Effects of Habitat and Fruit Scent on the Interactions between Short-tailed Fruit Bats and Piper Plants.

Piper is a mega-diverse genus of pioneer plants that contributes to the maintenance and regeneration of tropical forests. In the Neotropics, Carollia bats use olfaction to forage for Piper fruit and are a main disperser of Piper seeds via consumption and subsequent defecation during flight. In return, Piper fruits provide essential nutrients for Carollia year-round. There is evidence that the types and diversity of Piper frugivores are influenced by the primary habitat type of different Piper species (forest and gap), with forest Piper depending more on bats for seed dispersal; however, this pattern has not been tested broadly. We aimed to characterize and compare the interactions between Carollia and Piper across forested and gap habitats, and further investigate whether differences in fruit traits relevant to bat foraging (i.e., scent) could underlie differences in Carollia-Piper interactions. We collected nightly acoustic ultrasonic recordings and 24 h camera trap data in La Selva, Costa Rica across 12 species of Piper (six forest, six gap) and integrated this information with data on Carollia diet and Piper fruit scent. Merging biomonitoring modalities allowed us to characterize ecological interactions in a hierarchical manner: from general activity and presence of bats, to visitations and inspections of plants, to acquisition and consumption of fruits. We found significant differences in Carollia-Piper interactions between forested and gap habitats; however, the type of biomonitoring modality (camera trap, acoustics, diet) influenced our ability to detect these differences. Forest Piper were exclusively visited by bats, whereas gap Piper had a more diverse suite of frugivores; the annual diet of Carollia, however, is dominated by gap Piper since these plants produce fruit year-round. We found evidence that fruit scent composition significantly differs between forest and gap Piper, which highlights the possibility that bats could be using chemical cues to differentially forage for gap vs. forest Piper. By integrating studies of Piper fruit scent, plant visitation patterns, and Carollia diet composition, we paint a clearer picture of the ecological interactions between Piper and Carollia, and plant-animal mutualisms more generally.

Piper es un género megadiverso de plantas pioneras que contribuyen al mantenimiento y regeneración de los bosques tropicales. En el Neotrópico, los murciélagos de género Carollia utilizan el sentido del olfato para encontrar frutos de Piper y son los principales dispersores de estas plantas a través del consumo de los frutos y posterior defecación de las semillas durante el vuelo. A cambio, los frutos de Piper proporcionan nutrientes esenciales para Carollia durante todo el año. Existe evidencia de que los tipos y la diversidad de frugívoros que consumen Piper están influenciados por el tipo de hábitat primario (bosques y claros) de las diferentes especies, y que los Piper de bosque dependen más de los murciélagos para la dispersión de semillas. Sin embargo, este patrón no ha sido corroborado ampliamente. Nuestro objetivo fue caracterizar y comparar las interacciones entre Carollia y Piper en hábitats boscosos y en claros, e investigar más a fondo si las diferencias en los rasgos de las frutas relevantes para la búsqueda de frutos por los murciélagos (es decir, el olor) podrían explicar las diferencias en las interacciones entre Carollia y Piper. Para ello, compilamos grabaciones acústicas ultrasónicas durante la noche y videos con cámaras trampa por 24 horas/día en La Selva, Costa Rica, para 12 especies de Piper (6 de bosque, 6 de claros) e integramos esa información con datos sobre la dieta de Carollia y el aroma de los frutos de Piper. Esta combinación de modalidades de biomonitoreo nos permitió caracterizar las interacciones ecológicas de manera jerárquica: desde la actividad general y la presencia de murciélagos, sus visitas e inspecciones de las plantas, hasta la adquisición y consumo de frutos. Encontramos diferencias significativas entre hábitats boscosos y claros en las interacciones de Carollia y Piper;sin embargo, el tipo de modalidad de biomonitoreo (cámara trampa, acústica, dieta) influyó en nuestra capacidad de detectar estas diferencias. Los Piper de bosque fueron visitados exclusivamente por murciélagos, mientras que los Piper de claros tuvieron un grupo más diverso de frugívoros. La dieta anual de Carollia, sin embargo, está dominada por Piper de claros, ya que estas plantas producen frutos durante todo el año. Encontramos evidencia de que la composición del aroma de los frutos difiere significativamente entre los Piper de bosque y de claros, lo que resalta la posibilidad que los murciélagos puedan estar usando señales químicas para forrajear diferencialmente por Piper de estas dos categorías. La integración de estudios del aroma de los frutos de Piper, patrones de visita a las plantas y composición de la dieta de Carollia nos permitió generar una imagen más clara sobre las interacciones ecológicas entre Piper y Carollia y de los mutualismos planta-animal en general.

Size And Locomotor Ecology Have Differing Effects on the External and Internal Morphologies of Squirrel (Rodentia: Sciuridae) Limb Bones.

Mammals exhibit a diverse range of limb morphologies that are associated with different locomotor ecologies and structural mechanics. Much remains to be investigated, however, about the combined effects of locomotor modes and scaling on the external shape and structural properties of limb bones. Here, we used squirrels (Sciuridae) as a model clade to examine the effects of locomotor mode and scaling on the external shape and structure of the two major limb bones, the humerus and femur. We quantified humeral and femoral morphologies using 3D geometric morphometrics and bone structure analyses on a sample of 76 squirrel species across their four major ecotypes. We then used phylogenetic generalized linear models to test how locomotor ecology, size, and their interaction influenced morphological traits. We found that size and locomotor mode exhibit different relationships with the external shape and structure of the limb bones, and that these relationships differ between the humerus and femur. External shapes of the humerus and, to a lesser extent, the femur are best explained by locomotor ecology rather than by size, whereas structures of both bones are best explained by interactions between locomotor ecology and scaling. Interestingly, the statistical relationships between limb morphologies and ecotype were lost when accounting for phylogenetic relationships among species under Brownian motion. That assuming Brownian motion confounded these relationships is not surprising considering squirrel ecotypes are phylogenetically clustered; our results suggest that humeral and femoral variation partitioned early between clades and their ecomorphologies were maintained to the present. Overall, our results show how mechanical constraints, locomotor ecology, and evolutionary history may enact different pressures on the shape and structure of limb bones in mammals.

EspañolLos mamíferos exhiben una amplia gama de morfologías de las extremidades, las cuales están asociadas con diferentes ecologías de locomoción y mecánicas estructurales. Sin embargo, aún queda mucho por investigar sobre cómo los tipos de locomoción y el tamaño corporal han afectado conjuntamente la forma externa y las propiedades estructurales de los huesos de las extremidades. En este estudio, usamos al clado de las ardillas (Sciuridae) como un modelo para examinar los efectos del tipo de locomoción y el tamaño en la forma externa y la estructura de los dos huesos principales de las extremidades, el húmero y el fémur. Utilizando morfometría geométrica en 3D y análisis de estructura ósea, cuantificamos la morfología humeral y femoral en una muestra de 76 especies de ardillas que abarcan sus cuatro ecotipos principales. Posteriormente, usamos modelos filogenéticos generalizados lineales para investigar cómo la ecología locomotora, el tamaño, y la interacción entre estos factores influencian los rasgos morfológicos. Encontramos que el tamaño y el tipo de locomoción exhiben diferentes relaciones con la forma externa y la estructura de los huesos de las extremidades, y que estas relaciones difieren entre el húmero y el fémur. La variación de la forma externa del húmero y, en menor medida, del fémur está más relacionada con la ecología locomotora que con el tamaño. Por otro lado, las diferencias en la estructura de ambos huesos se explican mejor por una combinación de efectos de la ecología locomotora y el tamaño. Curiosamente, las relaciones estadísticas entre la morfología de las extremidades y el ecotipo se pierden al incorporar las relaciones filogenéticas entre las especies bajo un modelo de movimiento browniano. El hecho de que asumir un modelo de movimiento browniano modifique estas relaciones no es sorprendente, considerando que los ecotipos de ardillas están agrupados filogenéticamente. Nuestros resultados además sugieren que la variación en morfología humeral y femoral se dividieron tempranamente entre clados y estas ecomorfologías se mantuvieron hasta el presente.En general, nuestros resultados demuestran cómo las restricciones mecánicas, la ecología locomotora y la historia evolutiva pueden ejercer diferentes presiones sobre la forma y la estructura de los huesos de las extremidades en los mamíferos.

Sensory adaptations reshaped intrinsic factors underlying morphological diversification in bats.

BACKGROUND: Morphological evolution may be impacted by both intrinsic (developmental, constructional, physiological) and extrinsic (ecological opportunity and release) factors, but can intrinsic factors be altered by adaptive evolution and, if so, do they constrain or facilitate the subsequent diversification of biological form? Bats underwent deep adaptive divergences in skull shape as they evolved different sensory modes; here we investigate the potential impact of this process on two intrinsic factors that underlie morphological variation across organisms, allometry, and modularity. RESULTS: We use comparative phylogenetic and morphometric approaches to examine patterns of evolutionary allometry and modularity across a 3D geometric morphometric dataset spanning all major bat clades. We show that allometric relationships diverge between echolocators and visually oriented non-echolocators and that the evolution of nasal echolocation reshaped the modularity of the bat cranium. CONCLUSIONS: Shifts in allometry and modularity may have significant consequences on the diversification of anatomical structures, as observed in the bat skull.

A Fruitful Endeavor: Scent Cues and Echolocation Behavior Used by Carollia castanea to Find Fruit.

Frugivores have evolved sensory and behavioral adaptations that allow them to find ripe fruit effectively, but the relative importance of different senses in varying foraging scenarios is still poorly understood. Within Neotropical ecosystems, short-tailed fruit bats (Carollia: Phyllostomidae) are abundant nocturnal frugivores that rely primarily on Piper fruits as a food resource. Previous research has demonstrated that Carollia employs olfaction and echolocation to locate Piper fruit, but it is unknown how their sensory use and foraging decisions are influenced by the complex diversity of chemical cues that fruiting plants produce. Using free-ranging C. castanea and their preferred food, Piper sancti-felicis, we conducted behavioral experiments to test two main hypotheses: (1) foraging decisions in C. castanea are primarily driven by ripe fruit scent and secondarily by vegetation scent, and (2) C. castanea re-weights their sensory inputs to account for available environmental cues, with bats relying more heavily on echolocation in the absence of adequate scent cues. Our results suggest that C. castanea requires olfactory information and relies almost exclusively on ripe fruit scent to make foraging attempts. Piper sancti-felicis ripe fruit scent is chemically distinct from vegetation scent; it is dominated by 2-heptanol, which is absent from vegetation scent, and has a greater abundance of ß-caryophyllene, ß-ocimene, γ-elemene, and α-cubebene. Although variation in echolocation call parameters was independent of scent cue presence, bats emitted longer and more frequent echolocation calls in trials where fruit scent was absent. Altogether, these results highlight the adaptations and plasticity of the sensory system in neotropical fruit bats.

Los frugívoros han evolucionado adaptaciones sensoriales y conductuales que les permiten encontrar frutos maduros de manera efectiva, pero aún existe una falta de conocimiento sobre la importancia relativa de los diferentes sentidos que los frugívoros utilizan en diferentes escenarios de forrajeo. Dentro de los ecosistemas neotropicales, los murciélagos de cola corta (Carollia: Phyllostomidae) son frugívoros nocturnos abundantes que dependen principalmente de los frutos de Piper como recurso alimentario. Previamente se ha demostrado que Carollia emplea el olfato y la ecolocalización para encontrar frutos de Piper, pero se desconoce cómo su uso sensorial y decisiones de forrajeo están influenciados por la compleja diversidad de señales químicas producidas por las plantas. En este trabajo, utilizamos C. castanea y su especie de frutos preferida, Piper sancti-felicis, para llevar a cabo experimentos conductuales y probar dos hipótesis principales: (1) las decisiones de forrajeo de C. castanea son incitadas principalmente por el aroma del fruto maduro y, en segundo lugar, por el aroma de la vegetación, y (2) C. castanea modula el uso de sus sentidos de acuerdo a las señales ambientales disponibles y utiliza la ecolocalización en mayor grado en ausencia de señales olfativas adecuadas. Nuestros resultados sugieren que C. castanea requiere información olfativa y se basa casi exclusivamente en el aroma del fruto maduro para hacer intentos de forrajeo. El aroma del fruto maduro de P. sancti-felicis es químicamente distinto al aroma de su vegetación; está dominado por 2-heptanol, el cual está ausente del aroma de la vegetación, y tiene una mayor abundancia de ß-cariofileno, ß-ocimeno, γ-elemeno, y α-cubibeno. Aunque encontramos que la variación en los parámetros de llamadas de ecolocalización es independiente de la presencia de diferentes señales aromáticas, los murciélagos emitieron llamadas de ecolocalización más largas y frecuentes en los experimentos donde el aroma de fruto estaba ausente. Conjuntamente, estos resultados destacan las adaptaciones y plasticidad del sistema sensorial de los murciélagos frugívoros neotropicales.

Serological evidence of widespread exposure of Grenada fruit bats to chikungunya virus.

Antibody detection against selected potentially zoonotic vector-borne alphaviruses and flaviviruses was conducted on sera from bats from all six parishes in Grenada, West Indies. Sera were tested for (i) antibodies to flaviviruses West Nile virus, St. Louis encephalitis virus, Ilhéus virus, Bussuquara virus (BSQV), Rio Bravo virus and all four serotypes of dengue virus (DENV) by plaque reduction neutralization test (PRNT); (ii) antibodies to alphaviruses western equine encephalitis virus, Venezuelan equine encephalitis virus and eastern equine encephalitis virus by epitope-blocking enzyme-linked immunosorbent assay (ELISA); and (iii) antibodies to the alphavirus chikungunya (CHIKV) by PRNT. Two species of fruit bats were sampled, Artibeus jamaicensis and Artibeus lituratus, all roosting in or within 1,000 m of human settlements. Fifteen (36%) of the 42 bats tested for neutralizing antibodies to CHIKV were positive. The CHIKV-seropositive bats lived in localities spanning five of the six parishes. All 43 bats tested for epitope-blocking ELISA antibody to the other alphaviruses were negative, except one positive for Venezuelan equine encephalitis virus. All 50 bats tested for neutralizing antibody to flaviviruses were negative, except one that had a BSQV PRNT80 titre of 20. The CHIKV serology results indicate that bats living close to and within human settlements were exposed to CHIKV in multiple locations. Importantly, bats for this study were trapped a year after the introduction and peak of the human CHIKV epidemic in Grenada. Thus, our data indicate that bats were exposed to CHIKV possibly during a time of marked decline in human cases.

A Bigger Picture: Organismal Function at the Nexus of Development, Ecology, and Evolution: An Introduction to the Symposium.

Over the past 40 years of research, two perspectives have dominated the study of ecomorphology at ontogenetic and evolutionary timescales. For key anatomical complexes (e.g., feeding apparatus, locomotor systems, sensory structures), morphological changes during ontogeny are often interpreted in functional terms and linked to their putative importance for fitness. Across larger timescales, morphological transformations in these complexes are examined through character stability or mutability during cladogenesis. Because the fittest organisms must pass through ontogenetic changes in size and shape, addressing transformations in morphology at different time scales, from life histories to macroevolution, has the potential to illuminate major factors contributing to phenotypic diversity. To date, most studies have relied on the assumption that organismal form is tightly constrained by the adult niche. Although this could be accurate for organisms that rapidly reach and spend a substantial portion of their life history at the adult phenotype (e.g., birds, mammals), it may not always hold true for species that experience substantial growth after one or more major fitness filters during their ontogeny (e.g., some fishes, reptiles). In such circumstances, examining the adult phenotype as the primary result of selective processes may be erroneous as it likely obscures the developmental configuration of morphology that was most critical to early survival. Given this discrepancy-and its potential to mislead interpretations of how selection may shape a taxon's phenotype-this symposium addresses the question: how do we identify such ontogenetic "inertia," and how do we integrate developmental information into our phylogenetic, ecological, and functional interpretations of complex phenotypes?

Does nasal echolocation influence the modularity of the mammal skull?

In vertebrates, changes in cranial modularity can evolve rapidly in response to selection. However, mammals have apparently maintained their pattern of cranial integration throughout their evolutionary history and across tremendous morphological and ecological diversity. Here, we use phylogenetic, geometric morphometric and comparative analyses to test the hypothesis that the modularity of the mammalian skull has been remodelled in rhinolophid bats due to the novel and critical function of the nasal cavity in echolocation. We predicted that nasal echolocation has resulted in the evolution of a third cranial module, the 'nasal dome', in addition to the braincase and rostrum modules, which are conserved across mammals. We also test for similarities in the evolution of skull shape in relation to habitat across rhinolophids. We find that, despite broad variation in the shape of the nasal dome, the integration of the rhinolophid skull is highly consistent with conserved patterns of modularity found in other mammals. Across their broad geographical distribution, cranial shape in rhinolophids follows two major divisions that could reflect adaptations to dietary and environmental differences in African versus South Asian distributions. Our results highlight the potential of a relatively simple modular template to generate broad morphological and functional variation in mammals.

Predicting bite force in mammals: two-dimensional versus three-dimensional lever models.

Bite force is a measure of whole-organism performance that is often used to investigate the relationships between performance, morphology and fitness. When in vivo measurements of bite force are unavailable, researchers often turn to lever models to predict bite forces. This study demonstrates that bite force predictions based on two-dimensional (2-D) lever models can be improved by including three-dimensional (3-D) geometry and realistic physiological cross-sectional areas derived from dissections. Widely used, the 2-D method does a reasonable job of predicting bite force. However, it does so by over predicting physiological cross-sectional areas for the masseter and pterygoid muscles and under predicting physiological cross-sectional areas for the temporalis muscle. We found that lever models that include the three dimensional structure of the skull and mandible and physiological cross-sectional areas calculated from dissected muscles provide the best predictions of bite force. Models that accurately represent the biting mechanics strengthen our understanding of which variables are functionally relevant and how they are relevant to feeding performance.

Connecting behaviour and performance: the evolution of biting behaviour and bite performance in bats.

Variation in behaviour, performance and ecology are traditionally associated with variation in morphology. A neglected part of this ecomorphological paradigm is the interaction between behaviour and performance, the ability to carry out tasks that impact fitness. Here we investigate the relationship between biting behaviour and performance (bite force) among 20 species of ecologically diverse bats. We studied the patterns of evolution of plasticity in biting behaviour and bite force, and reconstructed ancestral states for behaviour and its plasticity. Both behavioural and performance plasticity exhibited accelerating evolution over time, and periods of rapid evolution coincided with major dietary shifts from insect-feeding to plant-feeding. We found a significant, positive correlation between behavioural plasticity and bite force. Bats modulated their performance by changing their biting behaviour to maximize bite force when feeding on hard foods. The ancestor of phyllostomids was likely a generalist characterized by high behavioural plasticity, a condition that also evolved in specialized frugivores and potentially contributed to their diversification.