Flying Foxes as Strong Interactors in South Pacific Island Ecosystems: A Conservation Hypothesis

Abstract: The dependency of highly endemic island floras on few potential pollinators in depauperate island faunas suggests that pollinators and seed dispersers may be crucial in the preservation of biodiversity in isolated oceanic islands. We discuss the hypothesis that flying foxes are "strong interactors" in South Pacific islands where they serve as the principal pollinators and seed dispersers, This suggests that the ongoing decline and ultimate extinction of flying fox species on Pacific islands may lead to a cascade of linked plant extinctions. We propose an empirical test of this hypothesis: comparisons of plant reproductive success in Guam, which has virtually lost its flying fox populations, and Samoa, where significant populations remain.     

Flying foxes cease to function as seed dispersers long before they become rare

Rare species play limited ecological roles, but particular behavioral traits may predispose species to become functionally extinct before becoming rare. Flying foxes (Pteropodid fruit bats) are important dispersers of large seeds, but their effectiveness is hypothesized to depend on high population density that induces aggressive interactions. In a Pacific archipelago, we quantified the proportion of seeds that flying foxes dispersed beyond the fruiting canopy, across a range of sites that differed in flying fox abundance. We found the relationship between ecological function (seed dispersal) and flying fox abundance was nonlinear and consistent with the hypothesis. For most trees in sites below a threshold abundance of flying foxes, flying foxes dispersed < 1% of the seeds they handled. Above the threshold, dispersal away from trees increased to 58% as animal abundance approximately doubled. Hence, flying foxes may cease to be effective seed dispersers long before becoming rare. As many species' populations decline worldwide, identifying those with threshold relationships is an important precursor to preservation of ecologically effective densities.     

Flying Foxes (Chiroptera: Pteropodidae): Threatened Animals of Key Ecological and Economic Importance

Abstract: Flying foxes are animals of extraordinary ecological and economic importance throughout forests of the Old World tropics Nearly 200 species play an essential role as forest pollinators and seed dispersers, yet they are frequently misunderstood intensely persecuted and exceptionally vulnerable to extinction Their role in the propagation of numerous important plants remains virtually uninvestigated. However, our review of already available literature demonstrates that at least 289 plant species rely to vatying degrees on large populations of flying foxes for propagation. These plants, in addition to their many ecological contributing produce some 448 economically valuable products. The fact that flying foxes are increasingly threaten and that few baseline data exist on population trends is cause for concern Many appear to be in severe decline, and several species are already extinct. We present initial observations on flying fox importance and survival threats in hopes of highlighting research and conservation needs.     

Responses of Tuatara (Sphenodon punctatus) to Removal of Introduced Pacific Rats from Islands

Abstract:  Invasive mammalian predators such as rats are now widespread on islands, but hypotheses about their effects have rarely been tested. Circumstantial evidence from New Zealand indicates that, when introduced to islands, Pacific rats ( Rattus exulans ) have negative effects on endemic plants, invertebrates, birds, and reptiles, including the tuatara ( Sphenodon punctatus ). We tested the effects of Pacific rats on tuatara by comparing the demographic structure and body condition of tuatara populations on three islands before and after removal of rats and on a fourth island where rats remained. In the presence of rats, juvenile tuatara constituted on average 0–5% of the sample tuatara populations. When Pacific rats were removed after at least 200 years' occupancy, the proportion of juvenile tuatara increased 3.5- to 17-fold and body condition of adult males and females also improved (sometimes dramatically). We predict that, unless Pacific rats are removed from Taranga Island, the tuatara population will collapse because of low population density and the lack of juvenile recruitment. Our results demonstrate that when invasive species exert subtle effects on recruitment and body condition, the effects on populations of long-lived endemic species may only become apparent long after the invasion.     

Darwin's Fox: A Distinct Endangered Species in a Vanishing Habitat

The temperate rain forest of Chiloé Island, Chile, is inhabited by an endemic fox ( Dusicyon fulvipes ) first described by Charles Darwin and now designated Darwin's fox. Despite morphological differences, Darwin's fox has been considered only an insular subspecies of the mainland chilla fox ( D. griseus ). This follows the assumption that the island population, with an estimated population of less than 500, has been separated from the mainland chilla fox for only about 15,000 years and may have received occasional immigrants from the mainland. Consequently, this island population has not been protected as endangered or bred in captivity. Recently, a population of Darwin's fox was discovered on the Chilean mainland 600 km north of Chiloé Island. This population exists in sympatry with chilla and possibly culpeo ( D. culpaeus ) foxes, which suggests that Darwin's fox may be reproductively isolated. To clarify the phylogenetic position of Darwin's fox, we analyzed 344 bp of mitochondrial DNA control-region sequence of the three species of Chilean foxes. Darwin's foxes from the island and mainland populations compose a monophyletic group distinct from the two other Chilean fox species. This indicates that Darwin's fox was probably an early inhabitant of central Chile, and that its present distribution on the mainland may be a relict of a once much wider distribution. Our results highlight the ability of molecular genetic techniques to uncover historical relationships masked by recent events, such as local extinctions. The "rediscovery" of Darwin's fox as a distinct species implies that greater significance should be given to the protection of this species and its unique habitat and to documenting the extent of its mainland distribution.     

Nonredundancy in the dispersal network of a generalist tropical forest tree

Plant species with generalized dispersal mutualisms are considered to be robust to local frugivore extinctions because of redundancy between dispersal agents. However, real redundancy can only occur if frugivores have similar foraging and ranging patterns and if fruit is a limiting resource. We evaluated the quantitative and qualitative contributions of seed dispersers for an endochorus mast-fruiting species, Prunus javanica (Rosaceae) in Khao Yai National Park, Thailand, to evaluate the potential redundancy of dispersers. Data were collected from tree watches, seed/fruit traps, and seed transects under and away from fruiting trees, feeding and seed deposition by gibbons (Hylobates lar), and evaluations of seed and first-year seedling survival. We identified three clusters of dispersers within the network. Most (>80%) frugivore species observed were small birds and squirrels that were not functional dispersers, dropping most seeds under or very near the tree crown, where seedling survival was ultimately nil. Monkeys (Macaca leonina) were low-quality, short-range dispersers, but they dispersed large numbers of seeds and were responsible for 67% of surviving first-year seedlings. Gibbons and Oriental Pied Hornbills (Anthracoceros albirostris) handled few fruits, but they provided the highest quality service by carrying most seeds away from the canopy to medium and long distances, respectively. Although there was overlap in the deposition patterns of the functional dispersers, they displayed complementary, rather than redundant, roles in seed dispersal. Satiation of all functional dispersers further limited their capacity to "replace" one another. Redundancy must be evaluated at the community level because each type of disperser may shift to different species in the non-masting years of P. javanica. Our results underscore the need for research on broader spatial and temporal scales, which combines studies of dispersal and plant recruitment, to better understand mechanisms that maintain network stability.     

Hunting Increases Dispersal Limitation in the Tree Carapa procera, a Nontimber Forest Product

Abstract:  The sustainability of seed extraction from natural populations has been questioned recently. Increased recruitment failure under intense seed harvesting suggests that seed extraction intensifies source limitation. Nevertheless, areas where more seeds are collected tend to also have more intense hunting of seed-dispersing animals. We studied whether such hunting, by limiting disperser activity, could cause quantitative dispersal limitation, especially for large crops and for crops in years of high seed abundance. In each of four Carapa procera (Meliaceae) populations in French Guiana and Surinam, two with hunting and two without, we compared seed fate for individual trees varying in crop size in years of high and low population-level seed abundance. Carapa seeds are a nontimber forest product and depend on dispersal by scatter-hoarding rodents for survival and seedling establishment. Hunting negatively affected the proportion of seeds dispersed and caused greater numbers of seeds to germinate or be infested by moths below parent trees, where they would likely die. Hunting of seed-dispersing animals disproportionally affected large seed crops, but we found no additional effect of population-level seed abundance on dispersal rates. Consistently lower rates of seed dispersal, especially for large seed crops, may translate to lower levels of seedling recruitment under hunting. Our results therefore suggest that the subsistence hunting that usually accompanies seed collection is at the cost of seed dispersal and may contribute to recruitment failure of these nontimber forest products. Seed extraction from natural populations may affect seedling recruitment less if accompanied by measures adequately incorporating and protecting seed dispersers.     

Seed dispersal by pulp consumers, not "legitimate" seed dispersers, increases Guettarda viburnoides population growth

We examined the effect of seed dispersal by Purplish Jays (Cyanocorax cyanomelas; pulp consumers) and the Chestnut-eared Ara?ari (Pteroglossus castanotis; "legitimate" seed dispersers) on population growth of the small tree Guettarda viburnoides (Rubiaceae) in northeastern Bolivian savannas. Because each bird species differs with respect to feeding and post-feeding behavior, we hypothesized that seed dispersal by each species will contribute differently to the rate of increase of G. viburnoides, but that seed dispersal by either species will increase population growth when compared to a scenario with no seed dispersal. To examine the effects of individual dispersers on the future population size of G. viburnoides, we projected population growth rate using demographic models for G. viburnoides that explicitly incorporate data on quantitative and qualitative aspects of seed dispersal by each frugivore species. Our model suggests that seed dispersal by C. cyanomelas leads to positive population growth of G. viburnoides, whereas seed dispersal by P. castanotis has a detrimental effect on the population growth of this species. To our knowledge, this is the first study to report negative effects of a "legitimate" seed disperser on the population dynamics of the plant it consumes. Our results stress the importance of incorporating frugivore effects into population projection matrices, to allow a comprehensive analysis of the effectiveness of different dispersers for plant population dynamics.     

Habitat fragmentation and effects of herbivore (howler monkey) abundances on bird species richness

Habitat fragmentation can alter herbivore abundances, potentially causing changes in the plant community that can propagate through the food web and eventually influence other important taxonomic groups such as birds. Here we test the relationship between the density of red howler monkeys (Alouatta seniculus) and bird species richness on a large set of recently isolated land-bridge islands in Lago Guri, Venezuela (n = 29 islands). Several of these islands host relict populations of howler monkeys at densities up to more than 30 times greater than those on the mainland. These "hyperabundant" herbivores previously have been shown to have a strong positive influence on aboveground plant productivity. We predicted that this should lead to a positive, indirect effect of howler monkey density on bird species richness. After accounting for passive sampling (the tendency for species richness to be positively associated with island area, regardless of differences in habitat quality) we found a significant positive correlation between howler monkey density and bird species richness. A path analysis incorporating data on tree growth rates from a subset of islands (n = 9) supported the hypothesis that the effect of howler monkeys on the resident bird communities is indirect and is mediated through changes in plant productivity and habitat quality. These results highlight the potential for disparate taxonomic groups to be related through indirect interactions and trophic cascades.     

Nectar secondary compounds affect self-pollen transfer: implications for female and male reproduction

Pollen movement within and among plants affects inbreeding, plant fitness, and the spatial scale of genetic differentiation. Although a number of studies have assessed how plant and floral traits influence pollen movement via changes in pollinator behavior, few have explored how nectar chemical composition affects pollen transfer. As many as 55% of plants produce secondary compounds in their nectar, which is surprising given that nectar is typically thought to attract pollinators. We tested the hypothesis that nectar with secondary compounds may benefit plants by encouraging pollinators to leave plants after visiting only a few flowers, thus reducing self-pollen transfer. We used Gelsemium sempervirens, a plant whose nectar contains the alkaloid gelsemine, which has been shown to be a deterrent to foraging bee pollinators. We found that high nectar alkaloids reduced the total and proportion of self-pollen received by one-half and one-third, respectively. However, nectar alkaloids did not affect female reproduction when we removed the potential for self-pollination (by emasculating all flowers on plants). We then tested the assumption that self-pollen in combination with outcrossed pollen depresses seed set. We found that plants were weakly self-compatible, but self-pollen with outcrossed pollen did not reduce seed set relative to solely outcrossed flowers. Finally, an exponential model of pollen carryover suggests that high nectar alkaloids could benefit plants via increased pollen export (an estimate of male function), but only when pollinators were efficient and abundant and plants had large floral displays. Results suggest that high nectar alkaloids may benefit plants via increased pollen export under a restricted set of ecological conditions, but in general, the costs of high nectar alkaloids in reducing pollination balanced or outweighed the benefits of reducing self-pollen transfer for estimates of female and male reproduction.     

Introduced Birds and the Fate of Hawaiian Rainforests

Abstract:  The Hawaiian Islands have lost nearly all their native seed dispersers, but have gained many frugivorous birds and fleshy-fruited plants through introductions. Introduced birds may not only aid invasions of exotic plants but also may be the sole dispersers of native plants. We assessed seed dispersal at the ecotone between native- and exotic-dominated forests and quantified bird diets, seed rain from defecated seeds, and plant distributions. Introduced birds were the primary dispersers of native seeds into exotic-dominated forests, which may have enabled six native understory plant species to become reestablished. Some native plant species are now as common in exotic forest understory as they are in native forest. Introduced birds also dispersed seeds of two exotic plants into native forest, but dispersal was localized or establishment minimal. Seed rain of bird-dispersed seeds was extensive in both forests, totaling 724 seeds of 9 native species and 2 exotics with over 85% of the seeds coming from native plants. Without suitable native dispersers, most common understory plants in Hawaiian rainforests now depend on introduced birds for dispersal, and these introduced species may actually facilitate perpetuation, and perhaps in some cases restoration, of native forests. We emphasize, however, that restoration of native forests by seed dispersal from introduced birds, as seen in this study, depends on the existence of native forests to provide a source of seeds and protection from the effects of ungulates. Our results further suggest that aggressive control of patches of non-native plants within otherwise native-dominated forests may be an important and effective conservation strategy.     

Hybridization and the Extinction of Rare Plant Species

Much has been written about the role of interspecific competition, disease, herbivory, and the loss of key mutualisms in the extinction of rare plant species. Interspecific hybridization rarely is considered among the biotic interactions that promote extinction. We show how hybridization may contribute to the demise of rare plant species through demographic swamping and genetic assimilation by an abundant congener. We contend that the growth of the hybrid subpopulation is the key to rare species assimilation, and we show how the production of hybrid seed, the fitness of hybrids, and pest pressure affect hybrid proliferation. We also discuss how habitat disturbance, unspecialized pollinators, and weak crossing barriers promote hybridization, and how the negative consequences of hybridization are unlikely to be compensated for by immigration from conspecific populations. We also illustrate stages in the demise of species in island floras. We suggest that hybridization is an increasing threat to rare species because ecological barriers are being disrupted by human activities.     

Effects of Native and Non‐Native Vertebrate Mutualists on Plants

Abstract: Extinctions can leave species without mutualist partners and thus potentially reduce their fitness. In cases where non‐native species function as mutualists, mutualism disruption associated with species’ extinction may be mitigated. To assess the effectiveness of mutualist species with different origins, we conducted a meta‐analysis in which we compared the effectiveness of pollination and seed‐dispersal functions of native and non‐native vertebrates. We used data from 40 studies in which a total of 34 non‐native vertebrate mutualists in 20 geographic locations were examined. For each plant species, opportunistic non‐native vertebrate pollinators were generally less effective mutualists than native pollinators. When native mutualists had been extirpated, however, plant seed set and seedling performance appeared elevated in the presence of non‐native mutualists, although non‐native mutualists had a negative overall effect on seed germination. These results suggest native mutualists may not be easily replaced. In some systems researchers propose taxon substitution or the deliberate introduction of non‐native vertebrate mutualists to reestablish mutualist functions such as pollination and seed dispersal and to rescue native species from extinction. Our results also suggest that in places where all native mutualists are extinct, careful taxon substitution may benefit native plants at some life stages.     

Importance of Assessing Population Genetic Structure before Eradication of Invasive Species: Examples from Insular Norway Rat Populations

Abstract:  Determining the inter-island migration abilities of pest species and delimiting eradication units enable more viable long-term eradication campaigns because recurrent colonization from neighboring islands is avoided. We examined the genetic structure of the invasive Norway rat ( Rattus norvegicus ) to identify gene flow between islands and delimit population units at different geographical scales. We investigated variation in eight microsatellite loci in rat populations from 18 islands, representing five archipelagos off the Brittany coast (France). Although most of the islands are isolated from each other, short genetic distances, weak F_ST values between close islands, and a high level of cross-assignment showed that individuals collected on different islands could represent a single population unit. A Bayesian clustering method also supported the existence of high levels of gene flow between some neighboring islands. Thus, the statement "one island equals one population" can be false when inter-island distances are less than a few hundred meters. Genetic studies enable the definition of island clusters among which migration may occur that should be considered eradication units. To avoid reinvasion and to minimize ecological and economic costs, rats on all islands in an eradication unit should be eradicated simultaneously. We suggest that the genetic monitoring we performed here can be applied for management of any pest.     

An Experiment Testing whether Condition and Survival are Limited by Food Supply in a Reintroduced Hihi Population

Abstract: The Hihi (Stitchbird, Notiomystis cincta ) is an endemic New Zealand honeyeater that after European colonization survived on only one offshore island. Attempts to reintroduce Hihi to other islands have been unsuccessful, with populations slowly declining. The main hypothesis for these declines was an inadequate year-round supply of carbohydrate food (nectar and fruit) due to human impacts on the forest habitat. When Hihi were reintroduced to Mokoia, another island with regenerating forest, we tested whether survival was limited by carbohydrate food in the year after release. We conducted an "on-off" experiment in which ad libitum sugar water was available to birds for 2 out of every 4 weeks. We compared the masses of individual birds at the end of on and off periods to identify times when birds lost condition with no supplementary food and would be likely to starve. We also used mark-recapture analysis of resighting data to test whether mortality rates were higher when supplementary food was unavailable. The only effect of the supplementary food was that Hihi spent less time foraging for nectar and fruit and more time foraging for invertebrates. There was no time of year when birds lost mass when the food was taken away, and survival rates were not significantly lower when supplementary food was absent. The low (38%) annual survival rate could not be accounted for by shortage of carbohydrate food, and population viability analysis suggests that the population is likely to slowly decline. Our experiment shows that declines of reintroduced Hihi populations may be unrelated to food supply and that alternative hypotheses should be developed and tested. Our results also show the importance of using experimental methods, when possible, to test hypotheses about factors thought to be limiting reintroduced populations.     

Imperfect Replacement of Native Species by Non‐Native Species as Pollinators of Endemic Hawaiian Plants

Native plant species that have lost their mutualist partners may require non‐native pollinators or seed dispersers to maintain reproduction. When natives are highly specialized, however, it appears doubtful that introduced generalists will partner effectively with them. We used visitation observations and pollination treatments (experimental manipulations of pollen transfer) to examine relationships between the introduced, generalist Japanese White‐eye (Zosterops japonicus) and 3 endemic Hawaiian plant species (Clermontia parviflora, C. montis‐loa, and C. hawaiiensis). These plants are characterized by curved, tubular flowers, apparently adapted for pollination by curve‐billed Hawaiian honeycreepers. Z. japonicus were responsible for over 80% of visits to flowers of the small‐flowered C. parviflora and the midsize‐flowered C. montis‐loa. Z. japonicus‐visited flowers set significantly more seed than did bagged flowers. Z. japonicus also demonstrated the potential to act as an occasional Clermontia seed disperser, although ground‐based frugivory by non‐native mammals likely dominates seed dispersal. The large‐flowered C. hawaiiensis received no visitation by any birds during observations. Unmanipulated and bagged C. hawaiiensis flowers set similar numbers of seeds. Direct examination of Z. japonicus and Clermontia morphologies suggests a mismatch between Z. japonicus bill morphology and C. hawaiiensis flower morphology. In combination, our results suggest that Z. japonicus has established an effective pollination relationship with C. parviflora and C. montis‐loa and that the large flowers of C. hawaiiensis preclude effective visitation by Z. japonicus. Remplazo Imperfecto de Especies Nativas por Especies No‐Nativas como Polinizadores de Plantas Endémicas de Hawaii     

Isolation and population divergence of a widespread Indo-West Pacific marine gastropod at Easter Island

Oceanic islands represent excellent systems for studying the link between geographic isolation and population divergence. Easter Island is the world’s most isolated island and exhibits a high level of endemicity in the nearshore marine environment. Yet few studies have examined the effect of such extreme isolation on the divergence of populations of widespread species that occur at Easter Island. Conus miliaris, a marine gastropod distributed throughout much of the Indo-West Pacific, occurs at Easter Island where the population is ecologically and morphologically distinct from other populations of the species. To determine whether these phenotypic differences are associated with genetic isolation of the Easter Island population, we investigated the phylogeography of this species by examining mitochondrial COI sequences obtained from 141 individuals from eight localities occurring predominantly in the western, central and southeastern Pacific. Results from our analyses show that C. miliaris at Easter Island differs genetically from other populations. We estimate that C. miliaris colonized Easter Island shortly after the origin of the island ≤0.7 million years ago and that since population founding, gene flow has occurred predominantly from Easter Island to the west and that little migration has occurred into Easter Island.     

Measuring social-ecological dynamics behind the generation of ecosystem services.

The generation of ecosystem services depends on both social and ecological features. Here we focus on management, its ecological consequences, and social drivers. Our approach combined (1) quantitative surveys of local species diversity and abundance of three functional groups of ecosystem service providers (pollinators, seed dispersers, and insectivores) with (2) qualitative studies of local management practices connected to these services and their underlying social mechanisms, i.e., institutions, local ecological knowledge, and a sense of place. It focused on the ecology of three types of green areas (allotment gardens, cemeteries, and city parks) in the city of Stockholm, Sweden. These are superficially similar but differ considerably in their management. Effects of the different practices could be seen in the three functional groups, primarily as a higher abundance of pollinators in the informally managed allotment gardens and as differences in the composition of seed dispersers and insectivores. Thus, informal management, which is normally disregarded by planning authorities, is important for ecosystem services in the urban landscape. Furthermore, we suggest that informal management has an important secondary function: It may be crucial during periods of instability and change as it is argued to promote qualities with potential for adaptation. Allotment gardeners seem to be the most motivated managers, something that is reflected in their deeper knowledge and can be explained by a sense of place and management institutions. We propose that co-management would be one possible way to infuse the same positive qualities into all management and that improved information exchange between managers would be one further step toward ecologically functional urban landscapes.     

The Biogeography of Globally Threatened Seabirds and Island Conservation Opportunities

Seabirds are the most threatened group of marine animals; 29% of species are at some risk of extinction. Significant threats to seabirds occur on islands where they breed, but in many cases, effective island conservation can mitigate these threats. To guide island‐based seabird conservation actions, we identified all islands with extant or extirpated populations of the 98 globally threatened seabird species, as recognized on the International Union for Conservation of Nature Red List, and quantified the presence of threatening invasive species, protected areas, and human populations. We matched these results with island attributes to highlight feasible island conservation opportunities. We identified 1362 threatened breeding seabird populations on 968 islands. On 803 (83%) of these islands, we identified threatening invasive species (20%), incomplete protected area coverage (23%), or both (40%). Most islands with threatened seabirds are amenable to island‐wide conservation action because they are small (57% were <1 km²), uninhabited (74%), and occur in high‐ or middle‐income countries (96%). Collectively these attributes make islands with threatened seabirds a rare opportunity for effective conservation at scale. La Biogeografía de Aves Marinas Amenazadas Globalmente y las Oportunidades de Conservación en Islas