Ethology 108, 557—564 (2002) 2002 Blackwell Verlag, Berlin ISSN 0179–1613

Burrow Use and the Influence of Ectoparasites in Brants’ Whistling brantsii

T. J. Roper*, T. P. Jackson , L. Conradtà & N. C. Bennett§ *School of Biological Sciences, University of Sussex, Brighton, UK; Department of Zoology and Entomology, University of Pretoria, Pretoria 0002, Republic of South Africa; àSchool of Biology, University of Leeds, Leeds, UK; § Research Institute, Department of Zoology and Entomology, University of Pretoria, Pretoria 0002, Republic of South Africa

Abstract In Brants’ whistling rat, Parotomys brantsii, single inhabit unusually complex burrow systems containing several nest chambers. We investigated burrow use and examined the effect of ectoparasites on choice of alternative nest chambers by radiotelemetrically monitoring the nocturnal sleeping locations of individual whistling , before and after treating themto removeectoparasites. Prior to treatment, animals used several different nest chambers within a single burrow, moving from one chamber to another every 1.6 d on average, and most individuals also slept in more than one burrow. Anti-parasite treatment reduced the rate at which animals switched from one nest chamber to another within a burrow. Screening of a separate sample of animals for ectoparasites revealed that they were infested with fleas, mainly Xenopsylla eridos. We suggest that by switching periodically fromone nest chamberto another, whistling rats reduce the rate at which ectoparasites, especially fleas, accumulate. Corresponding author: Professor T. J. Roper, School of Biological Sciences, University of Sussex, Brighton BN1 9QG, UK. E-mail: [email protected]

Introduction Burrowing is a dominant feature of mammalian behaviour: an estimated 447 of the 777 genera of terrestrial contain that spend at least some of their time in subterranean burrows (Kinlaw 1999). The architecture and internal environment of mammalian burrows have been relatively well investi- gated (Reichman & Smith 1990; Kinlaw 1999; Roper et al. 2001a) but there have been few behavioural studies of how animals use the underground space provided by a burrow system. Furthermore, such behavioural investigations as have been published are mainly concerned with completely subterranean species

U. S. Copyright Clearance Center Code Statement: 0179-1613/2002/1086/0557$15.00/0 www.blackwell.de/synergy 558 T. J. Roper, T. P. Jackson, L. Conradt & N. C. Bennett (Nevo 1999), although these constitute only a small minority of mammalian burrowers. Here, we investigate burrow use in Brants’ whistling rat, Parotomys brantsii. Like most burrowing mammals, whistling rats are semifossorial and occupy, year- round, a multifunctional burrow system (Du Plessis et al. 1992; Coetzee & Jackson 1999). However, despite being occupied usually by only a single (Jackson 1999), burrows in this species typically possess 50–100 entrances, cover an average area of about 70 m2 and contain up to six nest chambers (De Graaf & Nel 1965; Du Plessis & Kerley 1991; Jackson 2000a). Given that burrow construction is energetically costly (Vleck 1979), the question arises as to how individual whistling rats benefit fromhaving such extensive burrows. We tested the hypothesis that by having access to a burrow containing several nest chambers, whistling rats gain protection against ectoparasites. That is, by switching from one nest chamber to another rats may be able to prevent the accumulation of parasites that would occur if a single chamber were permanently occupied (see Neal & Roper 1991; Butler & Roper 1996; Roper et al. 2001b). We tested three predictions of this hypothesis, namely: (i) whistling rats should carry a significant ectoparasite burden; (ii) individuals should regularly switch fromone nest chamber to another within a burrow; and (iii) treatment of animals to remove ectoparasites should reduce the rate of switching between nest chambers.

Methods Study Area and Species The study was conducted between mid-Aug. and mid-Sep. 1999 in a 6-ha part of the Goegap Nature Reserve (2937¢ S, 1759¢ E), 10 kmnortheast of Springbok in the Northern Cape Province, South Africa. The area is semiarid, with average rainfall of 160 mm (Northern Cape Nature Conservation, unpubl. data), and is described as Ôupland succulent KarooÕ (Low & Rebelo 1996). During the study, surface shade temperature ranged from 34.5 C (day) to 1.1 C (night) (see Jackson et al. in press for further details). The area contained 243 whistling rat burrows and an estimated population of 36 individuals, most of which had been marked with colour-coded tags as part of a long-termresearch project (see Jackson 1998 for details). Burrows, which were located in sandy areas dominated by succulent vegetation and winter ephemerals, were roughly circular or ellipsoidal in shape. Excavation of a sample of unoccupied burrows has shown that each burrow consists of a single, discrete systemof interconnected tunnels and nest chambers(Jackson 2000a). Neigh- bouring burrows were sufficiently far apart (1–25 m), in relation to the distance between entrances within a burrow, for separate burrows to be easily distinguishable (see also Jackson 2000a). At the time of the study, when the population density was relatively low (see Jackson 1999), no burrow was occupied by more than one animal and most animals had access to more than one burrow. Burrow Use in Brants’ Whistling Rat 559

Trapping and Radio-Telemetry Whistling rats were live-trapped using double-ended wire-mesh cage traps baited with the succulent perennial Augea capensis. Trapped animals were weighed and sexed, and fitted with radio-collars consisting of a two-stage transmitter attached to a plastic cable-tie. Each collar was uniquely colour- marked by melting onto it a combination of rings of coloured heat-shrink tubing, so as to enable day-time recognition of individuals. The necks of recaptured individuals showed no evidence of irritation or hair loss fromthe collars, and the collars did not have any observable effect on burrowing or other activities. Collar weight was equal to 1.7% of mean body weight and did not exceed 2% of the body weight of any individual. Each burrow at which an individual was trapped, or in which it was subsequently found sleeping, was marked with a numbered wooden stake. In order to map the sleeping location of a radio-collared animal, its burrow was visited at night (between 2 and 5 h after sunset) and the precise underground location of the animal was determined using a 3-element Yagi antenna. We refer to these radiotelemetrically determined fixes as Ôsleeping locationsÕ. A small plastic numbered marker was then inserted into the ground at the relevant sleeping location in order to provide a permanent record. At the end of the study, a pair of orthogonal axes was laid out on the ground along two adjacent sides of each burrow, and the position of each sleeping location was measured relative to these axes and expressed as a pair of coordinates. The reliability of this method of locating animals underground was checked in two ways. First, trials carried out before the start of the study showed that radiotransmitters that had been buried at an undisclosed location could be reliably pinpointed to within 5 cmof their actual position. Secondly, at the end of the study, we partially excavated the burrows of three animals that had been killed by predators, in order to see whether the radiotelemetrically determined sleeping locations corresponded with underground nest sites. We found a significant quantity of nest material (shredded vegetation) immediately below each of five sleeping locations that were excavated, indicating that nest sites had been accurately localised. Sleeping locations were normally determined early in the night but, in order to see whether animals remained in the same place during the whole of the night, we re-determined the underground position of each animal 1–2 h before dawn on four nights. In all cases (n ¼ 32 determinations in eight animals), individuals were found at the same sleeping locations just before dawn as they had occupied shortly after dusk.

Procedure The study consisted of two phases. In the pre-treatment phase, eight animals (six females, two males) were radio-collared and we planned to record the sleeping locations of each of these for 14 consecutive nights, starting two nights after 560 T. J. Roper, T. P. Jackson, L. Conradt & N. C. Bennett trapping. However, owing to predation of one animal after 13 nights and difficulties in re-trapping the others, the duration of the pre-treatment phase ranged from13 to 20 nights (Table 1). In the post-treatment phase, the seven surviving animals were re-trapped and treated with 0.025 ml of the veterinary insecticide ÔFrontlineÕ (Fipronil 10% w⁄v), applied by a micropipette to the skin on the neck and shoulders of the animal. This dose was calculated on the basis of veterinary advice, taking into account the animals’ body weight of about 120 g. The animals were then returned to the burrows at which they had been trapped, with the intention of recording their night-time sleeping locations for a further 2-week period, starting two nights after release. However, predation of a further two animals, plus adverse weather conditions, meant that adequate post-treatment data were only obtained for five animals, all of which were females, for a period of 12–13 nights. Rates of switching between different locations, before and after treatment, were compared using a Wilcoxon matched-pairs signed-ranks test (Sokal & Rohlf 1981). A one- tailed probability value is cited because a similar previous experiment, on badgers Meles meles, had shown a decrease in the rate of switching between sleeping locations following anti-parasite treatment (Butler & Roper 1996). Thus, we had a priori reason to expect a similar result in Parotomys brantsii.

Ectoparasite Burden Ectoparasites were sampled in seven males and seven females that had been previously trapped in the study area. None of these animals was used in the radiotelemetric investigation. After sedation of the animals with ether, each was combed for 90 s with a small, fine-bristled nylon brush, and ectoparasites were collected in a plastic bag. In addition, the pelage of each animal was searched manually for ticks.

Table 1: Summary of data on burrow use in individual untreated whistling rats. Number of moves from one sleeping location to another, number of different sleeping locations used, and number of different burrows used, expressed as number per 10 observation days

Observation Moves between Locations Burrows Home Animal Sex days locations used used rangea (m2)

1 F 14 7.1 2.1 1.0 18 2 F 17 6.5 2.4 1.2 241 3 F 18 8.3 5.0 1.7 426 4 F 20 5.5 2.5 1.0 280 5 F 17 6.5 3.5 1.2 438 6 F 15 9.3 4.7 1.3 228 7 M 13 4.6 3.9 2.3 463 8 M 16 4.4 4.4 3.1 2615 aCalculated as a minimum-area polygon containing all sleeping locations. Burrow Use in Brants’ Whistling Rat 561 Results Ectoparasite Burden of Untreated Animals Of seven males and seven females that were examined, all except one female were found to have fleas (mainly Xenopsylla eridos but also a few Epirimia aganippes and Chiastopsylla numae). The number of fleas per animal ranged from one to nine (mean for males: 3.6; mean for females: 2.3) with no significant difference between the sexes (Mann–Whitney test, U7,7 ¼ 46, p > 0.1). Fleas were also found in nest material that was excavated in the course of checking whether sleeping sites could be accurately located (see Methods: Trapping and Radio- telemetry). No other ectoparasites were evident, either on the animals themselves or in samples of nest material.

Burrow Use in Untreated Animals All eight radio-collared animals used a variety of sleeping locations and all but one of them (a female) slept in more than one burrow during the period of observation (Table 1). The absolute number of different sleeping locations used per animal during the study period ranged from three to nine and the number of burrows fromone to five. However, in order to take into account differences in the number of observation days between individuals, values are expressed in Table 1 as the number of sleeping locations or burrows used per 10 observation days. Animals moved between different sleeping locations every 1.6 d on average, and between different burrows every 6.25 d; no animal spent more than five consecutive days in the same sleeping location. Thus, animals showed considerable mobility both within and between burrows. The two males moved more often from one sleeping location to another than did any of the females, used more burrows and had larger home ranges (Table 1). However, the sample size of males was too small to enable these sex differences to tested statistically.

Effects of Anti-Parasite Treatment In all of the five females for which both pre- and post-treatment radiotracking data were available, antiparasite treatment resulted in a decrease in the rate at which animals switched from one sleeping location to another (Fig. 1). The mean number of movements between different locations per 10 observation days was 6.8 in the pre-treatment phase, by comparison with 2.7 post-treatment. A sixth female, for which we had only pre-treatment data, showed a movement rate of 9.3, which was higher than the post-treatment scores of any of the other five females. Taken together, these data suggest that anti- parasite treatment reduced the rate at which animals moved from one sleeping location to another within a burrow (Wilcoxon matched-pairs test, T ¼ 0, p ¼ 0.03, one-tailed). 562 T. J. Roper, T. P. Jackson, L. Conradt & N. C. Bennett

Fig. 1: Rate at which individual whistling rats switched fromone sleeping location to another (number of moves per 10 days) before and after treatment against ectoparasites

Discussion Three hypotheses have been put forward to explain why the burrows of P. brantsii contain multiple nest chambers when each burrow usually contains only a single adult (Coetzee & Jackson 1999; Jackson 2000a). First, the existence of more than one nest chamber may reflect periods when the population density is high in relation to the number of available burrows, forcing adults to share burrows. In such cases, several (up to four) adults can set up separate territories within a single burrow system, such that each individual uses a different part of the burrow and, presumably, sleeps in a different nest chamber (Jackson 1999). Secondly, burrows are also shared by females and their offspring during the period between breeding and dispersal, and observational evidence suggests that towards the end of this period individual maturing young occupy different parts of the burrow (Jackson 2000b). Thus, the different chambers within a burrow may be used by the maturing offspring of a female resident, prior to dispersal. Thirdly, the use of multiple nest chambers by a single animal may be a form of defence against ectoparasites, allowing burrow occupants to avoid the high level of infestation that would occur in a single nest that was permanently occupied (Arnold & Lichtenstein 1993; Butler & Roper 1996). Our results argue against the first and second of these hypotheses by showing that even when burrows are inhabited by a single individual (i.e. when population density is low and there are no offspring present, as was the case in our study), burrow occupants frequently (every few nights) switch fromone nest chamberto another. The second hypothesis is also undermined by the existence and use of multiple nest chambers in burrows that were occupied by a single male, because male burrows are not shared with offspring. By contrast, the anti-parasite hypothesis is supported by the fact that in all five individuals in which the manipulation was undertaken, treatment of an animal against ectoparasite Burrow Use in Brants’ Whistling Rat 563 infestation resulted in a reduction in the frequency with which it switched between alternative sleeping sites. This result is similar to that of a previous study in European badgers (Butler & Roper 1996) which, like P. brantsii, occupy unusually complex burrows containing several nest chambers (Roper 1992). Other evidence consistent with the hypothesis is our finding that P. brantsii do carry ectoparasites in the formof fleas, and the fact that they periodically removeold bedding from their burrows and replace it with new material, possibly because of ectoparasite infestation (Jackson 2000a). It could perhaps be argued that anti-parasite treatment reduced the use of alternative nest sites by making the animals more lethargic, but this is unlikely because the treatment involved a widely used, commercially available prepar- ation that had been fully tested and found to have no side-effects on domestic animals. Additionally, our animals showed no obvious reduction in daytime surface activity or mobility. Alternatively, the post-treatment change in nest-site use might be attributable to some time-related confounding variable such as climatic change, because, for logistic reasons, we were unable to use a between- subjects experimental design in which the nest-site use of treated and untreated animals was simultaneously monitored. However, treatment of different individuals was staggered over time, so that monitoring of treated and untreated animals overlapped, in some cases completely. This, plus the fact that individual records show an immediate post-treatment change in within-burrow mobility, suggests that the difference was a real effect of the treatment. It remains to be determined precisely how the use of multiple nest sites affects ectoparasite burden in unmanipulated animals. It seems likely that the relevant ectoparasites are fleas, rather than ticks or lice, not only because these were the only class of parasites found in the present study but also because patterns of burrow use in the European badger seemto be related specifically to the intensity of flea infestation (Roper et al. 2001b). The most likely mechanism is that when an infested nest is vacated, the development of immature fleas that remain behind in the nest material is slowed or terminated (Butler & Roper 1996; Cox et al. 1999). Ticks and lice, by contrast, remain attached to the host and so would travel with it fromone nest site to another.

Acknowledgements We thank Northern Cape Nature Conservation for their invaluable assistance with this work, particularly Mr Julius Koen, Assistant Director of Research, and Messrs. Klaas van Zyl, Enrico Oosthuisen and their staff at Goegap Nature Reserve. We also thank Joyce Segerman, South African Institute for Medical Research, for identifying the fleas. TPJ was supported by a University of Pretoria postdoctoral bursary awarded to Professor N.C. Bennett, and TJR by a travel grant fromthe National Research Foundation, Republic of South Africa.

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Received: May 22, 2000

Initial acceptance: January 22, 2002

Final acceptance: January 31, 2002 (M. Taborsky)