Patterns of oviposition site selection of four sympatric species of amphibians in ephemeral streams

doi:10.21203/rs.3.rs-4709228/v1

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Patterns of oviposition site selection of four sympatric species of amphibians in ephemeral streams

https://doi.org/10.21203/rs.3.rs-4709228/v1

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Many oviparous animals are selective about where to lay eggs, as this greatly affects their offspring’s survival. Theoretically, species sharing the same habitat are expected to experience similar selective pressures, leading to the prediction that they might share similar oviposition preferences. However, this hypothesis has not yet been tested. In this study, through an extensive field survey, we examined the oviposition site selection of four sympatric amphibian species (Rana uenoi, Hynobius quelpaertensis, Bombina orientalis, and Dryophytes japonicus) that reproduce in the same natural ephemeral stream. Our focus was on understanding how abiotic and biotic factors influence their reproductive choices. We primarily found that drought avoidance is a universal selective pressure affecting all species, with a tendency to avoid laying eggs in smaller pools prone to drought. Species-specific responses to leaf litter and canopy coverage were observed, but none of the species' oviposition choices correlated with the quantity of stones in pools. We also explored biotic influences, revealing species-specific trends in the selection of pools with conspecific and heterospecific juveniles, predators, and mosquito larvae, indicating a complex ecological interplay. These findings highlight the complexity of ovipositional patterns in animals, where decisions are not driven solely by a single factor such as the avoidance of predators or competitors but also by intricate assessments of multiple factors. The study highlights that amphibian oviposition in ephemeral streams is influenced by a diverse interplay of biotic and abiotic factors, essential for understanding their reproductive strategies in dynamic environments.

ephemeral pool

anuran

reproduction

predator avoidance

conspecific avoidance

multiple factors

Where and when eggs are deposited greatly impacts offspring survival in egg-laying species, particularly in fluctuating environments. Despite extensive research on egg-laying behaviours, mainly focusing on single species, there is a knowledge gap regarding the behaviour of multiple species sharing the same habitat. We hypothesized species sharing the same habitat might exhibit analogous egg-laying choices due to shared selective pressures. A thorough field study on four amphibian species in an ephemeral stream reveals a shared trend of avoiding drought among all species. Additionally, various biotic and abiotic factors influenced egg-laying decisions differently across species. Surprisingly, factors detrimental to juvenile survival, such as predators or competitors, were not consistently avoided in natural systems.

Animals have evolved diverse parental care strategies to increase the survival of their progeny (Clutton-Brock 1991). For example, many species show nesting, guarding, or brooding behaviours to directly protect and care for their young (Royle et al. 2012). Parental care varies widely between taxa: many birds and mammals have evolved the costly parental feeding while other vertebrates and invertebrates often have simpler forms of parental behaviours that do not involve direct feeding of their offspring (Balshine 2012; Trumbo 2012). These simpler forms include the lack of post-laying care. In such animals, the choice of where and when to lay eggs has profound consequences on the reproductive success, especially when the eggs and/or juvenile stages are immobile or confined to local regions (Doak et al. 2006; Refsnider and Janzen 2010). Thus, natural selection favours the ability of parents to prefer oviposition sites that increase the chance of offspring survival, their performance, or even parental survival (Resetarits Jr. 1996; Brodin et al. 2006; Hirayama and Kasuya 2013; Dimitrie and Benard 2023). There has been ample evidence of the selective oviposition in wide array of taxa including insects, reptiles, amphibians, and fish (Schwarzkopf and Brooks 1987; Spieler and Linsenmair 1997; Mokany and Shine 2003a).

Oviposition site selection is more likely to evolve under conditions when (i) potential egg-depositing sites are temporally and spatially heterogeneous in terms of suitability for offspring survival, (ii) juveniles are unable to disperse from the egg-spawning spots, and (iii) parents are able to evaluate suitable sites by comparison of alternatives (Resetarits Jr 1996). Species that laying eggs in pools of ephemeral streams present an excellent platform for studying oviposition site selection because the habitat structure often meets all of the above conditions: (i) potential oviposition sites are locally scattered, allowing parents to compare the suitability of multiple pools, (ii) the characteristics (i.e. suitability as a egg-laying site) of pools are often both spatially and temporally varying, and (iii) juveniles are restricted to the pools where mothers laid eggs unless disturbed (e.g. heavy rains) (Buxton and Sperry 2017). Indeed, species of various taxa in ephemeral streams have been extensively studied for their selective oviposition (Spieler and Linsenmair 1997; Peckarsky et al. 2000; Murphy 2003; Baek et al. 2021; Gould et al. 2021).

Amphibians have served as an excellent platform for studying selective oviposition. Both biotic and abiotic factors have been demonstrated to affect female choice of amphibians. Females often choose oviposition sites based on the degree of risk from predators, con- or heterospecifics. Predators are ubiquitous problems for eggs/juveniles and yield negative consequences for offspring survival not only through direct predation but also through non-consumptive effects (Preisser et al. 2005; Buxton and Sperry 2017; Buxton et al. 2017). Naturally, many studies have revealed the presence of predator avoidance (Buxton and Sperry 2017; Resetarits et al. 2021). The presence of con- or heterospecifics of related taxa may function as predators (through cannibalism) or putative competitors but may also give a cue about site quality (Dillon and Fiaño 2000; Rudolf and Rödel 2005; Gould et al. 2020). The risk of cannibalism also affects female choice, and females may avoid laying eggs in the sites with higher risk of cannibalism (Iwai et al. 2007); however, reducing the risk of cannibalism does not appear to be universal, with some notable exceptions (Poelman and Dicke 2007; Rojas 2014). Food availability, such as leaf litter, could also affect female choice especially when egg-laying sites are small and isolated (McDiarmid and Altig 1999; Stoler and Relyea 2021; Magee-Christian and Earl 2022). When it comes into abiotic factors, temperature and water-holding potential are demonstrated as main selective agents because the avoidance of thermal damage or desiccation is critical for juvenile survival and development (Spieler and Linsenmair 1997; Goldberg et al. 2006).

To date, studies on female oviposition preference have mostly been conducted on a single species, and studies that examined the selective oviposition in multi-species level are surprisingly scarce (Miaud 1995; Ortiz-Ross et al. 2020). However, various species co-occur in the same habitat and one can predict that species that co-occur in the same habitat would be under similar selective pressures for oviposition or affect each other interactively. In this study, we investigated the oviposition choice of multiple amphibian species that reproduce in the same ephemeral stream to (i) identify biotic and abiotic factors that correlate with female oviposition choice for each species and (ii) investigate that species that occur in the same habitat (thus likely to be under similar selective pressures) show similar oviposition decisions.

We formulated predictions regarding assemblage-wide or species-specific responses to several abiotic and biotic factors. About assemblage-wide responses, we firstly predict that natural selection may shape female behaviours to avoid the pools with high risk of desiccation (Spieler and Linsenmair 1997; Goldberg et al. 2006). Second, females would selectively lay eggs in pools with sufficient organic matter or potential food materials for tadpoles (Kern et al. 2013; Magee-Christian and Earl 2022). Third, predation (or cannibalism) risk might also affect female choice. This includes (i) the avoidance of pools that are already occupied by aquatic predators and (ii) laying eggs in pools with potential refuges (Resetarits Jr and Wilbur 1989). In contrast, there are certain factors that we predict species-specific or circumstantial responses. First, in regards to the presence of con-/heterospecific eggs or juveniles, we had two competing predictions. Females might avoid to lay eggs in pools with con-/heterospecific juveniles to avoid the risk of cannibalism. Alternatively, the presence of other eggs or juveniles may be an indicator of pool quality or decrease individual risk of predation through dilution (Rudolf and Rödel 2005). In that case, females may selectively lay eggs in pools where other amphibian larvae are already present. Second, canopy coverage may also affect female choice in two different ways. Pools with less canopy coverage are directly exposed to sunlight, which can cause faster evaporation of water and increase the risk of overheating. In that case, we predict the females to avoid laying eggs in pools under low canopy coverage. However, under the direct sunlight, the water temperature can be maintained higher than those under high canopy coverage which can boost development, a favourable condition in ephemeral streams (Oh et al. 2021). In the latter scenario, we predict females to selectively lay eggs in pools under higher canopy coverage.

Study species and environments

We conducted this study within Bangcheon stream in Jeju Island, South Korea (N33.4722, E126.5432) from March to August, 2021. Jeju Island, a volcanic island, is largely covered by basalt layers that quickly drain surface water underground. As a consequence, in most streams, including our study site, water flows only during rain. In these ephemeral streams, oviposition sites were available in the form of pools of varying sizes. Along the stream, the pools were patchily distributed, with distances varying from less than a metre between each pool and its nearest neighbour (Fig 1A). Each pool remained isolated until rainfall occurred. Heavy rains usually swept most, if not all, organisms in the pools. Rains did not alter the location of each pool, although some pools temporarily merged into larger ones just after heavy rains. There were no fish in our study sites.

We chose a study site occupying approximately 730 m² area. This area spanned a longitudinal distance of ~120 metres along the stream and contained 321 different pools, as estimated a day after rain when all identifiable pools were filled with water. In the study site, three frogs and one salamander species mainly occurred and reproduced during our study period from 8th March to 24th August, 2021: Rana uenoi, Hynobius quelpaertensis, Bombina orientalis, and Dryphytes japonicus. While Kaloula borealis also laid some eggs in our study site, their numbers were only a few and we did not include K. borealis in our analysis. The timing of reproduction largely overlapped between R. ueonoi and H. quelpaertensis, and between B. orientalis and D. japonicus (Fig. 1B). For R. uenoi, although reproduction started before our study period, we only analysed the eggs laid during our study period.

Field surveys to study oviposition preference in relation to abiotic and biotic factors

To monitor the oviposition choices of females, we visited each pool within our study site between 0800 and 1300 on almost every non-rainy day of our study period. We refrained from visiting the stream on rainy or foggy days for the safety of the experimenters. Each pool was marked with a unique number on a rock surface adjacent to it, using non-toxic silicone.

We recorded several biotic and abiotic characteristics of each pool daily (see Table 1): (i) whether water was present or absent (Dry; a binary variable), (ii) the amount of leaf litter (Leaves; an ordinal variable), (iii) the quantity of stones as potential refuges (Stones; ordinal), (iv) the turbidity of the pool water (Turbidity; ordinal), (v) the presence of aquatic predators (Predators; binary, specie names are listed in Table 1), and (vi) the presence of mosquito larvae (MosqLarvae; binary). Variables concerning the presence of amphibian juveniles were coded for each species as follows: (vii) the presence of newly spawned eggs (NewEggs; binary), (viii) the presence of conspecific eggs that were not newly spawned (ConEggs; binary), (ix) the presence of conspecific tadpoles (ConTadpoles; binary), (x) the presence of heterospecific eggs that were not newly spawned (HeteroEggs; binary), and (xi) the presence of heterospecific tadpoles (HeteroTadpoles; binary).

Although we initially started by counting the number of con-/heterospecific eggs and tadpoles, we decided to use these variables in binary form due to the heterogeneity of errors among pools; pools with larger size, more turbid water, or a higher number of stones were more likely to have inaccuracies in their counts. Leaves, Stones, and Turbidity (all ordinal variables) were subjectively but consistently assessed and rated by a single experimenter (DO) throughout the survey. The criteria can be found in Table 1. Mosquito larvae have primarily been described as competitors, but also as predators or prey of tadpoles (Blaustein and Margalit 1994, 1996; Mokany and Shine 2003b). While we were unsure of the ecological relationship between our studied species and mosquito larvae, we nonetheless analysed correlational patterns between their presence and female oviposition choice. Invertebrates other than mosquito larvae, such as mayfly or Chironomidae larvae, were also occasionally present, but their occurrence was very low (less than 0.3% of pools) and thus were not included in our analysis.

Occasionally, a pool was transiently divided into multiple pools (under consecutive non-rainy days), or two pools merged together (this rarely happened just after rain). When a pool divided, we recorded the characteristics of each separate pool and used the averaged value for analysis, retaining the original pool ID for these transiently separated pools. When pools merged, we noted the characteristics of the merged pool and applied them to both original pools. During the breeding seasons of R. uenoi and H. quelpaertensis, from March to May, all 321 pools were surveyed. However, for the breeding seasons of B. orientalis and D. japonicus, from 5th May to August, we limited the survey to 192 pools in the lower parts of our study site, where more oviposition activities were observed. This reduced scale was necessary to complete the surveys in a timely manner, as the increased oviposition activities resulted in longer times required to survey each pool.

Egg clutches from different females were clearly distinguishable for R. uenoi and H. quelpaertensis, in which eggs were either densely grouped together or found in a sac. However, distinguishing eggs from different mothers in the same pool posed a challenge for B. orientalis and D. japonicus. This difficulty arose because not only was the number of eggs highly variable, but also the boundaries between different egg clutches were not clearly defined. Therefore, instead of counting the number of egg clutches, we employed a binary variable to denote whether newly spawned eggs were found in each pool each day. This approach, however, resulted in an inability to detect instances where more than one female laid eggs in the same pool on the same day.

In addition to the pool characteristics that we surveyed daily, we also measured (i) pool volume (PoolVolume) and (ii) canopy coverage (CanopyCover). Unlike the aforementioned variables, these two characteristics were measured only once during our study period. While PoolVolume could change daily (decreasing gradually due to evaporation but increasing during rain), all pools were expected to be simultaneously affected by these changes. Therefore, we measured PoolVolume only once and used this as a size index for each pool. PoolVolume was estimated just after a rainy day when all pools were fully filled with water. The three-dimensional shape of each pool was highly irregular; thus, we crudely estimated PoolVolume by multiplying the surface area by the deepest depth of each pool. The surface area was measured by aerial photography using a drone (MAVIC PRO, DJI, Guangdong, China), with a ruler placed next to each pool for area calibration. CanopyCover was estimated using a mobile phone camera (Galaxy Note 8, Samsung, Seoul, South Korea). This measurement was taken on a summer day when foliage was dense. We positioned the camera just above the suspected centroid of the water surface, facing upwards, and took a photograph. The percentage of plant cover in the image was then calculated, using this percentage as an index of CanopyCover with ImageJ 1.80 (National Institute of Health, Maryland, USA). The camera’s angle of view was 77°, as specified by the manufacturer.

Abiotic factor analysis

We considered Dry, Leaves, Stones, Turbidity, PoolVolume, and CanopyCover as abiotic factors that could potentially affect female oviposition choice. All analyses were conducted separately for each species. Firstly, we calculated a representative index for each variable for each pool, generating a pool-level dataset. For Dry, we calculated the proportion of the days that each pool found to be dry during the breeding season of each species. For Leaves, Stones, and Turbidity, we first examined whether the intra-pool variation of each variable across the study period was smaller than the inter-pool variation. For this, we employed the intraclass correlation coefficient (ICC) test in the ‘irr’ package in R, using a one-way consistency model (Koo and Li 2016). Within-pool variability was lower than among-pool variability for all three variables (all P < 0.001, estimated ICC ranged from 0.39 to 0.77). Then, for each pool, we averaged each variable across the breeding season and used these averaged values to characterise each pool. PoolVolume was log-transformed to reduce distributional skewness. After all these processes, we had one representative value for each abiotic factor for each pool. We excluded transiently appearing pools in the abiotic factor analysis (i.e., when either a pool was divided into multiple pools during consecutive non-rainy days due to the exposure of bottom surfaces, or multiple pools were connected to each other just after rain) because averaging across the entire breeding season was impossible for those temporary pools.

As an index of each pool's oviposition frequency, we employed two different methods depending on the species. For R. uenoi and H. quelpaertensis, we used a binary variable to indicate whether eggs were found in each pool at least once during the breeding season. This approach was chosen because (i) the total number of egg clutches per pool was generally one or a few, and (ii) a small fraction of pools (14% for R. uenoi and 7% for H. quelpaertensis) were used for oviposition. Conversely, for B. orientalis and D. japonicus, a higher number of pools were used for oviposition (56% and 36%, respectively), with each pool often being used multiple times on different dates. Therefore, we counted the number of days new eggs were found in each pool throughout the breeding season and used this count variable for our analysis.

We fitted generalised linear models (GLZs) to examine the effect of abiotic variables on female oviposition choice. Firstly, we examined the presence of multicollinearity among predictors and found that Leaves and Turbidity were highly correlated (Pearson’s r > 0.78 for all species data). To resolve the multicollinearity issue, we removed the Turbidity variable from further analysis, leaving only five abiotic factors (Dry, Leaves, Stones, Pool Volume, and Canopy Cover). For R. uenoi and H. quelpaertensis, we fitted binomial GLZs using the binary response of whether each pool was used for oviposition at least once and the five abiotic factors as predictors. For B. orientalis and D. japonicus, we used the number of days new eggs were found during the breeding season for each pool as a response variable and the abiotic factors as predictors. Overdispersion was detected when we fitted Poisson GLZs, so we instead fitted negative binomial GLZs (Lindén and Mäntyniemi 2011). Visual inspections of predictors and our response variables suggested putative polynomial relationships for Leaves and PoolVolume for B. orientalis and D. japonicus; thus, we additionally included quadratic terms of Leaves and PoolVolume for these two species. We did not include interaction terms in our predictors because (i) we did not specifically predict interactive effects among the predictors, and (ii) with five main predictors, including unplanned interaction terms leads to the addition of 10 extra predictors (more when polynomial terms are simultaneously considered) for each species, which makes interpretations challenging in our multi-species datasets.

To estimate the parameters of variables and predict their effects, we applied multimodel inference and performed model averaging using the ‘MuMIn’ package (Grueber et al. 2011). We averaged the parameters of models that appeared within the 0.95 cumulative sum of AIC weights using full averaging. The full averaging is a type of shrinkage estimator and assumes that the parameter values of factors that do not appear in each model are zero, thus yielding rather conservative results.

Biotic factor analysis

We considered Predators, MosqLarvae, ConEggs, ConTadpoles, HeteroEggs, HeteroTadpoles as biotic factors that could potentially affect female oviposition site choice. Unlike abiotic factors, which did not vary much throughout the breeding season within each pool, biotic conditions changed frequently; thus, generating and analysing averaged pool-level data was inappropriate. The most ecologically relevant approach may be analysing each day separately, as the female's decision was made by comparing the conditions of currently available pools. To achieve this, we first excluded pools that had never been used during the study period from the analysis. We considered that these pools were not used for oviposition, regardless of the biotic conditions, likely because the abiotic conditions were not favourable to frogs. For example, pools that were substantially smaller than other pools were never used for oviposition in all four species. Thus, we used the data of biotic conditions among the pools that had been used for oviposition at least once for each species. We also excluded transiently appearing pools from the analysis, as well as the data from dates when no new oviposition was observed. The latter was necessary to incorporate ‘date’ into the statistical models.

Next, we generated a dataset with 8 binary factors for each day and each species: whether each pool had (i) ConEggs without ConTadpoles, (ii) ConTadpoles without ConEggs, (iii) both ConEggs and ConTadpoles, (iv) HeteroEggs without HeteroTadpoles, (v) HeteroTadpoles without HeteroEggs, (vi) both HeteroEggs and HeteroTadpoles, (vii) Predators, and (viii) MosqLarvae (all binary variables). Then, we fitted generalized linear mixed models (GLMMs) using the above eight factors as predictors, pool ID and each date as random factors to account for temporal and spatial blocks (Bolker et al. 2009).

We applied multi-model inference and averaged the parameters of models that appeared within the 0.95 cumulative sum of AIC weights using full averaging.

Correlational patterns between abiotic factors and female oviposition choice

The results are summarised in Tables 2-4 (detailed statistics) and Figs. 2,3. In all four species, PoolVolume and Dry consistently affected the oviposition choice of females; all species tended to avoid laying eggs in pools where the risk of desiccation was higher. Also, all species were more likely to lay eggs in larger pools over smaller ones, except for B. orientalis, which laid more eggs in intermediate-sized pools compared to smaller or larger ones. In contrast, we found no evidence that Stones affected female oviposition choice in any of the species. The effect of Leaves and CanopyCover varied among species. H. quelpaertensis and B. orientalis females laid eggs more frequently in pools with more leaf litter and in pools with intermediate-amount of leaf litter, respectively. In contrast, Leaves did not affect the oviposition choice of R. uenoi and D. japonicus. In terms of CanopyCover, D. japonicus females were more likely to lay eggs in pools under higher canopy coverage, while other species did not show such patterns.

Correlational patterns between biotic factors and female oviposition choice

The correlational patterns between biotic factors and female oviposition preferences were species-specific (see Table 3 for detailed statistics, Table 4 for the summary, and Fig. 3 for plots). The effect of predators and mosquito larvae was not analysable for R. uenoi and H. quelpaertensis, as both predators and mosquito larvae were scarcely present during their breeding seasons.

Regarding con-/heterospecific larvae, in R. uenoi, we found a tendency for females to lay eggs in pools with ConEggs. This pattern was opposite in H. quelpaertensis, where females showed a preference to lay eggs in pools without ConEggs (Fig. 3). All other factors remained insignificant for both species. In B. orientalis, we did not find any patterns related to either ConEggs or ConTadpoles. However, female B. orientalis showed a preference to lay eggs in pools with HeteroEggs but avoided HeteroTadpoles (Fig. 3). In contrast, female D. japonicus showed a preference to lay eggs in pools containing ConEggs regardless of the presence of ConTadpoles (Fig. 3).

In regards to Predators and MosqLarvae, both B. orientalis and D. japonicus preferred laying eggs in pools with MosqLarvae. D. japonicus also showed a preference to lay eggs in pools with Predators (Fig. 3).

Our results firstly reveal that the risk of drought is an important factor in oviposition site choice, shared by all four species; all species selectively laid eggs in pools where the risk of pool desiccation was lower. This is reflected in the patterns where all species avoided laying eggs in small-sized pools and in those that had experienced more frequent drought conditions. These results firmly demonstrate that avoiding desiccation is a universal selective pressure that shared by all studied species. The results also align well with accumulated evidence that many animals evolved to lay eggs in places with lower risk of desiccation in ephemeral environments (Rudolf and Rödel 2005; Goldberg et al. 2006; Kern et al. 2013; Baek et al. 2021). We additionally explored the alternative possibility that the observed smaller pool avoidance arose simply because smaller pools, which have a higher risk of desiccation, were less available than larger pools due to being dry for more days. To examine this possibility, we generated another pool-level dataset using a subset of the original data, but only including the dates when more than 95% of all pools contained water. We then conducted the same analyses for all four species. The results and trends generally aligned well with the main results for all four species (Fig. S2); pool size remained an important attribute of oviposition site selection. This suggests that the observed trends in the main results are not merely due to the availability of the pools, but rather to the females’ evaluation of future desiccation risk.

The results that B. orientalis laid more eggs in intermediate-sized pools corroborates a previous study, even though larger pools are less likely to experience drought (Baek et al. 2021). One potential reason is that the water temperature in large pools remains cooler even in summer, thus delaying the development time of juveniles (Álvarez and Nicieza 2002). Ephemeral streams are not a favourable environment juveniles of some species due to the high risk of desiccation, flooding, scarcity of food sources, and limited space for movement (Gould et al. 2022). Thus, faster development time is often preferred in ephemeral streams (Richter-Boix et al. 2011; Oh et al. 2021). In this context, the avoidance of larger pools can be adaptive because juvenile development is more rapid in smaller-sized pools where the water temperature can easily warm during the daytime (see Fig. S3 showing that large pools were cooler than small pools in our study site). However, it is still uncertain why the other species do not exhibit similar large-pool avoidance behaviours. The breeding seasons of R. uenoi and H. quelpaertensis are before summer, thus they may be adapted to lower temperatures. Also, D. japonicus lays a substantially larger number eggs at once than B. orientalis; thus, D. japonicus may require more space for their progeny, which could also lead to the absence of large-pool avoidance.

For the rest of the abiotic factors, we found that oviposition choice was either species-specific or not present at all. Firstly, the amount of leaf litter was correlated with oviposition choice in two species: H. quelpaertensis and B. orientalis. Leaf litter is one of the main food sources for tadpoles (McDiarmid and Altig 1999), so it is not surprising that these two species avoided pools with less leaf litter. The reason for the avoidance of pools with a large amount of leaf litter in B. orientalis may be that those with the highest level of leaf litter at our study site were almost filled with it, thus being highly turbid, leaving less space for tadpole movement and probably having a low amount of oxygen. In contrast, during the breeding season of H. quelpaertensis (early spring when new leaves had not yet proliferated), most of the leaf litter was the remnants of the previous year, so no pools were fully filled with leaf litter. This phenological difference may affect the differences between the two species. The reasons why the other two species, R. uenoi and D. japonicus, did not show any preference for leaf litter is puzzling. Ecological and behavioural differences may be a potential explanation; R. uenoi and D. japonicus lay substantially more eggs in a single pool than the other two species (several hundreds versus 10–100 eggs). Therefore, R. uenoi and D. japonicus may be better equipped to alleviate the costs of cannibalism and utilise alternative food sources (e.g., through cannibalism) compared to the other two species. This may explain the species-specific responses to the amount of leaf litter.

Both canopy coverage and the presence of stones were hardly correlated with oviposition choice, except for D. japonicus, which preferentially laid eggs in pools with open canopies. We had two competing predictions for canopy coverage, and D. japonicus females were more likely to lay eggs in pools that were at a higher risk of desiccation but warmer. As D. japonicus selectively lay eggs in larger-sized pools, this may alleviate the risk of desiccation. The lack of correlation between the amount of stone and oviposition preference suggests that the presence of potential refuges is not a strong driver of oviposition site selection. In our study sites, predation pressures from the predators that refuges could benefit (e.g., terrestrial predators) may not be strong.

In terms of biotic factors, the presence of conspecific eggs remained significant for all species except in B. orientalis but with contrasting trends; both R. uenoi and D. japonicus preferred to lay eggs in pools with conspecific eggs, while H. quelpaertensis avoided the pools with conspecific eggs. The response of H. quelpaertensis females corroborates the prediction that females would lay eggs where the risk of cannibalism is low (Spieler and Linsenmair 1997; Iwai et al. 2007). While ovipositing in pools where conspecific eggs are already present does not seem intuitive, it has been reported various insect and amphibian species (Hoffmann and Resh 2003; Rudolf and Rödel 2005; Raitanen et al. 2014). The Rana genus (including R. ueonoi) is a renowned group with explosive breeding and synchronised hatchings. A few days intervals in egg laying may not increase the degree of cannibalism in R. uenoi but could benefit juveniles through dilution effects (Petranka and Thomas 1995; Watt et al. 1997). D. japonicus also preferred to lay eggs in pools with conspecific eggs. Possibly, during the breeding seasons of R. uenoi and H. quelpaertensis, pools were mostly empty, leaving a variety of options for females on where to lay eggs after avoiding the filled ones. However, during the breeding seasons of B. orientalis and D. japonicus, a greater number of pools (that were probably preferred) were already filled on many days, thus the costs of choosing empty and likely less-preferred pools may not outweigh the benefits of choosing filled but more-preferred pools. Additionally, the preference to oviposit in pools that already occupied might have adaptive advantage in ephemeral pools because it can supply additional nutrient via cannibalism or decrease predatory risk through dilution effects (Hoffmann and Resh 2003; Doody et al. 2009; Buxton and Sperry 2017; Gould et al. 2021). This may also explain the preference of B. orientalis to oviposit in pools with heterospecific eggs. However, the cost of cannibalism should be greater when confronted with tadpoles, which in consequence resulted in no preference or avoidance of pools with only tadpoles present.

Unexpectedly, B. orientalis did not show any avoidance of pools with conspecific juveniles. This contrasts with a previous finding that showed conspecific avoidance (Baek et al. 2021). The discrepancy between Baek et al.’s study (2021) and ours may be due to the sampling interval; Baek et al. sampled twice per week, while we conducted the survey on a daily basis. Thus, it is possible that, in Baek et al.’s study, those that laid eggs in pools with others’ juveniles were quickly cannibalised, so that an intermittent survey would not reveal the true oviposition patterns. Indeed, in their own study, most of the newly spawned eggs were cannibalised under the presence of conspecific tadpoles within 24 hours. Considering that (i) egg cannibalism commonly occurs in this population (Baek et al. 2021; Oh et al. 2021), and (ii) there were always some available pools without conspecifics throughout the seasons, it is unclear why B. orientalis did not show any avoidance of conspecific juveniles.

While our initial prediction was the avoidance of both predators and mosquito larvae, our results show the opposing evidence; both B. orientalis and D. japonicus were more likely to lay eggs in pools with mosquito larvae, and D. japonicus even laid more eggs in pools with predators. One potential reason behind this observed pattern may be that the pool preference of predators and mosquitoes matches that of frogs. Indeed, desiccation risk has been reported to drive oviposition site selection in predatory species (Lambret et al. 2018). In our data, there were positive correlations between the number of days new eggs were found and the number of days predators were present for each pool (Fig. S3). The same correlations were found with mosquito larvae, some of which have also been demonstrated to prefer larger-sized pools (Saward-Arav et al. 2016) (Fig. S3). Therefore, there may be conflicting pressures in the wild; while avoiding organisms with any negative interactions may benefit individuals, the choice is not simple in reality because the competitors or predators can share similar preferences for certain abiotic conditions (Giao and Godoy 2007), such as those with a low risk of desiccation. The oviposition patterns in D. japonicus could be observed if their preference for abiotic factors overrides predator/competitor avoidance. This contrasts a previous finding that the risk of predators was prioritised over desiccation risk in the pantless treefrog which lay both aquatic and arboreal eggs (Touchon and Worley 2015). Whether D. japonicus and B. orientalis indeed show preference for, or an aversion to, pools with predators or mosquito larvae requires experimental work in manipulative environments. However, our results imply that such preference/avoidance may conflict with abiotic condition preference if predators or competitors share similar preferences.

Will the observed selective oviposition have fitness consequences? Although our data cannot confirm this due to the inability to track individuals, most of the eggs and juveniles were flushed out during occasional heavy rain before they become froglets. We observed only a few individuals that became froglets at our study site, but even it was unclear whether they had grown in the same pool or been flushed down from upstream. Therefore, we consider that the oviposition choice of females may have limited consequences only during the eggs and early juvenile stages before subsequent heavy rain events. Nevertheless, natural selection would favour an aversion to pools with a higher risk of desiccation, as this could lead to the complete death of the progeny at any time. After accounting for avoiding desiccation, the impact of other abiotic/biotic factors may become not straightforward because pools with a low risk of desiccation are fewer, making the choice multifaceted. This assumes that female amphibians prioritise the risk of desiccation over other factors when selecting an egg-laying site, which remains to be tested.

Ephemeral environments are complex systems with many biotic and abiotic factors interacting. In these circumstances, females may not decide where to lay eggs based on individual factors but rather use a holistic evaluation of the overall adequacy of the sites (Stahlschmidt and Adamo 2013; Gould et al. 2021). Although our study is observational and therefore does not reveal the causality of the relationship, the important insights that can be drawn from our study include (i) avoiding drought appears to be a universal driver shared by all species in the ephemeral streams, (ii) both abiotic and biotic factors correlate with the oviposition choice of females, showing species-specific patterns, and (iii) factors that apparently have negative consequences for juveniles, such as predators/competitors, are not always avoided. This could be because predators or competitors share similar pool preferences; thus, avoiding these organisms could lead to laying eggs in less profitable pools from other perspectives (Marsh and Borrell 2001; Gould et al. 2021). We consider that employing cost-benefit approaches, which account for the interplay of multiple factors, would advance our understanding of female oviposition behaviour in natural systems.

Author contributions

CK, DO, and US designed the study. DO and JL conducted field studies. DO, J-Y A, CK performed data analyses. DO and CK wrote the first version of the manuscript. All authors contributed in revising the manuscript.

Acknowledgments

We appreciate Sangeun Gwak, Seokhyun Lee for their invaluable assistant during the field survey. This study was supported by National Research Foundation of Korea (NRF-2019R1C1C1002466, RS-2024-00333709) and Creative-Pioneering Researchers Program through Seoul National University.

Competing interests

We declare no conflict of interest.

Ethics approval

All field studies were approved by Mokpo National University Institutional Animal Care and Use Committee (MNU-IACUC-2021-002). We adhered to the guidelines for the treatment of animals in behavioural research and teaching (Buchanan et al. 2012).

Data availability

Data available from Figshare repository (https://doi.org/10.6084/m9.figshare.25009685.v2) (Oh et al. 2024)

Code availability

The code used for analyses and figures in this manuscript are available from Figshare repository (https://doi.org/10.6084/m9.figshare.25009685) (Oh et al. 2024)

Consent to participate

Not applicable

Consent for publication

Not applicable

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Table 1. Variables measured for each pool during the field survey.

Variable	Explanation	Measured interval	Measured scale	Criteria used
Dry	Whether each pool had water or not	Daily	Presence/absence (binary)
Leaves	The amount of leaf litter	Daily	0 – 4 (ordinal)	0: No leaf litter 1: A small amount of leaf litter covering less than 5 % of pool bottom 2: Leaf litter covering more than 5% but less than 1/3 of the pool bottom 3: Leaf litter covering about half of the pool bottom 4: Pool bottom fully covered with leaf litter
Stones	The amount of stones	Daily	0 – 3 (ordinal)	0: No stones 1: A few small stones that covered less than 1/3 of the pool bottom 2: Stones covering about half of the pool bottom 3: Stones fully covering the pool bottom
Turbidity	The degree of water turbidity	Daily	0 – 3 (ordinal)	0: Fully transparent with no signs of turbidity 1: Low turbidity; slight murkiness detectable, but underwater visibility remains clear 2: High turbidity; underwater visibility is reduced but still possible at close range 3: Severe turbidity; underwater visibility is virtually impossible
NewEggs	Whether new eggs, oviposited the previous night, were found	Daily	Presence/absence (binary)
ConEggs	The presence of conspecific eggs	Daily	Presence/absence (binary)
ConTadpoles	The presence of conspecific tadpoles	Daily	Presence/absence (binary)
HeteroEggs	The presence of heterospecific eggs	Daily	Presence/absence (binary)
HeteroTadpoles	The presence of heterospecific tadpoles	Daily	Presence/absence (binary)
Predators	The presence of aquatic insect predators	Daily	Presence/absence (binary)	Cybister chinensis Laccotrphes japonensis Notonecta triguttata Odonate larvae
MosqLarvae	The presence of mosquito larvae	Daily	Presence/absence (binary)
PoolVolume	Pool volume	Once	Continuous
CanopyCover	Canopy coverage	Once	Percentage

Table 2. Summary statistics of the abiotic factor analysis. We highlighted the cells when there existed evidence supporting the presence of the effect of each factor (grey when P < 0.1; yellow when P < 0.05).

Species	Abiotic variable	*Estimate*	*S.E.*	z	P
Rana uenoi	PoolVolume	1.10	0.16	6.95	<0.001
	Dry	-3.82	2.29	1.67	0.10
	Leaves	-0.15	0.26	0.57	0.57
	CanopyCover	0.00	0.01	0.31	0.76
	Stones	-0.03	0.13	0.24	0.81
Hynobius quelpaertensis	PoolVolume	0.95	0.24	3.85	<0.001
	Dry	-10.92	5.99	1.82	0.07
	Leaves	1.27	0.52	2.45	0.01
	CanopyCover	0.01	0.01	0.56	0.57
	Stones	0.06	0.2	0.29	0.77
Bombina orientalis	PoolVolume	1.50	0.26	5.82	<0.001
	PoolVolume^2	-0.06	0.01	5.44	<0.001
	Dry	-3.13	0.64	4.85	<0.001
	Leaves	2.13	0.51	4.19	<0.001
	Leaves^2	-0.58	0.14	3.98	<0.001
	CanopyCover	0.00	0.00	0.79	0.43
	Stones	0.01	0.04	0.37	0.71
Dryophytes japonicus	PoolVolume	0.91	0.45	2.04	0.04
	PoolVolume^2	-0.02	0.02	0.89	0.37
	Dry	-2.71	1.03	2.63	0.008
	Leaves	0.52	0.93	0.55	0.58
	Leaves^2	-0.12	0.27	0.47	0.64
	CanopyCover	-0.03	0.01	4.78	<0.001
	Stones	-0.05	0.09	0.61	0.53

Table 3. Summary statistics of the biotic factor analysis. We highlighted the cells when there existed evidence supporting the presence of the effect of each factor (grey when P < 0.1; yellow when P < 0.05).

Species	Biotic variable	Estimate	*Adjusted SE*	z	P
Rana uenoi	ConEggs	0.80	0.42	1.91	0.056
	ConTadpoles	-0.99	0.66	1.49	0.14
	ConEgg + ConTadpoles	-0.33	0.56	0.59	0.55
	HeteroEggs	-0.43	0.53	0.80	0.42
	HeteroTadpoles	-4.87	1019	0.01	1
	HeteroEggs + HeteroTadpoles	0.23	0.73	0.32	0.75
	Predators	N.A.
	MosqLarvae	N.A.
Hynobius quelpaertensis	ConEggs	-2.25	0.64	3.50	<0.001
	ConTadpoles	-0.85	1.09	0.78	0.44
	ConEgg + ConTadpoles	-25.2	>1000	0	1
	HeteroEggs	0.25	0.47	0.52	0.60
	HeteroTadpoles	0.07	0.30	0.31	0.81
	HeteroEggs + HeteroTadpoles	0.39	0.59	0.66	0.51
	Predators	N.A.
	MosqLarvae	N.A.
Bombina orientalis	ConEggs	-0.02	0.19	0.08	0.91
	ConTadpoles	0.006	0.08	0.08	0.94
	ConEgg + ConTadpoles	0.38	0.20	0.19	0.85
	HeteroEggs	0.65	0.27	2.41	0.02
	HeteroTadpoles	-0.88	0.20	4.33	<0.001
	HeteroEggs + HeteroTadpoles	-0.21	0.28	0.76	0.45
	Predators	-0.03	0.10	0.25	0.80
	MosqLarvae	1.71	0.25	6.77	<0.001
Dryophytes japonicus	ConEggs	1.32	0.3	4.4	<0.001
	ConTadpoles	0.01	0.11	0.14	0.89
	ConEgg + ConTadpoles	1.48	0.25	5.92	<0.001
	HeteroEggs	-0.3	0.15	0.21	0.83
	HeteroTadpoles	0.02	0.09	0.24	0.81
	HeteroEggs + HeteroTadpoles	-0.07	0.17	0.41	0.68
	Predators	0.69	0.16	4.21	<0.001
	MosqLarvae	0.86	0.29	3.00	0.003

Table 4. Summary of the results showing the factors that were correlated with oviposition preferences (those with P < 0.1). ‘+’ and ‘–’ symbol indicates positive and negative correlation, respectively. ‘∩’ symbols show quadratic effects, indicating that oviposition was more frequent in the mid-range values.

Variable type	Variables	Rana uenoi	Hynobius quelpaertensis	Bombina orientalis	Dryophytes japonicus
Abiotic factors	PoolVolume	+	+	∩	+
	Dry	–	–	–	–
	Leaves	0	+	∩	–
	CanopyCover	0	0	0	-
	Stones	0	0	0	0
Biotic factors	ConEggs	+	–	0	+
	ConTadpoles	0	0	0	0
	ConEggs+ ConTadpoles Mix	0	0	0	+
	HeteroEggs	0	0	+	0
	HeteroTadpoles	0	0	–	0
	HeteroEggs+ HeteroTadpoles Mix	0	0	0	0
	Predators	N.A.	N.A.	0	+
	MosqLarvae	N.A.	N.A.	+	+

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Editorial decision: Minor Revisions Needed
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Patterns of oviposition site selection of four sympatric species of amphibians in ephemeral streams

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