Seabirds As Adhesive Seed Dispersers of Alien and Native Plants in the Oceanic Ogasawara Islands, Japan

Biodivers Conserv (2012) 21:2787–2801 DOI 10.1007/s10531-012-0336-9

ORIGINAL PAPER

Seabirds as adhesive seed dispersers of alien and native plants in the oceanic Ogasawara Islands, Japan

Yukiko Aoyama • Kazuto Kawakami • Satoshi Chiba

Received: 23 January 2012 / Accepted: 12 July 2012 / Published online: 25 July 2012 Ó Springer Science+Business Media B.V. 2012

Abstract Previous studies have shown that the dispersal of plant seeds to oceanic islands is largely attributable to birds. However, few studies have assessed the role of adhesive dispersal by birds even though this mechanism has long been recognized as a major vector of seed transport. Some data point to the possibility that adhesive transport by seabirds transfers alien plant seeds in island ecosystems. In the present study, we examined the seed-dispersing ability of seabirds among islands in the oceanic Ogasawara Islands, Japan. We used capture surveys to examine the frequency of seeds adhering to seabirds and tested the salt tolerances of the seeds. The distributions of the plant species were examined and the relationships between plant and seabird distributions were analyzed using generalized linear models. Seeds of nine plant species, including aliens, were detected on 16–32 % of captured seabirds. Seeds included those generally considered to be dispersed by wind or internally transported by birds in their guts. Seeds exposed to NaCl solution isotonic with seawater for up to 8 h suffered little or no loss of viability. Analyses of plant distributions demonstrated positive relationships between the distributions of some plants and seabirds. These results show that seabirds effectively disperse seeds of both native and introduced plant species. This is the ﬁrst study to comprehensively assess adhesive seed dispersal by seabirds; it provides essential information on long-distance dispersal.

Keywords Epizoochory Á Island ﬂora Á Long-distance dispersal Á Oceanic islands Á Alien species Á Seabirds

Electronic supplementary material The online version of this article (doi:10.1007/s10531-012-0336-9) contains supplementary material, which is available to authorized users.

Y. Aoyama (&) Á S. Chiba Graduate School of Life Sciences, Tohoku University, Aobayama, Sendai, Miyagi 980-8578, Japan e-mail: [email protected]

K. Kawakami Forestry and Forest Products Research Institute, Matsunosato 1, Tsukuba, Ibaraki 305-8687, Japan 123 2788 Biodivers Conserv (2012) 21:2787–2801

Introduction

Oceanic islands are islands that have had no previous connection to a continental land mass from which their current biota could have been derived (MacArthur 1972). Due to the biogeographical isolation of oceanic islands, the species that live on them must have arrived by long-distance dispersal. Carlquist (1974) suggested air flotation, oceanic drift, and birds as long-distance dispersal agents of plants, and estimated the modes of dispersal likely to have resulted in the present native floras of Pacific islands. On the Hawaiian Islands, which are remote oceanic islands, seed dispersal by birds has been the most important mechanism accounting for 74.8 % of immigrants. About half of the immigrants by birds were transported internally (in their guts) and the rest by seed adherence to feathers or feet (Carlquist 1974). Frugivorous land birds are well-known seed dispersal agents and their ability has been examined by many researchers (e.g., Howe and Primack 1975; Sorensen 1981; Moermond and Denslow 1983; Herrera 1984; Sorensen 1984). In contrast, the number of factual reports on adhesive dispersal by birds is very small and mostly focused on waterbirds in wetlands (Vivian-Smith and Stiles 1994; Figuerola and Green 2002; Brochet et al. 2010), particular plant species (Walker 1991; Burger 2005), or incidental observations (Chapman 1891; Taylor 1954; Carlquist 1974; Godley 1985), even though this mode of transport has long been recognized as a major vector of seed dispersal (Darwin 1859; Falla 1960; Carlquist 1966; van der Pijl 1972; Carlquist 1974; Sorensen 1986; Godley 1989; Morton and Hogg 1989). Early and more recent authors have reported seed adhesion to seabirds (Chapman 1891; Taylor 1954; Carlquist 1974; Godley 1985; Walker 1991; Burger 2005). Seabirds have the potential to be effective vectors of seeds, particularly on biogeograph- ically isolated oceanic islands, because of their extensive flying abilities and large population sizes at the breeding sites (Falla 1960). The aim of this study was to determine the roles of seabirds as adhesive seed dispersers on the Ogasawara Islands. The Ogasawara Islands is a group of oceanic islands located about 1,000 km south of the Japanese mainland. The archipelago is composed of four main island groups: Mu- kojima, Chichijima, Hahajima, and the Volcano groups (Fig. 1). Ono and Sugawara (1981) classified the original immigrants (taking into account the possibility that some species underwent speciation after arrival of small founder populations) of the native flora of the Ogasawara Islands by their dispersal mode following Carlquist (1974). They concluded that close to 70 % of original immigrants were transported by birds. Of these, about half were thought to have been dispersed by internal transport and the remainder by adhesive dispersal. This is consistent with the analysis of Hawaiian flora conducted by Carlquist (1974) and suggests that the Ogasawara flora has characteristics typical of oceanic islands. A few studies point to the possibility that seabirds transport seeds of alien plants (Bergstrom and Smith 1990). Among the Ogasawara Islands, only Chichijima, Hahajima, Iwoto, and Minamitorishima are now inhabited by humans; 10 other islands were settled before World War II (WWII: Tsuji 1995). Although most of the islands remain uninhabited and human visitation has been restricted since WWII ended, the distributions of alien plant species are still expanding among many uninhabited islands (Kobayashi and Ono 1987; Toyoda 2003). Seabird dispersal may offer one explanation for the expansion of alien plants among uninhabited islands as the Ogasawara Islands (and many other oceanic islands) provide large-scale breeding habitat for seabirds. Seabirds breed on all islands other than those that are heavily disturbed by humans or are too small for breeding purposes (Chiba et al. 2007). A few studies reported that some seabird species move between islands within seasons (Kress and Nettleship 1988; Dearborn et al. 2003; 123 Biodivers Conserv (2012) 21:2787–2801 2789

Fig. 1 Study site. The Ogasawara Islands comprises four main groups: Mukojima, Chichijima, Hahajima, and the Volcano groups. The islands in parentheses were not surveyed in the current study

Zuberogoitia et al. 2007) and it is reasonable to suppose that they play a role in the range expansion of alien plants. Most seabirds on the Ogasawara Islands breed in colonies in open habitats. Herbaceous plants that grow in such open habitats might be effectively dispersed by seabirds. 123 2790 Biodivers Conserv (2012) 21:2787–2801

We first conducted capture surveys and documented the occurrence of seed adhesion to seabirds to identify plant species that could potentially be dispersed by seabirds. Then we conducted germination experiments for these plant species to confirm seed survival in salty conditions, as seeds on feathers might be immersed in seawater doe to seabird behavior. Finally, to clarify the effects of seabirds on the ranges of these plants, the distributions of plants that were detected frequently in the capture surveys were investigated on 24 islands by field and literature surveys, and the relationships between the plant and seabird distributions were analyzed.

Methods

Species composition of seeds attached to seabirds and frequency of attachment

We focused on four species of seabird, the black-footed albatross (Phoebastria nigripes), the Bulwer’s petrel (Bulweria bulwerii), the wedge-tailed shearwater (Puffinus pacificus), and the brown booby (Sula leucogaster) because these species have wide breeding distributions and large population sizes on the Ogasawara Islands. We investigated the occurrence of seed adhesion to the feathers and feet of each seabird species by conducting capture surveys by hand or using brail nets at breeding sites. The black-footed albatross surveys were conducted in the Mukojima group, with one site on Mukojima and two sites on Torishima. The others were conducted in the Chichijima group, as follows: petrels at two sites on each of Higashijima and Minamijima and one site on Tatsumijima; shearwaters at one site on each of Hyotanjima, Nishijima, Higashijima, Tatsumijima, and Mi- namijima; and boobies at three sites on Minamijima (Fig. 1). Surveys were conducted during the breeding seasons, viz., in March 2009 for the albatross and in June 2009 for the petrel, shearwater, and booby. To avoid recapturing the same birds, we banded captured individuals or recorded band numbers when specimens carried bands from previous tag- gings. We carefully removed anything attached to the birds by placing a plastic tray underneath the animal and running a comb or hand through its feathers. All collected seeds were transferred to a plastic bag and transported to the laboratory for identification. We identified the species of the seeds attached to the birds and recorded their statuses, i.e., native or alien to the Ogasawara Islands (following Kobayashi and Ono 1987). Cenchrus echinatus was defined as an alien according to Nobushima (2010) because Kobayashi and Ono (1987) have not referred to this species. We classified dispersal modes of the seeds into the following categories (following Ono and Sugawara 1981): ‘‘air flotation,’’ seeds or fruits with flight structures such as plumose pappi; ‘‘internal transport,’’ seeds or fruits eaten and carried internally by birds; ‘‘mechanical adhesion,’’ seeds or fruits attached to feathers of birds mechanically by barbs, bristles, awns, trichomes, and so forth; ‘‘muddy adhesion,’’ seeds or fruits embedded in mud on the feet of birds with traits such as small seed size and the tendency for plants to grow in marshes, mud flats, or along streams ‘‘viscid adhesion,’’ seeds or fruits attached to feathers of birds by viscid substances or the viscid fruit parenchyma surrounding seeds; ‘‘water flotation,’’ seeds with the ability to float in the ocean for prolonged periods. To estimate how often adhesive dispersal occurs, the frequency of individuals with attached seeds was calculated for each dataset. Data acquired at the same sites on the same days were included in one dataset. These were not tested statistically because the sample sizes were too small and the variances were too high. 123 Biodivers Conserv (2012) 21:2787–2801 2791

Salinity tolerance of possibly dispersed seeds

We conducted germination experiments for the plant species detected in the aforemen- tioned capture surveys, except for Solanum nigrum and Coronopus didymus, because sufﬁcient amount of seeds could not be acquired. Seeds for the tests were collected from Chichijima, air-dried at room temperature for more than one night, and stored in a refrigerator at 4 °C until the start of the experiments. All germination experiments were performed on 1 % agarose gels because of the ease to homogenize conditions in 9 cm petri dishes placed in a temperature-controlled incubator on a 25/15 °C day/night cycle. Before planting, the seeds were subjected to three different salinity treatments: control (no treatment) or soaked in 3.5 % NaCl solution (isotonic with seawater) for either 10 min or 8 h. The salinity durations were determined by taking into account the amount of time birds spent on the water for a trip in breeding season, viz. a few min for the brown booby, whose trip duration is ca. 2–3 h (see Weimerskirch et al. 2009), and 7–8 h on average for black-footed albatross, whose trip duration extends over days to a week (see Fernandez and Anderson 2000). Five replications of 25 seeds were allocated to each treatment for each species. Evaporated water was replenished with 0.003 % benomyl solution every few days for fungal control. Incubation continued for 2 months or more until no new seed germination was observed. Multiple comparisons between the percent germination (i.e., the number of seeds that germinated/25 9 100) in different treatments were performed by Steel-Dwass tests.

Relationships between plant and seabird distributions

To evaluate the effects of seabirds on plant ranges, we investigated plant distributions on islands uninhabited by humans and analyzed the results. Plant species detected during the capture surveys were targeted, except for those for which only one or two seeds were detected; we investigated C. echinatus, Chloris barbata, Boerhavia diffusa, Oxalis corniculata, and S. nigrum. We recorded the presence/absence of each target plant species on each island using landing observations and literature data. Landing observations were conducted on 13 islands in the Chichijima group (Hyotanjima, Hitomarujima, Nishijima, Higashijima, Tatsumijima, Minamijima, Tatejima, Kannukijima, and ﬁve unnamed small islands) in June 2009, Kitanoshima in the Mukojima group, and Torishima, Minamitori- shima, and Futagojima in the Hahajima group in October 2009 (Fig. 1). We surveyed breeding site on islands C1 ha and the whole island on islands \1 ha. Literature surveys were conducted for seven islands where detailed investigation of plants had been conducted (Mukojima and Nakodojima in the Mukojima group, Anijima and Ototojima in the Chichijima group, Mukohjima in the Hahajima group, and Kitaiwoto and Minamiiwoto in the Volcano group) and the islands on which landing observations had been made when additional records were available (Fig. 1: Kobayashi and Ono 1987; Shimizu and Yasui 1992; Toyoda 2003; Yamamoto et al. 2003; Japan Forest Technology Association 2005). We tested the effects of seabirds on the ranges of each target plant species by ﬁtting generalized linear models (GLMs) with binomial probability distributions and logit link using R version 2.15.0 software (R Development Core Team 2012). The response variable was the presence/absence of each target plant species on each island (n = 24 in each model). Some plant species might be dispersed by some means including seabird dispersal. To evaluate the relative effect of seabird dispersal on each plant’s range, the following explanatory variables were adopted in the analyses: island size (ha) (AREA), distance from the nearest inhabited island (km) (DIST), estimated number of human visitors per year 123 2792 Biodivers Conserv (2012) 21:2787–2801

(HV), and seabird breeding colony size (SBS). These variables likely reflect effects of presumed dispersal vectors, which are wind dispersal, internal transport by land birds, human transport, and seabird dispersal. When wind dispersal contributes to the expansion of plant ranges, AREA and DIST should be selected for inclusion as explanatory variables. When internal transport by land birds makes a contribution, AREA and/or DIST should also be selected for inclusion as explanatory variables because most land birds are forest species and occur only on larger islands providing sufficient forests, and the largest islands are inhabited. If anthropogenic dispersal were essential, HV would be selected for inclusion. When seabird dispersal contributed, SBS should be selected for inclusion as an explanatory variable. AREA might be selected regardless of dispersal mode because island size ought to have considerable effects on plant occurrences (Begon et al. 1996). AREA was log10 transformed to remove right-skewness in the distribution of data. HV was calculated from migration data for 2005 and 2006 summarized by the Kanto Regional Environment Office (2007). SBS values were the estimated total seabird pairs breeding on each island based on the data of Chiba et al. (2007), which included all seabird species. The detailed methodology used to calculate SBS parameters is given in Online Resource 1. In these analyses, model selections were performed using the Akaike information criterion (AIC) to evaluate the relative importance of seabird dispersal versus other dispersal methods. We ranked all models by DAIC (DAICi = AICi - AICmin) and considered models for which DAIC B 2 to be the potential best models (Burnham and Anderson 2002). Data for C. echinatus and O. corniculata were not analyzed due to a software error message (‘‘algorithm did not converge’’). To avoid this error and because the relatively large seeds of this species are unlikely to be dispersed by wind, DIST was removed from the C. echinatus analysis. The error message for O. corniculata is thought to have arisen because the spatial distribution was too wide; the species occurred on all islands larger than 2.3 ha. Therefore, additional analyses were not conducted for this species.

Results

Species composition of seeds attached to seabirds and frequency of attachment

In total, 41 black-footed albatrosses, 45 Bulwer’s petrels, 45 wedge-tailed shearwaters, and 29 brown boobies were captured (Table 1). Seeds of nine plant species (C. echinatus, C. barbata, B. diffusa, O. corniculata, S. nigrum, C. didymus, Youngia japonica, Digitaria pruriens, and Sporobolus diander) were collected from the birds. The three most common species (C. echinatus, C. barbata, and B. diffusa) and C. didymus are alien species. Seeds were attached to 16–32 % of birds for each species (Fig. 2). All seeds were found on feathers, and none on the feet. Cenchrus echinatus has fruits with spines and C. barbata has seeds with awns as adhesive structures (see Fig. 3). D. pruriens, S. diander and these two were classified into the mechanical adhesion dispersal category. The seeds of B. diffusa are surrounded by a viscid substance and thus were classified into the viscid adhesion category. Seeds of O. corniculata (about 1.4 mm on the major axis) were found on three bird species (albatross, petrel, and booby), even though they have no special structures for adhesion. O. corniculata and C. didymus were not classifiable into any category (Ono and Sugawara 1981). Fleshless seeds of S. nigrum were detected on the feathers of shearwaters and boobies in spite of their 123 Biodivers Conserv (2012) 21:2787–2801 2793

Table 1 Species composition of seeds attached to seabirds Plant species Albatross Petrel Shearwater Booby Status Dispersal mode

C. echinatus 0 4 (8) 2 (15) 0 Introduced Mechanical adhesion C. barbata 7 (7) 0 2 (2) 1 (2) Introduced Mechanical adhesion B. diffusa 0 2 (3) 0 2 (10) Introduced Viscid adhesion O. corniculata 4 (4) 3 (5) 0 2 (2) Native Unknown S. nigrum 0 0 2 (9) 1 (1) Native Internal transport C. didymus 1 (2) 0 0 0 Introduced Unknown Y. japonica 0 0 1 (1) 0 Native Air ﬂotation D. pruriens 0 1 (1) 0 0 Native Mechanical adhesion S. diander 1 (1) 0 0 0 Native Mechanical adhesion No. of captures 41 45 45 29

Nine plant species, including four aliens, were detected. Four species had no obvious adhesive adaptations. Values are the number of individuals of each seabird species with seeds attached: black-footed albatross (Phoebastria nigripes), Bulwer’s petrel (Bulweria bulwerii), wedge-tailed shearwater (Puffinus pacificus), and brown booby (Sula leucogaster). Values in parentheses are total numbers of attached seeds. The number of C. echinatus seeds is represented by the number of fruits. Statuses of the plants follow Kobayashi and Ono (1987) or Nobushima (2010). Dispersal modes were classified following Ono and Sugawara (1981)

Fig. 2 Frequency of individual 50 birds with seeds attached 4 (mean ± SE). Values above bars are numbers of datasets. Data 40 acquired at the same sites on the 3 same days are included in one 30 dataset 5 6 20

10 seeds attached (%)

Frequency of individuals to which Black- Bulwer's Wedge- Brown footed petrel tailed booby albatross shearwater classification into the internal transport category. The seeds of Y. japonica,whichhave plumose pappi, were classified into the air flotation category.

Salinity tolerance of possibly dispersed seeds

Seeds of B. diffusa became moldy and none germinated. Proportions of S. diander seeds that germinated were very low (less than 10 %) under all treatments (Fig. 4f). We do not analyze these two species. Among seeds of C. echinatus, C. barbata,andO. corniculata, mean percent germination declined as salt concentration increased, although the results were signiﬁcantly different between only the control and the 8 h salinity treatment in the case of O. corniculata (P = 0.031; Fig. 4a, b, c). Mean percent germination of salt-treated seeds in Y. japonica, D. pruriens,andS. diander were higher than those of controls. There were signiﬁcant 123 2794 Biodivers Conserv (2012) 21:2787–2801

Fig. 3 Seeds or fruits detected by capture surveys. All images are shown to the same scale and each grid is 1 mm. a Cenchrus echinatus; 5–7 mm (except spines). A fruit includes approximately four seeds. b Chloris barbata; 2.5–4 mm (excluding awns). c Boerhavia diffusa; 3 mm. d Oxalis corniculata; 1.4 mm. e Solanum nigrum; 1.3 mm. f Coronopus didymus; 1.8 mm. g Youngia japonica; 1.9 mm (excluding pappus). h Digitaria pruriens; 3–3.5 mm. i Sporobolus diander; 1.6 mm difference between the control and NaCl 10 min for Y. japonica and D. pruriens and between the control and NaCl 8 h for D. pruriens (P = 0.019, 0.022, 0.030, respectively; Fig. 4d, e, f).

Relationships between plant and seabird distributions

The distributions of target plant species and variables used in the statistical analyses are presented in Online Resource 1. Table 2 shows the results of GLM model selections in analyses used to evaluate the relative importance of seabird effects on the ranges of each plant species. For C. echinatus, SBS was incorporated in all three models with DAIC B 2. Only AREA, both AREA and HV, or only HV were selected (in addition to SBS) in ascending order of DAIC; all 123 Biodivers Conserv (2012) 21:2787–2801 2795

a C. echinatus b C. barbata 100 100

80 80

60 60

40 40

20 20

Percent germination (%) 0 0

c O. corniculata d Y. japonica P <0.05 100 P <0.05 100

80 80

60 60

40 40

20 20

0 0 Percent germination (%)

e D. pruriens f S. diander

100 P <0.05 100

80 P <0.05 80

60 60

40 40

20 20

Percent germination (%) 0 0 Control Control NaCl 8h NaCl 8h NaCl 10min NaCl 10min

Fig. 4 Percent germination of potentially dispersible plant species (mean ± SE). Only that of O. corniculata declined signiﬁcantly in salinity treatments. Seeds of B. diffusa became moldy and did not germinate (data not shown)

coefﬁcients for these effects, including that of SBS, were positive. Only one model with all factors (AREA, DIST, HV, SBS) was selected for C. barbata, with distance having a negative relationship and other factors having positive relationships with plant ranges. The range of B. diffusa was positively correlated with SBS in all four models, with DAIC B 2. None, AREA only, DIST only, or HV only were selected (in ascending order of DAIC) as explanatory variables for incorporation into the models (in addition to SBS); all coefﬁ- cients were positive. For the range of S. nigrum, nine models had DAIC B 2. No factor was incorporated into all of the models, but each factor was incorporated into at least four models. DIST was negatively related to plant range; the other factors were positively 123 2796 Biodivers Conserv (2012) 21:2787–2801

Table 2 Coefﬁcients for each explanatory variable and AIC of each model with DAIC B 2 resulting from GLM analyses testing factors affecting the distribution patterns of each plant species AREA DIST HV SBS AIC DAIC

C. echinatus 2.908 – 1.213 18.6 0.00 1.497 – 0.015 1.487 18.7 0.18 – 0.030 1.741 19.4 0.81 C. barbata 3.040 -0.410 0.072 4.416 23.4 0.00 B. diffusa 1.582 20.7 0.00 0.497 1.389 22.1 1.38 0.016 1.441 22.2 1.49 0.0003 1.483 22.2 1.49 S. nigrum 0.017 0.820 28.4 0.00 1.514 -0.052 0.996 28.6 0.23 0.932 28.7 0.27 1.338 -0.066 0.006 1.318 28.8 0.44 0.930 0.502 29.0 0.58 0.508 0.008 0.677 29.7 1.28 -0.023 0.021 1.073 29.7 1.30 0.783 0.001 29.9 1.49 1.150 -0.019 30.2 1.77

Ranges of C. echinatus, B. diffusa, and C. barbata were positively correlated with seabird breeding distributions in all models selected. The response variable was the presence/absence of each target plant species on each island (n = 24 in each model). The following explanatory variables were adopted: log10 transformed island size (ha) (AREA), distance from the nearest inhabited island (km) (DIST), estimated number of human visitors per year (HV), and seabird breeding colony size (SBS). A hyphen indicates that the variable was not used in the analysis (see ‘‘Methods’’ section for details) related (see Table 2 for details). O. corniculata data were not analyzable due to an algorithm error, which may be related to the extremely broad distribution of this species.

Discussion

Possible dispersed plant species

All targeted seabird species had the potential to act as seed-dispersal agents. A wide variety of plant species can be transported in this way. At least nine species were attached to the seabirds, although some seeds may have been overlooked due to the incompleteness of the collection method (see Figuerola and Green 2002). Four of the nine plant species (including the three most abundant) were alien species. The current results indicate that seabirds contribute to the expansion of alien species. Although the seeds of five species had adaptations for adhesive dispersal, seabirds also appeared to disperse the seeds of plants with the following attributes: small seeds (e.g., O. corniculata and C. didymus), seeds enclosed in fleshy fruits including sticky parenchyma (e.g., S. nigrum), and seeds with plumose pappi (e.g., Y. japonica). The small size, flatness, and rough surface of seeds of O. corniculata might render it suitable for adhesion. However, the suitability of O. corniculata for adhesive dispersal is 123 Biodivers Conserv (2012) 21:2787–2801 2797 achieved by the morphological characteristics of the seeds as well as the mechanical characteristics of the fruits. In general, the dispersal mode of O. corniculata is considered to be autochory. If touched when the fruit is ripe, the capsule explodes suddenly and broadcasts seeds (Ridley 1930). This mechanism facilitates entry of the seeds into the feathers if seabirds touch the fruits. The fruits of S. nigrum are probably crushed by seabirds (e.g., when birds sit or step on them); the exposed sticky parenchyma then functions like a glue, adhering the seeds to the birds. The plumose pappi of Y. japonica seeds, usually considered to be structures for wind dispersal, may also serve as adhesive structures. Although the proportion of germination of O. corniculata was significantly reduced by salinity treatment, even in the 8-h treatment, none of the species had an average germination rate of less than 60 % of the value in the controls. The germination proportions among salt-treated seeds of Y. japonica and D. pruriens were significantly higher than those in the controls. This is attributed to immersion in water and the antifungal effects of the salinity treatment. Few or no seeds germinated in experiments with B. diffusa and S. diander; the incubation conditions may have been inappropriate for these species. Further studies on the adequate conditions for each plant will be required. On the whole, it is considered that the seeds of target species suffered nonfatal damage in seawater up to 8 h of continuous immersion. The germination experiments demonstrated that the plant seeds that we tested had the potential to survive the total time of immersion during a foraging trip in the breeding season, and seabirds move from tens to hundreds of kilometers during a single trip (Phalan et al. 2007; Weimerskirch et al. 2009). However, during their trips, seabirds repeatedly immerse their bodies for short periods of time (Fernandez and Anderson 2000). Burger (2005) tested repeated submersion effects and found reduced germination of Pisonia seeds immersed in seawater after 7 days of daily immersion for 30 min. Moreover, there are reports of the inter-island movements of seabirds (Kress and Nettleship 1988; Dearborn et al. 2003; Zuberogoitia et al. 2007), but the frequencies and spatial patterns of these movements are largely unknown. Further explorations of plant physiology and seabird behavior are necessary to quantify seabird dispersal ability.

Effects of seabirds on plant distributions

GLM analysis demonstrated that the ranges of C. echinatus, B. diffusa, and C. barbata were positively correlated with seabird colony size (SBS). SBS was selected as an explanatory variable in all models with DAIC B 2 of them. In particular, it is very likely that seabirds serve as the primary seed dispersal agents for C. echinatus and B. diffusa among uninhabited islands. For C. echinatus, AREA only, both AREA and HV, or HV only were selected in ascending order of DAIC (in addition to SBS). In general, plant establishment is more successful on larger islands, which tend to have more abundant and diverse habitats and resources (Begon et al. 1996). Some seeds are likely to be dispersed by humans where few seabirds breed but there are relatively large numbers of human visitors (e.g., Anijima and Ototojima). However, seabirds are the only likely seed dispersers for C. echinatus among the many other uninhabited islands where humans rarely visit. This alien plant occurs on Minamiiwoto, where only seven introduced plant species (5.4 % of all plant species) have been detected (Fujita et al. 2008). The island is free from human disturbance and has been isolated geographically throughout its history, but it is home to many breeding seabirds (Kawakami et al. 2008). The large population of seabirds might have contributed to the range expansion of C. echinatus. Only SBS was selected as a factor 123 2798 Biodivers Conserv (2012) 21:2787–2801 affecting the distribution of B. diffusa in the best model, although AREA, DIST, and HV were selected in addition to SBS in other models with DAIC B 2. At least several hundreds pairs of seabirds bred on all six uninhabited islands where B. diffusa occurred. This species has not been detected on Hahajima, but it was found on small satellite islands surrounding Hahajima, such as Minamitorishima and Torishima, where many seabirds breed. These observations are not in accord with the hypothesis of stepping stone introductions of alien species to these satellite islands via Hahajima, which is the largest and only inhabited island in the Hahajima group. These observations do provide strong evidence for seabird dispersal. Although the distribution of O. corniculata was not analyzable, the primary dispersers of this species are likely seabirds as well. This is because O. corniculata has a very wide distribution range, even though its seeds do not exhibit any adaptations for other dispersal methods that would enable trans-oceanic dispersal. Seabird dispersal was suggested to be one of the several dispersal methods for C. barbata. In our analysis of this species, only one model incorporating all factors was selected. Island area and distance from inhabited islands were selected as affecting factors that likely reﬂect the effect of wind dispersal, because light seeds of this species be readily dispersed by wind (Ridley 1930). C. barbata appears to be dispersed by wind, humans, and seabirds. The analysis of S. nigrum was confusing and factors contributing to its range were unclear. However, like C. barbata, S. nigrum can be dispersed by several means, including adhesion to humans as well as seabirds, and by internal transport by land birds, such as brown- eared bulbuls Hypsipetes amaurotis, blue rock-thrushes Monticola solitarius, and Japanese white-eyes Zosterops japonicus, which frequently forage on the fruits (Kawakami et al. 2009). Even if a plant is dispersed by several mechanisms, the dispersal pattern varies according to these mechanisms (Vittoz and Engler 2007). Seabirds appear to be especially effective agents of long-distance dispersal because of their great ﬂying ability and large population sizes at their breeding sites. Long-distance dispersal ability is necessary for trans-oceanic migration in island ecosystems such as those of the Ogasawara Islands. The positive correlations between some plant and seabird distributions are consistent with the hypothesis that seabirds disperse the plants. However, there is also a possibility that correlations may be attributable to seabird habitat choices or nutrient input from feces and pellets of seabirds; further explorations are needed to fully demonstrate that the positive relationships result from seabird seed dispersal.

Conclusions and implications

Long-distance seed dispersal is a key process, especially in island ecosystems, and yet there is little information on this process (Carlquist 1966; Howe and Smallwood 1982; Cain et al. 2000). Empirical studies on avian adhesive dispersal are scarce, although this mode of dispersal has long been recognized as a major method of long-distance dispersal (Darwin 1859; Ridley 1930; Taylor 1954; Falla 1960; Carlquist 1966; van der Pijl 1972; Carlquist 1974; Sorensen 1986; Godley 1989; Morton and Hogg 1989). Seabirds with extensive ﬂying ability and preferential nesting on isolated islands are good candidates as dispersal agents (Falla 1960). However, data on seabirds as adhesive dispersers have become available only incidentally (Chapman 1891; Taylor 1954; Carlquist 1974; Godley 1985) or are restricted to a few notable plant species (Walker 1991; Burger 2005). Ours is the ﬁrst comprehensive study on adhesive seed dispersal by seabirds and provides essential information on long-distance dispersal. 123 Biodivers Conserv (2012) 21:2787–2801 2799

Seeds of four species collected from seabird feathers had no morphological traits for adhesion. Thus, even plants that do not have highly adaptive morphologies are likely to be effectively dispersed by seabirds in isolated island ecosystems. Therefore, seed morphology is not always a reliable indicator of dispersal mode, especially when transport is over long distances (Higgins et al. 2003; Brochet et al. 2009; Vargas et al. 2012), although it is often assumed that morphology indicates dispersal mode (Carlquist 1974; Ono and Su- gawara 1981). The three most abundant plant species collected from feathers were aliens. However, we should point out that there is uncertainty about whether the plants are indeed introduced because it is difﬁcult to prove that they were absent before human occupation of the islands. Nonetheless, there is little doubt that seabird dispersal contributes to range expansion of some alien plants. Most seabirds breed on uninhabited islands and human access to most uninhabited islands is limited. However, some of these islands house a large number of visitors including tourists and researchers. They sometimes bring alien plant seeds by adhesion from inhabited islands; these aliens might establish themselves and subsequently spread to other islands via seabirds. Among the Ogasawara Islands, these are the circumstances on Minamijima, where three of the seabird species we targeted (Bul- wer’s petrel, wedge-tailed shearwater, and brown booby) breed and where many tourists visit ([6,000 people/year). Such islands could serve as gateways for alien plants to many other uninhabited islands via seabird dispersal. Dispersal of alien species by seabirds is a serious problem because these birds tend to breed on undisturbed islands with native habitats, such as Minamiiwoto. Thus, tourism on uninhabited islands should be very carefully managed because other islands might become indirect recipients of introduced plants via seabird dispersal.

Acknowledgments We thank Kazuo and Harumi Horikoshi, Hajime Suzuki, Tetsuro Sasaki, and To- mohiro Deguchi for ﬁeld assistance and other support; Minoru and Yukari Masuda, George Minami, Koji Yoshida, and Club Noah for transportation; Chikako Takahashi for help with collecting seeds; Noriko Iwai for help with the laboratory experiment; Hayato Iijima and Masaki Hoso for help with the statistical analysis; Donald R. Drake and members of the Laboratory of Community and Ecosystem Ecology, Tohoku University, for their critical comments; and members of the Department of Wildlife Biology, Forestry and Forest Products Research Institute for their generosity. This study was supported by the Global Environment Research Fund of the Ministry of the Environment of Japan (F-051) and Grants-in-Aid for Scientiﬁc Research of Japan Society for the Promotion of Science.

References

Begon N, Harper JL, Townsend CR (1996) Ecology: individuals, populations, and communities, 3rd edn. Blackwell, Oxford Bergstrom DM, Smith VR (1990) Alien vascular ﬂora of Marion and Prince Edward Islands: new species, present distribution and status. Antarctic Sci 2:301–308 Brochet AL, Guillemain M, Fritz H, Gauthier-Clerc M, Green AJ (2009) The role of migratory ducks in the long-distance dispersal of native plants and the spread of exotic plants in Europe. Ecography 32:919–928 Brochet AL, Guillemain M, Fritz H, Gauthier-Clerc M, Green AJ (2010) Plant dispersal by teal (Anas crecca) in the Camargue: duck guts are more important than their feet. Freshwater Biol 55:1262–1273 Burger AE (2005) Dispersal and germination of seeds of Pisonia grandis, an Indo-Paciﬁc tropical tree associated with insular seabird colonies. J Trop Ecol 21:263–271 Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information- theoretic approach, 2nd edn. Springer, New York

123 2800 Biodivers Conserv (2012) 21:2787–2801

Cain ML, Milligan BG, Strand AE (2000) Long-distance seed dispersal in plant populations. Am J Bot 87:1217–1227 Carlquist S (1966) The biota of long-distance dispersal. I. Principles of dispersal and evolution. Q Rev Biol 41:247–270 Carlquist S (1974) Island biology. Columbia University Press, New York Chapman FR (1891) The outlying islands south of New Zealand. Trans NZ Inst 23:491–522 Chiba H, Kawakami K, Suzuki H, Horikoshi K (2007) The distribution of seabirds in the Bonin Islands, Southern Japan. J Yamashina Inst Ornithol 39:1–17 Darwin C (1859) On the origin of species by means of natural selection. Murray, London Dearborn DC, Anders AD, Schreiber EA, Adams RMM, Mueller UG (2003) Inter-island movements and population differentiation in a pelagic seabird. Mol Ecol 12:2835–2843 Falla RA (1960) Oceanic birds as dispersal agents. Proc R Soc Lond B 152:655–659 Fernandez P, Anderson DJ (2000) Nocturnal and diurnal foraging activity of Hawaiian albatrosses with a new immersion monitor. Condor 102:577–584 Figuerola J, Green AJ (2002) How frequent is external transport of seeds and invertebrate eggs by waterbirds? A study in Donana, SW Spain. Arch Hydrobiol 155:557–565 Fujita T, Takayama K, Syumiya T, Kato H (2008) Vascular flora of Minami-Iwo-To Island. Ogasawara Res 33:49–62 (in Japanese) Godley DR (1985) A visit to the Auckland Islands in the summer of 1962–1963. Tuatara 28:1–13 Godley EJ (1989) The flora of Antipodes Islands. New Zeal J Bot 27:531–563 Herrera CM (1984) Adaptations to frugivory of Mediterranean avian seed dispersers. Ecology 65:609–617 Higgins SI, Nathan R, Cain ML (2003) Are long-distance dispersal events in plants usually caused by nonstandard means of dispersal? Ecology 84:1945–1956 Howe HF, Primack RB (1975) Differential seed dispersal by birds of the tree Caesearia nitidia (Flacour- tiaceae). Biotropica 7:278–283 Howe HF, Smallwood J (1982) Ecology of seed dispersal. Ann Rev Ecol Syst 13:201–228 Japan Forest Technology Association (2005) 2004 Report of planning study for promotion of nature res- toration in the Ogasawara area, vol 1. Japan Forest Technology Association, Tokyo (in Japanese) Kanto Regional Environment Office (2007) 2006 Report of research for inquest of management approach for ecosystem of Ogasawara National Park. Kanto Regional Environment Office, Saitama (in Japanese) Kawakami K, Suzuki H, Chiba H, Horikoshi K (2008) Avifauna of Minami-Iwo-To Island, Volcano Islands, the Bonin Islands. Ogasawara Res 33:111–127 (in Japanese) Kawakami K, Mizusawa L, Higuchi H (2009) Re-established mutualism in a seed-dispersal system con- sisting of native and introduced birds and plants on the Bonin Islands, Japan. Ecol Res 24:741–748 Kobayashi S, Ono M (1987) The revised list of vascular plants indigenous and introduced to the Bonin (Ogasawara) and the Volcano (Kazan) Islands. Ogasawara Res 13:1–55 Kress SW, Nettleship DN (1988) Re-establishment of Atlantic puffins (Fratercula arctica) at a former breeding site in the Gulf of Maine. J Field Ornithol 59:161–170 MacArthur RH (1972) Geographical ecology. Harper & Row, New York Moermond TC, Denslow JS (1983) Fruit choice in neotropical birds. J Anim Ecol 52:407–418 Morton JK, Hogg EH (1989) Biogeography of island floras in the Great Lakes II. Plant dispersal. Can J Bot 67:1803–1820 Nobushima F (2010) Ogasawara shoto ni shinnyu shiteiru gairaishokubutsu no genjo (The current state of alien plants in the Ogasawara Islands). Shokucho 44:5–15 (in Japanese) Ono M, Sugawara T (1981) An analysis of the flowering plant flora of the Ogasawara (Bonin) Islands with regard to their mode of dispersal. Ogasawara Res 5:25–40 (in Japanese) Phalan B, Phillips RA, Silk JRD, Afanasyev V, Fukuda A, Fox J, Catry P, Higuchi H, Croxall JP (2007) Foraging behaviour of four albatross species by night and day. Mar Ecol Prog Ser 340:271–286 R Development Core Team (2012) R: a language and environment for statistical computing. R foundation for statistical computing, Vienna (http://www.R-project.org) Ridley HN (1930) The dispersal of plants throughout the world. Reeve Ashford, New York Shimizu Y, Yasui T (1992) Flora of Ani-jima and distribution of rare plant species. WWFJ Sci Rep 1:107–122 (in Japanese) Sorensen AE (1981) Interactions between birds and fruit in a temperate woodland. Oecologia 56:242–249 Sorensen AE (1984) Nutrition, energy, and passage time: experiments with fruit preference in European blackbirds (Turdus merula). J Anim Ecol 53:545–557 Sorensen AE (1986) Seed dispersal by adhesion. Ann Rev Ecol Syst 17:443–463 Taylor BW (1954) An example of long distance dispersal. Ecology 35:369–372 Toyoda T (2003) Flora of Bonin Islands. Aboc-sha, Kamakura (in Japanese)

123 Biodivers Conserv (2012) 21:2787–2801 2801

Tsuji T (1995) Ogasawara syoto rekishi nikki Jokan (The history of the Bonin Islands I). Kindaibungeisha, Tokyo (in Japanese) van der Pijl L (1972) Principles of dispersal in higher plants, 2nd edn. Springer, New York Vargas P, Heleno R, Traveset A, Nogales M (2012) Colonization of the Gala´pagos Islands by plants with no specific syndromes for long-distance dispersal: a new perspective. Ecography 35:33–43 Vittoz P, Engler R (2007) Seed dispersal distances: a typology based on dispersal modes and plant traits. Botanica Helvetica 117:109–124 Vivian-Smith G, Stiles EW (1994) Dispersal of salt marsh seeds on the feet and feathers of waterfowl. Wetlands 14:316–319 Walker TA (1991) Pisonia Islands of the Great Barrier Reef. Part I. The distribution, abundance and dispersal by seabirds of Pisonia grandis. Atoll Res Bull 350:1–23 Weimerskirch H, Shaffer SA, Tremblay Y, Costa DP, Gadenne H, Kato A, Ropert-Coudert Y, Sato K, Aurioles D (2009) Species- and sex-specific differences in foraging behavior and foraging zones in blue-footed and brown boobies in the Gulf of California. Mar Ecol Prog Ser 391:267–278 Yamamoto H, Ichikawa S, Katoh S, Akimoto H, Yasui T, Wakabayashi M (2003) The flora of Mukojima Island and Nakodojima Island just after the eradication of feral goats. Ogasawara Res 28:29–48 (in Japanese) Zuberogoitia I, Azkona A, Castillo I, Zabala J, Martıńez JA, Etxezarreta J (2007) Population size estimation and metapopulation relationships of storm petrels Hydrobates pelagicus in the Gulf of Biscay. Ring Migration 23:252–254

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