diet of lowland tapir (tapirus terrestris) in el rey national park, salta, argentina

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© 2012 Wiley Publishing Asia Pty Ltd, ISZS and IOZ/CAS

Integrative Zoology 2013; 8: 48–56 doi: 10.1111/j.1749-4877.2012.12009.x

ORIGINAL ARTICLE

Diet of lowland tapir (Tapirus terrestris) in El Rey National Park, Salta, Argentina

Silvia C. CHALUKIAN,1,4 M. Soledad de BUSTOS2,4 and R. Leonidas LIZÁRRAGA3,4

1IUCN Tapir Specialist Group, Salta, Argentina, 2Secretaría de Ambiente, Gobierno de Salta, Argentina, 3National Parks Administration, Salta, Argentina and 4Tapir Conservation and Research Project, Salta, Argentina

AbstractLowland tapir (Tapirus terrestris) is the largest herbivore in the Neotropics and, in Argentina, it inhabits a vari-ety of habitats from 100 to 2100 m asl. Lowland tapirs importantly influence their habitat structure because they are selective browsers, seed predators and long-distance seed dispersers. However, increased knowledge of ta-pir ecology is necessary to support the conservation and management of the species in natural and human-mod-ified environments. Between Jun 2002 and Dec 2008 we assessed the tapir’s diet in El Rey National Park, Salta, northwestern Argentina. We collected fresh feces and recorded browsing signs, and we recorded direct obser-vations of tapirs while they were feeding. We analyzed 88 feces samples that had been dried and subsequently weighed. Feces were dominated by fibers and leaves (84.09%), while fruit parts represented a small proportion of the weight (15.91%). During the dry months, a greater percentage of seeds were found in the feces, mainly due to the availability of 3 species of Fabaceae fruits. We recorded a total of 57 plant species from 26 families. Tapirs are adapted to extreme habitats, switching their diet from frugivory to herbivory when fruits are scarce. Considering this, forest remnants and even secondary growth fields should be protected from deforestation.

Key words: diet, feces, lowland tapir, subtropical Andean montane forest

Correspondence: Silvia C. Chalukian, IUCN Tapir Specialist Group, Rio Negro 2508, Bº Tribuno, Salta, Argentina.Email: [email protected]

INTRODUCTIONLowland tapir [Tapirus terrestris (Linneaus, 1758)]

is the largest herbivore in the Neotropics and rang-es from Venezuela to northern Argentina. In Argentina, the species inhabits savannas, flooded grasslands, ripar-

ian forests, dry Chaco forests and Andean montane for-ests, and is found at altitudinal ranges between 100 and 2100 m asl (Bodmer & Brooks 1997; Chalukian & Me-rino 2006; Soler 2006; Taber et al. 2008; Chalukian et al. 2009a) (Fig. 1). The species is classified as ‘vulner-able’ at a global level (IUCN 2011), but is considered ‘endangered’ in Argentina (Ojeda et al. 2012). It is es-timated that the tapir’s distribution in Argentina has de-creased by 46% in the last 100 years (Taber et al. 2008; Chalukian et al. 2009b). Furthermore, the species’ sta-tus appears to be worsening as national and provincial policies enable an agricultural production model that

mailto:[email protected]

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Diet of lowland tapir in NW Argentina


is transforming large swaths of the region’s forests and wetlands to field or pasture (Chalukian 2006; Fig. 1).

Lowland tapirs importantly influence their habitat structure, as they are selective browsers, seed predators and long-distance seed dispersers (Bodmer 1990, 1991; Rodríguez et al.1993; Salas & Fuller 1996; Fragoso 1997; Olmos 1997; Painter 1998; Fragoso & Huffman 2000; Fragoso et al. 2003; de Bustos et al. 2004; Tobler et al. 2010). Tapir foraging behavior may be particular-ly important for the dispersion of palms and other spe-cies with large seeds (Fragoso & Huffman 2000; Tobler et al. 2010).

In tropical regions, tapirs are known to forage in tall and dense forests, as well as in open and secondary for-ests (Salas 1996; Salas & Fuller 1996; Painter 1998), behavior also reported in El Rey National Park (ERNP) (Lepera 2005). However, information on tapir diet and foraging is scarce in the subtropical Andean montane forests and better knowledge is needed to support con-servation and management planning in these regions. In this study, we assess tapir diet in ERNP, which is locat-ed in Andean montane forest in Argentina, and compare our results to similar studies in South America.

MATERIALS AND METHODS

Study area

The study was carried out in ERNP (44 162 ha), lo-cated in the southeastern part of Salta (24°33′–24°49′S,

64°30′–64°45′W, 700–2300 m asl) (Fig. 1). ERNP pro-tects a representative sample of subtropical Andean forest (Dinerstein et al. 1995; Taber et al. 2008), also referred to as Yungas forest (Cabrera 1976), and repre-sents the southernmost distribution of this forest type, which is still inhabited by tapirs. The climate is subtrop-ical or moderately temperate and rainy, with a non-rig-orous dry winter (Mendoza & González 2011). Mean annual rainfall was 996 mm in years 2000–2007, at 900 m asl (ERNP weather station records), with 82% of rain-fall occurring between December and April.

The area is covered by mature and secondary mon-tane and transitional forests, where 7 vegetation types have been described (Chalukian 1991; Chalukian et al. 2007). This study included 3 habitat types: ‘tipa’ (Tipua-na tipu) forest, ‘cebil’ (Anadenanthera colubrina and Parapiptadenia excelsa) forest, and secondary forests and riparian habitats. The study was conducted within an altitudinal range of 750 to 1200 m asl

ERNP protects most of Del Valle River upper basin. A variety of Yungas mammals are found in this area, in-cluding 8 carnivore species, 1 primate species and 5 un-gulate species: tapirs, 2 peccaries [Pecari tajacu (Lin-naeus, 1758) and Tayassu pecari (Link, 1795)] and 2 brocket deer [Mazama gouazoubira (Fischer, 1814) and Mazama americana (Erxleben, 1777)]. Although no density estimation has been conducted, tapirs are report-ed to be abundant (Chalukian & Taber 2007).

Plant species records, feces sample collection and preparation

The study area was surveyed monthly between Jun 2002 and Dec 2008 by walking on trails and roads and by examining streams and latrines commonly frequent-ed by the tapir. We collected evidence of browsing and fresh tapir feces (no more than a few days old). We considered that a plant was eaten by tapirs if the plant showed signs of teeth marks (Fig. 2) and tapir footprints were seen next to the eaten plant. We also recorded di-rect observations of tapirs feeding (Fig. 3). Plant species were classified according to their life forms.

We washed and rinsed feces in voile bags, drained liquids and dried the solid content in the sun or in a warm room while exposing the bags on 1 m2 plastic trays with kitchen paper. Each sample of dried feces was weighed individually.

Seeds that were visible were separated from dried fe-ces and its species identified by comparison with known seeds collected from field plants or specimens seen at the Herbarium of Salta University. Remaining contents

Figure 1 Lowland tapir distribution and status in Argentina (Chalukian et al. 2009) and study area location.

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of dry feces were sifted through sieves of 3 sizes (25, 1 and 0.25 mm2) to classify them into coarse, medium and small-sized material. From each feces samples, two 5 g samples of coarse and medium size materials (1 of each) were further separated into fruit parts (including seeds) and fiber plus leaves (including stems, bark and uniden-tified vegetative parts). They were then weighed us-ing a digital scale (Naranjo & Cruz 1998; Herrera et al. 1999).

Data analysis

The proportion of fruit/fiber by weight in the 5 g samples was extrapolated to the weight of coarse and medium size materials to obtain the overall proportion of fruit/fiber in each feces. We compared the proportion of fruit/fibers by weight between dry and wet seasons using a Mann–Whitney test (Zar 1984). We used INFO-STAT software (2010), with the Wilcoxon (Mann–Whit-ney) function.

RESULTSWe analyzed 88 feces samples. Mean dry weight was

301.62 g (SD = 170.14; min = 70.86; max = 796.77). A total of 25 feces samples (28.4%) were collected during the rainy season and 63 (71.6%) during the dry season. Dry feces material was dominated (84.09%) by fibers and leaves, while 15.91% of its weight was made up of fruit parts. In the dry season, there was a significant-ly higher proportion of fruit parts than in the wet season (18.33 vs 9.79%) (Table 1).

We recorded a total of 57 plant species (1 non-identi-fied) and 26 families in the tapir’s diet. Among these, 44 species were observed being eaten in the field, 8 species were only found in feces, and 5 species were recorded through both methods. Of the total species recorded, 22 species were trees, 8 were shrubs, 23 forbs, 4 vines, 3 grasses and 3 ferns. Tapirs consumed leaves and stems of 41 species, only fruits of 16 species, fruits and veg-etative parts from 3 species, flowers and fruits from 1 species, flowers and vegetative parts from 2 species and all parts from 6 species (Table 2).

DISCUSSIONOur results on food items encountered in feces of ta-

pirs at ERNP indicate that tapirs are mainly folivores (browsers and less grazers) and secondarily frugivores. A previous study in this area considered tapirs as foli-vorous, because they recorded 12 forb species from in-conspicuous seeds germinating in their feces (Varela & Brown 1995), which might be regarded as ‘passive fru-givory’ (see Hibert et al. 2011). However, they collected feces only during July, when most of the fruits we found are unripe and, therefore, not still fully unavailable.

According to our data, even though tapirs from Yun-gas are less frugivorous than in other forests of the Neo-tropics (Table 3), they consume a high percentage of fruits from a diversity of plant life forms, as also report-ed by Richard and Julia (2000). In ERNP, there are no naturally occurring palms (Arecaceae) nor trees with large fleshy fruits such as the ones found in tropical for-

Figure 2 Tapir’s teeth marks in a Vassobia breviflora sapling. Figure 3 Tapir feeding on shrub leaves in ERNP (G. Angell, IUCN Tapir Specialist Group).

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Table 1 Seasonal composition of the mean percent of dry weight of plant parts ± SD in lowland tapir fecal samples found between July 2002 and July 2006 in El Rey National Park, Salta, Argentina. Weight between seasons was compared using Mann–Whitney (U). **highly statistically significant amongst seasons, P ≤ 0.01

Food items in feces Season N Mean dry weight (% ± SD) U df P Fibers & leaves Wet 25 90.21 ± 17.32 1517.50 1 0.0002**

Dry 63 81.67 ± 14.37Fruit Wet 25 09.79 ± 17.32 707.50 1 0.0002**

Dry 63 18.33 ± 14.37

Table 2 Plant species recorded as tapir food from feces analysis, direct observations and other researchers, in El Rey National Park, Salta, Argentina

Plant species Life formParts eaten

Leaves & stems Flowers Fruits Whole

DoryopteridaceaePolystichum montevidense θ Fern xEquisetaceaeEquisetum giganteum θ Fern xEquisetum bogotense θ Fern xPiperaceaePiper hieronymi θ Tree xPiper tucumanum θ Tree xSmilacaceaeSmilax sp. θ Vine xCommelinaceaeTradescantia sp. * Forb x PhytolaccaceaePhytolacca bogotensis θ Forb x xVitaceaeCissus sp. θ Vine xZygophyllaceaePorlieria microphylla θ Tree xAmaranthaceaeChenopodium aff. ambrosioides θ Forb x xOxalidaceaeOxalis sp. θ* Forb xSantalaceaeAcanthosyris falcata δ Tree xPolygonaceaePolygonum hispidum θδ Forb xRumex sp. θ* Forb x xRuprechtia apetala θ Tree xRuprechtia laxiflora θ Tree x

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MyrtaceaeEugenia uniflora θ Tree xEugenia pungens θ Tree xMyrcianthes cisplatensis θ Tree xBlepharocalyx salicifolia θ Tree xOnagraceaeLudwigia sp. θ* Forb x xSalicaceaeSalix humboldtiana θ Tree xXylosma pubescens θ Tree xFabaceaeAcacia aroma δ Tree xAcacia praecox θ Tree xAnadenanthera colubrina δ Tree xEnterolobium contortosiliquum θδ Tree x xDesmodium sp. θδ Forb xGleditsia amorphoides δ Tree xRhamnaceaeScutia buxifolia θ Tree xRosaceaeDuchesnea indica θ Forb xUrticaceaeUrera baccifera θ Shrub xPhenax laevigatus θ* Shrub xUrtica dioica θ Forb xAnacardiaceaeSchinus gracilipes θ Tree xJuglandaceaeJuglans australis θδ Tree x xSapindaceaeAllophylus edulis θ Tree xAcanthaceaeDicliptera tweediana θ Forb x xAsteraceaePluchea sagitalis θ Forb xBaccharis dracunculifolia θ Forb xEupatorium sp. θ Forb xConyza sp. θ Forb xSolidago chilensis θ Forb xMikania cordifolia θ* Vine x x

Table 2 Continued

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Senecio sp. θ Forb xBaccharis medulosa θ Forb xOphryporus sp. θ Forb xTessaria sp. θ Shrub xVernonia squamulosa θ Shrub xSonchus sp. * Forb xNon identified θ Forb xSolanaceaeCestrum sp. * Shrub xSolanum lorentzii θδ Shrub x xSolanum tucumanense * Shrub xVassobia breviflora θ Tree xSolanum claviceps δ Shrub xSolanum sp. * Shrub xValerianaceaeValeriana effusa θ Forb xConvolvulaceae Ipomoea sp. * Vine xPoaceaePanicum laxum * Grass xPaspalum humboldtianum δ Grass xSetaria verticillata δ Grass xSorghum sp. δ Grass x

θ direct observations; δ feces analysis; *cited by Varela and Brown (1995).

ests (e.g. Sapotaceae, Apocynaceae, Anacardiaceae and Melastomataceae) (Fragoso & Huffman 2000; Frago-so et al. 2003; Tobler 2008; Sallenave 2009; Tobler et al. 2010; Hibert et al. 2011). Instead, most of the fruits available to tapir are legumes (e.g. Acacia aroma, En-terolobium contortisiliquum, Gleditsia amorphoides and A. macrocarpa) that fall to the ground during the dry season (Brown 1995; S. C. Chalukian, M. S. de Bustos & R. L. Lizarraga, pers. observ.). Further north in the subtropical Andean forests of Argentina, at similar ele-vations, tapirs have been reported to eat Agonandra ex-celsa and Chrysophyllum gonocarpum, fleshy fruits available during the dry season (M. S. de Bustos, pers. observ.), which are absent in ERNP. Latitudinal varia-

Table 2 Continued

tion in tapir diet is a consequence of food species avail-ability, as plant species diversity in Neotropical montane forests decreases from north to south, which is reflected in fruit diversity (Gentry 2001).

We found less diversity of fruit species in tapir diet in ERNP than the diversity reported in most of the other areas of the species’ range (Salas & Fuller 1996; Paint-er 1998; Herrera et al. 1999; Henry et al. 2000; Olivei-ra et al. 2005; Sallenave 2009; Talamoni & Assis 2009; Tobler et al. 2010; Hibert et al. 2011) (Table 3). The proportion of fruit parts in feces was also smaller than in other areas, but similar to reports in seasonal forests of Lago Caiman, Bolivia (Painter 1998; Herrera et al. 1999) (Fig. 4).

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Even though we did not evaluate seed dispersion, our observations suggest that due to the tapir’s alimentary plasticity (see Hibert et al. 2011), opportunistic behavior (see Tobler et al. 2010), mobility, and the fact that many seeds do germinate from their feces (M. S. de Bustos, pers. observ.), they exert a significant influence on the natural communities, as has been found in tropical for-ests (Painter & Rumiz 1999; Fragoso 2005).

Our results show that tapirs are adapted to extreme habitats, switching their diet from frugivory to herbiv-ory when fruits are scarce, such as observed in the im-poverished montane forest of El Rey and the dry Chaco forests. We believe that the reduction of their distribu-tion in Argentina is mostly due to habitat loss and hunt-ing, rather than a lack of food resources in secondary forests. Therefore, impoverished forest remnants and secondary growth fields must be valued and protected from further deforestation and hunting.

ACKNOWLEDGMENTSWe would like to thank the National Parks Admin-

istration for the research permits and El Rey Nation-al Park administration for providing lodging, transpor-tation, and other crucial logistic support. We thank the Wildlife Conservation Society and Wildlife Trust/Dur-rell M. Fund for their generous funding support. We also thank other donators that supported us during our field work as Idea Wild, Tapir Specialist Group, Tapir preservation Fund and Roger Williams Park Zoo. We are grateful to María Saravia, Mariana Saravia, Ceci-lia Acosta, Mariela Alveira, Aurel Heidelberg and many under graduate students for help with field and labora-tory work. We would like to thank Julio Tolaba (Sal-ta University) and Juan F. Garibaldi for their help with Ta

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Figure 4 Weight percentage of plant items found in feces in different habitats in South America (see details of the sites in Table 3).

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plant identification and systematics. We thank Natalia Politi and Luis Rivera for reviewing our manuscript and Loretta Baker for writing review.

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