Diet and Coexistence of Two Species of Mormoopid Bats in a Heavily Altered Neotropical Area

Bats are recognized as potential hosts of pathogens exploiting the food chain to reach them as definitive hosts. However, very little is known about their endoparasites, especially for Neotropical bats. In this study, we assessed the helminth fauna associated with 3 insectivorous bat species roosting in the same single hot cave in central Veracruz, México: Mormoops megalophylla, Pteronotus davyi, and Pteronotus personatus. During a period of 1 yr (April 2007-2008), 135 mormoopid bats in total were collected and examined for helminths. Six parasite species representing 3 types of intestinal helminths were found: 1 cestode Vampirolepis elongatus; 2 trematodes Maxbraunium tubiporum and Ochoterenatrema labda; and 3 nematodes Linustrongylus pteronoti, Molineidae gen. sp., and Capillaria sp. Overall, trematodes were the most abundant parasite group (72.4%), followed by nematodes (20.7%) and cestodes (6.9%). Species-accumulation curves suggest that the worms collected (n = 1,331) from these 6 parasite species comprise the helminth fauna associated with the 3 bat populations studied. The only species shared by the 3 bat species was Capillaria sp. Most (5/6) of the helminth species recorded use Lepidoptera and Diptera as intermediate hosts; therefore, diet is likely the main source of infection. Although insectivorous bats are considered dietary generalist species, the differences found in helminth diversity in these sympatric populations of closely related bat species, suggest that diet partitioning occurs in mormoopid bat communities. Helminths tend to exploit the food chain to reach their final hosts; therefore, studying these parasites can provide useful information to further understand the biology of bats.

Echolocating bats use respiratory muscles to power the production of biosonar vocalisations. The physical characteristics of these calls vary among species of bat, and variations also exist in the timing and patterns of respiratory muscle recruitment during echolocation. We recorded electromyograms from the respiratory muscles of three species of bat (Family Vespertilionidae) while the animals vocalised from stationary positions. Activity was recorded consistently from the lateral abdominal muscles (internal abdominal oblique and transversus abdominis) from all calling bats, but we found much variation within and among species. Bats in the family Vespertilionidae devoted longer periods of expiratory muscle activity to each call than did the mormoopid bat Pteronotus parnellii. These differences correlate negatively with the duration of calls. We suggest that morphological adaptations in some bats may facilitate the economic production of echolocation calls at rest.

The bat family Mormoopidae includes three species with distributions in the Caribbean. These taxa—Mormoops blainvillei, Pteronotus parnellii, and P. quadridens—roost predominantly in hot cave chambers where temperatures may reach 40° C and humidity is close to 100%. We tested the hypothesis that mormoopid bat extirpations in this region were due to climatic changes and the loss of suitable cave environments due to flooding caused by sea level rise associated with the late Pleistocene to Holocene (ca. 10 ka) climate change transition. Ecological niche models (ENMs) were developed to estimate the current, mid-Holocene, and Last Glacial Maximum distributions of these three bat species and to assess whether suitable climatic habitat for these taxa had been stable across time in the Caribbean. Additionally, we examined the importance of karst formations (where hot caves typically form) as a predictor for the distributions of Caribbean mormoopid bats. Our results show that mormoopid bat distributions i...

The structure of the forelimb of all currently recognized species of bats of the family Mormoopidae and 18 species of leaf-nosed bats (Phyllostomati-dae) were studied. Characteristic of mormoopids are specializations furthering reduction of weight of the wing; these adaptations are associated with maneuverable, rapid flight, and the ability to remain continuously on the wing for long periods. Certain modifications of muscles, muscle attachments, and articular surfaces parallel specializations of corresponding structures in vespertilionids and molossids. in contrast, the wings of phyllostomatids are less well adapted for efficient flight, and retain muscular patterns that allow the generalized wing to be used for food handling and clambering in vegetation as well as for flight. Perhaps mormoopid bats were established in the Neotropics and exploited some of the most important feeding niches open to insectivorous bats before vespertilionids reached this region. Intense competition with mormoopids may have limited the success of vespertilionids in this area.

Dietary differentiation can be a key mechanism for the coexistence of syntopic species with similar niches. On the Caribbean island of Puerto Rico, three species of bat from the family Mormoopidae — the Antillean ghost-faced bat (Mormoops blainvillei), sooty mustached bat (Pteronotus quadridens), and Parnell's mustached bat (Pteronotus parnellii portoricensis) — are aerial insectivores that roost in the same caves. To investigate the possibility of dietary differentiation, we estimated the percent volume and percent frequency of occurrence of the orders of arthropods consumed by these three species of bat, using standard fecal analysis. We also compared dietary diversity among species, as well as the amount of dietary overlap, with respect to season and habitat. Lastly, this study used canonical correspondence analysis (CCA), a method of ordination, to assess the effects of species, sex, age, reproductive condition, season, and habitat on intraspecific differences in the diet of the Puerto Rican Mormoopidae. Eight orders of arthropods were found in the diet of these mormoopids, with Lepidoptera, Hymenoptera, and Coleoptera being major staples. The CCA revealed differences in diet among the three species, suggesting that dietary differentiation is at least one mechanism for coexistence. In addition, the variables habitat and season correlated significantly with the diet of M. blainvillei and P. quadridens, whereas habitat and sex correlated with the diet of P. p. portoricensis. Thus, our study shows dietary differences among the three species of Mormoopidae living in the same caves on Puerto Rico, as well as intraspecific differences within the diet of each species.

Pteronotus psilotis, a mormoopid bat, is an insectivorous, gregarious and strict cave-dwelling species that is found areas between the sea level and an elevation of about 1000 masl. This species is present in diverse habitats ranging from rain forest to dry deciduous forest. Nine microsatellite loci were developed for Wagner's mustached bat, Pteronotus psilotis using the next-generation sequencing approach, and their utility for population genetics studies was assessed. All loci were polymorphic (7-15 alleles) and characterized in 30 individuals from three P. psilotis populations, with the levels of observed and expected heterozygosity ranging from 0.280 to 0.867 and 0.584 to 0.842, respectively. One locus showed significant departures from Hardy-Weinberg expectations after Bonferroni correction. Cross-amplification in 11 other bat species was tested, for which eight microsatellites were successfully amplified, and of these seven were polymorphic. The development of these new microsatellite loci will contribute to investigations of genetic population structure, genetic diversity and gene flow in P. psilotis populations, as well as in other closely related bat species.

A new genus and species of fossil bat, Koopmanycteris palaeomormoops, representing an ancient member of the endemic Neotropical family Mormoopidae, is described from the Oligocene of Florida. This new species is known from two paleokarst deposits in northern peninsular Florida, the early Oligocene (Whitneyan, 30–32 Ma) I-75 Local Fauna in Alachua County and the late Oligocene (early Arikareean, 26–28 Ma) Brooksville 2 Local Fauna in Hernando County. The discovery of Koopmanycteris extends the fossil record of the Mormoopidae back in time almost 30 million years. Compared to most other described taxa of North American Tertiary bats, the fossil sample of Koopmanycteris palaeomormoops is substantial, consisting of 50 specimens including: P4, all lower teeth from p3 through m3, dentary, petrosal, humerus, proximal radius, and femur. Koopmanycteris is morphologically intermediate between the two living genera of mormoopids, Mormoops and Pteronotus, but is most similar to the former taxon. Characters shared by Koopmanycteris and Mormoops include: large anterolabial basin on P4; large, double-rooted p3; secondary process ventral to angular process on dentary; absence of groove separating capitulum into medial and lateral portions on distal humerus; presence of prominent ridge on posterolateral edge of distal humeral shaft; rounded extremity on proximal radius; and presence of a prominent ridge or tubercle on posterodistal shaft of femur. All of these features appear to be relatively derived, with the exception of the large, double-rooted p3. In several mandibular characters, Koopmanycteris more closely resembles Pteronotus, including: pronounced posteroventral process on the symphysis; lack of curvature of ventral edge of horizontal ramus between posterior edge of symphysis and p4; and less pronounced dorsal upturning of ascending ramus compared to Mormoops. Koopmanycteris retains the primitive dental morphology of Mormoops, with a large double-rooted p3, and the primitive posterior mandibular morphology of Pteronotus, with the lesser degree of dorsal flexion of the ascending ramus. A phylogenetic analysis including all known extant mormoopid lineages as well as representative outgroups from other noctilionoid clades confirms that Koopmanycteris and Mormoops are sister taxa. These findings indicate that the lineages leading to Pteronotus and Mormoops were distinct by ∼30 Ma. The fossil record tentatively indicates that the Mormoopidae originated in North America in the early Oligocene or earlier, and may not have reached South America until the Pliocene following the onset of the Great American Biotic Interchange. Several lines of evidence support this hypothesis: (1) the earliest fossil record of the Mormoopidae is in the early Oligocene of Florida; (2) the greatest diversity and endemism of modern mormoopid species is in the West Indies; and (3) the absence of a pre–late Pleistocene record, lack of endemism, and marginal recent distribution of mormoopids in South America. Most species of living mormoopids are obligate cave dwellers, suggesting that the occurrence of caves and paleokarst deposits has affected both their modern distribution and fossil record.

We performed the first quantitative survey of ectoparasitic assemblages on three species of mormoopid bats living on the Caribbean island of Puerto Rico: Mormoops blainvillii Leach (n=40), Pteronotus quadridens Gundlach (n=40), and Pteronotus parnellii Gray (n=9). We examined bats for parasites primarily on 8-10 May and 24-27 July 2002 at Culebrones Cave, near Arecibo, Puerto Rico. Only 50% of M. blainvillii were infested with at least one parasite, compared with 85-100% for Pteronotus; infested individuals of both species of Pteronotus also harbored a greater number of parasites than did M. blainvillii. The assemblage on M. blainvillii was less diverse than in the other species and more dominated by a single group of parasites, the chiggers. Chirodiscid ear mites and spinturnicid wing mites were common on both species of Pteronotus but absent from M. blainvillii. All P. parnellii harbored streblid flies, but none typically was found on P. quadridens or M. blainvillii. Adult female M. blainvillii and P. quadridens sheltered a greater number of ectoparasites than did males. All host-parasite combinations represented new associations for Puerto Rico.

Relationships between renal morphology and diet in 26 species of new world bats (suborder microchiroptera)

Competing hypotheses explaining species' use of resources have been advanced. Resource limitations in habitat and/or food are factors that affect assemblages of species. These limitations could drive the evolution of morphological and/or behavioural specialization, permitting the coexistence of closely related species through resource partitioning and niche differentiation. Alternatively, when resources are unlimited, fluctuations in resources availability will cause concomitant shifts in resource use regardless of species identity. Here, we used next-generation sequencing to test these hypotheses and characterize the diversity, overlap and seasonal variation in the diet of three species of insectivorous bats of the genus Pteronotus. We identified 465 prey (MOTUs) in the guano of 192 individuals. Lepidoptera and Diptera represented the most consumed insect orders. Diet of bats exhibited a moderate level of overlap, with the highest value between Pteronotus parnellii and Pteronotus personatus in the wet season. We found higher dietary overlap between species during the same seasons than within any single species across seasons. This suggests that diets of the three species are driven more by prey availability than by any particular predator-specific characteristic. P.davyi and P.personatus increased their dietary breadth during the dry season, whereas P.parnellii diet was broader and had the highest effective number of prey species in all seasons. This supports the existence of dietary flexibility in generalist bats and dietary niche overlapping among groups of closely related species in highly seasonal ecosystems. Moreover, the abundance and availability of insect prey may drive the diet of insectivores.

Bats are highly mobile animals, moving rapidly over long distances. Detecting such movements is challenging, especially in cave areas, a commonly-used roost by bats. Brazil has a large number of caves and bat species, but details on bat mobility among caves is still poorly documented there. Such monitoring provides insights on the structuring and conservation of cave-dwelling communities, with possible legal implications for the environmental licensing in Brazil. Based on marking (2,490 bats captured; 2,142 marked) and recapture (35 events; 14 extra-site), here we present data on the mobility of mormoopid bats between two bat caves 15 km apart in northeastern Brazil. Sexual segregation between caves may explain mobility: one cave is likely a maternity roost; the other is a satellite cave used for copulae. Nomadic behavior due to seasonal distribution of resources in the semi-arid Northeastern Brazil cannot be ruled out. Based on the distance between the two caves, bats could potentially forage over an area of ~170,000 hectares, in a wider use of the landscape. Our data have implications for the conservation of bat species and their roosts, and contribute to a more evidence-based discussion of key concepts governing the environmental licensing of mining activities in Brazil.

Several bat species use caves as roosts and some of these caves can harbor high concentrations of individuals. Such caves may represent opportunities for certain predators, benefiting from the concentration of potential prey. Here, we report the predation of a Pteronotus bat by a Corallus hortulanus in the Brazilian Amazon. On three occasions over a year, individuals of C. hortulanus were observed around a cave that harbors populations containing tens of thousands of bats. On one occasion, an individual of this snake species was observed preying on a Pteronotus sp. as it left the cave. Our record extends the known diet for C. hortulanus, documenting the predation of a mormoopid bat by this snake species for the first time. This record reinforces the need for longitudinal studies at sites with exceptional bat populations to gain a deeper understanding of the ecological predator-prey relationships involving this diverse group of mammals.

We performed the first quantitative survey of ectoparasitic assemblages on three species of mormoopid bats living on the Caribbean island of Puerto Rico: Mormoops blainvillii Leach (n = 40), Pteronotus quadridens Gundlach (n = 40), and Pteronotus parnellii Gray (n = 9). We examined bats for parasites primarily on 8–10 May and 24–27 July 2002 at Culebrones Cave, near Arecibo, Puerto Rico. Only 50% of M. blainvillii were infested with at least one parasite, compared with 85–100% for Pteronotus; infested individuals of both species of Pteronotus also harbored a greater number of parasites than did M. blainvillii. The assemblage on M. blainvillii was less diverse than in the other species and more dominated by a single group of parasites, the chiggers. Chirodiscid ear mites and spinturnicid wing mites were common on both species of Pteronotus but absent from M. blainvillii. All P. parnellii harbored streblid flies, but none typically was found on P. quadridens or M. blainvillii. Adult female M. blainvillii and P. quadridens sheltered a greater number of ectoparasites than did males. All host-parasite combinations represented new associations for Puerto Rico.

A study was made of the nightly activities of four species of mormoopid bats ( Pteronotus parnellii, P. personatus, P. davyi , and Mormoops megalophylla ) that inhabited a cavern system in the Sierra Madre Occidental in Sinaloa, Mexico. The bats were observed, were mist-netted along heavily traveled flyways, and recaptures of previously marked individuals were recorded. Activity of bats began shortly after sunset and there was considerable light-testing prior to emergence. Some bats began returning to the roost as early as 1.5 hours after the exodus flight began, but most bats appeared to remain away from the roost for from 5 to 7 hours. The congestion just before dawn when masses of returning bats attempted to re-enter the roost suggested that size of the colony may have been limited by size of the roost entrance. Regarding evening dispersal flights: flyways to foraging grounds were long (to at least 3.5 kilometers but almost certainly several times this length for some individuals); bats sometimes used shortcuts along dispersal routes, but normally followed topographic features; in some cases there appeared to be distinct spatial separation between the flyways of different species; individuals showed some fidelity to particular flyways; and natural environmental stimuli may have caused abandonment of regularly used flyways. We estimated that the 400,000 to 800,000 bats comprising the large colony consumed from 1902 to 3805 kilograms of insects each night. Thus, these bats are of considerable significance in the energy flow of tropical ecosystems.

Echolocation calls emitted by the 4 species of Cuban mormoopid bats were compared to determine vocal signatures that enable identification of each species in the field during their evening exodus. Echolocation calls produced by Mormoops blainvilli are downward frequency-modulated (FM) signals in the range of 68.4– 52.5 kHz. Echolocation calls emitted by Pteronotus macleayii and P. quadridens have a similar design consisting of a short constant-frequency (CF) segment followed by a downward FM segment. The CF segment was at 70.0 kHz in calls from P. macleayii, and at 83.3 kHz in calls from P. quadridens. Echolocation calls from P. parnellii consist of a long CF segment, which is preceded by a short initial upward sweep and followed by a downward FM terminal sweep. The CF value of the 2nd harmonic was a good parameter for species identification. The features of the echolocation calls of each of the species were used to identify them during the evening exodus from 2 Cuban caves.