Attendance to Egg Clutches by Male Kurixalus Eiffingeri Increases Hatching Success and Decreases Predation by Invasive Slugs (Parmarion Martensi) in Taiwan

Received: 28 July 2018 | Revised: 30 August 2018 | Accepted: 16 October 2018 DOI: 10.1111/eth.12822

RESEARCH PAPER

Attendance to egg clutches by male Kurixalus eiffingeri increases hatching success and decreases predation by invasive slugs (Parmarion martensi) in Taiwan

Ming‐Feng Chuang1,2 | Amaël Borzée2 | Yeong‐Choy Kam1

1Department of Life Science, Tunghai University, Taichung, Taiwan Abstract 2Division of EcoScience, Department of Life Invasive species have a significant impact on amphibians, and most notably Chytrid Sciences, Ewha Womans University, Seoul, fungi together with a few vertebrates. However, invasive terrestrial invertebrates are Korea seldomly demonstrated to have a negative effect on their host environment, and few Correspondence studies investigated the behavioural interactions between invasive and local species, Yeong‐Choy Kam, Department of Life Science, Tunghai University, Taichung, limiting our knowledge of the adaptive response adopted by local organisms. These Taiwan. responses include whether parenting animals recognize predators as threats to their Email: [email protected] offspring and whether parental care is adequately corrected. Here, through manipu‐ Funding information lative experiments on a population of phytotelm‐breeder Kurixalus eiffingeri in central Taiwan Ministry of Science and Technology, Grant/Award Number: MOST 105-2621- Taiwan, we demonstrated the positive effects of parental care against predation by B-029-004– MY2; Korea Environmental the invasive slug Parmarion martensi, and against mould infection. Treatment groups, Industry & Technology Institute, Grant/ Award Number: KEITI RE201709001 in the absence of caring males, displayed a higher rate of predation by slugs and mould infections. The presence of the caring males was linked to an increase in Editor: M. Herberstein hatching success in control groups, suggesting hydration by the males, while skin peptides may be the factor limiting mould infection. We recommend further research on the impact of the invasive but widespread P. martensi on amphibian populations.

KEYWORDS amphibian conservation, parental care, phytotelm‐breeder, predator‐prey

1 | INTRODUCTION 1999; Summers, McKeon, & Heying, 2006), and includes behaviours such as egg and tadpole guarding and transport, canal building, feed‐ Parental care provides fitness advantages through a variety of be‐ ing and gestation (reviewed by Royle et al., 2012). Paternal care most haviours, including feeding, teaching, playing, protecting against likely evolved to exploit predator‐free breeding sites (Magnusson & predation and etc. (reviewed by Clutton‐Brock, 1991). Parental be‐ Hero, 1991) in areas where environmental variations require the reg‐ haviour has been described in detail for a large range of birds and ular transport of larvae (Bickford, 2004; Wells, 2010). As a result, the mammals, including primates (reviewed in Royle, Smiseth, & Kölliker, transport of eggs and tadpoles is common in anurans, for instance in 2012). Paternal parental care evolved through inter‐sexual selection, Allobates femoralis, where both breeding parents displace their tad‐ in which males may provide females with fitness benefits through poles depending on water availability (Pašukonis et al., 2016). breeding site selection, territory maintenance, offspring protection, Two types of paternal care generally expressed by anurans are nuptial gifts, low parasitic load and genetic advantages (Møller & predator removal, typically present in species where the offspring Thornhill, 1998). In amphibians, paternal parental care has evolved is vulnerable and cannot be transferred (Poo & Bickford, 2013; Poo, many times (reviewed in Seshadri & Bickford, 2018), as illustrated in Erickson, Mason, & Nissen, 2017) and egg care (Wells, 2010). Caring numerous taxa (Lehtinen, Green, & Pringle, 2014; Summers & Earn, for eggs can prevent dehydration and predation (Poo & Bickford, 2013),

40 | © 2018 Blackwell Verlag GmbH wileyonlinelibrary.com/journal/eth Ethology. 2019;125:40–46. CHUANG et al. | 41 and by removing egg predators, the attending parents maintain a pred‐ 2.2 | Study organism ator‐free condition resulting in a higher hatching success. For instance, two glassfrog species Hyalinobatrachium valerioi and H. fleischmanni re‐ Kurixalus eiffingeri is a small arboreal frog endemic to Taiwan and move arthropod predators from egg clutches (Delia, Cisneros‐Heredia, the islands of Iriomote and Ishigaki in Japan. The breeding seasons Whitney, & Murrieta‐Galindo, 2010; Vockenhuber, Hödl, & Amézquita, lasts from March to August, a period during which males occupy 2009). Predator removal behaviour is primarily constrained by one and defend their territory, like bamboo stumps, and emit calls to factor: the ability to identify threats. The lack of shared evolutionary attract females (Kam et al., 1996). Large males have a better mat‐ history, such as with alien species (Kats & Ferrer, 2003), can lead to ing success (Chuang, 1988), and egg clutches are more frequently the inability to recognise potential predators by parents. This case is found in holes with deeper water (Lin & Kam, 2008; Lin, Lehtinen, best illustrated by the repeated predation of passerine bird nestlings & Kam, 2008). This species exhibits bi‐parental care with males at‐ by the slug Arion vulgaris, where predator recognition has not evolved tending eggs and females providing non‐fecundated trophic eggs (Turzańska & Chachulska, 2017). to tadpoles (Chen, Yu, & Kam, 2007; Cheng & Kam, 2010; Kam, Numerous invasive species are known to have a negative effect Chen, Chen, & Tsai, 2000). Male frogs spend more time attending on amphibians, and the top detrimental groups of species are fish, breeding sites with more eggs, and egg survivorship is correlated crayfish and American bullfrogs (Lithobates catesbeianus; Howard & with attendance frequency (Cheng & Kam, 2010; Chuang et al., Bickford, 2014; Kats & Ferrer, 2003). However, seemingly non‐dis‐ 2017). Finally, K. eiffingeri eggs are subject to fungal infections, ruptive species such as plants are also linked to a decrease in the desiccation, predation and flooding (Chen et al., 2007; Kam et al., performances of amphibian larvae (Watling, Hickman, & Orrock, 1996). 2011). Invasive invertebrates and plants are less commonly found on the list of invasive species leading to the death of anurans, with the 2.3 | Field procedures exception of emergent pathogens such as Chytrid fungi (reviewed by Beebee & Griffiths, 2005). The presence of these invasive spe‐ Field work was conducted between July 13 and August 18, 2016, cies can elicit adaptive plastic responses by local ones, to keep pace between 19:00 and 23:00 each day. During this period, we assessed with changing conditions (Wong & Candolin, 2015). Altered be‐ the presence of newly laid egg clutches and monitored daily all haviours include predator recognition (Elmasri, Moreno, Neumann, clutches found. To be included in the dataset, egg clutches had to & Blumstein, 2012) and behavioural adaptation (Phillips & Shine, be found before reaching developmental stage 16 (Gosner, 1960), 2006), such as offspring defence (Lehtonen, McCrary, & Meyer, equivalent to <2 days old (Kishimoto & Hayashi, 2017). To estimate 2012). Here, we investigated the role of paternal parental care on the effects of attending males, we randomly assigned egg clutches the hatching success of Kurixalus eiffingeri in relation to flooding, to two groups. For the experimental group (i.e., male‐removal treat‐ dehydration, mould infection and invasive predatory slug Parmarion ment), we removed males from 21 egg clutches and released them at martensi. We hypothesized that male attendance to egg clutches least 200 m away. The bamboo stumps containing the egg clutches in K. eiffingeri increases the survival of egg clutches and predicted were covered with plastic nets (ca. 0.5 cm mesh size) to prevent the lower hatching ratio and egg survival in the absence of paternal care return of males and to prevent the arrival of new males. Small inver‐ because of dehydration, predation and mould infection. To quantify tebrates such as slugs were still able to go through the net. In the the benefits of parental care, we tested this hypothesis through a control group (i.e., males were not removed), we monitored 11 egg male‐removal experiment. clutches in natural conditions, attended by males. On the first day of the experiment, we photographed the egg clutches and counted the number of eggs. 2 | MATERIALS AND METHODS We then monitored their development and the number of eggs daily, until hatching or death following the criteria developed from previous study (Delia, Ramírez‐Bautista, & Summers, 2013; Lehtinen 2.1 | Study site et al., 2014; Warkentin, 2000). The condition of the jelly capsule The experiments were conducted in Chitou bamboo forest was the main clue to identify the cause of mortality; desiccated (23.6888°N, 120.7916°E), in Nantou County, central Taiwan. The eggs shrank and became dull, flooded eggs have a larger than usual mean annual rainfall at the site is 2,500 mm and is typically the jelly capsule and became dull inside, mould affection resulted in the heaviest between March and September. The mean annual air growth of fungal hyphae on the totality of the egg clutch, and pre‐ temperature is 17.0°C, with the coldest months in January and the dation resulted in the disappearance of the eggs, when not caused warmest in July. At the study site, the most abundant bamboo spe‐ by metamorphosis. cies, Phyllostachys edulis, is widely cultivated and periodically cut. To enable comparisons between clutches, we calculated a hatch‐ When cut, stumps are left and will take several years to degrade. ing ratio by dividing the number of hatched tadpoles by the initial During this period, they collect rain water and are used for calling, number of eggs in the clutch. Hatching was recorded as successful breeding and tadpole development by K. eiffingeri (Kam, Chuang, & from the first egg hatching, while a failed clutch referred to an egg Yen, 1996). clutch where none of the eggs hatched successfully. 42 | CHUANG et al.

TABLE 1 Clutch size and hatching Treatment (male success for control group and treatment Control removal) Statistics p‐value (mean ± SD); Median (Min–Max). n 11 21 Attending males were not removed in the Successful/failed 11/0 9/12 Fisher’s exact 0.002 control group whereas males were clutches test removed in the treatment group Clutch size 46.9 ± 16.7 52.1 ± 15.8 M–W test 0.258 41 (27–80) 52 (25–81) Z = −1.13 Hatching ratio (%) 43.6 ± 24.4 9.7 ± 15.3 M–W test <0.001 41.7 (13.2–91.9) 0 (0–52.0) Z = 3.77

Note. M–W test: Mann–Whitney U test.

males was related to a significantly higher hatching ratio (Table 1). 2.4 | Statistical analyses For the control group, hatching was detected for each of the eleven We used Fisher’s exact test to compare the ratios of successfully clutches. Oppositely, hatching was detected in less than half of the hatched clutches between control and experimental groups. We egg clutches where males were removed: nine out of 21. The aver‐ then used a binary General Linear Model to compare clutch sizes age hatching ratio described the same variation and was significantly and hatching ratios between control and experimental groups. higher in the control group (43.6 ± 24.4%) than in the experimental Following the distribution of the data, we used a logistic regres‐ group (9.7 ± 15.3%). sion to analyse the hatching success, set as dependent variable, in We recorded the factors leading to the mortality of egg clutches both the treatment group (Table 3) and in a combination of control (Table 2). Twelve out of 21 clutches failed to hatch in the male‐re‐ and treatment groups (Table 4). This analysis was selected after moval treatment, and we recorded four causes for hatching failure, testing a range of models (Tables 3 & 4) and comparing the AIC with causes not being mutually exclusive (Table 2). Two clutches were value to select the most appropriate one. This analysis was con‐ flooded after intense rain; two clutches dried out, three clutches ducted in two steps to remove the bias induced by the lack of were infected by moulds, three clutches were entirely consumed variation in hatching success for the control group. The explana‐ by the predatory slug P. martensi, and two more clutches were par‐ tory variables were flooding, mould infection and predatory slug. tially consumed by slugs, before the remaining eggs were infected Dehydration was removed from the explanatory variables due to by moulds. Predatory slugs were related to 41.6% of hatching fail‐ the low sample size (n = 2 for both breeding success and failure, ure under the male‐removal treatment. In the control group, we only while n ≥ 4 for all other variables for both breeding failure and found parts of the egg clutches infected by moulds, and no other success). All statistical analyses were performed in Statistica 10 factors were observed during the experimental period (Table 2). We (StatSoft, 2011); Palo Alto, CA, USA). Means are presented with also regularly found clutches unrelated to our study consumed by ±1.0 SD. predatory slugs at the study site as there were no attending males (Figure 1). When looking at the hatching success for all clutches, we found 3 | RESULTS no effect of flooding, mould infection and desiccation (Tables 3 and 4). From the full model and the best model with lowest AIC, The average clutch size was around 50 eggs, which was not different however, the hatching success was related to the presence of between treatments (Table 1). In contrast, the presence of attending predatory slugs (Table 3). When focusing on the hatching success

TABLE 2 Factors affecting the Control Male removal development of Kurixalus eiffingeri egg Successful Failed Successful Failed Total clutches. All control replicates reached successful hatching, as defined by at least Healthiness 9 3 12 one of the eggs hatching, while more than Flooding 2 2 4 half of the clutches failed to develop in Dehydration 2 2 case of male removal Mould infection 2 1 3 6 Predatory slug 3 3 Slug + mould 2 2 4 infection Flooding + mould 1 1 infection Total 11 0 9 12 32 CHUANG et al. | 43

4 | DISCUSSION

Through a male‐removal experiment in K. eiffingeri, we evaluated the benefits of egg guarding by males on the hatching outcome of egg clutches. We found that the presence of attending males enhances hatching ratio (Table 1) and hatching success (Table 3). Previous stud‐ ies also indicated that the presence of attending males significantly increases the benefit for offspring (Poo, Evans, Tan, & Bickford, 2016; Chuang et al., 2017). We confirmed the results of Cheng and Kam (2010) where male egg‐attending behaviour is negatively cor‐ related with daily mortality. However, we also identified and quanti‐ fied factors causing hatching failure. Egg consumption by the invasive slug P. martensi, together with mould infection, were among the principal factors for egg hatching FIGURE 1 An invasive slug, Parmarion martensi was consuming failure in the male‐removal group. Terrestrial gastropods are rarely Kurixalus eiffingeri eggs on the inner wall of a bamboo stem [Colour reported as vertebrate predators (Turzańska & Chachulska, 2017) figure can be viewed at wileyonlinelibrary.com] and even less so in amphibians (Kats & Ferrer, 2003), but the inva‐ sive P. martensi does not follow the general trend and was found of clutches under the male‐removal treatment, no relationship was feeding on egg clutches of K. eiffingeri. The main explanation for the found (Table 4); all four variables were not significantly related to frog egg consumption may be a general non‐selective feeding be‐ hatching success. haviour. Although gastropods are generally described as herbivores,

TABLE 3 Logistic regression for factors Variables Estimate Wald Stat Confidence Interval p‐value associated with hatching success for all 32 clutches of Kurixalus eiffingeri eggs. The Null model (AIC = 43.0) full model is the best model according to Full model (AIC = 36.0) AIC criterion. The variable with bold Mould −0.33 0.49 −1.24–0.59 0.482 highlighted has the significant effect on dependent variable Slug −1.21 5.22 0.17–2.25 0.022 Flooding −0.66 1.34 −0.46–1.78 0.247 Dehydration −9.53 Partial models (42.0 < AIC < 47.8) Mould + Slug + Flooding (AIC = 45.0) Mould −0.09 0.04 −0.93–0.75 0.833 Slug −0.98 3.85 0–1.97 0.049 Flooding −0.36 0.46 −0.68–1.39 0.499 Mould + Slug (AIC = 44.0) Mould 1.01 4.2 0.04–1.97 0.040 Slug −0.35 0.44 −0.68–1.37 0.509 Mould + Flooding (AIC = 47.8) Mould −0.27 0.48 −1.02–0.49 0.488 Flooding −0.11 0.05 −0.88–1.1 0.827 Slug + Flooding (AIC = 43.6) Slug −0.98 3.85 0–1.97 0.050 Flooding −0.36 0.460 −0.68–1.39 0.499 Mould (AIC = 45.9) Mould −0.26 0.45 −1–0.49 0.503 Slug (AIC = 42.0) Slug −0.93 3.85 0–1.86 0.049 Flooding (AIC = 46.3) Flooding −0.06 0.02 −0.91–1.04 0.900

Note. Dependent variable: hatching success of all clutches (N = 32). 44 | CHUANG et al.

TABLE 4 Logistic regression for factors Variables Estimate Wald Stat Confidence Interval p‐value associated with hatching success for Null model male‐removal clutches of Kurixalus (AIC = 30.7) eiffingeri eggs Full model (AIC = 32.7) Mould −0.01 0 −1.01–0.98 0.977 Slug −0.6 1.13 −0.51–1.71 0.288 Flooding 0.05 0.01 −1.28–1.17 0.932 Dehydration −8.75 Partial models (31.8 < AIC < 35.3) Mould + Slug + Flooding (AIC = 35.3) Mould 0.22 0.21 −0.73–1.18 0.647 Slug −0.38 0.48 −0.69–1.45 0.487 Flooding 0.37 0.41 −1.52–0.77 0.524 Mould + Slug (AIC = 33.7) Mould 0.16 0.11 −0.76–1.07 0.740 Slug −0.49 0.93 −0.51–1.5 0.334 Mould + Flooding (AIC = 33.8) Mould 0.18 0.14 −0.75–1.11 0.707 Flooding 0.51 0.88 −1.59–0.56 0.349 Slug + Flooding (AIC = 33.3) Slug −0.35 0.42 −0.7–1.4 0.518 Flooding 0.31 0.310 −1.42–0.8 0.579 Mould (AIC = 32.7) Mould 0.06 0.02 −0.82–0.93 0.899 Slug (AIC = 31.8) Slug −0.46 0.85 −0.51–1.43 0.356 Flooding (AIC = 31.9) Flooding 0.46 0.76 −1.49–0.57 0.382

Note. Dependent variable: hatching success of male‐removal clutches (n = 21). they may feed on animals when available, such as avian nestlings was combined with prior slug predation, it was the second main threat (Turzańska & Chachulska, 2017) and anuran eggs, in this study. This to hatching. Egg jelly acts as a layer of protection from outer harmful unusual behaviour of gastropods feeding on frog eggs has not been influences (Marquis, Millery, Guittonneau, & Miaud, 2006), so the con‐ recorded before and may be the result of adaptation to exploit new sumption by P. martensi may not only kill the embryo directly but also resources. increase the mould infection by removing part of the egg jelly or cover Furthermore, the presence of attending males is linked to the it with mucus. Comparatively, male egg‐attending behaviour may also decrease in predation, suggesting males have physically defended function in reducing mould infection. Male K. eiffingeri were observed the eggs against P. martensi. This is interesting as native species sweeping through the egg masses in this as well as past studies (Cheng without evolutionary history with alien species are usually not able & Kam, 2010). This sweeping behaviour is likely to be related to the to display the right response behaviours (Diamond & Case, 1986). prevention of dehydration (Chen et al., 2007; Delia et al., 2013) and Male K. eiffingeri may recognize invasive slugs as egg predators or the decrease in mould infection by spreading skin peptides on the egg they may remove any suspicious objects that may harm the eggs. surface (reviewed by Bevins & Zasloff, 1990). Therefore, even if a species does not have a shared evolutionary Despite predation threats by invasive species being commonly history with alien species, it may adopt the functional response ac‐ reported for taxa worldwide including anurans (Kats & Ferrer, 2003; quired through experiences with native predators, resulting in a sim‐ Silva, Filho, & Feio, 2011), this study offers evidence that invasive ilar adaptive response. invertebrate species can also have negative impacts to local verte‐ Moreover, predation events by P. martensi were half of the time brate species. This phenomenon may be more common than our cur‐ followed by mould infection, resulting in hatching failure. Thus, preda‐ rent understanding and should be further studied to assess the real tion by slugs may enhance mould infection, and when mould infection impact of invasive invertebrate species. CHUANG et al. | 45

ACKNOWLEDGEMENTS Elmasri, O. L., Moreno, M. S., Neumann, C. A., & Blumstein, D. T. (2012). Response of brown anoles Anolis sagrei to multimodal signals from a We thank Nien‐Tse Fuh, Jia‐Jiun Hu, Yo‐Chen Lin and Wen‐Yu Xu native and novel predator. Current Zoology, 58, 791–796. from Tunghai University and Chih‐Chien Huang from Lienhuachih Gosner, K. L. (1960). A simplified table for staging anuran embryos and Research Center, Taiwan forest research institute, for their assis‐ larvae with notes on identification. Herpetologica, 16, 183–190. Howard, S. D., & Bickford, D. P. (2014). Amphibians over the edge: Silent tance with field works at Chitou. We thank Katarzyna Turzańska‐ extinction risk of Data Deficient species. Diversity and Distributions, Pietras from University of Wrocław, Poland, for providing reference. 20, 837–846. We thank Dr. Marie Herberstein, Desiree K. Andersen and two Kam, Y.‐C., Chen, Y.‐H., Chen, T.‐C., & Tsai, I.‐R. (2000). Maternal anonymous reviewers for their thoughtful comments, which have brood care of an arboreal breeder, Chirixalus eiffingeri (Anura: Rhacophoridae) from Taiwan. Behaviour, 137, 137–151. helped improve this manuscript. We thank the National Taiwan Kam, Y. C., Chuang, Z. S., & Yen, C. F. (1996). Reproduction, oviposition‐ University College of Bio‐Resources and Agriculture for permission site selection, and tadpole oophagy of an arboreal nester, Chirixalus to carry out our study (Permit No #1030006132). This work was eiffingeri (Rhacophoridae), from Taiwan. Journal of Herpetology, 30, supported by the Taiwan Ministry of Science and Technology grants 52–59. Kats, L. B., & Ferrer, R. P. (2003). Alien predators and amphibian declines: to YCK (MOST 105‐2621‐B‐029‐004–MY2) and MFC and AB were Review of two decades of science and the transition to conservation. supported by a research grant from Korea Environmental Industry & Diversity and Distributions, 9, 99–110. Technology Institute (KEITI RE201709001). Kishimoto, K., & Hayashi, F. (2017). The complete embryonic and larval stages of the oophagous frog Kurixalus eiffingeri (Rhacophoridae). Current Herpetology, 36, 37–45. ORCID Lehtinen, R. M., Green, S. E., & Pringle, J. L. (2014). Impacts of paternal care and seasonal change on offspring survival: A multiseason exper‐ Ming‐Feng Chuang https://orcid.org/0000-0002-7328-2577 imental study of a Caribbean frog. Ethology, 120, 400–409. Lehtonen, T. K., McCrary, J. K., & Meyer, A. (2012). Introduced predator Amaël Borzée https://orcid.org/0000-0003-1093-677X elicits deficient brood defence behaviour in a crater lake fish. PLoS Yeong‐Choy Kam https://orcid.org/0000-0002-8847-3077 ONE, 7, e30064. Lin, Y.‐S., & Kam, Y.‐C. (2008). Nest choice and breeding phenology of an arboreal‐breeding frog, Kurixalus eiffingeri (Rhacophoridae), in a REFERENCES bamboo forest. Zoological Studies, 47, 129. Lin, Y.‐S., Lehtinen, R. M., & Kam, Y.‐C. (2008). Time‐and context‐depen‐ Beebee, T. J., & Griffiths, R. A. (2005). The amphibian decline crisis: A dent oviposition site selection of a phytotelm‐breeding frog in re‐ watershed for conservation biology? Biological Conservation, 125, lation to habitat characteristics and conspecific cues. Herpetologica, 271–285. 64, 413–421. https://doi.org/10.1655/08-020R1.1 Bevins, C. L., & Zasloff, M. (1990). Peptides from frog skin. Annual Review Magnusson, W. E., & Hero, J.‐M. (1991). Predation and the evolution of of Biochemistry, 59, 395–414. complex oviposition behaviour in Amazon rainforest frogs. Oecologia, Bickford, D. P. (2004). Differential parental care behaviors of arboreal 86, 310–318. and terrestrial microhylid frogs from Papua New Guinea. Behavioral Marquis, O., Millery, A., Guittonneau, S., & Miaud, C. (2006). Toxicity of Ecology and Sociobiology, 55, 402–409. PAHs and jelly protection of eggs in the common frog Rana tempo‐ Chen, Y.‐H., Yu, H.‐T., & Kam, Y.‐C. (2007). The ecology of male egg at‐ raria. Amphibia‐Reptilia, 27, 472–475. tendance in an arboreal breeding frog, Chirixalus eiffingeri (Anura: Møller, A. P., & Thornhill, R. (1998). Male parental care, differential pa‐ Rhacophoridae), from Taiwan. Zoological Science, 24, 434–440. rental investment by females and sexual selection. Animal Behaviour, Cheng, W.‐C., & Kam, Y.‐C. (2010). Paternal care and egg survivorship 55, 1507–1515. in a low nest‐attendance rhacophorid frog. Zoological Studies, 49, Pašukonis, A., Trenkwalder, K., Ringler, M., Ringler, E., Mangione, R., 304–310. Steininger, J., … Hödl, W. (2016). The significance of spatial memory Chuang, K.‐S. (1988). The reproductive biology of Chirixalus eiffingeri. A for water finding in a tadpole‐transporting frog. Animal Behaviour, master's thesis (in Chinese with English abstract). Taipei, Taiwan: 116, 89–98. National Taiwan Normal University. Phillips, B. L., & Shine, R. (2006). An invasive species induces rapid Chuang, M.‐F., Lee, W.‐H., Sun, J.‐S., You, C.‐H., Kam, Y.‐C., & Poo, S. adaptive change in a native predator: cane toads and black snakes (2017). Predation risk and breeding site value determine male be‐ in Australia. Proceedings of the Royal Society of London B: Biological havior and indirectly affect survivorship of their offspring. Behavioral Sciences, 273, 1545–11550. Ecology and Sociobiology, 71, 122. Poo, S., & Bickford, D. P. (2013). The adaptive significance of egg atten‐ Clutton‐Brock, T. H. (1991). The evolution of parental care. Princeton, NJ: dance in a south‐east Asian tree frog. Ethology, 119, 671–679. Princeton University Press. Poo, S., Erickson, F. T., Mason, S. A., & Nissen, B. D. (2017). Predation of Delia, J., Cisneros‐Heredia, D. F., Whitney, J., & Murrieta‐Galindo, R. Feihyla hansenae (Hansen’s bush frog) eggs by a nursery web spider. (2010). Observations on the reproductive behavior of a Neotropical Herpetological Bulletin, 139, 36–37. glassfrog, Hyalinobatrachium fleischmanni (Anura: Centrolenidae). Poo, S., Evans, T. A., Tan, M. K., & Bickford, D. P. (2016). Dynamic switch‐ South American Journal of Herpetology, 5, 1–12. ing in predator attack and maternal defence of prey. Biological Journal Delia, J. R., Ramírez‐Bautista, A., & Summers, K. (2013). Parents ad‐ of the Linnean Society, 118, 901–910. just care in response to weather conditions and egg dehydration Royle, N. J., Smiseth, P. T., & Kölliker, M. (2012). The evolution of parental in a Neotropical glassfrog. Behavioral Ecology and Sociobiology, 67, care. Oxford, UK: Oxford University Press. 557–569. Seshadri, K. S., & Bickford, D. P. (2018). Faithful fathers and crooked Diamond, J., & Case, T. J. (1986). Overview: Introductions, extinctions, ex‐ cannibals: The adaptive significance of parental care in the bush terminations and invasions. New York, NY: Harper & Row. frog Raorchestes chalazodes, Western Ghats, India. Behavioral 46 | CHUANG et al.

Ecology and Sociobiology, 72, 4. https://doi.org/10.1007/ Warkentin, K. M. (2000). Wasp predation and wasp‐induced hatching of s00265-017-2420-3 red‐eyed treefrog eggs. Animal Behaviour, 60, 503–510. https://doi. Silva, E. T. D., Filho, O. P. R., & Feio, R. N. (2011). Predation of native org/10.1006/anbe.2000.1508 anurans by invasive bullfrogs in southeastern Brazil: Spatial variation Watling, J. I., Hickman, C. R., & Orrock, J. L. (2011). Predators and in‐ and effect of microhabitat use by prey. South American Journal of vasive plants affect performance of amphibian larvae. Oikos, 120, Herpetology, 6, 1–10. https://doi.org/10.2994/057.006.0101 735–739. https://doi.org/10.1111/j.1600-0706.2010.19255.x StatSoft (2011). STATISTICA (data analysis software system), version 10. Wells, K. D. (2010). The ecology and behavior of amphibians. Chicago, IL: https://www.statsoft.com University of Chicago Press. Summers, K., & Earn, D. J. (1999). The cost of polygyny and the evolu‐ Wong, B., & Candolin, U. (2015). Behavioral responses to changing envi‐ tion of female care in poison frogs. Biological Journal of the Linnean ronments. Behavioral Ecology, 26, 665–673. Society, 66, 515–538. https://doi.org/10.1111/j.1095-8312.1999. tb01924.x Summers, K., McKeon, C. S., & Heying, H. (2006). The evolution of How to cite this article: Chuang M‐F, Borzée A, Kam Y‐C. parental care and egg size: A comparative analysis in frogs. Attendance to egg clutches by male Kurixalus eiffingeri Proceedings of the Royal Society of London B: Biological Sciences, 273, 687–692. increases hatching success and decreases predation by Turzańska, K., & Chachulska, J. (2017). Arion slugs as nest predators invasive slugs (Parmarion martensi) in Taiwan. Ethology. of small passerine species–a review. Journal of Avian Biology, 48, 2019;125:40–46. https://doi.org/10.1111/eth.12822 455–458. Vockenhuber, E. A., Hödl, W., & Amézquita, A. (2009). Glassy fathers do matter: Egg attendance enhances embryonic survivorship in the glass frog Hyalinobatrachium valerioi. Journal of Herpetology, 43, 340– 344. https://doi.org/10.1670/08-092R1.1