Bird dispersal of the larval stage of a seed predator

Multiflora rose seeds containing larvae of the phytophagous wasp Megastigmus aculeatus nigroflavus were fed to a caged mockingbird (Mimus polyglottos). Ninety percent of the seeds were recovered from the bird's feces, and there was no significant difference in subsequent emergence of the wasps from these seeds when compared to controls. This study indicates the dispersal of seed-feeding hymenoptera by avian frugivores may be a widespread and significant phenomenon.     

Ant seed removal in a non-myrmecochorous Neotropical shrub: Implications for seed dispersal

This study investigated ant seed removal of Piper sancti-felicis, an early successional Neotropical shrub. Neotropical Piper are a classic example of bat-dispersed plants, but we suggest that ants are underappreciated dispersal agents. We identified eleven ant species from the genera Aphaenogaster, Ectatomma, Paratrechina, Pheidole, Trachymyrmex, and Wasmannia recruiting to and harvesting P. sancti-felicis seeds in forest edge and secondary forest sites at La Selva, Costa Rica. We also tested for differences in ant recruitment to five states in which ants can commonly encounter seeds: unripe fruit, ripe fruit, overripe fruit, bat feces, and cleaned seeds. Overall, ants harvested more seeds from ripe and overripe fruits than other states, but this varied among species. To better understand the mechanisms behind ant preferences for ripe/overripe fruit, we also studied how alkenylphenols, secondary metabolites found in high concentrations in P. sancti-felicis fruits, affected foraging behavior in one genus of potential ant dispersers, Ectatomma. We found no effects of alkenylphenols on recruitment of Ectatomma to fruits, and thus, these compounds are unlikely to explain differences in ant recruitment among fruits of different maturity. Considering that P. sancti-felicis seeds have no apparent adaptations for ant dispersal, and few ants removed seeds that were cleaned of pulp, we hypothesize that most ants are harvesting its seeds for the nutritional rewards in the attached pulp. This study emphasizes the importance of ants as important additional dispersers of P. sancti-felicis and suggests that other non-myrmecochorous, vertebrate-dispersed plants may similarly benefit from the recruitment to fruit by ants.     

Impact of seed abundance on seed processing and dispersal by the red ant Myrmica rubra

1. Myrmecochory sensu stricto is an ant–plant mutualism in which non‐granivorous ants disperse plant diaspores after feeding on their nutrient‐rich seed appendage, the elaiosome. Phenological traits associated with the diaspore can influence the behaviour of ants and thus their ultimate efficiency as seed dispersers. 2. This study investigated how a contrasting availability of seeds (20 vs. 200 seeds) from the diplochorous Chelidonium majus (Papaveraceae, Linnaeus) plant species influences the behaviour of Myrmica rubra (Formicidae, Linnaeus) ants, from the retrieval of seeds until their dispersal outside the ant nest. 3. Regardless of seed abundance, the ants collected the first diaspores at similar rates. Then, seed retrieval sped up over time for large seed sources until satiation took place with only one‐third of the tested colonies wholly depleting abundant seed sources. 4. No active recruitment by trail‐laying ants was triggered, even to an abundant seed source 5. In both conditions of seed abundance, the majority of the diaspores retrieved inside the nest were discarded with the elaiosome removed and were dispersed at similar distances from the nest. 6. The paper concludes with a discussion of how the quantity of seeds released by a plant with a dual mode of dispersal can potentially influence the behaviour of ant dispersers and hence the dispersal efficiency derived from myrmecochory.     

Quantity,quality and the effectiveness of seed dispersal by animals

Disperser effectiveness is the contribution a disperser makes to the future reproduction of a plant. Although it is a key notion in studies of seed dispersal by animals, we know little about what determines the effectiveness of a disperser. The role of the present paper is to review the available information and construct a hierarchical framework for viewing the components of disperser effectiveness.Effectiveness has both quantitative and qualitative components. The quantity of seed dispersal depends on (A) the number of visits made to the plant by a disperser and (B) the number of seeds dispersed per visit. The quality of seed dispersal depends on (A) the quality of treatment given a seed in the mouth and in the gut and (B) the quality of seed deposition as determined by the probability that a deposited seed will survive and become an adult. In this paper I review the ways disperser behavior, morphology and physiology can influence these major components of disperser effectiveness, and when data permit present preliminary analyses of relationships among components.     

Environmental variability and the initiation of dispersal: turbulence strongly increases seed release

Dispersal is a critical process in ecology. It is an important biological driver of, for example, invasions, metapopulation dynamics, spatial pattern formation and pathogen movement. Much is known about the effect of environmental variability, including turbulence, on dispersal of diaspores. Here, we document experimentally the strong but under-explored influence of turbulence on the initiation of dispersal. Flower heads of two thistle species (Carduus nutans and Carduus acanthoides) with ripe seeds were exposed to series of laminar and turbulent air flows of increasing velocity in a wind tunnel. Seed release increased with wind speeds for both laminar and turbulent flows for both species. However, far more seeds were released, at significantly lower wind speeds, during turbulent flows. These results strongly suggest a need for more quantitative studies of abscission in the field, as well as dispersal models that incorporate variability in the diaspore release phase.     

The timing of frugivore‐mediated seed dispersal effectiveness

The seed dispersal effectiveness framework allows assessing mutualistic services from frugivorous animals in terms of quantity and quality. Quantity accounts for the number of seeds dispersed and quality for the probability of recruitment of dispersed seeds. Research on this topic has largely focused on the spatial patterns of seed deposition because seed fates often vary between microhabitats due to differences in biotic and abiotic factors. However, the temporal dimension has remained completely overlooked despite these factors—and even local disperser assemblages—can change dramatically during long fruiting periods. Here, we test timing effects on seed dispersal effectiveness, using as study case a keystone shrub species dispersed by frugivorous birds and with a fruiting period of 9 months. We evaluated quantity and quality in different microhabitats of a Mediterranean forest and different periods of the fruiting phenophase. We identified the bird species responsible for seed deposition through DNA barcoding and evaluated the probability of seedling recruitment through a series of field experiments on sequential demographic processes. We found that timing matters: The disperser assemblage was temporally structured, seed viability decreased markedly during the plant's fruiting phenophase, and germination was lower for viable seeds dispersed in the fruiting peak. We show how small contributions to seed deposition by transient migratory species can result in a relevant effectiveness if they disperse seeds in a high‐quality period for seedling recruitment. This study expands our understanding of seed dispersal effectiveness, highlighting the importance of timing and infrequent interactions for population and community dynamics.     

Effects of kin-structured seed dispersal on the genetic structure of the clonal dioecious shrub ilex leucoclada

Nonrandom patterns of gene dispersal have been identified as possible causes of genetic structuring within populations. Attempts to model these patterns have generally focused solely on the effects of isolation by distance, but the processes involved are more complex than such modeling suggests. Here, we extend considerations of gene dispersal processes beyond simple isolation by distance effects by directly evaluating the effects of kin-structured gene dispersal mediated by the group dispersal of related seeds within fruits (i.e., kin-structured seed dispersal) by birds on genetic structure in Ilex leucoclada, a clonal dioecious shrub. To examine the genetic structure patterns, we established two 30x30 m plots (one with immature soils in old-growth forest and one in secondary forest, designated IM and SC, respectively) with different I. leucoclada stem densities. In these two plots 145 and 510 stems were found, representing 78 and 85 genets, respectively, identified by analyzing their genotypes at eight microsatellite loci. The clonal structure was stronger in the SC plot than in the IM plot. Correlograms of coancestry for genets in both plots exhibited significant, positive, high values in the shortest distance class, indicating the presence of strong genetic structure. However, Sp statistics revealed that the pattern of the genetic structure differed between the plots. In addition, to estimate the family structure within fruits, we sampled forty fruits, in total, from 15 randomly selected plants in the area around the IM and SC plots, and found that 80% of the fruits were multiseeded and 42-100% of the multiseeded fruits contained at least one pair of full sibs. Simulations based on these estimates demonstrated that the group dispersal of related seeds produced through correlated mating both within and across fruits, but not unstructured half-sib dispersal, could generate the observed magnitude and trends of genetic structure found in the IM plot. Furthermore, in addition to kin-structured seed dispersal, isolation by distance processes is also likely to promote genetic substructuring in the SC plot. After discussing possible ecological factors that may have contributed to the observed genetic structure, we contrast our results with those predicted by general isolation by distance models, and propose that kin-structured seed dispersal should promote some evolutionary phenomena, and thus should be incorporated, where appropriate, in models of gene dispersal in natural plant populations.     

Bird diversity and seed dispersal along a human land-use gradient: high seed removal in structurally simple farmland

Only few studies have analysed the relationship between biodiversity and ecosystem function at the landscape scale although relationships and mechanisms known from experimental studies might be different in natural systems. We quantified bird diversity and seed removal from 38 wild cherry trees (Prunus avium) along a human land-use gradient from forest to structurally diverse to simple agricultural systems. High human land-use intensity led to low species richness and total abundance of the local bird community around wild cherry trees, as expected from previous studies. Nevertheless, trees in structurally simple agroecosystems were visited as frequently as trees in structurally complex landscapes and in forests. Furthermore, the number of seeds removed per tree did not decline with increasing human land-use intensity. Thus, ecosystem function was robust in spite of locally reduced bird diversity. The reason might be that movement behaviour and movement distances of birds changed along the human land-use gradient. It appears that birds moved longer distances to forage in fruiting cherry trees in structurally simple agroecosystems. This suggests that for systems where ecosystem function is mediated by highly mobile organisms, movement behaviour and distances are of considerable importance. Increases in movement distances with increasing human land-use intensity might also be common in other systems in which ecosystem function depends on mobile links.     

Effects of the Argentine ant Linepithema humile on seed dispersal and seedling emergence of Rhamnus alaternus

We studied influence of the Argentine ant's Linepithema humile occurrence on seed dispersal of Rhamnus alaternus (Rhamnaceae). Rhamnus alaternus is a fleshy fruit plant dispersed primarily by birds; the seeds have an elaiosome attractive to ants. The observations were made in two study plots of Mediterranean cork-oak forests (one invaded and the other not invaded by L. humile ) over two years. For R. alaternus , presence of L. humile was associated with of the following: reduction of seed transport to ant nests (80.2% of seed offered were removed in non-invaded vs 7.1% in invaded area), a shorter seed dispersal distance (mean=90.2 cm in non-invaded vs 1.1 cm in invaded area), increase in seed retention time on the soil surface (median time in non-invaded was 50 vs 209.2 min in invaded area) and increased vulnerability to predation. In addition there was lower probability of seedling emergence, due to little elaiosome removal from the seeds (82.0% of emergence for seeds without elaiosome and 57.3% for seeds with elaiosome). These results, similar to findings obtained in South African fynbos, confirm that the Argentine ant invasion can strongly affect ecosystem processes in the Mediterranean biome.     

Studying the quantity component of seed dispersal effectiveness from exclosure treatments and camera trapping

The quantity component of effectiveness of seed dispersal by animals is determined by two events: fruit removal (intensity of the interaction) and animal visitation to the plant (frequency of interactions). Considering dispersal of Prosopis flexuosa seeds as case study, this work aimed at investigating the strengths and weaknesses of the two methods for assessing the quantity component of seed dispersal effectiveness: exclosures and camera traps. Prosopis fruits were offered for 48 hr. Exclosure treatments were performed using two types of wire‐screen cages, allowing access to ants (“closed exclosure”) and to small mammals up to 100 g (“open to small mammals”), and a treatment without exclosure (“open to all removers”). The camera trapping experiment was carried out using vertically oriented cameras placed at approximately 1.80 m height and focused on the fruits. The cameras were set in “motion detect mode,” taking series of three consecutive photographs. The exclosures largely allowed estimation of fruit removal by size‐based groups of animals, but did not provide information on species identity. In contrast, camera traps were able to identify all visitors to species level and could not only determine the number of visits by each species but also the proportion of visits, which resulted in removal of fruits. Camera trapping allowed discriminating among small mammals playing different roles, without underestimating fruit removal by scatter‐hoarding species. The quality of estimation of the quantity component of seed dispersal is remarkably better when the camera trapping method is applied. Additional information obtained, such as activity patterns of visitors, can contribute to a better understanding of the seed dispersal process.     

Assisted dispersal and reproductive success in an ant species with matchmaking

Workers of the ant Cardiocondyla elegans drop female sexuals into the nest entrance of other colonies to promote outbreeding with unrelated, wingless males. Corroborating the results from previous years, we document that carrier and carried female sexuals are typically related and that the transfer initially occurs mostly from their joint natal colonies to unrelated colonies. Female sexuals mate multiply with up to seven genetically distinguishable males. Contrary to our expectation, the colony growth rate of multiple‐mated and outbred female sexuals was lower than that of inbred or single‐mated females, leading to the question of why female sexuals mate multiply at all. Despite the obvious costs, multiple mating might be a way for female sexuals to “pay rent” for hibernation in an alien nest. We argue that in addition to evade inbreeding depression from regular sibling mating over many generations, assisted dispersal might also be a strategy for minimizing the risk of losing all reproductive investment when nests are flooded in winter.     

Broad-scale reciprocity in an avian seed dispersal mutualism

Aim Coevolved relationships between individual species of birds and plants rarely occur in seed dispersal mutualisms. This study evaluates whether reciprocal relationships may occur between assemblages of bird and plant species. Location Vancouver Island, British Columbia, Canada (48°50′‐N, 125°22′‐W). Methods The distribution and fruiting phenologies of seven shrub species were compared to seasonal changes in habitat selection and seed dispersal by six fruit‐eating bird species. Results Shrub species inhabiting forest understorey habitat had earlier fruiting phenologies than shrub species inhabiting forest edge habitat along lake and bog margins. Birds showed a parallel pattern in habitat selection, being more abundant in the forest understorey early in the fruiting season, and more abundant in the forest edge later in the season. Rates of seed deposition covaried with avian habitat selection, in such a way that birds directed seed dispersal into habitats preferred by shrubs. Conclusions These results depict a broad‐scale pattern in the abundance of birds and fruits indicative of reciprocal interactions. Seasonal changes in seed dispersal to each habitat appear to reinforce the relationship between shrub habitat affinities and fruiting phenologies. Phenological differences between habitats may also reinforce seasonal changes in avian habitat selection. Therefore, although reciprocal interactions between pairs of bird and plant species are rare, broad‐scale reciprocal relationships may occur between assemblages of bird and plant species.     

Adaptive foraging tactics of greater short-nosed fruit bats on a spiny shrub and its effect on seed dispersal

Journal of Ethology - Many plant species have seeds embedded in their fleshy pulp to attract frugivores, which enhances the chance of seed dispersal. However, some tropical plants are evolved with...     

Seasonal changes in pollinator activity influence pollen dispersal and seed production of the alpine shrub Rhododendron aureum (Ericaceae)

In alpine ecosystems, microscale variation in snowmelt timing often causes different flowering phenology of the same plant species and seasonal changes in pollinator activity. We compared the variations in insect visitation, pollen dispersal, mating patterns, and sexual reproduction of Rhododendron aureum early and late in the flowering season using five microsatellites. Insects visiting the flowers were rare early in the flowering season (mid-June), when major pollinators were bumblebee queens and flies. In contrast, frequent visitations by bumblebee workers were observed late in the season (late July). Two-generation analysis of pollen pool structure demonstrated that quality of pollen-mediated gene flow was more diverse late in the season in parallel with the high pollinator activity. The effective number of pollen donors per fruit (N(ep)) increased late in the season (N(ep) = 2.2-2.7 early, 3.4-4.4 late). However, both the outcrossing rate (t(m)) and seed-set ratio per fruit were smaller late in the season (t(m) = 0.89 and 0.71, seed-set ratio = 0.52 and 0.18, early and late in the season, respectively). In addition, biparental inbreeding occurred only late in the season. We conclude that R. aureum shows contrasting patterns of pollen movement and seed production between early and late season: in early season, seed production can be high but genetically less diverse and, during late season, be reduced, possibly due to higher inbreeding and inbreeding depression, but have greater genetic diversity. Thus, more pollinator activity does not always mean more pollen movement.     

Variation in seed dispersal effectiveness: the redundancy of consequences in diversified tropical frugivore assemblages

Plant–frugivore mutualistic assemblages frequently combine multiple, complementary or not (i.e. redundant), distinct effects of animal species. To a large extent, the outcomes of these interactions crucially depend on the delayed consequences of frugivore effectiveness on plant recruitment. We evaluated seed dispersal effectiveness for three plant species in a Brazilian Atlantic forest with a marked habitat heterogeneity defined by bamboo and non‐bamboo patches. Twenty one, 23 and 14 bird species ate fruits of Euterpe edulis, Sloanea guianensis and Virola bicuhyba trees, respectively. For both Euterpe and Virola, visitation rate was the variable contributing for most variance across frugivore species in the quantitative component of effectiveness (QC, which depends on the combined effects of interaction frequency and per‐interaction effect), while the number of fruits manipulated/visit had the greatest contribution in Sloanea. By combining observational data and experimental seed addition for Euterpe we tested for consistent functional patterns among species in the frugivore assemblage, extending beyond the fruit removal stage. Rankings of QC across Euterpe frugivores remained consistent with their relative contributions to fruit removal and, importantly, with their contributions to seedling establishment. Yet, QC of effectiveness across Euterpe frugivores were more homogeneous at the fruit removal and dispersal stages (contribution to seed dispersal) than for the delayed, dissemination and post‐dispersal effects on recruitment. High complementarity of diversified frugivore assemblages may increase through added variance in their delayed effects related to qualitative components of effectiveness. Our results underscore the importance of assessing how dispersal services provided by mutualistic frugivores play complementary, rather than redundant, roles in seed dispersal within heterogeneous landscapes. Such ecological outcomes highlight the value of combining observational and experimental field designs to assess functional diversity patterns of tropical frugivore assemblages and delayed effects of their interactions with plants.     

Long-term consequences of the alteration of the seed dispersal process of Euphorbia characias due to the Argentine ant invasion

The alteration of the seed dispersal process due to the Argentine ant invasion and its consequences on emergence, recruitment, distribution, and survival of seedlings of Euphorbia characias were analyzed. The study was carried out in two zones of Mediterranean cork‐oak secondary forest, one invaded by L. humile and the other non‐invaded. Two cohorts of E. characias seedlings (those emerged in 2001 and those emerged in 2002) were studied in three study plots in each zone. The level of seed loss due to lack of viability, parasitizing, and vertebrate predation did not differ between the two zones. The mean seed sowing depth was lower in the invaded zone (13.5 mm) than in the non‐invaded zone (22.4 mm). This depth difference implies a longer time needed for seedlings to emerge in the non‐invaded zone but not a different emergence percent under laboratory conditions. In the field study plots seedling recruitment did not differ between the two zones, probably due to the trade‐off between the differences in the initial number of seeds released (higher in the non‐invaded zone) and the different emergence proportions (higher in the invaded zone). As for the spatial characteristics of emerged seedlings, no differences in the mean seedling distance to the nearest inflorescence or to the nearest seedling or in the pattern of seedling distribution were found between zones. Seedling survival was assessed once a month until they had reached maturity or until all of them had died. The median seedling survival time was similar between the invaded and the non‐invaded zones. Survival curves also did not differ between zones. The present study suggests a functional equivalence of the Argentine ant after the replacement of the native ant species. Despite the initial differences found, the final reproductive success of E. characias was not altered after the invasion. However, the case of E. characias seems unlikely to be the rule, and the seed dynamics of other species may be altered, i.e. increased or decreased, and thus positively or negatively affected by the invasion.     

New mutualism for old: indirect disruption and direct facilitation of seed dispersal following Argentine ant invasion

The indirect effects of biological invasions on native communities are poorly understood. Disruption of native ant communities following invasion by the Argentine ant (Linepithema humile) is widely reported to lead indirectly to the near complete collapse of seed dispersal services. In coastal scrub in southeastern Australia, we examined seed dispersal and handling of two native and two invasive alien plant species at Argentine ant-invaded or -uninvaded sites. The Argentine ant virtually eliminates the native keystone disperser Rhytidoponera victoriae, but seed dispersal did not collapse following invasion. Indeed, Argentine ants directly accounted for 92% of all ant-seed interactions and sustained overall seed dispersal rates. Nevertheless, dispersal quantity and quality among seed species differed between Argentine ant-invaded and -uninvaded sites. Argentine ants removed significantly fewer native Acacia retinodes seeds, but significantly more small seeds of invasive Polygala myrtifolia than did native ants at uninvaded sites. They also handled significantly more large seeds of A. sophorae, but rarely moved them >5 cm, instead recruiting en masse, consuming elaiosomes piecemeal and burying seeds in situ. In contrast, Argentine ants transported and interred P. myrtifolia seeds in their shallow nests. Experiments with artificial diaspores that varied in diaspore and elaiosome masses, but kept seed morphology and elaiosome quality constant, showed that removal by L. humile depended on the interaction of seed size and percentage elaiosome reward. Small diaspores were frequently taken, independent of high or low elaiosome reward, but large artificial diaspores with high reward instead elicited mass recruitment by Argentine ants and were rarely moved. Thus, Argentine ants appear to favour some diaspore types and reject others based largely on diaspore size and percentage reward. Such variability in response indirectly reduces native seed dispersal and can directly facilitate the spread of an invasive alien shrub.