Using seed-tagging methods for assessing post-dispersal seed fate in rodent-dispersed trees
Introduction
Determining the ultimate fate of individual seeds is an important aspect of studies on seed dispersal by animals, required to fully understand the role of seed-dispersing animals in forest dynamics, the ecological and evolutionary consequences of seed dispersal, and the coevolutionary interactions between these animals and plants. However, following the movements and fates of dispersed seeds has proven a major obstacle (Levey and Sargent, 2000; Wang and Smith, 2002). A wide range of marking techniques have been developed for tracking seeds, especially those dispersed by seed-caching rodents (reviewed by Forget and Wenny, 2005).
Which seed-marking method is used varies greatly among continents or vegetation types (Forget and Wenny, 2005). Radioisotope methods, in which seeds are given radioactive particles on their surface and are relocated after dispersal using a Geiger counter, are the most-used method in Europe (e.g. Jensen, 1985; Jensen and Nielsen, 1986) and Northern America (e.g. Lawrence and Rediske, 1959, Lawrence and Rediske, 1962; Abbott, 1961; Abbott and Quink, 1970; Vander Wall, 1992, Vander Wall, 1993, Vander Wall, 1994; Vander Wall and Joyner, 1998). Thread-marking methods, in which a piece of thread or wire (sometimes with flagging tape or a tag at the end) is attached to the seeds, allowing retrieval of cached seeds by marks protruding from the soil, are used in the majority of studies in Southern America (e.g. Hallwachs, 1986; Forget, 1990, Forget, 1991, Forget, 1992; Forget and Milleron, 1991; Wenny, 1999, Wenny, 2000a, Wenny, 2000b; Brewer and Rejmánek, 1999; Brewer, 2001; Jansen et al., 2002, Jansen et al., 2004; Chauvet et al., 2004), Australia (e.g. Theimer, 2001, Theimer, 2003; Dennis, 2003), and Asia (e.g. Yasuda et al., 1991, Yasuda et al., 2000; Wang and Ma, 1999; Zhang and Wang, 2001; Hoshizaki and Hulme, 2002; Li and Zhang, 2003; Xiao et al., 2004a, Xiao et al., 2004b, Xiao et al., 2005). The methodological bias complicates the comparison of results across the world because the differential effects of seed-marking techniques on seed handling by animals are largely unknown.
Radioisotopes are not apparent to man or animals, and isotope-labeling is therefore believed to not affect the removal and further handling of seeds by animals (Forget and Wenny, 2005). However, radioisotope methods are relatively expensive because they require specific detection equipment (Xiao and Zhang, 2003, Forget and Wenny, 2005). Moreover, radioisotopes are heavily regulated, and some countries prohibit use in the field for environmental reasons (e.g. Iida, 1996; Sone and Kohno, 1996). Thread-marking methods, in contrast, are cheap, simple, and versatile (Xiao and Zhang, 2003, Forget and Wenny, 2005). No study, however, has fully examined how the often-conspicuous thread marks affect seed removal and seed handling by animals, and how passage of thread through the seed affects seed survival and germination (but see Wenny, 2000b). Most thread-marking studies assume that the marking has little or negligible effect on seed fate or animal behavior (Forget and Wenny, 2005, but see Wenny, 2000b). A second problem is that thread marks are often bitten off by rodents, which seems to preclude the use of thread-marking where animals frequently cut or detach thread marks, e.g. the northern temperate zone.
We studied the effects of tags on seed handling by rodents and on germination for two seed-tagging methods: thread-marking, the most used technique, and wire tin-tagging, a relatively new method in which a tin tag is attached to the seed with a short metal wire that rodents cannot easily cut (Zhang and Wang, 2001; Li and Zhang, 2003, Xiao et al., 2004a, Xiao et al., 2004b, Xiao et al., 2005; Zhang et al., 2005). Wire tin-tagging may be suitable for use in both the northern temperate zone and the rest of the world, which would facilitate comparison, but has not yet been tested against other methods.
Section snippets
Materials and methods
Fieldwork was conducted in the Banruosi Experimental Forest (elevation 700–1000 m, 31°4′ N, 103°43′ E) in Dujiangyan City, Sichuan Province, Southwest China. The site lies in the middle of the subtropical zone, with a mean annual temperature of 15.2 °C, and an annual precipitation of 1200–1800 mm (Chen, 2000). The weather is often cloudy and foggy, with annual hours of sunlight typically in the range 800–1000 and a mean annual relative humidity of more than 80%. Common tree species include
Seed removal
Seed removal rates differed significantly among the three seed-tagging treatments, both for C. oleifera (Wald = 49.872, d.f. = 2, P < 0.001) and Q. variabilis (Wald = 32.633, d.f. = 2, P < 0.001). Unmarked seeds were removed faster than marked seeds, and thread-marked seeds were in turn removed faster than tin-tagged seeds (Fig. 1). Despite these differences, all seeds had been harvested from the seed stations after several days for C. oleifera or after about 2 months for Q. variabilis (except for two
Discussion
Both the tagging methods proved effective for tracking the fates of individual seeds upon their removal by seed-caching rodents. Fate pathways were similar to those found using radioisotope methods (Vander Wall and Joyner, 1998; Vander Wall, 2002, Vander Wall, 2003), which are believed not to affect animal behavior (Forget and Wenny, 2005). Some tagged seeds were handled, moved, and cached more than two times, which has been found in many rodent-dispersing species worldwide (Xiao et al., 2004c;
Acknowledgements
We thank the Subalpine Mountain Plant Garden of west China, CAS, and the Forest Bureau of Dujiangyan City of Sichuan Province, for support. Funds were provided by National Natural Science Foundation of China (30430130 and 30500072), key program of Ministry of Science and Technology (G2000046802) and CAS Innovative Research International Partnership Project (CXTDS2005-4). P.A.J. was supported by the Netherlands Foundation for the Advancement of Tropical Research (grant W84-584).
References (50)
- et al.
Grey squirrels remember the locations of buried nuts
Anim. Behav.
(1991) - et al.
Effect of rodents on acorn dispersal and survival of the Liaodong oak (Quercus liaotungensis Koidz.)
Forest Ecol. Manag.
(2003) Mechanisms of cache recovery in yellow chipmunks
Anim. Behav.
(1991)- et al.
Dispersal and germination of big and small nuts of Quercus serrata in subtropical evergreen broadleaved forest
Forest Ecol. Manag.
(2004) - et al.
Impacts of scatter-hoarding rodents on restoration of oil tea Camellia oleifera in a fragmented forest
Forest Ecol. Manag.
(2004) White pine seed consumption by small mammals
J. For.
(1961)- et al.
Ecology of eastern white pine seed caches made by small forest mammals
Ecology
(1970) Predation and dispersal of large and small seeds of a tropical palm
Oikos
(2001)- et al.
Small rodents as significant dispersers of tree seeds in a neotropical forest
J. Vege. Sci.
(1999) - et al.
Seed fates of two Sapotaceae species in a Guianan rain forest in the context of escape and satiation hypotheses
J. Trop. Ecol.
(2004)
The Dujiangyan region—pivot sector of assemblage, differentiation and maintenance of biodiversity in northern part of Hengduan mountain
Acta Ecol. Sin.
Scatter-hoarding by musky rat-kangaroos, Hypsiprymnodon moschatus, a tropical rain-forest marsupial from Australia: implications for seed dispersal
J. Trop. Ecol.
Seed-dispersal of Vouacapoua americana (Caesalpiniaceae) by caviomorph rodents in French Guiana
J. Trop. Ecol.
Scatterhoarding of Astrocaryum paramaca by Proechimys in French Guiana comparison with Myoprocta exilis
Trop. Ecol.
Seed removal and seed fate in Gustavia superba (Lecythidaceae)
Biotropica
Evidence for secondary seed dispersal by rodents in Panama
Oecologia
How to elucidate seed fate? A review of methods used to study seed removal and secondary seed dispersal
Agoutis (Dasyprocta punctata): the inheritors of quapinol (Hymenaea courbaril: Leguminosae)
Mast seeding and predator-mediated indirect interactions in a forest community: evidence from post-dispersal fate of rodent-generated caches
Quantitative analysis of acorn transportation by rodents using magnetic locator
Vegetatio
The role of seed size in dispersal by a scatter-hoarding rodent
Seed mass and mast seeding enhance dispersal by a neotropical scatter-hoarding rodent
Ecol. Mon.
Seed-predator interactions of European beech (Fagus silvatica L.) and forest rodents, Clethrionomys glareolus and Apodemus flavicollis
Oikos
Rodents as seed dispersers in a heather-oak wood succession
Oecologia
Radiotracer technique for determining the fate of broadcast Douglas-fir seed
Soc. Am. For. Proc.
Cited by (199)
Scatter-hoarding rodents are important seed dispersers in pine plantations
2024, Global Ecology and ConservationGrazing hinders seed dispersal during crop failure in a declining oak woodland
2024, Science of the Total EnvironmentThe distinct fruit size and physical defense promote divergent secondary seed dispersal strategies of three oak species
2023, Forest Ecology and ManagementMasting benefits seedling recruitment of Armeniaca sibirica through directed dispersal by rodents
2022, Forest Ecology and ManagementCanopy openness of individual tree promotes seed dispersal by scatter-hoarding rodents
2022, Forest Ecology and Management