40 Asian Primates Journal 5(1), 2015 A PRELIMINARY STUDY OF FRUIT HANDLING BY CAPTIVE BORNEAN ORANGUTANS Pongo pygmaeus pygmaeus AND THE EFFECTS ON SEED GERMINATION
Jayasilan Mohd-Azlan1*, Tracy Pail2, and Sundai Silang3
1,2 Department of Zoology, Faculty of Resource Science and Technology, Universiti Malaysia Sarawak, 94300 Kota Samarahan, Sarawak, Malaysia. 1 E-mail: [email protected]; 2 E-mail: [email protected] 3 Biodiversity and Conservation Department, Protected Areas and Biodiversity Conservation Unit, Sarawak Forestry Corporation, Sarawak, Malaysia. 2 E-mail: [email protected] * Corresponding author
ABSTRACT A preliminary study to investigate the efficacy of Northwest Bornean Orangutans Pongo( pygmaeus pygmaeus) as seed dispersers and predators was conducted in Matang Wildlife Centre, Kuching, Sarawak from November 2012 to April 2013. This wildlife facility is one of the official holding centres for orangutans in Malaysian Borneo. Three adult and three juvenile captive orangutans were fed with nine species of locally-available fruits. Approximately 1.5 kg of fruit was given once daily during the study period. Seeds from sieved faecal matter were collected and tested for germination. Three species of small-seeded plants germinated while two medium- seeded plants did not. The seeds from the other four species were damaged and not tested for germination. Fruit and seed-handling behaviour was also observed. A broad range of fruit-processing behaviour such as swallowing, spitting and masticating allows the orangutans to be both seed disperser and predator towards some large-seeded and small-seeded fruits. The morphological characteristics of seeds and age of orangutans appear to influence the fate of seed dispersal.
Keywords: behaviour, fruit-processing, germination, seed dispersal, seed morphology, tropical ecology
INTRODUCTION Orangutans, with a wide distribution across Borneo trees and they may play an important role in dispersal and Sumatra, are naturally limited to tropical rainforest of seasonal tropical fruits in the wild (Galdikas, 1982). although they have been reported in orchards, cultivated Seed dispersal and seed dissemination, which fields and gardens (Galdikas, 1988; Nadler et al., contributes to the spatial dynamics of plant 1990). The Bornean species has been classified under populations, is important in forest ecology (Cousens three subspecies, namely P. p. pygmaeus (Linnaeus), et al., 2008). The association of frugivory and seed the Northwest Bornean Orangutan, P. p. wurmbii dispersal has been consistently linked and theoretically (Tiedemann), the Southwest Bornean Orangutan, and framed on the idea of coevolution (Ehrlich & Raven, P. p. morio (Owen), the Northeast Bornean Orangutan 1964; Futuyma & Slatkin, 1983; Herrera, 2002). Being (Roos et al., 2014). Orangutans have been reported the largest primate in Asia, orangutans need large to utilize more than 500 species of plants (Ancrenaz quantities of food for nutrition and energy for their daily et al., 2008). The diet breadth of an orangutan is wide activities (Harrison, 1962). Adult orangutans may travel and they can consume more than 300 types of fruit from 300 m to 800 m per day, with a home range of available in forests (Harrison, 1962; Galdikas, 1982). over 6 km2 (Harrison, 1962; Bennett, 1998). Primates They are also known to forage on cultivated fruits such are important seed dispersers because of their varied as durians, figs, rambutans and mangoes (Payne & diet and their ability to travel far which leads to high Andau, 1989; Bennett, 1998; Kaplan & Rogers, 2000). dispersal distances (Galdikas, 1988; Wehncke et Most of their preferred fruits are from large-seeded 41 Asian Primates Journal 5(1), 2015 al., 2003; Corlett, 2009; Nielsen et al., 2011). These germination (emergence of radicle). functions are crucial in many of the degrading Bornean rainforests. RESULTS The most common modes of seed handling are The orangutans consumed all the given fruits, with seed spitting and swallowing (Lambert, 2002). The size no leftovers. Orangutans spent less than 30 minutes of the seed influences seed handling. Seed-spitting feeding on approximately 1.5 kg of fruits. They were may lead to seed dispersal within a short distance. In fed fruits with an estimated total of approximately contrast crushing of seeds during foraging may result 3,996 seeds, and only 696 (17.4%) intact seeds were in seed predation. Additionally, seed passage through retrieved from the faeces. The remaining seeds were mammalian guts may facilitate the germination of either spat out (N=984; 24.6%) or found damaged dormant seeds (Willson, 1993; Ramos et al., 2006). in the faeces. There was no significant difference in However, the germination of seeds from different plant proportion intact between the spat-out seeds and species will respond differently after ingestion, even by those found in the faeces (paired t-test, df=8, t=0.67 the same animal species (Traveset, 1998). This project P=0.52). The spat and dropped seeds appeared viable was initiated to investigate the efficacy of orangutans and mostly intact. Smaller seeds (<5mm, i.e. Carica as seed dispersers and the germination rates of papaya L. and C. lanatus) were likely to be chewed and selected seasonal and domestically available fruits. digested; thus not many seeds were retrieved from the faeces. Intact seeds from Artocarpus integer (Thunb.) Merr., Dialium indum L., Dimocarpus longan Lour. and MATERIALS AND METHODS Nephelium lappaceum L. were not found in the faeces Study area as most of them were spat out. The highest proportion The study was conducted at Matang Wildlife Centre, of intact seeds retrieved from the faeces were from Kuching, Sarawak in Borneo for six months from Baccaureum macrocarpa (Miq.) Muell.Arg (82.8%), November 2012 to April 2013. Matang Wildlife Centre A. integer (82.2%), N. lappaceum (70%) and Annona is an enclosed area of rainforest with captive animal muricata L. (56.1%). In contrast a high proportion of facilities established to conserve endangered species seeds was damaged for Dialium indum, Dimocarpus of wildlife in Sarawak. longan, Carica papaya and Citrullus lanatus for each of which only a minority (10.8%, 17.4%, 36.3% and Six individuals of semi-wild orangutans from two 37.2% respectively) of intact seeds were retrieved age categories were selected for this experiment. They (Table 1). included three adults, which consisted of two males and a female (13 to 29 years old), and three juvenile There was no significant difference in the number of males (3-4 years old). The orangutans were fed with seeds retrieved from the faeces between the adult and seasonally and commercially cultivated local fruits juvenile orangutans (paired t-test, df=8, t=1.6, P=0.15). in three seed-size classes (<5mm, small; 5-15mm, However the adult and juvenile animals behaved medium; >15mm, large) (Table 1). Two to seven types differently in fruit processing and handling where there of fruit were given per feeding session, depending on was a significant difference (paired t-test, df=8, t=3.8, availability. Samples of the fruits were weighed, sliced P=0.00) in the proportion of remnant seeds that were and their seeds counted or estimated. The number of spat out, suggesting that juvenile orangutans caused seeds in small-seeded species (e.g. Citrullus lanatus more damage to seeds than adults. (Thunb.) Matsum. & Nakai) was estimated and the The time of germination was measured in days. average number of seeds recorded from a sample Except for the seeds of Annona muricata and Lansium of eight of each fruit, of a representative range of fruit parasiticum (Osbeck) K.C. Sahni & Bennet most of sizes. the intact seeds retrieved from the orangutan faecal All seeds were retrieved from the faeces of the samples were successfully germinated (95%, N=618). orangutans for the germination experiment (Table 1). Egested seeds of Citrullus lanatus (watermelon) Control seeds were taken from the same batch of fruits and Carica papaya (papaya) germinated faster than for each species. The retrieved and control seeds were controls while B. macrocarpa (Tampoi) showed a identified and numbered and set in germination beds similar germination period. This evidence suggests using untreated sandy soil from the forest. All planting that passage through an orangutan’s gut improves the was conducted in controlled conditions in the UNIMAS probability of germination and shortens the time taken Nursery. Seeds were kept moist and checked daily for to germinate for Citrullus lanatus and Carica papaya. 42 Asian Primates Journal 5(1), 2015 0 0 NA NA NA NA 3 to 6 5 to 10 4 to 10 Faeces days 0 0 NA NA NA NA Germination time/ 5 to 10 5 to 10 5 to 10 Control - 6 1 9 4 6 9 83 14 15 147 niles Intact seeds by juve spat out 3 79 38 55 63 54 240 177 128 837 Intact seeds spat out by adults 4 0 0 0 7 0 66 98 30 205 from from Intact seeds juvenile retrieved retrieved faeces of 8 0 0 0 0 90 27 176 190 491 from from Intact seeds adults retrieved retrieved faeces of 0 0 0 0 (0) (0) (0) (0) (5) 5.6 (60) (41) (87) 603 34.7 10.4 17.2 78.5 (410) Missing seeds % - 0 0 (0) (0) 9.2 7.4 (16) (29) (22) 63.7 62.8 89.2 82.6 24.4 (570) (383) (365) (328) aged 1713 Dam seeds % from faeces from 70 (44) (69) (63) 56.1 82.2 82.8 36.3 37.2 10.8 17.4 21.5 (323) (420) (325) (227) (112) 1680 (97)** Intact seeds % 90 173 393 507 895 610 409 397 522 3996 given Total intact, damaged and missing seeds Total Seeds Size Medium Large Small Small Small Medium Medium Medium Large name Common Soursop Jackfruit Tampoi Papaya Watermelon Keranji Longan Langsat Rambutan * * * * * * * * Total seeds retrieved from faeces and spat out by adult and juvenile orangutans. The germination test was only conducted for control seeds and faeces and spat out by adult juvenile orangutans. The germination test was only conducted for control from seeds retrieved Total Scientific name Annona muricata Artocarpus integer Baccaurea macrocarpa Carica papaya Citrullus lanatus Dialium indum Dimocarpus longan Lansium parasiticum Nephelium lappaceum TOTAL in brackets indicate the sample size; NA=not available for germination test. counted and estimated; **figures *Seeds were Table 1. Table faeces. from retrieved 43 Asian Primates Journal 5(1), 2015
DISCUSSION In general, the germination trial demonstrated that The finding of this experiment is consistent with that most egested seeds were viable and reduced the of Galdikas (1982) that orangutans are seed dispersal period of time for germination. Seeds of cultivated agents for most fruits and could act as seed predators species such as Annona muricata and Lansium for some other plant species. In general the balance parasiticum may have features (toughness, possible between egestion (with seeds potentially dispersed content of poisons) affected by the domestication further away from the tree) and spitting out (i.e. seeds process such that they may not tolerate gut enzymes. dropping below and near the tree) is expected to be Seeds of many Annona spp. rapidly lose viability after similar in the wild, with more seeds spat out than removal from the fruit and scarification of seeds may retrieved from the faeces. In the wild, 46% of the seeds also prevent germination or delay germination (George recovered were from the faeces while the remainder & Nissen, 1987). It is therefore not clear to what were spat out (Galdikas, 1982). In the present study extent these results are representative of natural forest on captive orangutans fewer intact seeds (41%) conditions. were recovered from the faeces compared with the Further study to explore the behaviour and ability proportion spat out. The sizes of seed appear to be of orangutans to manipulate seeds from various size important in determining the fruit-processing behaviour classes and morphological characteristics will provide and dispersal distance. This study further supports the additional information to predict the seed dispersal postulation of Nielsen et al. (2011) that orangutans are distance and viability in the wild. effective seed dispersers for both large- and small- seeded fruits. In general larger-seeded fruits (i.e. A. integer and N. lappaceum) were not ingested but spat ACKNOWLEDGEMENTS out after consuming the pulp, while less fleshy fruits We are grateful to the Department of Zoology, and tasteless seeds tended to be masticated by the Faculty of Resource Science and Technology, Universiti orangutans and thereby destroyed. Spat-out seeds will Malaysia Sarawak, Sarawak Forestry Corporation have a shorter dispersal distance. and Sarawak Forest Department for supporting The viability of the seeds that are spat out in the our research in Sarawak (NCCD.907.4.4.[Jld.8]-78: wild may be dependent on the microhabitat in which 363/2012). Mohd-Azlan Jayasilan was supported by they land. In addition to this, seeds spat out that land research grant, NRGS-1087/2013(01). We are grateful directly under a tree, although perfectly intact, may to Beau Austin for his help on the manuscript. We not have much of a chance of survival as they have are also thankful to Mr Siali Laban and Mr Chong of a high probability of being eaten by seed predators or Sarawak Forestry Corporation from Matang Wildlife attacked by fungi or parasites (Wrangham et al., 1994). Centre for their assistance during the fieldwork. We would like to thank four anonymous reviewers for Even though the sizes of the seeds were enough to providing valuable comments on the previous version be swallowed by the animal, seed predatory behaviour of the manuscript. was observed on the seeds of Dialium indum and Dimocarpus longan (longan). This finding is consistent with that of Lambert (2002). It has been suggested REFERENCES that orangutans may be able to disperse smaller seeds Ancrenaz, M., Marshall, A., Goossens, B., van further (compared with larger, spat-out seeds) because Schaik, C., Sugardjito, J., Gumal, M. and Wich, S. of their long retention in the gut and because they are 2008. Pongo pygmaeus. In: The IUCN Red List not affected by the intestinal digestion system (Caton of Threatened Species. Version 2014.3.
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