Birds of Game Abundances in Evergreen Forests in Calakmul Biosphere Reserve, Campeche, Mexico

Simple Summary

The larger species are the most threatened due to human consumption. The objective of this study was to know the populations of three species of birds of hunting importance in the southern zone of the Calakmul Biosphere Reserve, Campeche. Species presence data were collected and analyzed with Principal Component Analysis and ANOSIM to relate abundances to vegetation types and seasons of the year. The results showed a higher abundance in the high sub-evergreen forest. This study provides relevant information on game bird populations in the southern region of Calakmul, which is currently little explored, so constant monitoring of these species throughout the CBR is necessary.

Abstract

The Calakmul Biosphere Reserve (CBR) is in the south of the Yucatán Peninsula and is known for its great biological diversity. However, despite the great diversity of species, they are under intense pressure from hunting activities, especially the larger ones that can be used for human food. Therefore, the objective of this study was to obtain knowledge about the hunting importance of populations of three species of birds (Crax rubra, Meleagris ocellata, and Penelope purpurascens) in the southern zone of the Calakmul Biosphere Reserve, Campeche. Sampling was conducted with transects where a total of 46 camera traps were installed from November 2021 to November 2022, distributed in two types of vegetation. Likewise, data on species presence were collected and analyzed with Principal Component Analysis and ANOSIM (ANOSIM; R = 0.10, p = 0.22) to relate abundances with vegetation types and seasons of the year. No significant differences were found between the two vegetation types. This study provides relevant information on the populations of game birds in the southern region of Calakmul, which is currently little explored, and constant monitoring of these species throughout the CBR is necessary.

1. Introduction

The Yucatán Peninsula is known for its diversity of bird species, making it one of the areas in Mexico where it is possible to find a rich variety of species [1,2]. Its importance in bird conservation is recognized due to the presence of eighteen important bird conservation areas, twenty-four natural protected areas, and three Mesoamerican biological corridors [3].

One of its NPAs is the Calakmul Biosphere Reserve, which is part of the southern–southeastern region of the Yucatán Peninsula, covering a total of approximately 723,185.12 hectares [4]. At present, it has reported a total of 403 bird species, which are distributed in 21 orders, 65 families, 37 subfamilies, and 256 genders, with the orders Passeriformes and Accipitriformes being the most abundant in biodiversity [5]. Despite the importance of this area, there is strong pressure from hunting activities of birds that are larger in size and can be used for different types of purposes by humans.

This family consumes fruits and berries, making them important seed dispersers [6,7,8]. Some species within this family have restricted distributions and inhabit diverse habitats. Among the species used for subsistence are Crax rubra (Great Curassow) and the Penelope purpurascens (Crested Guan). Additionally, another species from a different family, the Phasianidae, is the Meleagris ocellata (Ocellated Turkey), which is distributed across the entire Yucatan Peninsula, and in Campeche are located the largest populations of this species in the region [9].

Also, it is one of the major species used for subsistence in the Calakmul region [10,11]. These three species are significantly impacted by factors such as habitat destruction and hunting overexploitation [12]. However, in Mexico, they are categorized as “Threatened” under NOM-059 [13]. According to the IUCN Red List, C. rubra is classified as Vulnerable (VU), while P. purpurascens and M. ocellata are listed as Near Threatened (NT) [14,15].

Nevertheless, the CBR is an area with many scientific studies of different faunal groups such as vertebrates, including birds. The southern region, particularly the tropical rainforest near the Mayan Biosphere Reserve in Guatemala, contains unexplored sites, where no data on game birds are recorded, specifically in vegetation types such as high and medium sub-evergreen forests. One of the limitations is access to these areas. Therefore, the objective of this work was to obtain knowledge about the populations of hunting birds in the southern zone of the Calakmul Biosphere Reserve, Campeche, to provide more information on how their populations are in some areas and the vegetation types of the CBR.

2. Materials and Methods

2.1. Study Area

The Calakmul Biosphere Reserve (CBR) is in the southern portion of the Yucatán Peninsula (PY) and is part of the Greater Calakmul Region that includes the Maya Biosphere Reserve in Guatemala and the Río Bravo Dos Milpas conservation area in Belize [4]. The CBR has a warm and sub-humid climate (Aw), with a mean annual temperature of 24.6 °C. Its altitude ranges from 100 to 390 MSNM, and annual precipitation varies from 500 to 2500 mm [16]. The dominant vegetation types in the region are medium sub-evergreen forests, medium sub-deciduous forests, and low sub-deciduous forests [17,18].

2.2. Camera Trap Monitoring

From November 2021 to November 2022, a total of 46 digital camera traps were installed. Bushnell (Trophy Cam; Outdoor Operations LLC., Los Angeles, CA, USA), Browning (Strike force; Browning Trail Cameras, Birmingham, AL, USA) and Cuddeback (Cuddeback IR; Non-Typical Inc., De Pere, WI, USA) digital camera models were used, which were placed in sub-evergreen high forests and sub-evergreen medium forests south of the CBR, bordering the northern zone of the Maya Biosphere Reserve in Guatemala (Figure 1). These cameras were distributed along linear transects with a minimum distance of 2 km between each camera; a total of 92 km of transects were covered on roads and trails (60 km in the medium sub-evergreen forests and 32 in the medium sub-deciduous forests) [19,20]. The cameras were fixed 50 cm above the ground in trees adjacent to logging roads and lightly traveled trails. The cameras were set to capture photographs every 5 s for 24 h.

After the cameras were installed, they were reviewed over a period of four weeks, where the captured photographs were downloaded and a registration code was made for their location. Species identification was conducted manually, generating a database in CSV format, which contains data such as station, camera name, date, time, species, name, image, and number of individuals. At the end of the photographic data capture, a database was constructed with these data using the CamtrapR interface in Rstudio software 12.0 [21].

2.3. Data Analysis

To identify the hours of greatest presence of the species during the day, a chord diagram was made with the total abundances of each species, this diagram was made in Origin Pro10.0.5.157 software [22]. To identify gradients (eigenvectors) formed by the variables (habitat characteristics), Principal Component Analysis (PCA) was performed, in which the variables describing the habitat of the species were included and used to discriminate between sites potentially usable by the species studied, those for which the data indicating the presence of the species of interest were confirmed (presences). The PCA was performed with standardized variables (temperature, precipitation, humidity, wind, and NVDI) due to the difference in scales and units in which the variables were presented [23].

The variables used for habitat characteristics were temperature, wind, humidity, precipitation, and NDVI (Normalized Difference Vegetation Index). The data were obtained using the Land Viewer platform and its interface Crop Monitoring: Satellite-Based Software for Agricultural Needs, with the creation of polygons in the sampled areas and data obtained on the day of sampling. To know if there are significant differences between species abundances and vegetation types, a one-way ANOSIM was performed in PAST software version 4.12 [24]. Finally, to schematize the abundances of the 16 different camera trap stations installed in the southern zone of the CBR, the Clustering command in ArcGIS Pro software Ver 3.0.2 was used. The application of these clusters can be useful to know the areas where the species are more frequent.

3. Results

During dry seasons, the species showed greater activity (abundances) between 06:00 and 08:00 h, while in the rainy season they tended to have more activity at 06:00 h and during nortes at 8:00 h. The hours with the least activity were between 13:00 and 14:00 h during the nortes season (Figure 2a). The dry season showed a greater presence of the species, where M. ocellata had a higher frequency than in the rainy and northerly seasons, while C. rubra had a greater number of records during the rainy season (Figure 2b). Regarding the abundances in the seasons of the year, it was found that there was greater activity of individuals during the dry season with 336 records, followed by the rains with 267 and nortes with 76.

The abundances of the three examined species were higher in the high sub-evergreen forest (n = 477;

Table 1. Abundance of species of birds in the different types of vegetation with means and standard error.

Species	Evergreen Forest	Medium Stature Tropical Forest	Abundances	Mean ± Standard Error
Crax rubra	308	49	357	22.31 ± 5.98
Meleagris ocellata	163	140	303	18.93 ± 7.19
Penelope purpurascens	6	0	6	0.37 ± 0.15

), while in the medium sub-evergreen forest a total of 189 records were obtained. However, no significant differences were found between the abundances reported in the two vegetation types (ANOSIM; R = 0.10, p = 0.22). A highly significant difference in abundances was found between the three seasons (ANOSIM; R = 156, p = 0.009).

In the PCA, the first three components added up to an accumulated variance of 65.7%. Principal Component 1 showed a variance of 29.2, where the most influential variables were humidity and precipitation, positive and negative, respectively, showing negative values for the presence of C. rubra. On the other hand, in PCA2, temperature and wind were the most influential variables, both positive, showing positive values for the presence of M. ocellata. Finally, in PCA3, the variable with the greatest weight was NDVI, showing a positive association with the presence of P. purpurascens (Figure 3). The mapping generated with the buffers of species presence shows that some stations such as BUSHWWF-24 (n = 131) and BUSHWWF-N03 (137) were each distributed in a different vegetation type (Figure 4 and Figure 5).

4. Discussion

This research is one of the first studies to evaluate the populations of birds of hunting interest in the southern Yucatan Peninsula. The high sub-evergreen forest showed higher abundances of cracids, coinciding with several authors who mentioned that species such as P. purpurascens and C. rubra prefer to inhabit conserved and dense forests that do not have significant levels of disturbance (Figure 5) [25]. In this sense, it has been observed that C. rubra can move to areas with lower levels of disturbance where it finds available nesting sites such as tall trees [26].

The significant differences in the different seasons where a greater abundance of M. ocellata was found compared to the rainy and northerly seasons may be because this species tends to begin its reproductive period during February and concludes in May. This species modifies its diet according to the seasons of the year due to its reproductive needs (spring) when food resources are abundant. Regarding its population density by hour, it was found that it presents higher densities in the mornings and afternoons, coinciding with [27], who mention that it is a highly active bird during the early hours of the day, walking on established trails and paths.

In the buffers generated by the abundances in the seasons, it was found that there was a greater abundance in the medium sub-evergreen forest and the low flooded forest. Prior to the breeding season, it has been reported that M. ocellata tends to consume small snails found in lowland flooded forests or in the transition of this vegetation type with the medium forest [28].

Although there should be no hunting pressure in the southern zone (hunt evidence), there is occasional evidence of hunters transiting the area where the three bird species are among the main hunting prey (Contreras-Moreno Comps. Pers.). All three species face high hunting pressure in the region (Figure 6 [29,30]). Therefore, the population abundances of these species are negatively affected [31]. Additionally, it has been observed that hunting pressure can reduce their populations, forcing them to seek more conserved protected sites [32]. However, it has been observed that the species uses more conserved forests when hunting is present [33], since it is considered that greater abundance reflects greater hunting pressure in the areas where it lives, since it is synonymous with the availability of food for hunters [26]. It has been mentioned that M. ocellata populations have declined over time due to subsistence hunting, but also due to habitat degradation because of its low reproductive rate in the wild and its limited distribution range [27,34]. Another cause related to the overexploitation of species such as cracids has been correlated with the size and proximity of the human population, where population declines have been predicted in areas of central Mexico [35].

The populations evaluated are of conservation importance due to their role as seed dispersers. In Petén, Guatemala, it has been reported that the Great Curassow feeds on 44 different plant species [36]. Other authors have even found a diversity of 74 species of seeds consumed (70% seeds and 7% fruits) [26]. Balam-Castro et al. [27] report that for the diet evaluated in ocellated turkeys in three municipalities of Yucatan, 40% of their diet comes from wild species, some of which can also be found in the medium-sized forests of the southern region of the Yucatan Peninsula, such as chicozapote (Manilkara zapota), ramón (Brosimun alicastrum), and ciricote (Cordia dodecandra). Studies that evaluated samples of birds collected throughout Guatemala and Campeche found 72 plant species consumed by the Cojolita (P. purpurascens), where 79% of the weight was dominated by seeds [26].

Regarding activity patterns, it has been recorded that, to avoid the hottest hours of the day, Galliformes seek suitable microclimatic conditions that can function as temporary shelters [37], showing activity in the early morning hours and at dawn [38]. This activity pattern coincides with another study conducted in a tropical rainforest in southern Mexico, where Pérez-Irineo and Santos-Moreno [39] found that the activity of C. rubra showed a main peak after dawn (06:00–10:00 h), decreasing at midday, and increasing around 18:00 h. A similar pattern was observed for C. rubra in northern Costa Rica, where the main peaks were at dawn (06:00–08:00) and in the afternoon (16:00 h) [40].

Regarding the habitat descriptor variables, humidity and precipitation were those that represented the strongest association in Principal Component 1, and could be explained from the context of the characteristics of the region. In Calakmul, its karst soil surface water is not very available, so there are only of three types of semi-permanent water sources for wildlife during the dry season: small ponds scattered in the jungle, known locally as “aguadas” [16]; open crevices in the rocky soil, known locally as “sartenejas” [41]; and a type of arboreal water container (alcorques filled with water; [42]). Since Calakmul is a region of extensive droughts and high temperatures, birds are more present in sites where humidity conditions are more accentuated, since a higher local humidity would indicate a greater number of aguadas and nearby water sources.

This study represents an insight into the populations of the three bird species in the southern CBR. It is necessary that research on birds in the Calakmul region consider it a priority to determine the population status of the species listed in NOM-059-SEMARNAT-2010, as well as the effects of hunting on game species. It is necessary to accurately establish the reproduction and phenology of the species. Given the current pressures on biodiversity exacerbated by the impacts of global climate change, it will be necessary to delve deeper into how birds use resources at the local scale. The CBR represents an important bastion for the conservation of game bird species, where C. rubra and M. ocellata in particular can maintain viable population abundances [30,43]. However, the mean abundances of M. ocellata in the study of [43] in 1998–2000 were higher than that of the present study, with 3.2 ind/km² (18.93 ± 7.19).

5. Conclusions

This is one of the first investigations to evaluate the populations of birds of hunting interest in the southern Yucatán Peninsula. The various vegetation types are occupied by the species studied, where the sub-evergreen high forest showed higher abundances of cracids.

The climatic seasons influence the abundance of the species due to the phenology of the species. The three species maintain a diurnal activity that could be influenced by hunting pressure from natural predators and humans. Humidity and precipitation showed the greatest influence on the abundance of the cracid species.

It is necessary to precisely establish the breeding seasons and phenology of the species. In the face of current pressures on biodiversity exacerbated by the impacts of global climate change, it will be necessary to delve deeper into how birds use resources on a local scale.