Charadrahyla taeniopus
Creators: name: Cruz-Elizalde, Raciel
name: Magno-Benítez, Itzel
name: Berriozabal-Islas, Christian
name: Ortíz-Pulido, Raúl
name: Ramírez-Bautista, Aurelio
name: Hernández-Austria, Raquel
Publisher: name: Zenodo
Year: 2020
Subjects: Biodiversity
Taxonomy
Animalia
Chordata
Amphibia
Anura
Hylidae
Charadrahyla
Charadrahyla taeniopus

description: Areas of Occupation and Exchange Rates of Climate Availability
The distribution of C. taeniopus was restricted to cloud forests in the central region of the Sierra Madre Oriental (Fig. 2A–C) in the states of Hidalgo, Puebla, Veracruz, and the northern portion of Oaxaca, Mexico. The analysis of habitat occupancy under current conditions and in the future (to 2050 and 2070), showed a general loss of climatic niche in much of the range of C. taeniopus. This loss occurred in temperate areas, where the current area of occupation (18,262.23 km 2) will decrease to 15,678.45 km 2 by 2050, which represents a habitat availability decrease of 14.14% (Fig. 2B); and to an area of 11,032.93 km 2 by the year 2070, which represents a habitat availability decrease of 37.08% (Fig. 2C).
Diet
Fourteen taxa were identified in the stomachs, with 11 taxa present in both males and females (Table 1). The most important prey categories, according to the values of food importance for the species and for each sex, were orthopterans, plant material (leaves), and ants (Table 1). The overlap in diet between the sexes was high (O jk = 0.822; 63.21–100%), with males presenting a slightly higher value (B = 0.526) of diet niche breadth than females (B = 0.504).
Reproduction
The mean number of eggs was 722 ± 277.53 (range 426– 1,138, n = 11). There was no correlation between female SVL and either number of eggs (r s = 0.09, P = 0.79, n = 11) or egg mass in females (r s = 0.09, P = 0.79, n = 11). There were no differences among weights, lengths, widths, or volumes of the testes (P> 0.05 in all cases). The average weight, length, width, and volume of the right testis was 0.198 g, 14.78 mm, 6.05 mm, and 305.57 mm 3, respectively; and for the left testis the averages were 0.204 g, 14.63 mm, 6.0 mm, and 293.25 mm 3, respectively. There was no correlation between SVL and testicular volume (r s = 0.31, P = 0.17, n = 20), but there was a positive correlation between SVL and testicular mass in males (r s = 0.49, P = 0.02, n = 20).
Morphology
Five of the 15 characteristics measured exhibited sexual dimorphism, with females higher than males in SVL, IOD, HW, JL, and JW (Table 2). Females (mean SVL = 63.94 ± 2.35 mm; range 45.27–74.31, n = 11) were larger than males (mean SVL = 59.70 ± 1.09 mm, range 52.90–71.05, n = 20; U = 60, P = 0.04).
Conservation Status
Charadrahyla taeniopus is listed in conservation standards (DOF 2010; IUCN 2019) as being in high risk categories. According to the Mexican Standard NOM-059-SEMARNAT-2010 (DOF 2010), the species is considered to be Threatened. The IUCN Red List of Threatened Species places the species in the Vulnerable category, with a distributional area less than 20,000 km 2 in fragmented environments and with declining populations (status B1ab[iii]; IUCN 2019). In the EVS, it was classified as a medium environmental vulnerability species, with a value of 13 points. This EVS category was calculated from: (i) its distribution in Mexico, but not exclusive to the type locality (5 points), (ii) its occurrence in two vegetation types (pine-oak and cloud forest, 7 points), and (iii) a reproductive mode with egg laying in lentic or lotic water bodies (1 point; Wilson et al. 2013).
Discussion
Conserving native populations of tree frogs at a local scale requires information on their ecological distribution, feeding habits, reproduction, and morphology (Delia et al. 2013; Toledo et al. 2014). The analyses reported here suggestthatthedistributionof C.taeniopus willpotentially decrease during the next 50 years. Microhabitats in currently occupied habitats (montane environments) are subject to change because of temperature and moisture shifts, and also because of changes in vegetation cover associated with high deforestation rates (Kaplan and Heimes 2015) and potential climate change, including shifts in temperature and moisture (Ponce-Reyes et al. 2012). For example, several authors including Pineda and Halffter (2004), Pineda et al. (2005), and Murrieta-Galindo et al. (2013), have suggested that the existence of abundant vegetation and native shrub cover provide appropriate humidity and temperature conditions for the permanence of hylid frogs in temperate environments such as cloud forests. If the abiotic and biotic conditions change in the forests inhabited by C. taeniopus, this species could be negatively affected. Loss of climatic niche in our models is consistent with that reported by Roxburgh et al. (2004). These authors mentioned that the expected changes could generate ecological scenarios that will delimit the overall distribution of arboreal species from cloud forests (Roxburgh et al. 2004; Pineda et al. 2005), and therefore could affect their associations with their environment (Urbina-Cardona and Flores-Villela 2010; Ponce-Reyes et al. 2012).
In addition to the above considerations, the thermal tolerances of anurans in high elevation or low temperature environments can determine the presence and distribution of their populations (Wells 2007). The hylid frogs are an example of this, as their limits of distribution are in high latitude regions such as the arid and semi-arid climates of northern Mexico (Wiens et al. 2006). This may be the result of the thermal tolerances that hylid species show in temperate environments, which are different from those of species that occur in tropical environments (Navas 2006; Wells 2007). To date, there are no studies of thermal tolerances or maximum/minimum temperature limits for C. taeniopus; therefore, it is very difficult to know the behavior of individuals and/or populations of this species in their distribution area. Future field studies, and in situ and laboratory experiments on thermal preferences are therefore necessary for this species. They could complement the results obtained in the potential distribution model of the species, enabling the analysis of variables that could be interacting to a greater degree with the biology of the organism, and improving determinations of the distribution range of the species (Gross and Price 2000; Wiens et al. 2006).
Ochoa-Ochoa et al. (2009), stated that in addition to the loss of vegetation, climate change is a determining factor in the loss of amphibian species in conserved environments, mainly in sites outside of natural protected areas (NPAs). The Sierra Madre Oriental Corridor occupies large areas of cloud forest, a type of environment that is highly threatened by the effects of climate change (Ponce-Reyes et al. 2012), and in which the known distribution of the species is not included in any NPA (IUCN 2019). This shows the importance of evaluating the distribution of highly vulnerable hylid frogs throughout the potential distribution range based on climatic niche models and climate change scenarios. The results are worrisome, because despite the fact that amphibian richness in Mexico is high (Johnson et al. 2015, 2017), more than 50% of the species are listed in high vulnerability categories by the IUCN (Delia et al. 2013; Caviedes-Solis et al. 2015; IUCN 2019; Johnson et al. 2017). For example, recent studies have found that some mountain hylid species have not been recorded over prolonged periods of time (Delia et al. 2013; Caviedes-Solis et al. 2015). Due to multiple factors, such as vegetation loss, pollution, and in particular climate change, populations of these species tend to occur in highly vulnerable sites (Lips et al. 2004; Stuart et al. 2004). Therefore, the species that inhabit this type of environment (cloud forest, pine-oak) are highly threatened (Ochoa-Ochoa et al. 2009; Caviedes-Solis et al. 2015).
Inadditiontohabitatfragmentationandclimatechange, the presence of the pathogenic fungus Batrachochytrium dendrobatidis Longcore, Pessier, and Nichols, 1999 (Bd) has contributed to amphibian population and species losses in Mexico (Mendoza-Almeralla et al. 2015, 2016) and other regions of the world (Lips et al. 2003; Fisher et al. 2009). However, Bd has not been detected thus far in C. taeniopus (Murrieta-Galindo et al. 2014; Hernández-Austria 2017). Therefore, further studies are needed to examine the potential presence of Bd in C. taeniopus populations through their distribution area (Hernández-Austria 2017).
The lack of information on the natural history of this species inhibits the development of strategies for its conservation (Toledo et al. 2014). The data presented here on diet provide valuable information on the basic ecology of C. taeniopus. The diet of this species consists of orthopterans, plant material, and ants, and there is a high degree of overlap in diet between the sexes. In C. taeniopus, plant material is the second most important food item. This is particularly notable since the diet of most anuran species in Mexico consists primarily of arthropods (Ramírez-Bautista and Lemos-Espinal 2004; Suazo-Ortuño et al. 2007), and the ingestion of plant material, such as leaves and flowers, is usually considered to be accidental (Evans and Lampo 1996). In the case of C. taeniopus, further studies are necessary to determine if consumption of plant material (leaves) is accidental or part of their diet, which would be unusual, but not unprecedented. For example, some species of tree frogs, such as Ptychohyla zophodes Campbell and Duellman, 2000 (Luría-Manzano 2012) and Xenohyla truncata (Izecksohn, 1959) do consume large quantities of plant material, and the latter (X. truncata) has been reported as entirely omnivorous, consuming fruits, seeds, and flowers (da Silva and Britto-Pereira 2006).
Egg number and the relative sizes of eggs vary greatly in amphibians (Vitt and Caldwell 2009), and they are often related to female body size (Jorgensen 1992; Hartmann et al. 2010). The data presented here show that egg number is not related to female body size in C. taeniopus. This may be due to the fact that its reproductive period may have a longer duration, and the sample size obtained from the collections only reflects the behavior of the females in the first part of the year (March-April), not in the entire reproductive period. Females with eggs were found throughout the year, and aggregations of individuals of both sexes and amplexus were observed in the field in August. This seasonal variation in the correlation between egg size and size of females has been reported for other anuran species such as Leptodactylus fuscus (Schneider, 1799), L. podicipinus (Cope, 1862), and Dendropsophus nanus (Boulenger, 1889) [Prado and Haddad 2005]. Furthermore, testicular mass, but not testicular volume, increases with larger SVL. These data suggest that larger males invest more energy in sperm production to have greater reproductive success (Byrne et al. 2002).
Most species of frogs (nearly 90%) are sexually dimorphic, with females being larger than males (Wells 2007), and C. taeniopus is no exception. The larger size of females compared to males is presumably associated with the potential to produce more eggs. However, no correlation was found between SVL of females and egg number. Another explanation for sexual size dimorphism could be differences in growth rates (Kupfer 2007), in which the growth rate of males is faster than that of females in order to reach sexual maturity at a smaller size and compete with other males for access to calling sites, thereby maximizing the number of matings (Kupfer 2007; Wells 2007). Also, considering the ecological hypothesis to explain the sexual dimorphism, the larger jaw size in females compared to the males might indicate a larger gape in females, which could allow for partitioning of food resources in terms of prey size (Luría-Manzano 2012). However, additional studies on microhabitat use, behavior, and reproduction are required before the ecological significance of the sexual dimorphism in C. taeniopus can be determined.
Based on the information about climatic niche, feeding habits, reproduction, and morphology, C. taeniopus is highly threatened because it is distributed in environments (i.e., cloud, oak, and pine-oak forests) that are currently being dismantled by fragmentation and climate change (Ponce-Reyes et al. 2012). As with other hylid frogs (Caviedes-Solis et al. 2015), C. taeniopus could face a rapid rate of population decline, as has occurred in other species inhabiting the temperate areas of cloud forest in Oaxaca (Delia et al. 2013; Mata-Silva et al. 2015), Chiapas (Johnson et al. 2015), and areas of the Sierra Madre Oriental (Flores-Villela et al. 2010). To add to the information presented in this study, additional studies on demography, ecology, physiological tolerances to temperature, length of the reproductive period, effect of fragmentation on populations, and population dynamics of this species should be conducted in order to devise efficient conservation strategies for C. taeniopus, and other species of anurans that inhabit the temperate and tropical montane environments of central and southern Mexico (Delia et al. 2013; Caviedes-Solis et al. 2015).
description: Published as part of Cruz-Elizalde, Raciel, Magno-Benítez, Itzel, Berriozabal-Islas, Christian, Ortíz-Pulido, Raúl, Ramírez-Bautista, Aurelio & Hernández-Austria, Raquel, 2020, Climatic niche, natural history, and conservation status of the Porthole Treefrog, Charadrahyla taeniopus (Günther, 1901) (Anura: Hylidae) in Mexico, pp. 10-21 in Amphibian & Reptile Conservation (e 219) (e 219) 14 (1) on pages 13-17, DOI: 10.5281/zenodo.11263095