Population Dynamics, Herd Behavior, and Genetic Analysis of the Critically Endangered Tamaraw (Bubalus Mindorensis ): a Mini Review

Journal of Developments in Sustainable Agriculture/ : +-0ῌ +.* ( ,*+* )

Population Dynamics, Herd Behavior, and Genetic Analysis of the Critically Endangered Tamaraw (Bubalus mindorensis ): A Mini Review

Shinya Ishihara and Yukio Kanai*

Graduate School of Life and Environmental Sciences, University of Tsukuba, Tsukuba, Ibaraki-*/ῌ 2/1, , Japan

The tamaraw (Bubalus mindorensis ) is a wild bu# alo endemic to Island of Mindoro, Philippines and one of the world’s critically endangered animals. In the early+3** s the tamaraw could be seen all over the island of Mindoro, but its distribution is now restricted to only three protected areas, with a total estimated population of about,/* . The main reasons for its population decline have been unrelenting habitat destruction and illegal hunting. Recent ﬁeld surveys of the tamaraw have revealed that survival of the tamaraw in the Aruyan Preserve is critical, and the subpopulation in the Mount Iglit-Baco National Park seems to be the only core herd that can be subjected to a practical conservation program. Identiﬁcation of the tamaraw by fecal DNA analysis would be useful in further studies to verify the animal’s ecological behavior, including its existence, range, population dynamics, and genetic diversity.

Key words: tamaraw, population, behavior, fecal DNA, genetic analysis

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Introduction the ecological features of tamaraw, such as its population dynamics and herd behavior, from in- The tamaraw (Bubalus mindorensis ) (Fig.+ ) is a formation in the literature and from recent ﬁeld wild dwarf bu# alo endemic to the island of Mindoro surveys jointly organized by the Department of En- in the Philippines. This animal has been categorized vironment and Natural Resources (DENR) in the as “critically endangered” on the International Union Philippines, the Philippine Carabao Center (PCC), for the Conservation of Nature and Natural Re- and our group (Ishiharaet al., ,**1 , Matsubayashi sources (IUCN) Red List (Hedgeset al.,,**3 ), et al., ,**3 ). and it is listed in Convention on International Trade Changes in the Tamaraw Population and ,**3 in Endangered Species Appendix I (UNEP, ). Habitat during the,* th Century The Philippine government prohibited the killing or wounding of tamaraw, or their removal from their The population of the tamaraw in the early+3** s habitat, by law as early as+3-0 . However, the on Mindoro Island was estimated to be around population has remained low because of relentless+* , *** individuals, but over-hunting and exploita- habitat destruction and poaching. E# ective conser- tion of habitat due to human population increases vation strategies are needed to save the tamaraw resulted in a drastic decline in the population to less from extinction, but such strategies will need eco- than+*** by +3.3 (Harrison, +303 ). As a result, logical information on the animal, including its the distribution of tamaraw at the end of the,* th population dynamics, herd behavior, and genetic Century was highly fragmented and restricted to diversity. Such information is currently extremely three regions of Mindoro Island: the Mount Iglit- limited. This paper provides a general overview of Baco National Park (MIBNP), Mount Aruyan changes in the tamaraw’s population and habitat Preserve, and Mount Calavite Preserve; MIBNP during the,* th Century. It also describes some of held the largest tamaraw population. In+313 the

Received: October,0 , ,**3 , Accepted: December + , ,**3 * Corresponding author: Professor Yukio Kanai, University of Tsukuba, Tennodai+ῌῌ + + , Tsukuba, Ibaraki -*/ ῌ 2/1, , Japan. Tel:ῌῌ2+ῌῌῌ ,32 /- 002/ , Fax: 2+ ῌῌῌ ,32 /- 00+1 , E-mail: [email protected] Ishihara and Kanai: Population Dynamics, Herd Behavior, and Genetic Analysis of the Critically Endangered Tamaraw 137

Population Dynamics of Tamaraw in Mount Iglit-Baco National Park

Knowledge of population number is absolutely necessary for conservation biology, because this parameter is the best indicator to decide whether the species is going to the extinction or not (Primack,+33- ). MIBNP ( 1/ , .// ha) consists of hilly terraces at altitudes ranging between-** and +***m. The tamaraw conservation area ( +0 , *** ha; altitude range0** to + , *** m) consists of natural grassland covered with perennial herbage (Fig., ). PCC and DENR jointly conducted field surveys of ,**0 Fig.+ . Tamaraw (Bubalus mindorensis ) in MIBNP. the MIBNP tamaraw population in . Direct observations were made simultaneously from multiple vantage points. Sixteen sites were strategically Philippine government took action to conserve the located to minimize blind areas such as trees, tall tamaraw as part of its Tamaraw Conservation Pro- grass, hills, and valleys. Observations were made gram (TCP). As part of this program, in+333 the simultaneously from / : -* AM to 1 : ** AM and DENR initiated an annual survey of the tamaraw from/** : PM to 0-* : PM, because it is known population in MIBNP. The annual records of the that tamaraw leave their hiding places to graze on TCP show that the tamaraw population in MIBNP grass sprouts when it is cool, around sunrise or has remained at,/* for the past decade (Ishiharaet sunset. The tamaraw that were observed were al., ,**1). Only limited information is available on distinguished by age and sex by the method of the other two tamaraw habitats because of the Kuehn (+320 ). The tamaraw sighted at same time di$ culty in accessing these locations and in sighting and same location from more than, observation the animal there (Hedgeset al., ,**2 ). Recently, sites were classified as the same individuals that had Matsubayashiet al. (,**3 ) conducted a field survey been double or multiple-counted and deducted from in Mount Aruyan Preserve and found that the total counted individuals. Finally, the estimated tamaraw habitat completely overlaps with the dis- population size of tamaraw in MIBNP was decided. tribution of the local indigenous people, the From this survey, approximately,/* individuals Mangyan; slash-and-burn farming by the Mangyan were estimated to be present in MIBNP. Thus the has substantially reduced the tamaraw’s habitat. tamaraw population was still in the critical range. Moreover, poaching by outsiders with guns has There was also a considerable deviation in the sex directly contributed to the severe decline in the ratio of adult animals and in the proportion of animal’s population. Although Matsubayashiet al., juveniles to yearlings (Table+ ; Ishihara et al., succeeded in identifying one male tamaraw by,**1 ). In the observed adult tamaraw, there were camera trap and some individuals by hoof prints, significantly more females than males, and the juve- signs of foraging, and the presence of fresh feces, nile individual numbers were lower than expected their results indicate that conservation of the based on the yearling numbers. This may be be- tamaraw in the Mount Aruyan habitat is likely to cause some tamaraw such as solitary bulls or juve- prove extremely di$ cult. Whether the tamaraw nile males are driven out from the family and has survived in the Mt. Calavite area is still un- become distributed in the outer areas of MIBNP. known. Therefore, the tamaraw subpopulation in Herd Behavior of Tamaraw MIBNP seems to be the only one that can be subjected to a realistic conservation program. An understanding of the herd behavior, such as the mating system, of a species is important in both in situ and ex situ conservation. In situ, rare animals tend to su# er inbreeding depression be- 138 J. Dev. Sus. Agr./+ ( )

Fig., . Representative landscapes in MIBNP.

Table+ . Individual numbers of tamaraw in indicator of a population’s ability to maintain its Mount Iglit-Baco National Park in,**0 (Ishihara genetic diversity (Parker and Waite,+331 ). In ex et al., ,**1) situ systems an understanding of mating systems is Adult Juvenile Yearling Total very important for reproductive management in captivity. Since+32, , the Philippine government has /- 2 , 0- Mele captured,* tamaraw individuals in their habitat and +*, +, + ++/ Female has attempted to breed them in captivity. Howev- 1-,.02/ Unidentified er, this first trial of captive breeding was unsuccess- Total +0, /, .3 ,0- ful because of a lack of information on the animal’s Adults, estimated as more than/ years old; ecological behavior, especially in relation to its juveniles, estimated between+. and years old; mating system. At present, only one captured female yearlings, estimated at less than+ year old. is still alive, with her one descendant male. Kuehn (+320 ) examined the social behavior of the tamaraw in MIBNP and reported that, out of cause of their small populations. Inbreeding is,+2 observations during ,,+ days, +1, ( 2,ῌ ) were associated with fitness deficit, which may further lone bulls. He deduced that the tamaraw was orig- reduce the e# ective size of already small popula-inally forest-adapted, because forest-dwelling ungu- tions (Saccheriet al., +333 ). Mating systems such lates are largely solitary or monogamous (Geist, as monogynous, polygynous, and polyandry sys-+31. ). Ishiharaet al. ( ,**1 ) also studied the herd tems influence relatedness levels and have large behavior of tamaraw in MIBNP. They classified e## ects on e ective population size, which is an tamaraw sightings into single animals or herds. Ishihara and Kanai: Population Dynamics, Herd Behavior, and Genetic Analysis of the Critically Endangered Tamaraw 139

The observed herds of tamaraw were further classi- genetic diversity analysis, as has been used in some fied into seven types based on the ratios of bull to rare wild animals (Russelloet al., ,**. ). cows: monogamous (one bull and one cow), polyg- Conclusion amous (one bull and two cows or one bull and three cows), and so on. Our study showed that the Despite worldwide concern and protection by the majority of the tamaraw (23ῌ ) lived in families Philippine government, the tamaraw is still threat- ranging in size from two to seven individuals and ened by extinction, as shown by its distribution and the rest (++ῌ ) were solitary (mostly bulls). The population size. At present, the tamaraw sub- ratio of monogamous to polygamous families was population in MIBNP is the only one targetable by +0to ,* . These results may suggest that the tamaraw a practical conservation program, and continuous has changed its mating system from forest-dwelling and wider ranging surveys are needed in this pre- type to grassland-dwelling type between+320 and serve. To make the tamaraw conservation program ,**1by adapting its behavior to new environments. more e # ective, precise assessments of their ecologi- Genetic Analysis of Tamaraw cal behaviors (e.g. habitat selection, mating behavior, and genetic diversity) are urgently needed. As techniques of molecular analysis have de- References veloped, DNA has become a useful tool in conservation biology and wildlife management in terms of Avise, J.C.,,*** . Phylogeography: the History and Forma- acquiring valuable information on behavioral and tion of Species. Harvard University Press, Cambridge MA. ecological features. For example, phylogeographic Brown, W.M., M. George, and A.C. Wilson.,+313 . Rapid analysis using molecular techniques can reveal evi- evolution of animal mitochondrial DNA. Proceedings dence of both ancient and recent demographic of the National Academy Science (USA)10 , +301ῌ +31+ events, such as population size change or dispersal . ,**+ ,*** Garnier, J.N., Bruford, M.W. and Goossens, B., . (Avise, ). Mitochondrial DNA (mt-DNA) Mating system and reproductive skew in the black evolves much faster than nuclear DNA and thus rhinoceros. Molecular Ecology+*,*-+ῌ +*,*.+ . contains greater sequence diversity than nuclear Geist, V.,+31. . On the relationship of social evolution and DNA (Brownet al., +313 ). For example, mt-DNA ecology in ungulates. American Zoologist+. , ,*/ῌ ,,* . +303 cytochromeb has been used in species identification Harrison, T., . The Tamaraw and its Survival. The +330 tamaraw and its survival. International Union for the and phylogeographic analysis (Tanakaet al., ; Conservation of Nature and Natural Resources (New Paxinoset al., +331 ), and the D-loop has been used Series),,2/20 :ῌ . in studies of genetic diversity and in phylogeo- Hedges, S., Duckworth, J.W., de Leon, J., Custodio, C. and graphic analysis (Lauet al., +332 ). Microsatellites Gonzales, J.C.,,**2 .Bubalus mindorensis. In: IUCN ,**3. IUCN Red List of Threatened Species. Version have also been used to acquire ecological informa- ,**3. + . Retrieved on *0 June ,**3 from῍ http:// ,**+ tion. Garnieret al. ( ) studied the mating www.iucnredlist.org/῎ . system of the black rhinoceros by using micro- Ho¨ss, M., Kohn, M., Pa¨äbo, S., Knauer, F. and Schröder, satellites. However, it is di$ cult to collect DNA W.,+33, . Excrement analysis by PCR. Nature -/3 , +33 directly from rare animals like the tamaraw. . Ishihara, S., Ishida, A., Del Barrio, A.N., Lapitan, R.M., Fecal samples are very useful for collecting DNA Atabay, E., Boyles, R.M., Salac, R.L., de Leon, J.L., noninvasively (Ho¨sset al., +33, ) because their Eduarte, M.M., Cruz, L.C. and Kanai, Y.,,**1 . Field surfaces contain intestinal epithelial cells. Tamaraw survey on Tamaraw (Bubalus mindorensis )ῌ Present feces can be found easier than tamaraw individuals population size and herd behavior in wild. Italian Jour- 0 , +,.3ῌ +,/+ in MIBNP. Ishiharaet al. (,*+* ) developed a nal of Animal Science (suppl. ), . Ishihara, S., Herrela, R.J., Ijiri, D., Matsubayashi, H., method for identifying tamaraw from feces collect- Hirabayashi, M., Del Barrio, A.N., Boyles, R.M., ed in the wild by using the cytochromeb gene. This Eduarte, M.M., Salac, R.L., Cruz, L.C. and Kanai, Y., method o# ers promise for verifying the existence of ,*+*. Identification of tamaraw (Bubalus mindorensis ) tamaraw in the field in areas where it is hoped that from outdoor-derived fecal samples by PCR-RFLP analysis of cytochromeb gene. Animal Science Journal they still exist. If the feces are verified as originat- (under review). ing from the tamaraw, D-loop analysis of fecal Kuehn, D.W.,+320 . Population and social characteristics of samples can then be used as a powerful tool for the tamarao (Bubalus mindorensis ). Biotropica+2 , ,0-ῌ 140 J. Dev. Sus. Agr./+ ( )

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