Placental scar counts and litter size estimations in ranched red foxes (Vulpes vulpes)

Mammalian Biology

Mamm. biol. 68 (2003) 391±393 ã Urban & Fischer Verlag http://www.urbanfischer.de/journals/mammbiol

Zeitschrift fuÈr SaÈugetierkunde

Short communication

Placental scar counts and litter size estimations in ranched red foxes (Vulpes vulpes) By M. ELMEROS, VIVI PEDERSEN, and TRINE-LEE WINCENTZ National Environmental Research Institute, Department of Landscape Ecology, Rùnde, and Zoological Institute, University of Copenhagen, Copenhagen, Denmark Receipt of Ms. 23. 12. 2002 Acceptance of Ms. 14. 05. 2003

Key words: Vulpes vulpes, litter size, placental scars Reproductive performance is an important parameter in studies on population dynamic. Investigations based on direct observations of sparsely distributed or secretive species usually involve small sample sizes. Estimation of reproductive parameters is feasible by placental scar counts (PSC) in mammals although scars from resorption and abortion results in discrepancies between estimated and true litter size (Wydoski and Davis 1961). The assessment of litter size from PSC is further complicated in some species as scars from more than one breeding cycle are visible, e. g. the red fox (Vulpes vulpes) (reviewed in LindstroÈm 1981; Wandeler and LuÈps 1993). PSC of fresh scars in red foxes culled during or shortly after the breeding season present reliable estimates of whelping frequencies and litter sizes (Cavallini and Santini 1996; Heydon and Reynolds 2000). However, in countries where hunting is restricted to the autumn and winter seasons reproductive parameters must be estimated from vixens with older placental scars. LindstroÈm (1981, 1994) presented methods to estimate litter size from vixens killed through the whole year. Despite variations among species only few studies have tested the reliability of PSC on animals with known litter size (Sanderson 1950; Strand 1616-5047/03/68/06-391 $ 15.00/0.

et al. 1995). The aim of this study was to evaluate the accuracy of PSC by comparing estimated litter size with known litter size in red foxes. We examined 48 commercially ranched female red foxes between 1ݱ4Ý years old. All foxes had been mated during the previous mating season. Older foxes had produced litters each year. The size of the last litter assessed less than 7 days postpartum was compared with subsequent PSC. 15 unmated cubs of the year (age class 0) were examined for comparison. Foxes were killed 30±35 weeks postpartum. Reproductive tracks were removed from the carcasses immediately after death and stored at ±20° C until examination. Uteri horns were opened longitudinally and examined for placental scars. Scars were classified by shade of darkness from shade 1 (scars were barely visible) to shade 6 (black scars) (Englund 1970; LindstroÈm 1981). Ovaries were examined but no corpera lutea were detected. Analysis of variance was used to detect differences between litter size and PSC across age classes followed by Bonferroni-tests to compare group means. Differences in frequencies of placental scar shades across age classes were analysed by Goodness of Fit. Linear regressions and t-tests were used

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Table 1. Litter size and placental scars in red foxes. Age class 2 and age class 3 were combined for statistical analysis. a One female with no placental scars excluded from the analysis. * Significant different from females in age class 1 P < 0.001. Litter size

Placental scars

Placental scar shade classes

Age class

n

Mean ± SD

Mean ± SD

1

2

3

4

5

6

0 1 2 3 4

15 18a 8 3 19

0 1.9 ± 1.9 3.5 ± 2.5 1.3 ± 2.3 3.4 ± 2.5

0 5.2 ± 2.2 9.6 ± 2.5* 9.3 ± 4.2* 11.2 ± 2.3*

0 18 30 2 70

0 15 10 3 44

0 5 3 7 18

0 20 8 9 34

0 27 20 7 33

0 3 6 0 14

to describe the relationship between observed litter size and successive counts of placental scar shades. Age class 3 and age class 2 were combined for statistical analysis due to small sample sizes. 23% of mated vixens failed to produce cubs. 33% of primiparaous were barren. One primiparaous vixen had no placental scars while others had scars of shade 1 to 5. Two primiparaous barren foxes had only light placental scars. Twenty percentages of multiparaous vixens were barren and had dark placental scars. There were no significant differences in litter size between age classes (F = 1.72, D. F. = 46, P = 0.19), nor were any differences observed between vixens in age class 1 and older age classes (t = 1.80, D. F. = 45, P = 0.08). Placental scars increased with age classes (F = 29.75, D. F. = 46, P < 0.001, Tab. 1). Age class 4 and age class 2/3 had significantly more placental scars than age class 1 (P < 0.001, t = 7.58 and t = 4.73, respectively). Numbers of placental scars in age class 4 were higher but not significantly different from age class 2/3 (t = 1.84, P = 0.22). Numbers of placental scars in age class 1 were lower than all older age classes combined (t = 7.30, D. F. = 45, P < 0.001). Primiparaous vixens had fewer pale scars compared to all the older age classes combined (v2 = 16.87, D. F. = 5, P < 0.005) and each of the older age classes separately (age class 4: v2 = 25.50, D. F. = 5, P < 0.005; age class 2/3: v2 = 11.13, D. F. = 5, P < 0.05). Frequency of scars was similar in age class 2/3 and age class 4 (v2 = 10.21, D. F. = 5, N.S.).

Linear regression predicting individual litter size from PSC shade 5±6 was: y = 0.96 x + 0.51, where y = litter size and x = placental scars shade 5±6 (r2 = 0.45, F = 36.95, P > 0.001). A more exact prediction was obtained by linear relationship between individual observed litter size from PSC shade 4±6 (y = 0.85 x ± 0.54, y = litter size and x = placental scars shade 4±6) (r2 = 0.56, F = 56.20, P > 0.001). Placental scars shade 5±6 estimated known litter size most correctly (t = 0.96, P = 0.34) (Tab. 2). However, PSC shade 5±6 underestimated litter size by 15% and proportion of reproductive active vixens by 11%. PSC shades 4±6 overestimated observed litter size by 40% (t = 2.42, P = 0.018) and underestimated the proportion of reproductive active vixens by 4%. All whelping vixens were detected by counts of scar shade 4±6, while one whelping vixen was not recognised by counts of scar shade 5±6. Table 2. Estimates of litter size based on different shades of placental scars and observed litter size in 47 red foxes. Placental scar counts significantly different from observed litter size at P < 0.001** and P < 0.05*. Litter size estimates

Cubs and placental scars Mean

SD

95% C.I.

Live cubs 6 5±6 4±6 3±6 2±6 1±6

2.47 0.49** 2.34 3.85* 4.55** 6.09** 8.64**

2.36 3.58 2.52 2.50 2.06 1.66 1.00

0±7 0±3 0±5 1±7 1±8 2±10 3±14

Placental scars and litter size in red fox Exceeding numbers of placental scars compared to numbers of corpera lutea or embryo counts suggest that scars persist more than one breeding cycle in red fox (Englund 1970; LindstroÈm 1981; Allan 1983; Wandeler and LuÈps 1993). The increased number of scars and the higher proportion of pale scars in multiparaous vixens supported these suggestions. However, the occurrence of pale placental scars in barren primiparaous vixens showed that pale scars in red fox might originate from resorption and abortion of foetuses during the last pregnancy, as shown experimentally in Arctic fox (Alopex lagopus) (Strand et al. 1995). Strand et al. (1995) found that placental scars persisted 80 weeks in Arctic foxes, although no increase in placental scars were detected in multiparaous females. Pale scars in multiparaous vixens and in barren primiparaous vixens had similar appearance. This implies that it is not possible by PSC to estimate post-implantation mortality rates and frequency of barrenness in vixens, which have gone through more than one breeding cycle. Counts of dark placental scars unavoidably overestimate true litter sizes, as scars from late abortion scars were indistinguishable from full term scars. This discrepancy will also exist in investigations that estimate reproductive parameters in foxes killed shortly after parturition (e. g. Heydon and Reynolds 2000). The present study demonstrated that assessments of litter size is feasible by counting dark placental scars (shade 4±6) in uteris from red foxes collected up to 35 weeks postpartum.

Acknowledgements We are grateful to the Danish Furbreeders Research Centre Nord and its staff for practical work with the animals. Nick Leyssac, Heike Weber, Jaap Mulder and anonymous referees gave valuable comments on earlier drafts of this manuscript. Else-Marie Nielsen is thanked for improving our English.

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Authors' addresses: Morten Elmeros, National Environmental Research Institute Denmark, Department of Landscape Ecology; GrenaÊvej 14, Kalù, DK-8410 Rùnde (e-mail: [email protected]); Vivi Pedersen, Department of Animal Behaviour, Zoological Institute, University of Copenhagen, Tagensvej 16, DK-2200 Kùbenhavn N; Trine-Lee Wincentz, Department of Population Ecology, Zoological Institute, University of Copenhagen, Universitetsparken 15, DK-2100 Kùbenhavn é, Denmark