Beyond Predators: Carnivores as Secondary Dispersers of Mycorrhizal Fungi.

The effectiveness of a seed disperser depends on the quantity and quality of dispersal. The quality of dispersal depends in large part on factors that affect the post-dispersal fate of seeds, and yet this aspect of dispersal quality is rarely assessed. In the particular case of seed dispersal through endozoochory, the defecation pattern produced has the potential of affecting the fate of dispersed seeds and consequently, dispersal quality and effectiveness. In this study, I assessed the effects of dung presence and dung/seed densities on seed predation by rodents and secondary dispersal by dung beetles. In particular, I compared seed fates in clumped defecation patterns, as those produced by howler monkeys, with seed fates in scattered defecation patterns, as those produced by other frugivores. I also determined the prevalence of red howler monkeys (Alouatta seniculus) as seed dispersers at the plant community level in Central Amazonia by determining the number of species they dispersed in a 25-month period. I found that dung presence and amount affected rodent and dung beetle behavior. Seed predation rates were higher when dung was present, and when it was in higher densities. The same number of seeds was buried by dung beetles, in clumped versus scattered defecation patterns, but more seeds were buried when they were inside large dung-piles versus small piles. Seed density had no effect on rodent or dung beetle behavior. Results indicate that caution should be taken when categorizing an animal as a high or low quality seed disperser before carefully examining the factors that affect the fate of dispersed seeds. Red howler monkeys dispersed the seeds of 137 species during the study period, which is the highest yet reported number for an Alouatta species, and should thus be considered highly prevalent seed dispersers at the plant community level in Central Amazonian terra firme rain forests.

Disperser effectiveness is the contribution that a disperser makes to the future reproduction of a plant (Schupp 1993), and it has two components: quality and quantity of dispersal. Quantity of dispersal is a function of the number of visits that a disperser makes to a fruiting plant and the number of seeds that are dispersed during each visit. Quality of dispersal is a function of the treatment that a seed receives from its disperser and the site that the seed is finally deposited in. The quality of seed dispersal of the mistletoe Phragmanthera dschallensis (Engl.) M.G. Gilbert (Loranthaceae) by frugivorous birds was examined in this study.

Examining dispersal is critical for understanding the diversity of Andean-centered plant lineages, like Burmeistera (Campanulaceae). One-third of its species present an unusual inflated berry. Unlike the bright colors of non-inflated fruits in the genus, these fruits are typically dull-green; however, the fact that the seeds are loosely held in the placenta and easily removed when touched seems to suggest adaptation to animal dispersal. We studied two inflated-baccate species, Burmeistera glabrata and B. borjensis, with the aim of testing the non-exclusive hypotheses that their seeds are dispersed by (1) small mammals, (2) slugs, or (3) adult flies that develop inside the fruits. In two sites in the Ecuadorian Andes, we performed observations at dusk and dawn to examine the fate of fruits and seeds; recording fruit fall, formation of holes in the fruits, and seed loss from the placenta. We documented fruit visitors with cameras, and surveyed unopened fruits for the presence of insect larvae and seed condition. Finally, we performed an experiment to examine the effect of holes and rain in germination, in order to evaluate if holes are required for seeds to leave the fruits and subsequently germinate. For both species, most fruits fell and decomposed beneath the mother plant. However, we found limited support for small mammal dispersal; videos and observations revealed that mice and squirrels are potential, but rare, seed dispersers. We found no evidence for slug or fly dispersal; fly larvae were common inside fruits, but acted exclusively as seed predators. Crickets often chewed holes in fruits on plants and on the ground. Holes did not have an effect on germination, which was induced only by rain. Hence, the majority of seeds end up under the mother plant, with rare but potentially important events of primary or secondary dispersal by small mammals. The combination of limited dispersal due to gravity and rare events of mammal dispersal may have played a critical role in the rapid diversification of Burmeistera.

In tropical forests, forest fragmentation that alters species interactions between plants and animals, especially mutualisms, will affect the regeneration of trees. Fragmentation reduced Duckeodendron cestroides seed dispersal quantity and quality. The percent and distance of dispersed seeds were twice as great in continuous forest (31%, 4.9 m) as in fragments (15%, 2.5 m). Differences were even more exaggerated for each tree's furthest dispersed seeds. Distributions of dispersed seeds across distance showed more seeds at all distances in continuous forest than in fragments. Dispersal differences were strongest in years when fruit production was high and resulted in a greater number of first-year seedlings at distances far from the parent tree in continuous forests. Fruit production and post-dispersal seed fate of Duckeodendron were also different between fragments and continuous forest. Fruit production, measured by fruit fall, was reduced in fragments, more dramatically in years when fruit production was high. In continuous forest, seeds protected from mammal seed predators or secondary dispersers had high rates of seedling establishment (55%), but the majority of unprotected seeds were rapidly removed (77%). Seed predation was 17 times greater in continuous forest (53%) than in fragments (3%). More seeds in fragments had delayed germination than in continuous forest, resulting in seedlings half as tall as their continuous forest counterparts. Despite these differences in the processes leading up to seedling establishment, there was no difference between the percent of seedlings that established in fragments or continuous forest. Although fragmentation had dramatic effects on D. cestroides, responses of species interactions to fragmentation can vary. Although the number, percentage, distance, and distributions of dispersed seeds were reduced in fragments for the large-seeded Duckeodendron, they were not for the small-seeded Bocageopsis multiflora. Seed dispersal of large-seeded species may be more susceptible to fragmentation than small-seeded species because large-seeded species rely on fewer, extinction prone dispersers. Three lines of evidence from other tropical fragmentation research support this hypothesis. A rapid survey failed to detect differences in fruit production between fragments and continuous forest, probably because small sample sizes and high intraspecific variability caused a Type II error.

Omnivorous waterbirds play an important role in aquatic ecosystems as dispersal vectors via direct ingestion, transportation, and egestion of plant and invertebrate propagules (i.e. endozoochory). Predatory birds also have the potential to disperse plants and invertebrates that were first carried internally or externally by their prey animals. However, the potential contribution of predatory waterbird species to propagule dispersal in aquatic ecosystems remains understudied. We chose the grey heron Ardea cinerea (Ardeidae) to study the potential of predatory waterbirds to disperse propagules within and among aquatic ecosystems. We hypothesised that: (1) herons disperse a wide variety of plant and invertebrate propagules, from different habitats, with different morphologies (i.e. dispersal syndromes), and including both native and alien species; (2) propagules are ingested with prey species that are primary dispersal vectors (i.e., herons are secondary dispersers); (3) heron pellets show a similar abundance and richness of propagules across their widespread range. We collected 73 regurgitated heron pellets containing undigestible remains from 12 locations across the U.K. and The Netherlands, and examined the taxonomic diversity of plant seeds, invertebrates and prey remains. Pellets were dominated by mammal hairs (99% by volume), and bones confirmed the ingestion of small mammals (prevalence of 38%, e.g. water voles Arvicola amphibius), fish (14%), and birds or amphibians (6%). A total of 266 intact plant seeds were recovered from 71% of the pellets, representing 50 taxa from 17 plant families, including the alien Cotula coronopifolia. The cumulative number of plant species dispersed was lower at higher latitudes. Eight plant species recorded had not previously been recorded as dispersed via waterbirds, and only three species have an endozoochorous dispersal syndrome. Plant taxa were dominated by Caryophyllaceae, Cyperaceae, Juncaceae, and Poaceae, with 24 species from the littoral zone (Ellenberg moisture values of 7–12) and 21 terrestrial species (Ellenberg moisture values of 4–6). Intact invertebrate propagules were found in 30% of the pellets, dominated by Cladocera (Daphniidae) and Bryozoa (including the alien Plumatella casmiana). Our results demonstrate that grey herons disperse plant seeds and aquatic invertebrates widely in north‐western Europe. Herons regurgitate pellets that contain plant and invertebrate propagules from both aquatic or terrestrial habitats, for which secondary dispersal via ingestion along with prey is the likely underlying mechanism (i.e. propagules either attached to or in the digestive systems of the various prey). Our findings showcase the potential of predatory waterbirds as vectors of plants and invertebrates, and how they may facilitate connectivity between freshwater and terrestrial habitats.

The journey of wind‐dispersed seeds does not necessarily end when they land. Secondary dispersal and/or predation can positively or negatively affect the spread of invasive plants. Here we studied post‐dispersal seed removal of nodding and plumeless thistle (Carduus nutans and C. acanthoides) in part of their invaded range in Pennsylvania, USA. The relative impact of small mammals and insects was determined using exclusion treatments in the field. In cages that allowed insect access, 88 % of the seeds were removed after 1 day, and 99.9 % were removed after the 6‐day trial. When insects were excluded, the removal rate was significantly lower (18 % after 1 day, 40 % after 6 days). The seed removal rates provide an upper limit to the seed predation rate, with the understanding that it is also possible for seed removal to be an important secondary dispersal mechanism. We discuss a combined empirical‐theoretical approach to evaluate the impact of these alternative seed fates on the spread and management of these thistles.

Based on geographical and home range sizes, physiology, and gape limitation, a positive relationship between predator size and diet breadth is expected. Alternatively, larger predators might avoid smaller prey; in this case no relationship would be found. Here, I used a large data set on the diets of marine predators to describe and identify mechanisms responsible for the relationships among predator body size, diet breadth, and the mean, minimum, maximum, and variance of prey size. I found no relationship between predator size and diet breadth. Mean, minimum, maximum, and variance of prey size were all positively associated with predator size. I found that larger predators increase their minimum and maximum prey size with similar slopes, which explains the lack of relationship between predator size and diet breadth. The results support predictions of the hypothesis that optimal foraging is the main factor constraining the shape of the relationships among predator size, prey size, and diet breadth. Future research should focus on examining the relationship between body size and the breadth of different niche axis across different groups of organisms to assess whether a positive relationship between body size and niche breadth is a general rule in macroecology.

The effectiveness of a seed disperser is dependent on the impact it has on plant fitness. For fruiting species, plant fitness is dependent on the behaviour of its mutualists in (a) reducing seed mortality and (b) increasing the likelihood of future reproduction. The main aim of this thesis was to assess how intergroup variability in the feeding and movement behaviour of a highly social frugivore, influences seed dispersal effectiveness (SDE) and plant fitness. I achieved this by deconstructing the different components of seed dispersal, the quality of dispersal and the quantity of dispersal and investigated how the behaviour of samango monkeys influenced each component. Germination experiments demonstrated that although removal of germination inhibiting fruit pulp through seed-spitting increased germination potential compared to the mechanical and scarification of seeds via seed-swallowing, plants may trade quality for quantity, as the SDE of samango monkeys was greater for swallowed seeds. Time budget analysis showed that intergroup variability in feeding behaviour led to differences in the quantity of seeds dispersed by each group Movement behaviour analysis showed that differences in habitat quality influenced the quality of dispersal. Gut passage time analysis provided a reliable estimate of a gut passage time window between 16.63 – 25.12 hrs. The findings of this study highlight intergroup variability in SDE of neighbouring groups of social foraging frugivores, which possibly arose through ecological constraints associated with group size (Janson & van Schaik 1988; Chapman & Chapman 2000b). Intergroup variability in SDE could have important consequences on the maintenance of forest systems and the recruitment in, and colonization of, secondary forest or open habitats. Variation in SDE within animal populations can have important implications for spatial demographics in plant communities, and this thesis highlights the importance of including intergroup variability seed dispersal models.

The diets of predators and their selection of prey often shape prey community dynamics. Understanding how different predators select their prey could enable ecologists to predict their impact on specific prey populations. Here, we investigate the diets of the feral cat (Felis catus), red fox (Vulpes vulpes), and dingo (Canis dingo) in the Simpson Desert of central Australia, over a 1-year period between 2011 and 2012, and compare the selectivity of these predators for small mammalian prey. We found that cats showed the greatest consumption of small mammals, whereas dingoes consumed larger prey, thus indicating preferences for different prey sizes. High occurrence of small mammals in the diets of all predators probably reflected high abundances of small mammals in the environment; rodents declined after an irruption, but were still abundant at the time of sampling. The cat exercised greatest selectivity for small mammal species, whereas the dingo did not positively select for any species. Positive selection by predators for the long-haired rat (Rattus villosissimus) and negative selection for the spinifex hopping-mouse (Notomys alexis) may reflect inefficient and well-developed escape strategies by these 2 prey species, respectively. High selectivity by the cat for Forrest's mouse (Leggadina forresti) suggests that conservation of this rare rodent may depend on effective cat management.

The dependence of mistletoes on few dispersers and the directed dispersal they provide is well known, yet no recent work has quantified either the effectiveness of these ‘legitimate’ dispersers, or the extent of redundancy among them. Here, I use the seed dispersal effectiveness (SDE) framework to analyze how birds (Mionectes striaticollis and Zimmerius bolivianus) contribute to mistletoe (Struthanthus acuminatus and Phthirusa retroflexa) infection in traditional mixed plantations within a humid montane forest in Bolivia. I calculated SDE for each bird–mistletoe pair and for the disperser assemblage, by estimating both the quantity and the quality of dispersal. The quantity of dispersal was measured as: (1) disperser abundance; (2) frequency of visits; and (3) number of seeds dispersed per visit, and the quality of dispersal was measured as: (1) germination percentage and speed of germination of seeds regurgitated by birds; and (2) the concordance of deposited seeds and seedling distribution patterns with adult mistletoe distribution at three scales (habitat, host, and microhabitat). Dispersers were not redundant: the more generalist species M. striaticollis dispersed more seeds, but provided lower quality seed dispersal, whereas the mistletoe specialist Z. bolivianus provided low‐quantity and high‐quality seed dispersal. Whereas S. acuminatus benefited more from the SDE of Z. bolivianus, P. retroflexa benefited from the complementary seed dispersal provided by both birds. These results demonstrate how sympatric mistletoes that share the same disperser assemblage may develop different relationships with specific vectors, and describe how the services provided by two different dispersers (one that provides high‐quality and one that provides high‐quantity dispersal) interact to shape spatial patterns of plants.

Vulnerability of small and medium-sized prey mammals in relation to their habitat preferences, age classes and locomotion types in the temperate Monte Desert, Argentina

Seed dispersal allows plants to colonize new sites and contributes to gene flow among populations. Despite its fundamental importance to ecological and evolutionary processes, our understanding of seed dispersal is limited due to the difficulty of directly observing dispersal events. This is particularly true for the majority of plant species that are considered to have gravity as their primary dispersal mechanism. The potential for long-distance movement of gravity-dispersed seeds by secondary dispersal vectors is rarely evaluated. We employ whole-genome assays of maternally inherited cpDNA in Plagiobothrys nothofulvus to resolve patterns of genetic variation due to effective (realized) seed dispersal within a 16 hectare prairie that is characterized by a mosaic of habitat types. We evaluate the effects of microgeographic landscape features extracted from micro-UAV aerial surveys on patterns of seed dispersal using landscape genetics methods. We found evidence of high resistance to seed-mediated gene flow (effective dispersal) within patches of Plagiobothrys nothofulvus, and strong genetic structure over distances of less than 20 m. Geographic distance was a poor predictor of dispersal distance, while landscape features had stronger influences on patterns of dispersal (distance and direction of seed movement). Patterns of dispersal were best predicted by the combined distribution of flower patches, habitat type, and the network of vole runways, with the latter explaining the largest proportion of variation in the model. Our results suggest that primary dispersal occurs mostly within microhabitats and infrequent secondary dispersal may occur over longer distances due to the activity of small mammals and other vertebrates.

Members of the orderCarnivoraare a unique and important seed disperser who consume and deposit undamaged seeds while providing regular long‐distance seed dispersal opportunities. Some members ofCarnivora, such as coyotes (Canis latrans), are undergoing range expansions which may help the plant species they consume colonize new locations or replace dispersal services provided by recently extirpated species. In this study, we evaluated aspects of the seed dispersal effectiveness of coyotes and gut passage time to determine the potential dispersal distances for three commonly consumed and commonly occurring plant species (Amelanchier alnifolia, Celtis ehrenbergiana, andJuniperus osteosperma). We also investigated the potential effects of secondary dispersal of seeds away from scats by comparing seedling emergence from whole scats to those where seeds were first removed from scats. We found that seeds generally took between 4 and 24 h to pass through the digestive tract of coyotes, which could result in regular seed dispersal up to 7 km. Gut passage through coyotes had no effect on seed viability or emergence for any of the three plant species, including that gut passage forA. alnifoliaandJ. osteospermadoes not replace cold stratification for breaking physiological dormancy. By simulating secondary dispersal, we found that 22% (±8.2%) moreC. ehrenbergianaseedlings emerged when seeds were removed from scats and those seedlings emerged 7 d earlier (±5 d) compared to seeds that remained in the coyote scat. Coyotes are effective seed dispersers, with the potential for regular long‐distance dispersal services and for providing opportunities for secondary seed dispersal, which could aid in climate migration or serve to replace extirpated dispersal mutualists.

Context Many mycorrhizal fungi are vital to nutrient acquisition in plant communities, and some taxa are reliant on animal-mediated dispersal. The majority of animals that disperse spores are relatively small and have short-distance movement patterns, but carnivores – and especially apex predators – eat many of these small mycophagists and then move greater distances. No studies to date have assessed the ecosystem services carnivores provide through long-distance spore dispersal. Aims In this study, we aimed to investigate whether Australia’s free-ranging dogs (Canis familiaris), including dingoes, act as long-distance spore dispersers by predating smaller mycophagous animals and then secondarily dispersing the fungi consumed by these prey species. Methods To answer this question, we collected dingo scats along 40 km of transects in eastern Australia and analysed the scats to determine the presence of fungal spores and prey animals. Using telemetry and passage rate data, we then developed a movement model to predict the spore dispersal potential of dingoes. Key results We found 16 species of mammalian prey to be eaten by dingoes, and those dingo scats contained spores of 14 genera of mycorrhizal fungi. These fungi were more likely to appear in the scats of dingoes if primary mycophagist prey mammals had been consumed. Our model predicted dingo median spore dispersal distance to be 2050 m and maximum dispersal potential to be 10 700 m. Conclusions Our study indicates that dingoes are providing a previously overlooked ecosystem service through the long-distance dispersal of mycorrhizal fungi. Many of the fungi found in this study form hypogeous (underground) fruiting bodies that are unable to independently spread spores via wind. Because dingoes move over larger areas than their prey, they are especially important to these ecosystem functions. Implications Our novel approach to studying an overlooked aspect of predator ecology is applicable in most terrestrial ecosystems. Similar modelling approaches could also be employed to understand the dispersal potential of both primary and secondary spore dispersers globally. Because this study highlights an unrecognised ecosystem service provided by dingoes, we hope that it will stimulate research to develop a more comprehensive understanding of other apex predators’ ecosystem functions.

Small mammals as a bioindicator of mercury in a biodiversity hotspot – The Hengduan Mountains, China