Fine-scale spatiotemporal variation in seed-rodent interactions: A potential contribution to species coexistence

Seed predation and passage time through the digestive tract of captive golden snub-nosed monkeys (Rhinopithecus roxellana)

Annual variation in predation and dispersal of Arolla pine ( Pinus cembra L.) seeds by Eurasian red squirrels and other seed-eaters

Spatial scale affects seed predation and dispersal in contrasting anthropogenic landscapes

Examining spatio-temporal patterns of seed dispersal by a terrestrial non-obligate frugivore

Hepatica acutiloba and Trillium nivale are spring—flowering deciduous forest herbs whose seeds are dispersed by ants. We studied patterns of seed dispersal by ants and seed predation by rodents of these two herbs at three spatial scales: (1) among three woodlots that differed in density and size of Hepatica and/or Trillium populations, (2) between two sites within each woodlot located inside and outside a natural population, and (3) between replicate quadrats within each site. We estimated ant numbers and rodent presence using baits. In contrast to other studies done on other ant—dispersed species, seed predation by rodents was rare or nonexistent for both species even though rodents were present at all sites. Seed removal rates by ants were quite patchy at the scale of a few square metres within sites, but generally were slower where seed populations were dense and extensive. This indicates that ants become satiated during and immediately after seeds are released from parent plants growing in dense populations. Hence, seed dispersal is often ant—limited within well established populations of myrmecochores. Edaphic—topographic factors also play an important indirect role in seed dispersal through their effect on local ant numbers. The evolutionary role of seed predation on myrmecochory, and the demographic implications of density—dependent seed dispersal are discussed.

Seed predators and dispersers may drive the speed and structure of forest regeneration in natural ecosystems. Rodents and ants prey upon and disperse seeds, yet empirical studies on the magnitude of these effects are lacking. Here, we examined the role of ants and rodents on seed predation in 4 plant species in a successional gradient on a tropical rainforest island. We found that (1) seeds are mostly consumed rather than dispersed; (2) rates of seed predation vary by habitat, season, and species; (3) seed size, shape, and hardness do not affect the probability of being depredated. Rodents were responsible for 70% of seed predation and were negligible (0.14%) seed dispersers, whereas ants were responsible for only 2% of seed predation and for no dispersal. We detected seasonal and habitat effects on seed loss, with higher seed predation occurring during the wet season and in old-growth forests. In the absence of predators regulating seed-consumer populations, the densities of these resilient animals explode to the detriment of natural regeneration and may reduce diversity and carrying capacity for consumers and eventually lead to ecological meltdown.

This paper summarizes the ecological and evolutionary interactions for seed trees and Holarctic tree squirrels. The squirrel-seed interactions prior to dispersal and hoarding of seeds as well as those in which squirrels exert a significant positive effect on dispersal and establishment of seeds are reviewed. Across all Holarctic systems, three primary selective pressures that tree squirrels exert on tree seeds are recognized: two as seed predator and one as seed disperser. The close evolutionary relationship between several species of tree squirrels and tree species on which they feed, including the influence of tree squirrels on seed and tree characteristics and the effects of seeds on the demography, behaviour and social system of the squirrels are considered. It is suggested that in some systems tree squirrels might be considered keystone consumers as a result of their disproportionate influence on seed fates.

Secondary seed dispersal is an important plant-animal interaction, which is central to understanding plant population and community dynamics. Very little information is still available on the effects of dispersal on plant demography and, particularly, for ant-seed dispersal interactions. As many other interactions, seed dispersal by animals involves costs (seed predation) and benefits (seed dispersal), the balance of which determines the outcome of the interaction. Separate quantification of each of them is essential in order to understand the effects of this interaction. To address this issue, we have successfully separated and analyzed the costs and benefits of seed dispersal by seed-harvesting ants on the plant population dynamics of three shrub species with different traits. To that aim a stochastic, spatially-explicit individually-based simulation model has been implemented based on actual data sets. The results from our simulation model agree with theoretical models of plant response dependent on seed dispersal, for one plant species, and ant-mediated seed predation, for another one. In these cases, model predictions were close to the observed values at field. Nonetheless, these ecological processes did not affect in anyway a third species, for which the model predictions were far from the observed values. This indicates that the balance between costs and benefits associated to secondary seed dispersal is clearly related to specific traits. This study is one of the first works that analyze tradeoffs of secondary seed dispersal on plant population dynamics, by disentangling the effects of related costs and benefits. We suggest analyzing the effects of interactions on population dynamics as opposed to merely analyzing the partners and their interaction strength.

Seed dispersal and predation are key processes affecting the colonization and extinction of populations in fire‐prone environments. If these processes influence distribution and abundance, rare species may be expected to have less seed removal and/or greater seed predation than common congeners. I compared seed removal and predation under plants in two closely related pairs of fire‐sensitive common and rare Persoonia species with fleshy fruits in two replicate populations of each species. Seed removal by macropods was significantly greater in the two common species (>50% seeds/plant) than in their rare congeners (<25%). There was no overall effect of rarity on seed predation by rodents, but there were significantly more seeds of the rare Persoonia mollis subspecies maxima eaten than of the other three species. Plant size was the only attribute measured that was significantly correlated with seed removal ($$r=0.50$$ ). After including plant size as a covariate in the analysis, I still detected a significant effect of rarity on seed removal. High levels of seed removal were sustained in both small and large populations of the common Persoonia lanceolata, suggesting that population size may not be contributing to the differences between these common and rare species. The common‐rare difference in the seed removal of Persoonia species seems robust across several plant and population attributes.

Effects of mast seeding and insect infestation on predation and dispersal of Castanea mollissima nuts by rodents in the Qinling Mountains of China

Seed size may vary greatly among individuals within plant species. What effects the extremes of this variation have for seeds taken by small mammals are poorly understood. Not all seeds removed by small mammals are necessarily eaten. Small rodents are common seed predators, but they may disperse a significant proportion of seeds by scatter hoarding them via burial. Size‐dependent predation and dispersal of seeds has not been directly tested within a plant species for tropical rodents. This study tested whether or not large and small nuts of Astrocaryum mexicanum (Palmae) differed in their fates due to handling by the spiny pocket mouse Heteromys desmarestianus (Heteromyidae). Exclosures were used to give small rodents exclusive access to A. mexicanum nuts. H. desmarestianus preferentially consumed large over small A. mexicanum nuts, but cached (in burrows and by scatter hoarding) similar proportions of these nuts by size. Small nuts tended to be buried farther away from exclosures than large nuts. Although sample sizes of buried nuts were small, the rodents retrieved all buried large nuts, but 30% of the small nuts remained buried long enough to germinate. I also examined predispersal predation by insects and found that insects appear to have no size preference for A. mexicanum nuts, but insect predation appears to hinder nut development. Thus, nuts attacked by insects develop to be significantly smaller, with a low proportion of undamaged endosperm, than uninfested nuts. It is hypothesized that the preferential predation of large A. mexicanum nuts by H. desmarestianus is a response by these rodents to insect predation.

Black hornbills (Anthracoceros malayanus) appear to be the principal long-distance seed dispersers of Aglaia sp. (Meliaceae) at Pasoh Forest Reserve in Peninsular Malaysia. The squirrel Callosciurus prevostii removed some of the large seeds at least as far as adjacent crowns and sometimes dropped them after consuming only the orange, oily sarcotesta. It chased other squirrel species, which are probably seed predators, and hornbills out of the fruiting crown. Seeds on the ground beneath the parent crown were removed more rapidly than those farther away by rodent and (possibly) phasianid seed predators. Sitophilus sp. (Curculionidae) was also an Aglaia seed predator or parasite. Aglaia juveniles grew slowly under closed canopy, and small ones (<50 cm in height) had only 9.7 percent mortality per year during a 4-year period. Seedling survival was positively size dependent. For unknown reasons, small seedlings near the parent had a higher death rate than those at a greater distance; this was apparently a long-term pattern, because large seedlings and saplings did not occur within 10 and 35 m, respectively, of the parent tree's base. For this species an advantage of seed dispersal is avoidance of disproportionate seed and seedling mortality near the parent. Although Aglaia grows much faster in gaps than under closed canopy, it may require several episodes of growth in successive gaps before becoming reproductively mature. IN THEIR REVIEW OF SEED DISPERSAL, Howe and Smallwood (1982) remarked that little is known about its ecological and evolutionary advantages to the plant. Here we combine observations on seed dispersal and predation and juvenile mortality and spatial distribution to show how dispersal helps the tropical tree Aglaia sp. (Meliaceae) avoid seed and seedling mortality that is greater near the parent than farther away. Webb et al. (1967), Janzen (1970), and Connell (1971) suggested that such a mortality pattern, generated by seed predators, herbivores, or allelopathy, would promote the maintenance of high tree species richness in tropical forests. More recently, Connell (1978, 1979) has withdrawn his support for this hypothesis because field studies have shown that seed and seedling mortality is not invariably higher near conspecific adults. However, Clark and Clark's (1984) review of 24 data sets on mostly neotropical, woody plants showed that most evidence indicates either densityor distance-dependence in progeny mortality, as originally predicted by Janzen and Connell. Hubbell (1979, 1980) challenged the Janzen-Connell hypothesis on empirical and theoretical grounds, daiming the latter to demonstrate that spacing between conspecific adults could contribute little to the maintenance of high species richness. His theoretical analysis has been questioned by Becker et al. (1985), who consider the issue unresolved for nonequilibrium

Mediterranean type ecosystems are among the world's most fire-prone regions. Focusing on the Mediterranean basin, we review the literature and propose conceptual models to explain the direct and indirect effects of fire on plant-pollinator interactions, seed dispersers, and predators, as well as the temporal changes in these systems along post-fire succession and ecosystem recovery processes. Post-fire plant communities change in their composition, structure, floral resources, as well as seed and fruit resources. Fire directly affects communities of pollinators, seed dispersers, and seed predators mainly by mortality, and indirectly through changes in the quality and quantity of food and nesting resources. Pollinators, seed-dispersers, and seed predators depend on plant community composition and on the flower, seed, and fruit resources they produce. As a consequence, their community composition, structure, and function are expected to vary in response to post-fire temporal and spatial changes in plant com...

Seed dispersal is a key evolutionary process and a central theme in the population ecology of terrestrial plants. The primary producers of most land-based ecosystems are propagated by and maintained through various mechanisms of seed dispersal that involve both abiotic and biotic modes of transportation. By far the most common biotic seed transport mechanism is zoochory, whereby seeds, or fruits containing them, are dispersed through the activities of animals. Rodents are one group of mammals that commonly prey on seeds (granivores) and play a critical, often destructive, role in primary dispersal and the dynamics of plant communities. In North America, geomyid, heteromyid and some sciurid rodents have specialized cheek pouches for transporting seeds from plant source to larder, where they are often eliminated from the pool of plant propagules by consumption. These seed-laden rodents are commonly consumed by snakes as they forage, but unlike raptors, coyotes, bobcats, and other endothermic predators which eat rodents and are known or implicated to be secondary seed dispersers, the role of snakes in seed dispersal remains unexplored. Here, using museum-preserved specimens, we show that in nature three desert-dwelling rattlesnake species consumed heteromyids with seeds in their cheek pouches. By examining the entire gut we discovered, furthermore, that secondarily ingested seeds can germinate in rattlesnake colons. In terms of secondary dispersal, rattlesnakes are best described as diplochorous. Because seed rescue and secondary dispersal in snakes has yet to be investigated, and because numerous other snake species consume granivorous and frugivorous birds and mammals, our observations offer direction for further empirical studies of this unusual but potentially important channel for seed dispersal.

Shortly after our friend and colleague Gary R Bortolotti passed away in 2011, his widow Heather Trueman sent JLT ten photographs of parrots that Gary had taken in Brazil. In one of these images, we saw a flying chestnut-fronted macaw (Ara severus) carrying in its beak a defleshed fruit of the motacú palm (Attalea phalerata; upper-right arrow in Figure 1); upon enlarging this picture for publication in Frontiers, we noticed another macaw transporting a smaller-sized seed (lower-left arrow in Figure 1). Gary's photograph had captured what has been described as an unusual behavior: active seed dispersal by parrots. The unexpected nature of this observation was reinforced during discussions with colleagues who specialize in avian frugivory and seed dispersal. As they argued – and contrary to well-recognized avian seed dispersers such as frugivorous passerines, trogons, and toucans, which typically swallow whole fruits and disperse seeds after gut passage – parrots handle and destroy fruits in situ to eat the pulp or to gain access to the seeds. Although more than 400 known species of parrot inhabit the world's tropical ecosystems, only lesser vasa parrots (Coracopsis nigra; Böhning-Gaese et al. 1999) and plain parakeets (Brotogeris tirica; Sazima 2008) have previously been reported to regularly disperse seeds transported in their bills. This has led to the general assumption that parrots are seed predators and thus do not participate in seed-dispersal mutualisms (Fleming and Kress 2013). Chestnut-fronted macaws (Ara severus) transporting a defleshed motacú palm fruit (Attalea phalerata; upper-right arrow) and an unidentified seed (lower-left arrow). Photo taken on 17 Oct 2009 (Rio Cristalino, Brazil). Because only two parrot species were known to routinely carry seeds in flight, this behavior is considered to be unusual. However, these two species are among the more ancestral (Coracopsis) and more modern (Brotogeris) species within the phylogenetic tree of the Psittacidae family of parrots (Wright et al. 2008), suggesting that this behavior could be well-conserved through the evolution and diversification of this large lineage of birds, but nonetheless overlooked. Parrots often forage in the canopy of tropical forests, and their foraging behaviors are difficult to study due to remote locations and logistical constraints. Thus, the likelihood of observing a parrot in flight carrying a fruit or seed in its bill may be low, and such behaviors may go largely unreported. A new photograph (Figure 2) taken by JLT, this time of a large flock of red-fronted macaws (Ara rubrogenys) in Bolivia, led us to reconsider this second hypothesis. In this case, the transport of an ear of corn (Zea mays) by a macaw went unseen until the photograph was examined more closely. We then decided to reassess the foraging behavior of parrots, searching for indications of other dispersal events. Red-fronted macaw (Ara rubrogenys) transporting an ear of corn (Zea mays). Photo taken on 27 Aug 2011 (Los Negros, Bolivia). To that end, we joined a group of parrot biologists and ecologists studying foraging behavior who, since 2012, have recorded hundreds of observations of parrots dispersing fruits or seeds using their bills or, less often, their feet (WebFigure 1). Although preliminary, our data suggest that seed dispersal by parrots is not unusual. Observations came from 28 parrot species belonging to 16 genera, ranging in body size from the smallest parakeets to the largest macaws, and involved the dispersal of fruits and seeds from 94 species of trees (including palms) and shrubs. Instances were recorded in seven countries (Argentina, Bolivia, Brazil, Chile, Ecuador, Peru, and Spain), comprising mostly neotropical parrots but also an African and an Asian species from introduced populations of parrots in Spain. They covered a wide variety of ecosystems – from the sea-level Argentinean Pampas to high-altitude Andean forests, from continents to islands, from the wettest Amazonian savannas to the driest Caatinga forests, and from pristine to urban habitats. Regarding functional interactions, parrots –regardless of their origin – dispersed both native and non-native (including cultivated) plants. We measured the distances that fruits or seeds were carried by parrots, with the aid of laser rangefinders, in 686 dispersal events. Unsurprisingly, given the long-distance flying abilities of most parrot species, the distances spanned a wide range (maximum = 1200 m, median = 27 m, mean = 44 m; WebFigure 2). This indicates that parrots may serve as efficient long-distance seed dispersers. Moreover, we observed several incidents where transported fruits or seeds were accidentally dropped in flight or when the parrot perched during eating. Importantly, we often found uneaten, ripened seeds and seedlings growing under tree perches used by parrots, far from the nearest plant that could have provided those seeds. All of these observations point to parrots as genuine, but thus far overlooked, seed dispersers. This short story illustrates how serendipitous photographic evidence can lead scientists to question what has been considered unusual or difficult-to-observe behaviors, and highlights how much we have yet to learn about the natural history of most organisms. Given that parrots are large, colorful, and loud birds that have attracted the attention and company of humans for centuries (Tella and Hiraldo 2014), how many small yet important life-history details are we missing about numerous other, perhaps less charismatic, species? The net effect of parrots on the population dynamics of their food plants relies on the negative impact of seed predation versus the benefits for the genetic structure of tropical forests derived from long-distance seed dispersal. This contribution of parrots as antagonists and mutualists with respect to their diverse food plants warrants further research. The fact that one-third of parrot species in the world are threatened with extinction should urge the assessment of their ecological roles and the ecosystem-wide consequences of parrot population declines. Parrots may play a key role in the functioning and maintenance of biodiversity not only in tropical ecosystems but also in regions where parrots have been introduced. Gary's photograph presented us with an enlightening moment in our own research, and we hope that the preliminary data discussed here will encourage other researchers to more thoroughly explore the role of parrots in providing a key ecosystem service as seed dispersers. Gary R Bortolotti inspired us to explore this parrot behavior as well as many other aspects of avian behavior and ecology. Preliminary results on parrot seed dispersal were obtained through projects funded by Fundación Biodiversidad, Fundación Repsol, World Parrot Trust, and a Severo Ochoa award (to FH), and discussed within the ParrotNet COST Action group. Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.