American Journal of Primatology 76:1175–1184 (2014)
RESEARCH ARTICLE Seed Dispersal by Rhesus Macaques Macaca mulatta in Northern India ASMITA SENGUPTA*,a, KIM R. MCCONKEYb, AND SINDHU RADHAKRISHNAc School of Natural Sciences and Engineering, National Institute of Advanced Studies, Indian Institute of Science Campus, Bangalore 560 012, India
Frugivorous primates are important seed dispersers and their absence from forest patches is predicted to be detrimental to tropical forest regeneration and recruitment. With the reduction of primate populations globally, ecologically resilient primate species, characterized by dietary flexibility and the ability to thrive in a variety of habitats, assume new importance as seed dispersers. The most widely distributed non‐ human primate, the rhesus macaque Macaca mulatta has been intensively studied but little is known about its role in maintaining ecosystem structure and functions. Due to their frugivorous diet, large group sizes, large home ranges and tolerance to disturbance, rhesus macaques may be effective seed dispersers. We studied seed dispersal by rhesus macaques at the Buxa Tiger Reserve, India, through a combination of behavioural observations and germination experiments. Rhesus macaques dispersed 84% of the 49 species they fed on either through spitting or defecation. Nearly 96% of the handled seeds were undamaged and 61% of the species for which germination tests were performed had enhanced germination. Almost 50% of the monitored seeds among those deposited in situ germinated and 22% established seedlings, suggesting that rhesus macaques are important seed dispersers in tropical forests. Due to their widespread distribution and large populations, rhesus macaques are perceived as common and are categorized as Least Concern on the IUCN Red List, effectively excluding them from any conservation plans. Based on the results of our study, we argue that rhesus macaques fulfill critical ecological functions in their habitat and that this parameter must be taken into consideration when they are reviewed for conservation priorities. Am. J. Primatol. 76:1175–1184, 2014. © 2014 Wiley Periodicals, Inc. Key words:
rhesus macaque; frugivory; seed dispersal; India
INTRODUCTION As seed dispersers, frugivorous primates are ecologically critical species [Chapman & Russo, 2007; Garber & Lambert, 1998] and their absence from forest patches is predicted to lead to lowered rates of tropical forest regeneration and recruitment, thereby altering plant community structure [Anzures‐Dadda et al., 2011]. Land use changes involving forest transformations have led to the loss of large numbers of primate populations globally [Anzures‐Dadda et al., 2011]. In such a scenario, the importance of ecologically resilient primate species, characterized by dietary flexibility and ability to thrive in a variety of habitats, increases manifold [Albert et al., 2014]. It has, in fact, been suggested that in many parts of tropical and subtropical Asia, where forests are fragmented or native mammal fauna has gone extinct, disturbance‐tolerant macaques like the rhesus macaque Macaca mulatta, the bonnet macaque M. radiata and the long‐tailed macaque M. fascicularis may be the only seed dispersers, especially for the large fruit/seed bearing species [Lucas & Corlett, 1998]. Hence extirpation or even a decline in the number of these macaques would
© 2014 Wiley Periodicals, Inc.
negatively impact seed dispersal in such areas [Lucas & Corlett, 1998]. Rhesus macaques have the largest geographical distribution among non‐human primates with their range spanning Afghanistan, Bangladesh, Bhutan, India, Nepal, Pakistan, China, Burma, Laos, Thailand, and Vietnam [Brandon‐Jones et al., 2004; Correction added on August 27, 2014, after first online publication: Spelling of scientific names were corrected. Contract grant sponsor: Department of Science and Technology, Government of India; contract grant number: SB/SO/AS‐128/ 2012. a Research Scholar. b Adjunct Faculty. c
Associate Professor.
Correspondence to: Asmita Sengupta, School of Natural Sciences and Engineering, National Institute of Advanced Studies, Indian Institute of Science Campus, Bangalore 560 012, India. E‐mail: [email protected] Received 5 December 2013; revised 25 March 2014; revision accepted 19 April 2014 DOI: 10.1002/ajp.22302 Published online 16 May 2014 in Wiley Online Library (wileyonlinelibrary.com).
1176 / Sengupta et al.
Fooden, 2000]. Highly adaptable, often commensal and classified as “Least Concern” on the IUCN Red List [IUCN, 2014], M. mulatta has been intensively studied both in the field as well as laboratory [Richard et al., 1989]. Yet little is known about its role in maintaining ecosystem structure and functions. Although highly flexible in their feeding ecology, fruits may constitute as much as 70% [Fooden, 2000] of rhesus macaque diet. Being semi‐ terrestrial, they can also feed upon fruits of species at different strata of the forest [Albert et al., 2013]. Their large group sizes [mean: 40, Richter et al., 2013] mean that a large number of individuals can feed on a patch at the same time thereby dispersing considerable amounts of seeds at a time [sensu Albert et al., 2013]. Their large home [mean: 593.3 ha, Makwana, 1978] and daily ranges [mean: 1,803 m, Makwana, 1978] imply that individuals can carry seeds to large distances from the parent trees [Albert et al., 2013]. Finally, because of their ability to thrive in a range of habitats (including fragmented and disturbed habitats) these macaques are ecologically highly resilient [Albert et al., 2014]. These characteristics suggest that rhesus macaques can be highly effective seed dispersers in disturbed areas. However, available information on the effectiveness of rhesus macaques as seed dispersal agents is fragmentary [Dudgeon & Corlett, 1994; Lucas & Corlett, 1998] or limited to certain aspects like endozoochory [Tsuji et al., 2013]. Since its conception in 1993, Schupp’s SDE [initially Seed Disperser Effectiveness; modified to Seed Dispersal Effectiveness—Schupp et al., 2010] framework for assessing seed dispersal activities has been seminal in this field of research. Defined as the ‘number of new adults produced by the dispersal activities of a disperser’, SDE considers the quantitative aspect of seed dispersal (measured as the product of number of visits made to a tree and the number of seeds dispersed per visit) as well as the qualitative (measured as the product of the probability of seed survival in a viable condition post‐ handling and the probability of the survival and germination of the dispersed seed and the subsequent production of an adult tree) [Schupp, 1993; Schupp et al., 2010]. The most common variables examined with regard to assessment of SDE are seed handling behaviour, dispersal distance and handling effects on germination [Schupp et al., 2010]. In terms of seed handling mechanisms, primate species are categorised as “seed swallowers,” “seed spitters,” or “seed destroyers” [Corlett & Lucas, 1990]. While spat out seeds are usually deposited singly on the forest floor, swallowed (and defecated) seeds mostly have a clumped pattern of deposition [Chapman, 1995]. Suitable dispersal distance is a key component for effective dispersal; not only should seeds be deposited in an area suitable for germination, an effective disperser should also carry seeds away from the
Am. J. Primatol.
parent tree to escape mortality due to distance and density dependent predators, pathogens and herbivores targeting the adult [Connell, 1971; Howe & Smallwood, 1982; Janzen, 1970]. Handled seeds should also be in viable condition for a disperser to be called effective [Schupp et al., 2010]. Mechanical and/or chemical scarification of seed coat in the gut, separation of seeds from pulp and the presence of fecal matter surrounding the seeds can all have positive implications for the germination of swallowed and defecated seeds [Traveset & Verdú, 2002]. The aim of our study was to examine the role of rhesus macaques as seed dispersers taking into account the aforementioned aspects of SDE. More specifically, we addressed the following questions: (i) How many plant species are dispersed by rhesus macaques? (ii) How are the various seeds handled? (iii) How far from the parent tree are seeds deposited? (iv)What is the effect of seed handling on germination? and (v) What percentage of seeds deposited on the forest floor achieve establishment? METHODS Research Protocols The research was conducted after obtaining necessary permits from the West Bengal Forest Department. The research adhered to the American Society of Primatologists (ASP) Principles for the Ethical Treatment of Non‐Human Primates. Study Area We conducted our study at a protected forest area, the Buxa Tiger Reserve (BTR; 26°300 –23°500 N and 89°250 –89°550 E) in the northern part of West Bengal state, India (Fig. 1). BTR is located along the foothills of the Eastern Himalayan Region and covers an area of 761 km2 that includes a core area of 385 km2 [Sukumar et al., 2003]. The major portion of the reserve lies within the plains while the northern tracts are hilly with the elevation ranging from 60 to 1,750 m. Temperatures vary between 12 and 32°C and the average annual rainfall is 4,100 mm. While the main forest type is tropical moist deciduous, there are also patches of evergreen, semi‐evergreen and riverine forests alongside scrub, grasslands and plantations within BTR [Sivakumar et al., 2006]. Study Troop From July 2012 to June 2013, we followed and recorded observations on a troop of rhesus macaques near the Checko Timber Depot within the buffer zone of BTR. The area is in the immediate vicinity of Checko village and is affected by anthropogenic disturbances such as cattle grazing, tree felling, harvesting of firewood and poaching. The troop consisted of 41 individuals (9 adult males, 11 adult females, 9 juvenile males, 10 juvenile females, and 2
Seed Dispersal by Rhesus macaques / 1177
Fig. 1. Location of study area: a: Inset showing location of West Bengal within India. b: Inset showing location of Buxa Tiger Reserve within West Bengal. c: Map of Buxa Tiger Reserve.
infants) and was non‐provisioned and solely dependent on natural resources. The troop’s home range (mean: 45 ha; range: 25.5–70 ha, based on monthly means over the year; N ¼ 12 months) included a mosaic of natural forest and mixed‐species plantation and the dominant species were Terminalia chebula, Terminalia belerica, Terminalia crenulata, Terminalia myriocarpa, Tectona grandis, Shorea robusta, Lagerstroemia speciosa, Gmelina arborea, Syzygium cumini, and Michelia champaka. Seed Handling Mechanisms and Dispersal Distance We followed the macaques from their waking site to their sleeping tree for 10 days each month (12 hrs a day; 5 days each in the 2nd and 3rd weeks of each month) and recorded feeding activity using a 30‐min interval slow scan sampling method [Giraldo et al., 2007; Robinson, 1986]. In each sample, we scanned the troop for 15 min and noted the first item (plant species and part thereof—fruit, leaf, shoot, flower; insects; fungi) consumed by each individual. When macaques fed upon fruits, we employed 30 min‐ long focal sampling [Altmann, 1974] on any randomly chosen adult individual to make detailed observations on the part of the fruit consumed (whole fruit, pulp, seed) and the way seeds were handled. We checked fruits to determine the state of ripeness (ripe/unripe) and classified seed handling mechanisms as follows: swallowed (when the entire fruit was ingested, digested and the seeds egested intact), spat out (when the fruit was taken into the mouth,
mostly stored in cheek pouches, cleaned of the pulp and the seeds expectorated), dropped (when portions of fruits, e.g., epicarp, were fed upon and then discarded) and destroyed [when seeds were consistently crunched by macaques or if the fruits of those species were consumed in an unripe state—Albert et al., 2013; Kunz & Linsenmair, 2008]. We studied remnants of fruits/seeds beneath the feeding tree to confirm the exact part fed upon and recorded if the macaques spat out any seed during movement between trees. Often, a number of macaques fed upon fruits of the same tree and spat out the seeds. As it was difficult to distinguish seeds handled by different individuals in such conditions, we divided the number of spat out seeds found under a feeding tree immediately after a feeding event by the total number of macaques on the tree to obtain data on dispersal through seed‐spitting. We opportunistically collected fresh fecal material from focal individuals and examined it to check the number and status (intact/crunched) of seeds within. We measured spat out seeds and those found in fecal samples using callipers and assigned them to the following size categories according to their length: small (5 mm in length), medium (>5 mm but 100 m from the parent tree is defined as long‐distance dispersal [Cain et al., 2000]. However, shorter dispersal distances may also permit seeds to escape distance and density dependent effects under parent crowns. Appropriate dispersal distances are often species and habitat‐specific [Lambert & Chapman, 2005] and have been reported to vary between 2 and
RESEARCH ARTICLE Seed Dispersal by Rhesus Macaques Macaca mulatta in Northern India ASMITA SENGUPTA*,a, KIM R. MCCONKEYb, AND SINDHU RADHAKRISHNAc School of Natural Sciences and Engineering, National Institute of Advanced Studies, Indian Institute of Science Campus, Bangalore 560 012, India
Frugivorous primates are important seed dispersers and their absence from forest patches is predicted to be detrimental to tropical forest regeneration and recruitment. With the reduction of primate populations globally, ecologically resilient primate species, characterized by dietary flexibility and the ability to thrive in a variety of habitats, assume new importance as seed dispersers. The most widely distributed non‐ human primate, the rhesus macaque Macaca mulatta has been intensively studied but little is known about its role in maintaining ecosystem structure and functions. Due to their frugivorous diet, large group sizes, large home ranges and tolerance to disturbance, rhesus macaques may be effective seed dispersers. We studied seed dispersal by rhesus macaques at the Buxa Tiger Reserve, India, through a combination of behavioural observations and germination experiments. Rhesus macaques dispersed 84% of the 49 species they fed on either through spitting or defecation. Nearly 96% of the handled seeds were undamaged and 61% of the species for which germination tests were performed had enhanced germination. Almost 50% of the monitored seeds among those deposited in situ germinated and 22% established seedlings, suggesting that rhesus macaques are important seed dispersers in tropical forests. Due to their widespread distribution and large populations, rhesus macaques are perceived as common and are categorized as Least Concern on the IUCN Red List, effectively excluding them from any conservation plans. Based on the results of our study, we argue that rhesus macaques fulfill critical ecological functions in their habitat and that this parameter must be taken into consideration when they are reviewed for conservation priorities. Am. J. Primatol. 76:1175–1184, 2014. © 2014 Wiley Periodicals, Inc. Key words:
rhesus macaque; frugivory; seed dispersal; India
INTRODUCTION As seed dispersers, frugivorous primates are ecologically critical species [Chapman & Russo, 2007; Garber & Lambert, 1998] and their absence from forest patches is predicted to lead to lowered rates of tropical forest regeneration and recruitment, thereby altering plant community structure [Anzures‐Dadda et al., 2011]. Land use changes involving forest transformations have led to the loss of large numbers of primate populations globally [Anzures‐Dadda et al., 2011]. In such a scenario, the importance of ecologically resilient primate species, characterized by dietary flexibility and ability to thrive in a variety of habitats, increases manifold [Albert et al., 2014]. It has, in fact, been suggested that in many parts of tropical and subtropical Asia, where forests are fragmented or native mammal fauna has gone extinct, disturbance‐tolerant macaques like the rhesus macaque Macaca mulatta, the bonnet macaque M. radiata and the long‐tailed macaque M. fascicularis may be the only seed dispersers, especially for the large fruit/seed bearing species [Lucas & Corlett, 1998]. Hence extirpation or even a decline in the number of these macaques would
© 2014 Wiley Periodicals, Inc.
negatively impact seed dispersal in such areas [Lucas & Corlett, 1998]. Rhesus macaques have the largest geographical distribution among non‐human primates with their range spanning Afghanistan, Bangladesh, Bhutan, India, Nepal, Pakistan, China, Burma, Laos, Thailand, and Vietnam [Brandon‐Jones et al., 2004; Correction added on August 27, 2014, after first online publication: Spelling of scientific names were corrected. Contract grant sponsor: Department of Science and Technology, Government of India; contract grant number: SB/SO/AS‐128/ 2012. a Research Scholar. b Adjunct Faculty. c
Associate Professor.
Correspondence to: Asmita Sengupta, School of Natural Sciences and Engineering, National Institute of Advanced Studies, Indian Institute of Science Campus, Bangalore 560 012, India. E‐mail: [email protected] Received 5 December 2013; revised 25 March 2014; revision accepted 19 April 2014 DOI: 10.1002/ajp.22302 Published online 16 May 2014 in Wiley Online Library (wileyonlinelibrary.com).
1176 / Sengupta et al.
Fooden, 2000]. Highly adaptable, often commensal and classified as “Least Concern” on the IUCN Red List [IUCN, 2014], M. mulatta has been intensively studied both in the field as well as laboratory [Richard et al., 1989]. Yet little is known about its role in maintaining ecosystem structure and functions. Although highly flexible in their feeding ecology, fruits may constitute as much as 70% [Fooden, 2000] of rhesus macaque diet. Being semi‐ terrestrial, they can also feed upon fruits of species at different strata of the forest [Albert et al., 2013]. Their large group sizes [mean: 40, Richter et al., 2013] mean that a large number of individuals can feed on a patch at the same time thereby dispersing considerable amounts of seeds at a time [sensu Albert et al., 2013]. Their large home [mean: 593.3 ha, Makwana, 1978] and daily ranges [mean: 1,803 m, Makwana, 1978] imply that individuals can carry seeds to large distances from the parent trees [Albert et al., 2013]. Finally, because of their ability to thrive in a range of habitats (including fragmented and disturbed habitats) these macaques are ecologically highly resilient [Albert et al., 2014]. These characteristics suggest that rhesus macaques can be highly effective seed dispersers in disturbed areas. However, available information on the effectiveness of rhesus macaques as seed dispersal agents is fragmentary [Dudgeon & Corlett, 1994; Lucas & Corlett, 1998] or limited to certain aspects like endozoochory [Tsuji et al., 2013]. Since its conception in 1993, Schupp’s SDE [initially Seed Disperser Effectiveness; modified to Seed Dispersal Effectiveness—Schupp et al., 2010] framework for assessing seed dispersal activities has been seminal in this field of research. Defined as the ‘number of new adults produced by the dispersal activities of a disperser’, SDE considers the quantitative aspect of seed dispersal (measured as the product of number of visits made to a tree and the number of seeds dispersed per visit) as well as the qualitative (measured as the product of the probability of seed survival in a viable condition post‐ handling and the probability of the survival and germination of the dispersed seed and the subsequent production of an adult tree) [Schupp, 1993; Schupp et al., 2010]. The most common variables examined with regard to assessment of SDE are seed handling behaviour, dispersal distance and handling effects on germination [Schupp et al., 2010]. In terms of seed handling mechanisms, primate species are categorised as “seed swallowers,” “seed spitters,” or “seed destroyers” [Corlett & Lucas, 1990]. While spat out seeds are usually deposited singly on the forest floor, swallowed (and defecated) seeds mostly have a clumped pattern of deposition [Chapman, 1995]. Suitable dispersal distance is a key component for effective dispersal; not only should seeds be deposited in an area suitable for germination, an effective disperser should also carry seeds away from the
Am. J. Primatol.
parent tree to escape mortality due to distance and density dependent predators, pathogens and herbivores targeting the adult [Connell, 1971; Howe & Smallwood, 1982; Janzen, 1970]. Handled seeds should also be in viable condition for a disperser to be called effective [Schupp et al., 2010]. Mechanical and/or chemical scarification of seed coat in the gut, separation of seeds from pulp and the presence of fecal matter surrounding the seeds can all have positive implications for the germination of swallowed and defecated seeds [Traveset & Verdú, 2002]. The aim of our study was to examine the role of rhesus macaques as seed dispersers taking into account the aforementioned aspects of SDE. More specifically, we addressed the following questions: (i) How many plant species are dispersed by rhesus macaques? (ii) How are the various seeds handled? (iii) How far from the parent tree are seeds deposited? (iv)What is the effect of seed handling on germination? and (v) What percentage of seeds deposited on the forest floor achieve establishment? METHODS Research Protocols The research was conducted after obtaining necessary permits from the West Bengal Forest Department. The research adhered to the American Society of Primatologists (ASP) Principles for the Ethical Treatment of Non‐Human Primates. Study Area We conducted our study at a protected forest area, the Buxa Tiger Reserve (BTR; 26°300 –23°500 N and 89°250 –89°550 E) in the northern part of West Bengal state, India (Fig. 1). BTR is located along the foothills of the Eastern Himalayan Region and covers an area of 761 km2 that includes a core area of 385 km2 [Sukumar et al., 2003]. The major portion of the reserve lies within the plains while the northern tracts are hilly with the elevation ranging from 60 to 1,750 m. Temperatures vary between 12 and 32°C and the average annual rainfall is 4,100 mm. While the main forest type is tropical moist deciduous, there are also patches of evergreen, semi‐evergreen and riverine forests alongside scrub, grasslands and plantations within BTR [Sivakumar et al., 2006]. Study Troop From July 2012 to June 2013, we followed and recorded observations on a troop of rhesus macaques near the Checko Timber Depot within the buffer zone of BTR. The area is in the immediate vicinity of Checko village and is affected by anthropogenic disturbances such as cattle grazing, tree felling, harvesting of firewood and poaching. The troop consisted of 41 individuals (9 adult males, 11 adult females, 9 juvenile males, 10 juvenile females, and 2
Seed Dispersal by Rhesus macaques / 1177
Fig. 1. Location of study area: a: Inset showing location of West Bengal within India. b: Inset showing location of Buxa Tiger Reserve within West Bengal. c: Map of Buxa Tiger Reserve.
infants) and was non‐provisioned and solely dependent on natural resources. The troop’s home range (mean: 45 ha; range: 25.5–70 ha, based on monthly means over the year; N ¼ 12 months) included a mosaic of natural forest and mixed‐species plantation and the dominant species were Terminalia chebula, Terminalia belerica, Terminalia crenulata, Terminalia myriocarpa, Tectona grandis, Shorea robusta, Lagerstroemia speciosa, Gmelina arborea, Syzygium cumini, and Michelia champaka. Seed Handling Mechanisms and Dispersal Distance We followed the macaques from their waking site to their sleeping tree for 10 days each month (12 hrs a day; 5 days each in the 2nd and 3rd weeks of each month) and recorded feeding activity using a 30‐min interval slow scan sampling method [Giraldo et al., 2007; Robinson, 1986]. In each sample, we scanned the troop for 15 min and noted the first item (plant species and part thereof—fruit, leaf, shoot, flower; insects; fungi) consumed by each individual. When macaques fed upon fruits, we employed 30 min‐ long focal sampling [Altmann, 1974] on any randomly chosen adult individual to make detailed observations on the part of the fruit consumed (whole fruit, pulp, seed) and the way seeds were handled. We checked fruits to determine the state of ripeness (ripe/unripe) and classified seed handling mechanisms as follows: swallowed (when the entire fruit was ingested, digested and the seeds egested intact), spat out (when the fruit was taken into the mouth,
mostly stored in cheek pouches, cleaned of the pulp and the seeds expectorated), dropped (when portions of fruits, e.g., epicarp, were fed upon and then discarded) and destroyed [when seeds were consistently crunched by macaques or if the fruits of those species were consumed in an unripe state—Albert et al., 2013; Kunz & Linsenmair, 2008]. We studied remnants of fruits/seeds beneath the feeding tree to confirm the exact part fed upon and recorded if the macaques spat out any seed during movement between trees. Often, a number of macaques fed upon fruits of the same tree and spat out the seeds. As it was difficult to distinguish seeds handled by different individuals in such conditions, we divided the number of spat out seeds found under a feeding tree immediately after a feeding event by the total number of macaques on the tree to obtain data on dispersal through seed‐spitting. We opportunistically collected fresh fecal material from focal individuals and examined it to check the number and status (intact/crunched) of seeds within. We measured spat out seeds and those found in fecal samples using callipers and assigned them to the following size categories according to their length: small (5 mm in length), medium (>5 mm but 100 m from the parent tree is defined as long‐distance dispersal [Cain et al., 2000]. However, shorter dispersal distances may also permit seeds to escape distance and density dependent effects under parent crowns. Appropriate dispersal distances are often species and habitat‐specific [Lambert & Chapman, 2005] and have been reported to vary between 2 and
