First known satellite collaring of a viverrid species: preliminary performance and implications of GPS tracking Malay civets (Viverra tangalunga)

Ecological Research, Feb 2016

The application of advanced technologies to the study of little-known species is a necessary step in generating effective conservation strategies. Despite the biological importance of the small carnivore guild, a paucity of data exists in terms of the spatial ecology of these species, largely due to logistical constraints of large and bulky collar units. This study reports the first known satellite collaring of a viverrid, the Malay civet (Viverra tangalunga), in Sabah, Malaysian Borneo. Stationary tests of two generations of 65–70 g e-obs GmbH ‘Collar 1A’ units recorded high fix success rates and good accuracy and precision under semi-open canopy. From October 2013–August 2015, nine adult V. tangalunga were fit with e-obs collars recording hourly nocturnal GPS locations. Collars were successfully deployed for 27–187 days. Field GPS fix success varied from 22 to 88.3 %, with the study documenting a total GPS success of 58.1 % across all individuals. Despite this large in-field performance range, the quality and quantity of data collected by these units surpass that of previous VHF studies on Asian viverrids, collecting on average a 16-fold increase in locations per collaring day. The successful application of satellite technology to these little-known carnivores carries significant biological and conservation implications, and it is recommended that satellite collars are a viable technology to conduct detailed and well-designed ecological studies of Viverridae species.

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First known satellite collaring of a viverrid species: preliminary performance and implications of GPS tracking Malay civets (Viverra tangalunga)

First known satellite collaring of a viverrid species: preliminary performance and implications of GPS tracking Malay civets (Viverra tangalunga ) Meaghan N. Evans 0 1 2 Sergio Guerrero-Sanchez Mohd Soffian Abu Bakar 0 1 2 Peter Kille Benoit Goossens 0 1 2 0 M. S. A. Bakar Æ B. Goossens Sabah Wildlife Department , Wisma Muis, Block B, 5th Floor, 88100 Kota Kinabalu, Sabah , Malaysia 1 M. N. Evans Æ S. Guerrero-Sanchez Æ B. Goossens Danau Girang Field Centre, c/o Sabah Wildlife Department , Wisma Muis, Block B, 5th Floor, 88100 Kota Kinabalu, Sabah , Malaysia 2 M. N. Evans (&) Æ S. Guerrero-Sanchez Æ P. Kille Æ B. Goossens Organisms and Environment Division, Cardiff School of Biosciences, Cardiff University , Sir Martin Evans Building, Museum Avenue, Cardiff CF10 3AX , UK The application of advanced technologies to the study of little-known species is a necessary step in generating effective conservation strategies. Despite the biological importance of the small carnivore guild, a paucity of data exists in terms of the spatial ecology of these species, largely due to logistical constraints of large and bulky collar units. This study reports the first known satellite collaring of a viverrid, the Malay civet Introduction (Viverra tangalunga), in Sabah, Malaysian Borneo. Stationary tests of two generations of 65-70 g e-obs GmbH 'Collar 1A' units recorded high fix success rates and good accuracy and precision under semi-open canopy. From October 2013-August 2015, nine adult V. tangalunga were fit with e-obs collars recording hourly nocturnal GPS locations. Collars were successfully deployed for 27-187 days. Field GPS fix success varied from 22 to 88.3 %, with the study documenting a total GPS success of 58.1 % across all individuals. Despite this large in-field performance range, the quality and quantity of data collected by these units surpass that of previous VHF studies on Asian viverrids, collecting on average a 16-fold increase in locations per collaring day. The successful application of satellite technology to these little-known carnivores carries significant biological and conservation implications, and it is recommended that satellite collars are a viable technology to conduct detailed and well-designed ecological studies of Viverridae species. GPS collar Æ Satellite Æ Viverridae Æ Viverra tangalunga Æ Spatial ecology - Global biodiversity loss is progressing at increasingly alarming rates (Schipper et al. 2008; Barnosky et al. 2011; Ceballos et al. 2015; Ripple et al. 2015) . To mitigate further loss, effective conservation management plans are critical, which in turn require in-depth understandings of species’ biological requirements (Margules and Pressey 2000; Chetkiewicz et al. 2006; Cooke 2008) . Documenting and quantifying factors crucial to species survival are the central aims of applied wildlife research, and the design of innovative research tools facilitates the achievement of these goals. Remote tracking technologies in wildlife studies have revolutionized scientific understanding of animal behavioural patterns and processes (Cooke et al. 2004; Ropert-Coudert and Wilson 2005; Fuller and Fuller 2012) . The application of radio telemetry as very high frequency (VHF) collar transmitters allowed for the first remote documentation of animal movements in the 1960s (Craighead et al. 1963) . While revolutionary, VHF tracking often requires significant field effort for sparse and relatively inaccurate data (Recio et al. 2011a; Gitzen et al. 2013) . Furthermore, the collection, applicability, and quality of VHF data are limited by intrinsic biases such as observer presence, site remoteness, weather, and specific animal behaviours (Fuller et al. 2005; Recio et al. 2011b) . In response to these limitations, satellite-based tracking technologies, such as the global positioning system (GPS), were first applied to wildlife in the 1970s (Craighead et al. 1972) . This development meant the collection of larger, more consistent, fine-scaled and accurate datasets (Rodgers 2001; Kochanny et al. 2002) . 2006, 2010), this study represents the first known Satellite tracking minimizes logistical effort and elimi- application of GPS collars to the Viverridae family, and nates the influence of observer presence on recorded ultimately aimed to demonstrate the scientific and conbehavioural patterns, generating datasets otherwise servation value of GPS technology deployments on unobtainable by VHF tracking and more relevant to small carnivores. conservation actions (Hebblewhite and Haydon 2010) . Satellite collars have established habitat utilisation and preferences for wary and remote species (Amstrup et al. Methods 2004; Simcharoen et al. 2014) , uncovered areas of previously unknown reproductive significance in widely Study site migrating species (Lindsell et al. 2009; Schofield et al. 2009; Hays et al. 2014) , and discovered novel cryptic The Lower Kinabatangan Floodplain is located in behaviours ( Davis et al. 1999 ; Bandeira de Melo et al. eastern Sabah, Malaysian Borneo (approximate range: 2007; Lu¨ hrs and Kappeler 2013) . 5 18¢N to 5 42¢N and 117 54¢E to 118 33¢E). The cli However, the universal application of GPS to wildlife mate is humid tropical with temperatures ranging from tracking is still limited by technological constraints, as 21 to 34 C (Ancrenaz et al. 2004) . This study was based historically, both transmitters and batteries have been in the Lower Kinabatangan Wildlife Sanctuary bulky and large (>400 g, some up to 2.2 kg) (Rodgers (LKWS), a 270 km2 area of protected secondary forest 2001). Most terrestrial GPS studies have focused on flanking the Kinabatangan River (Ancrenaz et al. 2004; mammals >7 kg, so spatial research on small and Goossens et al. 2005) . Comprised of ten riparian lots of medium-sized species relies on VHF transmitters varying degrees of disturbance history, the sanctuary (Blackie 2010; Cagnacci et al. 2010) . Owing to recent contains a mixture of dry lowland, semi-inundated, and advancements in both battery longevity and the minia- swamp forests interspersed with small grasslands turization of GPS component design, long-term satellite (Abram et al. 2014). technologies are being applied to increasingly smaller mammalian species, such as the ocelot Leopardus pardalis (Haines et al. 2006) , European hedgehog Erinaceus Trapping and immobilization europaeus (Recio et al. 2011c) , fossa Cryptoprocta ferox (Lu¨ hrs and Kappeler 2013) , fisher Martes pennanti Trapping periods spanned October 2013–August 2015. (Brown et al. 2012) , and brushtail possum Trichosurus Small carnivores were trapped using locally constructed, vulpecula (Blackie 2010; Dennis et al. 2010) . specially designed box treadle traps (110 cm · 35 cm · The Viverridae family (Order Carnivora) comprises 40 cm). Traps were set by 18h00, checked between 07h00 34 species in 14 genera, the majority of which weigh and 08h00, and closed during the day to avoid non<8 kg (Jennings and Veron 2009) . There exists a sig- target diurnal captures. nificant paucity of data concerning even basic ecological Upon capture, animals were administered anesthesia information of this family (Schreiber et al. 1989), and by a qualified veterinarian. Animals were either sedated five viverrid species are not yet represented in peer-re- with Tiletamine/Zolazepam (Zoletil , Virbac Laboraviewed literature (Brooke et al. 2014) . What studies do tories, Carros, France), or a mixture of Ketamine occur are dominated by camera trap deployments (Narketan , Ve´ toquinol UK Limited, Buckingham, (Wilting et al. 2010; Jennings et al. 2015) , survey tran- UK), Xylazine (Ilium Xylazil , Troy Laboratories PTY sects (Heydon and Bulloh 1996; Iseborn et al. 2010) , and Limited, Glendenning, Australia) and Tiletamine/Zoa handful of VHF studies (Joshi et al. 1995; Grassman lazepam. In the case of the latter drug combination, the 1998; Grassman et al. 2005 a; Berhanu et al. 2013; Camps reversal agent Yohimbine (Reverzine , Bomac Pty and Alldredge 2013; Nakashima et al. 2013) . Viverrids Limited, Hornsby, Australia) was administered once are threatened by habitat loss and hunting, but also by sampling was complete. lack of scientific information regarding rudimentary survival parameters (Schipper et al. 2008; Brooke et al. 2014) . This knowledge gap poses a substantial threat to GPS collaring and tracking the effective conservation and management of these species. GPS collars (Collar 1A and second-generation Collar Therefore, this study sought to demonstrate the 1A, e-obs GmbH, Gru¨ nwald, Germany) weighed applicability, performance, and value of satellite track- 65–70 g, or between 1.3–1.4 % of average adult civet ing a model viverrid, the Malay civet (Viverra tan- body weight, well within the restrictions of the American galunga). Weighing between 3–7 kg, V. tangalunga is a Mammal Society for the ethical collaring of animals predominantly solitary and terrestrial small carnivore (Sikes and Gannon 2011) . Each tag contained a GPS found throughout the Sundaic region of Southeast Asia microchip, either a 2300 or 2500 mAh battery, UHF (Payne and Francis 1985) . Although several VHF radiotransmitter, a tri-axial accelerometer, and an anstudies have evaluated the spatial ecology of V. tan- tenna. The collar was constructed to degrade through a galunga ( Nozaki et al. 1994 ; Colo´ n 2002; Jennings et al. thin section of leather near the fastening, and efforts were made to retrieve the collar following the cessation of data collection. Civets are nocturnal, and utilize day bed resting sites in dense forest or grassy areas (Colo´ n 2002; Jennings et al. 2006) . To conserve tag battery life and obtain the highest resolution of relevant GPS fixes, collars were set to record 13 hourly GPS points from 18h00 until 06h00. Collars were programmed with a 150 s ‘GPS timeout’, whereby the unit would cease searching for available satellites if no successful fix was acquired within this limit. For each successful GPS point, the collar recorded longitude, latitude, date, time, time to first fix, battery voltage, temperature, speed estimate, and heading. Due to the small size of the tags, a remote ultra-high frequency (UHF) download was required to access GPS and activity sensor data. A hand-held device (BaseStation II, e-obs GmbH) needed to be within transmittable range of a tagged individual, following which a high-speed wireless radio-link would be established and logged data downloaded to the BaseStation. Collars emitted a UHF radio signal for two and a half hours daily to allow for tracking. Collared individuals were tracked using a UHF 7E 868 MHz Yagiantenna (e-obs GmbH), an AOR AR8200 handscanner radio receiver (AOR Ltd, Tokyo, Japan), and the BaseStation. For most data download events, animals were tracked via the UHF pinger until adequate tag proximity ( 50–150 m) was reached for data download to commence. Data extraction occurred through the use of DataDecoder software v5_1s6 and v7_1 (e-obs GmbH), which converted encrypted BaseStation data into a desired file format. These were imported into MS Excel and ArcGIS 10.1 for subsequent analysis. Collar stationary performance Prior to deployment, three first-generation and four second-generation collars were tested at a stationary reference point under semi-closed canopy for a 13-h nocturnal period. Collar performance was determined by proportion of successful fix attempts. Accuracy was measured as Euclidean distance between collar fixes and the unit’s true location, as recorded by a GPSmap 62 GPS (Garmin Ltd., Kansas, USA). The precision of fixes was evaluated by measuring the Euclidean interpoint distances between each collar’s hourly fixes. Each collar’s maximum linear error was determined as the greatest inter-point distance, representing effective point spread, collected throughout this trial period. Analysis was used to evaluate if linear error differed by collar generation. A Mann–Whitney U-test determined whether linear inter-point differences differed by collar generation. Maximum inter-point distances between generations were tested by a pooled, two-tailed, twosample t-test. For field-deployed collar data, in-field performance values were pooled regardless of collar generation. In order to quantify tracking data resolution per collaring effort, a mean value of location fixes per active collaring day was calculated for this study and other viverrid VHF research. The total number of successfully recorded locations was divided by the maximum active collaring days for each animal in each study, and a two-tailed, two-sample t-test compared the logtransformed mean fix values between GPS and VHF studies. Results Trapping From October 2013–August 2015, 731 trap nights (night · number of active traps) were conducted throughout the LKWS, resulting in 43 small carnivore captures (5.9 % trapping success rate). Of these, 27 unique Malay civets were captured, and nine of these individuals collared (eight males, one female). Collar stationary performance Of the collars tested, fix success was high and location error slight, with second-generation collars outperforming first in most parameters. First-generation units demonstrated a mean (±SE) fix success of 87.2 % ± 5.13 (n = 39), while second-generation collars obtained all attempted fixes (n = 50). In terms of collar accuracy, mean (±SE) Euclidean distance error between GPS fixes and true location was 21.0 m ± 2.60 for first-generation units (n = 34). Second-generation collars displayed a significantly lower mean horizontal distance error of 12.3 m ± 1.87, nearly half as large as that of the first-generation units (n = 50) (t = 3.9225, d.f. = 82, P < 0.001). Collar precision improved between first- (n = 177) and second-generation units (n = 288), with each collecting median interpoint distances of 19.65 m and 12.67 m, respectively (U = 33749, P < 0.01e-6). However, the mean (±SE) maximum linear point spread of first-generation collars [75.9 m ± 17.7 (n = 3)] did not significantly vary from that recorded by second-generation units [53.3 m ± 14.7 (n = 4), t = 0.9926, d.f. = 5, P = 0.3665]. All spatial analyses were carried out with ArcGIS software (Version 10.1, ESRI, Inc., Redlands, CA). In stationary accuracy tests, data were log transformed for normality, and a pooled, two-tailed, two-sample t test Collar field performance From October 2013–August 2015, nine Malay civets (eight males and one female) were fit with GPS collars. ID Data were successfully retrieved from seven of these nine 2005; Jiang et al. 2008 ; Dennis et al. 2010; LaPoint et al. individuals (Table 1). Four animals were recaptured 2013). The error associated with triangulation-based following completion of the data collection period, and VHF tracking can be upwards of 200 m, so this slight no change was documented in body condition or weight, GPS error is of little comparative consequence (Grassalthough minor hair loss was noted. man et al. 2005b; Bartolommei et al. 2012; Nakashima In total, 8,450 GPS fixes were attempted by all col- et al. 2013). These stationary trials demonstrate the lars, with 4906 successfully obtaining latitude and lon- much higher quality of GPS compared to VHF data in gitude, a total fix success of 58.1 %, with individual small carnivore research. collar performances ranging from 22.0 to 88.3 %. Collar This study reports the first known satellite collaring longevity reached a maximum of 187 days before bat- of a Viverridae species. Overall fix success rate was tery exhaustion. The shortest complete deployment oc- similar to the performances of other small, field-decurred when a collar was prematurely shed after 27 ployed GPS units (Haines et al. 2006; Blackie 2010; nights of data collection. Recio et al. 2010; Brown et al. 2012) . Large variability of Collars collected a mean (±SE) 8.1 ± 1.7 fix loca- GPS fix success rates between tracked individuals tions per active collaring day, representing a significantly (22.0–88.3 %) is a commonly documented trend in greater maximum data resolution than of that collected satellite tracking, and could be attributed to the specific by VHF studies on Asian viverrids (Table 2; t = 11.604, behaviours of collared animals (Blackie 2010; Mattisson d.f. = 36, P < 0.01e-10). et al. 2010; Recio et al. 2011a). Collar-bearing civets utilised a range of microhabitat types, with some individuals (Males 3, 4, 6–8) residing in areas of greater Discussion undergrowth and canopy densities than others (Males 1, 2). These environmental factors can influence fix success The recent downsizing of satellite tracking technologies rates, and should be taken into consideration when has allowed a greater diversity of species to be collared designing and analyzing studies on tropical terrestrial with the aim of providing accurate and high-resolution species (Rempel et al. 1995; Mattisson et al. 2010; Gitzen spatiotemporal data. This study demonstrated the suc- et al. 2013) . cessful preliminary performance of small satellite collars, The volume and fine-scale spatiotemporal resolution both in stationary tests and deployed upon a novel small of data collected by satellite collars exceeded that of carnivore, the Malay civet. Asian VHF-based Viverridae studies, with satellite units Stationary test performance parameters of both first- collecting, on average, more than 16-times more locaand second-generation collars were comparable to the tions per sampling day than traditional radio-telemetry high fix success rates, accuracy, and precision values of methods. This increased data resolution allows for more other small satellite unit performance studies (Cain et al. biologically rigorous questions to be answered on wary and cryptic species in demanding field conditions, accuracy, quantity and quality otherwise unobtainable without the negative effects of VHF observer bias, and in this study area with alternative methods such as VHF for significantly less effort per resultant fix. Positive re- or camera trap surveys. The successful application of sults from this first civet GPS collaring, along with the GPS collars to V. tangalunga generated a large dataset of high quality and resolution of stationary trial data, fine-scale spatiotemporal information useful for identiconfirms this method as a strong alternative to tradi- fying landscape features important for the persistence of tional VHF telemetry tracking for small carnivore re- small tropical carnivores. This information can begin to search. fill the knowledge gaps currently afflicting the guild, such Despite these successful first deployments, it is of that informed and effective conservation management value to note a design limitation with this brand of plans might be drafted. Given a well-crafted study and satellite units. There is currently no standardized inter- sufficient funds, small carnivore scientists can utilize nal calibration value of GPS fix quality in these collars, satellite technologies to explore the next frontier in such as a dilution of precision (DOP), a common com- understanding and conserving this unique guild. ponent of most unit design. These values facilitate the development of post hoc data screening protocols in Acknowledgments We thank the Sabah Wildlife Department and order to increase the biological relevancy of acquired the Sabah Biodiversity Centre for issuing the research permits GPS data (Lewis et al. 2007; Frair et al. 2010) . npreocevsisdaerdybtyoScimonedDucatrbthyiFsosutunddya.tiWone, HaroeusgtroanteZfuolot,oPhthoeenfiuxnZdoinog, Study designs must carefully consider the objectives and Danau Girang Field Centre. A hearty thank you goes out to L. of their research before deciding upon the deployment of Evans, S. Edwards, and S. Joscelyne for their assistance on the satellite units, as several shortcomings must be overcome project. Further thanks go to A. Jennings, G. Veron, W. Heidrich, before the technology becomes a standard method in saunpdpoFr.t.Ku¨ mmeth for their knowledge, guidance and continued small carnivore research (Cooke 2008) . While collars utilised in this study are currently the smallest known Compliance with ethical standards This study was approved by mammalian long-term GPS units, 65 g is still much too amnedntcaonndduwcittehd tuhnedceleratrhaencjeuroisfdtihcetioSnaboafh SBaiboadhiveWrsiiltdyliCfeenDtreep.artlarge for certain species. For those species large enough to bear a tag, battery life can be an issue, such that long- COrpeeantivAeccCeossmmTohniss Aartttircilbeuitsiodnis4t.r0ibIuntetedrnuantidoenralthLeicteenrmses (hotftpth:/e/ term behavioural patterns are unable to be determined., which permits unrestricted The balance between data resolution and study long- use, distribution, and reproduction in any medium, provided you evity must be considered when planning studies (Ko- give appropriate credit to the original author(s) and the source, channy et al. 2002; Land et al. 2006 ; Tomkiewicz et al. provide a link to the Creative Commons license, and indicate if 2010). changes were made. Furthermore, GPS hardware is currently more expensive than VHF transmitters (Rodgers 2001) . This high initial cost can pose a logistical barrier to projects, References and researchers must not sacrifice statistical power in the blind pursuit of advanced techniques. Many scientists Abram NK, Xofix P, Tzanopoulos J, MacMillan DC, Ancrenaz M, discuss that for certain research questions, analytical Chung R, Peter L, Ong R, Lackman I, Goossens B, Ambu L, rigor is strengthened more so by an increase in the Knight AT (2014) Synergies for improving oil palm production number of individuals tracked than by the number of a9:ned95f3o8r8e.stdocio:1n0se.1r3v7a1ti/ojonurinnafll.opoodnpe.l0a0in95l3a8n8dscapes. PLoS One locations per animal (Hebblewhite and Haydon 2010) . Amstrup SC, Mcdonald TL, Durner GM (2004) Using satellite Researchers must then carefully consider their specific radiotelemetry data to delineate and manage wildlife populastudy aims, budget, focal species, and working condi- tions. Wildl Soc Bull 32:661–679. doi: 10.2193/0091-7648(2004) tions to strike a balance between the deployment of 032[0661:USRDTD]2.0.CO;2 several expensive GPS units vs. a larger number of VHF Anccrreennaazz MI(,2G00o4o)sDseentserBm,inGaitmioenneozf Oap,eSdawistarnibguAtio,nLaacnkdmpaonp-uAlna-collars, as this study demonstrated. Additionally, when tion size using ground and aerial surveys: a case study with GPS collar failures do occur, they are considerably more orang-utans in lower Kinabatangan, Sabah, Malaysia. Anim costly in both value and relative data loss than VHF Conserv 7:375–385. doi:10.1017/S136794300400157X failures. A large amount of GPS collar failures have BanRdJe,irCaodeelhMoeCloML F(2,0L0i7m) aSeScar´beattloivMes Ao,f VmaaznMedawgnoilvEeMs(,CYhoryusnogbeen documented in field-deployed scenarios (Blake cyon brachyurus Illiger 1815): as revealed by GPS tracking et al. 2001; Johnson et al. 2002; Gau et al. 2004 ; Heb- collars. 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First known satellite collaring of a viverrid species: preliminary performance and implications of GPS tracking Malay civets (Viverra tangalunga), Ecological Research, 2016, DOI: 10.1007/s11284-016-1338-y