Prosser et al. BMC Zoology (2016) 1:8 DOI 10.1186/s40850-016-0007-5 BMC Zoology RESEARCH ARTICLE Open Access Body condition scoring of Bornean banteng in logged forests Naomi S. Prosser1,2*, Penny C. Gardner1,2, Jeremy A. Smith2,3, Jocelyn Goon Ee Wern1, Laurentius N. Ambu4 and Benoit Goossens1,2,4,5* Abstract Background: The Bornean banteng (Bos javanicus lowi) is an endangered subspecies that often inhabits logged forest; however very little is known about the effects of logging on their ecology, despite the differing effects this has on other ungulate species. A body condition scoring system was created for the Bornean banteng using camera trap photographs from five forests in Sabah, Malaysia, with various past and present management combinations to establish if banteng nutrition suffered as a result of forest disturbance. Results: One hundred and eleven individuals were photographed over 38,009 camera trap nights from April 2011 to June 2014 in five forests. Banteng within forests that had a recent history of reduced-impact logging had higher body condition scores than banteng within conventionally logged forest. Conversely, when past logging was conducted using a conventional technique and the period of forest regeneration was relatively long; the banteng had higher body condition scores. Conclusion: The body condition scoring system is appropriate for monitoring the long-term nutrition of the Bornean banteng and for evaluating the extent of the impact caused by present-day reduced-impact logging methods. Reduced-impact logging techniques give rise to individuals with the higher body condition scores in the shorter term, which then decline over time. In contrast the trend is opposite for conventional logging, which demonstrates the complex effects of logging on banteng body condition scores. This is likely to be due to differences in regeneration between forests that have been previously logged using differing methods. Keywords: Body condition scoring, Camera trap, Habitat degradation, Reduced-impact logging, Sabah, Tropical forest Background animals in the field; for example on Indian elephants Body condition scores (BCS) measure the amount of soft (Elephas maximus indicus) by Ramesh et al. [4], and from tissue an animal has relative to its size and are useful as photographs of mule deer (Odocoileus hemionus eremicus) a general guide to the health and fitness of an animal by Marshal et al. [5] and Sri Lankan elephant (Elephas [1, 2]. Usually BCS systems allocate a number that is asso- maximus maximus) by Fernando et al. [6]. Visual BCS ciated with condition, with lower scores given to animals systems are useful for animals that cannot be handled [7]. in poorer condition [3]. Many BCS systems for domestic Non-invasive scoring of mammal body condition using mammals use palpitation to more accurately assess the camera traps furthers the scope for BCS applications in condition [1, 2], however this is not practical in wild ani- wildlife management and for assessing the health of highly mal studies as they would first have to be captured, which elusive species such as the Bornean banteng (Bos is both costly and stressful for the animal. There are BCS javanicus lowi)thatarenotdirectlyobservableinthe techniques developed for visual assessment of wild wild. BCS systems are straightforward to conduct, al- though variability can arise between observer [7, 8]. Clear * Correspondence: [email protected]; [email protected] and systematic BCS systems are beneficial because they 1Danau Girang Field Centre, c/o Sabah Wildlife Department, Wisma Muis, can be implemented by wildlife managers [9] and because 88100 Kota Kinabalu, Sabah, Malaysia they are reliable in tracking changes in soft tissue carried 2Organisms and Environment Division, School of Biosciences, Cardiff University, Sir Martin Evans Building, Museum Avenue, Cardiff CF10 3AX, UK by an animal over time (Edmonson et al. 1989 cited in [3]). Full list of author information is available at the end of the article © 2016 The Author(s). Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Prosser et al. BMC Zoology (2016) 1:8 Page 2 of 8 BCS provide invaluable information on the health of destructive types of management should result in re- the animal on an individual scale that can be related to duced body condition. the strength of their immune system (e.g. [10]), age at The body condition of banteng in Sabah should reflect which they first breed (Carrion et al. 2007 cited in [8]), the habitat suitability of the forests and the health of the fertility [8] and mortality [11, 12]. Monitoring individual banteng populations (Adamczewski 1993 cited in [8]). health allows the tracking of the health at the population Logging alters the vegetation composition of a forest scale [13] and BCS can be used to evaluate the factors [18], therefore it is important to know how logging prac- limiting population growth [5]. If body condition is low, tices affect banteng body condition. This information nutrition is likely to be the key limiting factor in popula- will be especially important as there is currently very lit- tion growth (Bowyer 2005 cited in [5]) but it may also tle knowledge of the impact of logging on banteng [18]. indicate that the population has reached its carrying cap- At present there is very little unlogged forest remaining acity [5, 8]. For these reasons it is possible that compar- in Sabah [22] suggesting that it is likely that banteng will ing results of BCS across different habitats may show be confined to commercial forests in the very near fu- optimal management techniques and be an indication of ture. Comparisons of banteng BCS from forests that dif- the longer term effects of different treatments. fer in management may indicate the suitability of the Banteng are classified as endangered by the IUCN Red management techniques and the most effective approach List with the rate of their population decline being to conserve the banteng in commercially managed greater than 80 % in the last three generations in parts forest. of their range [14]. The population size and structure in We conducted the first identification of individual Sabah is unknown due to a lack of data [15]. The home banteng in Sabah using unique natural markings. We range of banteng in Borneo is also unknown, however a then created the first BCS system using non-invasive bull has been observed travelling 23 km (P. Gardner un- camera trap images to identify the impact of the imple- published observations cited in [15]) and herds of Bos mentation of conventional logging, RIL and protection javanicus birmanicus can occupy home ranges of up to from logging, both in the past and present, upon the 44.8 km2 (Prayurasithi 1997 cited in [15]). The subpopu- health of banteng in Sabah. It was expected that banteng lations studied here were not recaptured in any of the living in forests with longer post-logging regeneration other forests studied. Banteng are crepuscular in their times and which had been subjected to RIL instead of activities, spending more time on foraging and social ac- conventional techniques would have higher BCS. tivity at dawn and dusk, while the mid-part of the day is largely spent ruminating (P. Gardner unpublished obser- Methods vations cited in [15]). They feed on a wide variety of Study sites plant material, opting to graze in open areas and are Camera trap surveys were conducted in five forests in more frequently found in open dipterocarp forests when Sabah, Malaysian Borneo: Tabin Wildlife Reserve, Malua available [15–17]. The Bornean subspecies is recorded as Forest Reserve, the buffer zone of Maliau Basin Conserva- living in secondary forests and that logging, which opens tion Area, Sipitang Forest Reserve and Sapulut Forest Re- up the forest floor, may benefit banteng due to the in- serve, located in east, east-central, south-central, south creased understory growth [14, 17, 18]. This suggestion and west of Sabah, respectively (Fig. 1). Within these loca- is supported by Meijaard and Sheil [19] who observed tions the habitat that is inhabited by banteng is predomin- that, with the exception of frugivores, ungulates are ately lowland and hill dipterocarp forest and freshwater more successful in logged forests. Logging however swamp forest. The forests experience uniform tempera- removes timber and alters the habitat that may provide tures and very little variation in rainfall across the year vital food sources for the banteng [18] and creates ex- [23], however extensive climatic data is not available. tensive disturbance [20]. Ancrenaz et al. [20] found it These forests have undergone different past and present was possible to maintain populations of orangutans logging management methods (Table 1). (Pongo pygmaeus morio) within commercial forests that adopt reduced-impact logging (RIL) techniques, whereas Data collection conventional logging was more damaging and resulted Camera trap images of banteng were obtained from the in localized extinctions. This pattern is also likely to be five forest reserves at differing time periods and camera true for the Bornean banteng; Deramakot Forest Reserve trap stations were distributed in a grid format and/or on in Sabah utilizes RIL techniques and observations sug- an ad-hoc basis (Table 2). The differing sampling gest it may support a denser population of banteng [21]. schemes were due to two different prior studies of ban- Itispossiblethatpastandpresentloggingtechniques teng with different objectives: a PhD project by Gardner and management agendas will differ in their effect [24] and a state-wide survey of the remnant banteng upon banteng populations, and that the most populations.