Are insect frugivores always plant pests? The impact of fruit fly (Diptera: Tephritidae) larvae on host plant fitness

Herbivory is generally regarded as negatively impacting on host plant fitness. Frugivorous insects, which feed directly on plant reproductive tissues, are predicted to be particularly damaging to hosts. We tested this prediction with the fruit fly, Bactrocera tryoni, by recording the impact of larval feeding on two direct (seed number and germination) and two indirect (fruit decay rate and attraction/deterrence of vertebrate frugivores) measures of host plant fitness. Experiments were done in the laboratory, glasshouse and tropical rainforest. We found no negative impact of larval feeding on seed number or germination for three test plants: tomato, capsicum and eggplant. Further, larval feeding accelerated the initiation of decay and increased the final level of fruit decay in tomatoes, apples, pawpaw and pear, a result considered to be beneficial to the fruit. In rainforest studies, native rodents preferred infested apple and pears compared to uninfested control fruit; however, there were no differences observed between treatments for tomato and pawpaw. For our study fruits, these results demonstrate that fruit fly larval infestation has neutral or beneficial impacts on the host plant, an outcome which may be largely influenced by the physical properties of the host. These results may contribute to explaining why fruit flies have not evolved the same level of host specialization generally observed for other herbivore groups.

Selecting replacements for invasive plants to support frugivores in highly modified sites: a case study focusing on Lantana camara

Invasive plants are regarded as a major threat to biodiversity worldwide. Yet, in some cases, invasive plants now perform important ecological functions. For example, fleshy-fruited invasive plants provide food that supports indigenous frugivore populations. How can the disparate goals of conservation versus invasive weed control be managed? We suggest using the fruit characteristics of the invasive plant to select replacement indigenous plants that are functionally similar from the perspective of frugivores. These could provide replacement food resources at sites where plants with these characteristics are part of the goal plant community and where such plants would not otherwise regenerate. Replacement plants could also redirect seed dispersal processes to favour indigenous, rather than invasive, plant species. We investigated the utility of this approach by ranking all indigenous fleshy-fruited plant species from a region using a simple model that scored species based upon measures of fruit phenology, morphology, conspicuousness and accessibility relative to a target invasive species, Lantana (Lantana camara). The model successfully produced high scores for indigenous plant species that were used by more of the frugivores of Lantana than a random selection of plants, suggesting that this approach warrants further investigation.

Mammalian Frugivores With Different Foraging Behavior Can Show Similar Seed Dispersal Effectiveness

Frugivores with disparate foraging behavior are considered to vary in their seed dispersal effectiveness (SDE). Measured SDEs for gibbons and macaques for a primate-fruit' were comparable despite the different foraging and movement behavior of the primates. This could help facilitate fruit trait convergence in diverse fruit-frugivore networks.

The Asian elephant is amongst the top three frugivores of two tree species with easily edible fruit

Large animal species are prone to local extirpation, but ecologists cannot yet predict how the loss of megaherbivores affects ecosystem processes such as seed dispersal. Few studies have compared the quantity and quality of seed dispersal by megaherbivores versus alternative frugivores in the wild, particularly for plant species with fruit easily consumed by many frugivorous species. In a disturbed tropical moist forest in India, we examine whether megaherbivores are a major frugivore of two tree species with easily edible, mammal-dispersed fruit. We quantify the relative fruit removal rates of Artocarpus chaplasha and Careya arborea, by the Asian elephant (Elephas maximus) and alternative dispersers. Through focal watches and camera trapping, we found the elephant to be amongst the top three frugivores for each tree species. Furthermore, seed transects under A. chaplasha show that arboreal frugivores discard seeds only a short distance from the parental tree, underscoring the elephant's role as a long-distance disperser. Our data provide unprecedented support for an old notion: megaherbivores may be key dispersers for a broad set of mammal-dispersed fruiting species, and not just fruit inaccessible to smaller frugivores. As such, the elephant may be particularly important for the functional ecology of the disturbed forests it still inhabits across tropical Asia.

Does attraction to frugivores or defense against pathogens shape fruit pulp composition?

Fruit traits evolve in response to an evolutionary triad between plants, seed dispersers, and antagonists that consume fruits but do not disperse seeds. The defense trade-off hypothesis predicts that the composition of nutrients and of secondary compounds in fruit pulp is shaped by a trade-off between defense against antagonists and attraction to seed dispersers. The removal rate model of this hypothesis predicts a negative relationship between nutrients and secondary compounds, whereas the toxin-titration model predicts a positive relationship. To test these alternative models, we evaluated whether the contents of nutrients and secondary compounds can be used to predict fruit removal by mutualists and pathogens in 14 bird-dispersed plants on a subtropical island in São Paulo state, southeastern Brazil. We selected eight to ten individuals of each species and prevented fruit removal by covering four branches with a net and left fruits on four other branches available to both, vertebrate fruit consumers and pathogens. The persistence of ripe fruits was drastically different among species for bagged and open fruits, and all fruit species persisted longer when protected against seed dispersers. We found that those fruits that are quickly removed by vertebrates are nutrient-rich, but although the attack rate of pathogens is also high, these fruits have low contents of quantitative defenses such as tannins and phenols. Thus, we suggest that the fruit removal rate by seed dispersers is the primary factor selecting the levels of fruit defense. Likewise, nutrient-poor fruits have low removal of seed dispersers and low probability of attack by pathogens. These species retain ripe fruits in an intact condition for a prolonged period because they are highly defended by secondary compounds, which reduce overall attractiveness. However, this strategy might be advantageous for plants that depend on rare or unreliable dispersers.

Differential seed germination of a keystone palm (Euterpe edulis) dispersed by avian frugivores

The effectiveness of seed dispersal by vertebrates has been analysed by examining both quantitative and qualitative components (Jordano & Schupp 2000, Schupp et al. 2010). While the quantitative component is relatively easily assessed in the field (e.g. visitation rate, number of fruits eaten per visit), the qualitative component (e.g. fate of dispersed seeds, seed treatment in the digestive system of the disperser) is rarely studied under natural conditions, because it is difficult to measure the effects on seeds once ingested by the dispersers (Cortes et al. 2009). © Cambridge University Press 2012.

Effects of palm heart harvesting on avian frugivores in the Atlantic rain forest of Brazil

Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP)

Frugivores at higher risk of extinction are the key elements of a mutualistic network

Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP)

Differential seed germination of a keystone palm (Euterpe edulis) dispersed by avian frugivores

FAPESP (BIOTA Program) [2007/03392-6, 2010/04927-3]

Frugivores, seed dispersal and tree regeneration along a human disturbance gradient in East African tropical rainforests

Samenausbreitung und Regeneration von Bäumen sind wichtig für den langfristigen Bestand von Baum- und Frugivorengemeinschaften in tropischen Regenwäldern. Zunehmende Rohdung und Degradation gefährden den Ablauf dieser mutualistischen Prozesse in diesem Ökosystem. Um den Einfluss von kleinräumiger menschlicher Störung auf die Frugivorengemeinschaft und die zentralen Ökosystemprozesse Samenausbreitung und Regeneration zu erforschen, habe ich 1) die Frugivorengemeinschaft und die Samenausbreitungsrate von Celtis durandii (Ulmaceae) und 2) den Zusammenhang zwischen Baumarten mit fleischigen Früchten, Frugivoren und der Etablierung von Keimlingen dieser Baumarten in unterschiedlich stark gestörten Flächen dreier ostafrikanischer tropischer Regenwälder untersucht. Insgesamt konnte ich 40 frugivore Vogel- und Primatenarten in den drei untersuchten Waldgebieten nachweisen. Auf gering gestörten Flächen wurden mehr Frugivore als auf stark gestörten Flächen aufgenommen. Auch die Beobachtungen an C. durandii ergaben mehr frugivore Besucher in Bäumen auf gering gestörten als auf stark gestörten Flächen. Dies führte zu einer marginal signifikant höheren Samenausbreitungsrate auf den gering gestörten Flächen. Diese Ergebnisse waren auf regionaler Ebene in allen drei untersuchten Wäldern konsistent. Dies zeigt, dass kleinräumige Störung einen umfassenderen negativen Einfluss auf Frugivore und ihre Funktion als Samenausbreiter hat als zuvor angenommen. Bei der Vegetationserfassung nahm ich 131 verschiedene Baumarten mit fleischigen Früchten in den drei Regenwäldern auf. Kleinräumige menschliche Störung erhöhte den Artenreichtum dieser Baumarten marginal signifikant, hatte jedoch keinen direkten Einfluss auf die Frugivorendichte und den Artenreichtum von Keimlingen dieser Baumarten. Der Artenreichtum von Baumarten mit fleischigen Früchten zeigte einen marginal signifikant positiven Einfluss auf die Frugivorendichte, allerdings nicht auf die Keimlinge. Allerdings führte die Dichte der Frugivoren zu signifikant erhöhtem Artenreichtum der Keimlinge. Folglich scheint kleinräumige Störung die Keimlingsetablierung indirekt durch erhöhten Baumartenreichtum und erhöhte Frugivorendichte zu beeinflussen. Die Frugivorendichte hatte einen größeren Einfluss auf die Waldregeneration als kleinräumige Störung und Baumartenreichtum. Demnach scheint kleinräumige menschliche Störung sowohl positive als auch negative Effekte auf Samenausbreitung und Regeneration zu haben. Somit sind weitere Studien notwendig, die den Einfluss von kleinräumiger menschlicher Störung auf Mutualismen tropischer Regenwälder aufklären.

Utilisation of seed resources by small mammals : a two-way interaction

Within the Australian wet tropics bioregion, only 900 000 hectares of once continuous rainforest habitat between Townsville and Cooktown now remains. While on the Atherton Tableland, only 4% of the rainforest that once occurred there remains today with remnant vegetation now forming a matrix of rainforest dispersed within agricultural land (sugarcane, banana, orchard crops, townships and pastoral land). Some biologists have suggested that remnants often support both faunal and floral communities that differ significantly from remaining continuous forest. Australian tropical forests possess a relatively high diversity of native small mammal species particularly rodents, which unlike larger mammalian and avian frugivores elsewhere, have been shown to be resilient to the effects of fragmentation, patch isolation and reduction in patch size. While small mammals often become the dominant mammalian frugivores, in terms of their relative abundance, the relationship that exists between habitat diversity and structure, and the impacts of small mammal foraging within fragmented habitat patches in Australia, is still poorly understood. The relationship between foraging behaviour and demography of two small mammal species, Rattus fuscipes and Melomys cervinipes, and food resources in fragmented rainforest sites, were investigated in the current study. Population densities of both species were strongly related with overall density of seed resources in all rainforest fragments. The distribution of both mammal species however, was found to be independent of the distribution of seed resources. Seed utilisation trials indicated that M.cervinipes and R.fuscipes had less impact on seed resources (extent of seed harvesting) than did other rainforest frugivores. Experimental feeding trials demonstrated that in 85% of fruit species tested, rodent feeding increased seed germination by a factor of 3.5 suggesting that in Australian tropical rainforest remnants, small mammals may play a significant role in enhancing germination of large seeded fruits. This study has emphasised the role of small mammals in tropical rainforest systems in north eastern Australia, in particular, the role that they play within isolated forest fragments where larger frugivorous species may be absent.

Echolocation calls and wing morphology of bats from the West Indies

Echolocation calls of 119 bats belonging to 12 species in three families from Antillean islands of Puerto Rico, Dominica, and St. Vincent were recorded by using time-expansion methods. Spectrograms of calls and descriptive statistics of five temporal and frequency variables measured from calls are presented. The echolocation calls of many of these species, particularly those in the family Phyllostomidae, have not been described previously. The wing morphology of each taxon is described and related to the structure of its echolocation calls and its foraging ecology. Of slow aerial-hawking insectivores, the Mormoopidae and Natalidae Mormoops blainvillii, Pteronotus davyi davyi, P. quadridens fuliginosus, and Natalus stramineus stramineus can forage with great manoeuvrability in background-cluttered space (close to vegetation), and are able to hover. Pteronotus parnellii portoricensis is able to fly and echolocate in highly-cluttered space (dense vegetation). Among frugivores, nectarivores and omnivores in the family Phyllostomidae, Brachyphylla cavernarum intermedia is adapted to foraging in the edges of vegetation in background-cluttered space, while Erophylla bombifrons bombifrons, Glossophaga longirostris rostrata, Artibeus jamaicensis jamaicensis, A. jamaicensis schwartzi and Stenoderma rufum darioi are adapted to foraging under canopies in highly-cluttered space and do not have speed or efficiency in commuting flight. In contrast, Monophyllus plethodon luciae, Sturnira lilium angeli and S. lilium paulsoni are adapted to fly in highly-cluttered space, but can also fly fast and efficiently in open areas.

Approaches to selecting native plant replacements for fleshy-fruited invasive species

Invasive plants are a serious threat to biodiversity. Yet, in some cases, they may play an important ecological role in heavily modified landscapes, such as where fleshy-fruited invasive plants support populations of native frugivores. How can such conservation conflicts be managed? We advocate an approach in which native fleshy-fruited plants are ranked on their ability to provide the fruit food resources for native frugivores currently being provided by invasive plants. If these native taxa are preferentially used, where ecologically appropriate, in plantings for restoration and in park and garden settings, they could help support native frugivore populations in the event of extensive invasive plant control. We develop and critically examine six approaches to selecting candidate native plant taxa: a multivariate approach based on the frugivore assemblage, a scoring model, and several multivariate approaches (including trait combinations having the greatest correlation with the diet of the native frugivore assemblage) based on the functional traits of fruit morphology, phenology, conspicuousness, and accessibility. To illustrate these approaches, we use a case study with Bitou bush (Chrysanthemoides monilifera subsp. rotundata) (Asteraceae), an Australian Weed of National Significance. The model using a dissimilarity value generated from all available traits identified a set of species used by the frugivores of C. monilifera more than null models. A replacement approach using species ranked by either all traits available or the frugivore community appears best suited to guide selection of plants in restoration practice.

Cassowary dispersal of the invasive pond apple in a tropical rainforest: the contribution of subordinate dispersal modes in invasion.

Dispersal is a significant determinant of the pattern and process of invasions; however, weed dispersal distances are rarely described and descriptions of dispersal kernels are completely lacking for vertebrate-dispersed weeds. Here, we describe dispersal kernels generated by a native disperser, the endangered southern cassowary (Casuarius casuarius, L.) for an invasive, tropical rainforest plant, pond apple (Annona glabra, L.). Pond apple is primarily water-dispersed and is managed as such. We consider whether cassowary dispersal, as a numerically subordinate dispersal mode, provides an additional dispersal service that may modify the invasion process. In infested areas, pond apple seed was common in cassowary dung. Gut passage had no effect on the probability of single seed germination but deposition in clumps or as whole fruits reduced the probability of germination below that of single seeds. Gut passage times ranged from 65 to 1675 min. Combined with cassowary movement data, this resulted in estimated dispersal distances of 12.5-5212 m, with a median distance of 387 m (quartile range 112-787 m). Native frugivores can be effective dispersers of weeds in rainforest and even terrestrial dispersers can provide long-distance dispersal. Importantly, though pond apple might be expected to be almost entirely dispersed downstream and along the margins of aquatic and marine habitats, cassowaries provide dispersal upstream and between drainages, leading to novel dispersal outcomes. Even through the provision of small quantities of novel dispersal outcomes, subordinate dispersal modes can play a significant role in determining invasion pattern and influence the ultimate success of control programs by providing dispersal to locations unattainable via the primary mode.

Progress towards the eradication of three melastome shrub species from northern Australian rainforests

To eradicate a weed incursion, its extent must be delimited and each infestation extirpated. Measures for delimitation and extirpation are utilized to assess the progress of eradication programs currently targeting three melastome shrub species (Clidemia hirta, Miconia nervosa and M. racemosa) in north-eastern Australia. The main infested area for each species was determined during the year after initial detection, but expanded surveys have led to the discovery of isolated, smaller outlying patches. Programs are refining survey methods (including search frequency) to prevent reproduction. Weed incursions that are limited to single infestations represent a prime opportunity for eradication. However, population and dispersal data indicate that eradication will require an ongoing investment for some time for all three species. Highly persistent seed and dispersal by frugivores suggest that eradication may prove extraordinarily difficult should any of these species spread or be discovered at more locations.