Description of all the 27 localities that were studied and were classified among urban, suburban, and forests.
Urbanization is a phenomenon that results in fragmentation and eventual destruction of forests. Suburbanization is a subset of that same phenomenon in which fragmentation has resulted in the retention of small patches of the original forest and surviving old growth trees. Alternatively, the area surrounding the central city had been cleared for agricultural use and the suburban residents have planted many trees in parks and private property. This fragmentation will of course affect many species of bats, including species of the family Phyllostomidae. In this work, we estimate and compare the diversity of phyllostomid bats in three landscapes in Honduras: forests, suburban, and urban areas, from 2015 to 2018. Concurrently, we compared bat activity patterns based on the hour and percentage of moonlight at the time they were captured, and we compared external measurements, forearm and ear length. Urban areas are the least diverse and exhibited the lowest abundance. The forearm and ear length were significantly different only between forests and urban areas. The degree of lunar phobia also differed among those landscapes, but the time of capture did not differ. This is the first attempt to describe the activity patterns of phyllostomids in these studied areas and the effect of urbanization on Honduran bats. As expected, we found that from forests to cities, the diversity and abundance of phyllostomids decreased. However, there are many gaps in our knowledge of how totally or partially urbanized areas are affecting phyllostomid bats in Honduras.
- phyllostomid bats
- Río Plátano Biosphere Reserve
- taxonomic diversity
1.1 Urbanization, suburbanization, and bats
It is generally agreed that urbanization has had a major negative effect on populations and diversity of native plants and animals. Nevertheless, humans plant a wide variety of vegetation in their urban and suburban areas, thus initiating the food chain on which most animals depend. Although diversity is clearly greatly reduced in the urban setting, at the population level the effect has been extremely heterogeneous across the animal kingdom. Bats (Chiroptera) are an extremely diverse group, with more than 1400 species worldwide, living in almost all habitats. The reaction of bats to urban environments was recently reviewed . Jung and Caragh  determined that the behavioral and/or morphological traits at the level of individual species determine species’ adaptability to urban areas. Further, they determined that the driving factors for species adaptability to urban areas may be regionally divergent.
As Jung and Caragh  point out, bats are found in all cities over the world. Of the approximately 20 families of bats, only two tend to avoid cities entirely, the Rhinolophidae and Mormoopidae, whereas a heterogeneous reaction at the species level is typical of the other families.
Urban habitats have both potential disadvantages and advantages from the perspective of bats. Clearly cities are high in noise, light, and chemical pollution compared to natural habitats. Light pollution may be an especially difficult factor to which bats must adapt. Depending on roosting requirements, cities may provide abundant roost sites, such as buildings, or not, for example for bats that roost in vegetation. Often drinking water and food supplies are enhanced by the human residents of the city, again depending on the bats’ specific requirements. Since tree cover in cities averages less than 30% , bats adapted to forests may not do well, whereas in grassland and savannah areas, bats may find the tree cover advantageous .
Although there have been many studies of urban bats, these have been concentrated in temperate North America and Europe, and focus mainly on bats of the family Vespertilionidae, e.g., Dixon , Hale et al. , Pearce and Walters . Bat activity and diversity seem to be highest in older suburban areas and parks and decrease towards the center of cities where there is little vegetation. It is clear to us that the change from urban to suburban to rural is a continuum; therefore, it is not productive to divide this continuum into discrete units except very generally as we are doing here for comparative purposes. The differences between urban and suburban can, for example be exemplified by such physical differences as tree density, percent paved area, building size and density, etc. These variables change in a predictable way as we pass through the continuum. Thus, when we approach 0% paved area, very low building density, and/or 100% tree density, we have reached the end of the continuum and are in forest or agricultural zones.
Although a few species do very well in cities, as for example, the huge colony of
A threat to bat populations, clearly related to urbanization, is mortality on highways. This problem has been but rarely studied, mostly in the temperate zone (e.g., ) but clearly exists. Recently a study in Brazil demonstrated that significant bat mortality is occurring on Brazilian highways as well .
There are relatively few studies of bats in urban areas of the Neotropics. Jung and Kalko  in Panama, using audio recordings, report decreased diversity and abundance in the urban setting, compared to the high diversity in forests in that country. They also note that in the city, most of the bats are high flying species, primarily of the Molossidae. In Costa Rica one of us  found the same trend with audio recordings in a large metropolis and in a smaller provincial capital. Jung and Kalko , recording in a small city adjacent to forest, found higher diversity than in large urban centers, but noted that some species that were abundant in the nearby forest were never recorded in town. For our purposes, we may think of this town as a suburban area. In Costa Rica, in a large urban center, but recording only in city parks, the number of bat passes was much greater in the larger parks than in the smaller parks . Overall, those authors found considerably less activity than we consistently found in non-suburban settings . The urban bats identified from the calls were all from the families Vespertilionidae and Molossidae. In another Costa Rican study the author mist-netted in parks in the city, finding a relatively small number (for the netting effort) of bats of the family Phyllostomidae, all of which were very common species that eat fruit and/or nectar .
1.2 Bat diversity in Honduras
Because of its location on the relatively narrow isthmus of Central America, connecting North and South America, Honduras is home to species typical of South America, others typical of temperate North America, and some that are endemic to Central America and southern Mexico. According to a recent review,  there are 113 species of bats currently known from Honduras, and we expect several more species will be added in the future. In Central America, only Costa Rica has more species, with 120 listed . As detailed in the paper cited , the bats belong to seven different families, the Emballonuridae (9 species), the Phyllostomidae (59 species), the Mormoopidae (5 species), the Noctilionidae (2 species), The Thyropteridae (1 species), the Natalidae (2 species), the Molossidae (17 species), and the Vespertilionidae (18 species).
These species include frugivores, nectarivores, insectivores, sanguinivores, carnivores, and omnivores, and occupy many essential ecological niches in Honduras, dispersing seeds, pollinating flowers, and controlling insect numbers, among others.
1.3 Objectives and hypothesis
We lack information demonstrating how urbanization is affecting the diversity of bats in Honduras, Central America. We hypothesize that, on a continuum from forests to cities, the diversity of New World leaf-nosed bats (Phyllostomidae) will be significantly reduced. Therefore, this works aims to estimate and compare the diversity of phyllostomid bats in three landscapes in Honduras: forests, suburban, and urban areas; to determine if the forearm and ear length has any significant effect on species composition of bat assemblages in the three landscapes; and to describe the activity patterns of those assemblages.
2. Materials and methods
When defining “urbanization” and “suburbanization”, which are processes that are closely related and linked along a continuum, we follow Tammaru et al. . We will consider suburbanization as the expansion of suburbs by the increase of its population from the migration of residents of the central city [21, 22]. Thereby, we will refer to the Ciudad-Universitaria of the Universidad Nacional Autónoma de Honduras (CU-UNAH) as the “urban area” in this manuscript. The same authors described suburbanization is the redistribution of a population away from central cities and into suburbs. In this work, we are referring to Sabanagrande as the “suburban area”. All other studied areas in this work are considered as “forests” located in the Río Plátano Biosphere Reserve. See below for the description of each studied area.
2.2 Studied areas
|Departament||Locality||Municipality||Latitude||Longitude||Elevation (m asl)||Landscape|
|2||Gracias a Dios||Ciudad Blanca 1||Brus Laguna||15.246||−84.969||250||Forest|
|3||Gracias a Dios||Ciudad Blanca 2||Brus Laguna||15.246||−84.972||214||Forest|
|4||Gracias a Dios||Ciudad Blanca 3||Brus Laguna||15.245||−84.96||245||Forest|
|5||Gracias a Dios||Ciudad Blanca 4||Brus Laguna||15.245||−84.969||225||Forest|
|6||Gracias a Dios||Ciudad Blanca 5||Brus Laguna||15.248||−84.968||223||Forest|
|7||Gracias a Dios||Ciudad Blanca 6||Brus Laguna||15.245||−84.965||204||Forest|
|8||Gracias a Dios||Ciudad Blanca 7||Brus Laguna||15.251||−84.974||239||Forest|
|9||Gracias a Dios||Ciudad Blanca 8||Brus Laguna||15.244||−84.966||233||Forest|
|10||Gracias a Dios||Ciudad Blanca 9||Brus Laguna||15.241||−84.969||206||Forest|
|11||Francisco Morazán||El Ocotal||Sabanagrande||13.791||−87.314||976||Suburban|
|12||Francisco Morazán||La Finca “Divisadero”||Sabanagrande||14.561||−87.801||1105||Suburban|
|13||Francisco Morazán||La Tigra||Sabanagrande||13.800||−87.313||790||Suburban|
|14||Gracias a Dios||Las Marías Pesh 1||Juan Francisco Bulnes||15.680||−84.838||33||Forest|
|15||Gracias a Dios||Las Marías Pesh 2||Juan Francisco Bulnes||15.679||−84.846||50||Forest|
|16||Gracias a Dios||Las Marías Pesh 3||Juan Francisco Bulnes||15.676||−84.851||28||Forest|
|17||Gracias a Dios||Las Marías Pesh 4||Juan Francisco Bulnes||15.676||−84.843||33||Forest|
|18||Gracias a Dios||Pico Dama 1||Juan Francisco Bulnes||15.695||−84.915||373||Forest|
|19||Gracias a Dios||Pico Dama 2||Juan Francisco Bulnes||15.695||−84.915||360||Forest|
|20||Gracias a Dios||Pico Dama 3||Juan Francisco Bulnes||15.692||−84.915||394||Forest|
|21||Gracias a Dios||Pico Dama 4||Juan Francisco Bulnes||15.695||−84.917||433||Forest|
|22||Gracias a Dios||Pico Dama 5||Juan Francisco Bulnes||15.694||−84.915||383||Forest|
|23||Francisco Morazán||UNAH (CC)||Distrito Central||14.008||−87.165||1073||Urban|
|24||Francisco Morazán||UNAH (JB)||Distrito Central||14.087||−87.166||1050||Urban|
|25||Francisco Morazán||UNAH (Lagunas)||Distrito Central||14.086||−87.160||1050||Urban|
|26||Francisco Morazán||UNAH (Polideportivo)||Distrito Central||14.086||−87.169||1062||Urban|
|27||Gracias a Dios||Waikna Tara||Juan Francisco Bulnes||15.660||−84.893||44||Forest|
Surveys were carried out at the National University Campus’ Botanical Garden in Tegucigalpa, capital city of Honduras, in the Department of Francisco Morazán (Table 1). The ecosystem is a tropical dry forest . The species of Fabaceae, Myrtaceae, and Asteraceae are the most common, including
We studied a tropical moist forest  located in the central region of Honduras in the Department of Francisco Morazán, municipality of Sabanagrande (Table 1). The vegetation included
The RPBR, including La Moskitia, is located within the departments of Gracias a Dios, Olancho, and Colón. Based on Holdridge , the life zone represented is tropical wet forest. The RPBR is the only site in Honduras declared as world Heritage. Some plant species associated with the study area are
2.3 Taxonomy, mist-netting, and ethical guidelines
We followed the most recent taxonomic checklist of the bats that occur in Honduras . All the bats were captured using mist-nets of 12.5 x 2.5 m with a mesh of 35 mm. We followed Kunz and Kurta  for positioning the mist nets according to the vegetation, landscape, bodies and water and phenophases (fruits and flowers) of the plants. Bats were identified and measured (FA = forearm length; E = ear length; BH = body height) using taxonomic keys of Timm, LaVal and Rodriguez  Medina-Fitoria , and Mora . We quantified the sampling effort by multiplying the area of all of the mist-nets that were opened during each night by the number of hours that remained open  in which a total of 47,686.8 m2*h was accumulated. All the bats were handled according to the guidelines for the use of wild mammals in research and education .
2.4 Diversity, landscape, and activity patterns analyses
The diversity of each landscape was measured using the Alpha Diversity Index (following Jost  and Moreno et al. ), and species richness was estimated with Chao 1. These analyses were based in the sampling effort of each site and the abundances of each species using EstimateSMac 910 with 100 randomizations [35, 36].
For the activity patterns analyses we used the abundances of all the species  and correlated them with the time and the percentage of the moon illumination in which bats were captured from each type of landscape. Moon illumination was taken for each date from the following website: https://www.moongiant.com/ . We used the Shapiro–Wilk test to test for the normal distribution and Levene’s test to test for the homogeneity of variances of the data. Considering that data was normally distributed, means of the forearm length, ear length, body height, time, and moon percentage were represented by the ANOVA (Analysis of Variance) analyses in Table 2. To compare means we performed posthoc Tukey tests at a confidence level of 95%. For all the analyses we considered significant differences when p ≤ 0.05. Except for time, in which we use the Spearman’s correlation coefficient to determine any relation between the landscapes and the time activity.
|Landscape||Individuals||Species||Sampling effort (m2*h)||Chao 1 estimator||Alpha diversity index||Individuals per m2*h||Species per m2*h||FA (mm)||E|
|BH (mm)||Moon illumination (%)||Time|
|Forests||376||24||14,567.4||28.97||5.72||0.03||0.0016||74.68 (29.00–91.35)||30.75 (9.48–42.54)||53.29 (36.8–69.78)||65.26 (15.5–99.52)||5:30 PM – 5:20 AM|
|Suburban||169||17||18,839.4||19.24||4.71||0.01||0.0009||67.74 (33.01–69.46)||16.59 (7.67–17.83)||57.60 (45.9–69.30)||47.46 (0.24–94.43)||6:00 PM –|
|Urban||143||7||14,280.0||7.5||1.54||0.01||0.0005||67.71 (31.10–72.00)||23.99 (9.82–28.34)||68.73 (55.96–81.50)||50.06 (0.06–100)||5:30 PM –|
To determine taxonomic similarities between the landscapes (urban and suburban areas and forest) we performed multiple regressions of distance matrices . In addition, to represent graphically the taxonomic composition in the distinct habitat types, we performed a NMDS (non-metric multi-dimensional scaling) analysis with two dimensions and plotted the NMDS axes against landscapes . All analyses were performed in R Core Team  version 3.4.2, using the vegan  and ecodist .
3.1 Alpha diversity in three landscapes
According to Chao 1 (Table 2), urban areas (percentage of how many species According to Chao 1, urban areas (percentage of how many species were recorded in parentheses) are the least diverse, as expected, because only 7.5 species are expected (93.3%) followed by suburban areas (87.2%) with 19.24, and then by forests with 28.97 (82.2%). Supporting Chao 1, the Alpha diversity index was highest in forests with 5.72, followed by suburban and urban areas (Table 2), in that order. Considering the sampling effort, urban areas are not only the least diverse but also the least abundant based on number of bats captured, followed by suburban areas and forests (Table 2). Even though we found three different assemblages (Figure 2) we found no significant correlation between taxonomical α-diversity and the type of landscape (R2 = 0.04; DF = 1,24; P = 0.24). However, we found species such as
3.2 Activity patterns vs. morphological traits
Considering time (Figure 4), we found no significant correlations in any type of landscape: forests and suburban areas (R2 = 0.00; DF = 1,154; P = 0.23), forests and urban areas (R2 = −0.01; DF = 1,139; P = 0.62), and urban and suburban areas (R2 = −0.00; DF = 1,139; P = 0.99). In the case of body height means, only the suburban areas and forests have no significant differences (F (2,203) = 2.3, p = 0.21; Figure 5A), and were divided into two groups urban areas (a) and forests and subruban areas (b). See Table 4 to see the other p values of this and other analyses. The ear length means were only significant different in suburban and forests landscapes (F (2,165) = 4.57, p = 0.05; Figure 5B), however, all the landscapes were assigned to the same group (a). When comparing forearm length means with posthoc Tukey tests, landscapes were classified into two groups urban (a) and suburban and forests (a) and only the comparison between suburban areas and forests was not significant (F (2,431) = 21.41, p = 0.99; Figure 5C). Finally, the moon percentage mean in which bats were captured was significant different among all the landscapes (Figure 5D), categorized into three different groups a (forest), b (urban areas), and c (suburban areas).
|Forests - FA||—||0.99||<0.01|
|Suburban - FA||0.99||—||<0.01|
|Urban - FA||<0.01||<0.01||—|
|Forests – E||—||0.05||0.17|
|Suburban - E||0.05||—||0.61|
|Urban - E||0.17||0.61||—|
|Forests - BH||—||0.21||<0.01|
|Suburban - BH||0.21||—||<0.01|
|Urban - BH||<0.01||<0.01||—|
|Forests - moon||—||<0.01||<0.01|
|Suburban – moon||<0.01||—||<0.01|
|Urban - moon||<0.01||<0.01||—|
As expected in Honduras, there is a consistent decrease of phyllostomid bat diversity and abundance from forests to cities. As anticipated, we found that the diversity is less in urban areas (cities) and suburban areas in comparison to forests. However, these remnants of forest are important for bat conservation in urban areas. For example, the high abundance of
4.1 How urbanization is affecting bat diversity
Urbanization is the second most detrimental anthropogenic agent of landscape change , since bat diversity and species abundance are comparatively lower in cities than in primary forests or rural areas . This is the case not only for Honduras, but worldwide. For example, in Poland, urbanization pressure is a common phenomenon in several protected areas due to the dispersion of buildings and the expansion of summer construction . Additionally, artificial lighting and sound pollution can alter commuting processes in foraging bats, especially sound which has a more deterrent effect for bats than light as some insectivorous bats feed on the insects that are attracted to streetlights [50, 51, 52]. Interestingly, habitat degradation affects the diversity of bat communities in more complex ways than simply population stability .
Bat response and sensitivity to urbanization varies among species assemblages in urbanized landscapes. In this way species with high tolerance become more abundant and dominant. However, the low diversity and abundance of urban bat fauna can be attributed, at least partially, to a shortage of roosting sites . For a better understanding of bats that do not fly below canopy in urban areas, acoustic monitoring can provide data for species that are rarely captured in mist nets (, and see introduction, this chapter). Unfortunately, we have little such data for Honduras as of now.
The fact that forearm length was only significantly different between forests and urban areas and the ear length between suburban areas and forests can be explained from two points of view. First, we found that Sabanagrande has a mixture of the other two assemblages, and even has species that were found only there (e.g.,
Secondly, the functional traits varied. For example, the well-conserved forests of the RPBR have larger species that were only recorded there (e.g.,
Species such as
4.2 From cities to forests: Activity patterns of phyllostomids in Honduras
We hypothesize that New World leaf-nosed bats in forests are more likely to be negatively affected by brightness of the moon because of safety concerns (hunting activities by visually oriented predators like owls) when the moon is brighter . In contrast, urban and suburban areas have equally high light intensity every night (e.g., traffic lights, streetlights, shopping centers, etc.). Another feature that supports our hypothesis is that we found significant difference between all the areas. This is probably because the light intensity of suburban areas is increasing in the same way as in urban areas, and the bats that survive there are able to acclimatize quickly. However, the time patterns were not significantly different among the three landscapes due to the wide range and different foraging behaviors. In general, phyllostomids have an early activity peak and then declining activity through the night . Habitat specialization, nutrient intake, and food procurement are features that are associated with bat success in transformed landscapes [55, 58].
There are two more works describing activity patterns in Honduras. The first one, Medina-Fitoria et al.  studied certain areas included in the RPBR, and determined that in the Caribbean slope of Nicaragua and Honduras, mature and intact primary forests are the most important habitats to conserve. They also determined that fragmentation due to extensive cattle farming and agriculture is perhaps the major threat to these forests. And the second study, in the northwestern region of Honduras, in Cusuco National Park, by Medina-Berkum et al.  indicated that the presence of
Although we predicted that from forests to cities, the diversity of phyllostomids will decrease, this is the first attempt to describe their activity patterns in these areas in Honduras. Considering the extension of forests, Duarte et al.  mentioned that 48% of the Honduran territory is covered by forests. With the high rate in which they are being diminished is approximately 23,303.56 hectares per year , the probability of losing bat species in Honduras is all too real. On the other hand, there are some species that have been adapting very well, as is the case of
Undoubtedly, the RPBR is one of the most important regions in Honduras, and probably in Central America, for bat conservation due to the large extensions of pristine forests and the limited occurrence and abundance of certain species (e.g.,
We would like to thank to Alejandro Orellana, Diego Mazier, and Eduardo Ordoñez because most of the field work was done with them and for their comments to this chapter. We are grateful to the staff of El Ocotal, especially to Alejandro Velásquez, for all their support during this research. To the ICF, for the research permit: Resolución–DE–MP–064–2017. We want to thank to all the wildlife and forest manager, native people, civilians, and police and military officer that helped us during all this research. Finally, MATC wants to personally thank Marcia Flores-Casco and her family for their gracious hospitality in Brazil during the COVID-pandemic while he was writing this chapter.
Conflict of interest
The authors declare no potential conflict of interest.