Seed Dispersal By Animals

The general characteristics of seed dispersal were already treated in Sect. 18.1 of Chap. 18. Here we limit the discussion to issues directly relevant to interactions with animals. Most animals are mobile for at least one stage of their development; in contrast, plants are fundamentally sessile, with their only chance of dispersal being as seeds. Dispersal of seeds away from the parent may have a number of selective advantages. Firstly, it may reduce the exposure of the seed to predators or pathogens that are attracted to, or supported by, the parent. Further, it reduces the potential for competition between parent and offspring and among offspring. These concepts have been encapsulated in the Janzen-Connell hypothesis (Fig. 19.14) for the high species diversity in many plant communities (introduced independently by Daniel Janzen (1970) and Joseph Connell (1971).

This hypothesis suggests that diversity is maintained by two mechanisms:
1. Mortality of seeds and seedlings increases as their density increases, and
2. Survival of seeds or seedlings increases with increasing distance from the parent.

The likelihood of being dispersed an increasing distance from the parent decreases very strongly, however, beyond the immediate vicinity of the parent plant. This phenomenon is encapsulated in the key concept of the dispersal kernel. The dispersal kernel describes either the probability of a seed being dispersed or of dispersal and successful establishment as a function of distance from the parent plant (Cousens et al. 2008). Given the decreasing probability of a seed being dispersed greater and greater distances from the parent plant, the dispersal kernel of dispersal distances will generally show a monotonic decline to zero with increasing distance, whereas the likelihood of seed establishment may initially increase with distance before declining to zero again.

Dispersal distances by frugivores are highly variable; long-range dispersal over several kilometres does occur. Some large frugivores have long gut-retention times. Birds and primates can be very fast moving, covering distances of hundreds of metres in a few minutes. Thus, dispersal distances of up to tens of kilometres are certainly possible by this dispersal mode, and distances of tens or hundreds of metres are commonplace (Hardesty et al. 2006; Seidler and Plotkin 2006; Jordano et al. 2007). Dispersal distances will be very different for different frugivores. For example, while mammals were primarily responsible for long-distance dispersal of seeds of the cherry tree Prunus mahaleb (Jordano et al. 2007), birds and bats achieved longer dispersal distances than other mammals in a Neotropical forest (Seidler and Plotkin 2006). Although a good dispersal agent transports seeds away from the parent, there may not be selection for ever-further dispersal. Wenny (2000) followed the success of bird- dispersed seeds of the tree Beilschmiedia pendula in Costa Rica. Those transported less than 10 m from the parent suffered high mortality through predation and fungal diseases. However, those transported more than 30 m had lower survival than those transported 10-20 m. This effect likely arises because the environment close to the parent is more likely than more distant environments to be suitable to this species.

A very important characteristic of animal dispersal is that animals move non-randomly through a landscape, so they may deposit seeds non-randomly in ways that benefit subsequent germination. Wenny and Levey (1998) followed individuals of five bird species dispersing seeds of Ocotea endresiana in Costa Rica, monitoring the success of seeds through to the seedling stage a year after fruits were consumed. For four of the disperser species, dispersal distances were low (less than 20 m) and so were seed survival rates. However, over half the seeds transported by three- wattled bellbirds (Procnias tricarunculata) travelled over 40 m and often ended up under gaps in the canopy, where seedling success was high. The reason for this particular distribution is linked to male bellbirds commonly displaying to females from exposed perches where they are well-lit and can be seen from a distance. This behaviour of non-random seed dispersal can have important consequences, even at the landscape level. A landmark study based on data from 90,000 forest plots across Spain demonstrated that the distribution of animal-dispersed species is more resilient to fragmentation than that of wind-dispersed species (Montoya et al. 2008). Notably, dispersal mode was a better predictor of resistance to habitat fragmentation than any other variable, including seed size, and the results could not simply be explained by phylogeny. This effect is likely to be due to non-random movements of animal seed dispersers.

Defecation or regurgitation by frugivores is not always beneficial for seed preservation and subsequent germination. Quite often it results in seed clumping (Poulsen et al. 2001; Potthoff et al. 2006), particularly at sleeping sites (Russo and Augspurger 2004). Thus seed dispersal by animals may increase competition between seeds. However, this may lead to increased seed predation, for example, by ants and rodents, but sometimes these seed predators will also disperse seeds on the ground, for example, by caching them. Caching can lead to secondary seed dispersal when caches are not retrieved. For example, Central American agoutis (Dasyprocta punctata) scatter-hoard seeds across their home ranges of approx. 3 ha as food reserves for the low-fruit season. While agoutis initially cached seeds only over short distances, they subsequently recached the seeds up to 36 times, leading to total dispersal distances of >100 m (Jansen et al. 2012). This study shows that seed dispersal is a complex process that can consist of several different steps. It also shows that categorising animals as either mutualists or antagonists can oversimplify the interactions between plants and animals since even typically antagonistic animals such as seed predators (applying also to jays and squirrels) can confer fitness benefits to plants.

The insight that plants interact simultaneously with a variety of animals, bacteria and microbes is particularly important for explaining the contents of fleshy fruits. Nutrients, in particular lipids and carbohydrates, generally favour fruit consumption, whereas defensive secondary compounds, such as tannins and phenols, reduce fruit consumption (Schaefer et al. 2003b). Fruits can be very rich in either lipids or carbohydrates such as avocado and blackberries, respectively. There is a strong negative correlation between both types of nutrients, which can be explained by their biochemical properties; carbohydrates are water soluble, whereas lipids are hydrophobic. However, they contain more than double the energy of carbohydrates or proteins per weight unit.

Given that the meaning of fleshy fruits is that they are consumed and dispersed, the existence of deterrent secondary compounds may appear puzzling. However, there are myriads of organisms that consume fruit pulp but do not disperse seeds, such as microbes and fungi. The evolutionary triad between plants, their seed dispersers and fruit predators can explain the relative investment in nutrients and secondary compounds. Plants defend themselves against these unwanted fruit consumers with deterrent secondary compounds, some of which also affect the consumption rate of legitimate seed dispersers. Several studies (Cipollini and Levey 1997; Schaefer et al. 2003b; Cazetta et al. 2008) have found a negative relationship between the nutritional contents of fruits and their contents of secondary compounds, suggesting that plants employ alternative strategies to achieve seed dispersal. Nutrient-rich fruits are quickly consumed by seed dispersers, reducing the likelihood of predation by microbes and fungi. In contrast, less nutritious fruits are more strongly defended and can persist for months on plants, such as the guelder rose (Viburnum opulus).