Primates (2014) 55:161–165 DOI 10.1007/s10329-013-0403-1
NEWS AND PERSPECTIVES
Problems associated with the seed-trap method when measuring seed dispersal in forests inhabited by Japanese macaques Riyou Tsujino • Takakazu Yumoto
Received: 25 September 2013 / Accepted: 17 December 2013 / Published online: 31 December 2013 Ó Japan Monkey Centre and Springer Japan 2013
Abstract Despite the widespread use of seed/litter traps in seed dispersal ecology, several problems have arisen when using this method in forests inhabited by semi-terrestrial monkeys. The first issue is the height of the trap relative to the location where macaques spit seeds and/or defecate. For Japanese macaques in the lowland forests of Yakushima Island, southern Japan, 30–50 % of the seeds emitted from cheek pouches and faeces will not be caught by seed traps, leading to underestimation of seed fall. The second issue is the attractiveness of seed traps. Macaques sometimes play with the traps, potentially affecting the results of the seed-trap method in complex ways, including both negative and positive effects. To obtain reasonable estimates of total seed dispersal, we recommend that researchers conduct the seed-trap method concurrently with monkey observations, and that they should affix traps more securely to prevent macaques from destroying the traps.
R. Tsujino Center for Ecological Research, Kyoto University, Otsu, Shiga 520-2113, Japan Present Address: R. Tsujino (&) Center for Natural Environment Education, Nara University of Education, Takabatake-cho, Nara 630-8528, Japan e-mail: [email protected] T. Yumoto Research Institute for Humanity and Nature, 457-4, Motoyama, Kamigamo, Kita-ku, Kyoto 603-8047, Japan Present Address: T. Yumoto Primate Research Institute Kyoto University, Kanrin, Inuyama, Aichi 484-8506, Japan
Keywords Cheek pouch Faeces Height Physical attack Seed fall
Introduction Seed-trap methods are used to estimate the seed rain and the total amount and spatial distribution pattern of seed/ fruit fall in forests (e.g. Masaki et al. 1994; Clark et al. 1998; Moles and Drake 1999; Nathan and Muller-Landau 2000; Lichstein et al. 2004; Lee et al. 2004; Hanya 2005; Tsujino and Yumoto 2007). Despite the wide use of traps in seed dispersal ecology and the spatial structure analysis of plant populations, there are several potential biases inherent to the trap design, such as bouncing, wind effects, area effects, and seed removal by predators (Stevenson and Ivonne 2008). Stevenson and Ivonne (2008) also suggested that particular behaviours of predators and mechanical damage by megafauna should be taken into account. In addition, the seed-trap method is not a general method for evaluating seed dispersal by terrestrial and/or semi-terrestrial mammals (e.g. Russo et al. 2006; Sato 2013). In the study reported in the present paper, we defined terrestrial mammals as mammals which generally forage on the ground and rarely climb trees, semi-terrestrial mammals as mammals which forage on the ground as well as in the trees, and arboreal mammals as mammals which generally forage in the trees and rarely on the ground. To investigate terrestrial and/or semi-terrestrial mammal seed dispersal, a specific research framework is necessary, such as faecal analysis (Hanya 2005), focal animal sampling (Tsujino and Yumoto 2009), the direct collection of seeds of large-seeded species on the ground (Hoshizaki et al. 1999), or the placing and tracking of marked seeds to evaluate removal by dispersal agents (Iida 2006).
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The circumstances of semi-terrestrial mammal are not the same as those of birds, arboreal mammals or terrestrial mammals. While attempting to estimate the amount of seed fall in forests inhabited by high densities of semi-terrestrial monkeys, we noted several problems with the reliability of the seed-trap method in relation to the behaviour of monkeys. For example, Japanese macaques typically place fruits into their cheek pouches in the canopies of fruiting trees and then usually return to the ground and spit out the seeds if necessary. However, seed traps are often set 0.8–1.5 m above the ground (e.g. Masaki et al. 1994; Harms et al. 2000; Hanya 2005; Tsujino and Yumoto 2007) to avoid seed removal or physical disturbance by animals. Therefore, if the macaques spit or defecate seeds when they are on the ground, seed dispersal will be underestimated by the seed-trap method, even though primates play significant roles in seed dispersal (Terborgh 1986). Thus, our objective was to determine the degree of underestimation of seed-fall catch by traps that measure seed dispersal by Japanese macaques via cheek pouches and faeces in a warm-temperate forest on Yakushima Island, Japan. In addition, we report observations of macaques playing with the seed traps. We then discuss the difficulties of measuring total seed fall in a forest inhabited by high densities of semi-terrestrial monkeys, and the potential disruptive behaviours of monkeys that affect the estimation of total seed dispersal using the seed-trap method.
Methods Study area Yakushima Island (30°200 N, 131°300 E) is located approximately 70 km south of Kyushu, Japan. The study area was located in a warm-temperate forest at an altitude of 80–350 m along the western slope of Mt. Kuniwari-dake (1323 m a.s.l.). The mean annual temperature and rainfall were approximately 21 °C and 2600 mm, respectively (Tagawa 1980). The forest consists primarily of broadleaved evergreen Fagaceae, Hamamelidaceae, Myrsinaceae, and Lauraceae (Tsujino et al. 2006). Behavioural observations Macaca fuscata yakui, a subspecies of Japanese macaque, plays an important role in dispersing seeds of fleshy-fruited plants in the warm-temperate forests of Yakushima Island (Yumoto et al. 1998; Otani and Shibata 2000; Otani 2004; Tsujino and Yumoto 2009). Body lengths of Japanese macaques are 50–60 cm, and adult male and female body weights are 12–15 and 8–13 kg, respectively. In fact,
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Terakawa et al. (2008) reported that the mean number of Myrica rubra fruits consumed by macaques was 35.6-fold more than that consumed by brown-eared bulbuls Hypsipetes amaurotis on Yakushima Island, where macaques and brown-eared bulbuls are primarily consumers of Myrica rubra fruits. Macaca fuscata yakui individuals tend to hold fruits in their cheek pouches and spit out large seeds, whereas small seeds tend to be swallowed and defecated (Otani and Shibata 2000). Seed dispersal by Japanese macaques was studied in one troop of habituated macaques (B troop) composed of 10 members at the onset of the study (four adult females, two adult males, three juvenile males, one juvenile female). One adult female disappeared and four adult males immigrated during the study period. We collected behavioural feeding, height in the tree, seed spitting, and defecation data for four adult females and four adult males using a 2-min-interval point-sampling method. We conducted focal sampling for up to 1 h (unless seed deposition was occurring), during which time we recorded the activity of the feeding and seed-depositing focal macaque as well as the food items and location (on a map) at 2-min intervals. If a focal animal was depositing seeds from its cheek pouches when we should have switched to a new focal animal, we continued the observation until seed deposition was completed. We estimated the heights at which focal macaques were located to the nearest metre at 2-min intervals, as well as the heights from which seeds and faeces were dropped. We conducted field observations in the summer (June 2003), autumn (November and December 2003), and winter (March 2004) after a 1-month preliminary survey in May 2003. The total observation time was 240.2 h: 143.5 h for females and 97.7 h for males. We pooled data for females and males in the following analyses, because differences between the sexes were beyond the scope of this study.
Results and discussion In total, we observed 60 faecal depositions during 240.2 h of macaque observation time. Macaques spent 60.5 % of the daytime on the ground or at\2 m in height and 39.5 % of the daytime above 2 m in height, primarily in trees (Fig. 1). Among the 60 cases of faecal deposition, the macaques defecated 19 times (31.7 %) from heights \2 m and 41 times (68.3 %) from heights above 2 m (Fig. 1). We observed 2402 seeds being dispersed from cheek pouches, including 118 seeds of Myrica rubra, 319 of Persea thunbergii, 444 of Neolitsea sericea, 1306 of Litsea acuminata, and 215 of unidentified species. Macaques spat 1186 seeds (49.5 %) from heights \2 m and 1216 seeds (50.5 %) from heights above 2 m (Fig. 2). Therefore, the
Primates (2014) 55:161–165
Fig. 1 Percentages of macaque locations during scans (i.e. macaque foraging heights), faecal defecations, and seed dispersal via cheek pouches at the ground to below 2 m in height, 2–5 m, 5–10 m, and above 10 m
height issue associated with the location of seed traps would lead to underestimation of the extent of seed dispersal. The defecation height ratio (number of defecations at \2 m above the ground/total defecations; 31.7 %) and the seed spitting height ratio (number of seed spits at \2 m above the ground/total number of spits; 49.5 %) were both significantly different from the foraging height ratio (number of macaques foraging at locations\2 m above the ground/total number of scans; 60.5 %) (binomial test, p \ 0.0001). Although using a height of 2 m as a threshold caused overestimation of the defecation height ratio of the seed traps, the degree of overestimation was negligible for the defecation (2.1 %), seed spitting (1.9 %) and foraging
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(1.4 %) at 0–2 m in height. These results indicate that macaques dropped more seeds and faeces from more than 2 m above the ground than expected based on their foraging patterns. In general, 30–50 % of the seeds deposited via cheek pouches and faeces will not be caught by the seed traps. Therefore, an inappropriate seed trap height would lead to an underestimation of seed dispersal. In addition, we suggest that this effect will differ in magnitude among plant species. Seed-fall estimations for some plant species whose fruits/seeds are consumed/dispersed by macaques should be corrected for this height effect. In contrast, plant species whose fruits are not consumed by macaques need not be corrected. Placing seed traps on the ground is one of the ways that can be used to avoid the underestimation of seed dispersal if there are few large terrestrial and semiterrestrial mammals that trample on the traps or feed on fallen seeds and fruits in the traps in the study site (i.e. Au et al. 2006). Another solution is to directly count seeds of large-seeded plant species on the ground soon after the seeds are dispersed (i.e. Hoshizaki et al. 1999). However, these methodological solutions may only be applicable to limited study sites and plant species. The second problem associated with the seed-trap method is the attractiveness of traps to macaques, who sometimes play with them. On 4 October 2001, from approximately 10:42 to 11:04 in the study area, Tsujino observed young and adult Japanese macaques playing with seed traps that had been set for another purpose (Tsujino and Yumoto 2007). At least three macaques sat on and
Fig. 2 Photographs depicting macaques playing with seed traps in the study forest (photo by Tsujino, 4 October 2001). Seed traps were affixed with three poles and ropes
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rested on the edges of the seed traps, sometimes climbing into the traps to eat acorns of Pasania edulis (Fig. 2). Artificial constructions in the forest, such as seed traps, are conspicuous and may be particularly attractive to macaques. This attractiveness issue has several potential effects on the seed-trap method. First, because they may remain on or around seed traps for a longer period of time, macaques may defecate more faeces and spit more seeds into the seed traps than if they were not attracted by the traps. Second, as occurred during our case observations, macaques will consume fruits that had already collected in the seed traps, as seeds and fruits in the traps are attractive to macaques. When the macaques enter a trap, they do not need to search for fallen fruits, which are often contaminated and/or encumbered by the soil, tree roots, or decaying litter. This effect will lead to underestimations of fruit fall for species that are consumed by macaques. However, seed-fall estimations of species dispersed by macaques via cheek pouches will be overestimated, because macaques might feed on fruits and spit the seeds directly into the trap. If macaques leave the trap before spitting seeds into it, seed fall will be underestimated. Therefore, the attractiveness effect could lead to either the under- or overestimation of seed fall, depending on the circumstances. Third, physical attack by macaques, as shown in Fig. 2, will cause the destruction of traps. This effect will hinder the measurement efforts of the researchers. Moreover, trap destruction affects every type of seed as well as litter collection. Researchers must be aware of these physical disturbances and affix traps more securely. In conclusion, we highlighted the difficulties associated with the accurate measurement of seed dispersal using only the seed-trap method in forests inhabited by a high density of monkeys. Because several factors related to monkey behaviour affect the accuracy of these estimations, researchers may need to observe macaques directly to determine the degree to which animal seed dispersal is captured by seed traps. The monkey-related problems affecting the seed-trap method were complex and included both negative and positive effects. The extent of over- or underestimation is expected to vary among plant species. Direct observations of how monkeys handle seeds/fruits may help to determine the tendency for over- or underestimation. Therefore, to obtain reasonable estimates of total seed dispersal, we recommend that researchers should conduct the seed-trap method concurrently with monkey observations, and that they should affix traps more securely to prevent their destruction by macaques. Acknowledgments We would like to thank our friends and colleagues in Yakushima for their hospitality and help during the fieldwork. We are also grateful to Yakushima Forest Environment
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Primates (2014) 55:161–165 Conservation Center for permission to undertake the research. The Sarugoya Committee and Field Research Center of the Primate Research Institute, Kyoto University offered us excellent facilities. This research was partly supported by grants for Biodiversity Research of the 21st Century COE (A14), Research Projects D-01 and D-02 of the Research Institute for Humanity and Nature, and by Research Fellowships of the Japan Society for the Promotion of Science for Young Scientists for R.T., as well as the Environmental Research and Technology Development Fund (S9) of the Ministry of the Environment, Japan.
References Au AYY, Corlett RT, Hau BCH (2006) Seed rain into upland plant communities in Hong Kong, China. Plant Ecol 186:13–22 Clark JS, Macklin E, Wood L (1998) Stages and spatial scales of recruitment limitation in southern Appalachian forests. Ecol Monogr 68:213–235 Hanya G (2005) Comparisons of dispersal success between the species fruiting prior to and those at the peak of migrant frugivore abundance. Plant Ecol 181:167–177 Harms KE, Wright SJ, Caldero´n O, Herna´ndez Herre EA (2000) Pervasive density-dependent recruitment enhances seedling diversity in a tropical forest. Nature 404:493–495 Hoshizaki K, Suzuki W, Nakashizuka T (1999) Evaluation of secondary dispersal in a large-seeded tree Aesculus turbinate: a test of directed dispersal. Plant Ecol 144:167–176 Iida S (2006) Dispersal patterns of Quercus serrata acorns by wood mice in and around canopy gaps in a temperate forest. For Ecol Manage 277:71–78 Lee CS, Kim JH, You YH (2004) Seedling establishment and regeneration of Korean red pine (Pinus densiflora S. et Z.) forests in Korea in relation to soil moisture. For Ecol Manage 199:423–432 Lichstein JW, Grau HR, Arago´n R (2004) Recruitment limitation in secondary forests dominated by an exotic tree. J Veg Sci 15:721–728 Masaki T, Kominami Y, Nakashizuka T (1994) Spatial and seasonal patterns of seed dissemination of Cornus controversa in a temperate forest. Ecology 75:1903–1910 Moles AT, Drake DR (1999) Potential contributions of the seed rain and seed bank to regeneration of native forest under plantation pine in New Zealand. NZ J Bot 37:83–93 Nathan R, Muller-Landau MC (2000) Spatial patterns of seed dispersal, their determinants and consequences for recruitment. Trends Ecol Evol 15:278–285 Otani T (2004) Effects of macaque ingestion on seed destruction and germination of a fleshy-fruited tree, Eurya emarginata. Ecol Res 19:495–501 Otani T, Shibata E (2000) Seed dispersal and predation by Yakushima macaques, Macaca fuscata yakui, in warm temperate forest of Yakushima Island, southern Japan. Ecol Res 15:133–144 Russo SE, Portnoy S, Augspurger SK (2006) Incorporating animal behaviour into seed dispersal models: implications for seed shadows. Ecology 87:3160–3174 Sato H (2013) Seasonal fruiting and seed dispersal by the brown lemur in a tropical dry forest, north-western Madagascar. J Trop Ecol 29:61–69 Stevenson PR, Ivonne NV (2008) Sample size and appropriate design of fruit and seed traps in tropical forests. J Trop Ecol 24:95–105 Tagawa H (1980) Vegetation on the western slope of Mt. Kuniwaridake, Yakushima Island. Science reports of Kagoshima University 29:121–137 (In Japanese)
Primates (2014) 55:161–165 Terakawa M, Matsui K, Hamada T, Noma N, Yumoto T (2008) Reduced seed dispersal effectiveness in the large-seeded tree Myrica rubra in the absence of the Japanese macaque on Tanegashima Island, Japan. Jpn J Conserv Ecol 13:161–167 (in Japanese with English summary) Terborgh J (1986) Community aspects of fruigivory in tropical forests. In: Estrada A, Fleming TH (eds) Frugivores and seed dispersal. Springer, Netherlands, pp 371–384 Tsujino R, Yumoto T (2007) Spatial distribution patterns of trees at different life stages in a warm temperate forest. J Plant Res 120:687–695
165 Tsujino R, Yumoto T (2009) Topography-specific seed dispersal by Japanese macaques in a lowland forest on Yakushima Island, Japan. J Anim Ecol 78:119–125 Tsujino R, Takafumi H, Agetsuma N, Yumoto T (2006) Variation in tree growth, mortality and recruitment among topographic positions in a warm-temperate forest. J Veg Sci 17:281–290 Yumoto T, Noma N, Maruhashi T (1998) Cheek-pouch dispersal of seeds by Japanese monkeys (Macaca fuscata yakui) on Yakushima Island, Japan. Primates 39:325–338
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NEWS AND PERSPECTIVES
Problems associated with the seed-trap method when measuring seed dispersal in forests inhabited by Japanese macaques Riyou Tsujino • Takakazu Yumoto
Received: 25 September 2013 / Accepted: 17 December 2013 / Published online: 31 December 2013 Ó Japan Monkey Centre and Springer Japan 2013
Abstract Despite the widespread use of seed/litter traps in seed dispersal ecology, several problems have arisen when using this method in forests inhabited by semi-terrestrial monkeys. The first issue is the height of the trap relative to the location where macaques spit seeds and/or defecate. For Japanese macaques in the lowland forests of Yakushima Island, southern Japan, 30–50 % of the seeds emitted from cheek pouches and faeces will not be caught by seed traps, leading to underestimation of seed fall. The second issue is the attractiveness of seed traps. Macaques sometimes play with the traps, potentially affecting the results of the seed-trap method in complex ways, including both negative and positive effects. To obtain reasonable estimates of total seed dispersal, we recommend that researchers conduct the seed-trap method concurrently with monkey observations, and that they should affix traps more securely to prevent macaques from destroying the traps.
R. Tsujino Center for Ecological Research, Kyoto University, Otsu, Shiga 520-2113, Japan Present Address: R. Tsujino (&) Center for Natural Environment Education, Nara University of Education, Takabatake-cho, Nara 630-8528, Japan e-mail: [email protected] T. Yumoto Research Institute for Humanity and Nature, 457-4, Motoyama, Kamigamo, Kita-ku, Kyoto 603-8047, Japan Present Address: T. Yumoto Primate Research Institute Kyoto University, Kanrin, Inuyama, Aichi 484-8506, Japan
Keywords Cheek pouch Faeces Height Physical attack Seed fall
Introduction Seed-trap methods are used to estimate the seed rain and the total amount and spatial distribution pattern of seed/ fruit fall in forests (e.g. Masaki et al. 1994; Clark et al. 1998; Moles and Drake 1999; Nathan and Muller-Landau 2000; Lichstein et al. 2004; Lee et al. 2004; Hanya 2005; Tsujino and Yumoto 2007). Despite the wide use of traps in seed dispersal ecology and the spatial structure analysis of plant populations, there are several potential biases inherent to the trap design, such as bouncing, wind effects, area effects, and seed removal by predators (Stevenson and Ivonne 2008). Stevenson and Ivonne (2008) also suggested that particular behaviours of predators and mechanical damage by megafauna should be taken into account. In addition, the seed-trap method is not a general method for evaluating seed dispersal by terrestrial and/or semi-terrestrial mammals (e.g. Russo et al. 2006; Sato 2013). In the study reported in the present paper, we defined terrestrial mammals as mammals which generally forage on the ground and rarely climb trees, semi-terrestrial mammals as mammals which forage on the ground as well as in the trees, and arboreal mammals as mammals which generally forage in the trees and rarely on the ground. To investigate terrestrial and/or semi-terrestrial mammal seed dispersal, a specific research framework is necessary, such as faecal analysis (Hanya 2005), focal animal sampling (Tsujino and Yumoto 2009), the direct collection of seeds of large-seeded species on the ground (Hoshizaki et al. 1999), or the placing and tracking of marked seeds to evaluate removal by dispersal agents (Iida 2006).
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The circumstances of semi-terrestrial mammal are not the same as those of birds, arboreal mammals or terrestrial mammals. While attempting to estimate the amount of seed fall in forests inhabited by high densities of semi-terrestrial monkeys, we noted several problems with the reliability of the seed-trap method in relation to the behaviour of monkeys. For example, Japanese macaques typically place fruits into their cheek pouches in the canopies of fruiting trees and then usually return to the ground and spit out the seeds if necessary. However, seed traps are often set 0.8–1.5 m above the ground (e.g. Masaki et al. 1994; Harms et al. 2000; Hanya 2005; Tsujino and Yumoto 2007) to avoid seed removal or physical disturbance by animals. Therefore, if the macaques spit or defecate seeds when they are on the ground, seed dispersal will be underestimated by the seed-trap method, even though primates play significant roles in seed dispersal (Terborgh 1986). Thus, our objective was to determine the degree of underestimation of seed-fall catch by traps that measure seed dispersal by Japanese macaques via cheek pouches and faeces in a warm-temperate forest on Yakushima Island, Japan. In addition, we report observations of macaques playing with the seed traps. We then discuss the difficulties of measuring total seed fall in a forest inhabited by high densities of semi-terrestrial monkeys, and the potential disruptive behaviours of monkeys that affect the estimation of total seed dispersal using the seed-trap method.
Methods Study area Yakushima Island (30°200 N, 131°300 E) is located approximately 70 km south of Kyushu, Japan. The study area was located in a warm-temperate forest at an altitude of 80–350 m along the western slope of Mt. Kuniwari-dake (1323 m a.s.l.). The mean annual temperature and rainfall were approximately 21 °C and 2600 mm, respectively (Tagawa 1980). The forest consists primarily of broadleaved evergreen Fagaceae, Hamamelidaceae, Myrsinaceae, and Lauraceae (Tsujino et al. 2006). Behavioural observations Macaca fuscata yakui, a subspecies of Japanese macaque, plays an important role in dispersing seeds of fleshy-fruited plants in the warm-temperate forests of Yakushima Island (Yumoto et al. 1998; Otani and Shibata 2000; Otani 2004; Tsujino and Yumoto 2009). Body lengths of Japanese macaques are 50–60 cm, and adult male and female body weights are 12–15 and 8–13 kg, respectively. In fact,
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Terakawa et al. (2008) reported that the mean number of Myrica rubra fruits consumed by macaques was 35.6-fold more than that consumed by brown-eared bulbuls Hypsipetes amaurotis on Yakushima Island, where macaques and brown-eared bulbuls are primarily consumers of Myrica rubra fruits. Macaca fuscata yakui individuals tend to hold fruits in their cheek pouches and spit out large seeds, whereas small seeds tend to be swallowed and defecated (Otani and Shibata 2000). Seed dispersal by Japanese macaques was studied in one troop of habituated macaques (B troop) composed of 10 members at the onset of the study (four adult females, two adult males, three juvenile males, one juvenile female). One adult female disappeared and four adult males immigrated during the study period. We collected behavioural feeding, height in the tree, seed spitting, and defecation data for four adult females and four adult males using a 2-min-interval point-sampling method. We conducted focal sampling for up to 1 h (unless seed deposition was occurring), during which time we recorded the activity of the feeding and seed-depositing focal macaque as well as the food items and location (on a map) at 2-min intervals. If a focal animal was depositing seeds from its cheek pouches when we should have switched to a new focal animal, we continued the observation until seed deposition was completed. We estimated the heights at which focal macaques were located to the nearest metre at 2-min intervals, as well as the heights from which seeds and faeces were dropped. We conducted field observations in the summer (June 2003), autumn (November and December 2003), and winter (March 2004) after a 1-month preliminary survey in May 2003. The total observation time was 240.2 h: 143.5 h for females and 97.7 h for males. We pooled data for females and males in the following analyses, because differences between the sexes were beyond the scope of this study.
Results and discussion In total, we observed 60 faecal depositions during 240.2 h of macaque observation time. Macaques spent 60.5 % of the daytime on the ground or at\2 m in height and 39.5 % of the daytime above 2 m in height, primarily in trees (Fig. 1). Among the 60 cases of faecal deposition, the macaques defecated 19 times (31.7 %) from heights \2 m and 41 times (68.3 %) from heights above 2 m (Fig. 1). We observed 2402 seeds being dispersed from cheek pouches, including 118 seeds of Myrica rubra, 319 of Persea thunbergii, 444 of Neolitsea sericea, 1306 of Litsea acuminata, and 215 of unidentified species. Macaques spat 1186 seeds (49.5 %) from heights \2 m and 1216 seeds (50.5 %) from heights above 2 m (Fig. 2). Therefore, the
Primates (2014) 55:161–165
Fig. 1 Percentages of macaque locations during scans (i.e. macaque foraging heights), faecal defecations, and seed dispersal via cheek pouches at the ground to below 2 m in height, 2–5 m, 5–10 m, and above 10 m
height issue associated with the location of seed traps would lead to underestimation of the extent of seed dispersal. The defecation height ratio (number of defecations at \2 m above the ground/total defecations; 31.7 %) and the seed spitting height ratio (number of seed spits at \2 m above the ground/total number of spits; 49.5 %) were both significantly different from the foraging height ratio (number of macaques foraging at locations\2 m above the ground/total number of scans; 60.5 %) (binomial test, p \ 0.0001). Although using a height of 2 m as a threshold caused overestimation of the defecation height ratio of the seed traps, the degree of overestimation was negligible for the defecation (2.1 %), seed spitting (1.9 %) and foraging
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(1.4 %) at 0–2 m in height. These results indicate that macaques dropped more seeds and faeces from more than 2 m above the ground than expected based on their foraging patterns. In general, 30–50 % of the seeds deposited via cheek pouches and faeces will not be caught by the seed traps. Therefore, an inappropriate seed trap height would lead to an underestimation of seed dispersal. In addition, we suggest that this effect will differ in magnitude among plant species. Seed-fall estimations for some plant species whose fruits/seeds are consumed/dispersed by macaques should be corrected for this height effect. In contrast, plant species whose fruits are not consumed by macaques need not be corrected. Placing seed traps on the ground is one of the ways that can be used to avoid the underestimation of seed dispersal if there are few large terrestrial and semiterrestrial mammals that trample on the traps or feed on fallen seeds and fruits in the traps in the study site (i.e. Au et al. 2006). Another solution is to directly count seeds of large-seeded plant species on the ground soon after the seeds are dispersed (i.e. Hoshizaki et al. 1999). However, these methodological solutions may only be applicable to limited study sites and plant species. The second problem associated with the seed-trap method is the attractiveness of traps to macaques, who sometimes play with them. On 4 October 2001, from approximately 10:42 to 11:04 in the study area, Tsujino observed young and adult Japanese macaques playing with seed traps that had been set for another purpose (Tsujino and Yumoto 2007). At least three macaques sat on and
Fig. 2 Photographs depicting macaques playing with seed traps in the study forest (photo by Tsujino, 4 October 2001). Seed traps were affixed with three poles and ropes
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rested on the edges of the seed traps, sometimes climbing into the traps to eat acorns of Pasania edulis (Fig. 2). Artificial constructions in the forest, such as seed traps, are conspicuous and may be particularly attractive to macaques. This attractiveness issue has several potential effects on the seed-trap method. First, because they may remain on or around seed traps for a longer period of time, macaques may defecate more faeces and spit more seeds into the seed traps than if they were not attracted by the traps. Second, as occurred during our case observations, macaques will consume fruits that had already collected in the seed traps, as seeds and fruits in the traps are attractive to macaques. When the macaques enter a trap, they do not need to search for fallen fruits, which are often contaminated and/or encumbered by the soil, tree roots, or decaying litter. This effect will lead to underestimations of fruit fall for species that are consumed by macaques. However, seed-fall estimations of species dispersed by macaques via cheek pouches will be overestimated, because macaques might feed on fruits and spit the seeds directly into the trap. If macaques leave the trap before spitting seeds into it, seed fall will be underestimated. Therefore, the attractiveness effect could lead to either the under- or overestimation of seed fall, depending on the circumstances. Third, physical attack by macaques, as shown in Fig. 2, will cause the destruction of traps. This effect will hinder the measurement efforts of the researchers. Moreover, trap destruction affects every type of seed as well as litter collection. Researchers must be aware of these physical disturbances and affix traps more securely. In conclusion, we highlighted the difficulties associated with the accurate measurement of seed dispersal using only the seed-trap method in forests inhabited by a high density of monkeys. Because several factors related to monkey behaviour affect the accuracy of these estimations, researchers may need to observe macaques directly to determine the degree to which animal seed dispersal is captured by seed traps. The monkey-related problems affecting the seed-trap method were complex and included both negative and positive effects. The extent of over- or underestimation is expected to vary among plant species. Direct observations of how monkeys handle seeds/fruits may help to determine the tendency for over- or underestimation. Therefore, to obtain reasonable estimates of total seed dispersal, we recommend that researchers should conduct the seed-trap method concurrently with monkey observations, and that they should affix traps more securely to prevent their destruction by macaques. Acknowledgments We would like to thank our friends and colleagues in Yakushima for their hospitality and help during the fieldwork. We are also grateful to Yakushima Forest Environment
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Primates (2014) 55:161–165 Conservation Center for permission to undertake the research. The Sarugoya Committee and Field Research Center of the Primate Research Institute, Kyoto University offered us excellent facilities. This research was partly supported by grants for Biodiversity Research of the 21st Century COE (A14), Research Projects D-01 and D-02 of the Research Institute for Humanity and Nature, and by Research Fellowships of the Japan Society for the Promotion of Science for Young Scientists for R.T., as well as the Environmental Research and Technology Development Fund (S9) of the Ministry of the Environment, Japan.
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