Abstract
Estimating demographic parameters like survival or recruitment provides insight into the state and trajectory of populations, but understanding the contexts influencing those parameters, including both biotic and abiotic factors, is particularly important for management and conservation. At a high elevation national park in Central Spain, common toads (Bufo bufo) are apparently taking advantage of the near-extirpation of the midwife toad (Alytes obstetricans), as colonization into new breeding ponds is evident. Within this scenario, we expected demographic parameters of common toad populations to be affected favorably by the putative release from competition. However, we found the population growth rate was negative in 4 of 5 years at the long-standing population; survival probability at the long-standing population and newly-colonised breeding ponds was lower than reported for other toads living at high elevations and the probability of recruitment was inadequate to compensate for the survival rate in maintaining a positive trajectory for either of the breeding ponds. We assessed weather covariates and disease for their contribution to the context that may be limiting the common toad’s successful use of the niche vacated by the midwife toad.
Introduction
Biotic interactions among species range from complete exclusion of one species by another, to co-occurrence in the same habitat where interaction may affect demographic parameters in one or both species (e.g., survival as indexed by decreased body mass at metamorphosis and increased larval period length in Rana areolata compared to co-occurring species, Parris and Semlitsch, 1998), to niche partitioning (e.g., differential use of habitat, Indermaur et al., 2009). When one species is extirpated and leaves a co-occurring, ecologically similar species in its place, population growth and persistence by the remaining species may be due to a release from competition and adaptations that allow it to better cope with the changes that contributed to the other species’ extirpation (e.g., emerging disease, changing climate). Under these conditions, we expect the remaining species to colonize breeding ponds vacated by the extirpated species and to exhibit increased population growth prior to reaching the breeding pond’s carrying capacity. However, short-term success, facilitated by the extirpation of the other species, may not translate into long-term persistence. Accounting for biological associations, as well as abiotic factors, can provide information to better understand the long-term trajectory of populations and the consequences of location.
The midwife toad (Alytes obstetricans) and the common toad (Bufo bufo) are found in Guadarrama National Park (GNP), in Central Spain. The presence of midwife toad tadpoles reduces mass at metamorphosis, growth rate, and survival of common toad tadpoles in the laboratory (Richter-Boix et al., 2007). In the field, Bosch and Rincón (2008) reported an inverse relationship between the number of common toad clutches laid and the number of midwife toad tadpoles present at a breeding pond. In the laboratory, Bosch and Rincón (2008) tested whether or not midwife toad tadpoles consumed common toad eggs, as a mechanism behind this relationship, and found that while common toad eggs were not consumed by midwife toad tadpoles, common toads avoided laying eggs in tanks where overwintering midwife toad tadpoles were present. Therefore, the presence of Midwife toads appears to exclude or suppress common toads.
Between 1997 and 2002, midwife toads declined dramatically in GNP as a result of chytridiomycosis, a disease caused by the fungal pathogen Batrachochytrium dendrobatidis (Bd) (Bosch et al., 2001). Common toads are not compromised as severely by Bd as midwife toads, likely because they exhibit traits that theoretically reduce the impact of Bd (e.g., Lips et al., 2003). However, Bd generally incurs a cost for common toad tadpoles in terms of growth and can cause larval mortality before or soon after metamorphosis (Bosch and Martínez-Solano, 2006; Garner et al., 2009). Between 1999 and 2004, common toads, historically present only in the largest pond (Laguna Grande) in higher altitude areas of GNP, colonized 5 ponds vacated by the extirpation of midwife toads (Bosch and Rincón, 2008). Midwife toads returned to Laguna Grande in 2005, when the non-native brook trout (Salvelinus fontinalis) was finally extirpated, but its recent presence can be considered anecdotal since less than 20 tadpoles were counted since then.
(Top and bottom right) Location of the studied breeding ponds Laguna Grande and Laguna Chica, within Guadarrama National Park in the Iberian Peninsula. (Bottom left) Temporal changes in the number of B. bufo clutches in these ponds from 1998 to 2011; Laguna Grande: grey bars; Laguna Chica: black bars.
Citation: Amphibia-Reptilia 35, 3 (2014) ; 10.1163/15685381-00002952
While these observations suggest that successful colonizations are taking place in the wake of the extirpation of midwife toads, an examination of the populations at the original and more recently colonized breeding ponds may provide insights into the demography of colonization. We expected common toads at colonized breeding ponds to be thriving because of a lack of competition, lower density, and an apparent increased ability to co-exist with the disease (Bd). We also expected a high population growth rate (lambda) at colonized breeding ponds.
The long-term persistence of populations, both established and colonial, depends on a variety of factors. Weather (an abiotic factor) can be extreme at high elevation breeding ponds, negating even the most fecund reproductive effort (e.g., Scherer et al., 2008). Competitive interactions with other species (biotic factors) can also affect long-term persistence. In addition to more obvious effects of competition among co-occurring species, interactions among classes of organisms can affect persistence. The effect of the amphibian chytrid fungus appears to be reduced in common toads, but based on disease dynamics and density dependent behaviors of both the toads and the fungus (sensu Briggs et al., 2010), this relationship has the potential to change as density of common toads increases. Characteristics of the colonizer (other biotic factors) such as foraging ability are also potentially influential in the long-term persistence of a population. For common toads at GNP, the changes wrought by the extirpation of the midwife toad provided an opportunity, but their long-term persistence depends on their ability to exploit the niche and respond to challenges (i.e., disease, weather).
To better understand the demography of colonization by the common toad in GNP, we estimated demographic parameters (survival probability, recruitment rate, and population growth rate) at a recently colonized breeding pond (Laguna Chica) and at the pond where common toads have been present for at least two decades (Laguna Grande) (fig. 1). We also evaluated hypothesized relationships between demographic rates and weather conditions. The majority of the covariates that we evaluated describe conditions during the time of year when anurans, particularly at high elevations, are most vulnerable (e.g., Scherer et al., 2008). For example, breeding and preparing to hibernate are particularly critical (Reading, 2007). We relate model selection results to data from previous research at these breeding ponds and build a plausible scenario to explain the changes in the distribution of common toads in higher altitude areas of GNP.
Materials and methods
Study site
Laguna Grande (elevation 2018 m, surface 5452 m2, maximum depth 2.7 m) and Laguna Chica (elevation 1956 m, surface 739 m2, maximum depth 0.7 m) are two of the largest ponds in GNP, Sierra de Guadarrama, Central Spain, near Madrid (41°N, 4°W; fig. 1). The park is a protected, alpine habitat (1800-2430 m) and ponds are above the tree line, with little vegetation around the shore (Toro and Granados, 1999). Both sites are above the tree line and isolated, so that they are the only water bodies in the same hydrographic basin where B. bufo breeds (Bosch and Rincón, 2008).
Data collection
Routine yearly censuses were carried out in higher altitude areas of GNP since 1999, and common toad clutches and over-wintering Midwife toad tadpoles were counted individually whenever possible. Additionally, data on the distribution and reproduction of amphibian species in each of the 250 cataloged ponds in the area since 1982 is available. We conducted multiple nighttime capture sessions to collect data during the breeding season (April-June) from populations of common toads at Laguna Grande and Laguna Chica from 2006 to 2011. We completed 2-7 sessions each breeding season (table 1). During each session, we searched the entire shoreline and all animals were captured by dip net. We recorded sex, mass, snout-vent-length (SVL) and PIT (passive integrated transponder) tag number for each captured toad. If animals did not already have a tag, a new tag was inserted subcutaneously on the dorsal side. Toads were released at the point of capture immediately after data were collected. In 2009, a sub-sample of adults at Laguna Grande and Laguna Chica were tested for using standard field techniques and quantitative molecular methods (Hyatt et al., 2007) resulting in estimates for Bd load for each individual at each breeding pond.
Number of capture sessions and results from disease (Bd) sampling.
Analysis
We used the Pradel model (Pradel, 1996) for data collected under Pollock’s robust design (Pollock, 1982) in Program MARK (White and Burnham, 1999) to analyze the capture-recapture data for male toads only. Data collected under the robust design are characterized by multiple capture sessions within a year (each capture session is referred to as a secondary occasion). The collection of secondary occasions within each year is referred to as a primary period (Pollock, 1982; Kendall et al., 1997) thus primary periods were approximately 2 months with 10 months in between. The model assumes that the time between secondary occasions is sufficiently short that individuals are not added to or lost from the population (i.e., the closure assumption). The amount of time between primary periods, on the other hand, is long enough for gains and losses to occur (e.g., recruitment or mortality).
Because no gains or losses are assumed to occur across secondary occasions within a primary period, the only process being modeled is the capture process. On each occasion, an individual in the study area is either captured for the first time within a primary period, recaptured after being captured earlier within a primary period or not captured. The probabilities of these outcomes are represented as p (the probability of first capture) and c (the probability of recapture), while failing to capture an individual is represented as or . We used closed population models (Otis et al., 1978) to model p and c for secondary occasions within each primary period (Williams et al., 2002).
While the capture-recapture data within primary periods are used to estimate p, c, and N, the data across primary periods can be used to estimate a variety of demographic parameters (Pradel, 1996; Williams et al., 2002). We used the f-parameterization of the Pradel (1996) model to estimate apparent survival probability and recruitment rate between primary periods. Apparent survival probability (hereafter, survival probability, ), is the probability of an animal surviving and remaining in the study area between primary periods t and . The presence of temporary emigration (i.e., absence from the breeding pond in one or more years, but return to the breeding pond in subsequent years) can bias estimates of survival probability negatively (Kendall et al., 1997; Converse et al., 2009). We assume that estimates of survival probability from our analyses will be minimally biased because male toads in similar environments are seldom absent from breeding ponds (Muths et al., 2006) and analyses of the capture-recapture data from Laguna Grande suggests that males do not temporarily emigrate (Muths et al., 2013). We define recruitment rate, as the per capita number of individuals added to the breeding population between primary periods t and . Within Program MARK, we used the estimates of and to derive estimates of the finite population growth rate, , and associated standard errors using the equation . The finite population growth rate can also be written as the ratio between population sizes at time and t () where N represents population size. If , the number of individuals in the population increased between t and , whereas indicates a declining population (Williams et al., 2002).
Our interests were first to estimate , , and , and then to examine differences in those parameters between the populations at Laguna Chica and Laguna Grande. Second, we evaluated hypothesized causes for the temporal variation in the parameters. We hypothesized that survival and recruitment are higher with “good” weather, as represented by several covariates that we discuss below. Recruitment rate is partly dependent on conditions at the time of egg laying or metamorphosis and it takes approximately 2-4 years for common toads to reach breeding age (Reading, 1991). Therefore, for weather covariates hypothesized to be correlated with recruitment rate, we used the value for that covariate 2, 3 and 4 years previous to the year of recruitment (i.e., we lagged the effects of the weather covariates by 2, 3 and 4 years). Models that included 4-year lags had greater support; therefore, we excluded models with 2- and 3-year lags.
In capture-recapture analyses, models of , , and , are not fit to the data separately. A model for each parameter is combined with a model for the other parameters prior to fitting them to the data. We first developed a set of a priori hypotheses for capture probability and recapture probability for each population. In preliminary models, we found no evidence for heterogeneity between capture probability, p, and recapture probability, c; therefore we fixed for all subsequent models.
For each population, we assessed hypotheses regarding temporal variation in capture probability within each primary period (sensu Muths et al., 2011): i) capture probability will vary across all secondary occasions (where secondary occasion is a categorical variable), ii) capture probability will increase to a peak early in each primary period, then decline in later secondary occasions (a quadratic function), and iii) capture probability will decrease across secondary occasions (a linear trend). We also used weather data (sensu Scherer et al., 2008) from the days of the secondary occasions to determine if capture probability was correlated with median air temperature, average wind speed, the amount of precipitation, barometric pressure or a combination of median air temperature and average wind speed. We obtained climatic data from the nearest meteorological station located at a similar altitude (Puerto de Navacerrada, 1890 m, 40°46′50″N, 4°00′37″W), 5.4 km away from the study area. We quantified the support for each model with AICc values, , and Akaike weights, (Burnham and Anderson, 2002) and used all models of with AICc < 6 in subsequent stages of modeling.
After identifying the most strongly supported model or models of capture probability, p, we specified models for . We developed 8 hypotheses and associated mathematical models for (table 2A). The set of models includes effects of primary period on recruitment rate (where primary period is modeled as a categorical variable) and effects of six weather covariates, as well as a model of no variation in recruitment rate across primary periods. Hypotheses were based on our understanding of toad biology and observations by J.B. at these sites.
Hypotheses for modeling recruitment rate and adult survival probability. Note that all covariates for recruitment rate are lagged by 4 years.
The choice of weather covariates reflect our prediction that conditions the winter before tadpoles metamorphosed, and the late-summer and winter after metamorphosis are most critical to the survival of metamorphs and their subsequent recruitment into the adult population. We presume that higher precipitation in the winter before metamorphosis leads to wetter conditions and higher productivity in the year of metamorphosis; wetter and warmer conditions in the September of the year in which metamorphosis takes place delay or prevent desiccation of breeding ponds, promoting growth of metamorphosed individuals prior to their first winter; and that warmer winters after metamorphosis facilitate survival. We used all models of with AICc < 6 in subsequent models of (table 2B).
Finally, we combined the highest ranked models of and with every model of , fit the models to the data and evaluated them using and to identify the models with the most support (Burnham and Anderson, 2002). We hypothesized that cold winters, winters with variable temperatures, and hot summers would affect survival probability of common toads negatively (Scherer et al., 2008, table 2B). We used model-averaging (Burnham and Anderson, 2002) to derive estimates of , , and . To evaluate the importance of weather covariates, we examined the 95% confidence intervals of the estimates of regression coefficients. If confidence intervals do not include 0, we inferred a stronger association between the covariate and demographic parameter.
We used the results from testing in 2009 to test the hypothesis that individuals with high loads had lower survival probabilities than individuals with low loads. For this analysis, we only used the capture-recapture data for males that were tested ( at Laguna Grande; at Laguna Chica). We pooled the capture-recapture data across secondary occasions such that each individual was recorded as captured or not for each primary period. Since sample sizes were small, we also pooled the data across the two populations. We analyzed the data using the CJS model (Lebreton et al., 1992) in Program MARK and compared models that included an effect of Bd on individual survival probabilities from 2009 to 2010 to models without the Bd effect.
Results
We captured 462 male toads at Laguna Grande and 83 male toads at Laguna Chica between 2006 and 2010. The most strongly supported model of capture probability included variation among secondary occasions and primary periods. In both populations, the data provided no support for other models. Estimates of capture and recapture probabilities were small (⩽0.25), but the probability of capturing an individual at least once in a primary period was high due to the large number of secondary occasions (estimates ranged from 0.46 to 0.90). With the exception of 2006, estimates of capture and recapture probabilities at Laguna Chica were higher (⩽0.59).
The highest ranked models of recruitment rate, , for the population at Laguna Grande suggested that recruitment is negatively associated with average daily air temperature (TMINWIN) during the winter after the tadpoles metamorphosed and also negatively associated with the amount of precipitation the winter before the tadpoles metamorphosed (PRECWIN) (table 3). Both of the correlations were inconsistent with our hypotheses (table 2A).
Model selection results shown for recruitment rate (A) and survival probability (B). Models with AICc Wt of <0.1 are not shown.
The model selection results for recruitment rate at Laguna Chica indicate support for multiple models. However, when they are combined with estimates of regression coefficients for the weather covariates, the strongest support is for a positive association between recruitment rate, , and the number of days with minimum temperature < 0 in the winter after tadpoles metamorphosed (NUMWIN). The 95% confidence interval for the estimated regression coefficient for NUMWIN is the only one that does not include 0. The positive association was not consistent with our hypothesis (table 2A). Model-averaged estimates of recruitment rate in the two populations were similar in magnitude, though estimates at Laguna Chica were more variable among years (fig. 2).
Model averaged estimates of probability of survival (A), recruitment (B) and population growth rate (C) for Laguna Grande (grey) and Laguna Chica (black). Estimates include standard error (SE) and 95% upper and lower confidence intervals.
Citation: Amphibia-Reptilia 35, 3 (2014) ; 10.1163/15685381-00002952
The model selection results provided no evidence for a correlation between survival probability and any of the weather covariates at Laguna Grande, though there was strong support for variation among years (table 3). There was substantial uncertainty in model selection for survival probability at Laguna Chica, but in the top three models, the estimated relationships between survival probability and weather covariates were consistent with our hypotheses. The probability of survival decreased as: a) the number of times the average daily minimum temperature changed from above freezing to below freezing and vice versa (TEMPRANS; table 2B, 3); b) the number of days in winter with minimum temperature < 0°C increased (NUMWIN; table 2B, 5); and c) the average daily minimum temperature of the coldest 7-day period decreased (TMIN7AVE; table 2B, 6). Estimates of survival probability were generally higher at Laguna Chica, particularly in 2007 (fig. 2).
Of those toads tested for Bd in 2009, the proportion of individuals testing positive was similar (42% Laguna Grande and 35% Laguna Chica). Average prevalence was greater at Laguna Grande (table 1) and almost twice as many samples had zoospore equivalents of >20 at Laguna Grande (34%) relative to Laguna Chica (17%). However, we found no evidence that survival probability was lower for individuals with higher Bd loads or higher for individuals positive for Bd infection.
Discussion
We do not have demographic estimates for common toads before midwife toads were extirpated, but toads at high elevations are typically long-lived (e.g., 10+ years; common toads, Cvetkovic et al., 2008; Zhang and Lu, 2012; boreal toads, Muths and Nanjappa, 2005). Longevity, plus a release from competition with midwife toads, led to our expectation of high survival probabilities at both breeding ponds. We further expected increased recruitment rate of adults at both ponds, because common toad tadpoles would have more resources in the absence of midwife toads. Estimates of population growth rate from the population at Laguna Chica suggest it is stable, but contrary to what we expected, estimates from the population at Laguna Grande indicate a decline (fig. 2). There was little support in the data for an effect of our selected weather covariates on the targeted parameters, due possibly to the scale at which covariates were measured or because patterns did not emerge over our short time frame. Mindful that our data cover a relatively small time period, there are a variety of plausible explanations for our results including a source – sink dynamic (sensu Pulliam, 1988).
Survival
The probability of adult survival at both Laguna Chica and Laguna Grande was relatively high (>0.75) although survival probability at Laguna Chica was generally higher (fig. 2). While some disparity may be explained by variation in environmental conditions at the two ponds, common toads at GNP exhibited more variation in the probability of survival than expected relative to similar species (Pilliod et al., 2010; Muths et al., 2011). Variation in the probability of survival might simply be a reflection of challenges in acquiring adequate food and shelter (i.e., life at the edge of a generalist’s range). For example, common toads have a wide distribution in the Iberian Peninsula but are more likely to be found in areas where the climate (i.e., precipitation and temperature) is more predictable (Romero and Real, 1996); it is possible that the extreme conditions potentially experienced at higher elevations promote variability in survival in common toads.
Recruitment
In general food concentrations are low in the high-elevation, oligotrophic water bodies in GNP (Toro and Granados, 1999). We might expect greater productivity at Laguna Chica compared to Laguna Grande because it is shallower and likely achieves higher solar gain. However, because common toad tadpoles are inefficient foragers with low ingestion and filtering rates when concentrations of food are low (Viertel, 1990), this potential increase in production at Laguna Chica may not make a difference.
The idea of inadequate resources coupled with inefficient foraging ability has some support in that recruitment probabilities at the two ponds are generally lower (fig. 2) than recruitment rates reported for other toads in a similar environment (0.25-0.41, boreal toads, Muths et al., 2011). Lower recruitment could also reflect a response to a stressor such as disease. Mass mortalities of metamorphic common toads have been recorded in GNP since 2001 (Bosch and Martínez-Solano, 2006; Garner et al., 2009), although high numbers of healthy metamorphs are observed as well (J.B. pers. obs.). The survival probability of metamorphic common toads has not been quantified but clearly affects recruitment rate.
Data on disease were collected only occasionally and thus limit our ability to test hypotheses relative to the effect of disease on demographic parameters. However, the impact of Bd on the co-occurring midwife toad is acute (Bosch et al., 2001) such that an acknowledgement of a possible role of disease in common toad demography is appropriate. While common toads are not as susceptible to Bd as other species such as the midwife toad (Bosch et al., 2001; Bosch and Rincón, 2008), density dependent factors can affect the interplay of disease and host (e.g., Rachowicz and Briggs, 2007; Briggs et al., 2010) such that the Laguna Grande population () may have reached a size enabling the fungus to compromise adult survival and thus population growth. The possibility of a density-dependent response to disease at Laguna Grande is plausible and could be tested rigorously with additional data.
Population growth
A relatively high survival probability is typical in anurans that live in unpredictable environments (e.g., at high elevations), thus we expect adult survival to be a key component of population growth (lambda) (Sather and Bakke, 2000; Biek et al., 2002; Vonesh and De la Cruz, 2002; Spencer and Janzen, 2010). However, population growth is also determined by recruitment of adults. Recruitment may compensate for poor survival, maintaining a positive population trajectory or slowing a decline (e.g., Muths et al., 2011), potentially facilitating persistence in common toad populations despite fluctuations in breeding success. We expected to see the probability of recruitment at a level to maintain or increase the rate of population growth at Laguna Grande and Laguna Chica; instead we estimated a probability considerably lower than rates in other populations exposed to similar situations (extreme weather and disease) (Scherer et al., 2008; Muths et al., 2011).
Conclusion
There are many potential drivers of the scenario we describe at GNP. Consequences of disease dynamics and physiological consequences of living at the altitudinal extreme of the common toad’s range provide two likely avenues of investigation. Changes in climate are expected to impact both weather patterns and potentially host-pathogen disease dynamics, but a longer time series of data may be necessary to fully investigate this.
It is prudent to remember that our data are only a snapshot in time and long-term dynamics of common toad populations at GNP may be very different. We demonstrate that short time series of data can be useful, especially given the current state of amphibian affairs (e.g. Stuart et al., 2004), if assessed with the appropriate caveats.
Acknowledgements
We thank J.A. Vielva, director of the Peñalara Natural Park, and all people working at Guadarrama National Park and A. Díaz-Guerra, A. Rodriguez, O. Quiroga, B. Martín-Beyer and M. Beracoechea for assistance with fieldwork. Funding was provided by Comunidad Autónoma de Madrid, Fundación General CSIC and Banco Santander. S.F.B. was supported by Biodiversa project RACE: Risk Assessment of Chytridiomycosis to European Amphibian Biodiversity. E.M. is supported by the US Geological Survey Amphibian Research and Monitoring Initiative (ARMI). DNA standards for qPCR analyses were provided by Matthew Fisher from Imperial College London. Animal handling procedures were approved by Consejería de Medio Ambiente, Comunidad Autónoma de Madrid, Spain. This is contribution no. 476 of the USGS Amphibian Research and Monitoring Initiative. Use of trade, product, or firm names descriptive and does not imply endorsement by the US Government.
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Footnotes
Associate Editor: Benedikt Schmidt.
