Raptor Visitation to Natural and Artificial Water Sources in a Tropical Forest in Southern Mexico
ABSTRACT
Wildlife rely on water sources to meet their metabolic needs. As climate change alters precipitation patterns and increases temperatures, it is important to establish baseline data for the visits of key species to natural and artificial water sources to inform management planning. In this study, we compared the visit rates, species composition, and dissimilarity of raptors visiting natural and artificial water sources in Calakmul, Mexico. We set up cameras at 10 waterholes (locally called aguadas), 10 cavities in smaller rocks (sartenejas), and 10 artificial drinking troughs. We collected 4308 photographs documenting 13 resident species (primarily Accipitriformes [eight species]) visiting these water sources. Ten species visiting water sources are classified as globally declining. Natural water sources, which included waterholes and sartenejas, each attracted visits from nine species, while drinking troughs were frequented by seven species. We found a high species composition dissimilarity between sartenejas and drinking troughs (54%), followed by an intermediate dissimilarity between waterholes and sartenejas (50%), and the lowest dissimilarity between waterholes and drinking troughs (40%). Species turnover primarily caused the dissimilarity between waterholes and sartenejas, accounting for 20%. We found a high turnover between waterholes and drinking troughs (36%). Daily maximum air temperatures and the presence of drinking troughs were the best predictors of the number of raptor visits to water sources. As maximum temperature increased, visits by raptors to drinking troughs increased 4.5-fold and visits to sartenejas increased 4-fold. This study underscores the importance of conserving natural water bodies and the significance of drinking water management to support the presence of raptors in Calakmul.
RESUMEN
VISITAS DE AVES RAPACES A FUENTES DE AGUA NATURALES Y ARTIFICIALES EN UN BOSQUE TROPICAL DEL SUR DE MÉXICO
La fauna silvestre depende de fuentes de agua para satisfacer sus necesidades metabólicas. A medida que el cambio climático altera los patrones de precipitación y aumenta las temperaturas, es esencial establecer una serie de datos de referencia para las visitas de especies clave a fuentes de agua naturales y artificiales para informar así de medidas de gestión. En este estudio, comparamos las tasas de visitas, la composición de especies y la disimilitud de las aves rapaces que visitan fuentes de agua naturales y artificiales en Calakmul, México. Instalamos cámaras en 10 puntos de agua (localmente conocidos como “aguadas”), 10 en cavidades con agua en pequeñas rocas (“sartenejas”) y 10 en bebederos artificiales. Correlacionamos las tasas de visita con la temporada y con información meteorológica. Recopilamos 4308 fotografías que documentan visitas de 13 especies residentes a estas fuentes de agua, principalmente Accipitriformes (8 especies). Diez especies que visitan fuentes de agua están clasificadas como en declive global. Las fuentes naturales de agua, incluyendo aguadas y sartenejas, atrajeron ambas la visita de 9 especies, mientras que los bebederos fueron frecuentados por 7 especies. La disimilitud en la composición de especies fue mayor entre sartenejas y bebederos artificiales (54%), seguida de una disimilitud intermedia entre aguadas y sartenejas (50%), y la disimilitud más baja fue observada entre aguadas y bebederos (40%). La disimilitud entre bebederos y sartenejas se debió principalmente al recambio de especies, que representó el 20%. Hubo un alto recambio entre aguadas y bebederos (36%). Las temperaturas máximas del aire y la presencia de bebederos fueron los mejores predictores de las visitas de aves de presa a las fuentes de agua. A medida que aumentó la temperatura máxima, las visitas de aves rapaces aumentaron 4.5 veces a los bebederos y 4 veces a las sartenejas. Este estudio muestra la importancia de conservar los cuerpos de agua naturales y la importancia del manejo del agua para apoyar la presencia de aves rapaces en Calakmul.
[Traducción de los autores editada]
INTRODUCTION
Water is a limiting resource for wildlife and is essential for maintaining hydric balance and supporting physiological processes (Dayton 2019). Endothermic species have evolved behavioral and metabolic adaptations to cope with water. These adaptations include avoiding activity during the hottest times of the day, obtaining water from food, heterothermy (body temperature fluctuations), utilizing cooling systems mechanisms in neuronal organs (Davies 1982, Fuller et al. 2014), hyperthermy, and minimizing evaporative water loss through enhanced skin resistance to water vapor diffusion (Williams et al. 2005).
Raptors use water bodies for various purposes, such as for foraging (Whitacre and Burnham 2012), bathing and drinking (Cade 1965, Beck et al. 1973, O’Brien et al. 2006, Boal et al. 2023), and congregating for social interactions and thermoregulation (Reyes Martínez 2008). As patterns of precipitation and temperatures become irregular and extreme due to climate change (Alexander 2016), wildlife managers sometimes place water troughs to mitigate hydric stress of wildlife (Krag et al. 2023, Contreras-Moreno et al. 2024). However, the patterns of use of natural and artificial water sources by raptors throughout the Neotropics have not been identified (Whitacre and Burnham 2012).
The Neotropics harbor a remarkable diversity of raptors on a global scale. A substantial number of these species face significant threats, with an estimated 25% classified as endangered and approximately 80% experiencing population declines (Sarasola et al. 2018). Habitat loss emerges as a principal threat to these species, with few areas that retain sufficient cover to sustain viable populations. Notably, the expansive massif of the Mayan Forest, situated in the states of Campeche and Quintana Roo in southern Mexico, represents one such area. Here, raptors find refuge in protected natural spaces such as the Calakmul Biosphere Reserve (CBR).
The CBR is characterized by the absence of a surface water network capable of providing water to wildlife (García Gil et al. 2002). In this region, wildlife relies on two primary types of water bodies: waterholes (locally called aguadas) and cavities in rocks (locally called sartenejas). Waterholes are shallow lagoons with impermeable soil that collect water during the rainy season. They vary in size, ranging from 100 m2 to several hectares, but most are relatively small (<1 ha; García Gil et al. 2002). On the other hand, sartenejas are cavities in smaller rocks (<10 m2) that retain water, with a mean capacity of less than 100 liters (Delgado-Martínez et al. 2018). Reyna-Hurtado et al. (2010) estimated the density of waterholes at one per 10.5 km2, and García Gil et al. (2002) and O’Farrill et al. (2014) identified 187 large waterholes (>700 m2) in the CBR that persisted up to the dry season. However, the number of waterholes varies by season and year; during severe drought years, even large waterholes (90,000 m2) can be completely void of water (O’Farrill et al. 2014). In addition, to mitigate hydric stress in wildlife, 10 drinking troughs were created in 2017 (Contreras-Moreno et al. 2024). These troughs were elongated PVC receptacles with rounded and widened extremes (bone-shaped) with a 300-liter capacity (Rotoplas®, Mexico City, Mexico).
In the last few decades, the region experienced a decrease in both annual and seasonal precipitation, resulting in an increased frequency of droughts. This impact is particularly notable in the northern part of the CBR due to a high incidence of anomalies and a 10 mm decrease in rainfall compared to previous decades (Márdero et al. 2014, 2020). A deficiency in water resources can influence the behavior and ecology of raptors and other wildlife (Reyna-Hurtado et al. 2022). For example, natural water bodies are an important characteristic of commonly used roost sites for King Vultures (Sarcoramphus papa), whereas occasional and abandoned roost sites are typically located far from water bodies or in desiccated sites (Reyes Martínez 2008).
Rates of wildlife visitation to water sources are positively correlated to ambient temperatures in multiple studies (Gaudioso Lacasa et al. 2010, Abdu et al. 2018a, 2018b, Votto et al. 2020). In the CBR, Delgado-Martínez et al. (2018) and Reyna-Hurtado et al. (2022) documented the significance of natural and artificial water sources for wildlife; however, raptors were not included in the scope of those studies. Because management efforts in the CBR have provided artificial water sources for wildlife, we sought to compare artificial and natural water sources in terms of visitation rates and species composition. We hypothesized that ambient temperature would significantly influence visitation of raptors to artificial water sources, particularly during the dry season, when natural water availability declines. Our results offer novel insights into the visitation patterns of raptors to three types of water sources in the CBR.
METHODS
Study Area
The Calakmul Biosphere Reserve is located in the State of Campeche, southern Mexico (19°15′17″N, 90°10′89″W). This region encompasses the largest conserved rainforest nationwide, spanning 7232 km2, and is part of the biogeographic province of the Yucatán Peninsula (Morrone et al. 2002). The dominant vegetation types are rainforest, medium sub-deciduous forests, and low sub-deciduous forests (Martínez-Kú et al. 2008). In the CBR, 203 species of vascular plants have been identified (Gutiérrez-Báez et al. 2022). Additionally, 403 bird species occur in the CBR (González-Jaramillo et al. 2016), of which 50 species are raptors: four species of Cathartiformes, 29 species of Accipitriformes, eight species of Strigiformes, and nine species of Falconiformes.
In the CBR, a warm and subhumid climate prevails, marked by an average annual temperature of 24.6°C and a mean annual precipitation 300–900 mm, with the highest humidity occurring at low latitudes (Márdero et al. 2020). The climate exhibits pronounced seasonality, with the dry season from November to April and the rainy season from May to October (Vargas‐Contreras et al. 2009, Márdero et al. 2020).
Data Collection
We deployed camera-trap stations strategically positioned at various water sources across the CBR, according to five guidelines: 3–5 m from the water sources; securely fixed to trees or stakes at a height ranging from 30 to 50 cm above the ground; no vegetation in front of the device; viewable area covering the waterbody completely (achieved for sartenejas and drinking troughs but not for waterholes); and devices oriented to south or north to avoid sun damage to the sensors. Specifically, we set camera traps at 30 locations: 10 at waterholes (2016–2021), 10 at drinking troughs (2019–2021), and 10 at sartenejas (2020–2021).
We used motion-triggered Bushnell Corporation camera traps (Overland Park, KS, USA) in 2016 and 2017, Cuddeback motion-triggered camera traps (Green Bay, WI, USA) in 2019 and 2020, and Bushnell Corporation and Browning Trail camera traps (Birmingham, AL, USA) in 2021. We programmed the cameras to capture photographs continuously over a 24-hr period, three photographs per event, with a 5-sec interval between successive photographs. To identify bird species, we used regional field guides (Howell and Webb 1995). For every photographic event, we recorded the number of photographs, camera-trap station, water body type, species, date, and time. We consulted the International Union for the Conservation of Nature (IUCN) Red List (www.iucn.org) to determine the global conservation status of bird species, and for the conservation status specific to Mexico, we used the NOM-059-SEMARNAT-2010 (Secretaría de Medio Ambiente y Recursos Naturales 2019).
Data Analysis.
We recorded the number of photographs and independent records for each species, as well as the number of species present at each water body type. Because some birds linger at water sources for extended periods, we defined independent records as photographs of the same species separated by a minimum interval of 1 hr.
To assess species dissimilarity across various water body sources, we used dissimilarity partitioning methods, following Calderón-Patrón and Moreno (2019). Specifically, we calculated βcc, β−3, and βrich in accordance with the methodology proposed by Podani and Schmera (2011): and βrich = | b – c |/a + b + c,where a is the number of species shared between sites, and b and c are the numbers of exclusive species. The first index is based on Jaccard dissimilarity; the second index measures species turnover (i.e., proportion of different number of species between samples), and the third index measures the difference in the number of species among sites (Calderón-Patrón and Moreno 2019).
We fitted multiple regression models to examine the relationship between the number of visits of birds of prey and the type of water source (waterholes, sartenejas, and drinking troughs), season (dry and rainy), and meteorological data (precipitation, and maximum and minimum temperatures). We calculated the visitation rate as the number of independent events divided by the sampling effort, multiplied by 1000. We downloaded weather data (daily precipitation, maximum and minimum temperature) from the Mexican Meteorological Service for the years 2016 to 2021 from the nearest climatological station Conhuas (https://smn.conagua.gob.mx). Because Conhuas did not have data available for 2019, we obtained data from Laguna Zoh, the second nearest climatological station to fill this gap.
We calculated the visitation rate of raptors in 30-d subsamples for each camera-trap station and divided it by the corresponding survey effort measured as the number of days a camera was operational in the 30-d period. For these subsamples, we also calculated the total precipitation, mean precipitation, mean maximum and minimum temperatures, and the standard deviation as a measure of variation. A Pearson correlation test revealed total precipitation, mean precipitation, and standard deviation of precipitation were highly correlated (r > 0.80; P < 0.05). Because the data from the camera trap stations were correlated and the number of subsamples varied in sampling effort, we used generalized estimating equations to examine the relationship between visit rate and single covariates (maximum temperature, type of water source, and season), as well as their interactions, which allowed for incorporation of cross-sectionally clustered data (Hardin 2005, Højsgaard et al. 2006, Pekár and Brabec 2018). Then we iteratively dropped the nonsignificant covariates from the model and applied a Wald test to compare differences in the models and submodels (Zuur et al. 2009, Højsgaard et al. 2006, R Core Team 2015). For these analyses, we used the geepack package in R (Højsgaard et al. 2006).
RESULTS
Most of the camera stations (n = 25) operated for 1 yr, two stations ran for 2 yr, two stations for 3 yr, and only one station operated for 5 yr. We collected images from 11,872 trap-days, of which 3505 trap-days were during the dry seasons (November–April) and 8367 trap-days were during the rainy season (May–October). The majoring of our sampling effort occurred at waterholes (6825 trap-days: 1982 trap-days in the dry season and 4843 trap-days in the rainy season), followed by drinking troughs (3040 trap-days: 1362 trap-days in the dry season and 1678 trap-days in the rainy season). We sampled sartenejas with lower intensity (2007 trap-days: 161 trap-days in the dry season and 1846 trap-days in the rainy season).
We obtained 4308 photographs of raptors at waterholes, sartenejas, and drinking troughs. Within this comprehensive dataset, we identified 411 independent records, representing 13 resident species from the orders Accipitriformes (8), Falconiformes (2), Cathartiformes (2), and Strigiformes (1; Table 1). Despite being categorized as having a low risk on the IUCN Red List, 10 of the species exhibit decreasing population trends. According to Mexican legislation, five species are under special protection, one species is classified as threatened, and three species are considered endangered (Table 1).
Camera-trap stations recorded birds of prey primarily between May and August (75%; rainy season); May alone accounted for one-quarter of the total records. Despite this seasonal concentration, visitation rates remained consistent across seasons (Fig. 1). The Roadside Hawk (Rupornis magnirostris) emerged as the predominant species in independent records (39.2%), followed by Mottled Owl (Strix virgata; 27.5%), Ornate Hawk-Eagle (Spizaetus ornatus; 12.4%), and Common Black Hawk (Buteogallus anthracinus; 9.7%). The Turkey Vulture (Cathartes aura), King Vulture, Gray-headed Kite (Leptodon cayanensis), Doubled-toothed Kite (Harpagus bidentatus), Crane Hawk (Geranospiza caerulescens), and Gray Hawk (Buteo plagiatus) occurred in very low numbers (≤3 independent events; Table 1).
Citation: Journal of Raptor Research 59, 2; 10.3356/jrr243
Nine species visited waterholes, with the Roadside Hawk (35.4%), the Ornate Hawk-Eagle (33.6%), and the Common Black Hawk (17.7%) exhibiting the highest frequencies of independent records. The Crane Hawk and the King Vulture occurred only at waterholes (Table 1; Fig. 2). Nine species frequented sartenejas, with the Roadside Hawk leading in independent records (48.9%), followed by the Mottled Owl (17.7%). We obtained records of the Gray Hawk, the Double-toothed Kite, and the Gray-headed Kite only at these water sources (Table 1; Fig. 2). Among the drinking troughs, we observed seven species, with the Mottled Owl (51.6%) being the most common, followed by the Roadside Hawk (33.1%). The Black Hawk-Eagle (Spizaetus tyrannus) was the only species exclusively observed at drinking troughs (Table 1, Fig. 2).
Citation: Journal of Raptor Research 59, 2; 10.3356/jrr243
We obtained a 40% dissimilarity between waterholes and drinking troughs, encompassing a 20% species turnover. Additionally, a 20% difference in the number of species contributed to the overall dissimilarity between these water sources. The dissimilarity between waterholes and sartenejas reached 50%, primarily driven by species turnover, as both exhibited an identical number of species along with an equal number of exclusive species. Lastly, the dissimilarity between drinking troughs and sartenejas reached 54%, with a notable 36% increase in species turnover, coupled with an 18% difference in the number of species between the two water sources.
We observed a high correlation (r = 0.72) in the visitation rates of raptors among camera-trap stations. Our modeling approach revealed that maximum temperature and drinking troughs were positively and significantly associated with visitation rates (β = 1.54, Wald = 19.15, P < 0.0001 and β = 1.41, Wald = 8.44, P = 0.003, respectively). Based on the odds ratio, we found a 4.5 times higher probability of increased raptor visits with rising temperatures, and a 4 times higher probability of visits to drinking troughs. At temperatures below 30°C, water sources had indistinguishable visitation rates. However, as temperatures increased, raptors visited drinking troughs at higher rates than waterholes. At a maximum temperature of 40°C, visitation rates differed significantly between drinking troughs and both types of natural water sources. Although waterholes exhibited a slight increase in visitation rates with rising temperatures, this trend was not statistically significant.
DISCUSSION
Our study provides the first documented evidence of raptors visiting both natural and artificial water sources in the Mayan Forest. We found 25% (13 species) of the raptor assemblage reported for the region visited these water resources (Whitacre and Burnham 2012, González-Jaramillo et al. 2016). Few studies have examined how raptors utilize water sources, with most reports focusing primarily on their use of drinking troughs. For example, in the North American deserts, nine raptor species (O’Brien et al. 2006) or 14 raptor species (Boal et al. 2023) visited drinking troughs. In the CBR, drinking troughs were used by seven of the 13 recorded raptors species, indicating that this behavior is common in both deserts and tropical forests.
Boal et al. (2023) attribute the patterns in raptor use of water sources to both local abundance and the species-specific tolerance to water stress. In our study, the Roadside Hawk was the common diurnal species at water sources, closely followed by the Ornate Hawk-Eagle and the Common Black Hawk. The Roadside Hawk is common in Mexico, particularly along natural forest edges such as riverbanks (Iñigo et al. 1989, Thiollay 1989, Anderson 2001, Mañosa et al. 2002, 2003). This adaptability allows the species to exploit openings such as forest edges, agricultural areas, and roads (Iñigo et al. 1989) and trails within the CBR, where the Roadside Hawk benefits from the availability of waterholes, sartenejas, and drinking troughs.
The Ornate Hawk-Eagle and the Black Hawk-Eagle appear sensitive to habitat degradation, as their populations have declined due to forest loss and fragmentation (De Labra and Escalante 2013). We recorded the Ornate Hawk-Eagle in similar numbers at both sartenejas and drinking troughs, but it was notably more frequent at waterholes, suggesting a preference for natural, larger water sources. On the other hand, we observed the Black Hawk-Eagle, a species considered rare in our study area, exclusively at drinking troughs on few occasions.
Despite their lower water capacity (average 100 liters) and reduced survey effort compared to water holes (>1000 liters) and water troughs (300 liters), sartenejas had similar visitation rates and species richness. Delgado-Martínez et al. (2018) highlighted the importance of sartenejas for wildlife, finding a higher number of mammal and bird species visiting these water sources compared to larger waterholes. Our findings suggest that the number of species and visits are not related to water source size and raptors show a possible preference for sartenejas. Because sartenejas are located in smaller forest openings than water holes, forest specialists, such as kites, may prefer sartenejas for maintaining hydric balance. These findings emphasize the importance of sartenejas as the primary source of water for wildlife that prefer closed canopy forests (Delgado-Martínez et al. 2018), and water holes and drinking troughs for generalist species that are more tolerant to habitat degradation.
We found that trends in raptors’ use of water sources were related to maximum temperature and the presence of drinking troughs. These results align with findings from the Kalahari Desert, where temperature also emerged as a significant variable for granivorous, omnivorous, insectivorous (including raptors), and frugivorous birds (Smit et al. 2017). These birds were observed visiting natural water sources more frequently as temperature increased (Smit et al. 2017). We found that the use of drinking troughs, in relation to maximum temperature, was significantly higher than the use of natural water sources. Natural water sources are replenished by rainfall during the rainy season, but at lower precipitation rates and higher temperatures, they desiccate quickly, forcing birds to resort to artificial sources. Birds may perceive these artificial sources as a reliable water supply during the hottest periods, increasing their visits to drinking troughs regardless of the season. In summary, our study provides baseline information for monitoring both artificial and natural water sources using camera traps for recording rare and threatened raptors. The evidence we present underscores that installing drinking troughs serves as a viable strategy to compensate for the absence of natural water sources and thus contributes to the conservation of Neotropic raptors (McClure and Rolek 2020).
Overall visit rates of birds of prey to natural (water holes and sartenejas) and artificial water sources among seasons in Calakmul Reserve Biosphere, Mexico.
Visit rates of birds of prey to water sources in Calakmul Reserve Biosphere, Mexico. Species: Turkey Vulture (TV), King Vulture (KV), Gray-headed Kite (GK), Black Hawk-Eagle (BH), Ornate Hawk-Eagle (OHE), Double-toothed Kite (DT), Crane Hawk (CH), Common Black Hawk(CBH), Roadside Hawk (RH), Gray Hawk (GH), Mottled Owl (MO), Barred Forest-Falcon (BFF), and Collared Forest-Falcon (CFF).
Contributor Notes
Associate Editor: Vincent Slabe