How intraspecific variation in seed‐dispersing animals matters for plants

Seed dispersal by animals is a complex phenomenon, characterized by multiple mechanisms and variable outcomes. Most researchers approach this complexity by analysing context‐dependency in seed dispersal and investigating extrinsic factors that might influence interactions between plants and seed dispersers. Intrinsic traits of seed dispersers provide an alternative way of making sense of the enormous variation in seed fates. I review causes of intraspecific variability in frugivorous and granivorous animals, discuss their effects on seed dispersal, and outline likely consequences for plant populations and communities. Sources of individual variation in seed‐dispersing animals include sexual dimorphism, changes associated with growth and ageing, individual specialization, and animal personalities. Sexual dimorphism of seed‐dispersing animals influences seed fate through diverse mechanisms that range from effects caused by sex‐specific differences in body size, to influences of male versus female cognitive functions. These differences affect the type of seed treatment (e.g. dispersal versus predation), the number of dispersed seeds, distance of seed dispersal, and likelihood that seeds are left in favourable sites for seeds or seedlings. The best‐documented consequences of individual differences associated with growth and ageing involve quantity of dispersed seeds and the quality of seed treatment in the mouth and gut. Individual specialization on different resources affects the number of dispersed plant species, and therefore the connectivity and architecture of seed‐dispersal networks. Animal personalities might play an important role in shaping interactions between plants and dispersers of their seeds, yet their potential in this regard remains overlooked. In general, intraspecific variation in seed‐dispersing animals often influences plants through effects of these individual differences on the movement ecology of the dispersers. Two conditions are necessary for individual variation to exert a strong influence on seed dispersal. First, the individual differences in traits should translate into differences in crucial characteristics of seed dispersal. Second, individual variation is more likely to be important when the proportions of particular types of individuals fluctuate strongly in a population or vary across space; when proportions are static, it is less likely that intraspecific differences will be responsible for changes in the dynamics and outcomes of plant–animal interactions. In conclusion, focusing on variation among foraging animals rather than on species averages might bring new, mechanistic insights to the phenomenon of seed dispersal. While this shift in perspective is unlikely to replace the traditional approach (based on the assumption that all important variation occurs among species), it provides a complementary alternative to decipher the enormous variation observed in animal‐mediated seed dispersal.     

Ants remove virtually all western myall (Acacia papyrocarpa Benth.) seeds at Middleback,South Australia

Abstract Ants can have a profound effect on the numbers of seeds present in the seed-bank. We investigated the removal of seeds of an important arid zone tree species, the western myall (Acacia papyrocarpa Benth.). The species has seed characteristics typical of other Acacia species: a hard seed-coat and a small, white aril or elaiosome; the latter is reported to be attractive to ants. An experiment was conducted to see how rapidly and completely the seeds would be removed under various caging treatments. Observations were also made to discover the major seed removers and the fate of the seeds. Seed removal was rapid (< 12h) and was almost entirely by ants, and while our observations were not conclusive, we speculate that much of the seed supply is effectively destroyed by seed harvester ants which thus act as true granivores, not seed dispersers. Whether this matters for western myall in the long term is problematic because the species is so long-lived; rare but successful recruitment events may well be sufficient for its long-term survival.     

Large‐scale patterns of seed removal by small mammals differ between areas of low‐ versus high‐wolf occupancy

Because most tree species recruit from seeds, seed predation by small‐mammal granivores may be important for determining plant distribution and regeneration in forests. Despite the importance of seed predation, large‐scale patterns of small‐mammal granivory are often highly variable and thus difficult to predict. We hypothesize distributions of apex predators can create large‐scale variation in the distribution and abundance of mesopredators that consume small mammals, creating predictable areas of high and low granivory. For example, because gray wolf (Canis lupus) territories are characterized by relatively less use by coyotes (C. latrans) and greater use by foxes (Vulpes vulpes, Urocyon cinereoargentus) that consume a greater proportion of small mammals, wolf territories may be areas of reduced small‐mammal granivory. Using large‐scale, multiyear field trials at 22 sites with high‐ and low‐wolf occupancy in northern Wisconsin, we evaluated whether removal of seeds of four tree species was lower in wolf territories. Consistent with the hypothesized consequences of wolf occupancy, seed removal of three species was more than 25% lower in high‐wolf‐occupancy areas across 2 years and small‐mammal abundance was more than 40% lower in high‐wolf areas during one of two study years. These significant results, in conjunction with evidence of seed consumption in situ and the absence of significant habitat differences between high‐ and low‐wolf areas, suggest that top‐down effects of wolves on small‐mammal granivory and seed survival may occur. Understanding how interactions among carnivores create spatial patterns in interactions among lower trophic levels may allow for more accurate predictions of large‐scale patterns in seed survival and forest composition.     

Insect pests of Norway spruce cones: incidences and altitude preferences with emphasis on Cydia strobilella (L.)

Pest species infesting spruce cones were identified from 109 locations approved for the collection of seed material in the Czech Republic. Four (occasionally five) cones were studied from each location, and 448 cones were examined in total. Each cone was assessed for external damage and was then cut open along the spine. The predominant pest species, Cydia strobilella, was detected in 65% of the cones, while the next most common species, Dioryctria abietella, was detected in 13% of the cones. Ernobius abietis, Eupithecia sp., and Thekopsora areolata were less numerous. Kaltenbachiola strobi and Megastigmus sp. were recorded sporadically. Most cones (68%) were infested with only one species. The maximum number of C. strobilella larvae detected in one cone was 13. Cone damage resulting from C. strobilella declined markedly with increasing elevation. Thus, cone infestation by C. strobilella was greater in those forest vegetation zones located in lowlands and uplands rather than in highlands and at lower mountain elevations. The number of cones without damage tended to increase with elevation, but infestation by D. abietella was unrelated to elevation. In some cases, C. strobilella damage to cones was severe. External markings on the cone (resin and deformation) cannot by themselves serve as reliable criteria for predicting C. strobilella infestation, although cones with such signs should be preferentially assessed when seed material is inspected.     

A multi-species assessment of post-dispersal seed predation in the central Chilean Andes

BACKGROUND AND AIMS: Post-dispersal seed predation in alpine communities has received little attention despite evidence that seeds removed by granivores can decrease plant recruitment into ecosystems. Moreover, few studies have assessed the effects of removal of seeds of a range of species after dispersal on the seeds remaining in ecosystems. A comparison was made of the magnitude of seed removal by ants and birds of nine different shrubby-, herbaceous- and cushion-plant species in the central Chilean Andes in order to assess the interactions between birds, ants and wind, and the types of seeds. METHODS: A total of 324 soil-covered plates, each containing 50 seeds of one species, were placed in the field at an altitude of 2700 m and assigned to one of four treatments: control, exclusion of ants, birds, and both. The design also allowed the effects of wind to be assessed. Seed removal from plates was monitored over 20 d. KEY RESULTS: Mean accumulative seed removal by granivores averaged over all nine species combined was 25%. However, large differences between species were evident, with limited seed removal (3-11%) in three herbaceous species (Alstroemeria pallida, Sisyrinchium arenarium, Pozoa coriacea), moderate (18-33%) in five species, including a shrub (Chuquiraga oppositifolia), two herbs (Taraxacum officinale, Rhodophiala rhodolirion), and two cushion-plants (Laretia acaulis, Azorella monantha), and substantial (78%) in the shrub Anarthrophyllum cumingii. The magnitudes of losses caused by birds compared with ants did not differ for the majority of species, although removal by birds was greater than by ants in A. cumingii, and smaller for C. oppositifolia. CONCLUSIONS: Post-dispersal seed removal is shown to be an important cause of decreased potential plant species recruitment into alpine ecosystems. The substantial differences in the magnitude of seed losses to ants and birds demonstrate the need for evaluation of seed removal on a wide range of species in any given ecosystem.     

Mechanisms affecting the fate of Prosopis flexuosa (Fabaceae,Mimosoideae) seeds during early secondary dispersal in the Monte Desert,Argentina

Abstract The fate of seeds during secondary dispersal is largely unknown for most species in most ecosystems. This paper deals with sources of seed output of Prosopis flexuosa D.C. (Fabaceae, Mimosoideae) from the surface soil seed‐bank. Prosopis flexuosa is the main tree species in the central Monte Desert, Argentina. In spite of occasional high fruit production, P. flexuosa seeds are not usually found in the soil, suggesting that this species does not form a persistent soil seed‐bank. The magnitude of removal by animals and germination of P. flexuosa seeds was experimentally analysed during the first stage of secondary dispersal (early autumn). The proportion of seeds removed by granivores was assessed by offering different types of diaspores: free seeds, seeds inside intact endocarps, pod segments consisting of 2–3 seeds, and seeds from faeces of one herbivorous hystricognath rodent, the mara (Dolichotis patagonum). The proportion of seeds lost through germination was measured for seeds inside intact endocarps, seeds inside artificially broken endocarps, and free seeds. Removal by ants and mammals is the main factor limiting the formation of a persistent soil seed‐bank of P. flexuosa: >90% of the offered seeds were removed within 24 h of exposure to granivores in three of four treatments. Seeds from the faeces of maras, on the other hand, were less vulnerable to granivory than were other types of diaspores. These results suggest that herbivory might be an indirect mechanism promoting seed longevity in the soil (and likely germination) by discouraging granivore attack. On the other hand, germination did not seem to have an important postdispersal impact on the persistence of P. flexuosa seeds in the soil. Both direct and indirect interactions between vertebrate herbivores and plants may foster P. flexuosa's seed germination in some South American arid zones.     

Seed removal in a tropical North American desert: an evaluation of pre‐ and post‐dispersal seed removal in Stenocereus stellatus

• To determine seed removal influence on seed populations, we need to quantify pre‐ and post‐dispersal seed removal. Several studies have quantified seed removal in temperate American deserts, but few studies have been performed in tropical deserts. These studies have only quantified pre‐ or post‐dispersal seed removal, thus underestimating the influence of seed removal. We evaluated pre‐ and post‐dispersal seed removal in the columnar cactus Stenocereus stellatus in a Mexican tropical desert.
• We performed selective exclosure experiments to estimate percentage of seeds removed by ants, birds and rodents during the pre‐ and post‐dispersal phases. We also conducted field samplings to estimate abundance of the most common seed removers.
• Birds (10–28%) removed a higher percentage of seeds than ants (2%) and rodents (1–4%) during pre‐dispersal seed removal. Melanerpes hypopolius was probably the main bird removing seeds from fruits. Ants (62–64%) removed a higher percentage of seeds than birds (34–38%) and rodents (16–30%) during post‐dispersal seed removal. Pogonomyrmex barbatus was probably the main ant removing seeds from soil.
• Birds and ants are the main pre‐ and post‐dispersal seed removers in S. stellatus, respectively. Further studies in other S. stellatus populations and plants with different life forms and fruit types will contribute to evaluate seed removal in tropical American deserts.

     

Seed supply as a limiting factor for granivorous bird assemblages in the Monte Desert,Argentina

Seed availability may limit the size of granivorous bird populations, particularly in desert environments. Seasonal and annual fluctuations in the abundance of granivorous birds were studied at three sites in the Northern Monte Desert, Argentina. The way in which these changes were related to seed supply was also studied. Granivore abundance and biomass, as well as seed abundance, were greater in winter. Changes in total granivore abundance were mostly because of variations in numbers of the most mobile bird species, all of which were found to have similar patterns of variation in their abundance. Evidence suggests that during the non‐breeding season, the most mobile species are able to track patches of high seed availability over long distances, whereas the abundance of less vagile species largely depends on the local ecological conditions. Seed supply is a proximate factor that limits the abundance of granivorous birds in the Monte Desert during the winter, but does not limit species richness. Granivore abundance was not correlated with seed supply in spring.