How ecological opportunity relates to diversification is a central question in evolutionary biology. However, there are few empirical examples of how ecological opportunity and morphological innovation open new adaptive zones, and promote diversification. We analyse data on diet, skull morphology and bite performance, and relate these traits to diversification rates throughout the evolutionary history of an ecologically diverse family of mammals (Chiroptera: Phyllostomidae). We found a significant increase in diversification rate driven by increased speciation at the most recent common ancestor of the predominantly frugivorous subfamily Stenodermatinae. The evolution of diet was associated with skull morphology, and morphology was tightly coupled with biting performance, linking phenotype to new niches through performance. Following the increase in speciation rate, the rate of morphological evolution slowed, while the rate of evolution in diet increased. This pattern suggests that morphology stabilized, and niches within the new adaptive zone of frugivory were filled rapidly, after the evolution of a new cranial phenotype that resulted in a certain level of mechanical efficiency. The tree-wide speciation rate increased non linearly with a more frugivorous diet, and was highest at measures of skull morphology associated with morphological extremes, including the most derived Stenodermatines. These results show that a novel stenodermatine skull phenotype played a central role in the evolution of frugivory and increasing speciation within phyllostomids.
Omnivorous animals feed on several food items that often differ in macronutrient and isotopic composition. Macronutrients can be used for either metabolism or body tissue synthesis and, therefore, stable C isotope ratios of exhaled breath (delta(13)C(breath)) and tissue may differ. To study nutrient routing in omnivorous animals, we measured delta(13)C(breath) in 20-g Carollia perspicillata that either ate an isotopically homogeneous carbohydrate diet or an isotopically heterogeneous protein-carbohydrate mixture. The delta(13)C(breath) converged to the delta(13)C of the ingested carbohydrates irrespective of whether proteins had been added or not. On average, delta(13)C(breath) was depleted in (13)C by only ca. -2 per thousand in relation to the delta(13)C of the dietary carbohydrates and was enriched by +8.2 per thousand in relation to the dietary proteins, suggesting that C. perspicillata may have routed most ingested proteins to body synthesis and not to metabolism. We next compared the delta(13)C(breath) with that of wing tissue (delta(13)C(tissue)) in 12 free-ranging, mostly omnivorous phyllostomid bat species. We predicted that species with a more insect biased diet--as indicated by the N isotope ratio in wing membrane tissue (delta(15)N(tissue))--should have higher delta(13)C(tissue) than delta(13)C(breath) values, since we expected body tissue to stem mostly from insect proteins and exhaled CO(2) to stem from the combustion of fruit carbohydrates. Accordingly, delta(13)C(tissue) and delta(13)C(breath) should be more similar in species that feed predominantly on plant products. The species-specific differences between delta(13)C(tissue) and delta(13)C(breath) increased with increasing delta(15)N(tissue), i.e. species with a plant-dominated diet had similar delta(13)C(tissue) and delta(13)C(breath) values, whereas species feeding at a higher trophic level had higher delta(13)C(tissue) than delta(13)C(breath) values. Our study shows that delta(13)C(breath) reflect the isotope ratio of ingested carbohydrates, whereas delta(13)C of body tissue reflect the isotope ratio of ingested proteins, namely insects, supporting the idea of isotopic routing in omnivorous animals.
We compared the assemblages of phyllostomid bats in three Neotropical rainforests with respect to species richness and assemblage structure and suggested a method to validate estimates of species richness for Neotropical bat assemblages based on mist-netting data. The fully inventoried bat assemblage at La Selva Biological Station (LS, 100 m elevation) in Costa Rica was used as a reference site to evaluate seven estimators of species richness. The Jackknife 2 method agreed best with the known bat species richness and thus was used to extrapolate species richness for an Amazonian bat assemblage (Tiputini Biodiversity Station; TBS, 200 m elevation) and an Andean premontane bat assemblage (Podocarpus National Park; BOM, 1000 m elevation) in Ecuador. Our results suggest that more than 100 bat species occur sympatrically at TBS and about 50 bat species coexist at BOM. TBS harbours one of the most species-rich bat assemblages known, including a highly diverse phyllostomid assemblage. Furthermore, we related assemblage structure to large-scale geographical patterns in floral diversity obtained from botanical literature. Assemblage structure of these three phyllostomid assemblages was influenced by differences in floral diversity at the three sites. At the Andean site, where understorey shrubs and epiphytes exhibit the highest diversity, the phyllostomid assemblage is mainly composed of understorey frugivores and nectarivorous species. By contrast, canopy frugivores are most abundant at the Amazonian site, coinciding with the high abundance of canopy fruiting trees. Assemblage patterns of other taxonomic groups also may reflect the geographical distribution patterns of floral elements in the Andean and Amazonian regions.
Summary1. Species richness is a state variable of some interest in monitoring programmes but raw species counts are often biased due to imperfect species detectability. Therefore, monitoring programmes should quantify detectability for target taxa to assess whether it varies over temporal or spatial scales. We assessed the potential for tropical bat monitoring programmes to reliably estimate trends in species richness. 2. Using data from 25 bat assemblages from the Old and New World tropics, we estimated detectability for all species in an assemblage (mean proportion of species detected per sampling plot) and for individual species (species-specific detectability). We further assessed how these estimates of detectability were affected by external sources of variation relating to time, space, survey effort and biological traits. 3. The mean proportion of species detected across 96 sampling plots was estimated at 0AE76 (range 0AE57-1AE00) and was significantly greater for phytophagous than for animalivorous species. Species-*Correspondence author. E-mail: cmeyer@fc.ul.pt 1365-2664.2011.01976.x Ó 2011 The Authors. Journal of Applied Ecology Ó 2011 British Ecological Society averaged detectability for phytophagous species was influenced by the number of surveys and season, whereas the number of surveys and sampling methods [ground-or canopy-level mist nets, harp traps and acoustic sampling (AS)] most strongly affected estimates of detectability for animalivorous bats. Species-specific detectability averaged 0AE4 and was highly heterogeneous across 232 species, with estimates ranging from 0AE03 to 0AE84. Species-level detectability was influenced by a range of external factors such as location, season, or sampling method, suggesting that raw species counts may sometimes be strongly biased. 4. Synthesis and applications. Due to generally high species-specific detection probabilities, Neotropical aerial insectivorous bats proved to be well suited for monitoring using AS. However, for species with low detectability, such as most gleaning animalivores or nectarivores, count data obtained in bat monitoring surveys must be corrected for detection bias. Our results indicate that species-averaged detection probabilities will rarely approach 1 unless many surveys are conducted. Consequently, long-term bat monitoring programmes need to adopt an estimation scheme that corrects for variation in detectability when comparing species richness over time and when making regional comparisons. Similar corrections will be needed for other species-rich tropical taxa. Journal of AppliedEcology 2011, 48, 777-787 doi: 10.1111/j.
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