However, given that height of reproductive adults varies substantially more among than within species, it need not follow that the more limited inter individual variation in plant height will be a major driver of inter individual variation in seed dispersal distances. Nonetheless, limited empirical evidence suggests that inter individual height variation might be at least a minor driver of inter individual variation in dispersal, at least for abiotically dispersed species. With anemochory, plant height has been shown to be positively related to dispersal distances in trees and herbaceous perennials , in some cases relatively strongly . In Carduus nutans, height, and therefore dispersal potential, is environmentally plastic, increasing with simulated climate change . Interestingly, increasing tree height in Lophopetalum wightianum not only led to greater dispersal distances and larger seed shadows, but also more even seed dispersion, potentially decreasing density dependent mortality . Norghauer et al. suggest that tree height does not affect dispersal distances of mahogany in Amazonian forests because all reproductive trees are emergent above the canopy and exposed to winds. Note, however, that much of our understanding comes from controlled releases of seeds at fixed heights in wind tunnels, and that the heterogeneity of the real world likely reduces the explanatory power of plant height. Intraindividual variation in seed release height could further obscure any potential inter individual variation in dispersal distances based on variation in plant height. Increasing height resulted in increasing dispersal distances in the mustards Erysimum mediohispanicum , Arabidopsis thaliana and Lepidium campestre , but not in O. acetosella .
We have less direct evidence that height is important for biotic dispersal. Interspecific studies suggest that seed presentation height can affect the frequency of epizoochorousdispersal , drainage collection pot but data for intraspecific effects of height variation are limited. In two studies on small tropical trees, variation in inter individual plant height affected endozoochorous seed dispersal; in Casearia corymbosa, plant height very weakly affected fruit removal , and in Henrietta succosa, dispersers favoured shorter individuals . Other studies have documented vertical segregation of frugivore communities in tropical forests , so fruiting conspecifics of different heights may have at least marginally different disperser assemblages, which could affect both the quantity and quality of dispersal. Effects of variation in rewards and deterrents on seed dispersal have been studied extensively, though mostly from the perspective of interspecific differences ; effects of intraspecific variation have received much less attention. Nonetheless, available data suggest that inter individual variation in rewards and deterrents may be an important driver of inter individual variation in seed dispersal in some cases. Intraspecific variation in fleshy fruit seed dispersal driven by intraspecific variation in rewards offered to animal dispersers has been addressed in a variety of ways with some studies focusing on the quality of the reward, and some on the absolute or relative quantity of reward. Interspecific comparisons show that fruit colour is predictive of protein , sugar and lipid concentrations , and that these signals can be effective even if relationships are weak . We have long known of inter individual variation in fruit sugar content and that dispersers can distinguish these differences by taste . However, it is not known whether dispersers can distinguish intraspecific differences in nutrients based on colour.
Nonetheless, dispersers distinguish among plants that differ in rewards in some manner . In China, the frequency with which the deer Muntiacus muntjak visited fruiting Choerospondias axillaris trees was correlated with mean Kcal/fruit . Similarly, birds selected for Celtis ehrenbergiana trees and Sambucus pubens shrubs with greater mean sugar concentration of fruits. However, frugivores preferentially fed on Henriettea succosa individuals with intermediate sugar concentrations . These limited results suggest that variation in fruit energy content is a potential driver of inter individual variation in seed dispersal. We are aware of no evidence that endozoochorous dispersers discriminate among plants based on variation in other nutrients. Individual Virola nobilis trees varied substantially in protein, lipid and non-structural carbohydrate content, but this variation did not explain variation among trees in seed dispersal . There is more extensive evidence that either the absolute or relative quantity of reward is important in fruiting plant selection by dispersers. As noted previously, independent of body size, three rodent species preferentially selected larger fruits of the shrub M. coquimbensis; larger fruits had more pulp, and it was the pulp, not the seed, that was consumed . In Ocotea tenera, dispersers selected trees with larger diameter fruits, as noted above, apparently due to the greater pulp mass; fruit diameter explained much of the variation in total pulp mass but not in the ratio of seed mass/fruit mass . However, more typical are studies demonstrating selection driven by intraspecific variation in relative rather than absolute reward per fruit. In V. nobilis , V. calophylla and C. monogyna , variation in dispersal was explained in part by mean pulp:seed ratio but not by the absolute quantity of pulp. Sometimes this resulted in the selection of smaller fruits , sometimes the selection of larger fruits . Such interactions between fruit size and either pulp quantity or pulp:seed ratio suggest caution when considering the role of fruit or seed size variation in inter individual variation in seed dispersal.
As noted, many studies report fruit selection based on fruit or seed size, and size clearly has an impact on seed dispersal, at a minimum by filtering which dispersers can swallow and disperse the seeds of endozoochorously dispersed species. However, in many cases where dispersers select larger or smaller fruits, we do not know if it is selection based on fruit/ seed size or rather selection based on a correlated trait such as absolute or relative quantity of the reward. Most work on deterrents with fleshy-fruited plants has focused on hypotheses addressing why ripe fruits contain toxins rather than assessing inter individual variation in concentrations and dispersal. In the single field study of which we are aware, mean emodin concentration in Rhamnus alaternus fruit pulp was unrelated to fruit removal rate among plant individuals in 1 year but was positively correlated with removal rate in another year . Levey and Cipollini showed that cedar waxwings feeding on artificial fruits discriminated against ‘fruits’ containing realistic concentrations of α-solamargine compared to ‘fruits’ without this glycoalkaloid, but did not discriminate among artificial fruits that differed in α-solamargine concentration. However, potential seed disperser species differ in sensitivity to varying tannin concentrations in artificial fruits . Whitehead and Poveda reported a potential environmental influence on intraspecific variation in deterrents; in Hamelia patens, artificial herbivory of subtending leaves reduced fruit removal in adjacent inflorescences due to reduced palatability, presumably a result of herbivory-induced chemical changes. Plant secondary compounds also can alter gut retention times of seeds, which can affect seed dispersal distances and germination , although we know little about the degree of natural intraspecific variation, particularly inter individual variation, in secondary compounds, and the consequences of this variation. In myrmecochorous species, chemical composition of the elaiosome has been studied mostly through interspecific comparisons of seed and elaiosome chemical profiles . Fatty acid composition in Euphorbia characias elaiosomes, especially of oleic acid, round plastic pot varies among populations and among individuals within populations, but not within individuals . In the related Helleborus foetidus, this variation is ecologically important as seed-dispersing ants preferentially visited plants with elaiosomes richer in oleic acid. Many consider oleic acid to be an attractant or behavioural trigger rather than a reward because elaiosomes are rich in other critical nutrients, such as amino acids . However, it is likely both attractant and reward since it evokes seed harvesting and it is the biosynthetic precursor of the essential nutrients linoleic and linolenic acids .In synzoochorous dispersal systems, evidence presented above that these dispersers frequently preferentially harvest, disperse, disperse farther or cache larger seeds reflects a response to the reward offered since the seed is both the propagule being dispersed and the reward offered for dispersal . However, whether it is seed size itself or energy content that drives the decision is unclear. A study with artificial seeds suggests the answer is complicated in that energy was the primary predictor of initial harvest, but size was the primary determinant of post-harvest fate . Variation in seed defences can simultaneously affect the risk of seed predation and the probability of seed dispersal. A particularly well-studied example of this phenomenon involves mechanical seed defences in synzoochorous limber pine . Cone structure in this species is under a conflicting selective pressure from the red squirrel , a predispersal seed predator, and the Clark’s nutcracker, a seed disperser .
Individuals that produce particularly well-defended cones tend to be dispersed by Peromyscus mice rather than the Clark’s nutcracker , resulting in much shorter dispersal distances and different habitat destinations of the seeds. Endocarp or seed coat thickness as a deterrent has long been considered an evolutionary response to synzoochory, in particular to managing the dual role of seed dispersal and seed predation, and there is substantial interspecific support for the idea that these dispersers select and handle seeds at least partly based on endocarp or seed coat thickness . Intraspecific studies on the effects of seed coat thickness are sparse and inconsistent; mean endocarp thickness of the palm S. romanzoffiana did not influence tree selection by the squirrel Guerlinguetus ingrami , but P. flexilis seeds with thicker seed coats were more likely to be cached by rodents and were dispersed further than seeds with thinner coats . Chemical deterrents may also play a role in inter individual dispersal by synzoochorous dispersers. Mice preferred individual Quercus serrata trees producing acorns with lower mean and coefficient of variation of tannin concentration . Similarly, rodents were less likely to remove acorns produced by Q. rubra trees from nitrogen-addition plots, presumably due to changes in chemical composition . Interpretation of these results is complicated by frequent co-variation of size, nutritional content and concentration of secondary metabolites in fruits and seeds , as discussed above with co-variation of fruit size and absolute or relative quantity of reward in fleshy-fruited plants. Interestingly, co-variation of these traits can even vary with position of fruits in the plant canopy . Recent innovative work with artificial fruits has begun to tease apart the disparate roles of size, nutrients and secondary compounds in seed selection by caching rodents. Wang and Yang manipulated seed size, tannin, fat, protein and starch content in artificial seeds and showed how all these factors affected rodent foraging. Rodents preferentially removed seeds with less tannin; increasing fats, and to a lesser degree, proteins, reduced this negative effect. Seed size, tannins and nutrient content of artificial seeds all affected various stages of the seed dispersal process by rodents, with size and nutrients tending to favour dispersal, and tannins disfavouring dispersal . In contrast, artificial seed experiments with Dasyprocta punctata in Costa Rica suggest size but not tannin concentration affect seed dispersal decisions . Furthermore, artificial seeds with different characteristics were cached in different microhabitats, which can affect quality of dispersal; larger and more nutritious seeds were most likely to be cached under shrubs .Here we consider forms of morphological variation beyond fruit and seed size that might influence inter individual variation in dispersal. The most apparent cases of morphology driving inter individual variation in seed dispersal are with heterocarpic species that produce diaspores of two or more distinct morphologies differing in dispersal ability. For example, in the annual grass Bromus tectorum plants produce caryopses with and without sterile florets attached, which differ in dispersal ability because complex diaspores attach better to animal fur . Numerous plant species produce dimorphic, soft and hard seeds . Paulsen et al. argued that this strategy enables individual plants to benefit both from the antipredation advantages of hard seeds and the dispersal advantages of soft seeds. Hard seeds emit fewer volatiles than soft seeds and are more difficult to detect by granivores such as rodents that rely on olfaction. Because granivores act both as dispersers and predators, detection might be advantageous, but can also result in seed consumption. In heterocarpic species, the relative proportions of different propagule types often vary with environmental conditions. For example, increasing stress can result in either an increase or a decrease in the production of more dispersible morphs. Interestingly, Calendula arvensis produce three distinct fruit morphs, one adapted to epizoochory, one to anemochory and one without adaptations for dispersal, although the extent of inter individual variation in the production of different morphs is unknown .