Ornithol Sci 11: 121 – 128 (2012)

SHORT COMMUNICATION Relationships between controversa fruit phenology and fruit removal behaviors of frugivorous birds

Kyoko SANO1,*, Shinsuke KOIKE1,#, Akiko TAKAHASHI1,**, Norio TOKITA2, Chinatsu KOZAKAI1,*** and Kengo FURUBAYASHI1

1 Tokyo University of Agriculture and Technology, 3–5–8 Saiwai, Fuchu, Tokyo 183–8509, Japan 2 Nippon Veterinary and Life Science University, 1–7–1 Kyonan, Musashino, Tokyo 180–8602, Japan

Abstract The behavior of frugivorous birds during the removal of fruit from Swida ORNITHOLOGICAL controversa was investigated to compare the relationships between measures of fruit SCIENCE maturation and quantitative fruit removal behavior of birds. Bird exclusion devices © The Ornithological Society were used on some branches to allow comparison of the traits of removed and of Japan 2012 un-removed fruits. Nine bird visited S. controversa, but only four removed fruit, and each bird species removed a different number of fruits per visit. Only 11.5% of a branch’s fruits were removed by birds. Birds removed only larger, blacker, more mature fruits, suggesting birds were effective seed dispersers.

Key words Dispersal effectiveness, Endozoochory, Fruiting phenology, Hypsipetes amaurotis, Seed dispersal

Temperate forests in Japan contain many woody surviving to later stages are important points to with fleshy fruits (Nakanishi 1994). Most consider and these factors are related to whether indi- fleshy fruits are adapted to consumption by a variety vidual agents play an effective role in seed dispersal of vertebrates, which are putative dispersal agents for during the removal of fruit. We should consider sev- seeds from these fruits (e.g. Howe 1986; Willson eral important points related to these ideas. First, the 1993). Each plant species uses several agents of seed feeding period in terms of seasonal fruiting phenol- dispersal with different patterns of seed rain or ger- ogy (Koike et al. 2008a); if fruits are removed before mination success (Jordano et al. 2007; Traveset et al. seed maturation, the dispersed seeds cannot germi- 2007). The effectiveness of these patterns of seed nate. The relationship between the time period during dispersal needs to be studied so we can understand which fruit is removed by dispersal agents and fruit and compare the impacts of individual dispersal phenology and seed maturation must be considered agents on plant recruitment dynamics (Schupp 1993; when determining whether individual agents are Herrera et al. 1994; Schupp & Fuentes 1995). Schupp effective seed dispersers. Second, it is important to (1993) demonstrated that dispersal effectiveness document fruit selection by each agent, because vari- affects plant reproduction and has both qualitative ations exist in the characteristics of fruit that are and quantitative components. related to the seed dispersal success of different indi- For the qualitative components, the condition of viduals within the same species (e.g. size, pulp vol- seeds following handling and the probability of seeds ume, pulp nutritional condition, and seed germinabil- ity) (e.g. Herrera 2009). Clarifying the relationships (Received 14 November 2011; Accepted 10 October 2012) between the details of fruit characteristics and selec- # Corresponding author, E-mail: [email protected] tion by agents may contribute to a better understand- * Present address: Ministry of the Environment Government of ing of the individual agent’s qualitative role in suc- Japan, Takamatsu Ranger Office, 2–1–1Kotobuki, Takamatsu, Kagawa 760–0023, Japan cessful seed dispersal. ** Present address: Laboratory of Animal Ecology, Department of For the quantitative components, the frequency of Biological Science, Graduate School of Science and Engineer- visits to a plant and the number of fruits removed per ing, Tokyo Metropolitan University, 1–1 Minamioosawa, visit are important factors. Many studies have Hachiouji, Tokyo 192–0364, Japan *** Present address: Kanagawa Prefectural Museum of Natural addressed these two quantitative components over History, 499 Iriuda, Odawara, Kanagawa 250–0031, Japan the past 30 years, especially as they relate to avian

121 K. SANO et al. endozoochory (e.g. Jordano 1982; Herrera 1984). itation frequency and number of fruits removed per They have often been recorded by direct observation visit by each bird species was calculated based on (Jordano 1982; Herrera 1984). Measurement of qual- direct observation. The characteristics of fruit itative and quantitative factors has been more diffi- removed by birds were also quantitatively measured, cult in Japanese temperate deciduous forests, which using a fruiting phenology and bagged test. Direct have vertically layered structures. It is not easy to observations were used in order to answer the accurately observe bird visits and foraging behavior following questions: (1) Which bird species visit S. in closed stands of . Thus, few studies have controversa and remove its fruit? (2) When, in rela- examined the qualitative and quantitative compo- tion to fruiting phenology, do birds feed on the fruit? nents of seed dispersal in Japan. (3) What are the characteristics of the fruits removed Masaki et al. (1994) set many seed traps over large by birds? (4) How many fruits did each bird species spatial and temporal scales to collect seeds removed remove per visit? and (5) How abundant were the from Swida controversa to clarify the spatial patterns fruits removed by birds? of seed dissemination. They calculated fruit removal rates by birds for quantitative factors and compiled a MATERIALS AND METHODS list of bird species consuming S. controversa fruits using bird fauna census data for qualitative factors. 1) Study site However, their methods did not allow detailed iden- The study was conducted from an observation tification of the avian species actually removing tower in an isolated 100 m×50 m wood lot sur- fruits; consequently it was not possible to determine rounded by farmland at Oyasan University Forest the numbers of fruits removed by individual bird spe- Nursery (36°54′28″N, 139°34′93″E; 400 m a.s.l), cies. Tokyo University of Agriculture and Technology, Thus, the steps of visitation and removal are related Japan. During the period 1997–2002, the mean to these components during the process of seed dis- annual temperature at the site was 11.5–12.3°C and persal by vertebrates. Previous studies have shown the precipitation was 1,452–1,883 mm (Oyanagi et that many vertebrates, including birds, bats, primates al. 2003). This forest is dominated by Castanea cre- and carnivores, play roles as endozoochorous seed nata, Quercus serrata, and planted Cryptomeria dispersers (e.g. Howe 1986; Willson 1993; Jordano japonica. There were no other tall trees with fleshy 1995; Howe & Westley 1988; Koike et al. 2008b); fruit within 100 m of the target trees during the study however birds function as seed dispersers across period, although there were a few shrubby trees with broad areas and it is easier to observe their behavior fleshy fruit such as Callicarpa japonica. than other animals (Masaki 2009), thus they make The 9 m high observation tower was located within ideal species to study. an enclosure containing eight individual trees (>1 m The fruits of S. controversa were chosen for stud- tall) belonging to five species: S. controversa (N=2), ies focused on avian fruit removal during endozooch- Quercus crispula (N=1), Q. serrata (N=2), Carpinus ory), for two reasons. First, S. controversa is a com- cordata (N=1), and C. crenata (N=2). Parts of the mon species in the deciduous forests of Japan and its crowns of the taller trees projected above the tower. seeds are frequently dispersed by birds (Masaki et al. 1994; Masaki & Kodani 2009). Second, the demog- 2) Fruiting phenology of Swida controversa raphy or seed dispersal systems of this Japanese Plant species endozoochorous tree species is better known than for In Japan, the deciduous tree S. controversa occurs other Japanese tree species (e.g. Masaki et al. 1994). from the sub-alpine zone to the temperate zone. It The main objectives of this study were to: deter- prefers sunny sites with humid soil and when mature mine the quantitative and qualitative components of reaches a height of 15–20 m. It produces flowers seed dispersal effectiveness for each bird species from May to June, and its fruit, mature from August seen removing S. controversa fruit, compare the to October. The fruit (a small drupe about 10–15 mm fruits selected by different bird species, and to com- in diameter) contains a single hard-shelled stone pare the results related to the abundance of fruits (endocarp) 3–7 mm in diameter and 2–4 mm thick removed by birds to previous studies using different with from zero to two seeds inside the stone (Masaki methods. The abundance of fruits removed by the & Kodani 2009; Shinsuke Koike unpublished data). bird fauna was quantitatively measured, then the vis- Seed production by S. controversa varies annually,

122 Avian fruit removal behaviors with masting occurring every two to five years. While October for analysis of fruit sugar content (fructose, much remains unknown about its fruiting ecology glucose, and sucrose) in the mesocarp by liquid chro- (Masaki & Kodani 2009), it is known that birds con- matography (Shimadzu CA-4PJ, Kyoto, Japan) fol- sume its fruit and are major seed dispersers, as are lowing the method of Sweeley et al. (1962). some carnivores also (Koike & Masaki 2008). A wide variety of potential avian dispersal agents exist, but 3) Frugivore species, fruit removal behavior, and the period and patterns of visitation must vary from characteristics of removed fruits year to year, so the pattern of seed dispersal must The feeding habits of avian visitors were observed also vary from annually. Quantitative data identifying for two hours after sunrise once a week during the which species function as frugivores or seed dispers- fruiting period from the observation tower (9 July– ers are lacking. 12 November, 19 times) because most birds fed dur- Two S. controversa trees were monitored (No. 1: ing the morning. Preparations for observation were diameter at breast height (DBH) 24.0 cm; height 15.5 made before sunrise and the observers moved as little m; crown expanse N–S=8.5 m, W–E=6.3 m; No. 2: as possible during the observational period so as to DBH 32.0 cm; height 17.0 m; crown expanse N– avoid disturbing avian activity. Observations were S=11.5 m, W–E=7.8 m) from 16 July to 22 October usually made on sunny days, and bird species, num- 2005. Although these two trees were close to each bers of visits, and the numbers of fruits removed per other, their crowns did not overlap. The age of the visit were all recorded. When several birds removed trees is not known. As only one tree (No. 1) produced fruit simultaneously, it was not possible to record the fruit in sufficient quantities for observation, our cal- behavior of all of the birds, as many as possible were culations refer to a single tree. recorded. Three branches (A, B, C) on the tree were enclosed Fruit color and persistence in nylon nets to within 50 cm of the tips to exclude On 16 July, 600 fruits growing on nine inflores- birds to allow estimation of the removal rate by birds cences on the tree were chosen and all pedicels were and to determine the characteristics of fruits eaten by tagged. Fruit color and numbers of persisting pedi- birds; these were matched with three other branches cels were recorded once a week from 16 July to 22 (D, E, F) from the same tree to which birds were October. Fruits were categorized as green when all of allowed free access. First, the number of fruits on the the exocarp was green, white when small portions of freely accessible branches were counted. Fruit traps the fruit were white, purple when more than 50% of were set under the freely accessible branches to col- the surface area was purple, and black when the black lect any fruit that fell from those branches. Fruit traps portion exceeded 50% of the surface area. were made of nylon mesh and plastic pipe (diameter 80 cm; area 0.5 m2; height 50 cm), and set up from Fruit size and seed maturation the tower. Freely accessible branches were separated, Fifty fruits of each color category were randomly not overlapped. Removal rates were calculated by sampled from the tree once a week from 16 July to comparing the rates of fruit formation on the enclosed 22 October. The horizontal diameter of each fruit (at branches (A–C) and rates of fruit collection in the right angles to the pedicel) was measured with a pair traps. of calipers. As sufficient fruits were not available To estimate the size of fruits removed by birds, the after 24 September, the sample size was reduced relationship between mature fruit diameter and endo- from 50 to 20 fruits of each color category after 24 carp diameter ([Fruit diameter]=1.24×[endocarp September. We washed away the exocarp and meso- diameter]+1.06, R2=0.65, Kyoko Sano unpublished carp in water and conducted germination tests using data) was first determined because it was not possible either the tetrazolium staining method or by examina- to measure the diameters of fallen fruit, which spoiled tion of the albumen in cut seeds to determine the quickly. Fruit were measured as previously described, maturation status of the seeds (McDonald & Copeland and in addition the horizontal diameter of the endo- 1989). carp, which crosses the vallecula on the surface of endocarp at right angles, was also measured. The Sugar content of the fruits sizes of the endocarps on the enclosed branches (A, Twenty fruits of each color were randomly sam- B, C: potentially removed fruit and not potentially pled from the tree once a week from 16 July to 8 removed fruit) and the sizes of the endocarps in the

123 K. SANO et al. traps (not removed fruit) were then compared. Fruit sizes Means of fruit size differed among fruits of differ- RESULTS ent colors (Steel’s test, df=1–3, P<0.05; Fig. 1b). Fruit size increased from 16 July to 13 August and 1) Fruiting phenology of Swida controversa then stabilized. After 13 August there were no Fruit color and numbers per tree changes in fruit size in any color category. Average All fruits were green and white until 16 July (Fig. sizes (SD) were: green 7.2±0.1 mm; white 7.8±0.1 1a). Purple fruits appeared on 23 July, followed by mm; purple 8.3±0.1 mm; and black 8.7±0.1 mm. black fruits on 30 July. Purple and black fruits exceeded 50% of the total on 20 August and 80% of Sugar content in fruits the total on 10 September. Green fruits were last Sugar contents differed among fruit color catego- recorded on 17 September, and white fruits on 1 ries (Steel’s test, df=1–3, P<0.05), but not during October. The proportion of fruit that persisted on the fruit maturation within each fruit color category tree decreased gradually until August, and then (Steel’s test, df=13–19, P>0.05; Fig. 1d). Black fruit declined rapidly during September (Fig. 1c). always had higher sugar contents than fruits of other colors.

Fig. 1. Swida controversa fruit development and visitations by birds: (a) Changes in the color of fruit on trees (n=600) from 16 July to 22 October 2005, (b) Changes in fruit diameter (mm) by color; n=50 for each color, except after 24 September, n=20 for each color, (c) Proportion of fruit remaining on trees, (d) Changes in total sugar content (mg/fruit) by color; n=20 for each color, (e) Numbers of birds, by species, which visited the tree every two hours. For (a), white bars represent green fruit, shaded bars represent white fruit, gray bars represent purple fruit, and black bars represent black fruit. For (b) and (d), open circles indicate green fruit, open triangles indicate white fruit, closed triangles indicate purple fruit, and closed circles indicate black fruit. For (e), open squares are for Hypsipetes amaurotis, open circles for Zosterops japonicus, closed circles for Picus awokera, and open triangles are for Covus corone.

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Table 1. Percentage of germinating seeds of Swida contro- Japanese White-eye Zosterops japonicus (N=20, versa during fruit maturation in relation to fruit color. Values 4.2%), Japanese Green Woodpecker Picus awokera with the same lower-case letters do not differ significantly (N=15, 3.1%), and Carrion Crow (Corvus corone) between colors within dates (Steel’s test, P<0.05). (N=7, 1.4%). Birds visited from 16 July through 12 Seed maturation (%) November and H. amaurotis visited during the entire period, while Z. japonicus visited only during July Fruit color and August, and P. awokera and C. corone visited Date Green White Purple Black only after August (Fig. 1e). The number of visits by July 16 0 0 – – H. amaurotis and Z. japonicus peaked several times, July 23 4.5±3.0a 3.1±2.0a 6.1±4.3a – with peaks once a month during the entire visitation July 30 8.0±1.9a 4.3±3.0a 9.2±4.2a 29.3±10.1b period. August 6 3.3±0.3a 4.6±3.7a 5.6±2.8a 26.6± 7.6b Only four species (H. amaurotis, Z. japonicus, P. August 13 4.3±1.1a 4.8±2.8a 13.9±2.6b 18.0± 6.0b awokera, and C. corone) removed fruit during the August 20 5.6±2.3a 3.8±0.9a 13.0±2.6b 14.0± 6.6b sampling period from 30 July to 5 November (Table August 27 4.3±2.9a 2.1±0.8a 11.2±7.1b 15.0± 1.3b 2; Fig. 1e), and all birds removed only black fruits. September 3 0.8±1.4a 1.5±1.6a 8.4±4.9b 13.7± 0.7b The number of fruit removed per visit differed sig- September 10 3.8±3.3a 0 7.6±3.1a 16.1± 3.6b nificantly among species (Steel-Dwass test, P<0.001): September 17 2.2±1.5a 1.0±1.7a 1.2±1.0a 19.0± 2.5b P. awokera and C. corone removed the highest num- ber per visit, and H. amaurotis removed more fruit Seed maturation per visit than did Z. japonicus (Table 2). For H. No seeds matured until 16 July (Table 1). The seed amaurotis, we could not recognize all individual maturation rate was approximately 5% on 23 July, birds removing fruit behavior during the observa- and reached a maximum on 30 July. Seed maturation tions. Thus, we recorded only 25 birds removing rates were significantly higher among black and pur- fruits. ple fruit than among white and green fruit (Steel’s The comparison between the enclosed and exposed test, df=1–3, P<0.05). branches showed that 11.5%±6.2 (SD) of the fruits were eaten/removed, and the endocarps of the fruit 2) Frugivore species, fruit removal behavior, and on the enclosed branches (A, B, C) (5.61±0.45 mm) characteristics of removed fruits were larger than those of fallen fruit (D, E, F) Nine species of birds were observed making (5.21±0.41 mm) (Kruskal–Wallis test, df=5, 474 visits to S. controversa fruit during the survey P<0.05). (Table 2). The most frequent visitors were Brown- eared Bulbul Hypsipetes amaurotis (N=420, 88.6%), DISCUSSION Table 2. Visits by birds to a single Swida controversa tree. Although it was expected that all of the avian vis- Values in parentheses indicate the number of birds observed removing fruit during the observation period. itors to the study trees would remove fruit, some did not (Table 2). In fact of nine bird species observed Number of: visiting S. controversa during the limited period of this study, only four (H. amaurotis, Z. japonicus, P. Species Days Fruits Birds observed removed awokera, and C. corone) removed fruits and can be (n=19) per visit considered frugivorous and hence potential seed dis- persal agents of S. controversa. These results indicate Hypsipetes amaurotis 420 (25) 17 9.1±2.9 that estimates of frugivory based on faunal censuses Zosterops japonicus 20 ( 8) 5 1.2±0.4 alone may overestimate the numbers of actual fru- Picus awokera 15 ( 7) 8 15.3±5.1 givorous species. Thus, determining which bird spe- Corvus corone 7 ( 5) 3 15.6±2.9 cies are actually frugivorous requires direct observa- Muscicapa dauurica 6 5 – tion of birds actually swallowing fruit or DNA Streptopelia orientalis 3 2 – analysis from feces or pellets that include seeds. Dendrocopos kizuki 1 1 – The bird species visiting S. controversa changed Emberiza cioides 1 1 – over time (this study). Masaki (2006) also demon- Eophona personata 1 1 – strated that there were several peaks in the removal

125 K. SANO et al. of S. controversa fruit by birds, it suggesting that controversa may be using this same strategy. Our different species may remove fruit at different times. findings demonstrated frugivorous birds potentially Visits to fruiting trees by bird species also change function not as seed predators, but as potential seed seasonally (Ito & Fujiwara 2007), a pattern confirmed dispersers of S. controversa. by bird census investigations in a Japanese deciduous All of the birds in this study removed only mature forest (Takanose & Kamitani 2003). The abundance black S. controversa fruit, that were large and with a of various bird species generally changes over time high seed-germination potential (Fig. 1d). Such pref- from summer to winter and during migration. Other erences give S. controversa an advantage in seed dis- factors may be responsible for changes in bird num- persal if the birds don’t damage or digest the seeds. bers, including food resources and weather condi- Black S. controversa fruit have a consistently higher tions, but these ideas remain untested. Previous works sugar content than other colored fruit (Fig. 1d). Plant have reported seasonal variations in frugivorous producing large seeds species have a survival advan- bird species richness and abundance (Takanose & tage over species producing small seeds during seed- Kamitani 2003; Masaki 2006). However, to arrive at ling establishment (Moles & Westoby 2004). If birds definitive conclusions about the mechanisms underly- select large seeded species this may benefit plants ing any relationships between phenological patterns after the seed dispersal stage. Previous studies have in fleshy-fruited plants and the abundances of fru- shown that frugivorous birds select foods that are givorous birds, additional long-term, continuous relatively high in nutrients and easy to digest (Stiles studies are required (e.g. Herrera 1998). This study 1993; Smith et al. 2007). Stiles (1993) demonstrated was made over a limited period, thus the future chal- the importance of lipids in the fruit preferences of lenge is to observe the interactions between birds and frugivorous birds, and Masaki et al. (2012) showed fruits over a longer timeframe. Seasonal changes in that S. controversa fruits contain fats in addition to the frequency and/or abundance of visiting and/or sugars; these, along with the stored sugars, may serve fruit removing fauna are likely to be further impor- to reward foraging birds. Further work is warranted tant aspects of dispersal effectiveness in terms of the to determine the roles of other nutritional compo- amount of fruits presented to specific seed dispersers. nents of fruits in attracting birds as agents of seed In this study, birds removed S. controversa fruit dispersal. only after 30 July, and they only removed black fruit. The frequency with which birds visit trees and the Based on germination tests, the germination rate for number of fruits removed per visit by each bird spe- S. controversa increased after July 23 (Table 1), thus cies are further important aspects of frugivory (Table avian fruit removal occurred after seed maturation. 2), as is the digestive processing as seeds pass through This preference for removing only black fruits with avian digestive tracts, which leads to increased ger- mature seeds is probably a result of phenological mination rates (e.g. Fukui 1996). H. amaurotis is a changes in the fruit. Most frugivorous birds select well-known major seed dispersal agent in Japanese red or black fruits (e.g. Willson & Thompson 1982; temperate deciduous forests that occurs throughout Wheelwright & Janson 1985; Nakanishi 1996), sug- most of Japan and disperses a wide range of different gesting that color change (from green) is a cue that plant species’ seeds (Yoshikawa et al. 2009). During attracts frugivorous birds (Fig. 1a). In this study, as the course of the present study Picus awokera and C. fruit color changed so too did fruit size after seed corone ate more fruits per visit than other bird spe- maturation, change that has been described in detail cies, and although Zosterops japonicus made more also in Prunus jamasakura (Koike et al. 2008a). visits than these species, there were few visits or few Koike et al. (2008a) also indicate that most birds fruits eaten by these species and, when we consider removed P. jamasakura fruit during a period of time them as potentially quantitative seed dispersers (mul- when the proportion of black fruits increased in the tiplying the average number of fruits removed per tree crown. S. controversa exhibits a bicolor dis- visit by the frequency of visits) they may not have play, as in addition to its fruit changing color as they been effective dispersers of S. controversa seeds, mature, the pedicels redden. Willson and Thompson consequently, H. amaurotis was considered to be the (1982) suggested that a bicolor display may enhance main frugivore consuming S. controversa fruits at the fruit dispersal, particularly by juvenile birds, through study site. Both Eophona personata and Streptopelia increasing the level of attractiveness and reduc- orientalis also consume seeds , they are regarded as ing conspicuousness to invertebrate herbivores. S. seed predators (Yagihashi 2001; Yoshikawa et al.

126 Avian fruit removal behaviors

2009). If these species consumed fruits they may roll and fruit selection by birds in Japanese temperate the seed predators, but we did not observe these spe- forests has been documented for the first time, and cies consuming S. controversa fruit in this study. the practicality of using direct observation methods Very few previous studies have considered avian for studies of avian seed dispersal research in temper- visits to fruiting trees or the fruit removal behavior of ate forests has been demonstrated. Future research birds inhabiting Japanese temperate deciduous forests using direct observation is necessary during multiple (Masaki et al. 1994; Takanose & Kamitani 2003). years and of multiple trees of different species to Masaki et al. (1994) used many seed traps. Takanose clarify the effectiveness of birds in seed dispersal in and Kamitani (2003) compared the level of bird pop- Japanese temperate forests. ulations recorded by a line-census with the rates at which fruits disappeared. However, these methods ACKNOWLEDGMENTS did not allow detailed identification of bird species actually removing fruits; consequently it was not pos- We are grateful to N. Watanabe for his gracious coopera- sible to determine the numbers of fruit removed by tion. We also thank S. Kuwabara, M. Kuwabara, and the staff individual bird species. Thus this study may be the of FM Kusaki. We thank two anonymous referees for fruitful suggestions. This work was partly supported by a Grant-in Aid first to quantify fruit removal behavior by birds from for JSPS Fellows (20880012). woody plants with fleshy fruits in Japanese temperate forests. We estimated the amount of fruit removed by birds REFERENCES by comparing exposed branches to branches pro- Fukui AW (1996) Retention time of seeds in bird guts: tected by nylon nets. Birds removed only 11.5% of costs and benefits for fruiting plants and frugivorous fruit production. Previous work has demonstrated birds. Plant Spec Biol 11: 141–147. that only 3–11% of S. controversa seeds were dis- Herrera CM (1984) A study of avian frugivores, bird seminated by birds, and 17% of S. controversa seeds dispersed plants, and their interaction in Mediterra- were removed by birds (Tokui 1992; Masaki et al. nean scrublands. Ecol Monogr 54: 1–23. 1994). Takanose and Kamitani (2003) showed that Herrera CM, Jordano P, López-Soria L & Amat JA fruit removal rates for six fleshy-fruited plant species (1994) Recruitment of a mast-fruiting, bird-dispersed ranged from 16.4% to 85.5% and fruit removal rates tree: bridging frugivore activity and seedling estab- in fall-fruiting species differed greatly by tree species lishment. Ecol Monogr 64: 511–538. and from year to year. Herrera CM (1998) Long-term dynamics of Mediterra- S. controversa fruit are a food resource not only nean frugivorous birds and fleshy fruits: a 12-yr for birds, but for a range of mammals that include the study. Ecol Monogr 68: 511–538. Asiatic Black Bear Ursus thibetanus and the Japa- Herrera CM (2009) Multiplicity in Unity: Plant subindi- nese Macaque Macaca fuscata (Koike & Masaki vidual variation and interactions with animals. The 2008; Masaki et al. 2012). More than 80% of S. University of Chicago Press, Illinois. controversa fruits in the present study fell to the for- Howe HF (1986) Seed dispersal by fruit-eating birds est floor, thus a large proportion of fruit are available and mammals. In: Murray DR (ed) Seed Dispersal. for mammalian dispersal. To determine the relative pp 123–189. Academic Press, New York. Howe HF & Westley LC (1988) Ecological relation- importance of non-avian frugivores in the seed dis- ships of plants and animals. Oxford University Press, persal of S. controversa, it is necessary to account for New York. the fate of fallen fruit on the forest floor and to Ito C & Fujiwara K (2007) Habitat and ecological char- assemble quantitative data on the foraging activities acteristics of the alien species Ligustrum lucidum Ait. of other species groups for comparison with existing in urban forest in Japan–comparison with native data on the avian guild. Ligustrum species. Jpn J Conserv Ecol 12: 143–150 In general, some variations in fruiting phenology (in Japanese with English abstract). exist even between individual trees of the same spe- Jordano P (1982) Migrant birds are the main seed dis- cies, and from year to year. Because this study was persers of blackberries in southern Spain. Oikos 38: conducted on a single tree and during single year, it 183–193. is not appropriate to generalize from the results Jordano P (1995) Angiosperm fleshy fruits and seed obtained. However, the ways in which birds removed dispersers: a comparative analysis of adaptation and fruit were observed, the link between fruit quality constraints in plant-animal interactions. Am Nat 145:

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