were supported by Fondazione del Banco di Sardegna and SocietB Sardegna Resort S.r.l, respectively. The English version was reviewed and edited by A. Binelli.

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