Non-Invasive Methods to Study American and European ... › ... ›...

Badgers: systematics, biology, conservation and research techniques, pages 311–338.G. Proulx and E. Do Linh San, editors, 2016.Alpha Wildlife Publications, Sherwood Park, Alberta, Canada.

Chapter 12

Non-Invasive Methods to Study American and European Badgers — A ReviewGilbert PROULXAlpha Wildlife Research & Management Ltd., 229 Lilac Terrace, Sherwood Park, Alberta, Canada T8H 1W3. Email: [email protected]

Emmanuel DO LINH SANDepartment of Zoology and Entomology, University of Fort Hare, Private Bag X1314, Alice, 5700, South Africa. Email: [email protected]

311

Abstract – In an effort to minimize injury and to not disrupt the behaviour of studied animals, non-invasive methods have become popular among wildlife researchers and naturalists. This chapter describes methods that may be used to study American (Taxidea taxus) and European (Meles meles) badgers without capturing and handling animals: 1) tracks and track stations; 2) scats, food caches, and bait markers; 3) hair; 4) burrows and setts; 5) foraging signs; 6) scent markings and latrines; 7) cameras and videos; 8) direct observations and spotlighting; 9) natural markings; 10) carcasses; and 11) questionnaire surveys and web-interface records. The methods are being discussed for studies relative to badger distribution, populations and genetics, habitats, food habits, behaviour, diseases and parasites, and prophylactic treatments. This chapter stresses the need to use multiple methods to collect reliable datasets and proposes that non-invasive techniques could be used advantageously to increase our knowledge on the biology, ecology and behaviour of other, less-known badger species.

INTRODUCTION

Capturing and handling animals are often needed to collect information such as morphometric measurements and physiological state (Powell and Proulx 2003), and the use of these techniques has significantly contributed to our understanding of mammal biology. However, the capture of wild animals has the potential to cause injury and to change normal behaviour and physiology

312 Non-invasive methods to study badgers

(Kreeger et al. 1990; Cattet et al. 2008; Proulx et al. 2012). The negative effect of invasive methods has been reported for both American (Taxidea taxus; e.g., Quinn et al. 2010) and European (Meles meles; e.g., Ågren et al. 2000; Schütz et al. 2006) badgers. To minimize the impact of study and survey techniques on carnivores, several non-invasive methods have been developed (Zielinski and Kucera 1995; Gomper et al. 2006; Long and MacKay 2012).

This chapter reviews various non-invasive techniques that have been used to survey and study American and European badgers. We specifically aim to demonstrate that these techniques allowed to collect a large range of precious information on these 2 badger species, and that they could be used advantageously to increase our knowledge on the biology, ecology and behaviour of other, less-known badger species. After MacKay et al. (2008), we define as non-invasive every method which does not require the study animal to be physically or chemically immobilized. We extend this definition to include carcasses that are encountered along roads and fields or are collected from fur trappers and hunters. Although the death of these animals may have been caused by humans, their use is not the result of a physical or chemical immobilization by the researchers. Autopsies and analyses do not cause injuries and behavioural changes. We do not address survey designs and statistical analyses related to the use of these techniques. References to specific studies throughout the chapter, and specialized publications such as Long et al. (2008a), O’Connell et al. (2011), Ancrenaz et al. (2012), and Kelly et al. (2012) address these aspects of applying non-invasive methods.

CLASSES OF NON-INVASIVE METHODS FOR BADGERS

During the last 30 years, various non-invasive methods have been used to study the distribution and the ecology of badger species (Table 1). Most methods may be used to gather information on more than one aspect of the biology of a species. For example, camera-trapping may be useful to confirm the presence of a species in a specific area, and to describe habitats where it has been observed (e.g., Racheva et al. 2012). Scat analyses may be used for several purposes, e.g., diet and habitat preferences (Proulx, Chapter 7, this volume; Zagainova and Markov, Chapter 8, this volume), population size estimation (Frantz et al. 2004), territorial marking (Roper et al. 1993), and parasite surveys (Stuart et al. 2013). Therefore, classifying non-invasive methods on the basis of their purpose is difficult since each of them may be used in various projects depending on the questions to be answered and the inventiveness of researchers.

Long and MacKay (2012) developed a series of classes centered on tracks, scats, hair and cameras. For the purpose of this chapter, we expanded on their approach and identified 11 classes of non-invasive methods: 1) tracks and track stations; 2) scats, food caches, and bait markers; 3) hair; 4) burrows and setts; 5) foraging signs; 6) scent markings and latrines; 7) cameras and videos; 8) direct observations and spotlighting; 9) natural markings; 10) carcasses; and 11) questionnaire surveys and web-interface records.

DESCRIPTION OF NON-INVASIVE METHODS FOR BADGERS

Tracks and track stationsThe inventory of animal tracks (Figures 1 and 2) in sand, mud and snow allows to establish the species presence and distribution, monitor population trends, identify preferred micro- and macro-

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habitats, and learn more about the behaviour of animals at different times of the year (Proulx and O’Doherty 2006; Long and MacKay 2012). However, badger studies based on track counts are few. This is likely related to the fact that, during no-snow periods, proper substrates are necessary to record tracks. Also, during cold, snowy weather, badgers may not be active in northern regions (Kowalczyk et al. 2003a; Proulx and MacKenzie 2012a). Messick and Hornocker (1981) and Goszczyński et al. (2005) used snowtracking to complement radio-tracking data on home ranges. Rosalino et al. (2008) relied on tracks to assess European badger habitat use. Navarro et al. (2012) use tracking to assess the relative abundance of badgers. Do Linh San (2002) used tracks and other field signs (hair, feces, foraging and digging signs) to determine sett use by European badgers, and found that peaks of activity recorded during the year coincided with several of the main aspects of this species’ life cycle, particularly reproduction and winter sleep. Seiler et al. (1995) deployed track plates to record the presence of European badgers. Hein and Andelt (1995) used scent-station visitations to assess the relative abundance or American badgers. However, Mortelliti and Boitani (2008) showed that, by relying only on scent-station data, the distribution of European badgers would be underestimated.

Tracking has many advantages, notably to provide researchers with precise information about the location and path of an animal at scales from the landscape to the microhabitat level (Heinemeyer 2002; Andruskiw 2003). Vegetation composition, soil types, and other data on biotic and abiotic characteristics collected at track site provide researchers with a good understanding of badger habitat requirements (Proulx and O’Doherty 2006). Tracking may not be suitable to determine badger distribution in areas where population densities are low. Crooks (2002) found that American badgers were most sensitive to habitat fragmentation, with a lower probability of occurrence and relative abundance per unit area in smaller and more isolated habitat patches.

Backtracking is more informative than capture-recapture and discontinuous radio-telemetry fixes because it allows one to collect continuous information on the trajectories of paths and use of various habitats by animals. The main disadvantage of tracking is that it can only be used when substrates (e.g., snow, mud, fine sand) are adequate. Identification problems can arise due to substrate quality and animal movements (Heinemyer et al. 2008). Tracking definitely requires experienced trackers.

Scent-stations are frequently used to monitor carnivore populations, habitat use, and species presence. However, their efficacy varies among species (Foresman and Pearson 1998). The reliability of this methodology should be extensively field tested to avoid biased results (Mortelliti and Boitani 2008).

Scats, food caches, and bait markersBadger scats (Figure 3) that have been properly identified – e.g., collected at burrows/setts, latrines, or nearby fresh digging and animal tracks – lend a wealth of information about the food habits of the animals and the areas where they hunt their prey (Kruuk and Parish 1981; Messick and Hornocker 1981; Lampe 1982; Boesi and Biancardi 2002; Zabala et al. 2002; Fischer et al. 2005; Barea-Azcón et al. 2010; Remonti et al. 2011; Proulx, Chapter 7, this volume; amongst others). Likewise, food caches (Figure 4) may provide valuable information about the importance of some prey for American badgers at different times of year (Michener 2000). Fecal samples can be examined and analysed for diseases and parasites (Table 1). Since contact between livestock and feces in the environment is a potential parasite/pathogen transmission event, such analyses have a

Proulx and Do Linh San 317

Figure 1. Burrow systems freshly dug by an American badger (Taxidea taxus). Note tracks and scraping signs. Photo © Gilbert Proulx.


major impact on badger conservation programs (Smith et al. 2009).Non-invasive genetic tagging has emerged during recent years as an important tool for the

estimation of animal abundance. By using a number of microsatellites, a genetic profile can be obtained that is specific for an individual (Mills et al. 2000), enabling the number of individuals in a given population to be counted. Using this approach, estimates of badger group size have been obtained by generating genetic profiles from badger feces (Frantz et al. 2003; Wilson et al. 2003). Trained dogs are now used to find badger scats and latrines (Kauhala and Salonen 2012) as they are more efficient in detecting carnivore species living in an area than cameras, scent stations and hair snares (Harrison 2006; Long et al. 2007).

Bait-marking is a widely used technique for the delineation of European badger territories (Kruuk 1978; Roper et al. 1993; Delahay et al. 2000) and the determination of group affiliations of setts (Woodroffe and Macdonald 2000). It has also recently been used to determine the possible

Figure 2. Typical European badger (Meles meles) track in muddy terrain. The position of the thumb and the presence of long claw imprints indicate that the track corresponds to the left front foot. Photo © Emmanuel Do Linh San.


Figure 3. European badger scat deposited in a typical dung pit revealing the consumption of earthworms (A) and maize and plums (B). Photos © Emmanuel Do Linh San.

A

B


Figure 4. Partially uncovered above ground American badger cache. Note blood-stained spots in the upper torso where the Richardson’s ground squirrel (Urocitellus richardsonii) was grasped by the badger. Photo © Gilbert Proulx.


role of coordinated latrine use in territory defence (Kilshaw et al. 2009). In this technique, markers such as coloured plastic pellets are included in baits, and successfully retrieved at latrines (Delahay et al. 2000). Bait markers have also played an important role in identifying European badgers or the proportion of a population that ingested baits with vaccines (Southey et al. 2002).

Scat, food caches, and bait markers are advantageous as they allow one to collect valuable information about badger abundance and distribution, food habits, and habitat use. However, identification of badger scats based solely on morphology and size may be misleading. Scat identification may be more reliable with the presence of other signs such as tracks, burrow digging, and feeding. Genetic methods for assigning individual identification for non-invasively collected scats provide a higher level of rigor than methods based solely on scat measurements (Heinemeyr et al. 2008). Finally, while bait-marking is a technique that can be successfully used in well-managed landscapes such as in England, it is more difficult to retrieve bait markers in more pristine landscapes where access may be difficult and scats are more difficult to find.

HairHair traps consisting of adhesive tape (Sloane et al. 2000), or preferably of barbed wire (Figure 5) stretched near bird nests that may be potentially depredated by American badgers (Pasitschniak-Arts and Messier 1995) or suspended above runs/paths and main sett entrances (Scheppers et al. 2007; Balestrieri et al. 2010), can be used to pluck hair from badgers. An analysis of the hair in laboratory (e.g., Moore et al. 1974) can then lead to the confirmation that badgers were present at the study site. DNA can be extracted from hair follicles and used to recognize individuals and estimate population size (Scheppers et al. 2007; Huck et al. 2008; Frantz et al. 2010).

Hair collection is an inexpensive method used to confirm the presence of badgers in an area. The analysis of hairs can be done in laboratory through the examination of cuticular scales and medulla configuration (Proulx, Chapter 7, this volume). It is important to have a good reference collection of hairs of carnivores and other species to properly identify samples (Kelly et al. 2012). Also, of hairs from different parts of the body may have different morphology (e.g., Proulx and Proulx 2012). Hair collection may not be successful when the contact between the badger fur and the hair snagging device is inadequate. It is therefore important to properly set the hair snagging device at the entrance of a burrow system or a well-utilized trail. Hair collection may become time-consuming when badger abundance is low, or when non-target species disturb the hair-snagging device.

Burrows and settsConspicuous burrows of American badgers (Figure 1) and setts of European badgers (Figure 6) have been used to indicate species presence in various habitats (Fischer and Weber 2003; Eldridge 2004; Proulx, Chapter 7, this volume). There appears to be no correlation between density of burrows and American badger abundance (Messick and Hornocker 1981; Messick 1987). On the other hand, the density of European badgers has been estimated by counting main setts (Thornton 1988; Kowalczyk et al. 2003b; Lara-Romero et al. 2012) and using a mean number of resident badgers per sett (Kowalczyk et al. 2003b). The bedding of setts may be investigated for the presence of parasites (Hancox 1988).

Burrow and sett are relatively easy to survey. It may be more difficult to find them in areas where their low density may be due both to human factors (e.g., persecution and habitat loss)


Figure 5. European badger hair caught in barbed wire. Photo © Emmanuel Do Linh San.

and to a possible low suitability value of habitats (Virgós and Casanovas 1999; Biancardi et al. 2014). It is important to recognize active burrow from inactive ones. Kruuk (1978) defined 3 types of setts: 1) “main setts” are multi-entrance burrows that are permanently occupied and used for breeding; 2) “outlier setts” are only intermittently occupied and usually have only 1 entrance; and 3) “annex setts” are close to main setts, have an intermediate number of entrances, and are occupied most of the time.

Figure 6. European badger main sett in a deciduous woodland. Main setts often have between 8 and 15 entrances, but some may comprise of several dozens of them. Photo © Denis-Richard Blackbourn.


Foraging signsWhen hunting, American badgers may dug small, shallow holes (Figure 7, or enlarge the burrow entrances of fossorial rodents (Proulx and MacKenzie 2012b). When foraging for earthworms, insect larvae or plant tubercles and roots, European badgers thrust their nose into the ground surface and begin simultaneously grubbing with the snout and digging with their forepaws (Do Linh San 2006). Grubbing with the snout, with or without digging, produces a variety of “snuffle holes”. If the substrate is grassland, sizeable chunks of turf can be turned up by the forepaws, leaving a 5–10-cm-deep hole, up to 20 cm in diameter (Roper 2010). When foraging for insect larvae and plant material, badgers may remove the litterfall over a large area (Figure 8). To a trained observer, the presence of European badgers may also be confirmed in wheat and barley crops. Badgers make about 20-cm-wide paths through the crops, trampling the individual plants down to ground level. They also feed on ripening cereals and, in doing so, flatten discrete patches of crop up to a few 100 m2 in area (Roper et al. 1995).

Foraging signs may be used to infer habitat selection and hunting activities (Proulx, Chapter 7, this volume). However, investigators require some experience to identify badger signs. This is particularly true in agricultural areas where damage to crops may be caused by animals other

Figure 7. Series of shallow holes made by an American badger while hunting for Richardson’s ground squirrels. Photo © Gilbert Proulx.


than badgers.

Scent marking and latrinesFecal scent marks of the European badger are typically deposited in latrines, which are communal scent marking sites (Kruuk 1978; Buesching and Jordan, in press). A large proportion of latrines are associated with boundary areas of badger social group territories (Kruuk 1978; Roper et al. 1993). Urine marking also occurs at both latrine and non-latrine sites, particularly where badgers cross through linear features such as hedgerows and fences (White et al. 1993). Tuyttens et al. (2001) found that all latrine-use measures – e.g., number of pits (depressions), number of pits with feces, volume of fresh feces per km of transect – were positively associated with population density. Hutchins et al. (2002) found that the patterns of deposition of feces and urine at latrine

Figure 8. European badgers may remove soil and leaves to forage on insect larvae and other food items. Photo © Emmanuel Do Linh San.


were associated with adult badger population density. Rosalino et al. (2008) and Balestrieri et al. (2009) considered that latrines could be used to broadly infer habitat preferences of badgers at landscape level.

European badger latrines are easy to spot and to identify (Mortelliti and Boitani 2008). However, latrines may be spread over a 50-m radius area, and not all of them may be actively used. Latrines reach a peak of utilization from January to March (Do Linh San 2006). A systematic search of the territory is required to find all the latrines used by badgers.

Cameras and videosToday’s digital cameras are fast, equipped with infrared illumination, and capable of capturing many thousands of images over days and even weeks before the memory card requires changing (Long and MacKay 2012). These cameras have been used to detect the presence of badgers and describe their habitats (Table 1).

Video cameras have been used to study the behaviour of European badgers (Tolhurst et al. 2009; O’Mahony, Chapter 9, this volume), and monitor American badger predation at waterfowl nests (Pietz and Granfors 2000). Remote-controlled, battery-operated, infrared video surveillance equipment was used for continuous nocturnal observation of setts to study the social behaviour of European badgers, e.g., allo-marking of conspecifics with subcaudal gland secretions (Buesching et al. 2003), and interspecific encounters (Macdonald et al. 2004). Cameras and video cameras may provide researchers with a sound estimate of individuals at a sett or in a specific area when badgers can be individually recognized (Racheva et al. 2012).

Although remote cameras may be relatively expensive, they are advantageous because they can be left unattended in the field to record the presence and the behaviour of the animals. The proper maintenance and placement of cameras are essential to collect valuable information. Inspecting, testing, and preparing equipment is a requisite to reduce system failures and increase its efficiency in the field (Kays and Slauson 2008). Precipitation, humidity, and cold temperatures may cause system failure. The placement of cameras in the field must be judiciously selected to minimize false triggers due to moving vegetation or sunlight fluctuations. It is noteworthy to mention that reviewing photographs and videos is time-consuming, and may require a team of analysts to properly assess recordings in a timely manner.

Direct observations and spotlightingDirect observations may provide unique information on the hunting behaviour, habitat, and movements of badgers (Proulx and MacKenzie 2012b). Also, Hounsome et al. (2005) and Parrott et al. (2012) walked transect surveys to estimate European badger abundance. Direct observations can be carried out during daylight with the naked eye or binoculars, or at night with night vision binoculars and spotlights. For example, the number of European badger residents within a sett at any given time is difficult to establish because trappability may vary between individuals, groups, seasons (Tuyttens et al. 1999) and weather conditions. Observers using binoculars and/or night vision equipment to watch badgers at setts can provide estimates of the number of residents (Kowalczyk et al. 2003b; Wilson et al. 2003; Do Linh San et al. 2011; Mysłajek et al. 2012). Do Linh San et al. (2007) used spotlighting as a complementary method to den-watching in order to estimate badger social group size.

Using spotlighting, Proulx and MacKenzie (2012b) identified American badger hunting


grounds, and described the nocturnal hunting behaviour of individuals. The researchers described systematic back-and-forth movements of badgers to find and dig out hibernating Richardson’s ground squirrels (Urocitellus richardsonii). Such movements had never been described before, and it is unlikely that someone could surmise their existence without witnessing American badgers in action (Proulx and MacKenzie 2012b). Spotlighting was also used to survey badgers in prairie dog (Cynomys ludovicianus) colonies (Clark et al. 1982). Spotlighting was used to determine spacing between American badger family groups (Messick and Hornocker 1981), and to investigate the relative abundance of American badgers in two study areas with different levels of poisoning (Proulx and MacKenzie 2012c).

Direct observations and spotlighting allow the collection of unique datasets. However, this non-invasive technique is time- and labour-intensive. Field work must obviously be in sync with the diel activity of animals, and a team of investigators may be required to record observations during day and night.

Natural markingsRecognizing individuals in the field often involves using naturally occurring phenotypic variation. Dixon (2003) showed that European badgers could be reliably identified in the field on the basis of variation in the appearance of the tail. Natural markings used in studies must be readily identifiable during day and night, and during all seasons.

CarcassesWe argue that the collection of data from carcasses of animals that have been trapped or shot, or found dead along roadsides (Figure 9) may be a non-invasive method as it allows collecting information on the reproduction (Wandeler and Graf 1982; Page et al. 1994; Do Linh San 2004) and dispersal (Frantz et al. 2010), food habits (Roper and Lüps 1995) and diseases/parasites (Do Linh San et al. 2003; Do Linh San 2007) of this species (Table 1) without further impacting on populations. Roadkills may provide a general index of badger abundance over large areas (Case 1978) and seasonal behavioural activities (Davies et al. 1987).

Carcasses may be easily obtained from hunters and trappers for a minimal fee, but such monetary compensation should not result in an overexploitation of badgers and the extirpation of populations.

Questionnaire surveys and web-interface recordsInterviews and surveys have been commonly used to determine the distribution of badgers (Matyáštík and Bičík 1999; Bičík et al. 2000), and assess badger damages and examine farmers’ attitudes vis-à-vis European badgers (Macdonald 1984; Symes 1989; Moore et al. 1999) and American badgers (Proulx and MacKenzie 2009; Weir et al., Chapter 11, this volume). Such surveys help recovery teams in directing their education efforts at those groups that have negative views of badgers (Weir et al., Chapter 11, this volume).

To provide the information needed by public agencies and private institutions to assess and monitor changes in species distributions, NatureServe (a non-profit conservation organization) maintains a network of biological inventories known as Natural Heritage Programs or Conservation Data Centers that include both anecdotal and verifiable occurrence records for a wide array of species (Aubry and Jagger 2006). Natural resources agencies have also developed internet websites


Figure 9. Road-killed badgers represent an important source of biological information. Photo © Emmanuel Do Linh San.

that consist of a permanent data archive and an interactive mapping application (e.g., Aubry and Jagger 2006). The Jeffersonii Badger Recovery Team (2013) maintains a website where people can indicate where and when they have observed badgers throughout British Columbia, Canada. In the development of recovery programs, these websites are important non-invasive methods to monitor the status of a species or subspecies across its range.

Questionnaire surveys and website reports may be useful to map the geographic distribution of a badger population. However, while the percentage of surveys returned to investigators varies among studies (e.g., Groves 1988; Proulx and Drescher 1993; Weir et al., Chapter 11, this volume), and not all observations are being reported on websites, many of these observations may be false identifications. For this reason, Aubry and Jagger (2006) suggested that anecdotal observations should not be used for making conservation decisions or management recommendations. However, anecdotal observations inform biologists of the potential presence of animals in a given area, and may be useful for guiding future survey efforts using detection devices that produce verifiable evidence of species presence (Aubry and Jagger 2006).

DISCUSSION

Some non-invasive methods may be more effective than others to answer specific questions, in various regions, and under different environmental conditions. Long and MacKay (2012) pointed out that advances in molecular laboratory methods, digital camera technologies, and statistical analyses have paved the way for modern non-invasive survey methods. Although high-tech


methods may be available to study badger species, one should not dismiss traditional techniques. Likewise, not everybody can effectively use some of these non-invasive methods. For example, although snowtracking is a traditional technique, it is also specialized work and must be used with a scientifically sound protocol to record tracks and analyze data properly (Proulx and O’Doherty 2006; Figure 10). Using multiple methods can increase the likelihood of detecting a species and securing valuable datasets. The range of experience required from investigators, technological requirements, and costs is highly variable (Figure 10), but most non-invasive techniques can be advantageously used to study badgers’ distribution, populations and habitats (Table 1). It is important, however, that researchers publish their assessment of non-invasive techniques so that

Figure 10. Schematic representation of required experience from investigator, technological requirements and costs associated with various non-invasive techniques to study American and European badgers.

wildlife biologists can select methods that are best suited for their study area, or modify the basic methods to improve research success.

Proulx et al. (2012) recommended that researchers apply Russell and Burch’s (1959) “3 Rs”, i.e., Replacement, Reduction and Refinement, to the use of animals in field research. Replacement strategies include non-invasive methods such as the collation and use of information already gained, population suitability simulations, and archived tissue samples. Reduction could be achieved by reducing stress in animals and limiting studies to the lowest acceptable number of animals needed to provide valid information and statistical inference. Refinement strategies require that researchers use the most humane, least invasive techniques to minimize pain and distress (Proulx et al. 2012). Non-invasive methods are valuable alternatives to the capture and handling of animals and should be considered in the study of badgers, particularly when it involves species at risk.

This chapter focused on non-invasive techniques that have been used for the study of American and European badgers. However, these techniques could be advantageously used in the study of species for which we know little such as hog-badgers (Arctonyx spp.), ferret-badgers (Melogale spp.) and stink-badgers (Mydaus sp.) (Proulx et al., Chapter 2, this volume). Whereas many non-invasive methods are relatively inexpensive and provide datasets comparable to those obtained with capture-based methods (e.g., Proulx and O’Doherty 2006), they have the capacity to be deployed over very large areas and thus to monitor entire populations (Long et al. 2008b).


With the improvement of current technologies, and the development of new ones, non-invasive methods cannot be overlooked in today’s badger studies.

ACKNOWLEDGMENTS

We thank Denis-Richard Blackbourn for his picture of a badger main sett. We express our gratitude to 4 anonymous referees for providing helpful comments on earlier drafts of the manuscript.

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