Short Amplexus Duration in a Territorial Anuran: A Possible Adaptation in Response to Male-Male Competition

Abstract

Mating duration is a reproductive behaviour that can impact fertilization efficiency and offspring number. Previous studies of factors influencing the evolution of mating duration have focused on the potential role of internal sperm competition as an underlying source of selection; most of these studies have been on invertebrates. For vertebrates with external fertilization, such as fishes and frogs, the sources of selection acting on mating duration remain largely unknown due, in part, to the difficulty of observing complete mating behaviours in natural conditions. In this field study, we monitored breeding activity in a population of the territorial olive frog, Rana adenopleura, to identify factors that affect the duration of amplexus. Compared with most other frogs, amplexus was short, lasting less than 11 min on average, which included about 8 min of pre-oviposition activity followed by 3 min of oviposition. We evaluated the relationship between amplexus duration and seven variables: male body size, male condition, operational sex ratio (OSR), population size, clutch size, territory size, and the coverage of submerged vegetation in a male’s territory. We also investigated the influence of these same variables, along with amplexus duration, on fertilization rate. Amplexus duration was positively related with clutch size and the degree of male-bias in the nightly OSR. Fertilization rate was directly related to male body size and inversely related to amplexus duration. Agonistic interactions between males in amplexus and intruding, unpaired males were frequent. These interactions often resulted in mating failure, prolonged amplexus duration, and reduced fertilization rates. Together, the pattern of our findings indicates short amplexus duration in this species may be an adaptive reproductive strategy whereby males attempt to reduce the risks of mating and fertilization failures and territory loss resulting from male-male competition.

Ecological and social drivers of neighbor recognition and the dear enemy effect in a poison frog

“…This is because even though Kai rocket frogs share territory boundaries with neighbors for shorter durations than golden rocket frogs, they still defend territories for at least several weeks, which is should provide ample opportunity for males to learn their neighbors' calls. For example, male bullfrogs (Howard 1978) and olive frogs (Chuang et al 2013) also defend territories for several weeks during the breeding season, and both of these species exhibit neighbor recognition and the dear enemy effect (Davis 1987;Chuang et al 2017).…”

Polyandry, Predation, and the Evolution of Frog Reproductive Modes

“…The reasons for this scarcity in parentage and mating system studies may be a combination of the difficulty in observing nocturnal and cryptic mating behaviors and the challenge of genotyping the often large number of progeny produced during mating. In addition, as we have discussed, mating behaviors are often facultative and context dependent (Caldwell 1992;Wells 2007;Chuang et al 2013), thus lowering the likelihood of observing specific behaviors. Finally, the number of researchers focused on mating systems and reproductive modes in frogs is highly biased toward species in temperate zones.…”

“…For example, Hypsiboas faber exhibit facultative parental care depending on the degree of competition from surrounding males; males protect eggs deposited in clay nests when male density in ponds is high (Martins et al 1998). Male Crinia georgiana allocate less time to attracting females and more time to multimale spawning when densities and OSR are high (Byrne and Roberts 2004), and Rana adenopleura shortens amplexus time as an adaptive reproductive strategy to reduce risks of fertilization failures and territory loss resulting from male-male competition when OSR are high (Chuang et al 2013). To date, we know of no examples that clearly show plasticity in egg deposition site and amplexus site as a response to male-male competition or perceived risk of sperm competition.…”

“…Amphibian mating systems offer plenty of opportunity for loss of male fitness through simulta-neous polyandry because fertilization is external in most species, breeding aggregations are often large, and operational sex ratios (OSR) can be highly skewed in favor of males (Kvarnemo and Ahnesjo 1996;Byrne and Roberts 2004). Simultaneous polyandry is likely more common in explosive breeders that congregate around ponds and lakes for reproduction and have fully exposed amplexus, because a large number of males are actively searching for females (Wells 1977;Chuang et al 2013), increasing the probability that more than one male will try to fertilize a female's clutch. The probability of simultaneous polyandry will be smaller in prolonged breeders that congregate around water bodies at lower densities and will be much smaller in breeders that do not congregate around water (such as direct-developing species), in species that actively defend territories or nest sites (Chuang et al 2013), or in species that hide from competitors during amplexus (Ovaska and Rand 2001;Mangold et al 2015).…”

“…Simultaneous polyandry is likely more common in explosive breeders that congregate around ponds and lakes for reproduction and have fully exposed amplexus, because a large number of males are actively searching for females (Wells 1977;Chuang et al 2013), increasing the probability that more than one male will try to fertilize a female's clutch. The probability of simultaneous polyandry will be smaller in prolonged breeders that congregate around water bodies at lower densities and will be much smaller in breeders that do not congregate around water (such as direct-developing species), in species that actively defend territories or nest sites (Chuang et al 2013), or in species that hide from competitors during amplexus (Ovaska and Rand 2001;Mangold et al 2015). Our hypothesis is that the selective mechanism driving diversification of reproductive modes is not simply predation of eggs and tadpoles but that intrasexual selection, specifically the escape from male-male competition for fertilization, also contributes to the observed diversification in reproductive modes among frogs.…”