Growth in seed dispersal studies has been fast-paced since the seed disperser effectiveness (SDE) framework was developed 17 yr ago. Thus, the time is ripe to revisit the framework in light of accumulated new insight. Here, we first present an overview of the framework, how it has been applied, and what we know and do not know. We then introduce the SDE landscape as the two-dimensional representation of the possible combinations of the quantity and the quality of dispersal and with elevational contours representing isoclines of SDE. We discuss the structure of disperser assemblages on such landscapes. Following this we discuss recent advances and ideas in seed dispersal in the context of their impacts on SDE. Finally, we highlight a number of emerging issues that provide insight into SDE. Overall, the SDE framework successfully captures the complexities of seed dispersal. We advocate an expanded use of the term dispersal encompassing the multiple recruitment stages from fruit to adult. While this entails difficulties in estimating SDE, it is a necessary expansion if we are to understand the central relevance of seed dispersal in plant ecology and evolution.

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Seed dispersal effectiveness revisited: a conceptual review

Some plants that are dispersed by scatter-hoarding animals appear to have evolved the ability to manipulate the behaviour of those animals to increase the likelihood that seeds and nuts will be stored and that a portion of those items will not be recovered. Plants have achieved this in at least four ways. First, by producing large, nutritious seeds and nuts that are attractive to animals and that stimulate hoarding behaviour. Second, by imposing handling costs that cause animals to hoard rather than to eat items immediately. These handling costs can take one of two forms: physical barriers (e.g. hard seed coats) that take time to remove and secondary chemicals (e.g. tannins) that impose metabolic costs. Third, by masting, where a population of plants synchronizes reproductive effort, producing large nut crops at intervals of several years. Mast crops not only satiate seed predators, but also increase the amount of seed dispersal because scatter-hoarding animals are not easily satiated during caching (causing animals to store more food than they can consume) but are satiated during cache recovery. And fourth, by producing seeds that do not emit strong odours so that buried seeds are less likely to be discovered. These, and perhaps other, traits have increased the relative success of plant species with seeds dispersed by scatter-hoarding animals.

/pdf/how-plants-manipulate-the-scatter-hoarding-behaviour-of-seed-fk59yf7hl9.pdf

How plants manipulate the scatter-hoarding behaviour of seed-dispersing animals

Detection in studies of species abundance and distribution is often imperfect. Assuming perfect detection introduces bias into estimation that can weaken inference upon which understanding and policy are based. Despite availability of numerous methods designed to address this assumption, many refereed papers in ecology fail to account for non-detection error. We conducted a quantitative literature review of 537 ecological articles to measure the degree to which studies of different taxa, at various scales, and over time have accounted for imperfect detection. Overall, just 23% of articles accounted for imperfect detection. The probability that an article incorporated imperfect detection increased with time and varied among taxa studied; studies of vertebrates were more likely to incorporate imperfect detection. Among articles that reported detection probability, 70% contained per-survey estimates of detection that were less than 0.5. For articles in which constancy of detection was tested, 86% reported significant variation. We hope that our findings prompt more ecologists to consider carefully the detection process when designing studies and analyzing results, especially for sub-disciplines where incorporation of imperfect detection in study design and analysis so far has been lacking.

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Accounting for imperfect detection in ecology: a quantitative review.

A mechanistic understanding of seed movement and survival is important both for the development of theoretical models of plant population dynamics, spatial spread, and community assembly, and for the conservation and management of plant communities under global change. While models of wind-borne seed dispersal have advanced rapidly over the past two decades, models for animal-mediated dispersal have failed to make similar progress due to their dependence on interspecific interactions and complex, context-dependent behaviours. In this review, we synthesize the literature on seed dispersal and consumption by scatter-hoarding, granivorous rodents and outline a strategy for development of a general mechanistic seed-fate model in these systems. Our review decomposes seed dispersal and survival into six distinct sub-processes (exposure, harvest, allocation, preparation, placement, and recovery), and identifies nine intermediate (latent) variables that link physical state variables (e.g. seed and animal traits, habitat structure) to decisions regarding seed allocation to hoarding or consumption, cache placement and management, and deployment of radicle-pruning or embryo excision behaviours. We also highlight specific areas where research on these intermediate relationships is needed to improve our mechanistic understanding of scatter-hoarder behaviour. Finally, we outline a strategy to combine detailed studies on individual functional relationships with seed-tracking experiments in an iterative, hierarchical Bayesian framework to construct, refine, and test mechanistic models for context-dependent, scatter-hoarder-mediated seed fate.

Seed fate and decision‐making processes in scatter‐hoarding rodents

Scatter-hoarding rodents play an important dispersal role for many large-seeded plants. Seed traits affect their foraging behavior; however, it is difficult to isolate their effects because of the covariance among traits. Here, we used artificial seeds to partition the effects of seed size, tannin content, and nutrient content on scatter-hoarding rodents in a natural pine forest in Northwest Yunnan, China. Apodemus, a common genus of Old World rodents, consistently consumed small seeds in situ but removed medium-sized seeds (1.2-2.5 cm in diameter) and transported bigger seeds farther. Seed nutrient and tannin contents also significantly influenced rodents' behavior, but response varied substantially between years. Rodent behavior did involve some aspects of multivariate optimization. Our results strongly indicate that seed size is a decisive factor for scatter-hoarding rodents in the choice between seed predation and dispersal, while nutrient and tannin content played a less consistent role, possibly responding to confounding factors in the community. This result also has important implications for seed production by trees, which can improve the probability of long-distance dispersal of high-quality offspring by simply making them larger. The ability to tease apart the relative influence of different seed traits on the behavior of predators provides powerful insight into this important coevolutionary dynamic.

/pdf/seed-size-more-than-nutrient-or-tannin-content-affects-seed-3y9b4h8uhp.pdf

Seed size, more than nutrient or tannin content, affects seed caching behavior of a common genus of Old World rodents

Scatter-hoarding rodents should space food caches to maximize cache recovery rate (to minimize loss to pilferers) relative to the energetic cost of carrying food items greater distances. Optimization models of cache spacing make two predictions. First, spacing of caches should be greater for food items with greater energy content. Second, the mean distance between caches should increase with food abundance. However, the latter prediction fails to account for the effect of food abundance on the behavior of potential pilferers or on the ability of caching individuals to acquire food by means other than recovering their own caches. When considering these factors, shorter cache distances may be predicted in conditions of higher food abundance. We predicted that seed caching distances would be greater for food items of higher energy content and during lower ambient food abundance and that the effect of seed type on cache distance variation would be lower during higher food abundance. We recorded distances moved for 8636 seeds of five seed types at 15 locations in three forested sites in Pennsylvania, USA, and 29 forest fragments in Indiana, USA, across five different years. Seed production was poor in three years and high in two years. Consistent with previous studies, seeds with greater energy content were moved farther than less profitable food items. Seeds were dispersed less far in seed-rich years than in seed-poor years, contrary to predictions of conventional models. Interactions were important, with seed type effects more evident in seed-poor years. These results suggest that, when food is superabundant, optimal cache distances are more strongly determined by minimizing energy cost of caching than by minimizing pilfering rates and that cache loss rates may be more strongly density-dependent in times of low seed abundance.

https://www.jstor.org/stable/pdfplus/27651399.pdf

Determinants of seed removal distance by scatter-hoarding rodents in deciduous forests

Scatter hoarding is a common food-hoarding strategy of many granivores, known to significantly contribute to seed dispersal. Models of scatter hoarding typically hold that the spatial distribution of the scatter hoards made by birds and mammals result from a trade-off between the energetic cost of spacing caches and the increased risk of pilferage as cache densities increase. Here, we present evidence from 3 field experiments that eastern gray squirrels (Sciurus carolinensis) rely on an alternative strategy in which preferred food items are stored in open habitats, beyond tree crowns, where the probability of predation is higher but the risk of cache pilferage is also reduced (hereafter the habitat structure hypothesis). In the first 2 experiments, squirrels cached larger, more profitable acorns at significantly greater distances from canopy edges than smaller acorns, which were more often cached under trees. In the third experiment, in which we tested the effects of both tree canopy cover and cache density on pilferage rates, we found no effect of density on pilferage rates but significantly higher pilferage rates under canopy cover. Our results indicate that habitat heterogeneity, potentially as it relates to predation risks, influences the distribution of scatter-hoarded seeds, with more profitable seeds placed in more open vegetation beyond the shadow of parent plants. We suggest that this behavior may reflect a general strategy of other scatter-hoarding mammals and birds that likely increases the probability of dispersal and establishment of seeds.

Thomas A. Contreras

Papers

Determinants of seed removal distance by scatter-hoarding rodents in deciduous forests

Do scatter hoarders trade off increased predation risks for lower rates of cache pilferage

The innate basis of food-hoarding decisions in grey squirrels: evidence for behavioural adaptations to the oaks