Short-tailed Bat Research Articles

Alternative reproductive tactics, sperm mobility and oxidative stress in Carollia perspicillata (Seba’s short-tailed bat)

In social systems with alternative reproductive tactics, sneakers face a higher level of sperm competition than harem males and hence are predicted to allocate more resources to ejaculates. Antioxidants can protect sperm against oxidative stress, and thus, their allocation to the ejaculate may depend on mating tactic. In this study on the frugivorous bat Carollia perspicillata, we assessed, for harem and sneaker males, four sperm mobility traits, blood and ejaculate markers of the redox balance and the ejaculate to blood ratios of the redox markers. Under higher sperm competition, sneaker males should allocate proportionally more antioxidant resources to the protection of sperm than harem males. In contrast, harem males should favour pre-copulatory functions, which comprise the protection of blood. We found significantly higher sperm velocity and sperm survival in sneakers. There was no correlation between sperm mobility and sperm enzymatic antioxidant activity or ejaculate levels of lipid peroxidation (oxidative damage). Ejaculate levels of lipid peroxidation and sperm survival showed a significantly positive correlation, which could be attributed to the role of reactive oxygen species for sperm capacitation. Harem and sneaker males showed similar levels of redox balance markers in ejaculate and blood. However, harem males showed a higher ratio of oxidized over reduced glutathione in blood, which may indicate higher cellular stress due to higher metabolism. Overall, our findings suggest that sneakers of C. perspicillata compensate for a higher level of sperm competition by higher sperm mobility. In social systems with alternative reproductive tactics, sneakers face higher level of sperm competition than harem males and hence are predicted to allocate more resources to ejaculates. Antioxidants can protect sperm against oxidative stress, and thus, their allocation to the ejaculate may depend on mating tactic. In this study on the frugivorous bat Carollia perspicillata, we found sperm swimming significantly faster and longer in sneaker males compared to harem males. However, traits other than the investigated antioxidant may favour higher sperm mobility. Measured redox pattern in blood of harem males may indicate higher cellular stress due to higher metabolism. Our results provide support to the current sperm competition models at the intraspecific level, which is still debated for internal fertilizers. This study contributes to better understanding the trade-offs and adaptations resulting from alternative reproductive tactics in mammals.

Development and characterization of fourteen novel microsatellite markers for the chestnut short-tailed fruit bat (Carollia castanea), and cross-amplification to related species

Rapid anthropogenic land use change threatens the primary habitat of the Chestnut short-tailed bat (Carollia castanea) throughout much of its range. Information on population genetic structure can inform management strategies for this widespread frugivorous bat, and effective protection of C. castanea will also benefit the more than 20 mutualistic plant species of which this bat is the primary seed disperser. To facilitate understanding of population genetic structure in this species, fourteen novel microsatellite markers were developed using restriction-site-associated DNA libraries and Illumina sequencing and tested on 28 individuals from 13 locations in Costa Rica. These are the first microsatellite markers developed for C. castanea. All loci were polymorphic, with number of alleles ranging from 2–11 and average observed heterozygosity of 0.631. Markers were also cross-amplified in three additional frugivorous bat species threatened by habitat loss and fragmentation: Sowell’s short-tailed bat (Carollia sowelli), Seba’s short-tailed bat (Carollia perspicillata), and the Jamaican fruit bat (Artibeus jamaicensis), and 10, 11, and 8 were polymorphic, respectively.

Cold and alone? Roost choice and season affect torpor patterns in lesser short-tailed bats.

Seasonal changes in weather and food availability differentially impact energy budgets of small mammals such as bats. While most thermal physiological research has focused on species that experience extreme seasonal temperature variations, knowledge is lacking from less variable temperate to subtropical climates. We quantified ambient temperature (T a) and skin temperature (T sk) responses by individuals from a population of New Zealand lesser short-tailed bats (Mystacina tuberculata) during summer and winter using temperature telemetry. During summer, communal roosts were more thermally stable than T a. During winter, solitary roosts were warmer than T a indicating significant thermal buffering. Communal roost trees were used on 83% of observation days during summer, and individuals occupying them rarely entered torpor. Solitary roosts were occupied on 93% of observation days during winter, and 100% of individuals occupying them used torpor. During summer and winter, bats employed torpor on 11 and 95% of observation days, respectively. Maximum torpor bout duration was 120.8h and winter torpor bout duration correlated negatively with mean T a. Torpor bout duration did not differ between sexes, although female minimum T sk was significantly lower than males. The summer Heterothermy Index varied, and was also significantly affected by T a. Mean arousal time was correlated with sunset time and arousals occurred most frequently on significantly warmer evenings, which are likely associated with an increased probability of foraging success. We provide the first evidence that torpor is used flexibly throughout the year by M. tuberculata, demonstrating that roost choice and season impact torpor patterns. Our results add to the growing knowledge that even small changes in seasonal climate can have large effects on the energy balance of small mammals.

The electrocardiogram signal of Seba's short-tailed bat, Carollia perspicillata.

A number of studies have successfully used electrocardiogram (ECG) signals to characterize complex physiological phenomena such as associative learning in bats. However, at present, no thorough characterization of the structure of ECG signals is available for these animals. The aim of the present study was to quantitatively characterize features of the ECG signals in the bat species Carollia perspicillata, a species that is commonly used in neuroethology studies. Our results show that the ECG signals of C. perspicillata follow the typical mammalian pattern, in that they are composed by a P wave, QRS complex and a T wave. Peak-to-peak amplitudes in the bats' ECG signals were larger in measuring configurations in which one of the electrodes was attached to the right thumb. In addition, large differences in the instantaneous heart rate (HR) distributions were observed between ketamine/xylazine anesthetized and awake bats. Ketamine/xylazine might target the neural circuits that control HR, therefore, instantaneous HR measurements should only be used as physiological marker in awake animals.

Claustrum of the short-tailed fruit bat, Carollia perspicillata: Alignment of cellular orientation and functional connectivity.

The claustrum is a gray-matter structure that underlies neocortex and reciprocates connections with cortical and subcortical targets. In lower mammals, the claustrum is directly adjacent to neocortex, making the definition of claustral boundaries challenging. Latexin, an endogenous inhibitor of metallocarboxypeptidases, localizes to claustral cells, enabling a clear delineation of claustrum. Given its proportionately large claustrum, we hypothesized that the short-tailed fruit bat, Carollia perspicillata, can be a useful model for claustral structure-function relations. We used latexin immunohistochemistry to identify claustral boundaries and intrinsic structure and multielectrode recordings from brain slices to explore intrinsic excitatory connectivity of the claustrum. Carollia's claustrum contains cells whose intrinsic connectivity and alignment permit the generation of spontaneous, synchronous population events and mirror their pattern of spread in disinhibited brain slices over millimeters. Carollia shows cellular alignment and spontaneous population-activity spread along both horizontal and dorsoventral axes. Carollia claustrum possesses intrinsic excitatory connectivity sufficient to: 1) generate single, spontaneous, synchronized burst discharges, 2) support activity spread along axes where claustral cells are aligned, and 3), because of multiple axes for cell alignment, support activity spread along both rostrocaudal and dorsoventral axes. The smaller event sizes in bat claustrum compared with rat claustrum are consistent with events occurring in population subsets rather than the full claustral cell population. The overall size of claustrum, its pronounced vascularity, and its more complex intrinsic connectivity than rat suggest that the bat is an animal model for claustral structure and function that will permit unique access to claustrum's processing capabilities. J. Comp. Neurol. 525:1459-1474, 2017. © 2016 Wiley Periodicals, Inc.

Modification of sperm quality after sexual abstinence in Seba's short-tailed bat, Carollia perspicillata.

In polygynous mating systems, few males have stable access to sexual mates. With an expected higher copulation rate, harem males may deplete seminal fluids or increase epididymal sperm maturation, generating poor sperm quality. In a first study, we reported a higher sperm quality in sneaker males of Carollia perspicillata To test whether the lower sperm quality observed in harem males was generated by an elevated copulation rate, we temporarily removed males of both social statuses from the colony. We thus assessed status-related changes of sperm quality resulting from sexual abstinence. Moreover, released from territory and female guarding, harem males were expected to show a reduction in somatic costs. On the basis of sperm competition models, we predicted a higher resource investment in the ejaculate with the reduction of pre-copulatory efforts. In line with our predictions, sperm quality of harem males improved significantly in contrast to sneaker males, whose sperm quality did not change. Without an increase in ejaculate lipid peroxidation, our results also provide evidence that the duration of sexual abstinence was not sufficient to generate sperm oxidative damage through senescence. Harem males did not show a reduction in blood lipid peroxidation or in the ratio of oxidized to reduced glutathione. In line with the maintenance of these somatic costs, harem males did not invest more superoxide dismutase to the ejaculate to maintain sperm quality. Our results suggest that a difference in copulation rate rather than an adaptation to sperm competition provides sneaker males with higher sperm quality in C. perspicillata.

Sneaker male athletic sperm outstrips harem male sperm to get egg

![Figure][1] Seba's short-tailed bat. Photo credit: Emmanuel Rey. When Nicolas Fasel, from the University of Bern, Switzerland, talks about bat reproduction, it sounds more like war than a love story. Having established their supremacy over a territory, dominant ‘harem’ males then have

Environmental and spatial characteristics that affect roost use by Seba’s short-tailed bat (Carollia Perspicillata) in a Colombian cave

Bats use roost sites to reduce energy costs, for reproduction, and to protect themselves from harsh weather conditions and predators. The roosts differ in the environmental and spatial features that may be used by bats during roost selection, but the relationship between the types of roosts and the physical and spatial characteristics remain poorly understood. We studied the characteristics of roost sites used by Carollia perspicillata in a cave with an area of approximately 600 m 2 located in a remnant of tropical dry forest in Colombia. A total of 156 roost sites were sampled. Temperature, relative humidity, distance of the roost site from the cave entrance, relative location within the cave, the roost-site height, and the roost-site area were correlated with each other by canonical correlation analysis. A total of seven types of roost were identified, Cavity, Protrusion, Crack-with- Protrusions, Cavity-with-Protrusions, Cavity-with-Crack-and-Protrusions, Stalactite, and Rock-Structure. Protrusions had the highest frequency (64) and was preferred, along with Crack-with-Protrusions (32), over Rocky-Structure (9) and Stalactite (4), and these were not positively related to the measured characteristics. The Cavity-with-Protrusions, Cavity-with-Crack-and-Protrusions, and Cavity types were not used by Carollia perspicillata. The results indicate that the selection of the roost sites is addressed by the tendency of lower values, environmental characteristics, and spatial measures.

First reported observation of phoresy of pseudoscorpions on an endemic New Zealand mammal, the lesser short-tailed bat, Mystacina tuberculata

The pseudoscorpion Apatochernes vastus Beier, 1976 (Chernetidae) is recorded for the first time on the pelage of the endemic New Zealand lesser short-tailed bat, Mystacina tuberculata. Despite previous descriptions of numerous species of pseudoscorpions throughout New Zealand, the distribution, abundance and life history strategies of pseudoscorpions is poorly known.

Adoption of alternative habitats by a threatened, “obligate” forest-dwelling bat in a fragmented landscape

While they are among the most ecologically important animals within forest ecosystems, little is known about how bats respond to habitat loss and fragmentation. The threatened lesser short-tailed bat (Mystacina tuberculata), considered to be an obligate deep-forest species, is one of only 2 extant land mammals endemic to New Zealand; it plays a number of important roles within native forests, including pollination and seed dispersal, and rarely occurs in modified forests. We used radiotelemetry to study the movements, roosting behavior, and habitat use of M. tuberculata within a fragmented landscape comprised of 3 main habitat types: open space (harvested forest and pastoral land), native forests, and exotic pine plantations. We found that the bats had smaller home-range areas and travelled shorter nightly distances than populations investigated previously from contiguous native forest. Furthermore, M. tuberculata occupied all 3 habitat types, with native forest being preferred overall. However, individual variation in habitat selection was high, with some bats preferring exotic plantation and open space over native forest. Roosting patterns were similar to those previously observed in contiguous forest; individual bats often switched between communal and solitary roosts. Our findings indicate that M. tuberculata exhibit some degree of behavioral plasticity that allows them to adapt to different landscape mosaics and exploit alternative habitats. To our knowledge, this is the first such documentation of plasticity in habitat use for a bat species believed to be an obligate forest-dweller.

The Use of Commercial Fruits as Attraction Agents May Increase the Seed Dispersal by Bats to Degraded Areas in Southern Mexico

Fruit-eating bats play a fundamental role in animal seed dispersal and should be considered key actors in tropical forest restoration. We explored the use of commercial fruits as attractants for bats to increase seed dispersal to areas affected by forest fires in southern Mexico. We captured bats and collected seeds from feces and seed rain at perturbed sample sites where mature bananas and mangos were placed, and from non-treated control sites. Bat and bat-dispersed plant species richness and abundance were analyzed, and the importance of each bat species as a disperser was evaluated. Additionally, germination boxes were set up to evaluate the germination of seeds found in bat feces. We captured 724 individuals of 16 frugivorous bat species, 15 spp in treated and 12 spp in control sites. Sowell's Short-tailed bat, Toltec Fruit-eating bat and the Western Long-tongued bat showed higher abundances in treated sites, suggesting that these three species were attracted by fruits. The most important disperser was the Sowell's Short-tailed bat, followed by the Jamaican Fruit-eating and Toltec Fruit-eating bat. A greater proportion of pioneer species and trees, followed by shrubs, were found in the overall bat diet. The germination percentage was > 50%, suggesting that the use of fruits to attract bats can be a feasible wildlife management activity to encourage the succession process. We recommend further studies to test and improve this activity.

Discovery of novel virus sequences in an isolated and threatened bat species, the New Zealand lesser short-tailed bat (Mystacina tuberculata)

Bats harbour a diverse array of viruses, including significant human pathogens. Extensive metagenomic studies of material from bats, in particular guano, have revealed a large number of novel or divergent viral taxa that were previously unknown. New Zealand has only two extant indigenous terrestrial mammals, which are both bats, Mystacina tuberculata (the lesser short-tailed bat) and Chalinolobus tuberculatus (the long-tailed bat). Until the human introduction of exotic mammals, these species had been isolated from all other terrestrial mammals for over 1 million years (potentially over 16 million years for M. tuberculata). Four bat guano samples were collected from M. tuberculata roosts on the isolated offshore island of Whenua hou (Codfish Island) in New Zealand. Metagenomic analysis revealed that this species still hosts a plethora of divergent viruses. Whilst the majority of viruses detected were likely to be of dietary origin, some putative vertebrate virus sequences were identified. Papillomavirus, polyomavirus, calicivirus and hepevirus were found in the metagenomic data and subsequently confirmed using independent PCR assays and sequencing. The new hepevirus and calicivirus sequences may represent new genera within these viral families. Our findings may provide an insight into the origins of viral families, given their detection in an isolated host species.

English

Frugivorous animals may use morphological traits of food items such as size, hardness, shape, color and smell as cues that allow them to assess cost-benefit relationship of foraging activity. Fruit size is an important trait that influences feeding behavior of most frugivores, since there is a functional correlation between fruit size and frugivores’ body size. Therefore, size-based preference is fundamental to understand plant-frugivore interactions and seed dispersal. In this sense, we tested the hypothesis of preferential consumption of larger fruits of Piper arboreum by the short-tailed fruit bat Carollia perspicillata in the Brazilian tropical dry forest. Results showed considerable variation in fruit size among and within plants. There was also significant difference in fruit ripening time among plants, which was not related to fruit size. Average size of remaining fruits reduced as they were removed from plants by the bats, which indicates preferential consumption of larger fruits. On the other hand, plant phenology constrained consumption of bigger fruits. Only a small fraction of plant crop was available for consumption each night, regardless of fruit size, which probably coerced bats to feed on smaller fruits as the availability of larger ones decreased. Results suggest that bat preference on fruit size is mediated by plant phenological strategies.

Nontarget mortality of New Zealand lesser short-tailed bats (Mystacina tuberculata) caused by diphacinone.

Primary and secondary poisoning of nontarget wildlife with second-generation anticoagulant rodenticides has led to restrictions on their use and to increased use of first-generation anticoagulants, including diphacinone. Although first-generation anticoagulants are less potent and less persistent than second-generation compounds, their use is not without risks to nontarget species. We report the first known mortalities of threatened New Zealand lesser short-tailed bats (Mystacina tuberculata) caused by diphacinone intoxication. The mortalities occurred during a rodent control operation in Pureora Forest Park, New Zealand, during the 2008-09 Austral summer. We observed 115 lesser short-tailed bat deaths between 9 January and 6 February 2009, and it is likely that many deaths were undetected. At necropsy, adult bats showed gross and histologic hemorrhages consistent with coagulopathy, and diphacinone residues were confirmed in 10 of 12 liver samples tested. The cause of mortality of pups was diagnosed as a combination of the effects of diphacinone toxicity, exposure, and starvation. Diphacinone was also detected in two of 11 milk samples extracted from the stomachs of dead pups. Eight adults and 20 pups were moribund when found. Two adults and five pups survived to admission to a veterinary hospital. Three pups responded to treatment and were released at the roost site on 17 March 2009. The route of diphacinone ingestion by adult bats is uncertain. Direct consumption of toxic bait or consumption of poisoned arthropod prey could have occurred. We suggest that the omnivorous diet and terrestrial feeding habits of lesser short-tailed bats make them susceptible to poisoning with the bait matrix and the method of bait delivery used. We recommend the use of alternative vertebrate pesticides, bait matrices, and delivery methods in bat habitat.

Females as mobile resources: communal roosts promote the adoption of lek breeding in a temperate bat

Free to read on publisher website Males of lek-breeding species defend clustered territories from which they display to visiting females. However, the mechanisms leading to the adoption of clustered male display sites are often unknown. In this study, we examined the possibility of a resource-based lek in New Zealand’s lesser short-tailed bat (Mystacina tuberculata) (Mammalia: Chiroptera), by assessing the placement of “singing roosts” used by males in relation to communal roosting sites used by females. The “resource-based lek” model posits that males settle near resources required by females to increase female encounter rates. For most bat species, where females are highly mobile and widely dispersed across landscapes while foraging, communal daytime roosts dominated by females may represent such a resource. Through use of video footage, spatial analyses of singing-roost locations, and passive-integrated transponder tags we confirmed that M. tuberculata employs a lek mating system. We found that male singing roosts were significantly clustered in space, were defended by resident individuals, and were visited by females (who did not receive resources from males) for mating purposes. Transponder records also indicated that some singing roosts were shared between multiple males. Spatial logistic regression indicated that singing-roost locations were associated with communal roosting sites. Communal roosts are selected based on criteria independent of the locations of singing roosts, suggesting that males responded to the location of communal roosts and not the reverse. Mystacina tuberculata thus provides evidence of a resource-based lek, and is only the second bat species worldwide confirmed to use a lek-mating system.

Large Home Range Size in the Ground Foraging Bat,Mystacina tuberculata, in Cold Temperate Rainforest, New Zealand

Large home range sizes are not unusual for small forest-dwelling bats living in cold temperate climates. However, lesser short-tailed bats (Mystacina tuberculata) feed on the ground for a proportion of their time, so their home range requirements may not conform to predictions based on other bat species. The home range size requirements of a population of M. tuberculata were investigated in cold temperate rainforest in the Eglinton Valley, Fiordland, New Zealand. Home range data was collected from a total of 21 out of 23 radio-tagged bats during late summer to early autumn of 1997 and 1998. Individual bats were followed for an average of 7.8 ± 3.2 (SD) days and collectively ranged over a total area of 14,710 ha. Thirteen colonial roosts were located within a central roosting area occupying 17 ha. A further 10 solitary roosts were located within individual foraging areas. Individual 100% minimum convex polygons varied considerably in size from 127.3 to 6,223.4 ha (median = 478.5 ha) with a range length of 2.2–23.0 km (median = 5.0 km). Cluster analyses revealed individual home ranges contained multi-nuclear patches of activity. Despite their large home ranges, bats concentrated activity (85%) in small core areas of 0.6–270.3 ha (median = 26.5 ha), with 85% of core areas less than 62 ha in size. Moderate levels of home range overlap amongst individuals (median = 26.8%) decreased to low levels for individual core areas (median = 3.7%). Our results show that M. tuberculata have relatively large home ranges, similar to many other small temperate rainforest bats, and implies that conservation areas designed for M. tuberculata should be large. Our predictions should be tested on populations of this species in areas with more abundant resources and milder climates.

When bats are boxing: aggressive behaviour and communication in male Seba's short-tailed fruit bat

Aggressive behaviours have an important impact on the social organization of animals and on the social status of individuals, especially in gregarious species. Agonistic interactions between territory holders are essential to set and reinforce territorial borders. Additionally, agonistic displays are used to demonstrate ownership of a territorial site and may indicate social status of the signaller. Between neighbouring territory owners, dynamic borders require frequent interactions. In daily repeated aggressive encounters, ritualization can help to avoid the need for serious fights and their costly consequences. In the bat Carollia perspicillata, a gregarious frugivore with resource defence polygyny, males defend territories at valuable roosting sites for females. Working with a captive bat colony of about 400 individuals, housed under seminatural conditions in a tropical zoo, we found that males defended territories aggressively by the use of a succession of displays forming a ritualized structure. Simultaneously, males used three different vocalization types during aggressive displays, namely down-sweeps, warbles and aggressive trills. A statistical analysis of 58 aggressive trills from five adult males showed that they contained sufficient variation to encode an individual signature. Using a habituation–dishabituation paradigm playback experiment, we found that males could discriminate between vocalizing males based on aggressive calls alone. Such discrimination is probably useful for distinguishing between neighbouring territory owners and more unfamiliar intruders, and thus allows for an economical response.

The aerodynamic cost of flight in the short-tailed fruit bat (Carollia perspicillata): comparing theory with measurement

Aerodynamic theory has long been used to predict the power required for animal flight, but widely used models contain many simplifications. It has been difficult to ascertain how closely biological reality matches model predictions, largely because of the technical challenges of accurately measuring the power expended when an animal flies. We designed a study to measure flight speed-dependent aerodynamic power directly from the kinetic energy contained in the wake of bats flying in a wind tunnel. We compared these measurements with two theoretical predictions that have been used for several decades in diverse fields of vertebrate biology and to metabolic measurements from a previous study using the same individuals. A high-accuracy displaced laser sheet stereo particle image velocimetry experimental design measured the wake velocities in the Trefftz plane behind four bats flying over a range of speeds (3-7 m s(-1)). We computed the aerodynamic power contained in the wake using a novel interpolation method and compared these results with the power predicted by Pennycuick's and Rayner's models. The measured aerodynamic power falls between the two theoretical predictions, demonstrating that the models effectively predict the appropriate range of flight power, but the models do not accurately predict minimum power or maximum range speeds. Mechanical efficiency--the ratio of aerodynamic power output to metabolic power input--varied from 5.9% to 9.8% for the same individuals, changing with flight speed.

Erratum to: Opportunistic predation by Crested Owl Lophostrix cristata upon Seba’s Short-tailed Bat Carollia perspicillata

As shown in figure 1a and b, the owl identified as a Crested Owl Lophostrix cristata (Daudin, 1800) in Rocha & López-Baucells (2014) is indeed a Mottled Owl Strix virgata (Cassin, 1849). Therefore, all results and conclusions in the paper pertaining to L. cristata refer in fact to S. virgata. Both the authors and the Editor in Chief of Revista Brasileira de Ornitologia thank readers for noticing this inconsistency and apologize for this misidentification error.

Murciélagos de cola corta (Carollia: Phyllostomidae) del Parque Nacional Natural Gorgona (Colombia) y sus implicaciones biogeográficas

La identidad de la especie de Carollia (Chiroptera: Phyllostomidae) en el Parque Nacional Natural Gorgona ha sido controvertida debido a la alta similitud entre C. perspicillata y C. brevicauda. C. perspicillata es la especie con mayor probabilidad de habitar en la isla debido a que actualmente se distribuye en las tierras bajas de la costa pacifica colombiana, mientras C. brevicauda es una especie predominantemente de tierras altas. Con el objetivo de resolver la controversia acerca de la especie del genero Carollia que habita la isla, se realizaron analisis morfometricos con base en caracteristica de craneos y mandibulas de especimenes de las dos especies y del PNN Gorgona. Los resultados evidenciaron que, contrario a lo esperado, esta poblacion insular es morfologicamente mas similar a C. brevicauda. Evidencia biologica para diferentes grupos de organismos sugiere que Gorgona puede haber estado conectada a los andes y las zonas bajas del pacifico del sur de Colombia-norte de Ecuador en el pasado. Por otra parte, existe evidencia geologica que muestra que Gorgona es la parte mas alta de una cordillera (Cordillera de la Costa) que se encuentra sumergida actualmente, pero que probablemente fue parte del continente durante el Pleistoceno. Por lo tanto, con base en esta evidencia biologica y geologica se plantea la hipotesis de una ruta de colonizacion de C. brevicauda a Gorgona desde los Andes a traves de la Cordillera de la Costa. Este proceso pudo facilitarse por el descenso marino durante las glaciaciones del Pleistoceno.