Plants often recruit frugivorous animals to transport their seeds; however, gut passage can have varying effects on plant fitness depending on the physical and chemical treatment of the seed, the distance seeds are transported, and the specific site of deposition. One way in which plants can mediate the effects of gut passage on fitness is by producing fruit secondary compounds that influence gut-retention time (GRT). Using frugivorous bats (Carollia perspicillata: Phyllostomidae) and Neotropical plants in the genus Piper, we compared GRT of seeds among five plant species (Piper colonense, Piper peltatum, Piper reticulatum, Piper sancti-felicis, and Piper silvivagum) and investigated the role of fruit amides (piperine, piplartine and whole fruit amide extracts from P. reticulatum) in mediating GRT. Our results showed interspecific differences in GRT; P. reticulatum seeds passed most slowly, while P. silvivagum and P. colonense seeds passed most rapidly. Piplartine and P. reticulatum amide extracts decreased GRT, while piperine had no effect. In addition, we examined the effects of GRT on seed germination success and speed in laboratory conditions. For germination success, the effects were species specific; germination success increased with GRT for P. peltatum but not for other species. GRT did not influence germination speed in any of the species examined. Plant secondary compounds have primarily been studied in the context of their defensive role against herbivores and pathogens, but may also play a key role in mediating seed dispersal interactions.
The seed dispersal cycle forms the basis of vegetation establishment and population dynamics. Evidence shows varied results for the role of frugivorous bats, where ingestion and gut passage enhance seed germination for some plant species, but not for others. Using meta‐analysis techniques with a novel data base spanning 31 years of study, we answered the following questions: (1) does seed passage through bat digestive tracts result in higher probability of seed germination than seed pulp removal by humans? (2) Are there effects of seed origin, germination conditions, bat species, and plant species on the probability of seed germination? (3) Is there an effect of fruit bat dietary preferences on the probability of ingested seed germination? And (4) does seed ingestion by bats result in shorter germination time than seed pulp removal by humans? In general, seed passage through bat digestive tracts neither significantly increased the probability of germination nor reduced seed germination time. However, seed germination varied mainly with plant species and bat species, and fewer than 25% of plant species responded to bat gut passage in a positive or negative way. Plant species that were preferred by a species of bat were more likely to germinate after ingestion than non‐preferred plant species, in line with the core plant taxa hypothesis. These results suggest that: (1) the principal role of frugivorous bats in seed dispersal is to transport seeds away from parent plants, (2) handling of fruit by bats does not enhance or hinder seed germination, and (3) germination of the seeds of fruits consumed by bats is idiosyncratic to the bat and plant species in question.
Background: Was there a mid-Cenozoic vertebrate extinction and recovery event in Madagascar and, if so, what are its implications for the evolution of lemurs? The near lack of an early and mid-Cenozoic fossil record on Madagascar has inhibited direct testing of any such hypotheses. We compare the terrestrial vertebrate fauna of Madagascar in the Holocene to that of early Cenozoic continental Africa to shed light on the probability of a major mid-Cenozoic lemur extinction event, followed by an "adaptive radiation" or recovery. We also use multiple analytic approaches to test competing models of lemur diversification and the null hypothesis that no unusual mid-Cenozoic extinction of lemurs occurred. Results: Comparisons of the terrestrial vertebrate faunas of the early Cenozoic on continental Africa and Holocene on Madagascar support the inference that Madagascar suffered a major mid-Cenozoic extinction event. Evolutionary modeling offers some corroboration, although the level of support varies by phylogeny and model used. Using the lemur phylogeny and divergence dates generated by Kistler and colleagues, RPANDA and TESS offer moderate support for the occurrence of unusual extinction at or near the Eocene-Oligocene (E-O) boundary (34 Ma). TreePar, operating under the condition of obligate mass extinction, found peak diversification at 31 Ma, and low probability of survival of prior lineages. Extinction at the E-O boundary received greater support than other candidate extinctions or the null hypothesis of no major extinction. Using the lemur phylogeny and divergence dates generated by Herrera & Dàvalos, evidence for large-scale extinction diminishes and its most likely timing shifts to before 40 Ma, which fails to conform to global expectations. Conclusions: While support for large-scale mid-Cenozoic lemur extinction on Madagascar based on phylogenetic modeling is inconclusive, the African fossil record does provide indirect support. Furthermore, a major extinction and recovery of lemuriforms during the Eocene-Oligocene transition (EOT) would coincide with other major vertebrate extinctions in North America, Europe, and Africa. It would suggest that Madagascar's lemurs were impacted by the climate shift from "greenhouse" to "ice-house" conditions that occurred at that time. This could, in turn, help to explain some of the peculiar characteristics of the lemuriform clade.
metabolites obstruct seed dispersal by altering bat behavior and physiology at multiple temporal scales. Ecology 101(2):Abstract. The paradoxical presence of toxic chemical compounds in ripe fruits represents a balance between plant enemies and allies: chemical traits can defend seeds against antagonistic herbivores, seed predators, or fungal pathogens, but also can impose costs by repelling mutualistic seed dispersers, although the costs are often difficult to quantify. Seeds gain fitness benefits from traveling far from the parent plant, as they can escape from parental competition and elude specialized herbivores as well as pathogens that accumulate on adult plants. However, seeds are difficult to follow from their parent plant to their final destination. Thus, little is known about the factors that determine seed dispersal distance. We investigated this potential cost of fruit secondary compounds, reduced seed dispersal distance, by combining two data sets from previous work on a Neotropical bat-plant dispersal system (bats in the genus Carollia and plants in the genus Piper). We used data from captive behavioral experiments, which show how amides in ripe fruits of Piper decrease the retention time of seeds and alter food choices.With new analyses, we show that these defensive secondary compounds also delay the time of fruit removal. Next, with a behaviorally annotated bat telemetry data set, we quantified postfeeding movements (i.e., seed dispersal distances). Using generalized additive mixed models we found that seed dispersal distances varied nonlinearly with gut retention times as well as with the time of fruit removal. By interrogating the model predictions, we identified two novel mechanisms by which fruit secondary compounds can impose costs in terms of decreased seed dispersal distances: (1) small-scale reductions in gut retention time and (2) causing fruits to forgo advantageous bat activity peaks that confer high seed dispersal distances.
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