Herpetology Notes, volume 14: 617-623 (2021) (published online on 02 April 2021)

Expression of metamorphic traits in four species of anurans (from south India) reared in the laboratory

Santosh M. Mogali1,*, Bhagyashri A. Shanbhag1, and Srinivas K. Saidapur1

Abstract. We reared tadpoles of four species of anurans (Duttaphrynus melanostictus, Sphaerotheca breviceps, Microhyla ornata and Hoplobatrachus tigerinus) belonging to different families with different foraging habits in the laboratory under relaxed conditions (absence of predator pressure, desiccation threat, intra- and inter-specific competition for food or space, and free from anthropogenic threats). The metamorphic traits (age and size) of the tadpoles reared in the laboratory (stress-free conditions) were compared with the members of their batch mates completing metamorphosis in the wild who faced predator pressure and desiccation threat leading to crowed condition (stressed conditions). In all four species (reared in the laboratory), the larval period was longer, and size at metamorphosis was significantly bigger than that of their batch mates completing metamorphosis in their natural . The study shows that in the absence of environmental stressors tadpoles take longer time to complete development and grow bigger in size before metamorphosis despite differences in their foraging habits.

Keywords. Anuran , laboratory-reared, metamorphosis, tadpoles, wild-caught

Introduction competition (inter and intra-specific) for food and space constraints (population density) (Wilbur, 1980; Griffiths Most of the anuran amphibians have a complex et al., 1991; Girish and Saidapur, 1999; Saidapur and life history strategy with an aquatic and terrestrial Girish, 2001; Miner et al., 2005). In addition to this, stage (Wassersug, 1975; Wilbur, 1980; Werner, 1986; Schoch, 2009). The aquatic larval stage is critical as it aquatic environments are increasingly impacted by has to complete development and attain a threshold size anthropogenic disturbances including pollution such before emergence on land following metamorphosis. as pesticides and livestock activity (grazing, trampling, The size at metamorphosis and the duration of the dunging) (McLaughlin and Mineau, 1995; Schmutzer et larval period are the two important traits in anuran al., 2008; Egea-Serrano et al., 2012; Thambirajah et al., amphibians that have larval stages (Lynn, 1961; Wilbur 2019), habitat degradation (Delis et al., 1996; Cushman, and Collins, 1973; Wilbur, 1980; Kulkarni et al., 2011). 2006; Squires et al., 2008; Arntzen et al., 2017; Strong et These traits exhibit considerable phenotypic plasticity al., 2017), and emerging infectious diseases (Daszak et in their expression and are related to the prevailing al., 2003; Lips et al., 2006; Densmore and Green, 2007; environmental conditions and challenges like predation Blaustein et al., 2018). Such challenges are routinely risk (Van Buskirk et al., 1997; Laurila and Kujasalo, encountered in nature. 1999; Van Buskirk and McCollum, 1999; Benard, In southern India, following south-west monsoon 2004; Mogali et al., 2011a, 2020a), desiccation threat rains, many anuran species opportunistically breed (Newman, 1988, 1992; Denver, 1997; Loman, 1999; in small rain-filled ephemeral ponds and puddles Mogali et al., 2011b, 2016; Szekely et al., 2017), and their larvae coexist in such water bodies until variations in the water temperature (Hayes et al., 1993; metamorphosis (Saidapur, 2001). The resources in such Alvarez and Nicieza, 2002; Maciel and Junca, 2009; ponds are limited. Also, crowding and competition are Tejedo et al., 2010; Wijethunga et al., 2016), and overwhelmingly present and more importantly, ponds dry up quickly if rains stop. In addition, these ponds also harbour diverse types of predators (Sharma et al., 2008; Sugur et al., 2008; Saidapur et al., 2009; Mogali et al., 1 Department of Zoology, Karnatak University, Dharwad-580 2011a, b, 2015, 2020b). 003, Karnataka State, India. It is well known that anuran larvae are endowed with * Corresponding author. E-mail: [email protected] the ability of developmental plasticity under challenging © 2021 by Herpetology Notes. Open Access by CC BY-NC-ND 4.0. environmental conditions (Girish and Saidapur, 1999, 618 Santosh M. Mogali �� al.

2003; Gramapurohit et al., 2004, 2006; Mogali et al., tigerinus tadpoles were reared in one tub each (n = 20 2016, 2017). Hence, the present study was undertaken tadpoles × 1 replicate/ tub = 20 tadpoles per species). to examine the effect of rearing tadpoles under a relaxed All the rearing tubs were placed on a flat surface in environmental (i.e., stress-free) on the metamorphic a room under natural photoperiod. The positions of traits, and compare to the metamorphosis under natural the rearing tubs were randomised on an alternate day conditions. Thus, in the laboratory, tadpoles were raised to avoid possible effects of place, if any. When the in the absence of predation, and desiccation, intra- tadpoles reached the feeding stage (Gosner stage 25; specific competition for food or space, and free from Gosner, 1960) they were fed daily. The tadpoles of D. anthropogenic threats. In the natural habitat, the tadpoles melanostictus and S. breviceps were daily provided with were under pressure from predators, pond desiccation, finely chopped and freshly prepared boiled spinach (5 intra- and interspecific competition for food and space, g). The carnivorous tadpoles of H. tigerinus were and likely livestock activity (stressful conditions). Here, provided daily with 150 prey tadpoles (D. melanostictus, we selected four anuran species given their differing n = 75 + S. breviceps, n = 75) as food. The tadpoles of foraging habits, spanning three different families. The M. ornata were daily provided with detritus matter (4 tadpoles of Duttaphrynus melanostictus (Bufonidae) and g) from natural ponds (decayed leafy material, micro- Sphaerotheca breviceps () feed on detritus plankton) and squeezed boiled spinach material (1 g). matter or algae (herbivores) while those of Microhyla The food materials (either boiled/ squeezed spinach, ornata (Microhylidae) are suspension feeders, feeding prey tadpoles, detritus matter or micro-plankton) were on detritus matter or micro-plankton or algae. The always ad libitum in all the rearing tubs. Tub water was tadpoles of Hoplobatrachus tigerinus (Dicroglossidae) changed thrice in a week. When reaching metamorphic are aggressively carnivorous and feed on any coexisting climax stage (emergence of forelimbs; Gosner stage tadpole or insect and their larvae (Khan, 2000; Hiragond 42; Gosner, 1960), tadpoles were housed individually and Saidapur, 2001; Saidapur, 2001; Grosjean et al., in small tubs (19 cm diameter and 7 cm depth with 2004; Saidapur et al., 2009; Dey and Goswami, 2015). little water) covered with fine nylon mesh. These tubs In the present study, we hypothesised that tadpoles of were kept inclined to provide a semi-terrestrial area for these four species should attain a bigger body size if tadpoles to emerge from the water. On completion of reared under relaxed conditions and also metamorphose metamorphosis (Gosner stage 46; Gosner, 1960), snout- late than those metamorphosing in the wild. vent length (SVL in mm; measured using digital calliper with accuracy 0.01 mm) and body mass (in mg; weighed Material and Methods using an electronic balance with accuracy 0.001 g) of All four species naturally co-exist during their larval the individuals of each species was recorded. stage, sharing the temporary ponds (rain-filled) at the One of us (SMM) regularly visited the natural ponds Karnatak University Campus, Dharwad (15.4404°N, from where the eggs were collected to keep track of the 74.9852°E). Small portions of the egg mass from a progression of development of tadpoles. Additionally, clutch were collected for each species in different the water level (i.e. desiccation), density of tadpoles temporary ponds in June 2012 (approximately 50–60 and presence of predators were visually observed and eggs of D. melanostictus and S. breviceps; 25–30 eggs noted. Disturbance caused by cattle and dogs were often of M. ornata and H. tigerinus). The remaining majority reported near the water bodies. Whenever tadpoles in portions of the egg masses were left in nature to monitor the wild, reached Gosner stages 42–44 (emergence of their developmental progress. Eggs of each species were forelimbs and initiation of shortening of tail) they were placed in separate glass aquariums (75 L × 45 W × 15 H brought to the laboratory. The day of emergence of each cm) filled with 10 L of aged (dechlorinated) tap water. tadpole was also noted. These tadpoles were maintained The eggs of all the species hatched (Gosner stage 19; in the same way as described earlier for laboratory reared Gosner, 1960) the day after collection. Twenty tadpoles tadpoles until complete metamorphosis (Gosner stage per tub/ each species were reared separately in plastic 46). At metamorphosis, SVL (in mm) and body mass tubs (42 cm diameter and 16 cm height) with 5 L of aged (in mg) of the individuals of each species (wild-caught) tap water. Tadpoles of D. melanostictus and S. breviceps were recorded (D. melanostictus, n = 40; S. breviceps, n were maintained in two tubs each (n = 20 tadpoles per = 40; M. ornata, n = 20 and H. tigerinus, n = 20). tub × 2 replicates/ tub = 40 tadpoles per species; density All newly metamorphosed toadlets/ froglets of all of 4 tadpoles per L), while those of M. ornata and H. species (laboratory-reared and wild-caught) appeared Expression of metamorphic traits in four species of anurans reared in the laboratory 619 to be healthy and active and hence, after completion Morphometrics and larval period duration of of experiments, they were released near natural water laboratory-reared and wild-caught metamorphs. No bodies in the University campus. Data on SVL, body mortality was observed during the experiment in our mass and larval period of the two different treatment laboratory-reared tadpoles. Density was thus maintained groups (laboratory-reared vs. wild-caught) of each constant until individuals started to leave the water. A species were compared separately by nonparametric significant difference was observed in the age and size at analyses (Mann-Whitney U test). Statistical tests were metamorphosis of laboratory-reared compared to those performed using SPSS software (ver. 16.0). growing in the wild in all the four species of anurans studied (Fig. 1–3). Both SVL and body mass (size) of Results laboratory-reared individuals were significantly greater than that of the corresponding wild-caught subjects at Observations on temporary water bodies/ sites. metamorphosis (p < 0.001; Fig. 1, 2). Likewise, the Similar to the laboratory condition, tadpoles in the wild larval period (age) of laboratory-reared individuals was also hatched the day after egg collection. During the significantly greater than their batch mates completing two weeks following egg collection we recorded no metamorphosis in the wild (p < 0.001; Fig. 3). The changes in water levels in the ponds; these were kept means, standard deviations and range values for SVL full due to the continuous rains, and were also rich in (mm), body mass (mg) at metamorphosis and the length food resources (decayed leaves/ algae/ phytoplankton). of the larval period (days) in four species of south Indian The tadpole density appeared low (visually) in this anurans, reared in either laboratory or wild are given in period. However, the sudden decline in the rainfall later Table 1. in the third week, led to a natural process of desiccation, converting these ponds into small isolated puddles/ Discussion pockets with lower water levels, and increasing this way the tadpole density. The temporary ponds housed diverse A number of factors (biotic and abiotic) such as types of predators; all the monitored ponds presented a predator pressure, larval density, desiccation of water, combination of at least three of the following species: anthropogenic activity are known to influence the dragonfly/ damselfly larvae, water scorpions, water developmental (phenotypic) plasticity involving a trade- boatmen, crabs, beetles. These temporary ponds on off between larval duration and size at transformation in University campus are away from agricultural fields or anuran amphibians (Rudolf and Rödel, 2007). Predation industries (free from pesticides or water pollution) but risk is known to enhance or delay metamorphosis these are perhaps affected by physical interferences of depending upon the prey/ predator species (Laurila et domestic like cattle and dogs. al., 1998; Relyea, 2007; Mogali et al., 2011a; Mogali, 2018), whereas desiccation threat invariably hastens

Table 1. Snout-vent length (mm), body mass (mg) at metamorphosis and length of the larval period (days) in four species of south IndianTable anurans 1. Snout-vent reared in length laboratory (mm), bodyand masswild (mg)caught. at metamorphosis Data represented and length as mean of the ± larval SD, figuresperiod (days) in parenthesis in four species represent of south range. Indian anurans reared in laboratory and wild caught. Data represented as mean ± SD, figures in parenthesis represent range.

Treatment/ species SVL (mm) Body mass (mg) Larval period (days) Duttaphrynus melanostictus Laboratory-reared 10.16 ± 0.46 (9.20 – 11.06) 113.20 ± 17.27 (80 – 150) 33.15 ± 1.33 (31 – 37) Wild-caught 7.20 ± 0.24 (6.48 – 7.75) 43.83 ± 4.73 (32 – 58) 27.28 ± 0.45 (27 – 29) Sphaerotheca breviceps Laboratory-reared 14.48 ± 0.64 (13.09 – 15.94) 399.28 ± 75.70 (286 – 600) 38.10 ± 1.35 (35 – 41) Wild-caught 9.69 ± 0.74 (7.70 – 11.52) 95.77 ± 21.03 (65 – 179) 31.35 ± 0.48 (30 – 33) Microhyla ornata Laboratory-reared 10.93 ± 0.46 (9.98 – 11.65) 141.55 ± 14.31 (116 – 169) 40.45 ± 1.84 (37 – 44) Wild-caught 8.20 ± 0.37 (7.45 – 8.96) 61.70 ± 7.56 (50 – 77) 35.45 ± 0.51 (35 – 37) Hoplobatrachus tigerinus Laboratory-reared 22.16 ± 1.43 (20.00 – 24.25) 1194.80 ± 217.92 (880 – 1567) 50.05 ± 3.63 (43 – 56) Wild-caught 16.00 ± 1.11 (14.09 – 18.36) 491.20 ± 103.09 (315 – 719) 43.40 ± 0.50 (42 – 45)

620 Santosh M. Mogali �� al.

vent length (mm) - Body mass (mg) Snout

LR WC LR WC LR WC LR WC LR WC LR WC LR WC LR WC

D. melanostictus S. breviceps M. ornata H. tigerinus D. melanostictus S. breviceps M. ornata H. tigerinus

Figure 1. Box-whisker plot depicting the snout-vent Figure 2. Box-whisker plot depicting the body mass (mg) length (mm) in laboratory reared (LR) or wild caught in laboratory reared (LR) or wild caught (WC) metamorphs (WC) metamorphs of four anuran species. Boxes represent of four anuran species. Boxes represent interquartile ranges. interquartile ranges. Horizontal bars in the boxes represent Horizontal bars in the boxes represent medians; whiskers medians; whiskers represent the farthest data points that are represent the farthest data points that are not outliers; open not outliers, open circles represent outliers; triangular represent circles represent outliers, triangular represent extreme outliers. extreme outliers. The asterisk denotes significant differences The asterisk denotes significant differences in body mass of in SVL of metamorphs between LR and WC groups (Mann- metamorphs between LR and WC groups (Mann-Whitney U Whitney U test). test). metamorphosis in all anuran species studied so far developmental plasticity among anuran larvae. Thus, in (Richter-Boix et al., 2011; Mogali et al., 2011b, 2016, nature and in laboratory experiments, depending upon 2017). Similarly, tadpole density (Dash and Hota, 1980; the perceived threat and its intensity, a given species may Hokit and Blaustein, 1994; Saidapur and Girish, 2001; hasten or delay metamorphosis and emerge at a small or Gramapurohit et al., 2004; Mogali et al., 2016, 2017) bigger size (Wilbur, 1980; Vonesh and Warkentin, 2006; and presence of anthropogenic threats (Schmutzer Relyea, 2007; Fabrezi et al., 2009; Mogali et al., 2011a, et al., 2008; Egea-Serrano et al., 2012; Thambirajah 2016; Mogali, 2018). et al., 2019; Trudeau et al., 2020) also influence the The tadpoles of all four species of anurans, belonging to three different families and different in foraging habits, took longer duration to complete metamorphosis when reared under stress-free or relaxed conditions. These individuals left the water with significantly greater size (length and weight) than their batch mates growing in their natural habitat (under stress). Due to the intrinsic stressful nature of temporary water bodies, wild tadpoles (all four species) invariably experienced inter- and intra-specific competition for food and space, predation risk, desiccation threats and also, sometimes, anthropogenic-driven stress. All these factors prevailing in the water body conjointly influence larval period and size at metamorphosis in wild growing tadpoles. Though Figure 3. Average larval period (days) in laboratory-reared metamorphosing at a small body size is disadvantageous, (LR) and wild-caught (WC) of four anuran species. 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Accepted by Gonçalo Rosa