Le Roux, A; Cherry, M I; Manser, M B (2008). The effects of population density and sociality on scent marking in the yellow mongoose. Journal of Zoology, 275(1):33-40. Postprint available at: http://www.zora.uzh.ch University of Zurich Posted at the Zurich Open Repository and Archive, University of Zurich. Zurich Open Repository and Archive http://www.zora.uzh.ch Originally published at: Journal of Zoology 2008, 275(1):33-40.
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Year: 2008
The effects of population density and sociality on scent marking in the yellow mongoose
Le Roux, A; Cherry, M I; Manser, M B
Le Roux, A; Cherry, M I; Manser, M B (2008). The effects of population density and sociality on scent marking in the yellow mongoose. Journal of Zoology, 275(1):33-40. Postprint available at: http://www.zora.uzh.ch
Posted at the Zurich Open Repository and Archive, University of Zurich. http://www.zora.uzh.ch
Originally published at: Journal of Zoology 2008, 275(1):33-40. The effects of population density and sociality on scent marking in the yellow mongoose
Abstract
We investigated scent marking behaviour in the yellow mongoose Cynictis penicillata, focusing on a low-density population where all offspring dispersed upon reaching sexual maturity. Dominant males appeared to be the main territory defenders and demarcators, with offspring foraging and marking only near the territory cores. The cheek-marking rates of dominant males increased during the breeding season and may have been involved in olfactory mate guarding. We compared our low-density population with a high-density population displaying natal philopatry. The two populations differed markedly in terms of individual contributions to territorial marking, as subordinate group members in the low-density population performed almost no territorial marking or defence, but were the primary scent-markers and territory defenders in the high-density population. We discuss scent-marking distinctions between populations in the context of ecological and social differences. 1 Journal of Zoology (2008), 275: 33-40 2 doi: 10.1111/j.1469-7998.2007.00404.x 3 4 5 The effects of population density and sociality on scent marking in the yellow 6 mongoose 7 8 Aliza Le Roux1, Michael I. Cherry1, Marta B. Manser2 9 10 1. Department of Botany and Zoology, University of Stellenbosch, South Africa 11 2. Animal Behaviour, Department of Zoology, University of Zurich 12
13
14 We investigated scent marking behaviour in the yellow mongoose Cynictis penicillata,
15 focusing on a low-density population where all offspring dispersed upon reaching sexual
16 maturity. Dominant males appeared to be the main territory defenders and demarcators,
17 with offspring foraging and marking only near the territory cores. The cheek-marking
18 rates of dominant males increased during the breeding season and may have been
19 involved in olfactory mate guarding. We compared our low-density population with a
20 high-density population displaying natal philopatry. The two populations differed
21 markedly in terms of individual contributions to territorial marking, as subordinate group
22 members in the low-density population performed almost no territorial marking or
23 defence, but were the primary scent-markers and territory defenders in the high-density
24 population. We discuss scent-marking distinctions between populations in the context of
25 ecological and social differences.
26
27 Keywords: mate guarding, population density, scent marking, territory, yellow
28 mongoose
1 1 Introduction
2
3 Scent-marking forms an integral part of the communicative repertoire of many
4 mammals (Eisenberg & Kleiman, 1974; Gorman & Trowbridge, 1989). Marking rates
5 typically increase around the onset of puberty (e.g. Woodmansee et al., 1991), and many
6 mammals are able to discriminate between individuals' scents (Swaisgood, Lindburg &
7 Zhou, 1999; Mendl, Randle & Pope, 2002; Mateo, 2006). In solitary animals, age,
8 gender and territory ownership appear to be the main determinants of scent-marking rates
9 (e.g. in honey badgers Mellivora capensis Begg, du Toit & Mills, 2003), whereas social
10 mammals are, additionally, affected by position in the dominance hierarchy, relative
11 contributions to territory defence, and the frequency of aggressive interactions (e.g.
12 coyotes Canis latrans Gese & Ruff, 1997). Although the dominant male in a group is
13 usually the primary scent marker, subordinate adult group members often contribute
14 substantially to marking and defence (Gese & Ruff 1997; Jordan 2007). Additionally,
15 males may overmark females’ scent, as a form of olfactory mate guarding (e.g. Brashares
16 & Arcese, 1999) or other males’ scents, indicating intrasexual dominance (e.g. Rich &
17 Hurst, 1999). Within a social group, allomarking – marking other individuals – often
18 occurs, probably to maintain a ‘familiar’ group smell and tolerance between group
19 members (e.g. in European badgers Meles meles Buesching, Stopka & MacDonald,
20 2003).
21 Olfactory communication is involved in a variety of functions as diverse as dominance
22 advertisement (e.g. in guinea pigs, Carla porcellus, Drickamer & Martan, 1992) and the
23 marking of food caches (e.g. in in the short-tailed shrew, Blarina brevicauda, Robinson
2 1 & Brodie, 1982). However, in solitary as well as social mammals, scent marks are usually
2 implicated in two primary functions, i.e. territory demarcation and sexual advertisement.
3 Territory holders typically mark and actively defend their home ranges (Ralls, 1971).
4 Scent marks serve as information exchange points (Eisenberg & Kleiman, 1974),
5 containing, inter alia, information on the ability of an owner to defend its territory (Rich
6 & Hurst, 1999). During the breeding season, this information may include indications of
7 oestrus in females (e.g. in kangaroo rats, Dipodomys spectabilis, Randall, 1986), and
8 males may also increase signaling during this season as a form of sexual advertisement
9 (Kappeler, 1998). In some species, the male may attempt to mask the female’s sexual
10 advertisement by overmarking her scent marks, thereby performing mate guarding (e.g.
11 Roberts & Dunbar, 2000; Lewis, 2005).
12
13 As there may be great intraspecific variation in territory size, group composition
14 and degree of sociality in vertebrates (Lott, 1991), scent marking behaviour within a
15 species is potentially variable. For example, the scent marking strategies of hyenas can be
16 strongly affected by territory size. Whereas marks were concentrated in the territory core
17 of large territories (the ‘hinterland’ marking strategy), they were concentrated along the
18 borders (border marking strategy) of smaller territories (Gorman & Mills, 1984). These
19 distinct strategies are seen as the most economical means of marking a territory, ensuring
20 that intruders will come across a scent mark before reaching the protected territory core.
21 However, relatively few studies have performed intraspecific comparisons of scent
22 marking behaviour between populations with different territory sizes, and in particular we
3 1 found no intraspecific comparisons between populations that show different social
2 structures.
3
4 The yellow mongoose Cynictis penicillata dens together with conspecifics in
5 groups ranging between two and 13 individuals in size, but individuals typically forage
6 alone or in pairs (Rasa et al., 1992; Cavallini, 1993). Females are polyestrous,
7 occasionally giving birth to two litters per season, and young typically disperse during
8 spring (Rasa et al., 1992). Similar to many mammals (Ralls, 1971; Gorman &
9 Trowbridge, 1989), the yellow mongoose is territorial and uses various forms of marking
10 in its territory (Earlé, 1981; Wenhold & Rasa, 1994). Yellow mongoose mark vegetation
11 and other prominent objects using anal marks, cheek marks (‘cheek wipes’) and body
12 rubs (‘sidewipes’) (after Earlé, 1981; Wenhold & Rasa, 1994). Body rubbing appears to
13 be a form of self-anointing with odours (including own scent marks) from the
14 environment, rather than the actual deposition of scent, as yellow mongooses lack scent
15 glands on their flanks (Pocock, 1916). Urination and defecation are considered to be
16 secondary forms of marking (e.g. Wenhold & Rasa, 1994), and we have not included the
17 analysis of defecation and urination in this study as there was no evidence of a primary
18 communicative function (le Roux 2007).
19
20 Scent marking in the yellow mongoose has been described in varying degrees of
21 detail in populations of intermediate to high densities [23 – 26 individuals per km2
22 (Balmforth, 2004) to 133 – 200 individuals per km2 (Earlé, 1981; Wenhold & Rasa,
23 1994)]. Of these studies, only Wenhold and Rasa’s (1994) quantified the marking
4 1 behaviour of a group of mongooses (n = 13 group members) and tested specific
2 hypotheses. They presented individuals' marking rates as averages over nine months
3 (April – December) (Wenhold & Rasa, 1994). Whereas Wenhold and Rasa (1994)
4 showed that subordinate adults were the primary territory defenders and markers, Earlé
5 (1981) found in the same Big Island (BI) population in the Vaal Dam (26º52’S, 28
6 º11’E), South Africa, that the dominant males played the main role in this respect.
7
8 We focused our research on a low-density population of yellow mongooses at the
9 Kuruman River Reserve (KRR) in South Africa. The mated pair constituted the only
10 adult members of each group and offspring were not involved in raising new litters but
11 dispersed on reaching sexual maturity. Similar to other low-density populations
12 (Cavallini, 1993), aggression between family members and neighbours was low. In
13 contrast, groups in the BI population consisted of the mated pair, recent offspring and
14 related adults that cooperated in the rearing of young and aggressive territory defence
15 (Earlé, 1981; Wenhold, 1990; Wenhold & Rasa, 1994).
16
17 Here we describe the scent marking behaviour of the KRR population and
18 compare it with the scent marking behaviour of the BI population (Wenhold & Rasa,
19 1994). We predicted that, as in many mammals (Ralls, 1971), the dominant male would
20 be the main territory defender in terms of scent marking and active defence. As territory
21 sizes were much larger in the KRR than the BI population, the KRR population may use a
22 hinterland-marking strategy. We did not expect the adult females or offspring to show
23 strongly territorial behaviour. We predicted that offspring would show no evidence of
5 1 sexual advertisement, as they rarely encountered potential mates before dispersal, and did
2 not stay in the natal territory as adults.
3
4
5 Materials and Methods
6
7 We studied a habituated population of wild yellow mongooses at the Kuruman River
8 Reserve (28°58’S, 21°49’E), South Africa (le Roux, Cherry & Manser, in press). The
9 study area included the dry Kuruman River bed and surrounding dune areas, primarily
10 covered in low shrubs, Acacia trees and grasses (Clutton-Brock et al., 1998). The field
11 site had a large number of bolt-holes and potential sleeping burrows (Manser & Bell,
12 2004) maintained and used by yellow mongooses, meerkats Suricata suricatta and Cape
13 ground squirrels Xerus inauris. During the study period from February 2004 to March
14 2006 we collected data for six adult (dominant) males, 10 of their offspring (four male,
15 six female) and one adult (dominant) female. Offspring were classified as pups (0 – 3
16 months), juveniles (3 – 6 months) and sub-adults (up to 12 months), and adults were older
17 than one year of age. In each group one adult animal was radio collared with collars from
18 Sirtrack© (Havelock North, New Zealand), and non-collared individuals were identified
19 through non-permanent, renewable dye-marks on their fur (for more details, see le Roux
20 et al., in press). We were able to follow all these habituated animals at a distance of less
21 <5 m. We obtained the following number of sessions for individuals: adult males: 30 +
22 2.9 (mean + SE); offspring: 19 + 6.7 and adult female: 14.
23
6 1 During active foraging periods, we recorded the position of focal animals at 10-
2 min intervals and the location of all scent marks, using all-occurrence sampling, on an
3 eTrex Garmin ® (Olathe, KS, USA) global positioning system (GPS), to an accuracy of
4 <10 m. Observational data were collected using a handheld computer (Psion organiser II
5 model LZ64, Bourne End, UK). Each scent marking act was typically preceded by
6 sniffing the object to be marked. We described the object (or individual) marked and
7 whether or not it was within 2m of a bolt-hole or sleeping burrow. During morning
8 observation sessions we noted all marking acts from the time of emergence, but hourly
9 marking rates were determined using only data from active foraging periods away from
10 the sleeping burrow in the morning and afternoon. Some marking occurred at the sleeping
11 burrow before foraging trips, and these data were included in the ArcView GIS data
12 which we used to determine scent-mark densities.
13
14 Spatial data were analysed using ArcView GIS and its animal movements
15 extension (Hooge, Eichenlaub & Solomon, 1999). Using all coordinates recorded at t10-
16 minute intervals, we determined home-range sizes as the 95% kernel, with least-squares
17 cross-validation smoothing factors (Worton, 1989; Seaman et al., 1999). Although
18 autocorrelation between successive data points may reduce the accuracy of home range
19 estimations (Swihart & Slade, 1985), we used a data collection protocol that allowed us
20 to retain all these data in our calculations. The effect of autocorrelation is typically
21 addressed by subsampling the spatial dataset (e.g. Jordan, Cherry & Manser, 2007).
22 However, de Solla, Bonduriansky & Brooks (1999) demonstrated that using the entire
23 dataset could improve home range estimations substantially, compared to sub-sampling,
7 1 if data were collected with a constant sampling interval over an extended period of time.
2 Our regular data collection spanning several months satisfied these recommendations and
3 the number of GPS points per individual (adult males: 310 + 64.3 (mean + SD);
4 offspring: 115 + 60.2; dominant female: 80 points) exceeded the recommended minimum
5 of 50 points for home range estimations (Seaman et al., 1999).
6
7
8
9 65% (territory core) # ## # # # # # 85% (kernel border) # # ## 95% (territory border) ## # # # # # # 10 # # # # # # # # # ## # # ## # # # # 11 # # # # ## ### # # # # # # #### # ## # ### # # # # # # # # # 12 # ## # ### # ### # # ## # # # ## # ###### ## # # ##### # # # # # ############ # # # # ########### # # ## ### # # # ## # # # # # # # # # ### # # # # # ### # # # # 13 # # # ## # #### ## # ### ## ################ # # # ## ############# # # # # # ### #### # # # ##### ######## # # # # # # # ################### # # # ## ### # # # ## # ### ###### # ### # ########## # ### # ##### ## # # # ###### ## ## ############### ## ############## # ######### 14 # ######### ########### ## ### # # ## ## ####### # # ######### # ############# # 15 # Overlap zone between neighbouring territories
N 16 W E
0.7 0 0.7 1.4 Kilometers 17 S
18
19 Fig. 1. The main subdivisions of territory areas are shown for dominant male CM03. 20 Anal marks indicated by filled circles. The density of anal marks appears higher in the 21 area where neighbouring territories overlapped. 22
23
24 We defined adult males’ home ranges as territories, as these areas were defended
25 against intruders from other groups (Maher & Lott, 1995). The undefended areas
8 1 occupied by offspring and the dominant female were termed home ranges, as we never
2 observed intruder defence in these locations. We defined core and border areas (Fig. 1)
3 following Jordan et al.s’ (2007) categorization of meerkat territory areas at the same
4 study site. The area between the 85% and 95% kernel was the ‘territory border’ and the
5 65% kernel was the ‘territory core.’ The area between the territory border and core was
6 the ‘kernel border.’ Densities of scent marks were calculated for each of these areas and
7 also for the whole area inside the border (i.e. the entire 85% kernel).
8
9 Owing to small sample sizes, we used mainly nonparametric statistical techniques
10 (Siegel & Castellan, 1988), in the programme R for Microsoft Windows, version 2.3.1 (R
11 Development Core Team, 2006). When t-tests were appropriate, we used unequal
12 variance t-tests of the ranked data (Ruxton, 2006). Results are all presented as means +
13 SE unless indicated otherwise. During the summer season we could not record all
14 activities, for individuals were usually highly active after sunset and impossible to follow
15 even with night vision goggles. In summer, adults were primarily babysitting at the
16 sleeping burrow during daylight hours and started foraging late in the afternoon, not
17 returning from foraging and, presumably, scent marking, until after dark. Out of 201
18 summer observation sessions, mainly focused on habituation, we obtained eight ad
19 libitum foraging sessions in total, for three adult males. This number of sessions was too
20 small to compare statistically with the six to 14 sessions per adult male (n = 6) obtained
21 for each of the other seasons.
22
23
9 1 Results
2
3 Home range sizes and scent mark locations
4 Yellow mongoose densities in the KRR population varied between four (non-breeding
5 season) and 14 (breeding season) individuals per km2. Groups consisted of 3.7 + 0.4
6 members (range: 2-7), including offspring. Dominant male territories were 0.76 + 0.21
7 km2 in size (n = 6), ranging between 0.17 and 1.53 km2, with a perimeter length of 5.49 +
8 0.96 km. These territory sizes remained constant across seasons. Each male’s territory
9 completely encompassed the home ranges of his offspring, which were far smaller at 0.18
10 + 0.20 km2 (n = 10; range: 0.11 - 0.28 km2) with a 2.34 + 0.19 km perimeter length. The
11 only dominant female that we followed had a home range size of 0.20 km2 (perimeter
12 length: 3.05 km) near the centre of her mate’s territory, which was 1.11 km2 in size.
13 Dispersing animals established new territories 2.5 + 0.4 km (n = 6) from their natal
14 territories.
15
16 Territorial defence
17 Only dominant males were observed to patrol territory borders, whereas their offspring
18 remained within a smaller area inside the males’ territories, marking at low rates (Table
19 1). The scent marking rates of dominant males were significantly higher than those of
20 their offspring (unequal variance t-test: anal marks: t15.9 = 6.97, P < 0.001; cheek marks:
21 t12.0 = 4.33, P < 0.001; body rubs: t10.0 = 5.60, P < 0.001).
22
23
10 1 Table 1. Average scent marking rates (marks per hour, mean + SE) for the dominant 2 males (n = 6), offspring (n = 10), and one dominant female habituated at the Kuruman 3 River Reserve. Significant differences were found between dominant males and offspring 4 in terms of glandular marking rates. 5 Identity Anal mark Cheek mark Body rub Dominant male 9.11 + 2.01 4.80 + 1.13 1.89 + 0.47 Offspring 1.08 + 0.22 0.80 + 0.56 0.28 + 0.14 Adult female 1.02 + 0.60 0.55 + 0.28 0.04 + 0.04 6
7 Some differences were evident in the density of dominant males’ scent marks
8 throughout their territories (Table 2). Anal marks in the territory core were denser than in
9 the territory border as well as in the kernel border, but denser on the territory border than
10 in the kernel border (Kruskal-Wallis Anova: χ²2 = 12.43, P = 0.002; post hoc tests: P <
11 0.05). There were no differences between these areas in cheek mark density (χ²2 = 4.53, P
12 = 0.104) or ‘body rub’ density (χ²2 = 4.10, P = 0.129).
13
14 Table 2. Dominant male (n = 6) scent mark densities, presented as number of marks per 15 km2 (mean + SE). Different parts of territories are based on kernel methods (elaborated 16 on in text and Fig. 1). 17 Territory core Kernel border Territory border Type of mark 85% kernel (65% kernel) (65 - 85%) (>85% kernel) Anal mark 1391.1 + 784.4 145.2 + 22.3 640.6 + 284.4 258.8 + 37.9 Cheek mark 881.0 + 576.2 142.1 + 97.5 432.0 + 270.6 162.0 + 63.0 Body rub 213.3 + 91.1 24.1 + 15.1 103.7 + 44.3 37.5 + 12.3 18
19
20 Sexual advertisement: seasonal changes and overmarking
21 There was some seasonal variation in the hourly marking rate of adult males (Fig. 2), but
22 offspring’s marking rates did not vary across seasons (Fig. 3). Dominant males’ cheek-
23 marking rates were higher during ( spring (pre-breeding season) than autumn (post-
24 breeding season; Kruskal-Wallis Anova: χ²2 = 8, P = 0.018), and body-rubbing rates
11 1 differed in the same respect (χ²2 = 6.26, P = 0.044). Anal-marking rate did not differ
2 between seasons (χ²2 = 3.14, P = 0.208). None of the offspring’s marking rates (Fig. 3)
3 were affected by month of the year or age.
4
8
autumn 7 * * winter spring 6
5
4
3
Hourly marking rate marking Hourly 2
1 ▲ ▲ ▲ 0 ▲ anal mark cheek mark body rub Type of mark 5 6 Fig. 2. Dominant male scent marking rates as affected by season (* P < 0.05). Summer 7 marking rates (for n = 3 males) were 7.1 + 2.0 per hour for anal marks, 1.9 + 0.7 for 8 cheek marks, and 2.5 + 0.8 for body rubs. Filled triangles represent average marking rates 9 of dominant males in a high density population, calculated across nine months, which 10 excluded the summer season (after Wenhold & Rasa, 1994). 11 12 13 No overmarking was observed between adults and offspring, even though group
14 members were observed foraging together. However, the area where the dominant female
15 deposited most of her cheek marks was a location where her mate concentrated a high
16 number of cheek marks (15 marks in a 10m radius). Her anal marks were in an area
17 where the male also marked anally, but the closest male anal mark was 20m from her
18 marks.
19
20
12 1
1.6 pup 1.4 juvenile subadult 1.2
1
0.8
0.6
Hourly marking rate marking Hourly 0.4 ▲ ▲▲ 0.2
0 anal mark cheek mark body rub Type of mark 2 3 Fig. 3. Offspring scent marking rate as a function of age class. Scent marking rates were 4 not affected by age or season. Filled triangles are average marking rates for ‘juvenile’ (< 5 1 year old) yellow mongooses in a high density population, calculated across nine 6 months, which excluded the summer season (after Wenhold & Rasa, 1994). 7
8
9 When offspring dispersed (spring season), dominant-male marking rates increased
10 (Fig. 2). However, this increase was not focused specifically in the territory core, where
11 offspring used to mark. Although a high proportion of marks were made in the territory
12 core (Fig. 4), the distribution of marks did not vary across seasons for anal marks
13 (Friedman Anova: χ²2 = 0.4, P = 0.819) or body rubs (χ²2 = 0.4, P = 0.819). Cheek-mark
14 distribution varied, however (χ²2 = 7.6, P = 0.022), as winter and autumn proportions
15 were significantly higher than spring proportions (post hoc tests: P < 0.05). Relatively
16 more cheek marks were therefore located outside the territory core during spring.
17
13 0.9 autumn * winter 0.8 spring
0.7
0.6
0.5
0.4 Proportion of marks in core Proportion of marks 0.3
0.2 anal mark cheek mark body rub Type of mark 1
2 Fig. 4. The proportion of dominant male scent marks that were made inside territory 3 cores, according to season. The proportion of cheek marks inside the territory core was 4 significantly smaller in spring than in winter and autumn. (* P < 0.05) 5
6
7 Discussion
8
9 Territoriality
10 In the low-density KRR population, only the dominant males were observed to defend
11 and mark their territories, in contrast to the high-density BI population, where especially
12 subordinate individuals maintained the territory borders (Wenhold & Rasa, 1994). In
13 obligate social carnivores, the dominant male is usually the main scent marker, but group
14 members often contribute substantially to territory defence and scent marking, for
15 example in Ethiopian wolves Canis simensis (Sillero-Zubiri & MacDonald, 1998), and
16 meerkats (Jordan et al., 2007). Group defence appears to occur together with other
17 cooperative behaviours, such as the communal rearing of young (Sillero-Zubiri &
14 1 Gottelli, 1994; Clutton-Brock et al. 2001). Unlike the KRR population, subordinate
2 mongooses in the BI population not only share the mated pair’s territory, but contribute to
3 the rearing of their subsequent litters (Wenhold, 1990; Balmforth, 2004), which may
4 explain why their pattern of territory defence resembles that of obligate social carnivores.
5
6 Dominant males in the low-density population had high marking rates compared
7 to individuals in the high-density population, but group’ cumulative marking rates were
8 similar between populations (see Wenhold & Rasa, 1994). Territories in the BI
9 population were five times smaller than those at KRR, implying a five times greater
10 density of scent marks in BI territories. This probably allowed dominant males in the BI
11 population to use the border-marking strategy in territory defence (sensu Gorman &
12 Mills, 1984). The hinterland-marking strategy (Gorman & Mills, 1984) used by dominant
13 males in the large KRR territories is used by a number of carnivores such as the solitary
14 honey badgers (Begg et al., 2003), and social meerkats (Jordan et al., 2007). This strategy
15 reflects the need to protect core resources, such as sleeping burrows and feeding sites, in
16 large territories where intruders may not come across border marks while traveling
17 through an area (Gorman & Mills, 1984; Jordan et al., 2007).
18
19 As with other herpestids (Rasa, 1973; Baker, 1982; Baker, 1988), anal marking
20 was the predominant form of territorial marking in yellow mongooses. Anal gland
21 secretions in the yellow mongoose (Apps, Viljoen & Taylor, 1989) and other herpestids
22 function as long-lasting markers carrying information on individual identity (Rasa, 1973;
23 Hefetz, Ben-Yaacov & Yom-Tov, 1984; Decker, Ringelberg & White, 1992). Dominant
15 1 males in the KRR population increased body-rubbing rates during spring, when intruder
2 pressure increased as dispersers attempt to find new territories. Males also had high anal
3 marking and body rubbing rates after dispersal, while establishing new territories. The
4 combination of anal marking, border latrines (le Roux, 2007) and body rubbing could
5 function as a scent-matching system of territory defence (Gosling, 1982), whereby
6 intruders match the scent of territorial marks with the scent of the owner when
7 encountering this individual. The scent-matching system is found in various mammals,
8 including beavers Castor canadensis (Sun & Müller-Schwarze, 1998), and snow voles
9 Chionomys nivalis (Luque-Larena, Lou Pez & Gosaulbez, 2001). This facilitates
10 recognition of ownership, which in turn reduces the aggression of agonistic interactions,
11 to the mutual advantage of intruder and owner (Gosling & McKay, 1990).
12
13 Aggression between familiar neighbours appeared to be low in the KRR
14 population. During more than 100h of observing two habituated neighbours, we observed
15 only five encounters, which were brief chases and fighting (<2 min in duration) that did
16 not appear to draw blood. Adult males had almost no visible scars, and territory
17 expansion into neighbouring territories was never observed. Preliminary experiments
18 with fresh faeces from foreign (non-neighbouring) males (A. le Roux, unpublished data)
19 indicated that foreign males’ latrines always provoked an immediate countermarking
20 reaction. Latrines of familiar neighbours typically evoke only sniffing (le Roux, 2007).
21 Such a tolerance of familiar neighbours, with higher aggression against unfamiliar
22 intruders, is known as the ‘dear enemy’ effect (Fisher, 1954), and occurs in a variety of
23 territorial species (reviewed in Temeles, 1994). This contrasts with the ‘nasty neighbours’
16 1 effect found in, for example, banded mongooses, Mungos mungo (Müller & Manser,
2 2007), that treat neighbours more aggressively than transients because groups readily
3 expand into neighbouring territories. In high-density populations of yellow mongooses,
4 intergroup encounters appeared to be more violent and frequent (Wenhold & Rasa, 1994;
5 Balmforth, 2004) and scent-mark densities were much higher than the KRR population.
6 This may be ascribed to the definite risk of territory reduction in areas with high territory
7 saturation.
8
9 Sexual advertisement?
10 In the low-density population there was no support for Wenhold & Rasa’s (1994)
11 hypothesis that scent marking is used as sexual advertisement by subordinate individuals.
12 Whereas mongooses in the BI population found mating opportunities in neighbouring
13 groups (Wenhold & Rasa, 1994), sexually mature offspring in the KRR population
14 dispersed to new territories beyond neighbouring groups. The marks of offspring in the
15 low-density population may, however, have functioned in intra-group communication.
16 Allo-marking, displayed by high-density yellow mongoose populations (Earlé, 1981) and
17 social mongooses such as the dwarf mongoose Helogale undulata (Rasa, 1973), was
18 extremely rare in the KRR population. In the absence of such a ‘group odour’ (sensu
19 Sheppard & Yoshida, 1971) familiarity could be established through scent marks they
20 encountered on the substrate. In other group-living mammals, such as the collared
21 lemming Dicrostonyx groenlandicus (Huck & Banks, 1979), the familiarity of an
22 individual’s scent has been shown to reduce aggression from the dominant male. The
23 scent marks of KRR offspring may therefore have facilitated tolerance by the dominant
17 1 male during the time they shared a home range. In addition, offspring scent marks could
2 have augmented dominant male marks around key resource areas, thereby contributing to
3 territorial defence (Revilla & Palomares, 2002). However, dominant males did not
4 ‘compensate’ for the absence of these marks once offspring dispersed.
5
6 Dominant males’ cheek marking rates increased when offspring dispersed, but
7 this increase was primarily outside the territory core, and could have been related to
8 higher intruder pressure during this season, rather than the decrease in number of group
9 members. In water mongooses, Atilax paludinosus (Baker, 1988), and dwarf mongooses
10 (Rasa, 1973), cheek marks appear to carry a short-lived threatening message. During
11 fights between males, scent from cheek glands is probably exchanged, as yellow
12 mongooses attack the face and neck of their rivals (ALR, personal observation). Yellow
13 mongoose cheek marks were concentrated around bolt-holes, which are noticeable
14 landmarks regularly inspected by other yellow mongooses, especially adult males.
15 Limited data suggested that a dominant male over-marked the area that his mate cheek
16 marked. It is therefore probable that cheek marks had a function in mate guarding
17 (Roberts & Dunbar, 2000; Lewis, 2005), although the possibility of male sexual
18 advertisement could not be excluded.
19
20 Conclusion
21 The scent-marking patterns of yellow mongooses were affected by the long-term group
22 composition. In temporary groups where the mated pair constituted the only long term
23 residents in a territory, marking behaviour resembled that of solitary territorial mammals,
18 1 with only the dominant male appearing to defend and mark his territory. Natal philopatry
2 in high-density populations may have implications for increased facultative cooperation
3 that includes cooperation in scent marking and inter-group contests. Larger groups in
4 high-density populations interact with neighbours more frequently, causing more conflict
5 but also opportunities for mating and sexual advertisement between neighbours. Although
6 none of these results are unexpected, considering the characteristics of the different
7 populations, this may be the first mammalian study to show how individuals’ scent
8 marking patterns can be affected by intra-specific fluctuations in social structure rather
9 than just group/ territory size.
10
11
12 Acknowledgements
13 We thank Tim Clutton-Brock, University of Cambridge, for allowing us to use facilities
14 at the KRR. Thanks are also due to Helen Eaton and Samuel Guiton for their help in data
15 collection and Gilberto Passinelli for advice concerning spatial analyses. We are grateful
16 for the comments of anonymous reviewers, which improved earlier drafts of this
17 manuscript. This study was partially funded by grants to A.L.R. from the Roche Research
18 Foundation (Switzerland) and the Harry Crossley Foundation, a grant to M.I.C. from the
19 National Research Foundation (South Africa), and the Swiss National Foundation to
20 M.B.M. (SNF Förderprofessur).
19 1 References
2
3 Apps, P. J., Viljoen, H. W. & Taylor, P. J. (1989). Volatile components from the anal
4 glands of the yellow mongoose Cynictis penicillata. S. Afr. J. Zool. 24: 361-362.
5 Baker, C. M. (1982). Methods of communication exhibited by captive slender mongooses
6 Herpestes sanguineus. S. Afr. J. Zool. 17: 143-146.
7 Baker, C. M. (1988). Scent marking behaviour in captive water mongooses (Atilax
8 paludinosus). Z. Saugertierk. 53: 358-364.
9 Balmforth, Z. E. (2004). The demographics, spatial structure and behaviour of the yellow
10 mongoose, Cynictis penicillata, with emphasis on cooperative breeding. PhD
11 thesis, University of Sussex, England.
12 Begg, C. M., du Toit, J. T. & Mills, M. G. L. (2003). Scent-marking behaviour of the
13 honey badger, Mellivora capensis (Mustelidae), in the southern Kalahari. Anim.
14 Behav. 66: 917-929.
15 Brashares, J. S. & Arcese, P. (1999). Scent marking in a territorial African antelope: II.
16 The economics of marking with faeces. Anim. Behav. 57: 11-17.
17 Buesching, C. D., Stopka, P. & MacDonald, D. W. (2003). The social function of allo-
18 marking in the European badger (Meles meles). Behaviour 140: 965-980.
19 Cavallini, P. (1993). Spatial organization of the yellow mongoose Cynictis penicillata in
20 a coastal area. Ethol. Ecol. Evol. 5: 501-509.
21 Clutton-Brock, T. H., Brotherton, P. N. M., O'Riain, M. J., Griffin, A. S., Gaynor, D.,
22 Kansky, R., Sharpe, L. & McIllrath, G. M. (2001). Contributions to cooperative
23 rearing in meerkats. Anim. Behav. 61: 705-710.
20 1 Clutton-Brock, T. H., Gaynor, D., Kansky, R., MacColl, A. D. C., McIllrath, G.,
2 Chadwick, P., Brotherton, P. N. M., O'Riain, M. J., Manser, M. & Skinner, J. D.
3 (1998). Costs of cooperative behaviour in suricates (Suricata suricatta). Proc. R.
4 Soc. Lond., B 265: 185-190.
5 Decker, D. M., Ringelberg, D. & White, D. C. (1992). Lipid components in anal scent
6 sacs of three mongoose species (Helogale parvula, Crossarchus obscurus,
7 Suricata suricatta). J. Chem. Ecol. 18: 1511-1524.
8 Earlé, R. A. (1981). Aspects of the social and feeding behaviour of the yellow mongoose
9 Cynictis penicillata (G. Cuvier). Mammalia 45: 143-152.
10 Eisenberg, J. F. & Kleiman, D. G. (1974). Olfactory communication in mammals. Ann.
11 Rev. Ecol. Syst. 3: 1-32.
12 Fisher, J. B. (1954). Evolution and bird sociality. In Evolution as a process: 71-83.
13 Huxley J., Hardy A. C. and Ford E. B. (Ed.). London: Allen & Unwin.
14 Gese, E. M. & Ruff, R. L. (1997). Scent-marking by coyotes, Canis latrans: the influence
15 of social and ecological factors. Anim. Behav. 54: 1155-1166.
16 Gorman, M. L. & Mills, M. G. L. (1984). Scent marking strategies in hyaenas
17 (Mammalia). J. Zool., Lond. 202: 535-547.
18 Gorman, M. L. & Trowbridge, B. J. (1989). The role of odor in the social lives of
19 carnivores. In Carnivore Behavior, Ecology and Evolution: 57-88. Gittleman J. L.
20 (Ed.). London: Chapman & Hall.
21 Gosling, L. M. (1982). A reassessment of the function of scent marking in territories.
22 Zeitschrift für Tierpsychologie 60: 89-118.
21 1 Gosling, L. M. & McKay, H. V. (1990). Competitor assessment by scent matching: an
2 experimental test. Behav. Ecol. Sociobiol. 26: 415-420.
3 Hefetz, A., Ben-Yaacov, R. & Yom-Tov, Y. (1984). Sex specificity in the anal gland
4 secretion of the Egyptian mongoose Herpestes ichneumon. J. Zool., Lond. 183:
5 205-209.
6 Hooge, P. N., Eichenlaub, W. & Solomon, E. (1999). The animal movement program.
7 USGS: Alaska Biological Science Center.
8 Huck, U. W. & Banks, E. M. (1979). Behavioral components of individual recognition in
9 the collared lemming (Dicrostonyx groenlandicus). Behav. Ecol. Sociobiol. 6: 85-
10 90.
11 Jordan, N. R. (2007). Scent-marking investment is determined by sex and breeding status
12 in meerkats. Anim. Behav. 74: 531-540.
13 Jordan, N. R., Cherry, M. I. & Manser, M. B. (2007). Latrine distribution and patterns of
14 use by wild meerkats: implications for territory and mate defence. Anim. Behav.
15 73: 613-622.
16 Lewis, R. J. (2005). Sex differences in scent-marking in sifaka: mating conflict or male
17 services? Am. J. phys. Anthrop. 128: 389-398.
18 Luque-Larena, J. J., Lou Pez, P. & Gosaulbez, J. (2001). Scent matching modulates space
19 use and agonistic behaviour between male snow voles, Chionomys nivalis. Anim.
20 Behav. 62: 1089-1095.
21 Lynch, C. D. (1980). Ecology of the suricate, Suricata suricatta and yellow mongoose,
22 Cynictis penicillata with special reference to their reproduction. Memoirs of the
23 National Museum of Bloemfontein 14: 1-144.
22 1 Maher, C. R. & Lott, D. F. (1995). Definitions of territoriality used in the study of
2 variation in vertebrate spacing systems. Anim. Behav. 49: 1581-1597.
3 Manser, M. B. & Bell, M. B. (2004). Spatial representation of shelter locations in
4 meerkats, Suricata suricatta. Anim. Behav. 68: 151-157.
5 Müller, C. A. & Manser, M. B. (2007). ‘Nasty neighbours’ rather than ‘dear enemies’ in a
6 social carnivore. Proc. R. Soc. Lond., B 274: 959-965.
7 Pocock, R. I. (1916). On the external characters of the mongooses (Mungotidae). Proc.
8 Zool. Soc. Lond. 1916: 349-374.
9 R Development Core Team. (2006). R: A language and environment for statistical
10 computing. Vienna, Austria: R Foundation for Statistical Computing.
11 Ralls, K. (1971). Mammalian scent marking. Science 171: 443-449.
12 Rasa, O. A. E. (1973). Marking behaviour and its social significance in the African dwarf
13 mongoose, Helogale undulata rufula. Zeitschrift für Tierpsychologie 32: 293-318.
14 Rasa, O. A. E., Wenhold, B. A., Howard, P., Marais, A. & Pallett, J. (1992).
15 Reproduction in yellow mongoose revisited. S. Afr. J. Zool. 27: 192-195.
16 Revilla, E. & Palomares, F. (2002). Spatial organization, group living and ecological
17 correlates in low-density populations of Eurasian badgers, Meles meles. J. Anim.
18 Ecol. 71: 497-512.
19 Rich, T. J. & Hurst, J. L. (1999). The competing countermarks hypothesis: reliable
20 assessment of competitive ability by potential mates. Anim. Behav. 58: 1027-
21 1037.
23 1 Roberts, S. C. & Dunbar, R. I. M. (2000). Female territoriality and the function of scent-
2 marking in a monogamous antelope (Oreotragus oreotragus). Behav. Ecol.
3 Sociobiol. 47: 417-423.
4 le Roux, A. (2007). Communication in the yellow mongoose, Cynictis penicillata. PhD
5 Thesis, Stellenbosch University, South Africa.
6 le Roux, A., Cherry, M. I. & Manser, M. B. (in press). The audience effect in a
7 facultatively social mammal, the yellow mongoose, Cynictis penicillata. Anim.
8 Behav.
9 Ruxton, G. D. (2006). The unequal variance t-test is an underused alternative to Student's
10 t-test and the Mann-Whitney U test. Behav. Ecol. 17: 688-690.
11 Seaman, D. E., Millspaugh, J. J., Kernohan, B. J., Brundige, G. C., Raedeke, K. J. &
12 Gitzen, R. A. (1999). Effects of sample size on kernel home range estimates. J.
13 Wildl. Man. 63: 739-747.
14 Sheppard, D. H. & Yoshida, S. M. (1971). Social behavior in captive Richardson's
15 ground squirrels. J. Mammal. 52: 793-799.
16 Siegel, S. & Castellan, N. J., Jr. (1988). Nonparametric Statistics for the Behavioral
17 Sciences. New York: McGraw-Hill Book Company.
18 Sillero-Zubiri, C. & Gottelli, D. (1994). Canis simensis. Mammalian Species 485: 1-6.
19 Sillero-Zubiri, C. & MacDonald, D. W. (1998). Scent-marking and territorial behaviour
20 of Ethiopian wolves Canis simensis. J. Zool., Lond. 245: 351-361.
21 Sun, L. & Müller-Schwarze, D. (1998). Beaver response to recurrent alien scents: scent
22 fence or scent match? Anim. Behav. 55: 1529-1536.
24 1 Swaisgood, R. R., Lindburg, D. G. & Zhou, X. (1999). Giant pandas discriminate
2 individual differences in conspecific scent. Anim. Behav. 57: 1045-1053.
3 Swihart, R. K. & Slade, N. A. (1985). Testing for independence of observations in animal
4 movements. Ecology 66: 1176-1184.
5 Temeles, E. J. (1994). The role of neighbours in territorial systems: when are they 'dear
6 enemies'? Anim. Behav. 47: 339-350.
7 Wenhold, B. A. (1990). The ethology and social structure of the yellow mongoose,
8 Cynictis penicillata. MSc thesis, University of Pretoria, South Africa.
9 Wenhold, B. A. & Rasa, O. A. E. (1994). Territorial marking in the yellow mongoose
10 Cynictis penicillata: sexual advertisement for subordinates? Z. Saugertierk. 59:
11 129-138.
12 Woodmansee, K. B., Zabel, C. J., Glickman, S. E., Frank, L. G. & Keppel, G. (1991).
13 Scent marking (pasting) in a colony of immature spotted hyenas (Crocuta
14 crocuta): a developmental study. J. Comp. Psychol. 105: 10-14.
15 Worton, B. J. (1989). Kernel methods for estimating the utilization distribution in home-
16 range studies. Ecology 70: 164-168.
17
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