Frugivores of Poisonous Herbaceous Plants Arisaema in the ...

77Frugivores of Poisonous Herbaceous Plants Arisaema spp.

Frugivores of Poisonous Herbaceous Plants Arisaema spp. (Araceae) in the Southern Kanto District, Central Japan

Tadashi Suzuki*† and Naoko Maeda*

Abstract. Plants of the genus Arisaema (Araceae) are poisonous perennial herbs that produce an assemblage of fruits similar in appearance to peeled cobs of maize (sweetcorn). Since the ripe fruits are bright orange-red and very conspicuous, it has been believed that birds eat the fruits and disperse the seeds. However, although there are many species of Arisaema in Japan, there is no detailed information on their frugivores. We used automatic cameras to ex-amine foraging on two species of Arisaema, A. limbatum and A. serratum, in secondary for-ests, mainly in Kanagawa Prefecture, southern Kanto District, central Japan. These species are very similar in appearance but their fruiting seasons differ: the former in midsummer, and the latter in autumn-winter. We discovered that for A. limbatum the Brown-eared Bulbul Hypsip-etes amaurotis was an exclusively important frugivorous bird in the study area. However, for A. serratum, several species ̶ the Brown-eared Bulbul, Red-flanked Bluetail Tarsiger cyanu-rus, Pale Thrush Turdus pallidus, Copper Pheasant Syrmaticus soemmerringii, Red-billed Leiothrix Leiothrix lutea, Scaly Thrush Zoothera dauma, Brown-headed Thrush T. chrysolaus and Daurian Redstart Phoenicurus auroreus ̶ ate the red fruits. Among them, the first four species were regarded as being major frugivores of A. serratum. Twelve mammal species were confirmed in close proximity to the fruits of Arisaema. We observed that the large Japanese field mouse Apodemus speciosus foraged the fruits of A. limbatus and ate seeds rather than the fleshy fruit pulp, and so appeared to be a seed predator rather than a seed disperser. No other mammals were observed taking the fruits of Arisaema.

Key words: Apodemus, Arisaema, Frugivore, Hypsipetes amaurotis, Tarsiger cyanurus.キーワード：アカネズミ属，テンナンショウ属，果実食者，ヒヨドリ，ルリビタキ．

Introduction

The genus Arisaema (Araceae) (ten-nan-sho or mamusi-gusa in Japanese, and cobra lily or Jack-in-the-pulpit in English) is a group of perennial herbaceous plants often present at the edges and floors of temperate forests in Japan. Although taxonomic studies on this group are still advancing, about 180 species are known worldwide, nearly 50 of which occur in Japan (Murata 2011).

Arisaema species are toxic plants harmful to mammals, primarily owing to the presence of calcium oxalate crystals (e.g., Veterinary medicine library, University of Illinois, http://www.library.illinois.edu/vex/toxic/jackpulp/jckpulp.htm; Knight & Walter 2001, Aganga et al. 2011). Therefore, Arisaema is considered as being generally unpalatable to herbivores (e.g.

77

山階鳥学誌（J. Yamashina Inst. Ornithol.），45: 77‒91, 2014 ©Yamashina Institute for Ornithology

Original Article （原著論文）

Received 16 July 2013, Revised 13 December 2013, 2nd Revision 21 January 2014, Accepted 23 January 2014.* Department of Biological Science, Tokyo Metropolitan University, Minami-ohsawa 1‒1, Hachioji, Tokyo

192‒0397, Japan.† Present address: Higashi-tawara 395‒19, Hadano, Kanagawa 257‒0028, Japan. E-mail: [email protected]

78 Tadashi Suzuki and Naoko Maeda

Tamura & Katsuyama 2007), and while usually occurring at low densities where present, it can become a predominant plant in overgrazed fields (Takatsuki 2009). The poisonous effects of Arisaema on wild birds and mammals are poorly understood, but the Wild Turkey Meleagris gallopavo was recorded to eat leaves of Arisaema (Meanley 1956), and the Asiatic black bear Ursus thibetanus is likely to normally consume leaves and stems of Arisaema (Hashimoto & Takatsuki 1997 and references therein, Koike 2010, Kudo-Hirotani & Naganawa 2010). It is uncertain whether other chemicals in Arisaema negatively influence birds and mammals in comparison with the influence on other creatures (Liu et al. 2012).

Arisaema produces small fleshy fruits (berries) that cluster at the fruiting spike and re-semble peeled cobs of maize (sweetcorn) in appearance (hereafter the assemblage is called an infructescence). When ripe, the fruits turn from green to bright orange-red (‘red’ hereafter) (Murata 2011). Since the red fruits of Ariasema are very conspicuous, at least to the human eye, it has been believed that birds eat Arisaema fruits and disperse the seeds (e.g. Renner et al. 2004).

However, reports of the frugivores of Arisaema are both scarce and fragmentary. In North America, where several Arisaema species occur, two bird species, the Grey Catbird Dumetella carolinensis (Bierzychudek 1982) and Wood Thrush Hylocichla mustelina (Schultz 2005), were noted as being frugivores of A. tryphyllum, although no data was given. Addition-ally, in captive feeding experiments, the Hermit Thrush Catharus guttatus consumed the fruits of A. tryphyllum (Johnson et al. 1985). In Japan, although many species of Arisaema occur, only a small number of bird species have been recorded as eating the fruits: the Common Pheasant Phasianus colchicus for A. tosaense (Kojima & Wada 1967), Naumann’s Thrush Turdus naumanni for Arisaema sp. (Kiyosu 1978a), the Daurian Redstart Phoenicurus auroreus for A. angustatum (Yahara 1988), and the Red-billed Leiothrix Leiothrix lutea for A. serratum (Tojo & Nakamura 1999). There is, to our knowledge, no quantitative study detailing the fru-givores of Arisaema, probably in part because of the difficulty of field observations.

In Japan, Arisaema is a taxonomically-diverse group, and the distributional ranges of many species tend to be locally restricted (Murata 2011). If the red ripe fruits of Arisaema are very conspicuous to frugivorous birds on the forest floor and are eaten by them, it is of inter-est to know which bird species are the main consumers. This is of importance because, de-pending on species-specific traits, birds as seed dispersers appear to affect in different ways the dispersal of Arisaema seeds both at small and large spatial scales (Jordano et al. 2007, Martinez et al. 2008). For instance, different species may differentially contribute to the movement of each seed from a mother plant to another site suitable for germination and growth, and migrating birds may affect, through long-distance seed dispersion, the population genetic structures and/or genetic differentiation among populations more so than resident ones.

In Japan, most terrestrial forest-dwelling mammals, except many of the Soricomorpha (the shrews and moles), eat some fruits (e.g. Ohdachi et al. 2009, Masaki et al. 2012). The low height of Arisaema, mostly less than 1 m and usually only several tens of centimetres tall (e.g. Murata 2011), means that these mammals can access and collect Arisaema fruits easily and readily if necessary. In fact, a Japanese macaque Macaca fuscata was once observed to pick a fruit of Arisaema in Kinka-zan Island (Izawa 2004) and in the U.S.A rodents (unspeci-


fied) were recorded as eating fruits of A. tryphyllum (Bierzychudek 1982). Therefore, to clari-fy whether or not Japanese mammals normally take fruits of Arisaema is of interest not only from the perspective of seed dispersers and/or seed predators of Arisaema, but also in terms of the interspecific relationships among fruit-eating birds, Arisaema and mammals, as was eluci-dated for the European holly Ilex aquifolium (Obeso 1998).

To address these shortcomings in knowledge regarding frugivory upon Arisaema, we studied the fruit-eating agents of two Arisaema species, A. limbatum and A. serratum, under natural conditions in the southern Kanto District, central Japan, using data obtained from au-tomatic cameras. We also made general observations on both species in the study areas.

Methods

Focal species of ArisaemaWe focused on two species of Arisaema, A limbatum (mimigata-ten-nansho in Japanese)

and A. serratum (kanto-mamushi-gusa). Both occur naturally in the lowland of Kanto District, central Japan (Murata 2011), where we conducted the present study. Although similar in gen-eral morphological appearance and the form and size of their fruits, these two species differ in the fruiting season when red ripe, fleshy fruits are present: midsummer in A. limbatum, and the autumn-winter in A. serratum.

Study areasWe conducted this study mainly on the southern forested foothills of the Tanzawa Moun-

tains, Hadano, Kanagawa (around 35°25′N, 139°12′E, alt. ca. 200 m to 500 m), in southern Kanto District, and secondarily in the forest area at Field Museum Tama Hills of Tokyo Uni-versity of Agriculture and Technology, Hachioji, Tokyo (35°38′N, 139°23′E, alt. ca. 160 m). The study areas consist primarily of artificial secondary forests (so-called Satoyama in Japa-nese), which comprise mainly patches of sugi Cryptomeria japonica and/or hinoki (Japanese cypress) Chamaecyparis obtusa plantations of various ages, and mixed deciduous and ever-green woodland containing oaks Quercus spp., maples Acer spp., cherries Prunus spp., horn-beams Carpinus spp., and giant dogwoods Swida controversa. The forest floor was covered with various herbaceous plants (e.g. dwarf-bamboo Pleioblastus chino) and shrubs (e.g. Japa-nese laurel Aucuba japonica), but was usually poorly developed at the study sites owing to forestry management and/or grazing by large mammals, such as the sika deer Cervus nippon.

Appendix 1 lists bird species recorded during the study period in and near the study sites in Hadano. A list of the bird species occurring at Field Museum Tama Hills is given in Maeda et al. (1995), although an introduced species, the Chinese Hwamei Garrulax canorus has since been newly recorded and has become common there in summer (Togo et al. 2012). Overall, species compositions of both study areas were similar. The species of mammals in the two study areas were recorded directly. Scientific names of birds and mammals follow the Ornithological Society of Japan (2012) and Ohdachi et al. (2009), respectively.

MethodsWe studied A. limbatum in the summers of 2009‒2011 in Hadano, and A. serratum in the


autumn-winter of 2008 in Tama Hills, and in the autumn of 2009 to early spring of 2013 in Hadano. We searched extensively for Arisaema within the study areas, and found them mainly at forest edges and on relatively well-illuminated forest floors. We examined the reproductive state of discovered plants at roughly one-week intervals. Distributions of both species general-ly overlapped in Hadano, although A. serratum tended to be in slightly higher parts of the foothills.

We used automatic cameras to record foraging upon Arisaema. A camera was positioned 0.6 to 2.5 m in front of targeted wild plants which had red ripe fruits or green unripe but full-grown fruits, and remained there recording until the disappearance of most if not all fruits. Plants and cameras were checked at roughly one-week intervals. The height of plants and the size, number and condition of fruits, environmental conditions of growing sites, timing and duration of camera-setting (mostly longer than two weeks), and the kind of cameras used var-ied depending on the individual plants. No baits were used to attract animals.

Three kinds of automatic camera were used in this study: FieldNote II (film camera, sen-sitive to infrared rays) by Marif Co., Ltd., Japan; BirdWatchCam (digital camera, sensitive to moving warm objects); and GardenWatchCam (time-lapse digital camera, set to record at one-minute intervals) by Brinno Inc., USA. Each camera had different characteristics and func-tions, and owing to their respective shortcomings, we were unable to take photographs of ev-ery animal approaching Arisaema: (1) We were able to use FieldNote II to take photographs in the daytime and nighttime, but not BirdWatchCam and GardenWatchCam, which function only in the daytime (light condition); (2) We could not take photographs of animals, especial-ly smaller ones, partly because of their quick movements compared to the delayed response of the cameras (in particular, FieldNote II); (3) Many photographs were false positives, triggered by passing rays of sunlight and/or the movement of warm objects. This wastage of film often resulted in a dramatic reduction in the amount of film or SD media available (FieldNote II and BirdWatchCam); (4) We took photographs at fixed intervals (GardenWatchCam), or the cam-era was set to not respond for two minutes after taking a shot (FieldNote II). Because the cam-eras occasionally did not respond even when there were foraging animals present, data ob-tained was not comprehensive.

Although the photographic data obtained by different cameras was not always equiva-lent, we nevertheless used pictured photographs as data without distinguishing among camera sources, especially between BirdWatchCam and GardenWatchCam.

We examined approaching and/or foraging animals using photographs. Animals were photographed when on Arisaema or in its close vicinity, normally within a range of about 50 cm from Arisaema in birds and smaller mammals, and about 1 m in larger mammals. It was, however, difficult in general to photograph the animals actually collecting/eating fruits.

We considered animals to have collected (taken or eaten) fruits when: (a) they either held a fruit in the mouth or exhibited a posture of picking or eating it, or (b) when the successive photographs of animals indicated the disappearance of one or more visible fruits during their stay. Otherwise, we categorized animals conservatively as being close to fruits, even when they were on the plants bearing fruits and probably took the fruits.

We utilized photographic records to count the number of approaches by animals to Arisaema. When two pictures of animals were taken consecutively within less than 5 min., we


considered the animal as being the same individual and counted the number of approaches as one. In most cases, only a single bird or mammal was recorded, although rarely, two birds vis-ited a plant together; this was also regarded as a single approach. We also counted the number of times of fruit collecting (eating) as one when an animal took fruits during one visit, even when it collected successively several fruits during the visit. Owing to the difficulties in counting the actual number of fruits eaten, data were examined mainly from the perspective of how many times the targeted plants were visited and utilized by frugivores.

Results

Fruiting seasons and fruit sizes of Arisaema limbatum and A. serratumBrief general observations of both species in the study area (Hadano) were as follows: In

A. limbatum, a stem and peduncle supporting the infructescence (i.e., fruits) stood nearly up-right above the ground throughout a fruiting season (summer). In contrast, in A. serratum it mostly fell down on the ground in a fruiting season (autumn-winter), even when many or all ripe fruits were still attached to the infructescence, the fruits being virtually on the ground. Normally, ripe fruits of both species remained attached to the mother plant until some agents removed them. The mean height from the ground to the tip of an infructescence was 58.7 cm (s.d.＝20.3, n＝35) for A. limbatum and 72.7 cm (s.d.＝22.3, n＝11) for A. serratum.

Each female plant of A. limbatum bore roughly 100 fruits per infructescence (mean＝85.8, s.d.＝23.1, n＝22). Red ripe fleshy fruits appeared in mid-July in the study fields. In 2010, for example, on 10 July only six of 40 (15.0％) plants bearing fruits had red fruits, but by 24 July 36 of 40 (90.0％) had red fruits. Color change of the individual fruits from green to red took only three days at most (n＝33 fruits), and occurred asynchronously, usually resulting in a mixture of green (unripe) and red (ripe) fruits on the same infructes-cence. Fresh fruits were globular and 8.6 mm (s.d.＝1.4, n＝20) in mean width (measured as the horizontal diameter of the fruit); fruit sizes generally varied much both among and within individual plants. Red fruits usually began to disappear some days after achieving coloration, and most if not all fruits had been removed from the infructescence by mid to late August, ex-cepting some individual plants with many fruits which remained up to early September. Green unripe fruits rarely disappeared from the infructescence.

A. serratum bore about 100‒200 fruits per infructescence (mean＝152.4, s.d.＝38.3, n＝8), significantly more than A. limbatum (t-test, P＜0.05). The red ripe fruits resemble those of A. limbatum, and at the study areas, emerged in October to November. In 2012, for example, on 21 October none of seven 7 (0％) plants bore red fruits, but by 5 November, five of them (71.4％) bore red fruits. Red fruits emerged asynchronously on the same infructes-cence, as seen in A. limbatum, though we did not examine the time necessary for color change of each fruit. They disappeared gradually in the same year, excepting some plants where most if not all fruits remained until January to February the following year. The mean width (hori-zontal diameter) was 9.4 mm (s.d.＝1.8, n＝50), and fruit size generally varied greatly both among and within individual plants. The fruit size tended to be slightly larger in A. serratum than in A. limbatum, though the mean widths were not significantly different (t-test, P＞0.25).


Frugivores of A. limbatumA total of 46 plants were monitored using camera-trapping. Table 1 shows the species

composition of birds and mammals camera-trapped and their fruit foraging. Additionally, illustrative photographs are presented in Appendix 2A.

For birds, four species (the Brown-eared Bulbul Hypsipetes amaurotis, Chinese Hwamei, Japanese Bush Warbler Cettia diphone and Blue-and-White Flycatcher Cyanoptila cyanomelana) were recorded as being close to A. limbatum in the daytime, and one species, the Eurasian Woodcock Scolopax rusticola, at night. Among these birds, only the Brown-eared Bulbul visited frequently and collected fruits actively (Table 1, Appendix 2A). All fruits taken by the Brown-eared Bulbul were red in color. We found bird’s feces, seemingly of the Brown-eared Bulbul, on a leaf of A. limbatum visited by this species. It contained an intact seed of Arisaema, undoubtedly A. limbatum because no other Arisaema species bore fruits at that time in the study area.

Four other bird species were recorded only once (Table 1). Among these, the Eurasian Woodcock and Japanese Bush Warbler were likely incidentally passing by A. limbatum rather than actively seeking it, judging from their positions and postures. One male Blue-and-White Flycatcher was photographed standing on the infructescence and one Chinese Hwamei was recorded near a plant. However, neither were likely to have collected fruits because no fruits disappeared.

For mammals, eight species were recorded close to A. limbatum, mainly at night (Table

Table 1. Animal species and the number of individuals camera-trapped in the proximity of Arisaema limbatum with ripe fruits at Hadano, Kanagawa Pref., in the summers of 2009‒2011.

Species camera-trapped

Camera I (FN) Daytime and night-time

N＝22

Camera II (BR) Daytime only

N＝24

n c f n c f

Birds Eurasian Woodcock Scolopax rusticola 1 1 0Brown-eared Bulbul Hypsipetes amaurotis 11 29 1 19 123 96Japanese Bush Warbler Cettia diphone 1 1 0Chinese Hwamei* Garrulax canorus 1 1 0Blue-and-white Flycatcher Cyanoptila cyanomelana 1 1 0

Mammals Japanese Macaque Macaca fuscata 1 1 0Large Japanese Field Mouse Apodemus speciosus 11 45 10Raccoon Dog Nyctereutes procyonoides 1 1 0Asiatic Black Bear Ursus thibetanus 1 1 0Japanese Badger Meles anakuma 7 14 0 1 1 0Masked Palm Civet* Paguma larvata 1 2 0 2 3 0Wild Boar Sus scrofa 3 4 0 1 1 0Sika Deer Cervus nippon 2 2 0

*Introduced speciesFN : FieldNote, Marif, and BR: BirdWatchCom and GardenWatchCom, Brinno.N : Total number of observed individuals of A. limbatum.n : Number of plants where respective animal species were camera-trapped.c : Number of times where animals were camera-trapped in the proximity of the plants.f : Number of times where animals were ascertained to forage fruits, based upon photographs.


1). Among them, the large Japanese field mouse Apodemus speciosus came most frequently, and was recorded taking red fruits of A. limbatum (Table 1, Appendix 2A), climbing the plant to reach the fruit. We recorded the Brown-eared Bulbul and the large field mouse visiting the same infructescence in the daytime and at night, respectively (Appendix 2A), indicating that disappearance of fruits is not necessarily due to foraging by birds only.

Rarely, we found the remains of gnawed fruits on the ground near A. limbatum (Appen-dix 2A). These comprised red and/or green fruit skins with pulp, and sometimes also small fragments of seed coats, indicating some foragers to eat the seeds but not the fruit pulp.

We attached a fresh infructescence containing both green and red fruits to one A. limbatum, the original fruits of which had all disappeared, and recorded the large Japanese field mouse taking both red and green fruits, and to leave remains as described above (data not included in Table 1). In preliminary tests with caged mice, we also observed them to eat seeds removed from fruits by themselves, and to rarely eat fruit pulp in addition to seeds (unpublished). These observations indicate that the large Japanese field mouse eats seeds rather than fruit pulp of A. limbatum.

None of the seven other mammal species recorded (Table 1) were observed to take fruits of A. limbatum, even when in close proximity.

Frugivores of A. serratumWe monitored three plants in Hachioji and 18 plants in Hadano. In autumn 2008 at Hachi-

oji, we camera-trapped one bird species, the Chinese Hwamei (6, where the numeral in paren-theses is the number of approaches), and four species of mammals: the field mouse Apodemus sp. (1), Japanese hare Lepus brachyurus (10), raccoon dog Nyctereutes procyonoides (7) and Japanese badger Meles anakuma (1). However, none of these was recorded taking any fruits from monitored plants. Table 2 shows the birds and mammals camera-trapped in Hadano. Of the 15 bird species recorded, eight (the Copper Pheasant Syrmaticus soemmerringii, Brown-eared Bulbul, Red-billed Leiothrix Leiothrix lutea (introduced species), Scaly Thrush Zoo-thera dauma, Pale Thrush Turdus pallidus, Brown-headed Thrush T. chrysolaus, Red-flanked Bluetail Tarsiger cyanurus and Daurian Redstart) took red fruits from the infructescence (Table 2, Appendix 2B).

The bird species that most-frequently visited and took fruits were the Brown-eared Bul-bul, Red-flanked Bluetail, Pale Thrush and Copper Pheasant (Table 2). The Red-billed Leio-thrix collected fruits, but repeatedly did so only from one A. serratum. A wintering flock of this species was present in the vicinity and it is probable that different group members visited in turn. We did not record the Red-billed Leiothrix as foraging upon A. serratum fruits at other locations.

For mammals, we recorded all species found in Hachioji, and 10 or 11 species in Hadano (Table 2). In the survey of A. serratum in Hadano we recognized two species of Apodemus, the large Japanese field mouse and small Japanese field mouse A. argenteus. However, owing to the presence of smaller individuals of the large Japanese field mouse, it was not always easy to separate the two species. Therefore, they were grouped together as the field mouse Apodemus spp. in Table 2.

Camera-trapped mammals, in particular the field mouse, were often observed close to the


fruits of A. serratum lying on the ground. Two individuals of the large Japanese field mouse were recorded eating the fruits. However, no other mammals took the fruits, even when close proximity to them (Table 2), e.g. one Japanese hare foraged upon grasses while almost step-ping on a cluster of red fruits on the ground.

Discussion

Frugivorous birdsOnly the Brown-eared Bulbul frequently visited and took the fruits of A. limbatum (Table

1), and this species was therefore the predominant, if not the sole, fruit-eater of A. limbatum in the study area in summer.

The Brown-eared Bulbul is one of the commonest birds in many temperate forests in Ja-

Table 2. Animal species and the number of individuals camera-trapped in the proximity of Arisaema serratum with ripe fruits at Hadano, Kanagawa Pref., in the autumn-winter periods of 2010‒2012.

Species camera-trapped

Camera I (FN) Daytime and night-time

N＝14

Camera II (BR) Daytime only

N＝4

n c f n c f

Birds Copper Pheasant Syrmaticus soemmerringii 4 13 4Oriental Turtle Dove Streptopelia orientalis 2 3 0Japanese Pygmy Woodpecker Dendrocopos kizuki 1 1 0Japanese Green Woodpecker Picus awokera 1 1 0Eurasian Jay Garrulus glandarius 1 2 0Japanese Tit Parus minor 4 4 0Brown-eared Bulbul Hypsipetes amaurotis 5 16 9 2 13 11Red-billed Leiothrix* Leiothrix lutea 1 7 7Scaly Thrush Zoothera dauma 1 1 1Pale Thrush Turdus pallidus 4 13 3 1 2 2Brown-headed Thrush Turdus chrysolaus 1 3 1Red-flanked Bluetail Tarsiger cyanurus 7 34 14 2 3 2Daurian Redstart Phoenicurus auroreus 2 7 0 1 1 1Black-faced Bunting Emberiza spodocephala 2 14 0Grey Bunting Emberiza variabilis 1 1 0

Mammals Field Mouse# Apodemus spp. 10 52 2Japanese Squirrel Sciurus lis 3 4 0Japanese Hare Lepus brachyurus 2 3 0Red Fox Vulpes vulpes 1 1 0Raccoon Dog Nyctereutes procyonoides 2 2 0Japanese Marten Martes melampus 1 1 0Japanese Badger Meles anakuma 2 5 0Masked Palm Civet* Paguma larvata 1 2 0Wild Boar Sus scrofa 1 6 0Sika Deer Cervus nippon 1 1 0

*Introduced species#Including Apodemus speciosus and possibly A. argenteus.Abbreviations (FN, BR, N, n, c and f) are as in Table 1.


pan (Ueta et al. 2011) including our study areas, and is a generalist fruit-eater and seed-dis-perser (e.g. Fukui 1995, Yoshikawa et al. 2009). Since the Brown-eared Bulbul eats various kinds of fruits, A. limbatum may be merely one of many food plants for this species. Never-theless, it is most probable that the Brown-eared Bulbul undertakes exclusively the fruit con-sumption and dispersion of seeds of A. limbatum. If so, evolutionary theory would suggest that A. limbatum may have some specific characteristics that enhance the attraction of the Brown-eared Bulbul. For instance, the fruiting period of A. limbatum in the midsummer (mid July to mid or late August) may correspond to the life history of the Brown-eared Bulbul, as below.

The breeding season of the Brown-eared Bulbul continues until late July or early August in the study area. Thus, in addition to adults, there are undoubtedly many young birds search-ing for food, including fruits, at that time. In midsummer in temperate Japan, fleshy-fruited plants available for the frugivorous birds are relatively few (Kominami et.al. 2003, Takanose & Kamitani 2003, Masaki et al. 2012). In such circumstances, the Brown-eared Bulbul may readily find and consume the ripe red fruits of A. limbatum which, in turn, may be able to de-crease competition over seed dispersers with other fleshy-fruited plants by producing ripe fruits in that season.

In contrast, several birds visited and took the fruits of A. serratum that ripened in mid to late autumn (Table 2). The Brown-eared Bulbul, Pale Thrush, Red-flanked Bluetail and Copper Pheasant were relatively frequent visitors taking fruits. Other species, such as the Scaly Thrush, Brown-headed Thrush and Daurian Redstart, were observed to come close to and took fruits less frequently, though this is possibly due to the birds being at a low population level (Scaly Thrush), passage migrants (Brown-headed Thrush) or outside their usual habitats (Daurian Redstart). All of above-mentioned species consume various kinds of fruits (e.g. Kiyo su 1978a, b, Yoshikawa et al. 2009) and various species of birds take the fruits of A. serratum. There may not be a close relationships between A. serratum and a particular bird species.

The Red-billed Leiothrix is a frugivorous bird both in its native and introduced lands (Corlett 1998, Tojo & Nakamura 1999) and in this study took fruits of A. serratum, as noted also at other locations by Tojo & Nakamura (1999). While it remains uncertain whether their frugivory on A. serratum is common, the Red-billed Leiothrix may be viewed as a new con-sumer of Arisaema fruits in Japan.

The mean fruit sizes of A. limbatum and A. serratum were 8.6 and 9.1 mm, respectively, which is within the range of edible sizes for medium-sized bird species such as the Brown-eared Bulbul and the Pale, Scaly, and Brown-headed Thrushes (mean values of the gape width ＞10.0 mm; Fukui 1995, Yoshikawa et al. 2009, Hamao et al. 2010, Kaneko et al. 2012). However, for small-sized birds such as the Red-billed Leiothrix, Red-flanked Bluetail and Daurian Redstart (mean gape values ＜8.0 mm for the latter two species; Hamao et al. 2010, Kaneko et al. 2012), the mean fruit sizes of A. limbatum and A. serratum are likely rather large. These small-sized passerines may tend to select smaller fruits from the assemblage of the fruits on the infructes-cence of A. serratum, or may be able to gulp large fruits relative to their gape size, as suggested for the Red-flanked Bluetail (Hamao et al. 2010).

Among the birds foraging upon A. serratum, the Copper Pheasant may occupy a distinct position. This species inhabits forest areas and is largely herbivorous, but also consumes in-


vertebrates (Ogasawara 1968, Kiyosu 1978b, Yamaguchi & Kawaji 2003, Kawaji & Yokoya-ma 2009, Yoshikawa et al 2009). After ingestion, the Copper Pheasant grinds its foods in the gizzard, rather than gulping items down intact, and is therefore a seed-predator rather than a seed-disperser (Yoshikawa et al 2009). However, it is unknown whether it is a seed-predator or seed-disperser for A. serratum. If a seed-predator, it may at times negatively impact the fruiting A. serratum, because it is a large bird and would be able to kill many if not most seeds that it ingests. Conversely, when the Copper Pheasant defecates at least a portion of relatively intact seeds and is so able to serve as a seed-disperser, it may have a positive effect on the seed dispersion of A. serratum. The Copper Pheasant forages widely across the forest floor within a habitat where herbaceous plants are able to survive and grow well, resulting in the mass seed dispersal into a good growing habitat. The Copper Pheasant is presently not com-mon in Japan, but seems to have previously been abundant in forest areas (Brazil 1991). The ecological relationships between this species and Arisaema may have formerly been stronger than at present.

The species composition of birds taking fruits of A. limbatum and A. serratum differed greatly, mainly owing to the difference in their fruiting season. The Brown-eared Bulbul is a resident breeder and is present in the study area throughout the year (Appendix 1, pers. obs.), the winter population including both resident and migrant individuals. This enables the Brown-eared Bulbul to consume both the fruits of A. limbatum in summer and A. serratum in autumn-winter. Though the Scaly Thrush appears to also inhabit the study area both in sum-mer and winter (Appendix 1), it seems very rare (pers. obs.) and at present we have no record of its consumption of A. limbatum.

Conversely, excepting the Brown-eared Bulbul and the Scaly Thrush in part, the birds foraging upon the fruits of A. serratum were winter visitors or temporary transients in the study area. Therefore, they can take only the fruits of A. serratum, but not A. limbatum, in the study area.

Among fruit-eating birds recorded in the study area (Appendix 1), medium to large sized species such as the Common Pheasant Phasianus colchicus, Oriental Turtle Dove Streptopelia orientalis, Japanese Green Woodpecker Picus awokera, Japanese Green Pigeon Treron siebol-dii and Eurasian Jay Garrulus glandarius, are also plausible candidates to eat fruits of A. lim-batum and/or A. serratum. Of these, only the Common Pheasant and Japanese Green Pigeon were not observed in the close vicinity of Arisaema, but none of these species were observed collecting Arisaema fruits. The introduced Chinese Hwamei is a fruit-eating species (Corlett 1998, Togo et al. 2012) and another probable candidate for a fruit-eater of Arisaema. It was present intermittently in the study area throughout the year, but was not recorded taking the fruits of Arisaema. Even if the above species did take fruits of Arisaema, the amount is likely negligible.

Frugivorous mammalsOwing to difficulties in accurate differentiation between the two Apodemus field mouse

species at the site, we are unclear as to whether only one or both were frugivores of Arisaema. However, it was clear that a total of 12, perhaps 13, species which consume fruits to varying degrees (Ohdachi et al. 2009) were recorded in the proximity of Arisaema fruits (Tables 1 &


2). Among them, a regular consumer was the large Japanese field mouse (Table 1), which for-aged upon both red and green fruits of A. limbatum by climbing the plant. This mouse con-sumed Arisaema seeds rather than fruit pulp and so behaved as a seed predator rather than a seed disperser. It is unknown whether it sometimes stored the fruits or seeds of Arisaema, which may result in the dispersion of surviving seeds in some cases.

It is likely that seed predation by field mice strongly affects Arisaema recruitment rates. Some fruit/seed traits of Arisaema may have evolved partly not only to facilitate seed disper-sion by birds, but also to decrease seed predation by mice. If it had no traits to deter fruit/seed consumption by field mice, the mice would be able to consume the fruits/seeds before birds located and foraged upon them, especially A. serratum lying on the ground. If so, it is plausi-ble that the field mice prefer the fruits of A. serratum less than A. limbatum. Our observations suggest this possibility. The proportion of approaches that resulted in seed predation was rela-tively small in A. serratum (2/52) compared with A. limbatum (10/45) (Tables 1 & 2), though the difference was only marginally significant (Chi-square test, P＝0.055, one-tailed). Further study that considers other factors, such as the species composition of the mice and the avail-ability of other foods, is warranted.

Of the 12 mammal species observed, only the large Japanese field mouse took the fruits of Arisaema. Others did not take the fruits. It is difficult to judge from the fieldwork whether they ignored it or did not recognize the presence of the fruits. We suppose that they may rec-ognize the fruits but regard the fruit pulps or the infructescence as being those of poisonous unpalatable plants. The Asiatic black bear is known to eat leaves and stems of Arisaema (Hashimoto & Taka tsuki 1977 and references therein, Koike 2010, Kudo-Hirotani & Naganawa 2010). However, it is unclear whether or not it takes the fruits, or infructescence, of Arisaema, even if the bear is likely to eat fruits.

Acknowledgements

We thank Takashi Sugawara, Shinsuke Sakamoto and Eri Miyazawa for their helpful in-formation and Hiroshi Hara for permitting the survey at Field Museum Tama Hills of Tokyo University of Agriculture and Technology.

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南関東地方における有毒草本植物テンナンショウ属の果実食者

テンナンショウ属Arisaema（サトイモ科Araceae）は良く目立つ鮮紅色の集合果（果実序）を生産する。本属の果実は鳥によって摂食され，その種子は鳥によって散布されると考えられている。しかしテンナンショウ属の種が多数知られている日本でも，その果実食者（種子散布者）についての詳しい調査は未だ行われていない。著者らは，南関東低地で生育するミミガタテンナンショウA. limbatumとカントウマムシグサA. serratumを対象にして，自動撮影カメラを利用してその主要な果実食者を調査した。ミミガタとカントウは植物本体や果実の形状・サイズなど似通っているが，前者では夏季の7‒8月に，後者では秋10月以降に鮮紅色の成熟果実が出現するという違いがある。調査は2008‒2013年の期間に東京都八王子市内（多摩丘陵）と神奈川県秦野市内（丹沢山麓）の二次林で行われた。なお結果的に資料は概ね後者で得られている。ミミガタの果実を採取した鳥はヒヨドリHypsipetes amaurotis 1種であった。ヒヨドリは本種にとって最重要な果実食者と見なせた。このほかアカネズミApodemus speciosusも果実を採取するのを確認した。本種は果実というより種子を摂食していた。一方，カントウでは8種の鳥が果実食者として記録された。そのうち主要と思われるのはヒヨドリ，ルリビタキTar-siger cyanurus，シロハラTurdus pallidusおよびヤマドリSyrmaticus soemmerringiiの4種であった。他の4種はソウシチョウLeiothrix lutea（外来種），トラツグミZoothera dauma，アカハラ T. chrysolaus，ジョウビタキPhoenicurus auroreusである。またそれ以外にアカネズミ属の個体による採食も記録された。

鈴木惟司*・前田尚子：首都大学東京理工学研究科生命科学，〒192‒0397 東京都八王子市南大沢1‒1．

* 現住所：〒257‒0028 神奈川県秦野市東田原395‒19．


Appendix 1. Bird species recorded in and near the study sites at Hadano, Kanagawa Pref., in 2009‒2013. Some species flying above the forest were included. Absence of records was considered mainly due to the seasonal movements/migrations of the birds in the area. The species names and arrangement follow the Ornithological Society of Japan (2012), excepting the addition of introduced species. Records of the consumption of vegetable foods (fruits and/or seeds) are cited from Kiyosu 1978a, b, Nakamura & Nakamura 1995, Corlett 1998, and Kaneko et al. 2012.

Species recorded Season Vegetable foods (fruits and/or seeds)Family Common name Scientific name Summer

Jun-AugWinter

Oct-Mar

Phasianidae Chinese Bamboo Partridge* Bambusicola thoracicus ○ ○ ＋Copper Pheasant Syrmaticus soemmerringii ○ ＋Common Pheasant Phasianus colchicus ○ ○ ＋

Columbidae Oriental Turtle Dove Streptopelia orientalis ○ ○ ＋Japanese Green Pigeon Treron sieboldii ○ ○ ＋

Cuculidae Rufous Hawk-Cuckoo Hierococcyx hyperythrus ○Lesser Cuckoo Cuculus poliocephalus ○

Scolopacidae Eurasian Woodcock Scolopax rusticola ○ ＋Accipitridae Black Kite Milvus migrans ○

Northern Goshawk Accipiter gentilis ○Common Buzzard Buteo buteo ○ ○

Picidae Japanese Pygmy Woodpecker Dendrocopos kizuki ○ ○ ＋Great Spotted Woodpecker Dendrocopos major ○ ＋Japanese Green Woodpecker Picus awokera ○ ○ ＋

Monarchidae Japanese Paradise Flycatcher Terpsiphone atrocaudata ○Laniidae Bull-headed Shrike Lanius bucephalus ○ ○ ＋Corvidae Eurasian Jay Garrulus glandarius ○ ○ ＋

Large-billed Crow Corvus macrorhynchos ○ ○ ＋Paridae Varied Tit Poecile varius ○ ○ ＋

Coal Tit Periparus ater ○ ＋Japanese Tit Parus minor ○ ○ ＋

Hirundinidae Barn Swallow Hirundo rustica ○Asian House Martin Delichon dasypus ○

Pycnonotidae Brown-eared Bulbul Hypsipetes amaurotis ○ ○ ＋Cettiidae Japanese Bush Warbler Cettia diphone ○ ○ ＋

Asian Stubtail Urosphena squameiceps ○ ＋Aegithalidae Long-tailed Tit Aegithalos caudatus ○ ○ ＋Phylloscopidae Eastern Crowned Leaf Warbler Phylloscopus coronatus ○Zosteropidae Japanese White-eye Zosterops japonicus ○ ○ ＋Timaliidae Chinese Hwamei* Garrulax canorus ○ ○ ＋

Red-billed Leiothrix* Leiothrix lutea ○ ＋Troglodytidae Eurasian Wren Troglodytes troglodytes ○ ＋Sturnidae White-cheeked Starling Spodiopsar cineraceus ○ ○ ＋Cinclidae Brown Dipper Cinclus pallasii ○ ○Muscicapidae Scaly Thrush Zoothera dauma ○ ○ ＋

Pale Thrush Turdus pallidus ○ ＋Brown-headed Thrush Turdus chrysolaus ○ ＋Naumann’s Thrush Turdus naumanni ○ ＋Red-flanked Bluetail Tarsiger cyanurus ○ ＋Daurian Redstart Phoenicurus auroreus ○ ＋Narcissus Flycatcher Ficedula narcissina ○ ＋Blue-and-white Flycatcher Cyanoptila cyanomelana ○ ＋

Prunellidae Japanese Accentor Prunella rubida ○ ＋Passeridae Eurasian Tree Sparrow Passer montanus ○ ○ ＋Motacillidae Grey Wagtail Motacilla cinerea ○ ○

Japanese Wagtail Motacilla grandis ○ ＋Fringillidae Oriental Greenfinch Chloris sinica ○ ○ ＋

Eurasian Siskin Carduelis spinus ○ ＋Eurasian Bullfinch Pyrrhula pyrrhula ○ ＋Japanese Grosbeak Eophona personata ○ ○ ＋

Emberizidae Meadow Bunting Emberiza cioides ○ ○ ＋Rustic Bunting Emberiza rustica ○ ＋Black-faced Bunting Emberiza spodocephala ○ ＋Grey Bunting Emberiza variabilis ○ ＋

*Introduced species.


Appendix 2. Photographs showing Arisaema and frugivores.(A) Arisaema limbatum. Upper (left to right): an automatic camera (BirdWatchCam), and Hypsipetes amaurotis

and Apodemus speciosus holding a fruit. Lower: remains of fruits considered to have been foraged by mice, and H. amaurotis and A. speciosus visiting the same A. limbatum in the daytime and at night, respectively.

(B) A. serratum. Upper: Syrmaticus soemmerringii, H. amaurotis, Zoothera dauma. Lower: Turdus pallidus, Tarsiger cyanurus and Phoenicurus auroreus. All individuals in the pictures collected fruits.

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