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Introduction
The Order Chiroptera is one of the most diverse and widely distributed vertebrate groups on the planet. Bats represent almost a quarter of all mammals (Hutson et al., 2001), with more than 1400 species (Simmons & Cirranello, 2020; Zachos, 2020), and they are the second most diverse group after the Order Rodentia (Solari & Baker, 2007).
Bats play a key trophic role being both prey and predatory species; presenting a very broad trophic spectrum that includes blood, insects, nectar, pollen, fruits and floral tissues. These habits provide diverse ecosystem services, such as pest control, seed dispersal, pollination and energy recycling (Galindo-González, 1998; Vaughan et al., 2011).
In Mexico, studies on bats have reported the presence of eight families and a total of 140 species (Rivas-Camo et al., 2020), of which seven families and 55 species are reported for the state of Sinaloa. However, studies on bat populations in this area are scarce or nonexistent (Almazán-Catalán et al., 2015). This result in lack of knowledge on their environmental needs, current threats and their impact at population level (Hutson et al., 2001). This makes it difficult to identify the ecological role of these organisms and their role as keystone mutualist in the ecosystem (Horner et al., 1998; Menchaca et al., 2020). Acquiring this knowledge is essential, especially in areas of ecological importance such as the Sierra de Navachiste protected area.
Sierra de Navachiste, Mexico is classified as a Ramsar site forming part of the polygons for both the Macapule-Navachiste-San Ignacio lagoon system and the Santa María-Ohuira lagoon system (Zavala-Norzagaray et al., 2007) and is considered an ecological island, because it is surrounded by livestock farming and other agricultural activities.
In the region, 18 species of cacti have been identified on islands and the continental zone, where the dominant vegetation is Sternocereus thurberi and Pachycereus pecten-aboriginum (Saturnino-Díaz, 2008). These species are of great importance forming ecological corridors for bat migrations from the southeast to the northwest, as bats follow the flowering season's progression (Bustamante & Búrquez, 2005; Bustamante et al., 2016). The above highlights the importance of studying population status, temporal ecology and the key bat habitat, particularly for migratory species such as lesser long-nosed bats (Leptonycteris yerbabuenae) along their migratory routes.
The species L. yerbabuenae is a migratory bat considered a priority for the maintenance of dry ecosystems dominated by columnar cacti (Rojas-Martínez et al., 2012). In Mexico, it is a species that migrates latitudinally along the Mexican Pacific coast from the northwest of Mexico and southwestern United States. This migration is linked to the flowering and fruiting season of columnar plants (Valiente-Banuet, 2002; Frick et al., 2018) that produce chiropterophilic flowers including Carnegiea gigantea, P. pringlei and S. thurberi (Valiente-Banuet, 2002). It is known that this species can move more than 50 km in one night towards the foraging area and maintain an activity of up to 7.5 hours and they always return to the same cactus patches due to the use of reinforcement learning (Egert-Berg et al., 2018; Goldshtein et al., 2020).
Although the species seasonal ecology and population status has been extensively studied in central Mexico, little is known about its distribution in the northwest of the country (Frick et al., 2018). In the state of Sinaloa, studies on bat populations are scarce to nonexistent (Almazán-Catalán et al., 2015). Therefore, the environmental needs, current threats and possible impacts facing the existing bat populations are unknown (Hutson et al., 2001).
This makes it difficult to determine the ecological role of these organisms and their role as keystone mutualist in the ecosystem (Hornet et al., 1998; Menchaca et al., 2020). Particularly, if the lesser long- nosed bat play a key role in the maintenance of biodiversity in dry environments of the region. Acquiring this knowledge is essential, especially in areas of ecological importance such as the Sierra de Navachiste protected area.
The purpose of this study was to identify and measure seasonal bat roost occupation and reproductive timing on the population of bats on the Sierra de Navachiste, Mexico, to assess the seasonal ecology.
Methodology
Study area
The Sierra de Navachiste is a natural protected area of state jurisdiction registered as an area subject to Ecological Conservation. It is classified as a Ramsar site forming part of the polygons for both the Macapule-Navachiste-San Ignacio lagoon system and the Santa María-Ohuira lagoon system (Zavala-Norzagaray et al., 2007). The region has a territorial extension of 17,055 hectares, and is located between the municipalities of Guasave and Ahome, Sinaloa, Mexico, between geographic coordinates 25° 27’ 10’’ and 25° 36’ 30’’ N, 108° 48’ 05’’ and 109° 05’ 00’’ W. This area presents characteristics that denote an ecological island, due to its geographical location as a small peninsula and the effects of anthropogenic activities such as agriculture, which isolates the Sierra de Navachiste from other natural areas (Figure 1).
During fieldwork, we identified a total of 15 caves, of which 14 held small populations of bats for only a few days, serving more as temporary shelters. Of the identified caves, only one had bat populations throughout the year. Furthermore, this site was chosen based on information collected through a citizen science project, with support from residents from the local fishing communities.
It was considered appropriate to focus efforts on the cave called "Cerro de Arena" due to its large size, the composition of the bat community it houses, as well as being considered an important site for the extraction of guano. The cave is located at coordinates 25°29'40.1'’ N and 109°04’31.82’’ W (Figure 1).
During the period 2012-2013 four nocturnal samplings were carried out in a lapse of 12 h (18:00 to 6:00 h). One for each season of the year during the new moon period, to avoid the “Lunar phobia” syndrome, which is a behavior of evasion of the periods of greater brightness generated by the moon (Heithaus & Fleming, 1978; Santos-Moreno et al., 2010).
Environmental conditions were also considered to easily access to the study site. Bats were captured by placing mist nets at dusk at the entrance of the cave. Nets were checked up every 30 min. The bats were placed in cages until the data and samples were taken. Captured bats were identified to genus and species level, the life stage (pup, juvenile and adult), sex and trophic guild (Medellín et al., 2008) were also recorded. The handling was carried out according to PREDICT Operating Procedures: Bat Sampling Methods (PREDICT Consortium, 2013) and under permission no. FAUT-0250 of the Secretaría de Medio Ambiente y Recursos Naturales, Mexico.
Sampling sufficiency
Diversity was estimated from the basic community data. The species richness (S) was determined as the total number of species observed, without considering its importance value. The relative abundance (R), or the proportion of a species within the community, was obtained from the total number of individuals by species (n) among the total number of individuals captured (N) multiplied by 100.
Morphometric data such as size (mm) and weight (g) of the captured bats were presented as (mean ± SD) followed by minimum and maximum intervals in parentheses (Min-Max).
Additionally, an accumulation curve was calculated using INEXT program (iNterpolation and EXTrapolation) to know whether the number of species found were representative with respect to the sampling effort made (Jiménez-Valverde & Hortal, 2003; Hsieh et al., 2016) (Figure 2).
Diversity and evenness of the bat community were determined using the indices of Shannon - Wiener (H ’) and Simpson (λ). Pielou index [J’]) was used to measure the equitability between the diversity observed in relation to the maximum expected diversity (H'max), being this the maximum possible value of H’ (if every species had the same evenness) (Moreno, 2001).
Results
The cave "Cerro de arena" is the largest and most complex in the Sierra de Navachiste, Sinaloa, with an approximate distance to the sea of 340 meters. The cave has two entries and an approximate depth of 70 m (Figure 3).
The samplings were carried out per season between 2012-2013, to know the species richness, abundance, and diversity of bats. A species accumulation curve was made to know whether the identified bat species in the study area were representative of the sampling effort. It was estimated a total number of 41 bats per sampling effort (Figure 2). During each survey up to 71 bats were captured (Summer), therefore the sampling effort was enough to include all the species present in the study area.
Bats (n = 370) were captured belonging to three families and five species: Leptonycteris yerbabuenae (n=205), Pteronotus psilotis (n=110), Macrotus californicus (n=29), Mormoops megalophylla (n=24) and Balantiopteryx plicata (n=2). The highest relative abundance of the captured organisms occurred in spring, followed by autumn, summer and winter, respectively (Table 1). By species, L. yerbabuenae presented the highest percentage of bats captured throughout the year and during three seasons (spring, summer, and winter). However, P. psilotis was the most abundant species during autumn (Table 1). Of the total female bats collected, 29 were identified gestating and other 29 were lactating. The gestating individuals were 20 L. yerbabuenae and nine P. psilotis. The lactating females were four L. yerbabuenae, two P. psilotis and one M. californicus.Table 1 presents the total bats captured by family and species, relative abundance, life stage and sex.
By sex, a higher proportion of females was observed compared to males over the study year. However, in spring, autumn and winter, the population was represented mainly by females, while in summer the proportion of male and female bats was similar. Of the total female bats (77), 20 were gestating and four lactating. The pregnant females were observed in winter and the lactating females in spring (Table 1).
Table 1 Number of organisms captured, life stage and sex of Bats community from Navachiste, México, by annual season
| Family Specie | Number of organisms captured | Total | Life Stage | Sex | |||||
|---|---|---|---|---|---|---|---|---|---|
| Autumn | Winter | Spring | summer | Annual | J | A | M | F | |
| Mormoopidae Mormoops megalophylla | 13 (15) | 11 (20) | 0 (0) | 0 (0) | 24 (6) | 0 | 24 | 10 | 14 |
| Pteronotus psilotis | 49 (56) | 12 (22) | 20 (13) | 29 (41) | 110 (30) | 50 | 60 | 43 | 67 |
| Emballonuridae Balantiopteryx plicata | 2 (2) | 0 (0) | 0 (0) | 0 (0) | 2 (1) | 2 | 0 | 0 | 2 |
| Phyllostomidae Macrotus californicus | 15 (17) | 6 (11) | 2 (1) | 6 (8) | 29 (8) | 4 | 25 | 15 | 14 |
| Leptonycteris yerbabuenae | 8 (10) | 26 (47) | 135 (86) | 36 (51) | 205 (55) | 112 | 93 | 77 | 128 |
| Total | 87 | 55 | 157 | 71 | 370 | 168 | 202 | 145 | 225 |
Note: Number of organisms captured followed by percentage of relative abundance in parentheses. Life Stage: (J) juvenile, (A) Adult; Sex: (M) Male, (F) Female.
By trophic guild, we registered one Nectarivore species (L. yerbabuenae), three aerial insectivores (P. psilotis ˃M. Megalophylla and B. plicata) and one gleaning insectivorous (M. californicus) (Kalko et al., 1996).
With regard to species richness, the greatest number of species occurred in autumn, followed by winter, spring and summer, respectively. The bat M. megalophylla was the only species found in autumn and winter, while B. plicata was only found in autumn. Bat biodiversity in the Cerro de Arena cave, presented high annual diversity among the species present in the study area (H’=1.09; λ=0.59), which were evenly distributed (J’=0.68). By season, winter has the highest biodiversity indexes, and spring the lowest (table 2). Spring was the season with the lowest index among species, mainly characterized by L. yerbabuenae (Table 2).
Table 2. Ecological component, diversity and evenness of the bats community from Navachiste, México by annual season.
| Component | Autumn | Winter | Spring | summer | General |
|---|---|---|---|---|---|
| Richness (S) | 5 | 4 | 3 | 3 | 5 |
| Abundance (R) | 24% | 15% | 42% | 19% | 100% |
| Shannon-Wiener (H') | 1.22 | 1.25 | 0.45 | 0.92 | 1.09 |
| Simpson (λ) | 0.62 | 0.68 | 0.24 | 0.57 | 0.59 |
| Pielou (J') | 0.76 | 0.90 | 0.41 | 0.84 | 0.68 |
It is important to mention that these species can share not only the same cave but also the same roost area, as has been observed with M. megalophylla, P. psilotis and L. yerbabuenae, using the same ledge areas. That said, L. yerbabuenae preferred the first chamber but were also observed during the breeding season in the central section of the cave, whereas bats of the genus Pteronotus also shared ledge area with other bat species. They preferred the second chamber of the cave and were not observed in the vaults of the first section.
Regarding species composition, L. yerbabuenae was the dominant bat species with 205 individuals captured during the study. The largest proportion of bats was captured during spring, followed by summer, winter, and autumn. Of the total captured organisms, juveniles were slightly more abundant than adults. However, by season, adults were the most abundant in summer, autumn and winter, while in spring juveniles were up to two times more abundant than adults.
Discussion
Mexico is considered a megadiverse country in both animal and plant species. Studies on chiroptera richness in Mexico indicate that diversity is highest in the warmer and more humid states in the southern part of the country, e.g., Chiapas has 106 species (Retana & Lorenzo, 2002) and Oaxaca 94 (García-García, 2006). Sinaloa, despite being a state that presents a dryer climate than those further souths, has 55 bat species (Alvarez-Castañeda & Patton, 1999).
Part of this species diversity was reported by Espericueta-Viera (2012) in the Meseta de Cacaxtla, located between the municipalities of Mazatlán and San Ignacio, Sinaloa. The author reports 12 species and five families. The only species captured in our study that was absent in the Meseta de Cacaxtla was M. californicus. This may be explained due to the distribution of the species which southern limit is northern Sinaloa.
L. yerbabuenae is included on the IUCN red list (International Union for the Conservation of Nature) as a "vulnerable" species, and in Mexico it is listed within the NOM-059-SEMARNAT-2010 as a " Special protection" species. This bat is considered a "keystone mutualist species" due to its role within the ecosystem directly influencing the survival of other species through strong trophic relationships, which even influence the very structure of the ecosystem (Paine, 1995; Hornet et al., 1998; Menchaca et al., 2020). Notably, L. yerbabuenae has a mutualistic relationship with some cacti and agaves playing a key role in pollinating the columnar (Pachycereus pecten-aboriginum) and Pitahaya (Stenocereus thurberi) cacti that dominate the areas landscape. These species display a type of plant-pollinating interaction known as "pollination syndrome" (Bustamante & Búrquez, 2005), which consists of a plant species producing only one type of flower that is only suitable for a particular pollinator species (Isasi-Catalá, 2011). Of all Mexican columnar cacti, 72% present this selective pollination syndrome (Valient-Banuet et al., 1996). On the other hand, the feeding habits of the bat L. yerbabuenae contribute to the scarification process which results when bats eat cacti fruits, helping soften the seed coat in their digestive tract, favoring its permeability, and with it, taking up water towards the seeds accelerating germination (Fleming et al., 1996; Bustamante & Búrquez, 2005). It is important to emphasize that the cacti P. pecten-aboriginum and S. thurberi are xenogames species unable to self-pollinate. Therefore, any reduction or loss in the population of L. yerbabuenae, would result in a decrease in the production of fruits of these cacti species and with this their decline in the ecosystem. However, L. yerbabuenae does not only feed on pollen, but also the fruit produced by these same species of cacti.
The bat L. yerbabuenae has a great flight capacity and given its migratory nature it may be the phylostomid with the longest flight distances, which indicates that its feeding sites are not necessarily close to its refuges (Medellín et al., 2018). Therefore, given their characteristics, they could completely cover the Sierra de Navachiste, pollinating and dispersing seeds throughout the area. However, further studies are needed to understand the role of this species in the pollination of cacti and the health of the floral ecosystem of the study area.
Species richness
The bat community of the "Cerro de Arena" cave was composed of five species. We recorded the presence of L. yebabuenae throughout the entire year and identified this population to be reproductively active. A breeding colony of L. yebabuenae has been previously identified in the Meseta de Cacaxtla, Sinaloa (Espericueta-Viera, 2012). However, we observed the complete reproduction cycle in Navachiste. Mating was recorded in summer and autumn, although in the latter season a smaller number of animals were captured. Winter was characterized by the capture of gravid females, and in spring, lactating females and a many offspring were collected (n = 111). In contrast to observations reported by Espericueta-Viera (2012), L. yebabuenae was found to present the same behavior in spring as that reported by the authors in November, although no offspring were reported. According to Ceballos et al. (1997), it seems to be two reproductive populations of L. yebabuenae in Mexico; one that gives birth in spring (February-May) and another in winter (November-January). Therefore, the reproductive population of Cacaxtla could be different from that found in the Sierra Navachiste.
Abundance
The relative and general abundance varied greatly throughout the year. This is probably due to bats undertaking migrations due to climatic factors, food availability and reproductive needs. In Mexico, at least 25 of the 140 species exhibit migrational behavior (Medellín et al., 2008). We captured one migratory species in the Sierra de Navachiste: L. yerbabuenae and one regional seasonal migratory species: M. megalophylla (Schmidly & Bradley, 2021). Yearly abundance varied with M. megalophylla, absent in summer due to regional movements. On the other hand, L. yerbabuenae was collected in the four seasons, although its abundance varied depending on the season. The population structure of this species changed drastically showing variations in the proportion of sexes and ages, as well as different physiological stages. This may be due to the migratory habit and the behavior of the species since the females form maternity caves where they give birth and nurse the young and juveniles, while the males inhabit other refuges (Haywar & Cockrum, 1971). Therefore, in the summer and autumn samplings, males with scrotal testes were captured and the sex ratio (males / females) was 1.09 and 3, respectively. In contrast in the winter, gestating females were captured, and in spring the proportion of lactating females and juveniles was 0.13 and 0.09, respectively.
Studies on the species L. yerbabuenae commonly focus on northern regions of Mexico, from upper Sonora to the United States of America, where large refuges have been registered (Cole & Wilson, 2006). However, geographic gaps exist in our knowledge of bat abundance, as highlighted by the case of Sinaloa. Other regions to the south also have records of L. yerbabuenae populations. For example, L. yerbabuenae is present year-round on the "Don Panchito" island in Jalisco (Stoner et al., 2003). Although the population varied in abundance, autumn and winter were the seasons with the largest number of individuals, while spring and summer had the lowest abundance of L. yerbabuenae. This contrasts with our findings from Sierra Navachiste, where the greatest abundance was in spring and summer. This reflects the migratory habits of this species with “Cerro de Arena” cave being a destination not just a stop off point during migration of bats from southern regions moving north. That said, further studies are needed on the migration and distribution of L. yerbabuenae in Mexico.
The species M. californicus and P. personatus were present in all four seasons. In contrast, B. plicata was not captured in summer or winter. The total abundance for B. plicata was just three individuals. According with Berry et al. (2004), the insectivorous bats have a high efficiency in the detection of mist nets and harp traps, which often leads to their absence on species lists. Based on this characteristic and the fact that M. californicus and P. psilotis had a higher abundance despite being insectivores, we can infer that the population of these species is higher within the cave, while B. plicata is found in a lower proportion.
The study area presented climatic temporality with a rainy season in summer followed by a pronounced dry season in winter, that influences the growth of the plants (Saturnino-Díaz, 2008). Ceballos et al. (1997) and Chávez & Ceballos (2001) reported that these conditions affect the structure of the faunal communities. This was clearly observed through seasonal and temporal changes in bat community diversity.
The dry season presented a greater abundance; however, this result was influenced by the spring sampling in which 135 polinivorous bats were captured, of which 111 were juveniles and 24 adults. This high number of captured organisms coincides with peak flowering of many regional cacti species which provide higher nectar availability in relation to regions of lower latitudes during the dry season (Fleming et al., 2001). Although polinivorous species were most abundant during the dry season this shifted towards insectivorous species during the rainy season when they increased by 63% (114 organisms) compared to the summer and autumn dry season (70 organisms). This is a result of the increased abundance of insects during the rainy season due to increased plant growth and therefore food availability (Marco, 2001).
Conclusion
This is the first study on bat ecology undertaken at the Sierra de Navachiste in which three families and five species were identified: Emballonuridae (B. plicata), Mormoopidae (M. megalophylla and P. psilotis) and Phyllostomidae (L. yerbabuenae and M. californicus). The identified species were divided into three trophic guilds: gleaning insectivores, aerial insectivores and pollinivores. The diversity of bats in the "Cerro de Arena" cave varied throughout the year. This variation was influenced by climatic seasonality and the presence of one migratory species such as L. yerbabuenae and one species with regional movements such as M. megalophylla.
The study area has a breeding population of the species L. yerbabuenae, which is listed on the Mexican red list (NOM-059-SEMARNAT-2010) with the status of Special protection and in the IUCN red list as vulnerable. It is a keystone within the ecosystem due to its function as pollinator of the dominant columnar cacti as well as a disperser of its seeds though fruit consumption. This activity promotes the spreading of these plants and maintains the structure and health of the ecosystem.
Due to the importance of the Sierra Navachiste as a refuge for at least five bat species, including one migratory and protected species, it is necessary to establish a management plan in order to protect the chiroptera community that depends on it.
