Dispersal Effectiveness Research Articles

Linking animal behaviour and tree recruitment: Caching decisions by a scatter‐hoarder corvid determine seed fate in a Mediterranean agroforestry system

Abstract Seed dispersal by scatter‐hoarder corvids is key for the establishment of important tree species from the Holarctic region such as the walnut (Juglans regia). However, the factors that drive animal decisions to cache seeds in specific locations and the consequences of these decisions on seed fate are poorly understood. We experimentally created four distinct, replicated habitat types in a Mediterranean agricultural landscape where the Eurasian magpie (Pica pica) is a common scatter hoarder: soft bare soil; compacted bare soil; compacted soil with a dense herbaceous cover; and soft linear bare soil made up of the irrigation furrows that separated the rest of the treatments. We also experimentally placed visual landmarks (stones, sticks and bunches of dry plants) to test if magpies use them to place seed caches. Walnut dispersal from feeders to the habitats was monitored by radiotracking and camera traps. A sowing experiment simulating natural caches tested the effect of caching type on seed germination and seedling emergence. Seed mass was controlled for the dispersal and sowing experiments. Magpies selected the two habitats with soft soil, and avoided the one with compacted soil, to cache nuts. Seed mass did not affect dispersal distance, germination or emergence; however, heavier seeds were cached more often under litter and in the habitat with herbaceous cover, whereas lighter seeds were more often buried in the soft bare soil habitat. Seed burial under soil or litter determined seed fate, as there was virtually no emergence from unburied nuts. There was no evidence of any effect of the visual landmarks. Synthesis. The consequences of seed caching for seedling early establishment are driven by a fine decision‐making process of the disperser. Magpies seemed to ponder the characteristics of the habitat and the seed itself to determine where and how to cache each nut. By doing so, magpies reinforced the quality of seed dispersal effectiveness, as they cached walnuts in locations that enhanced both seed survival and seedling emergence.

Dispersal success of a specialized tropical tree depends on complex interactions among diverse mammalian frugivores

The study of seed dispersal in tropical forest communities is complicated by the high diversity of frugivores and the complex interactions among species and their environments. Determining which species are effective dispersers and which are opportunists with neutral or even negative effects on fruiting plants is a major problem which requires detailed studies focused on particular plant species. In this study we focused on seed dispersal of the wild rambutan (Nephelium melliferum) which supplies energy-rich fruits to primates and other mammals in a seasonal evergreen forest in central Thailand. We hypothesized that gibbons (Hylobates lar) were the most important dispersers and were capable of carrying and defecating seeds away from the tree crown where seeds or seedlings could escape increased distance or density-dependent mortality. We determined the seed dispersal effectiveness of all major arboreal consumers of Nephelium fruit (gibbons, pig-tail monkeys, squirrels) by using data on fruit production and consumption from fruit/seed traps under the canopies of eight sample trees, observations on animals feeding in fruiting trees, and seed deposition data at varying distances from tree crowns. We assessed the survival of seeds and seedlings in relation to distance from the crown by experiments and transect counts. Camera traps were used to detect consumption of seeds on the ground by terrestrial consumers. About half of the ripe fruit crop was harvested by squirrels which gnawed off the outer husk, ate the pulp and dropped intact seeds to the ground. Monkeys chewed and sucked off the pulp and dropped most seeds to the ground not far from the tree. Seeds and intact fruits dropped by squirrels and monkeys supported a large variety of terrestrial mammals most of which were seed predators. Gibbons, which swallow the seed with pulp attached, consumed only 16 % of the fruit crop but were the most effective and reliable seed dispersers overall, and appear to be the most specialized seed dispersal mutualist. Distance-dependent mortality was found in first-year seedlings, as well as evidence that further mortality must space out older saplings prior to recruitment into the tree population, which validates the importance of dispersal by gibbons. However, the great majority of fruits of Nephelium melliferum were consumed by mammalian opportunists and seed predators which interacted with one another in ways which depend on composition of the local community.

Foraging Strategies of Invasive Macaca fascicularis may Promote Plant Invasion in Mauritius

The effectiveness of seed dispersal by frugivorous primates may vary between seasons and plant species, depending on foraging strategies. We investigated how foraging strategies of an invasive frugivorous primate (the long-tailed macaque, Macaca fascicularis) affect seed dispersal effectiveness (SDE) between native and invasive plants in Mauritius’ native remnant forests. By collecting behavioural data on a group of partially habituated macaques via scan sampling from December 2019 until December 2020 (mean 19.2 ± SD 7.3 hours per month), we investigated seasonal patterns in diet, home range, and fruit availability to identify foraging strategies and determine fruit preference. We simultaneously assessed SDE for invasive vs native plants by quantifying native and invasive fruits consumed or dropped intact by macaques during feeding bouts (n = 114). Macaques fed increasingly on ripe invasive fruits and less on other food items as fruit availability increased, due to preference for invasive fruits and disproportionate availability of invasive vs native fruits. When fruit became scarcer, macaques had larger home ranges, increasingly fed on scarce unripe native and invasive fruits, and expanded their diet by eating orchard crops, indicating use of energy-maximizing strategies. Macaques consumed more native than invasive fruits when unripe and commonly destroyed seeds of native fruits, indicating higher SDE for invasive vs native plants. Higher discard rates of unripe compared to ripe fruits further reinforced these differences in SDE. Our results highlight potential facilitation of plant invasion by an invasive primate, due to foraging strategies shaped by the availability of invasive fruits.

A seed dispersal effectiveness framework across the mutualism–antagonism continuum

Many angiosperms rely on vertebrates for seed dispersal via gut passage, an interaction that has been traditionally classified as a mutualism. The seed dispersal effectiveness (SDE) framework provides a mechanistic approach to evaluate evolutionary and ecological characteristics of animal‐mediated seed dispersal, by synthesising the quantity and the quality of the dispersal that a plant species receives from each of its animal dispersers. However, the application of the SDE framework has been largely restricted to plant–frugivore interactions, whereas animal‐mediated seed dispersal results from plant–disperser interactions that cover a continuum from pure mutualisms to antagonisms. This biases ecological and evolutionary knowledge on plant–disperser interactions. Here, we propose an extended SDE framework (‘eSDE') that allows comparing plant–disperser interactions in the full mutualism–antagonism continuum ranging from pure mutualisms (frugivores) to conditional mutualisms (scatter‐hoarding granivores and folivores) and antagonisms (pure granivores). We present the eSDE framework, and use examples to illustrate how it can be applied to compare effectiveness among plant–disperser interaction types. Our initial comparison based on available data suggests that vertebrate species differ more in the number of seeds they deposit away from the mother plant (quantity), than in the effects such dispersal processes have on seed fate (quality). Scatter‐hoarding granivores provide the most effective dispersal due to high removal rates, closely followed by frugivores due to high deposition rates. Folivores and pure granivores provide low quantity dispersal, but of high and moderate quality, respectively. These early comparative insights illustrate the necessity and usefulness of more standardized data collection protocols, for which we provide recommendations. Applying the eSDE framework can reveal broad‐scale patterns across and within plant–disperser interaction types, which will advance our evolutionary understanding of plant–animal interactions. This will provide new insights into the consequence of anthropogenic impacts on vertebrate‐mediated seed dispersal in a world in which plant–animal interactions are increasingly threatened.

Nondormant Acorns Show Higher Seed Dispersal Effectiveness Than Dormant Ones

Seed dormancy has been thought to be an important survival strategy to tune the seed dispersal timing. Although a theoretical trade-off between seed dormancy and dispersal is often proposed, empirical field evidence of the trade-off between seed dormancy, spatial dispersal, and seedling recruitment is still lacking. Here, we tracked seed dispersal of several Fagaceae species exhibiting different levels of dormancy both in artificial enclosures and in the field. We presented evidence that oak species with nondormant acorns rather than those bearing dormant species exhibit reduced spatial dispersal. Despite the empirical evidence that seed germination is negatively correlated with spatial dispersal, nondormancy rather than dormancy showed higher seed dispersal effectiveness, demonstrating a negative correlation between seed dormancy and dispersal fitness. Our study, using the oak-rodent system, may provide solid evidence of a dispersal–germination trade-off between spatial and temporal correlation, highlighting the ecological role of seed germination schedule in seed dispersal and life-history evolution.

The Influence of Seed Characteristics on Seed Dispersal Early Stages by Tibetan Macaques.

Simple SummarySeed dispersal by frugivores is critical to forest regeneration. However, the Tibetan macaque’s seed dispersal function and the effect of seed physical characteristics on seed dispersal effectiveness need to be confirmed. We not only demonstrated that Tibetan macaques could act as seed dispersers, but we also investigated the effect of seed physical characteristics on gut passage time and seed damage rates. Smaller seeds are less likely to be damaged and remain for longer periods of time, whereas larger and heavier seeds are defecated more quickly. In our experiments, the seed-to-shell investment rate had no effect on the damage rate. Understanding the role of seed dispersal in primates can aid in the understanding of seed dispersal symbiosis.There are numerous ecological and evolutionary implications for the ability of frugivores to predate on fruits and consume or disperse their seeds. Tibetan macaques, which are considered important seed predators, typically feed on fruits or seeds. However, systematic research into whether they have a seed dispersal function is still lacking. Endozoochory allows seeds to disperse over greater distances by allowing them to remain in the animal’s digestive tract. Consumption of fruit may not imply effective seed dispersal, and the physical characteristics of seeds (e.g., size, weight, specific gravity, etc.) may influence the dispersal phase’s outcome. We conducted feeding experiments with three captive Tibetan macaques (Macaca thibetana) and nine plant seeds to determine the influence of seed characteristics on Tibetan macaques’ early stages of seed dispersal. The results revealed that the percentage of seed destruction (PSD) after ingestion was 81.45% (range: 15.67–100%), with the PSD varying between plant species. Among the three passage time parameters, the transit time (TT) (mean: 18.8 h and range: 4–24 h) and the time of seed last appearance (TLA) (mean: 100.4 h and range: 48–168 h) differed significantly between seed species, whereas the mean retention time (MRT) (mean: 47.0 h and range: 32–70.3 h) did not. In terms of model selection, PSD was influenced by seed size, weight, volume, and specific gravity; TT was influenced by seed-to-shell investment rate, weight, volume, and specific gravity; and TLA was influenced only by seed size. These findings imply that seeds with a smaller size, specific gravity, volume, and greater weight pass more easily through the monkeys’ digestive tracts. Particularly, seeds with a mean cubic diameter (MCD) of <3 mm had a higher rate of expulsion, larger volume, and weight seeds pass faster, while smaller remained longer. Tibetan macaques, as potential seed dispersers, require specific passage time and passage rates of small or medium-sized seeds. Larger and heavier seeds may be more reliant on endozoochory. Tibetan macaques have the ability to disperse seeds over long distances, allowing for gene flow within the plant community.

Seed Size Variation of Trees and Lianas in a Tropical Forest of Southeast Asia: Allometry, Phylogeny, and Seed Trait - Plant Functional Trait Relationships.

Seed size is a key trait for understanding and predicting ecological processes in a plant community. In a tropical forest, trees and lianas are major components driving ecosystem function and biogeochemical processes. However, seed ecological research on both components remains limited, particularly phylogenetic patterns and relationships with other traits. Here, we compiled a unique dataset of seed size (seed mass and geometrical size metrics) based on collections of more than 5,200 seeds of 196 woody plant species, covering >98 and 70% of tree and liana stems, respectively, located on a 30-ha plot in a tropical evergreen forest in central Thailand. We aimed to (1) develop allometric equations among seed size metrics to predict seed mass; (2) examine phylogenetic influence on seed size variation; and (3) examine relationships among seed traits and several other functional plant traits. Our allometric equations relating seed mass, seed volume, and width were well-fitted with data (R2= 0.94, 0.87 respectively). A phylogenetic signal test found that seed size was randomly distributed across the phylogeny. To study the functional trait relationships, we separately tested seed size data of the tree and liana communities (146 and 50 species, respectively), against mean body size of frugivores, successional niches, leaf, and structural traits. For the tree community, seed size was significantly related to mean body size of frugivores, which we believe is a basic driver of seed size because it is related to the gape width affecting dispersal effectiveness. Nearly all leaf traits were significantly positively correlated with seed size (p < 0.03). The significant positive correlation of leaf area and greenness suggested the high-energy demand of large-seeded species. We found a strong positive correlation between seed size and leaf toughness, suggesting a coordination between seed size and leaf defense. However, all these patterns disappeared in the same analysis applied to the liana community. Liana seed size variation was lower than that of trees, perhaps because lianas grow in relatively more uniform conditions in the forest canopy. Frugivore size was the strongest driver of seed size variation. Our study shows a surprising contrast between trees and lianas that is worth further investigation.

Temporary Translocation of Entire Mistletoe Plants to Understand the Mechanistic Basis of Animal Foraging Decisions.

Fruiting mistletoes present a model system for understanding decisions made by foraging animals when locating food. Where, when, and how animals find food is central to many ecological questions, relating to the basis of individual foraging decisions and the extent to which these decisions are innate or acquired. Ecologists have paid particular attention to frugivores, quantifying their preference for fruits with specific shapes, colors, or scents, which, over evolutionary time, confer selection for suites of traits in their favored plants whose seeds they disperse. This work outlines a novel experimental approach to manipulating food plant occurrence and measuring the response of wild, free-living animals, ideally suited to studying the evolutionary origin and ecological maintenance of seed dispersal. This "cut and paste" protocol involves removing an entire fruiting mistletoe plant from its host and either returning it to its original location or moving it to a novel location, affixing it to a 'pseudo-host' of the same or different tree species. By counting visits to the mistletoe and noting the duration, species, and behaviors, a series of comparisons can discern the most important factors affecting foraging decisions and the consequences for both plant and animal. Here, the protocol is illustrated with a case study to determine between-guild differences in mistletoe frugivory. The experimental approach teases apart the mechanistic basis of search image formation and refinement, spatial learning, interspecific differences in foraging strategies, and how these changes modify seed dispersal effectiveness. Finally, potential modifications are considered with respect to addressing other questions on foraging ecology, plant-animal interactions, and coevolution.

Effect of Seed Traits and Waterbird Species on the Dispersal Effectiveness of Wetland Plants.

Simple SummaryQuantifying the effects of seed traits on waterbird-mediated seed dispersal effectiveness contributes to understanding wetland plant ecology and hence can be used for improving wetland conservation and restoration, especially in the global scenario of wetland degradation and destruction. Waterbirds, especially dabbling ducks, can effectively disperse wetland plant seeds through their guts (endozoochory). Here, we experimentally quantified the effects of seed traits (length and lignin) on retention time, retrieval, and germination of surviving seeds. The results showed that the germination rate of recovered seeds was higher than the controls, suggesting that endozoochory contributes to seed germination. Local seed dispersal was more efficient, and long-distance dispersal was possible. Furthermore, smaller seeds passed through the guts faster, and there was no significant effect of disperser species on germination. We concluded that waterbird-mediated endozoochory plays an important role in wetlands.Seed dispersal is an important ecological process in wetland ecosystems and helps maintain community structure and ecosystem biodiversity. Waterbird-mediated endozoochory is an effective and feasible dispersal mechanism for wetland plants; however, the influence of vectors and seed traits on this mechanism remains unclear. To investigate the effects of vector species and seed traits (length and lignin) on retention time, retrieval and germination of gut-surviving seeds, we fed Baikal teals (Anas formosa) and green-winged teals (Anas crecca) eight common plant seeds (Polygonum aviculare, Rumex dentatus, Polygonum orientale, Vallisneria natans, Ranunculus polii, Polygonum hydropiper, Carex cinerascen and Euphrasia pectinata) in the Shengjin Lake wetland (a Ramsar site). We collected fecal samples at intervals of 2–6 h for 36 h, and found that the percentage of recovered seeds differed significantly among teal and plant species (3%~30%); 94% of viable seeds were recovered within 12 h after feeding. Moreover, the germination rate of the recovered seeds (25%~56%) was higher than that of the control. The seed retention time was affected by seed lignin and disperser species; higher lignin made digestion difficult with higher retrieval. Smaller seeds passed through the guts but had no significant effect on recovered seeds. Seed length and disperser species showed no significant correlation with germination. These findings suggested endozoochory by dabbling ducks as an effective wetland seed dispersal mechanism.

Seed fate in ant‐mediated dispersal: Seed dispersal effectiveness in the Ectatomma ruidum (Formicidae)—Zanthoxylum ekmanii (Rutaceae) system

AbstractPlants are often dispersal limited relying on passive or active agents to find suitable microhabitats for germination. Seeds of pioneer tree species, for example, require light gaps for growth but have short median dispersal distances and often do not provide a food reward to encourage animal dispersal. Zanthoxylum ekmanii seeds are frequently moved by ants but evaluating the effectiveness of ant‐mediated seed removal requires knowledge of the species moving the seeds, how far they are moved, and the deposition site. To assess the effectiveness of ants as seed dispersers of Z. ekmanii, we utilized the seed dispersal effectiveness framework. We tracked the movement of seeds from caches on the forest floor, revealing that foragers of Ectatomma ruidum moved 32.8% of seeds an average first distance of 99.8 cm with 68.3% of those seeds taken into a colony. The quality of deposition location was assessed using a seedling emergence study where freshly germinated seeds were buried at different depths. Seedlings were primarily able to emerge from the shallowest depths. Wax castings of E. ruidum colonies demonstrated that seeds brought into the colony were deposited in chambers that had larvae present and experienced more damage than seeds unhandled by ants. Foragers, however, did not have a strong enough bite force to rupture Z. ekmanii seeds likely because their muscle morphology is not structured to maximize force generation. Overall, E. ruidum may help fine tune deposition location, incorporating seeds into the topsoil, though few seeds will likely emerge if soil bioturbation is low.Abstract in Spanish is available with online material

Predation risk can modify the foraging behaviour of frugivorous carnivores: Implications of rewilding apex predators for plant-animal mutualisms.

Apex predators play key roles in food webs and their recovery can trigger trophic cascades in some ecosystems. Intra‐guild competition can reduce the abundances of smaller predators and perceived predation risk can alter their foraging behaviour thereby limiting seed dispersal by frugivorous carnivores. However, little is known about how plant–frugivore mutualisms could be disturbed in the presence of larger predators.We evaluated the top‐down effect of the regional superpredator, the Iberian lynx Lynx pardinus, on the number of visits and fruits consumed by medium‐sized frugivorous carnivores, as well as the foraging behaviour of identified individuals, by examining the consumption likelihood and the foraging time.We carried out a field experiment in which we placed Iberian pear Pyrus bourgaeana fruits beneath fruiting trees and monitored pear removal by frugivorous carnivores, both inside and outside lynx ranges. Using camera traps, we recorded the presence of the red fox Vulpes vulpes, the Eurasian badger Meles meles and the stone marten Martes foina, as well as the number of fruits they consumed and their time spent foraging.Red fox was the most frequent fruit consumer carnivore. We found there were fewer visits and less fruit consumed by foxes inside lynx ranges, but lynx presence did not seem to affect badgers. We did not observe any stone marten visits inside lynx territories. The foraging behaviour of red foxes was also altered inside lynx ranges whereby foxes were less efficient, consuming less fruit per unit of time and having shorter visits. Local availability of fruit resources, forest coverage and individual personality also were important variables to understand visitation and foraging in a landscape of fear.Our results show a potential trophic cascade from apex predators to primary producers. The presence of lynx can reduce frugivorous carnivore numbers and induce shifts in their feeding behaviour that may modify the seed dispersal patterns with likely consequences for the demography of many fleshy‐fruited plant species. We conclude that knowledge of the ecological interactions making up trophic webs is an asset to design effective conservation strategies, particularly in rewilding programs.

Cascading effect of source limitation on the granivore-mediated seed dispersal of Korean pine (Pinus koraiensis) in secondary forest ecosystems

BackgroundGranivore-mediated seed dispersal is susceptible to changes in seed availability and silvicultural management, which alters synzoochorous interactions in the antagonism-mutualism continuum and affects the seed dispersal effectiveness (SDE), and eventually, the plant recruitment. We conducted a whole-year study of seed addition to quantify the granivores-Korean pine (Pinus koraiensis) synzoochorous interactions and the SDE in the same secondary forests with two treatments. Both treatments had seed source limitations: one was caused by the disappearance of Korean pine due to the historical disturbance, the other by pinecone harvesting in Korean pine plantations adjacent to the secondary forests. Thinning with different intensities (control, 25%, and 50%) were also performed to further explore the synzoochorous interactions and SDE in response to silvicultural management in the second type of forests.ResultsSource limitation increased the proportion of pre- and post-dispersal seed predation, and made the granivores-Korean pine interaction shift more towards antagonism, with the estimated SDE of 2.31 and 3.60, respectively, for the secondary forests without and with Korean pine. Thinning with different intensities did not alleviate the reactions towards antagonism but altered SDE; granivores occurrence decreased, but the proportion of pre- and post-dispersal seed predation increased, resulting in a fivefold decreased seedling recruitment in 25% thinning (the lowest SDE of 0.26).ConclusionThe source limitation coupling thinning biased the synzoochorous interactions more towards antagonism and significantly lowered granivore-mediated SDE, which limited the successful recruitment of Korean pine in secondary forests. Forest managers should control pinecone harvesting, protect the synzoochorous interaction, and take into account masting event for Korean pine regeneration in the future.

Linking howler monkey ranging and defecation patterns to primary and secondary seed dispersal.

To define the chances of a dispersed seed to produce a new recruit, it is essential to consider all stages of the dispersal process. Howler monkeys are recognized to have positive impacts on forest regeneration, acting as primary dispersers. Furthermore, dung beetles attracted to their feces protect the seeds against predators, and provide a better microenvironment for germination due to the removal of fecal matter, to seed burial, and/or by reducing the spatial aggregation of seeds in fecal clumps. Despite the recognized positive effects of primary seed dispersal through defecation by howler monkeys for plant recruitment, there are some important aspects of their behavior, such as the habit of defecating in latrines, that remain to be explored. Here, we investigated the fate of Campomanesia xanthocarpa seeds defecated by brown howlers, Alouatta guariba clamitans, and the secondary seed dispersal by dung beetles, considering how this process is affected by the monkey's defecation patterns. We found that brown howler monkeys dispersed seeds from several species away from fruit-feeding trees, partly because defecation under the canopy of such trees was not very frequent. Instead, most defecations were associated with latrines under overnight sleeping trees. Despite a very similar dung beetle community attracted to howler feces in latrines and fruit-feeding sites, seeds were more likely to be buried when deposited in latrines. In addition, C. xanthocarpa seeds showed higher germination and establishment success in latrines, but this positive effect was not due to the presence of fecal matter surrounding seeds. Our results highlight that A. guariba clamitans acts as a legitimate seed disperser of C. xanthocarpa seeds in a preserved context of the Brazilian Atlantic Forest and that defecations in latrines increase the dispersal effectiveness.

Releases of the parasitoid Anisopteromalus calandrae (Hymenoptera: Pteromalidae) can control Sitophilus zeamais (Coleoptera: Curculionidae) in big bags of paddy rice

Sitophilus zeamais is a key pest in stored rice in Spain and other Mediterranean countries. Today, it is mostly controlled with a few pesticides, such as pyrethroids or phosphine. Apart from the problem of pesticide resistance, this can lead to the accumulation of toxic residues in the stored rice. Therefore, alternative control methods are needed. Biological control with the parasitoid Anisopteromalus calandrae is a feasible and sustainable alternative since it is very effective at limiting the growth of the weevil population. In this study, we evaluated the dispersal capacity and effectiveness of this parasitoid in controlling S. zeamais larvae located deep in 500 kg bags of paddy rice during two seasons, summer and autumn. The parasitoid was easily able to reach the bottom of the bags (1 m) in both seasons. At the released parasitoid-to-host ratio, the parasitoid was also able to limit weevil population growth by around 60% compared to the control treatment, based on the released parasitoid-to-host ratio, indicating that it offers an effective alternative control method.

Mesopredator frugivory has no effect on seed viability and emergence under experimental conditions

AbstractMembers 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.

Studying seed dispersal through the lens of movement ecology

Frugivore movement plays a critical role in animal‐mediated seed dispersal. Frugivores utilize resources that are heterogeneously distributed in the landscape and execute complex movement to exploit these resources. Employing the ‘movement ecology paradigm', we discuss the drivers behind frugivore movement, categorize movement into canonical activity modes and explore the potential impacts on seed dispersal effectiveness via removal and deposition of seeds. Among the movement drivers, frugivore physiology determines the goals, motion capacities determine how frugivores move across their heterogenous landscape, navigation capabilities determine how frugivores acquire and process both internal and external information that set them in motion, and biotic interactions further modulate frugivore movement. The movement process that emerges from the interactions of these drivers can be classified into different canonical activity modes that determine levels of seed removal and generate clumped, even or other spatial distributions of seed deposition. We provide a novel framework to integrate movement drivers, frugivore activities and seed dispersal services. We provide future directions utilizing advances in animal movement research to better understand the role of animal movement in the effectiveness of seed dispersal, highlighting potential impacts of increased anthropogenic activities. To advance a mechanistic understanding of animal‐mediated seed dispersal, we encourage increased collaboration between animal movement and plant ecologists.

Changes in the structure of seed dispersal networks when including interaction outcomes from both plant and animal perspectives

Interaction frequency is the most common currency in quantitative ecological networks, although interaction quality can also affect benefits provided by mutualisms. Here, we evaluate if interaction quality can modify network topology, species' role and whether such changes affect community vulnerability to species loss. We use a well‐examined study system (bird–lizard and fleshy‐fruited plants in the ‘thermophilous' woodland of the Canary Islands) to compare network and species‐level metrics from a network based on fruit consumption rates (interaction frequency, IF), against networks reflecting functional outcomes: a seed dispersal effectiveness network (SDE) quantifying recruitment, and a fruit resource provisioning network (FRP), accounting for the nutrient supply of fruits. Nestedness decreased in the FRP and the SDE networks, due to the lack of association between fruit consumption rates and 1) nutrient content and; 2) recruitment at the seed deposition sites, respectively. The FRP network showed lower niche overlap due to resource use complementarity among frugivores. Interaction evenness was lower in the SDE network, in response to a higher dominance of lizards in the recruitment of heliophilous species. Such changes, however, did not result in enhanced vulnerability against extinctions. At the plant species level, strength changed in the FRP network in frequently consumed or highly nutritious species. The number of effective partners decreased for species whose seeds were deposited in unsuitable places for recruitment. In frugivores, strength was consistent across networks (SDE vs IF), showing that consumption rates outweighed differences in dispersal quality. In the case of lizards, the increased importance of nutrient‐rich species resulted in a higher number of effective partners.Our work shows that although frequency strongly impacts interaction effects, accounting for quality improves our inferences about interaction assembly and species role. Thus, future studies including interaction outcomes from both partners' perspectives will provide valuable insights about the net effects of mutualistic interactions.

Interspecific competition in germination of bird-dispersed seeds in a habitat with sparse tree vegetation in South Africa

BackgroundBy transporting and scarifying the seeds during ingestion, avian frugivores reduce the competition with siblings, and may improve the germination which is critical for dispersal effectiveness and population recruitment. However, generally, there is limited knowledge on how deposited seeds interact/compete in the new microsite. We tested the hypothesis that the bird-dispersed seeds benefit from improved germination after their passage through the bird’s gut; and we investigated the potential impact of seed density on competition at the microsites by determining whether seed density and species diversity influence germination in the Free State Province, South Africa.ResultsOverall, the results partly supported the hypothesis. Germination trials with defecated seeds of five plant species compared with the manually depulped seeds showed that only Searsia lancea had significantly higher seed germination success and improved germination speed after passage through the bird gut while Ziziphus mucronata only benefited rapid germination. There was a significant correlation between seed size and the germination of bird-ingested seeds except in Olea subsp. africana possibly due to possession of extremely hard protective seed cover. Seed competition experiments pointed to Z. mucronata and O. subsp. africana having significant germination performance that was positively correlated to seed density and seed size while Ehretia rigida did not germinate at all. Seed species diversity in the germination trays did not have a significant impact since the seeds of two former plant species consistently displayed significantly higher germination across the competition levels.ConclusionsWe conclude that different plant species respond differently to seed ingestion by birds, and that further long-term tests for germination physiological responses of the seeds’ samples used in this study are required since poor germination observed in other tree/shrub species cannot be attributed to competition solely.

Larger Doesn't Mean Longer: Neither Body Size Nor Seed Size Affect the Gut Retention Times of Aldabra Giant Tortoises

Seed dispersal through endozoochory is a critical ecosystem function worldwide. Seed gut retention time (GRT; the duration that seeds are retained in the digestive tract) is an important part of the qualitative component of the seed dispersal effectiveness framework. GRT is a major determinant of when and how far away seeds are dispersed, aiding seeds in escaping predation in space as well as in time. In this study, we examined whether the size of the disperser and/or the size of the ingested seeds affect the GRT in Aldabra Giant Tortoises (Aldabrachelys gigantea) on Aldabra Atoll, Seychelles. We selected tortoises of varying body mass (mean ± 1 SD = 48.6 ± 27.2 kg, range = 0.6–104.0 kg) and fed them different-sized artificial seeds (plastic beads; 2, 4.5, and 10 mm diameter). Tortoises defecated the first beads a mean of 12.0 ± 2.7 d after ingestion, and the last beads 20.4 ± 6.0 d after ingestion. Mean GRT was 14.6 ± 3.7 d. We show that neither tortoise body size nor bead size had an effect on the patterns and time of defecation. We discuss the relevance of our result for seed dispersal and for rewilding projects that use Aldabra Giant Tortoises as substitute species for extinct giant tortoises on other oceanic islands.

Seed dispersal effectiveness by oilbirds (Steatornis caripensis) in the Southern Andes of Colombia

AbstractOilbirds are specialized frugivores that disperse seeds; however, no study has evaluated their seed dispersal effectiveness (SDE). We estimated SDE for nine plant species and tested if high‐altitude plants are more effectively dispersed than lowland species and if there are high SDE scores in non‐breeding periods of oilbirds. The quantity factor was estimated from seed rain data in the main cave of Cueva de Los Guacharos National Park (Colombia). The quality component considered germination chance, the probability that seeds reach suitable habitats (using data from GPS devices on three birds) and the probability of establishment in different habitats (literature review). Our model showed that the habitat with more seedrain was the cave (41%), followed by dense forest and mosaics of crops and forests (both ca. 20%). Seed germination was evidenced in 7 of the species, and the other two indicated viability (using tetrazolium tests). The most dispersed species corresponded to palms (Prestoea acuminata and Geonoma undata), but, in terms of biomass, P. acuminata and Dacryodes olivifera (Burseraceae) were the top species. D. olivifera, G. undata, and P. acuminata showed the highest SDE values. No relationship was found between the probability of arrival to suitable habitats and the altitudinal level of the species, but the oilbirds were more effective dispersing seeds in non‐breeding periods. Despite a large amount of seeds dropped at the caves, oilbirds disperse seed to suitable habitats, move seeds long distances, and disperse large seeds. As some of these ecosystem services are unique, oilbird's conservation seems imperative.Abstract in Spanish is available with online material.