Scent marking is widely recognised to have a crucial function in many species. Most research has focussed on adults and very little is known about scent marking patterns during juvenile development. Using video records of juvenile red fox Vulpes vulpes across 6 years, we tested whether scent marking rates varied with age or sex, or whether juveniles remaining on the natal territory (philopatry) marked more frequently than those that disappeared. Our data show that male juvenile red foxes scent marked more than females during early development, but rates rapidly declined as they aged. In contrast, females showed a significantly later and slower rate of decline. Within females, individuals that remained in the natal area had higher scent marking rates than those that disappeared, suggesting that scent marking has a role in social group affiliation within litters. These results demonstrate that scent marking plays an important role in juveniles, including their intra-litter social interactions

Fawcett, John K.

Soulsbury, Carl

English

University of Lincoln Institutional Repository

 1 Ontogenic patterns of scent marking in red 1 foxes, Vulpes vulpes (Carnivora: Canidae) 2  3 Carl D. Soulsbury1 and John K. Fawcett2 4 1 School of Life Sciences, University of Lincoln, Brayford Pool, Lincoln LN6 7TS 5 2 14 Forest Glade Close, Brockenhurst, Hampshire SO42 7QY 6  7  8  9  10  11 Corresponding author: Carl Soulsbury 12 Email: csoulsbury@lincoln.ac.uk 13 Address: School of Life Sciences 14  University of Lincoln 15 Brayford Pool 16  Lincoln 17  LN6 7TS 18 19  2 Abstract 20 Scent marking is widely recognised to have a crucial function in many species. Most 21 research has focussed on adults and very little is known about scent marking patterns 22 during juvenile development. Using video records of juvenile red fox Vulpes vulpes across 6 23 years, we tested whether scent marking rates varied with age or sex, or whether juveniles 24 remaining on the natal territory (philopatry) marked more frequently than those that 25 disappeared. Our data show that male juvenile red foxes scent marked more than females 26 during early development, but rates rapidly declined as they aged. In contrast, females 27 showed a significantly later and slower rate of decline. Within females, individuals that 28 remained in the natal area had higher scent marking rates than those that disappeared, 29 suggesting that scent marking has a role in social group affiliation within litters. These 30 results demonstrate that scent marking plays an important role in juveniles, including their 31 intra-litter social interactions. 32  33 Key words: sociality, sibling rivalry, dominance hierarchy, urine 34 35  3 Introduction 36 Scent marking may be defined as the deposition of odour by urination, defecation or the 37 release of glandular secretions (Kleiman 1966). In different species and under different 38 ecological conditions, chemical cues found in urine, faeces and scent gland secretions can 39 serve as reliable signals to transmit information about the relative health (Zala et al. 2004), 40 sex (Ferkin & Johnston 1995), social status (Hurst et al. 2001) or reproductive state 41 (Washabaugh & Snowdon 1998) of an individual. In carnivores, scent marking has multiple 42 functions including demarcating territory boundaries, and conveying social and individual 43 information (Gorman & Trowbridge 1998).  44 There are numerous studies of scent marking among adults within populations (e.g. 45 Sillero-Zubiri et al. 1998, Gould & Overdroff 2002). Urine marking has an important social 46 role in many mammal groups, with sex (e.g. Fawcett et al. 2013) and status differences 47 among adult individuals (e.g. Gese & Ruff 1997; Sillero-Zubiri et al. 1998). In contrast, only a 48 few studies have considered scent marking rates of juvenile individuals (e.g. Gese & Ruff 49 1997) and even fewer note ontogenic development of marking. Scent marking behaviours 50 begin relatively early during development (Rasa 1973, Roeder 1984, Sliwa 1996, Sharpe et 51 al. 2012). However, it is unknown at what age they develop or whether there are differences 52 according to sex or social status.  53  Red foxes (Vulpes vulpes) are widespread medium-sized (4-7kg) canids with 54 substantial social and ecological plasticity (Baker & Harris 2004). Scent marking has diverse 55 functions including territorial demarcation and social interactions (Henry 1977, 1980, 56 Macdonald 1979a, Baker et al. 2000, Goszczyński 2002, Macdonald 1979a, Arnold et al. 57 2011). Under some conditions, offspring from previous years remain in the natal territory, 58 leading to the formation of social groups (Macdonald 1979b, Baker et al. 1998, Baker & 59 Harris 2004). Previous work has shown that social behaviour is crucial in determining which 60 cubs remain in the natal territory and which disperse; dispersing individuals had less social 61 interaction (Harris & White 1992) and spent more time away from the home range core 62 areas (Woollard & Harris 1990). Scent marking may be crucial in social interactions among 63  4 juveniles of red fox groups, possibly relating to social status. Despite this possible 64 importance, there are no empirical data on scent marking patterns in litters of red foxes and 65 what drives variation in frequency. This study had three aims: to test whether patterns of 66 scent marking among cubs (1) varied with month; (2) differed between males and females; 67 (3) differed between individuals remaining philopatric or dispersing. 68  69 Materials and Methods 70 Study site and video setup 71 The study site and recording protocols were identical to those described in a previous study 72 (see Fawcett et al. 2013). Briefly, the study site was a largish garden in the New Forest, 73 Hampshire, where foxes regularly attended a feeding station about 15m x 20m, mainly 74 comprising rough lawn backed by shrubs. The openness of the lawn facilitated reliable 75 observations. Foxes were filmed with two infra-red/colour video cameras recording 76 continuously from approximately one hour before sunset throughout each night. The study 77 site was illuminated with six infra-red lamps (Fawcett et al. 2013).  78  79 Data collection 80 Foxes were identified by distinctive morphological features and sex was established 81 by observing the genitalia. All urine markings were recorded; though brief (Henry 1977), 82 they were easily observable (Fawcett et al. 2013). Data were documented according to 83 whether an individual was seen to urine mark or completely abstain during attendance that 84 night. We recorded urine marking by juveniles (0-12 months) from first appearance until they 85 disappeared or became adults (>12 months). We could not ascertain the exact fate of 86 individuals (i.e. whether voluntarily dispersed) but, since most disappearance occurred 87 during the dispersal period (October – March: Soulsbury et al. 2011) and not during peaks of 88 juvenile mortality (e.g. July: Baker et al. 2001), we believe that most disappearances were of 89 dispersing individuals and our categorisation of status as philopatric or dispersed is valid.  90  91  5 Data analysis 92 Data were collated on a daily basis for each individual observed attending the 93 feeding site, for a total of 6 years (spring 2007 to spring 2013). Urination was categorised as 94 binomial (0= no urination, 1= urination observed) irrespective of the number of urine marks 95 observed during the whole night. To assess monthly, sex- and status-specific patterns of 96 urination in cubs we carried out two binomial general linear mixed-effect models with 97 urination (0, 1) as a dependent variable. In the first model (a), we included month, sex 98 (female/male) and their interaction as fixed factors in the model. In the second model (b), we 99 included month, status (philopatric/dispersed) and their interaction; we had sufficient data to 100 analyse females only. For both models, year and individual were included as random 101 factors. Models were run using the lme4 package (Bates et al. 2014) in R 2.14.1 (R 102 Development Core Team 2012).  103  104 Results 105 General 106 We collected data on 14 juvenile foxes (4 males, 10 females), across 6 years, for a total of 107 1676 observations of daily presence/absence of scent marking. For females, 5 were 108 philopatric and 5 disappeared, whereas only 1 male remained philopatric. The peak month 109 for disappearances was October for males (3/3) whereas females disappeared later 110 (October 1/5, December 2/5, February 2/5). 111  112 Sex and ontogenic development of urine marking 113 There was no significant effect of month on overall urine marking rates (Table 1), but the 114 difference between sexes neared significance (P=0.079), whilst the interaction between sex 115 and month was significant (P=0.031; Table 1). Males marked more often than females  in 116 June and July when juveniles were fairly young (3-4 months old), but males’ marking rates 117 declined rapidly as they aged (Fig. 1a), whereas female marking rates declined later and 118 much more slowly (Fig. 1b).  119  6  120 Status and ontogenic variation in scent marking  121 Using data from only females, there was no effect of month or the interaction between 122 month and status (philopatric or dispersing) on urine marking rates (Table 1). In contrast, 123 status was highly significant (Table 1). Individuals that remained philopatric had significantly 124 higher urine marking rates than individuals that dispersed (Fig. 2). 125  126 Discussion  127 The effects of sex and ontogeny on scent marking 128 Our results demonstrated complicated patterns of scent marking in red fox cubs. Male cubs 129 marked more frequently than females during early development (3-4 months old), but this 130 difference disappeared as juvenile foxes became older. This contrasts with other social 131 species: studies of spotted hyaenas during the pre-puberty failed to report sex differences 132 either in the wild (Mills & Gorman 1987) or in captivity (Woodmansee et al. 1991). In 133 sexually dimorphic species with different adult social roles one expects sex differences in 134 scent marking during development (Whitworth & Southwick 1984). However, in 135 behaviourally and physically monomorphic carnivores, like aardwolves Proteles cristatus, 136 one would predict minimal sex differences in early development (Sliwa 1996). Red fox cubs 137 show low, but clear, sexual dimorphism in body size at an early age (Soulsbury et al. 2008). 138 Hence it is likely that that the higher rate of scent marking by male juvenile foxes during 139 June and July reflects some aspect of social relationships possibly including dominance.   140  Red foxes establish a dominance hierarchy when very young (Meyer & Weber 1996) 141 and, like other carnivores, they scent mark when fairly young (Rasa 1973, Roeder 1984, 142 Sliwa 1996). Our results showed that for male juveniles there was a rapid decline in scent 143 marking rates as they aged. In contrast, females showed a later and slower decline. Many 144 social species show a decline in scent marking as they reach maturity, possibly avoiding 145 conflict with adult territory holders (Sliwa 1996). Our data may support this hypothesis for 146 males at least. Male red foxes disperse earlier than females (Soulsbury et al. 2011) and 147  7 conflict with dominant males in social groups may occur earlier for males. Evidence also 148 suggests that the factors linked to dispersal occur earlier in males than in females (Harris & 149 White 1992). Our evidence indicates that this earlier lowering of social group affiliation, or 150 increased within-group conflict among males, leads to earlier reductions in urine marking 151 rates, compared to females.  152  153 Status and scent marking rates in juvenile red foxes 154 In this study, females that disappeared/dispersed had lower rates of scent marking than 155 philopatric individuals. Previous studies have noted that individuals scent mark less during 156 dispersal (Gese and Ruff 1997); this is the first study to report differences in scent marking 157 rates pre-dispersal. In many species, more dominant adults show higher scent marking 158 rates (e.g. Sillero-Zubiri & Macdonald 1998), but there has been little previous study of 159 marking rates within juvenile groups. The only scent marking study comparing differences 160 dependent on social status occurred in a captive spotted hyena colony (Woodmansee et al. 161 1991). Here too, dominant individuals marked more frequently than subordinates 162 (Woodmansee et al. 1991). In red foxes, offspring of subordinate females usually disperse 163 (Whiteside et al. 2010) and dispersing individuals in fox groups are usually subordinate and 164 less socially-bonded pre-dispersal (Woollard & Harris 1990, Harris & White 1992). Our 165 evidence suggests that the social relationships within litters of red foxes already manifests 166 itself in patterns of scent marking.  167 In conclusion, we found the interaction between month and sex affected the 168 frequency of urine marking by juvenile red foxes. Males scent-marked more frequently than 169 females during early development but the frequency quickly declined as they aged. Marking 170 rates decreased later and more gradually in females than in males.  Marking rates were 171 significantly higher among females remaining philopatric than among those 172 disappeared/dispersing. Overall, these results highlight the importance of scent marking 173 during ontogeny. 174  175  8 Acknowledgements 176 We are extremely grateful to Jeanne Fawcett whose help in recording, watching and 177 interpreting the videos was of fundamental importance to this paper.   178  179 References 180 Arnold J., Soulsbury C.D. & Harris S. 2011: Spatial and behavioral changes by red foxes 181 (Vulpes vulpes) in response to artificial territory intrusion. Can. J. 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Ecol. 15: 338-344. 261 262  12 Table 1.  Binomial GLMM output for (a) daily urine marking rates comparing month, sex and 263 their interaction and (b) female daily urine marking rates comparing month, status 264 (philopatric or dispersed) and their interaction  265  266 Model Variable Estimate SE z P (a) (Intercept) -0.84 0.95    Month -0.03 0.04 -0.86 0.391  Sex 2.64 1.51 1.76 0.079  Month x Sex -0.36 0.17 -2.16 0.031 (b) (Intercept) -2.26 1.37    Month 0.05 0.08 0.57 0.566  Status 2.84 0.96 2.97 0.003  Month x Status -0.12 0.10 -1.26 0.206  267 268  13 Figure legends 269 Fig. 1.  Median (± IQR) proportion of daily visits with urine mark (a) male juvenile red foxes 270 and (b) female juvenile red foxes. 271  272 Fig. 2.  Boxplot showing the differences in median proportion of daily visits with urine mark 273 between female red foxes that were philopatric and those that dispersed. 274  275 276  14  277 Figure 1 278  279 280 00.10.20.30.40.50.60.70.80.9Jun. Jul. Aug. Sept. Oct. Nov. Dec. Jan. Feb. Mar.Month00.10.20.30.40.50.60.70.8Jun. Jul. Aug. Sept. Oct. Nov. Dec. Jan. Feb. Mar.MonthProportion of daily visits with a urine mark (a) (b)  15  281  282  283 Figure 2 284 Proportion of daily visits with a urine mark Status 

Ontogenic patterns of scent marking in red foxes, Vulpes vulpes (Carnivora: Canidae)

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