Inability of mate and species recognition by male Asian toads, bufo gargarizans
Inability of mate and species recognition by male Asian toads, bufo gargarizans
Cheong, Seokwan; Sung, Hacheol; Park, Shiryong
2008-01-01 00:00:00
Animal Cells and Systems 12: 93-96, 2008 Inability of Mate and Species Recognition by Male Asian T o ads, Bufo gargarizans Seokwan Cheong, Hacheol Sung and Shiryong Park* Department of Biology Education, Korea National University of Education, Chungbuk 363-791, Korea Abstract: In recent years, we frequently observed miss- 1988; Schwartz, 1989; Ryan, 1990; Gerhardt, 1991): for matche d p a i r s betwe en mal e As i an toad s, Bufo ga rgar izan s , example, the vocal characteristics of males, such as louder and bullfrogs, Rana catesbeiana, at the toad breeding calls or lower frequency calls, play a role in female choice ponds, where scramble competition for mating occurred and male-male competition (Halliday, 1983). In addition, among the male toads. Thus, we performed two-choice such calls possess species-specific characteristics functioning experiments to investigate recognition ability of mates and as a pre-mating isolating mechanism (Duellman and Pyles, species in male toads. The test males did not discriminate sexes, but the clasped stimulus males immediately 1983; Schneider et al., 1984). In contrast with prolonged produced release calls and stopped it while the clasped breeders, very intense scramble competitions occur in stimulus female did not. In addition, the test male toads did explosive breeders because of synchronous arrival at a not discriminate reproductive state of females and even breeding site with limited mating opportunities of a short species. However , male toads chose larger individuals. The breeding period. Males may actively search for females present results indicate that the main reason of miss- rather than attract females with vocalizations, where males matched amplexus by the male toads is due to 1) the lack of approach and attempt to clasp any moving objects nearby re co gnit i o n c ues of co ns pe cif i c s , 2) th e lac k o f c o m m u n i ca t i on tools like release calls, and 3) the larger size of bullfrogs (Arak, 1983; Olson, 1989). The species may use other than male toads themselves. recognition cues, such as chemical cues and tactile cues, for sex and mate recognition (Davies and Halliday, 1978; Key words: Asian T oad, Bufo gargarizans , two-choice experi- Duellman and Trueb, 1994). ment, bullfrog, Rana catesbeiana , recognition cue, release call The Asian toad, Bufo gargarizans , is widely distributed over the large part of East Asia and is common in Korea (Yang et al., 2001). The species was once classified into Communication occurs when cues given by senders influence Bufo bufo gargarizans, a subspecies of Bufo bufo, the the behavior of receivers (Endler, 1993). Receivers should Eu ropean toad or the commo n toad (Kang and Y oon, 1975 ). benefit from recognizing between desirable and undesirable They are typical ‘explosive breeders’, yearly visiting a cues. When the recognition cues are overlapped, selection breeding pond in early spring, where they are staying up to may favor an optimal balance between accepting 1-3 weeks before returning to terrestrial areas for non- un desirable cues (accep tan c e er rors) and rejecting d e si rable breeding season. The male toads usually experience intense cues (rejection errors), where the balance could be altered scramble competition for possession of females without by changing decision rules or recognition templates of producing advertisement calls. In recent years, unusual receivers (Sherman et al., 1997). mismatched pairing between bullfrogs ( Rana catesbeiana ) The recognition of species and mates may be important and male toads has been observed frequently in some for successful reproduction in anuran amphibians. Species breeding ponds (Fig. 1). The bullfrog is a large, an average of prolonged breeders that have multiple mating opportunities length of 10 cm with weight of 142 g, and exotic invasive mainly use vocalizations in relation to both interspecific species rapidly spreading in the western and southern and intraspecific mate selection (Sullivan, 1983; Wells, Korean Peninsula since being introduced from Japan at the end of 1970 (Kang and Youn, 1994). To date, no certain * T o whom correspondence should be addressed. explanation has been given how it does happen. T el: +82-43-230-3719; Fax: +82-43-233-6263 E-mail: srpark@knue.ac.krIn this paper, we hypothesized that male Asian toads lack ANIMAL CELLS AND SYSTEMS Vo l. 12 No. 2 93 Cheong Seokwan, Hacheol S ung and Shiryong P ark spring of the toad breeding season. We designed the five experiments considering the methods used by Marco et al. (1998). We prepared for a rectangular tank (120 ×50 ×30cm) filled with about 5cm of pond's water for all experiments. We replaced the water after each trial in order not to contaminate the tank with chemicals. W e put stimulus individuals on each end of the tank at ran dom position . Th e stimulus individuals were tied with string 15 cm long to the tank ends so that they were allowed to move for a short distance. We placed a single test male in a small container (20 ×20 × 20 cm) constructed of fiber glass screen into the center of the tank. The test male was acclimatized for two minutes. All experiments were started with removing the container, and we counted the number of attempts to amplex one of the stimulus Fig. 1. Miss-matched amplexus between a bullfrog (bottom) and individuals. We decided the male selected a stimulus several male Asian toads (top). The male toads strongly clasped the su b ject if th ere was an amplexus mo re than 30 second s. W e bullfrog to death. stopped the trial if any amplexus attempt was not observed for 1 0 minutes. an ability o f mate recog nition. Using choice experiments in W e used student’ s t-test to examine the variation of SVL the lab, we tested the hypothesis: whether male Asian toads between stimulus individuals and used Binomial test to discriminate 1) between the sexes of conspecifics, 2) determine whether there is a significant difference between between reproductive states of female toads, and 3) even the observed and the expected frequencies in mate choice between female toads and bullfrogs as a potential mate. experiments. Numerical data in the text are presented as Furthermore, we tested whether the males show size- mean±SD. Data were analyzed using SPSS statistical assortative mating preference using different sizes ofsoftware (v.11.5; SPSS 2002). bullfrogs. This is the first study on the effects of alien species to breeding biology of native species occupying RE SU L T S similar eco lo gical status. W e captured 133 males and 46 females of the Asian toads. MA TERIALS AND METHOD Mean SVL of males was 8.08 cm (±0.67) and female was 10.77 cm (±0.78). Females were significantly larger than We collected the Asian toads at a pond (3617'43"N, males (student’s t-test, t=20.75, p ≤ 0.001). The mean SVL 12730'30"E) in Okcheon Gun, Chungbuk Province, Korea, of used stimulus to ad s and b ullfro gs in each trial are shown in March 1999. W e measured snout-vent lengths (SVL) of in Table 1: there were no significant differences between the toads to the nearest 0.01 mm with vernier calipers and two groups of stimulus individuals in Experiment 1, 2, 3. isolated them by sex. The sex of each toad was determinedHowever, the large size of bullfrogs was significantly larger by the presence of nuptial pads of males. We performedthan small or medium size of bullfrogs as expected. five experiments to investigate the recognition ability of In experiment 1, when similar sizes of a female toad and male Asian toads for species and mate choice: we used a bullfrog were presented to male toads, 7 of 20 males choice experiments to determine whether the males (35%) attempted to amplex female toad while 13 males to discriminate 1) between the sexes of conspecifics, 2) bullfrogs, which was not significantly different from between gravid versus non-gravid females of the similar random (z = 1.34, p = 0.13, Fig. 2). The test males tightly size, 3) even between female toads and bullfrogs as aclasped not only female toad but also bullfrog. The bullfrog potential mate, 4) between small (7~9 cm of SVL) versus more struggled to escape from being amplexed than female large (12~15 cm) stimulus, and 5) between medium (9~12toad, but failed till we stopped the trial at 30 seconds. cm) and large stimulus. As a stimulus, we used bullfrogs In experiment 2, when test males received a choice because we are interested in revealing whether they tend to between a female and a male toad in similar sizes, 9 of 20 have size-assortative selection in mate choice even if the males (45%) chose female over male, which did not bullfrogs are not the same species. We captured the significantly differ from random (z = 0.41, p = 0.45, Fig. 2). o o bullfrogs in Youngjong island (37 29'12"N, 12630'E), The stimulus male produced release calls in amplexus Incheon City, in November 1998. We kept the bullfrogs while the stimulus female did not. Male-male amplexus provided loaches for food in an aquarium till the next never lasted more than 5 seconds in response to the call, 94 ANIMAL CELLS AND SYSTEMS Vol. 12 No. 2 Mate and S pecies Recognition by Male Asian T oads Table 1. Comparisons of body sizes between stimulus 1 and 2 in the five experiments. Mean (±SD) SVL (snout-vent length) of stimulus individuals, where N means number of trials Stimulus 1 Stimulus 2 Experiment (N) Individual SVL (cm) Individual SVL (cm) 1 (20) Female toad 10.79 ± 0.73 Bullfrog 1 1.78 ± 0.17 2 (20) Female toad 09.72 ± 0.28 Male toad 09.39±0.21 3 (20) Non-gravid female 10.75 ± 0.98 Gravid female 10.76 ± 0.95 4 (21) Small bullfrog 07.93 Large bullfrog 13.17 5 (20) Medium bullfrog 11.35 Large bullfrog 14.62 male-biased sex ratio (Sung et al., 2007). This allows male to have few opportunities to amplex a female. This may lead to sexual selection favoring males that actively search for females, but not vice versa. The active males may attempt to vigorously clasp close individuals without discriminating sex, gravid female, and even conspecifics. Due to such a behavioral strategy for male reproductive success, the toads may not use an advertisement call to attract a potential mate. The advertisement call has been extensively used in one of recognition cues indicating male quality (i.e. large males) by female choice (Davies and Fig. 2 . Mate choice by male Asian toads. Experiment 1: female toad ( □ ) vs. bullfrog ( ■ ); Experiment 2: female toad ( □ ) vs. male toad Halliday, 1978; Arak, 1983; Wells, 1988). The western toad ( ■ ); Experiment 3: Non-gravid female toad ( □ ) vs. gravid female (Bufo boreas) is the similar species that lacks this kind of toad ( ■ ); Experiment 4: small bullfrog ( □ ) vs. large bullfrog ( ■); advertisement calls (Marco et al., 1998). Like the Asian Experiment 5: medium bullfrog ( □ ) vs. large bullfrog ( ■ ). Significan t level of binomial test: * p < 0.05, ***p<0.001. toad, the western toads use a se riou s of release calls as o nly recognition cue whether the amplexed ind ividual is ma le or female. while male-female amplexus lasted till we separated paired Males chose larger individuals given a choice, which couples. may be another reproductive strategy to increase the In experiment 3, when test males received a choice probability of selecting correct females rather than males. between a gravid female and a non-gravid female in similar Females are usually about 1.3 times larger than males sizes, 9 of 20 males (45%) chose gravid female over non- (Sung et al., 2007). The sexual dimorphism in anurans has gravid female, which did not significantly differ from been described as resulting from the interaction between random (z = 0.41, p=0.45, Fig. 2). natural and sexual selection (Lande and Arnold, 1983; In experiment 4 and 5, when test males received a choice Ryan, 1985; Arak, 1988). Males tended to favor larger between small or medium vs. large stimulus, the males fe males as a mate because the lar ger fe males lay mo re eggs significantly preferred large ones: 20 of 21 males (95%) in so that males in amplexus increase the number of their small vs. lar ge stimulus experiment (z = 4.15, p < 0.001, Fig. fertilizing eggs (Davies and Halliday, 1977; Arntzen, 2) and 15 of 20 males (75%) in medium vs. large stimulus 1999). It may be true in an excess of females, where males experiment (z=2.24, p=0.02, Fig. 2). may be able to evaluate female size to choose the larger ones. However, in case female choice by male is temporally and spatially limited, the male may attempt to claps a DISCUSSION potential female quickly using size cues as well as release The present results suggest that male Asian toads do notcalls. recognize sex, reproductive state of females, and even In recent years, we frequently observed miss-matched species. The males randomly chose similar sizes of male amplexus of male toads and the bullfrogs in the fields, toads over female toads, bullfrogs over female toads, non- which, in turn, a toad k ept clasping a bullfrog to d eath . The gravid over gravid females. However, the males preferred bullfrogs do not have ribs protect internal organs from large individual to small or middle one. external pressure by toad clasp. Thus, the main reason of As a typical explosive breeder, the Asian toads aggregate miss-matched amplexus by the male toads is due to 1) the synchronously into breeding sites forming high-density lack of recognition cues of conspecifics, 2) the lack of populations, where they have a short breeding period with a communication tools like release calls, and 3) the larger ANIMAL CELLS AND SYSTEMS Vo l. 12 No. 2 95 Cheong Seokwan, Hacheol S ung and Shiryong P ark a population of common toads (Bufo bufo ). A m ph ibi a - R e p ti lia size of bullfrogs than male toads themselves. As an exotic 8: 321-330. invasive species, the bullfrogs are evolutionary absent in Kang EJ and Y oun CH (1994). The settlement and distribution of this country so that it is an unusual phenomenon in nature the introduced bullfrog, Raja catesbeiana, in Korea. nat ur e in these days. conservation report 13: 231-250. We do not know how the male sizes influence male Kang YS and Y oon IB (1975) Illustrated encyclopedia of fauna mating success. However, from the study of the common and flora of Korea Vol 17 Amphibia'Reptila. The Korean toad, when breeding period is short, mating in relation to ministry of education. Seoul. body size is random (Davies and Halliday , 1977; Hoglund Lande R and Arnold SJ (1983) The measurement of selection on correlated characters. E v ol uti o n 37: 1210-1226. and Robertson, 1987). Although small clasped males is often displaced by large ones at the time of spawning, small Marco A, Kesecker JM, Chivers DP, and Blaustein AR (1998) Sex recognition and mate choice by male western toads, Bufo males, considered to be disadvantageous in male-male boreas. Anim Behav 5 5 : 16 31- 16 35. competition, still have some opportunities for mating Olson DH (1989) The ecological and behavioral dynamics of (Davies and Halliday, 1977). Thus, the male mating success breeding in three sympatric anuran amphibians. Ph.D. thesis, in this species is almost density and time dependent. We Oregon State University. more need to investigate the male size effects of mate R y an MJ ( 198 5) T he T ung ara Fr ogs: A S tud y in Sexu al S elect ion selection processes in the Asian toad. and Communication. Univ Chicago Press, Chicago and L o n don . REFERENCES Ryan MJ (1990) Sensory systems, sexual selection, and sensory e xpl oit a ti on. Oxford Surv Evol Biol 7: 157-195. Schneider H, Sofianidou TS, and Kyriakopoulou-Sklavounou ARAK A (1983) Male-male competition and mate choice in (1984) Bioacoustic and morphometric studies of water frogs anuran amphibians. In: P. Bateson (ed), Mate Choice, ( g e nus Rana) of Lake Ioannina in Greece, and description of a Cambridge, Cambridge University Press, pp 181-210. new species (Anura, Amphibia). J Zool Syst Evolut-forsch . Ar ak A ( 1 9 88) Sex u al siz e dimo rp hism i n bod y size: a model and 22: 349-366. a test. Evolution 4 2 : 8 20- 825 . Schwartz JJ (1989). Graded aggressive calls of the spring peeper , Arntzen JW (1999) Sexual selection and male mate choice in the Pseudacris crucifer. Herpe t ol ogi ca 45: 172-181. common toad, Bufo bufo. Ethol Ecol Evol 11: 407-414. Sherman PW, Reeve HK, and Pfennig DW (1997) Recognition Da vies NM and Hal lid ay TR ( 197 7) Op timal ma t e se lect ion i n the systems. In: Krebs JR and Davis NB (eds.), Behavioural to ad Bufo bufo. Nature 269: 56-58. Ecology: An Evolutionary Approach, Oxford, Blackwell, pp Davies NB and Halliday TR (1978) Deep croaks and fighting 6 9 - 96. assessment in toads Bufo bufo. Nature 274: 683-685. Sung HC, Park OH, Kim SK, Park DS, and Park SR (2007) Duellman WE and Pyles RA (1983) Acoustic resource Abundance and breeding migration of the Asian Toad (Bufo partitioning in anuran communities. Cop e ia 1983: 639-649. gargarizans ). J Ecol Field Biol 30: 287-292. Duellman WE and Trueb L (1994) Biology of Amphibians. Sullivan BK (1983) Sexual selection in W ood house’ s toad (Bufo Baltimore: The Johns Hopkins University Press. woodhousei). II. Female choice. Anim Behav 31: 1011-1017. Endler JA (1993) Some general comments on the evolution and Wells KD (1988) The effect of social interactions on anuran vocal design of animal communication systems. Phil Tran R Soc beha vi or . In: Fritzsc h B, R y an MJ, W ilczynski W , He th erington London B 340: 215-225. T E , and W a l kowi a k W ( e ds) , Th e E vol ut ion o f t h e Amphi bian Gerhardt HC (1991) Female mate choice in treefrogs: static andEar, New York, John Wiley, pp 433-454. dynamic acoustic criteria. Anim Behav 42: 615-636. Y a ng SY , Ki m JB , Mi n MS , S uh JH , and Kan g YJ ( 200 1) Ko rean Halliday TR (1983) The study of mate choice. In: P. Bateson (ed), a mphi bi ans. A cademic P r e ss. Mate choice, Cambridge Univ. Press, Cambridge, pp 3-52. [Received May 9, 2008[ accepted June 13, 2008] Hoglund J and Robertson JG M (1987) Random mating by size in 96 ANIMAL CELLS AND SYSTEMS Vol. 12 No. 2
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Inability of mate and species recognition by male Asian toads, bufo gargarizans
Inability of mate and species recognition by male Asian toads, bufo gargarizans
Abstract
Abstract In recent years, we frequently observed miss‐matched pairs between male Asian toads, Bufo gargarizans, and bullfrogs, Rana catesbeiana, at the toad breeding ponds, where scramble competition for mating occurred among the male toads. Thus, we performed two‐choice experiments to investigate recognition ability of mates and species in male toads. The test males did not discriminate sexes, but the clasped stimulus males immediately produced release calls and stopped it while...
Animal Cells and Systems 12: 93-96, 2008 Inability of Mate and Species Recognition by Male Asian T o ads, Bufo gargarizans Seokwan Cheong, Hacheol Sung and Shiryong Park* Department of Biology Education, Korea National University of Education, Chungbuk 363-791, Korea Abstract: In recent years, we frequently observed miss- 1988; Schwartz, 1989; Ryan, 1990; Gerhardt, 1991): for matche d p a i r s betwe en mal e As i an toad s, Bufo ga rgar izan s , example, the vocal characteristics of males, such as louder and bullfrogs, Rana catesbeiana, at the toad breeding calls or lower frequency calls, play a role in female choice ponds, where scramble competition for mating occurred and male-male competition (Halliday, 1983). In addition, among the male toads. Thus, we performed two-choice such calls possess species-specific characteristics functioning experiments to investigate recognition ability of mates and as a pre-mating isolating mechanism (Duellman and Pyles, species in male toads. The test males did not discriminate sexes, but the clasped stimulus males immediately 1983; Schneider et al., 1984). In contrast with prolonged produced release calls and stopped it while the clasped breeders, very intense scramble competitions occur in stimulus female did not. In addition, the test male toads did explosive breeders because of synchronous arrival at a not discriminate reproductive state of females and even breeding site with limited mating opportunities of a short species. However , male toads chose larger individuals. The breeding period. Males may actively search for females present results indicate that the main reason of miss- rather than attract females with vocalizations, where males matched amplexus by the male toads is due to 1) the lack of approach and attempt to clasp any moving objects nearby re co gnit i o n c ues of co ns pe cif i c s , 2) th e lac k o f c o m m u n i ca t i on tools like release calls, and 3) the larger size of bullfrogs (Arak, 1983; Olson, 1989). The species may use other than male toads themselves. recognition cues, such as chemical cues and tactile cues, for sex and mate recognition (Davies and Halliday, 1978; Key words: Asian T oad, Bufo gargarizans , two-choice experi- Duellman and Trueb, 1994). ment, bullfrog, Rana catesbeiana , recognition cue, release call The Asian toad, Bufo gargarizans , is widely distributed over the large part of East Asia and is common in Korea (Yang et al., 2001). The species was once classified into Communication occurs when cues given by senders influence Bufo bufo gargarizans, a subspecies of Bufo bufo, the the behavior of receivers (Endler, 1993). Receivers should Eu ropean toad or the commo n toad (Kang and Y oon, 1975 ). benefit from recognizing between desirable and undesirable They are typical ‘explosive breeders’, yearly visiting a cues. When the recognition cues are overlapped, selection breeding pond in early spring, where they are staying up to may favor an optimal balance between accepting 1-3 weeks before returning to terrestrial areas for non- un desirable cues (accep tan c e er rors) and rejecting d e si rable breeding season. The male toads usually experience intense cues (rejection errors), where the balance could be altered scramble competition for possession of females without by changing decision rules or recognition templates of producing advertisement calls. In recent years, unusual receivers (Sherman et al., 1997). mismatched pairing between bullfrogs ( Rana catesbeiana ) The recognition of species and mates may be important and male toads has been observed frequently in some for successful reproduction in anuran amphibians. Species breeding ponds (Fig. 1). The bullfrog is a large, an average of prolonged breeders that have multiple mating opportunities length of 10 cm with weight of 142 g, and exotic invasive mainly use vocalizations in relation to both interspecific species rapidly spreading in the western and southern and intraspecific mate selection (Sullivan, 1983; Wells, Korean Peninsula since being introduced from Japan at the end of 1970 (Kang and Youn, 1994). To date, no certain * T o whom correspondence should be addressed. explanation has been given how it does happen. T el: +82-43-230-3719; Fax: +82-43-233-6263 E-mail: srpark@knue.ac.krIn this paper, we hypothesized that male Asian toads lack ANIMAL CELLS AND SYSTEMS Vo l. 12 No. 2 93 Cheong Seokwan, Hacheol S ung and Shiryong P ark spring of the toad breeding season. We designed the five experiments considering the methods used by Marco et al. (1998). We prepared for a rectangular tank (120 ×50 ×30cm) filled with about 5cm of pond's water for all experiments. We replaced the water after each trial in order not to contaminate the tank with chemicals. W e put stimulus individuals on each end of the tank at ran dom position . Th e stimulus individuals were tied with string 15 cm long to the tank ends so that they were allowed to move for a short distance. We placed a single test male in a small container (20 ×20 × 20 cm) constructed of fiber glass screen into the center of the tank. The test male was acclimatized for two minutes. All experiments were started with removing the container, and we counted the number of attempts to amplex one of the stimulus Fig. 1. Miss-matched amplexus between a bullfrog (bottom) and individuals. We decided the male selected a stimulus several male Asian toads (top). The male toads strongly clasped the su b ject if th ere was an amplexus mo re than 30 second s. W e bullfrog to death. stopped the trial if any amplexus attempt was not observed for 1 0 minutes. an ability o f mate recog nition. Using choice experiments in W e used student’ s t-test to examine the variation of SVL the lab, we tested the hypothesis: whether male Asian toads between stimulus individuals and used Binomial test to discriminate 1) between the sexes of conspecifics, 2) determine whether there is a significant difference between between reproductive states of female toads, and 3) even the observed and the expected frequencies in mate choice between female toads and bullfrogs as a potential mate. experiments. Numerical data in the text are presented as Furthermore, we tested whether the males show size- mean±SD. Data were analyzed using SPSS statistical assortative mating preference using different sizes ofsoftware (v.11.5; SPSS 2002). bullfrogs. This is the first study on the effects of alien species to breeding biology of native species occupying RE SU L T S similar eco lo gical status. W e captured 133 males and 46 females of the Asian toads. MA TERIALS AND METHOD Mean SVL of males was 8.08 cm (±0.67) and female was 10.77 cm (±0.78). Females were significantly larger than We collected the Asian toads at a pond (3617'43"N, males (student’s t-test, t=20.75, p ≤ 0.001). The mean SVL 12730'30"E) in Okcheon Gun, Chungbuk Province, Korea, of used stimulus to ad s and b ullfro gs in each trial are shown in March 1999. W e measured snout-vent lengths (SVL) of in Table 1: there were no significant differences between the toads to the nearest 0.01 mm with vernier calipers and two groups of stimulus individuals in Experiment 1, 2, 3. isolated them by sex. The sex of each toad was determinedHowever, the large size of bullfrogs was significantly larger by the presence of nuptial pads of males. We performedthan small or medium size of bullfrogs as expected. five experiments to investigate the recognition ability of In experiment 1, when similar sizes of a female toad and male Asian toads for species and mate choice: we used a bullfrog were presented to male toads, 7 of 20 males choice experiments to determine whether the males (35%) attempted to amplex female toad while 13 males to discriminate 1) between the sexes of conspecifics, 2) bullfrogs, which was not significantly different from between gravid versus non-gravid females of the similar random (z = 1.34, p = 0.13, Fig. 2). The test males tightly size, 3) even between female toads and bullfrogs as aclasped not only female toad but also bullfrog. The bullfrog potential mate, 4) between small (7~9 cm of SVL) versus more struggled to escape from being amplexed than female large (12~15 cm) stimulus, and 5) between medium (9~12toad, but failed till we stopped the trial at 30 seconds. cm) and large stimulus. As a stimulus, we used bullfrogs In experiment 2, when test males received a choice because we are interested in revealing whether they tend to between a female and a male toad in similar sizes, 9 of 20 have size-assortative selection in mate choice even if the males (45%) chose female over male, which did not bullfrogs are not the same species. We captured the significantly differ from random (z = 0.41, p = 0.45, Fig. 2). o o bullfrogs in Youngjong island (37 29'12"N, 12630'E), The stimulus male produced release calls in amplexus Incheon City, in November 1998. We kept the bullfrogs while the stimulus female did not. Male-male amplexus provided loaches for food in an aquarium till the next never lasted more than 5 seconds in response to the call, 94 ANIMAL CELLS AND SYSTEMS Vol. 12 No. 2 Mate and S pecies Recognition by Male Asian T oads Table 1. Comparisons of body sizes between stimulus 1 and 2 in the five experiments. Mean (±SD) SVL (snout-vent length) of stimulus individuals, where N means number of trials Stimulus 1 Stimulus 2 Experiment (N) Individual SVL (cm) Individual SVL (cm) 1 (20) Female toad 10.79 ± 0.73 Bullfrog 1 1.78 ± 0.17 2 (20) Female toad 09.72 ± 0.28 Male toad 09.39±0.21 3 (20) Non-gravid female 10.75 ± 0.98 Gravid female 10.76 ± 0.95 4 (21) Small bullfrog 07.93 Large bullfrog 13.17 5 (20) Medium bullfrog 11.35 Large bullfrog 14.62 male-biased sex ratio (Sung et al., 2007). This allows male to have few opportunities to amplex a female. This may lead to sexual selection favoring males that actively search for females, but not vice versa. The active males may attempt to vigorously clasp close individuals without discriminating sex, gravid female, and even conspecifics. Due to such a behavioral strategy for male reproductive success, the toads may not use an advertisement call to attract a potential mate. The advertisement call has been extensively used in one of recognition cues indicating male quality (i.e. large males) by female choice (Davies and Fig. 2 . Mate choice by male Asian toads. Experiment 1: female toad ( □ ) vs. bullfrog ( ■ ); Experiment 2: female toad ( □ ) vs. male toad Halliday, 1978; Arak, 1983; Wells, 1988). The western toad ( ■ ); Experiment 3: Non-gravid female toad ( □ ) vs. gravid female (Bufo boreas) is the similar species that lacks this kind of toad ( ■ ); Experiment 4: small bullfrog ( □ ) vs. large bullfrog ( ■); advertisement calls (Marco et al., 1998). Like the Asian Experiment 5: medium bullfrog ( □ ) vs. large bullfrog ( ■ ). Significan t level of binomial test: * p < 0.05, ***p<0.001. toad, the western toads use a se riou s of release calls as o nly recognition cue whether the amplexed ind ividual is ma le or female. while male-female amplexus lasted till we separated paired Males chose larger individuals given a choice, which couples. may be another reproductive strategy to increase the In experiment 3, when test males received a choice probability of selecting correct females rather than males. between a gravid female and a non-gravid female in similar Females are usually about 1.3 times larger than males sizes, 9 of 20 males (45%) chose gravid female over non- (Sung et al., 2007). The sexual dimorphism in anurans has gravid female, which did not significantly differ from been described as resulting from the interaction between random (z = 0.41, p=0.45, Fig. 2). natural and sexual selection (Lande and Arnold, 1983; In experiment 4 and 5, when test males received a choice Ryan, 1985; Arak, 1988). Males tended to favor larger between small or medium vs. large stimulus, the males fe males as a mate because the lar ger fe males lay mo re eggs significantly preferred large ones: 20 of 21 males (95%) in so that males in amplexus increase the number of their small vs. lar ge stimulus experiment (z = 4.15, p < 0.001, Fig. fertilizing eggs (Davies and Halliday, 1977; Arntzen, 2) and 15 of 20 males (75%) in medium vs. large stimulus 1999). It may be true in an excess of females, where males experiment (z=2.24, p=0.02, Fig. 2). may be able to evaluate female size to choose the larger ones. However, in case female choice by male is temporally and spatially limited, the male may attempt to claps a DISCUSSION potential female quickly using size cues as well as release The present results suggest that male Asian toads do notcalls. recognize sex, reproductive state of females, and even In recent years, we frequently observed miss-matched species. The males randomly chose similar sizes of male amplexus of male toads and the bullfrogs in the fields, toads over female toads, bullfrogs over female toads, non- which, in turn, a toad k ept clasping a bullfrog to d eath . The gravid over gravid females. However, the males preferred bullfrogs do not have ribs protect internal organs from large individual to small or middle one. external pressure by toad clasp. Thus, the main reason of As a typical explosive breeder, the Asian toads aggregate miss-matched amplexus by the male toads is due to 1) the synchronously into breeding sites forming high-density lack of recognition cues of conspecifics, 2) the lack of populations, where they have a short breeding period with a communication tools like release calls, and 3) the larger ANIMAL CELLS AND SYSTEMS Vo l. 12 No. 2 95 Cheong Seokwan, Hacheol S ung and Shiryong P ark a population of common toads (Bufo bufo ). A m ph ibi a - R e p ti lia size of bullfrogs than male toads themselves. As an exotic 8: 321-330. invasive species, the bullfrogs are evolutionary absent in Kang EJ and Y oun CH (1994). The settlement and distribution of this country so that it is an unusual phenomenon in nature the introduced bullfrog, Raja catesbeiana, in Korea. nat ur e in these days. conservation report 13: 231-250. We do not know how the male sizes influence male Kang YS and Y oon IB (1975) Illustrated encyclopedia of fauna mating success. However, from the study of the common and flora of Korea Vol 17 Amphibia'Reptila. The Korean toad, when breeding period is short, mating in relation to ministry of education. Seoul. body size is random (Davies and Halliday , 1977; Hoglund Lande R and Arnold SJ (1983) The measurement of selection on correlated characters. E v ol uti o n 37: 1210-1226. and Robertson, 1987). Although small clasped males is often displaced by large ones at the time of spawning, small Marco A, Kesecker JM, Chivers DP, and Blaustein AR (1998) Sex recognition and mate choice by male western toads, Bufo males, considered to be disadvantageous in male-male boreas. Anim Behav 5 5 : 16 31- 16 35. competition, still have some opportunities for mating Olson DH (1989) The ecological and behavioral dynamics of (Davies and Halliday, 1977). Thus, the male mating success breeding in three sympatric anuran amphibians. Ph.D. thesis, in this species is almost density and time dependent. We Oregon State University. more need to investigate the male size effects of mate R y an MJ ( 198 5) T he T ung ara Fr ogs: A S tud y in Sexu al S elect ion selection processes in the Asian toad. and Communication. Univ Chicago Press, Chicago and L o n don . REFERENCES Ryan MJ (1990) Sensory systems, sexual selection, and sensory e xpl oit a ti on. Oxford Surv Evol Biol 7: 157-195. 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