For wind dispersal, modelling suggests that even moderate topographic variability can have large impacts on variation in dispersal distances and directionality . Finally, slope steepness influences dispersal distances of heavy seeds, which are more likely to roll down downhill , and the likelihood of seed dispersal via runoff . Individual plants might also differ in the quantity and quality of animal-mediated seed dispersal due to the actions of thirdparty players. Some of these effects are mediated by vegetation structure, with plants in more open and risky places receiving fewer visits by dispersers . In other situations, animals respond to olfactory, visual or acoustic predator cues, leading to reduced seed removal rates in frugivorous birds , bats and granivorous rodents . In addition, rodents are sensitive to ungulate presence because of trampling risk or disturbance by rooting ; in Q. ilex, the presence of ungulates was associated with lower quality seed dispersal by rodents and changes in caching sites . Finally, responses to predators and competitors can interact with other traits, such as the presence and concentration of deterrents . Insects frequently infest fruit pulp, seeds or dispersal structures, which can affect seed dispersal. Howler monkeys preferentially feed in Ocotea diospyrifolia trees with high fruit infestation by curculionids and low fruit infestation by moths . The seed parasitoid wasp Macrodasyceras hirsutum reduces attractiveness of Ilex integra berries to frugivorous birds through ‘colour manipulation’; infested fruits are less likely to ripen and turn red, decreasing the risk that the fruits will be eaten and wasps killed .

In synzoochorous dispersal, seed infestation can increase the probability of rejection or of immediate consumption , round plastic plant pot but generally reduces caching rates , thus decreasing dispersal quality. However, not all scatter hoarders discriminate between infested and sound seeds, particularly before insect emergence . Note that these synzoochorous examples are based on responses to individual seeds and it is unknown to what degree they translate into selection among trees differing in infestation levels. Insect attack also affects anemochory. For example, Rhinocyllus conicus larvae feeding on C. nutans receptacles induce callus formation, resulting in inhibited seed release, shortened pappus filaments and reduced dispersal distances . In turn, insect infestation is often affected by masting , thereby creating another, indirect pathway through which temporal variation in seed output can affect seed dispersal.Most of what we know about intraspecific variation in seed dispersal represents a snapshot in time—a frame or two in a potentially long movie of life. While these frames might accurately represent the fitness outcomes for an annual plant, the majority of plants discussed in this review are long-lived perennials that are interacting with an extremely dynamic world where both intrinsic and extrinsic factors vary through time. Although we are not in a position to evaluate the overall consequences of this variation, it is important to acknowledge the variation exists. Fruit crop sizes vary between years. Sometimes this variation is relatively subtle and driven by such factors as resource availability or climatic conditions . Sometimes the variation is extreme, as seen in masting species . Different dispersal kernels are necessary to capture mast versus non-mast years , with potentially greater LDD when acorn density is low . The fitness impacts of this variation should depend at least partially on how synchronous fruit crop size variation is in the population and community. Fruit crop size also varies over longer, ontogenetic time scales; crop sizes increase with perennial plant age and size, often plateauing at some point and remaining relatively constant until death, sometimes showing declines with senescence late in life .

Many other intrinsic traits relevant to intraspecific variation in dispersal are temporally dynamic. Fruit/seed size, and most likely such traits as pulp:seed ratio, vary across years . Plant height increases ontogenetically . Rewards and deterrents can change from year to year and in some cases even seasonally. Temporal variation in extrinsic factors, or the ecological context, is perhaps even more extreme. Fruiting neighbourhoods can change from year to year as different individuals and species respond differently to changing resources and climate . Other aspects of habitat structure around individual plants can change through time due to successional processes and demographic processes , as well as anthropogenic impacts . Lastly, interactions with non-disperser animal communities can vary greatly from year to year as a function of, among other drivers, changes in individual crop sizes and in fruiting neighbourhoods, and population fluctuations of other interacting animal species .Although many exceptions exist, much work on intraspecific variation in seed dispersal has taken a more or less univariate approach; for example, the impact of fruit crop size, fruit size or plant height on dispersal. Alternatively, some address multiple traits affecting dispersal and quantify the relative importance of each and the presence or absence of interactions. In a recent study using an individual-plant-based network analysis of frugivory, locations of individual H. succosa trees within the network were determined by a combination of plant height, fruit size and sugar concentration, with shorter individuals with larger fruits and intermediate sugar concentration being most central . Nonetheless, the true complexity of dispersal is often overlooked. In this review we have also taken primarily a univariate approach, which we argue has value, especially at our early stage of understanding the drivers of inter individual variation in seed dispersal. However, it is critical to understand that we do not believe that this is really how the world exists.

We noted the difficulties of knowing what animal seed dispersers base their harvesting decisions on when so many potentially important traits co-vary: fruit size, absolute and relative quantity of reward, seed number and size, nutrients, toxins and more . For example, do frugivores select fruits to harvest based on size per se or on the underlying variation in pulp:seed ratio ? Such complexities surely exist in other dispersal systems as well. For example, in anemochorous plants, the size of the dispersal structure increases with seed mass, but generally not sufficiently to maintain a constant wing loading . Co-variation of seed release height and seed terminal velocity , and of abscission force and terminal velocity have also been reported. It is highly likely that co-variation of traits relevant to seed dispersal is as extensive with wind dispersal as with frugivory. Complexity also arises in animal-dispersed species because foraging animals often make foraging decisions hierarchically . For example, foraging frugivores must first select the foraging patch, then choose the individuals to feed in, and then choose which fruits to harvest from that plant. In addition, multiple cues may be used hierarchically at any single stage of this process. For example, experiments with the large fleshy-fruited shrub C. monogyna elegantly demonstrated hierarchical selection by Turdus migratorius of individual trees in which to forage. First, birds preferred trees with larger crop sizes, but if crop sizes were constant, they preferred plants with larger fruits, and, finally, if fruit size was constant, they preferred plants with greater pulp:seed ratios . Understanding variation in seed dispersal is further complicated by the concomitant inter individual variation in seed dispersers, including sexual dimorphism, ontogenetic changes, inter individual variation in specialization and unique animal personalities . For example, our discussion of fruit size variation in M. communis and its effect on fruit availability to different seed dispersers was based on measured intra individual and inter individual variation in fruit diameters but only mean gape width for the dispersal agents . Interpretations could be different if inter individual variation in the seed disperser species was also incorporated. More generally, 25 liter rount pot inter individual variation in plants and dispersers interact and it might be difficult to understand one without understanding the other . Plants almost certainly respond at the individual level to variation in how seed dispersers interact with them; these eco-evolutionary feedbacks mean that intraspecific variation is important in both sides of the interaction, perhaps even intensifying the individual-level variation in both players . Further complexity is likely in particular dispersal systems, such as for example with diplochorous dispersal, where dispersal is accomplished by a sequence of steps that involve different dispersal agents such as primary dispersal by a frugivorous bird and secondary dispersal by a rodent . We predict that, all else being equal, diplochorous dispersal systems would have even greater inter individual variation in seed dispersal success than non-diplochorous systems given that variability arising during the second phase of dispersal is building on variability created during the first phase of dispersal.

For example, as discussed previously, intraspecific variation in seed size can affect selection by both frugivorous birds and rodents, sometimes in the same way and sometimes not.While we show substantial evidence that drivers of intraspecific variation in seed dispersal are diverse and pervasive, we also reveal large gaps in our understanding, partly due to a paucity of research directly addressing intraspecific, especially inter individual, variation in seed dispersal, and partly due to the complexity of interactions among drivers. Our understanding is limited further by the existing empirical work’s focus on the quantity of seed dispersal, with much less consideration of the quality of dispersal or LDD. Of particular interest are the intrinsic trait-based drivers that can respond to natural selection. The best-supported and best-understood intrinsic driver of inter individual variation in seed dispersal is crop size; with more seeds produced, more seeds are dispersed. Crop size is also likely the most widespread driver, being relevant to most if not all forms of dispersal. Though less well supported and less well understood, fruit/seed size is likely the second most widespread intrinsic driver. Again, it seems to be relevant to a broad range of seed dispersal modes. However, when it comes to animal-mediated dispersal we do not have a good understanding of the ultimate cause of size-based fruit or seed selection—is it fruit/seed size per se, or some co-varying trait such as pulp:seed ratio? Remaining intrinsic drivers are even more poorly understood, though apparently range from widespread but weak, such as plant height, to sporadic and variable in strength, such as colour polymorphism. For extrinsic drivers, a variety of studies have addressed the impact of fruiting neighbourhoods on inter individual variation in seed dispersal, but we do not understand well when to expect competition for dispersers and when to expect facilitation of dispersal. With respect to habitat structure, much relevant work has been from the perspective of anthropogenic impacts of habitat fragmentation and degradation on seed dispersal rather than from the perspective of interspecific variation in seed dispersal. Beyond limited empirical work, we are further hindered by an even greater lack of theory related to the drivers of intraspecific, especially inter individual variation in seed dispersal. While there have been some theoretical developments around fruit crop size and seed dispersal success , we are aware of no other developed theory that can guide our understanding of the drivers of inter individual variation in dispersal and potential demographic and evolutionary responses to such variation. Looking forward towards potential research directions, in Box 2 we highlight a selection of outstanding questions concerning intrinsic drivers of intraspecific variation in seed dispersal that we personally believe to be especially informative and intriguing to answer. We present these questions as a starting point to advance our understanding of intraspecific drivers of seed dispersal. One promising approach to answer these questions and disentangle the complexity inherent in intraspecific seed dispersal is a frugivore-centred modelling approach . This approach advocates parameterizing field data on intrinsic animal factors and behaviour, as well as extrinsic landscape factors, to test and quantify the strength of the variables affecting the spatially explicit deposition of seeds across the landscape . Mechanistic simulations can be used in a hierarchical manner to test the effect of multiple factors one at a time, to quantify their relative influence on patterns of seed deposition . Studies using this approach have successfully quantified the impact on seed dispersal of edge-following behaviour in a fragmented landscape , fruiting neighbourhoods and drivers of reduced LDD . Although primarily envisioned to study endozoochory, similar methods have been applied to epizoochory and other dispersal modes by considering relevant intrinsic and extrinsic factors . Additionally, a powerful molecular approach that matches individual seeds or seedlings to maternal plants across dispersal modes is also promising for studying individual variation in seed dispersal and may compliment simulation modelling approaches. D