Endozoochorous seed dispersal by sympatric mustelids, Martes melampus and Mustela itatsi, in western Tokyo, central Japan

We investigated seed dispersal by two sympatric mustelid species, the Japanese marten (Martes melampus) and Japanese weasel (Mustela itatsi), along an intercity forest path in western Tokyo, central Japan, from Jul 2007 to Jul 2008. We aimed to investigate the effect of food/habitat preference of these mustelids (martens are semi-arboreal frugivores while weasels are terrestrial carnivores) on their seed dispersal characteristics, which determine their efficacy as seed dispersers. In total, we analyzed 478 fecal samples collected from the two mustelids (N_marten = 381, N_weasel = 97). The proportions of feces containing seeds for martens and weasels were 81.4% and 55.7%, respectively. The number of plant species whose seeds were found within the feces were 28 and 17, respectively. Almost all seeds within feces of both mustelids were intact. The number of plant species whose seeds were found within a single fecal sample ranged from one to four, but no significant difference was detected between the two mustelids. However, marten feces contained a significantly greater number of seeds of most plant species as well as total number of seeds than did weasel feces. The numbers of plant species and seeds represented in marten feces varied seasonally, but those represented in weasel feces did not. Our findings suggest the possibility that both mustelids act in some ways as seed dispersers, although martens seem to disperse a greater diversity and total amount of seeds.     

Seed Dispersal by Monkeys and the Fate of Dispersed Seeds in a Peruvian Rain Forest1

Primary seed dispersal by two species of monkeys and the effects of rodents and dung beetles on the fate of dispersed seeds are described for a rain forest in southeastern Perú. During the six-month study period (June–November 1992) spider monkeys (Ateles paniscus) dispersed the seeds of 71 plant species, whereas howler monkeys (Alouatta seniculus) dispersed seeds of 14 species. Spider and howler monkeys also differed greatly in their ranging behavior and defecation patterns, and as a consequence, produced different seed rain patterns. Monkey defecations were visited by 27 species of dung beetles (Scarabaeidae). Dung beetles buried 41 percent of the seeds in the dung, but the number of seeds buried varied greatly, according to seed size. Removal rates of unburied seeds by rodents varied between 63–97 percent after 30 d for 8 plant species. The presence of fecal material increased the percentage of seeds removed by seed predators, but this effect became insignificant with time. Although seed predators found some seeds buried in dung balls (mimicking burial by dung beetles), depth of burial significantly affected the fate of these seeds. Less than 35 percent of Brosimum lactescens seeds buried inside dung balls at a depth of 1 cm remained undiscovered by rodents, whereas at least 75 percent of the seeds escaped rodent detection at a depth of 3 cm and 96 percent escaped at 5 cm. Both dung beetles and rodents greatly affected the fate of seeds dispersed by monkeys. It is thus important to consider postdispersal factors affecting the fate of seeds when assessing the effectiveness of frugivores as seed dispersers.     

Persistence of the effect of frugivore identity on post‐dispersal seed fate: consequences for the assessment of functional redundancy

Large frugivores play an important role as seed dispersers and their extinction may affect plant regeneration. The consequences of such extinctions depend on the likelihood of other species being functionally redundant and on how post‐dispersal events are affected. We assess the functional redundancy of two seed dispersers of the Atlantic Forest, the muriqui (Brachyteles arachnoides) and the tapir (Tapirus terrestris) through the comparison of their seed dispersal quality, taking into account post‐dispersal events. We compare tapirs and muriquis for: (1) the dung beetle community associated with their feces; (2) the seed burial probability and burial depth by dung beetles; and (3) the seed mortality due to predators or other causes according to burial depth. We determine how seed burial affects seed dispersal effectiveness (SDE) and compare the dispersal quality of four plant species dispersed by these frugivores. Muriqui feces attract 16‐fold more dung beetles per gram of fecal matter and seeds experience 10.5‐fold more burial than seeds in tapir feces. In both feces types, seed mortality due to predation decreases with burial depth but seed mortality due to other causes increases. Total seed mortality differ within plant species according to the primary disperser. Therefore, the effect of seed burial on SDE varies according to the plant species, burial depth, and primary disperser. As tapirs and muriquis differently affect the seed fate, they are not functionally redundant. Since the effect of the primary disperser persists into the post‐dispersal events, we should consider the cascading effects of these processes when assessing functional redundancy.     

The role of avian ‘seed predators’ as seed dispersers

Seed dispersal is a central process in plant ecology with consequences for species composition and habitat structure. Some bird species are known to disperse the seeds they ingest, whereas others, termed ‘seed predators’, digest them and apparently play no part in dispersal, but it is not clear if these are discrete strategies or simply the ends of a continuum. We assessed dispersal effectiveness by combining analysis of faecal samples and bird density. The droppings of seed dispersers contained more entire seeds than those of typical seed predators, but over a quarter of the droppings of seed predators contained whole seeds. This effect was further magnified when bird density was taken into account, and was driven largely by one frequent interaction: the Chaffinch Fringilla coelebs, a typical seed predator and the most abundant bird species in the area and dispersed seeds of Leycesteria formosa, a non‐native plant with berry‐like fruits. These results suggest the existence of a continuum between seed predators and seed dispersers.     

Response of ants to human‐altered habitats with reference to seed dispersal of the myrmecochore Corydalis giraldii Fedde (Papaveraceae)

Anthropogenic habitat disturbance has potential consequences for ant communities. However, there is limited information on the effects of ant responses on associated ecological processes such as seed dispersal. We investigated the effect of disturbance on the abundance, richness, and composition of ant communities and the resulting seed‐dispersal services for a herbaceous myrmecochore, Corydalis giraldii (Papaveraceae), in an undisturbed habitat (forest understory), moderately disturbed habitat (abandoned arable field), and highly disturbed habitat (road verge) on Qinling Mountains, China. In total, we recorded 13 ant species, and five out of these were observed to transport seeds. The community composition of dispersers was significantly different amongst habitats. The richness of the dispersers did not differ among the habitats, but their total abundance varied significantly across habitats and was 21% lower in the road verge than in the abandoned arable fields. The major seed‐dispersing ant species in both the forest understory and the abandoned arable field were large‐bodied (Myrmica sp. and Formica fusca, respectively), whereas the major seed‐dispersing ants found in the road verge were the small‐bodied Lasius alienus. This difference resulted in lower seed removal rates and dispersal distances in the road verge than in the other two habitats. The different dispersal patterns were attributed primarily to differences in dispersing ant abundance and identity, most likely in response to habitats with different degree of anthropogenic disturbance. The possible influence of disturbance on the ecological specialization of ant‐seed dispersal interaction is also discussed.     

Unexpected relationships and valuable mistakes: non‐myrmecochorous Prosopis dispersed by messy leafcutting ants in harvesting their seeds

Abstract Ants generally disperse seeds while feeding on fruits or structures attached to the seed. Seed dispersal as a by‐product of seed predation (dyszoochory) was recognized in specialized harvester ants, but not in ants predating seeds opportunistically. Leafcutting ants are the main herbivores in much of the Neotropics, and they have been reported to remove fruits and seeds, but their role as seed predators and dispersers has not been acknowledged. Prosopis flexuosa D.C. (Fabaceae, Mimosoideae) is the most abundant tree species in the central Monte Desert, Argentina, and it is likely to depend on secondary animal dispersal. Mammalian frugivores are usually considered its main dispersers, but the opportunity for dispersal may be small since the removal of fruits and seeds by seed predators is very intense. The objective of this study was to identify which ant species interact with P. flexuosa fruits and to evaluate their relative importance as seed predators and dispersers. In a field experiment, whole and segmented pods were offered and several ant species exploiting the fruits were identified. Additionally, all pod segments remaining around nests of the three ant species able to remove them (the leafcutters Acromyrmex lobicornis Emery and Acromyrmex striatus Roger, and Pheidole bergi Mayr) were examined during and after the P. flexuosa primary dispersal season. Up to 753 pod segments and 90 sound seeds were found accumulated in a circle of 1 m radius over nests of A. lobicornis, and even more in an examined trail. Acromyrmex striatus left a smaller proportion of sound seeds and P. bergi left a smaller number of pod segments. All tendencies were similar during shorter known periods of accumulation. Leafcutting ants are acting as important seed predators, and ‘by mistake’ may be dispersing a key non‐myrmecochorous tree. This is an unexplored path in the seed dispersal cycle of P. flexuosa that challenges the tendency to predict interactions based on classifications made with other goals.     

Geographic variation in walnut seed size correlates with hoarding behaviour of two rodent species

Seeds of the Japanese walnut, Juglans ailanthifolia, are usually scatter-hoarded by two rodent species, the Japanese squirrel Sciurus lis and the field mouse Apodemus speciosus, but only by the latter in several areas where S. lis is absent. We examined seed-size-mediated interactions of these three species across a wide geographic range. Field tracking of walnuts with miniature radio-transmitters revealed that squirrels hoarded larger seeds more frequently and at greater distances than smaller seeds. In contrast, mice hoarded smaller seeds more frequently and transported them farther than larger seeds. These seed dispersers could affect the evolution of seed size because seeds hoarded at sites farther from source trees are known to survive better until germination and as seedlings. We expect that larger seeds may be advantageous in regeneration if the main seed dispersers are squirrels, whereas smaller seeds may be advantageous if mice are the dominant dispersers. These predictions were supported by the fact that seed size was smaller on islands inhabited only by mice and at the edge of the squirrel distribution, compared to areas where mice and squirrels are both common.     

The Role of Arboreal Seed Dispersal Groups on the Seed Rain of a Lowland Tropical Forest1

Most tropical plants produce fleshy fruits that are dispersed primarily by vertebrate frugivores. Behavioral disparities among vertebrate seed dispersers could influence patterns of seed distribution and thus forest structure. This study investigated the relative importance of arboreal seed dispersers and seed predators on the initial stage of forest organization–seed deposition. We asked the following questions: (1) To what degree do arboreal seed dispersers influence the species richness and abundance of the seed rain? and (2) Based on the plant species and strata of the forest for which they provide dispersal services, do arboreal seed dispersers represent similar or distinct functional groups? To answer these questions, seed rain was sampled for 12 months in the Dja Reserve, Cameroon. Seed traps representing five percent of the crown area were erected below the canopies of 90 trees belonging to nine focal tree species: 3 dispersed by monkeys, 3 dispersed by large frugivorous birds, and 3 wind‐dispersed species. Seeds disseminated by arboreal seed dispersers accounted for ca 12 percent of the seeds and 68 percent of the seed species identified in seed traps. Monkeys dispersed more than twice the number of seed species than large frugivorous birds, but birds dispersed more individual seeds. We identified two distinct functional dispersal groups, one composed of large frugivorous birds and one composed of monkeys, drop dispersers, and seed predators. These groups dispersed plants found in different canopy strata and exhibited low overlap in the seed species they disseminated. We conclude it is unlikely that seed dispersal services provided by monkeys could be compensated for by frugivorous birds in the event of their extirpation from Afrotropical forests.     

Seed dispersal by ungulates in the point calimere wildlife sanctuary: A scientific and perspective analysis

Exotic woody weed plants are a very serious threat to seed dispersed by ungulate in the tropical forest of Asia. The ungulates in Point Calimere Wildlife Sanctuary (PCWS) are a significant role in native indigenous seed dispersal. The exotic woody weed tree Prosopis juliflora prevalence distributed in the PCWS and they might potentially alter the native medicinal plant species. In the present investigation, we have assessed the seed dispersal by ungulates in PCWS from January to March 2017. Four different ungulate species were selected to understand their seed dispersal rate of different plant species in selected sanctuary. This investigation was planned to confirm the seed dispersal by ungulates of blackbuck, spotted deer, wild boar and feral horse. Among the four different ungulates tested, the maximum numbers of pellets collected from blackbuck and no seed found in their pellets. The low quantities of pellets were collected from wild boar and this study has recorded medium-sized ungulates which dispersed variety of plant. However, the dispersal of the seed of medicinal plants were not considerably high and relatively moderate percentage of seeds dispersal occurred in medium-sized ungulates like wild boar and spotted deer. P. juliflora had 100% seed germination rate were observed from the faecal samples of wild boar and feral horse. The control seed achieved maximum seedling rate than the ungulates seeds.     

Non-native mammals are weak candidates to substitute ecological function of native avian seed dispersers in an island ecosystem

Although prominent examples exist of non-native species causing substantial ecological harm, many have neutral or positive effects, including filling surrogate roles once performed by extinct native organisms. We tested the ecological roles of two non-native mammals as seed dispersers or seed predators in Guåhan, which, due to invasive brown tree snakes (Boiga irregularis), is devoid of native seed dispersers–birds and bats. We conducted feeding trials with captive rats (Rattus spp.), which are present but uncommon due to predation by snakes, and pigs (Sus scrofa), which are abundant. We examined if and how they interacted with common forest fruits. We then compared how any gut-passed or animal-handled seeds germinated compared to seeds left in whole fruit or depulped seeds. Rats and pigs interacted with most of the fruits and seeds (>80%) that they were fed. Of those, most seeds were destroyed—78% for rats and 90% for pigs, across both native and non-native plant species. Compared to seeds germinating within whole fruits, rats improved germination of the seeds that they handled without ingesting, while pigs diminished the germination of seeds that they handled. The small percentage of seeds (approximately 1.5% for rats and 5% for pigs) that survived gut passage germinated in higher proportions than those in whole fruits. Percentages of seed survival to germination are lower than found in similar studies with native avian frugivores. Our results indicate that pigs and rats have mixed effects on seeds, but are not suitable surrogates for native seed dispersers.     

Efficiency of endozoochorous seed dispersal in six dry-fruited species (Cistaceae): from seed ingestion to early seedling establishment

We combined laboratory and nursery experiments to analyse the effectiveness of sheep as endozoochorous seed dispersers of six native shrubby Cistaceae species collected in SE Spain (Helianthemum apenninum (L.) Mill., H. violaceum (Cav.) Pers., Fumana ericoides (Cav.) Grand., F. thymifolia (L.) Spach, Cistus monspeliensis L. and C. laurifolius L.), considering the main stages after seed ingestion, i.e. seed recovery, seed germination, seedling emergence and early seedling establishment. Seed recovery after gut passage was high (around 40%) for all the species, except F. thymifolia (12%). Most seeds (ca. 90%) were recovered within 48 h after ingestion for all the species, although seeds were still recovered up to 96 h after ingestion. Gut passage increased germination up to seven-fold compared to non-ingested seeds. Furthermore, seedling emergence from seeds contained in pellets was overall similar (intact pellets) to or higher (crumbled pellets) than emergence from seeds without dung. Survival of emerged seedlings and mass of seedlings after 20 days were not reduced by dung. Sheep act therefore as effective dispersers of these Cistaceae species by scattering seeds and promoting germination, while faeces do not hamper seedling establishment. We conclude that the interaction between herbivorous ungulates and these dry-fruited species may be considered a mutualism qualitatively similar to the mutualism between frugivorous vertebrates and fleshy-fruited plants.     

The role of nocturnal omnivorous lemurs as seed dispersers in Malagasy rain forests

Fruit-eating animals play important roles as seed dispersal agents in terrestrial systems. Yet, the extent to which seed dispersal by nocturnal omnivores may facilitate germination and the recruitment of plant communities has rarely been investigated. Characterizing their roles in seed dispersal is necessary to provide a more complete picture of how seed dispersal processes affect ecosystem functioning. We investigated the roles and impacts of two species of nocturnal omnivorous lemur species, Microcebus jollyae and M. rufus, on seed dispersal in Madagascar's rain forests, through analysis of fecal samples and germination experiments. Data show that these lemur species, which are among the world's smallest primates, dispersed 22 plant species from various forest strata and that the defecated seeds germinated faster and at higher rates than control seeds for the eight plant species we tested. Even though mouse lemurs dispersed both native and non-native plant species, non-native plant species represented a relatively small proportion (17%). These results demonstrate that overlooked nocturnal omnivores can act as important seed dispersers, which may have critical implications for forest regeneration and the maintenance of plant diversity in fragmented/degraded forests. Finally, we provide critical insights into the previously unobserved behavior and diet of endangered nocturnal lemurs for their effective conservation.     

Asymmetrical Dependence Between a Neotropical Mistletoe and its Avian Seed Disperser

The degree of interdependence among interacting species has major implications for our understanding of the coevolutionary process and biodiversity maintenance. However, the mutualism strength among fruiting plants and their seed dispersers remains poorly understood in tropical ecosystems. We evaluated simultaneously the effectiveness of the avian seed dispersers of the mistletoe Struthanthus flexicaulis (Loranthaceae) and the contribution of its fruits to their diets in a highland rocky savanna in southeastern Brazil. The mistletoe fruits are small lipid‐rich pseudoberries available throughout the year. Four passerine birds fed on fruits, but Elaenia cristata (Tyrannidae) was the most effective disperser, responsible for more than 96 percent of the dispersed seeds. This bird swallowed fruits whole, expelling and depositing undamaged seeds by regurgitation and bill wiping on perches. From 646 dispersed seeds, 56 percent were deposited on safe sites, thin live twigs of 38 susceptible host species. Elaenia cristata were predominantly frugivorous, feeding on typically ornithocoric fruits of at least 12 species, but also on arthropods. Although fruits represented 75 percent of the feeding bouts along the year, S. flexicaulis fruits represented only 34 percent of the E. cristata diet. Our results highlight the asymmetrical nature of this mutualistic interaction, with the mistletoe life cycle locally linked to one highly effective seed disperser that is more weakly dependent on mistletoes fruits as a food source. We suggest that merging the seed dispersal effectiveness framework with diet assessment of seed dispersers is needed to clarify the asymmetries in mutualistic pairwise interactions involving plants and their animal partners.     

Comparative Seed Dispersal Effectiveness of Sympatric Alouatta guariba and Brachyteles arachnoides in Southeastern Brazil1

I compared the effectiveness of sympatric brown howlers (Alouatta guariba) and muriquis (Brachyteles arachnoides) as seed dispersers in terms of quantitative and qualitative attributes. I hypothesized that differences in feeding and behavioral patterns between these large‐bodied folivorous/frugivorous primates would lead to dissimilarities in their effectiveness as endozoochoric seed dispersal agents. The study was carried out in a semideciduous forest fragment of Fazenda Barreiro Rico, southeastern Brazil. Through behavioral sampling of frugivory and defecation events as well as analyses of fecal samples, I determined that A. guariba dispersed fewer species and produced a lower proportion of dung with intact seeds than B. arachnoides. There was no difference between the number of seeds in fecal samples of A. guariba and B. arachnoides. These primates affected to a similar degree both germination percentage and latency to germination of seeds they ingested or removed the pulp from. Howlers and muriquis were also similar in carrying seeds away from the parent trees. Contrary to muriquis, howlers defecated seeds under the canopy of conspecific lianas, where seeds are expected to suffer high mortality rates, and voided seeds predominantly in a clumped pattern. B. arachnoides was a more effective seed disperser when compared to A. guariba in some attributes evaluated, but not in others. Given the interspecific variation in recruitment patterns of tropical plants and the loss of frugivorous bird species at the study site, the differences between howlers and muriquis in their abilities as seed dispersers may crucially influence the composition and maintenance of seedling diversity.     

Primary Seed Dispersal by Red Howler Monkeys and the Effect of Defecation Patterns on the Fate of Dispersed Seeds1

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 beedes, in dumped 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.     

Seed dispersal of Diospyros virginiana in the past and the present: Evidence for a generalist evolutionary strategy

Several North American trees are hypothesized to have lost their co‐evolved seed disperser during the late‐Pleistocene extinction and are therefore considered anachronistic. We tested this hypothesis for the American persimmon (Diospyros virginiana) by studying the effects of gut passage of proposed seed dispersers on seedling survival and growth, natural fruiting characteristics, and modern animal consumption patterns. We tested gut passage effects on persimmon seeds using three native living species, the raccoon (Procyon lotor), Virginia opossum (Didelphis virginiana), and coyote (Canis latrans), and two Pleistocene analogs; the Asian elephant (Elephas maximus) and alpaca (Vicugna pacos). Persimmon seeds excreted by raccoons, coyotes, and elephants survived gut transit. Gut passage did not affect sprouting success, but did tend to decrease time to sprout and increase seedling quality. Under field conditions, persimmon fruits were palatable on the parent tree and on the ground for an equal duration, but most fruits were consumed on the ground. Seven vertebrate species fed upon persimmon fruits, with the white‐tailed deer (Odocoileus virginianus)—a species not capable of dispersing persimmon seeds—comprising over 90% of detections. Conversely, potential living seed dispersers were rarely detected. Our results suggest the American persimmon evolved to attract a variety of seed dispersers and thus is not anachronistic. However, human‐induced changes in mammal communities could be affecting successful seed dispersal. We argue that changes in the relative abundance of mammals during the Anthropocene may be modifying seed dispersal patterns, leading to potential changes in forest community composition.     

Mammal Abundances and Seed Traits Control the Seed Dispersal and Predation Roles of Terrestrial Mammals in a Costa Rican Forest

In Neotropical forests, mammals act as seed dispersers and predators. To prevent seed predation and promote dispersal, seeds exhibit physical or chemical defenses. Collared peccaries (Pecari tajacu) cannot eat some hard seeds, but can digest chemically defended seeds. Central American agoutis (Dasyprocta punctata) gnaw through hard‐walled seeds, but cannot consume chemically defended seeds. The objectives of this study were to determine relative peccary and agouti abundances within a lowland forest in Costa Rica and to assess how these two mammals affect the survival of large seeds that have no defenses (Iriartea deltoidea, Socratea exorrhiza), physical defenses (Astrocaryum alatum, Dipteryx panamensis), or chemical defenses (Mucuna holtonii) against seed predators. Mammal abundances were determined over 3 yrs from open‐access motion‐detecting camera trap photos. Using semi‐permeable mammal exclosures and thread‐marked seeds, predation and dispersal by mammals for each seed species were quantified. Abundances of peccaries were up to six times higher than those of agoutis over 3 yrs, but neither peccary nor agouti abundances differed across years. Seeds of A. alatum were predominantly dispersed by peccaries, which did not eat A. alatum seeds, whereas non‐defended and chemically defended seeds suffered high levels of predation, mostly by peccaries. Agoutis did not eat M. holtonii seeds. Peccaries and agoutis did not differ in the distances they dispersed seeds. This study shows that seed fates are contingent upon many factors such as seed defenses, frugivore–granivore abundances, and seed‐handling capabilities. Mammal–seed interactions are complex; the outcomes of these interactions depend on the inherent characteristics of seeds and their potential dispersers.     

Seed preferences by rodents in the agri‐environment and implications for biological weed control

Post‐dispersal seed predation and endozoochorous seed dispersal are two antagonistic processes in relation to plant recruitment, but rely on similar preconditions such as feeding behavior of seed consumers and seed traits. In agricultural landscapes, rodents are considered important seed predators, thereby potentially providing regulating ecosystem services in terms of biological weed control. However, their potential to disperse seeds endozoochorously is largely unknown. We exposed seeds of arable plant species with different seed traits (seed weight, nutrient content) and different Red List status in an experimental rye field and assessed seed removal by rodents. In a complementary laboratory experiment, consumption rates, feeding preferences, and potential endozoochory by two vole species (Microtus arvalis and Myodes glareolus) were tested. Seed consumption by rodents after 24 h was 35% in the field and 90% in the laboratory. Both vole species preferred nutrient‐rich over nutrient‐poor seeds and M. glareolus further preferred light over heavy seeds and seeds of common over those of endangered plants. Endozoochory by voles could be neglected for all tested plant species as no seeds germinated, and only few intact seeds could be retrieved from feces. Synthesis and applications. Our results suggest that voles can provide regulating services in agricultural landscapes by depleting the seed shadow of weeds, rather than facilitating plant recruitment by endozoochory. In the laboratory, endangered arable plants were less preferred by voles than noxious weeds, and thus, our results provide implications for seed choice in restoration approaches. However, other factors such as seed and predator densities need to be taken into account to reliably predict the impact of rodents on the seed fate of arable plants.     

Pogonomyrmexcunicularius as the keystone disperser of elaiosome‐bearing Jatropha excisa seeds in semi‐arid Argentina

Myrmecochory or seed dispersal by ants is often described as a diffuse mutualism, because many of the ant species that function as partners are considered to be similar in terms of the frequency and consequences of their interactions. In this work, we test this assumption by conducting ant community surveys and seed removal experiments in six study sites located within a semi‐arid region of northwest Argentina. At each site, we characterized the ant assemblage that interacted with the seeds of Jatropha excisa Griseb. (Euphorbiaceae), an ant‐dispersed native shrub. Our results demonstrate that seed removal was dominated by one species, Pogonomyrmex cunicularius Mayr (Hymenoptera: Formicidae: Myrmicinae), which was responsible of 84% of the observed seed removal events. Although several ant species were attracted to the elaiosome‐bearing seeds of J. excisa, seed removal did not depend on ant community composition (species richness and ant activity) but was significantly influenced by the abundance of P. cunicularius. Its physical, behavioral, and ecological attributes are common with other ant species that have been characterized as keystone seed dispersers in other regions of the world. Nest feeding with marked seeds revealed that once P. cunicularius ants consume the elaiosomes, seeds are left inside the nests undamaged and at an appropriate depth for emergence. Our results support the hypothesis that myrmecochory is often an unevenly diffuse mutualism (i.e., one partner species is particularly important) and that at a local scale P. cunicularius is the keystone seed disperser of J. excisa.     

Differentiation during fig ontogeny suggests opposing selection by mutualists

Dioecy allows separation of female and male functions and therefore facilitates separate co‐evolutionary pathways with pollinators and seed dispersers. In monoecious figs, pollinators' offspring develop inside the syconium by consuming some of the seeds. Flower‐stage syconia must attract pollinators, then ripen and attract seed dispersers. In dioecious figs, male (“gall”) figs produce pollen but not viable seeds, as the pollinators' larvae eat all seeds, while female (“seed”) figs produce mostly viable seeds, as pollinators cannot oviposit in the ovules. Hence, gall and seed figs are under selection to attract pollinators, but only seed figs must attract seed dispersers. We test the hypothesis that seed and gall syconia at the flower stage will be similar, while at the fruiting stage they will differ. Likewise, monoecious syconia will be more similar to seed than gall figs because they must attract both pollinators and seed dispersers. We quantified syconium characteristics for 24 dioecious and 11 monoecious fig species and recorded frugivore visits. We show that seed and gall syconia are similar at the flower stage but differ at the fruit stage; monoecious syconia are more similar to seed syconia than they are to gall syconia; seed and gall syconia differentiate through their ontogeny from flower to fruit stages; and frugivores visit more monoecious and seed syconia than gall syconia. We suggest that similarity at the flower stage likely enhances pollination in both seed and gall figs and that differentiation after pollination likely enhances attractiveness to seed dispersers of syconia containing viable seeds. These ontogenetic differences between monoecious and dioecious species provide evidence of divergent responses to selection by pollinators and seed dispersers.