Pollinators of Syntopic Marcgravia Species in Costa Rican Lowland Rain Forest: Bats and Opossums

Abstract: The visitors of four syntopically occurring species of Marcgravia (M. nervosa, M. serrae, M. mexicana , and M. nepen-thoides ) in the Atlantic lowland rain forest at La Selva Biological Station in Costa Rica were observed. The four species differed in flowering phenology and morphology of inflorescences. Flowers of all species opened during the night and the stamens dropped before dawn. All species were visited by small nectar-feeding bats (Phyllostomidae: Glossophaginae). Marcgrovia nepen-thoides , with much larger nectaries, additionally attracted two species of opossums, Caluromys derbianus and Didelphis marsu-pious . Judging from the large distance between nectaries and flowers, glossophagine bats probably are inefficient pollinators of this species, and merely exploit a non-flying mammal pollination system.     

Flower and Fruit Availability along a Forest Restoration Gradient

Frugivores and pollinators are two functional groups of animals that help ensure gene flow of plants among sites in landscapes under restoration and to accelerate restoration processes. Resource availability is postulated to be a key factor to structure animal communities using restoration sites, but it remains poorly studied. We expected that diverse forests with many plant growth forms that have less‐seasonal phenological patterns will provide more resources for animals than forests with fewer plant growth forms and strongly seasonal phenological patterns. We studied forests where original plantings included high tree species diversity. We studied resource provision (richness and abundance of flowers and fruits) of all plant growth forms, in three restoration sites of different ages compared to a reference forest, investigating whether plant phenology changes with restoration process. We recorded phenological data for reproductive plant individuals (351 species) with monthly sampling over 2 years, and found that flower and fruit production have been recovered after one decade of restoration, indicating resource provision for fauna. Our data suggest that a wide range of plant growth forms provides resource complementarities to those of planted tree species. Different flower phenologies between trees and non‐trees seem to be more evident in a forest with high non‐tree species diversity. We recommend examples of ideal species for planting, both at the time of initial planting and post‐planting during enrichment. These management actions can minimize shortage and periods of resource scarcity for frugivorous and nectarivorous fauna, increasing probability of restoring ecological processes and sustainability in restoration sites.     

Low plant density enhances gene dispersal in the Amazonian understory herb Heliconia acuminata

In theory, conservation genetics predicts that forest fragmentation will reduce gene dispersal, but in practice, genetic and ecological processes are also dependent on other population characteristics. We used Bayesian genetic analyses to characterize parentage and propagule dispersal in Heliconia acuminata L. C. Richard (Heliconiaceae), a common Amazonian understory plant that is pollinated and dispersed by birds. We studied these processes in two continuous forest sites and three 1‐ha fragments in Brazil's Biological Dynamics of Forest Fragments Project. These sites showed variation in the density of H. acuminata. Ten microsatellite markers were used to genotype flowering adults and seedling recruits and to quantify realized pollen and seed dispersal distances, immigration of propagules from outside populations, and reproductive dominance among parents. We tested whether gene dispersal is more dependent on fragmentation or density of reproductive plants. Low plant densities were associated with elevated immigration rates and greater propagule dispersal distances. Reproductive dominance among inside‐plot parents was higher for low‐density than for high‐density populations. Elevated local flower and fruit availability is probably leading to spatially more proximal bird foraging and propagule dispersal in areas with high density of reproductive plants. Nevertheless, genetic diversity, inbreeding coefficients and fine‐scale spatial genetic structure were similar across populations, despite differences in gene dispersal. This result may indicate that the opposing processes of longer dispersal events in low‐density populations vs. higher diversity of contributing parents in high‐density populations balance the resulting genetic outcomes and prevent genetic erosion in small populations and fragments.     

Flower and Fruit Characteristics in Small and Isolated Populations of a Fleshy-Fruited Shrub

Abstract: During a warm period after the last glaciation the fleshy-fruited shrub, Prunus mahaleb, extended its area of distribution from the Mediterranean basin towards central Europe. Under a subsequent cooler climate, and probably increased competition from trees, the species became restricted to steep, south-facing cliffs and scree slopes with a particularly sunny and warm microclimate. Thus, the small relict populations in central Europe have been isolated for about 5000 - 6000 years. To investigate whether or not reproductive traits of P. mahaleb are affected by isolation and population size, several flower and fruit characteristics were sampled in ten populations in Switzerland. A Canonical Correlation Analysis (CCA) based on these reproductive characteristics differentiated the populations. The first CCA axis was determined by flower size, pollination frequency, pulp and seed mass. This ran parallel to increasing precipitation and decreasing altitude. The second axis correlated with the number of fruits per raceme and seed viability, and ran parallel to increasing sunshine. None of the six flower and fruit variables correlated with population size or with the degree of isolation. However, flower size, pollination frequency, pulp and seed mass showed a negative correlation with altitude. The results suggest that, in populations of P. mahaleb in central Europe, climatic conditions explain more of the observed variation in flower and fruit characteristics than population size or degree of isolation.     

Tamarins and Dung Beetles: An Efficient Diplochorous Dispersal System in the Peruvian Amazonia

Dung beetles fulfill several key functions in ecosystems but their role as secondary seed dispersers is probably one of the most complex ones. Various factors, such as seed characteristics, dispersal pattern induced by the primary disperser, season, and habitat, can affect the seed–beetle interaction. Particularly little is known about the fate of seeds primarily dispersed in small feces. The aim of this study was to investigate the effects of these factors on the dung beetle community (species composition, number and size of individuals) and its consequences on burial occurrence and depth of seeds primarily dispersed by two tamarin species. We captured dung beetles in a Peruvian rain forest with 299 dung‐baited pitfall traps to characterize the dung beetle community. Seed burial occurrence and depth were assessed by marking in situ 551 dispersed seeds in feces placed in cages. Among these seeds, 22.5 percent were buried by dung beetles after 2 d. We observed a significant effect of the amount of dung, season, time of deposition, and habitat on the number of individuals and species of dung beetles, as well as on seed burial occurrence and depth, while the tamarin species significantly influenced only the number and the size of dung beetles. This seed dispersal loop is particularly important for forest regeneration: small to large seeds dispersed by tamarins in secondary forest can be buried by dung beetles. These seeds can thus benefit from a better protection against predation and a more suitable microenvironment for germination, potentially enhancing seedling recruitment.     

The ecology of seed dispersal in two species of callitrichid primates (Saguinus mystax and Saguinus fuscicollis)

Data collected during a 12-month field investigation of mixed species troops of Saguinus mystax and Saguinus fuscicollis in the Amazon Basin of north-eastern Peru indicate that callitrichid primates play an important role in tropical forest seed dispersal. Moustached and saddle-back tamarins were observed to ingest seeds from a variety of tree and liana species and pass them unharmed. These seeds tended to be large and heavy, and passed through the tamarin digestive tract in one to three hours. Experimental plantings of defecated seeds yielded a germination success rate of 70%. The specific gravity of these seeds (weight/volume) was inversely correlated with passage time and apparently had an indirect influence on the distance that seeds were dispersed from the parent tree. In the case of three preferred fruiting species, Leonia glycycarpa, Pourouma sp., and Hippocrateaceae #283, the present distribution of adult trees closely resembled the pattern of the seed shadow created by Saguinus. Moustached and saddle-back tamarins appeared to be reliable and high-quality dispersal agents for a number of tree and liana species. In this role, they are likely to exert an important influence on the composition, distribution, and regeneration patterns of Amazonian rain forest.     

Flower Visitation by Bats in Cloud Forests of Western Ecuador1

The importance of bat pollination has been demonstrated for many plant species. Yet this mutualism has rarely been studied on a community–wide level. In this paper we present results of a yearlong study of a bat–flower community in cloud forests on the western slopes of the Ecuadoran Andes. Of eight plant–visiting bat species caught, only Anoura caudifera and A. geoffroyi were carrying pollen. These species of Anoura supplement their diets with insects. Unlike glossophagines in other environments, however, which switch completely to a frugivorous or insectivorous diet during certain seasons, they are nectarivorous year–round and were never found with seeds or fruit pulp in their feces. Of the 13 morphotypes of pollen carried by the bats, 11 were identified to genus and 7 to species. Floral characteristics of all of these plants fit the traditional chiropterophilous syndrome well. Our study represents the first direct evidence of bat pollination for those plants identified to species, including four species of Burmeistera (Campanulaceae), as well as the first record of bat pollination for a plant of the genus Meriania (Melastomataceae). While overlap in the diets of the two Anoura was high, significant differences in visitation frequencies to particular plant species were detected. The larger bat species (A. geoffroyi) preferred large flowers, whereas the smaller species (A. caudifera) preferred small flowers.     

Contemporary pollen and seed dispersal in a Prunus mahaleb population: patterns in distance and direction

Pollination and seed dispersal determine the spatial pattern of gene flow in plant populations and, for those species relying on pollinators and frugivores as dispersal vectors, animal activity plays a key role in determining this spatial pattern. For these plant species, reported dispersal patterns are dominated by short-distance movements with a significant amount of immigration. However, the contribution of seed and pollen to the overall contemporary gene immigration is still poorly documented for most plant populations. In this study we investigated pollination and seed dispersal at two spatial scales in a local population of Prunus mahaleb (L.), a species pollinated by insects and dispersed by frugivorous vertebrates. First, we dissected the relative contribution of pollen and seed dispersal to gene immigration from other parts of the metapopulation. We found high levels of gene immigration (18.50%), due to frequent long distance seed dispersal events. Second, we assessed the distance and directionality for pollen and seed dispersal events within the local population. Pollen and seed movement patterns were non-random, with skewed distance distributions: pollen tended moved up to 548 m along an axis approaching the N-S direction, and seeds were dispersed up to 990 m, frequently along the SW and SE axes. Animal-mediated dispersal contributed significantly towards gene immigration into the local population and had a markedly nonrandom pattern within the local population. Our data suggest that animals can impose distinct spatial signatures in contemporary gene flow, with the potential to induce significant genetic structure at a local level.     

Types of pollination and seed dispersal in Mediterranean plants

Abstract

Selected examples of pollen and seed dispersal in Mediterranean plants are described. The aspects of pollination considered are: comparison between cleistogamous and chasmogamous forms in the same species; differences in attractants and rewards; duration of pollen viability according to pollination syndrome. The aspects of seed dispersal considered are: presence or absence of specialized structures for dispersal; examples of active, passive and induced dispersal; animals involved in seed dispersal and their reward; type and functions of elaiosomes.     

The impact of cropping on wild populations of Saguinus mystax and Saguinus fuscicollis in Peru

A transect census technique was used to estimate the population densities of Saguinus mystax and Saguinus fuscicollis at two sites in Peru. Cropping of these two species had occurred five years before the census at one site and two years before at the other. The populations of S. mystax at both sites had recovered completely from cropping, and the relationship between S. mystax and S. fuscicollis had not been altered at one site and had been reversed in favor of S. mystax at the other.     

Effects of support size and orientation on symmetric gaits in free-ranging tamarins of Amazonian Peru: implications for the functional significance of primate gait sequence patterns

The adoption of a specific gait sequence pattern during symmetrical locomotion has been proposed to have been a key advantage for the exploitation of the fine branch niche in early primates. Diverse aspects of primate locomotion have been extensively studied in technically equipped laboratory settings, but evolutionary conclusions derived from these investigations have rarely been verified in wild primates. Bridging the gap from the lab to the field, we conducted an actual performance determination of symmetrical gaits in two free-ranging tamarin species (Saguinus mystax and Saguinus fuscicollis) of Amazonian Peru by analyzing high-speed video recordings of naturally occurring locomotor bouts. Tamarins arguably represent viable models for aspects of early primate locomotion. We tested three specific hypotheses derived from laboratory studies to test for the influence of support size and orientation and to gain further insight into the functional significance of primate gait sequence patterns: (1) The tamarins utilize symmetrical gaits at a higher rate on small supports than on larger ones. (2) During symmetrical locomotion on small supports, diagonal sequences are utilized at a higher rate than on larger supports. (3) On inclines, diagonal sequences are predominantly used and on declines, lateral sequences are predominantly used. Our results corroborated hypotheses 1 and 3. We found no clear support for hypothesis 2. In conclusion, our results add to the notion that primate gait plasticity, rather than uniform adoption of diagonal sequence gaits, enabled early primates to accommodate different support types and effectively exploit the small branch niche.     

Isolation and characterization of 13 microsatellite loci for Neochamaelea pulverulenta (Cneoraceae)

We report 13 polymorphic nuclear microsatellite loci for Neochamaelea pulverulenta (Cneoraceae) using an enriched-library approach. Although this plant species is tetraploid, expected patterns for tetrasomic segregation were completely absent, and all loci analysed showed a diploid pattern of inheritance. We detected a total of 102 alleles in 57 individuals genotyped (mean number of alleles per locus was 7.85). The values of observed and expected heterozygosities ranged from 0.193 to 0.737 and 0.425 to 0.812 respectively. Disomic segregation, levels of polymorphism and the exclusionary power of the developed markers render them readily applicable for parentage assignment of dispersed seeds, and for analyses of spatial genetic structure and population connectivity.     

Characterization of animal communities involved in seed dispersal and predation of Guibourtia tessmannii (Harms) J.Léonard,a species newly listed on Appendix II of CITES

Characterization of the ecology of endangered timber species is a crucial step in any forest management strategy. In this study, we described the animal communities involved in seed dispersal and predation of a high‐value timber species Guibourtia tessmannii (Fabaceae; Detarioideae), which is newly listed on Appendix II of CITES. We compared the animal communities between two forest sites (Bambidie in Gabon and Ma'an in Cameroon). A total of 101 hr of direct observations and 355 days of camera trapping revealed that a primate (Cercopithecus nictitans nictitans) and a hornbill (Ceratogymna atrata) were important seed dispersers in Gabon. Conversely, a greater presence of a rodent (Cricetomys emini), which could act both as predator and disperser, was observed in Cameroon. This study suggests that animal communities involved in seed dispersal of G. tessmannii may vary depending on environmental conditions and anthropogenic impacts. However, further studies are needed to properly identify the factors involved in seed dispersal and predation of G. tessmannii.     

The Pacific Banyan in the Cook Islands: have its pollination and seed dispersal mutualisms been disrupted, and does it matter?

Fig trees (Ficus spp., Moraceae) are pollinated by species-specific fig wasps and have seeds that are mainly dispersed by fruit bats and birds. Consequently, they should be strongly dependent on mutualisms with animals for their reproductive success. As elsewhere in the Pacific, extinctions of potential seed dispersers have occurred on the islands in the southern Cook Islands archipelago. The abundance of the Pacific Banyan, Ficus prolixa, was found to be unrelated to the extent of potential seed disperser extinctions on different islands. There was no evidence of recruitment on Rarotonga, which has the most diverse bird and bat assemblage, and healthy populations on Mangaia, where all the native avian frugivores are extinct. Despite its very small population sizes on some of the islands, the trees pollinators are still present, showing that this mutualism has not yet been disrupted. Habitat loss, rather than a loss of mutualists, appears to be the main problem facing this species.     

Global patterns of the double mutualism phenomenon

A double mutualism (DM) occurs when two interacting species benefit each other in two different functions, e.g. when an animal species acts both as pollinator and seed disperser of the same plant. Besides the double benefit, a DM also imposes a larger risk to both functions if the performance of one partner declines. We conducted the first global review of DMs involving pollinators and seed dispersers, aiming to: 1) assess their prevalence across ecosystems and biogeographical regions; 2) identify the main plant and animal taxa, and their traits, implicated in DMs; and 3) evaluate the conservation status of double mutualist species. We compiled published and unpublished DM records using specific search terms, noting the species involved, their conservation status and geographic location, as well as the type of study (species vs community‐level) in which the DM was detected. We identified 302 DM cases involving 207 plant and 92 animal species from 16 mainland and 17 island areas. Most records come from tropical regions and islands. Animals included birds (62%), mammals (22%), and reptiles (16%), mostly opportunist species; only 18% were nectarivores. Plants were mainly fleshy‐fruited shrub or tree species (59%) with actinomorphic flowers that were visited by several or many pollinator species (87%). Most (56%) DMs were detected in community‐level studies. DMs are mostly prevalent in ecosystems with limited food resources and mutualist partners, and with high generalization levels. Nearly 30% of the species involved in DMs are threatened according to IUCN criteria, 68% of which are found on islands. The high prevalence of DM on islands paired with the threat status of island species suggest that the loss of a double mutualists and its cascading consequences may have a severe impact on community composition and functioning of fragile island ecosystems.     

Genetic architecture of multiple mutualisms and mating system in Turnera ulmifolia

Plants often associate with multiple arthropod mutualists. These partners provide important services to their hosts, but multiple interactions can constrain a plant's ability to respond to complex, multivariate selection. Here, we quantified patterns of genetic variance and covariance among rewards for pollination, biotic defence and seed dispersal mutualisms in multiple populations of Turnera ulmifolia to better understand how the genetic architecture of multiple mutualisms might influence their evolution. We phenotyped plants cultivated from 17 Jamaican populations for several mutualism and mating system-related traits. We then fit genetic variance–covariance (G) matrices for the island metapopulation and the five largest individual populations. At the metapopulation level, we observed significant positive genetic correlations among stigma–anther separation, floral nectar production and extrafloral nectar production. These correlations have the potential to significantly constrain or facilitate the evolution of multiple mutualisms in T. ulmifolia and suggest that pollination, seed dispersal and defence mutualisms do not evolve independently. In particular, we found that positive genetic correlations between floral and extrafloral nectar production may help explain their stable coexistence in the face of physiological trade-offs and negative interactions between pollinators and ant bodyguards. Locally, we found only small differences in G among our T. ulmifolia populations, suggesting that geographic variation in G may not shape the evolution of multiple mutualisms.     

Proximate Limitations to Fruit and Seed Set in Phellodendron amurense var. sachalinense

Abstract Fruit and seed set in a dioecious tree, Phellodendron amurense var. sachalinense grown in isolation, were studied for three years in Hokkaido, northern Japan. Hand pollination did not affect fruit set during the three years, but did affect seed-set by increasing the proportion of fruits with higher seed numbers. Artificial defoliation resulted in decreased mean seed mass, but caused no significant differences in mean seed number per fruit. Total seed mass per infructescence increased with inflorescence size except with artificial defoliation where it reached an upper limit. Although the results of the artificial defoliation treatment indicate that resources are most important for fruit and seed set, it is concluded that fruit and seed set of the tree are not limited by resources, since the number of fruits increased with inflorescence size and an artificial defoliation treatment did not decrease seed-number.