Forest rodents provide directed dispersal of Jeffrey pine seeds

Rocky Mountain Geographic Science Center, USGS, Box 25046 Denver Federal Center, Denver, Colorado 80225, USA.
Ecology (Impact Factor: 4.66). 04/2009; 90(3):675-87. DOI: 10.1890/07-0542.1
Source: PubMed


Some species of animals provide directed dispersal of plant seeds by transporting them nonrandomly to microsites where their chances of producing healthy seedlings are enhanced. We investigated whether this mutualistic interaction occurs between granivorous rodents and Jeffrey pine (Pinus jeffreyi) in the eastern Sierra Nevada by comparing the effectiveness of random abiotic seed dispersal with the dispersal performed by four species of rodents: deer mice (Peromyscus maniculatus), yellow-pine and long-eared chipmunks (Tamias amoenus and T. quadrimaculatus), and golden-mantled ground squirrels (Spermophilus lateralis). We conducted two caching studies using radio-labeled seeds, the first with individual animals in field enclosures and the second with a community of rodents in open forest. We used artificial caches to compare the fates of seeds placed at the range of microsites and depths used by animals with the fates of seeds dispersed abiotically. Finally, we examined the distribution and survival of naturally establishing seedlings over an eight-year period. Several lines of evidence suggested that this community of rodents provided directed dispersal. Animals preferred to cache seeds in microsites that were favorable for emergence or survival of seedlings and avoided caching in microsites in which seedlings fared worst. Seeds buried at depths typical of animal caches (5-25 mm) produced at least five times more seedlings than did seeds on the forest floor. The four species of rodents differed in the quality of dispersal they provided. Small, shallow caches made by deer mice most resembled seeds dispersed by abiotic processes, whereas many of the large caches made by ground squirrels were buried too deeply for successful emergence of seedlings. Chipmunks made the greatest number of caches within the range of depths and microsites favorable for establishment of pine seedlings. Directed dispersal is an important element of the population dynamics of Jeffrey pine, a dominant tree species in the eastern Sierra Nevada. Quantifying the occurrence and dynamics of directed dispersal in this and other cases will contribute to better understanding of mutualistic coevolution of plants and animals and to more effective management of ecosystems in which directed dispersal is a keystone process.

18 Reads
  • Source
    • "Not all of the buried seeds are retrieved by small rodents and those that escape predation may establish seedlings in suitable conditions (Gómez et al. 2003; Li and Zhang 2003; Lu and Zhang 2004; Abe et al. 2006). From the plant's perspective, burial of seeds may be the most important benefit of rodent seed handling (Briggs et al. 2009). Thus, small rodents may play important roles during seed dispersal and subsequent plant regeneration (Price et al. 2000; Forget and Vander Wall 2001; Yi and Zhang 2008; Birkedal et al. 2009; van Ginkel et al. 2013; Yu et al. 2013a). "
    [Show abstract] [Hide abstract]
    ABSTRACT: Recent studies have demonstrated the higher likelihood of regeneration in forest gaps compared with the understory for the dominant species in pine-oak mixed forest. Here, we tested whether rodent seed predation or dispersal was beneficial for gap regeneration. We tracked the seed predation and dispersal of Quercus aliena var. acuteserrata and Pinus armandii using coded plastic tags in the forest understory close to gaps. Our results demonstrated that the proportions of initial buried seeds of both species were significantly more abundant in the forest understory compared with gaps. After seed caching, however, significantly lower proportions of the seeds of both species survived in the forest understory compared with gaps during the 30-day observation period. The final survival proportions of the seeds cached in the forest understory were lower than those cached in the gaps the next spring, which indicated that small rodents rarely retrieved scatter-hoarded seeds from forest gaps. Our findings suggest that rodent seed predation patterns contribute to the regeneration of the dominant species in gaps compared with the understory in a pine-oak mixed forest. In the study area, reforestation usually involves planting seedlings but direct sowing in forest gaps may be an alternative means of accelerating forest recovery and successional processes.
    Acta theriologica 10/2014; 59(4). DOI:10.1007/s13364-014-0192-y · 1.20 Impact Factor
  • Source
    • "From a seed dispersal perspective, scatter hoarding is more beneficial because germination and seedling establishment is better due to, for example reduced density-dependent seed mortality and/or predation (McAuliffe 1990; Vander Wall 1994; Pizo 1997; Forget, Kitajima & Foster 1999; Wenny 1999). Dispersal to microsites that favour seed germination and seedling establishment (Vander Wall 1993a; Pearson & Theimer 2004; Briggs, Vander Wall & Jenkins 2009) is also higher when distributed widely in small caches compared to large larders. However, rodents often have mixed food-storing strategies, and many chipmunks and squirrels (Sciuridae), kangaroo rats (Dipodomys) and pocket mice (Perognathus, Heteromys) store seeds both in larders in their burrows and in scattered surface caches (Vander Wall 1990). "
    [Show abstract] [Hide abstract]
    ABSTRACT: Summery The water-impermeable seed coat of ‘hard’ seeds is commonly considered a dormancy trait. Seed smell is, however, strongly correlated with seed water content, and hard seeds are therefore olfactionally cryptic to foraging rodents. This is the rationale for the crypsis hypothesis, which proposes that the primary functions of hard seeds are to reduce seed predation and promote rodent seed dispersal. We use a mechanistic model to describe seed survival success of plants with different dimorphic soft and hard seed strategies. The model is based on established empirical–ecological relationships of moisture requirements for germination and benefits of seed dispersal, and on experimentally demonstrated relationships between seed volatile emission, predation and predator escape. We find that water-impermeable seed coats can reduce seed predation under a wide range of natural humidity conditions. Plants with rodent dispersed seeds benefit from producing dimorphic soft and hard seeds at ratios where the anti-predator advantages of hard seeds are balanced by the dispersal benefits gained by producing some soft seeds. The seed pathway predicted from the model is similar to those of experimental seed-tracking studies. This validates the relevance and realism of the ecological mechanisms and relationships incorporated in the model. Synthesis. Rodent seed predators are often also important seed dispersers and have the potential to exert strong selective pressures on seeds to evolve methods of avoiding detection, and hard seeds seem to do just that. This work suggests that water-impermeable hard seeds may evolve in the absence of a dormancy function and that optimal seed survival in many environments with rodent seed predators is obtained by plants having a dimorphic soft and hard seed strategy.
    Journal of Ecology 08/2014; 102(6). DOI:10.1111/1365-2745.12323 · 5.52 Impact Factor
  • Source
    • "The mechanism proposed to explain the persistence of these species is that seed dispersal by scatter-hoarding rodents may have substituted the services provided by the original dispersers (Guimarães et al. 2008). Scatter-hoarding rodents bury intact seeds in shallow caches, and those seeds that are not retrieved by the animals, are protected from invertebrate predation, and can germinate and establish (Briggs et al. 2009, Hirsch et al. 2012, Jansen et al. 2012). Thus, seed dispersal by scatter-hoarding rodents results from forgotten cached or re-cached intact seeds. "
    [Show abstract] [Hide abstract]
    ABSTRACT: Seed predation by rodents results in directed dispersal of viable seed fragments of an endangered desert shrub. Ecosphere 5(4): Abstract. Seed predation and seed dispersal are important ecological processes with antagonistic effects on plant recruitment. In the southern edge of the Atacama Desert in Chile, Myrcianthes coquimbensis is an endangered, large-seeded, vertebrate-dispersed shrub that in the present-day has no known dispersers. Native rodents hoard and eat the seeds of M. coquimbensis but leave viable seed fragments at the hoarding sites; soil interspaces within rock outcrops where seedlings recruit. Here we examined whether rodents act as effective dispersers of M. coquimbensis by discarding viable seed fragments in sites suitable for recruitment. We simulated different levels of endosperm loss to determine if seedlings could develop from seed fragments. We assessed how frequently rodents discarded fragments, and the probability that these fragments produced seedlings. Finally, we compared emergence and seedling survival at the hoarding sites and in two other habitats where seeds arrive to evaluate the suitability of the hoarding sites. Seeds of M. coquimbensis developed seedlings even after 87% of their storage tissue was removed. Rodents left seed fragments in more than 50% of the trials; almost 60% of the discarded fragments produced seedlings. Seedlings did not emerge from open ground habitats, and emergence was higher under M. coquimbensis shrubs than in rock habitats. Survival of two-year-old seedlings was higher in rock habitats than under conspecific adult shrubs. Our results suggest that rodents may play a dual role in the recruitment dynamics of M. coquimbensis, acting simultaneously as seed predators and effective dispersers. Therefore, though seed predators impose costs, their net effect on plant fitness in this system—where dispersers of large-seeded species have been lost—is likely positive.
    Ecosphere 04/2014; 5(4):1-9. DOI:10.1890/ES13-00283.1 · 2.26 Impact Factor
Show more