Amphibian conservation in Europe: the importance of pond condition
verfasst von:
A. López-de Sancha, D. Boix, L. Benejam, L. Briggs, T. A. Davidson, J. C. Fahy, V. Frutos-Aragón, H. M. Greaves, P. Lemmens, T. Mehner, L. Martín, B. Oertli, C. Sayer, S. Brucet
Der Artikel konzentriert sich auf die Bedeutung des Zustands der Teiche für den Schutz der europäischen Amphibien, die mit einem alarmierenden Rückgang konfrontiert sind. Es stellt den ECELS-Index als wertvolles Instrument zur Beurteilung des Erhaltungszustands von Teichen vor und diskutiert die bedeutende Rolle der Teichmorphologie und Wasserqualität bei der Unterstützung der Artenvielfalt von Amphibien. Die in sechs europäischen Ländern durchgeführte Studie zeigt, dass Teiche in besserem Zustand, mit höheren ECELS-Werten und niedrigeren Eutrophierungsgraden, einen größeren Artenreichtum an Amphibien, einschließlich geschützter Arten, aufweisen. Die Ergebnisse unterstreichen die Notwendigkeit wirksamer Managementstrategien zur Erhaltung der Merkmale von Teichen, die die Vielfalt der Amphibien fördern, und unterstreichen die dringende Notwendigkeit einer internationalen Zusammenarbeit, um die Krise des Amphibiensterbens anzugehen.
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Abstract
Most amphibians found in Europe inhabit ponds, small aquatic ecosystems commonly threatened by habitat degradation and destruction. Despite this situation, ponds are rarely considered in conservation policies. Thus, their effective management may present a significant opportunity to alleviate the ongoing decline of amphibian populations. In this study, we assessed if the favourable condition of a pond and its conservation status promotes its amphibian species richness, which was determined by using environmental DNA metabarcoding. For this, we investigated the condition of 154 ponds across six European countries, considered through measurements of their conservation status (Shallow Lentic Ecosystem Conservation Status index, ECELS), water quality and trophic state, and physical characteristics. By utilising Generalised Linear Mixed Models, we determined that a higher amphibian species richness, and a higher number of protected ones, are found in shallow ponds with a better pond condition, meaning a higher conservation status and a better water quality. Specifically, we observed that non-eutrophic ponds characterized by permeable and shallow basins with smooth slopes, and without weirs, foster a higher amphibian diversity. Conservation efforts targeting the preservation of natural pond hydrological processes and mitigating nutrient pollution are critical for safeguarding amphibian biodiversity in Europe and contributing to broader freshwater conservation goals.
Hinweise
Communicated by David Hawksworth.
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Introduction
Amphibians are the most threatened vertebrate class worldwide, with an alarming 40.7% of species currently included in the IUCN Red List categories of Critically Endangered, Endangered and Vulnerable. Such alarming declines of amphibians at a global scale necessitate immediate and effective habitat conservation and protection actions (Luedtke et al. 2023). Population declines are especially intense in Europe (Ribeiro et al. 2011), where nearly a quarter of European amphibian species are currently classified as threatened with extinction (Gozlan et al. 2019; Luedtke et al. 2023), underscoring the urgency for comprehensive conservation strategies. While climate change and diseases are significant global threats, the most common direct threats to amphibians include various forms of habitat degradation and destruction, particularly due to urbanization and agricultural development (Nori et al. 2015; Burrow and Maerz 2022; Luedtke et al. 2023).
Ponds play a pivotal role in the lifecycle of amphibians (Ribeiro et al. 2011; Ilg and Oertli 2017), and most palearctic species depend on pond habitats for reproduction (Curado et al. 2011). Defined as lentic water bodies covering less than 5 hectares in area, ponds are globally abundant, with estimates ranging from 547 million to 3.19 billion (Oertli et al. 2009; Hill et al. 2021). Given their ubiquity and importance, effective management and conservation of ponds offer a significant opportunity to alleviate the ongoing decline of amphibian populations (Rannap et al. 2010; Swartz and Miller 2019; Mathwin et al. 2021).
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However, despite their dire situation, both ponds and amphibians are insufficiently considered in conservation policy and action (Nori et al. 2015; Hill et al. 2021). This could be because tools for ecological assessment, which are particularly useful for managers and practitioners (Oertli et al. 2009), exist for running waters and lakes (Cellamare et al. 2011; Petrike et al. 2017; Ntislidou et al. 2018), whereas for ponds they remain relatively rare (Oertli et al. 2009; Usio et al. 2013). In this regard, the ECELS index, acronym for the catalan “Estat de Conservació d’Ecosistemes Lenítics Soms” (Shallow Lentic Ecosystem Conservation Status), has proved to be a useful assessment method for evaluating the ecological condition and conservation status of a pond, measured as the degree to which ponds retain natural attributes despite human activity (Sala et al. 2004; Quintana et al. 2016). This index is composed of five independent components that individually assess complementary aspects of a pond, allowing managers to identify those characteristics that should be focused on to improve the conservation status of a pond. Considered components include pond morphology, human activity inside and near the pond, multiple water quality aspects, and the extent of both emergent and hydrophytic vegetation (Sala et al. 2004).
Not only the conservation status, but also the water quality of a pond is crucial for amphibian conservation. For example, eutrophication and algal blooms promoted by increased nitrogen and phosphorus influxes (Nyenje et al. 2010; Sfriso et al. 2017; Merz et al. 2023) can detrimentally affect pond amphibian communities by reducing species richness (Schmutzer et al. 2008; Ruso et al. 2019) and through the promotion of tadpole pathogenic infections (Johnson et al. 2007; Peltzer et al. 2008). On this matter, the Trophic Index (TRIX) is a useful multimetric assessment tool of water quality and the trophic state of freshwater habitats, including ponds. Based on the combination of measured total nitrogen (TN), total phosphorus (TP), dissolved oxygen, and chlorophyll-a concentrations (Vollenweider et al. 1998; Pettine et al. 2007; Béjaoui et al. 2016), TRIX offers a comprehensive approach to the assessment of pond water quality.
The present study evaluates whether pond condition, assessed by its conservation status and water quality (ECELS and TRIX indices), promotes amphibian species richness, as well as the number of amphibian species under legal protection. We characterized 154 European ponds across six countries, measured the above-mentioned characteristics, and determined their amphibian species richness, including those species protected under the Annex IV of the EU Habitats Directive (1992), utilizing an eDNA metabarcoding approach. Pond size and depth, and its emersed vegetation cover within the pond, were also considered as potential additional drivers of amphibian species richness (Arribas et al. 2014; Semlitsch et al. 2015). Additionally, by assessing the effect of each component of the ECELS index on amphibian richness, we aim to identify the key natural attributes and characteristics of ponds that should be prioritized during habitat management actions to enhance amphibian richness, thus contributing to more effective conservation efforts for European amphibians. Our hypothesis posits that ponds in more favourable conditions, thus having a higher conservation status and water quality, will harbour higher amphibian species richness and, particularly, a higher number of protected species.
Material and methods
Pond selection and data collection
Data were collected from 154 ponds distributed across six European countries: Belgium (30), Denmark (28), Germany (20), Spain (28), Switzerland (26) and the United Kingdom (22) (Fig. 1). Ponds were selected within each country following an agricultural land use intensity and hydroperiod gradient criterion and cover a latitudinal and longitudinal geographic range of 41.81° to 56.28° and − 2.91° to 14.37°, respectively. They are located at altitudes below 800 m, with water column depth ranging from 0.12 to 9 m, and surface area ranging from 33 m2 to 1.47 ha. Ponds overgrown by vegetation were not selected for the study. Ponds in each country were distributed in pondscapes, with one to six ponds present in each, depending on the country.
Fig. 1
Geographical distribution of the 154 European ponds analyzed in this study, highlighting the spatial variation in key variables. The maps display (top left) amphibian species richness, (top right) the ECELS index value, (bottom left) the number of protected amphibian species listed in Annex IV of the Habitats Directive, and (bottom right) the TRIX index value. Each circle represents an individual pond, with marker size and colour corresponding to the metric’s magnitude: smaller, red circles indicate lower values, while larger, green circles denote higher values
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Pond characterization and sampling were conducted in April–May 2021, except for 12 Spanish ponds, which were characterized and sampled in May 2022 because they were dry the previous year. The characterization process involved measuring the variables required for computing the ECELS conservation status index (refer to Sala et al. 2004, for a comprehensive description of the variables utilized). This index ranges from 0 to 100, with a higher value indicating a better pond conservation status, defined as the degree of natural attributes that it maintains despite human activity. Ponds with a high conservation status are expected to present smooth littoral slopes that allow a wide area of inundation, negligible effects of human uses, and unaltered water quality and biotic communities (Sala et al. 2004). ECELS encompasses five classes for the numerical values of the index: Bad (less than 30), Poor (30–49), Moderate (50–69), Good (70–89), and High (greater than, or equal to 90). To determine the numerical value of ECELS, five components are calculated, each one including multiple variables of a different category: (I) pond morphology (marginal slope, presence of weirs and embankments, burial of the pond, and permeability of the pond bed), (II) human activity around the pond (presence of hydraulic infrastructures, transport infrastructures, nearby buildings, nearby agricultural, livestock or plantation land uses, human visits, presence of rubbish, environmental information and management, and presence of allochthonous or domestic fauna), (III) water aspects (transparency, odour and turbidity of natural origin), (IV) emergent vegetation (cover on the pond perimeter, cover inside the pond, identity of the dominant community, identity of the shrub stratum, and water permanence), and (V) hydrophytic vegetation (quantity of submersed or rooted floating-leaf vegetation, quantity of non-rooted floating vegetation on the pond surface, and identity of the hydrophytic community). ECELS index for each pond was calculated using the ECELS R package (López-de Sancha 2025).
Additionally, we calculated the multimetric index TRIX that characterizes pond water quality (Vollenweider et al. 1998; Pettine et al. 2007) by assessing the chlorophyll-a concentration, oxygen saturation, and total inorganic nitrogen and phosphorus levels in the water of each pond. This index ranges from 0 to 10 and its analytical expression is given as follows:
where TN and TP represent total nitrogen and phosphorus respectively (in mg L−1), |D%O2| represents the absolute value percentage deviation of the oxygen concentration from saturation conditions (in %), and Chla is the total chlorophyll-a concentration (in mg Chl-a ·L−1). The parameters a = 1.5 and b = 1.2 are scale coefficients used to set the index lower limit and the scale range from 0 to 10 (Vollenweider et al. 1998; Béjaoui et al. 2016). The eutrophication level and water quality status indicated by the values of this index are: (0–4): low eutrophication, high water quality, (4–5): medium eutrophication, good water quality, (5–6): high eutrophication, poor water quality, and (6–10): very high eutrophication, bad water quality.
To measure TN and TP at each pond, a depth-integrating water sample was collected using a tube sampler at eight locations, spanning the entire water column, and including all major microhabitats. All samples were pooled, resulting in a 10-L water collection where possible. We used a portable fluorometer to quantify in vivo concentrations of chlorophyll-a in this pooled water collection. A 250 mL subsample of this unfiltered sample was collected for TN and TP analysis, which was kept in cool and dark conditions in the field and subsequently frozen at − 20 °C in the laboratory prior to analysis. Oxygen concentration was measured directly at a central point in each pond (or in the centre of the largest open water patch in the case of macrophyte covered ponds) at a depth of 20 cm below water surface using standard electrodes (Hanna Instruments, HI9828).
We also incorporated percentage of emersed vegetation cover within the pond, as well as the pond area and mean depth, into our analysis to consider other important variables related to amphibian richness.
eDNA data collection
Amphibian species richness was obtained through eDNA metabarcoding. Water samples were collected from each pond during April–May using a pole equipped with a sterile Whirl–Pak bag. Between 15 and 20 subsamples from just below the water surface were taken, covering the entire pond and all associated microhabitats, and combined into a 30 L bucket with a sterile plastic bag. A predetermined volume of water from this composite sample was then passed through a sterile, encapsulated 0.8 μm pore size PES filter (50 mm diameter), which included a 5 μm glass fiber prefilter (NatureMetrics, Surrey, England). Following filtration, the filter was air-dried using a syringe and the capsule was subsequently filled with 1.5 mL of Longmire’s buffer for preservation (for detailed methodology, refer to Mauvisseau et al. 2021). Filters were stored in the dark at room temperature until DNA extraction.
Molecular analyses
DNA extraction was initiated within four months of sample collection at the Research Institute for Nature and Forest (INBO) in Geraardsbergen (Belgium). The extraction procedure took place in a dedicated PCR-free room specifically designed for low-copy-number template extractions, featuring particulate air-filtered compartments to prevent contamination of eDNA samples. It was conducted using Qiagen’s DNeasy Blood & Tissue Kit, followed by purification with Qiagen’s DNeasy PowerClean Cleanup Kit (for detailed methodology, refer to Everts et al. 2021). During the lysis-step in the extraction protocol, a fixed amount of internal positive control (IPC) was incorporated for each filter. This IPC comprised a 149 bp Dengue virus type 2 insert sequence (GenBank M29095.1) within a plasmid, serving both as quality control for the resulting DNA extract and as an indicator of PCR inhibition or failure (for more information, see Brys et al. 2021a). Subsequently, eDNA extracts underwent purification using MagNA beads and quantification using a Quantus Fluorometer following the manufacturer’s guidelines before amplification. When quality control measures for the initial filter of each pond revealed extraction failure or insufficient DNA quality for subsequent metabarcoding workflow or sequencing, DNA extraction was performed on the second filter from that pond. DNA amplification utilized vertebrate-specific Riaz primers (12S_F1: 5′-ACTGGGATTAGATACCCC-3′; 12S_R1: 5′-TAGAACAGGCTCCTCTAG-3′), targeting a 142-bp fragment within the mitochondrial 12S rRNA Gene (Riaz et al. 2011). Libraries were then constructed in triplicate following the methodology outlined by Brys et al. (2021b) and subjected to 150 bp paired-end sequencing on an Illumina HiSeq3000 platform (Admera Health, USA). Negative PCR controls were included in the workflow to monitor potential laboratory contamination.
Molecular data processing and cleaning
Raw sequencing data were processed following Brys et al. (2021b). Taxonomic assignments were made utilizing a meticulously curated reference database comprising Riaz amplicons of European amphibian species (Halfmaerten et al. 2020). Only sequences exhibiting a 100% match with this database were retained for subsequent analyses. The total number of reads per sample was used to standardize reads within a sample by converting raw read counts into relative read abundances (RRA). Additionally, to mitigate read noise, species with a relative read abundance of ≤ 0.001% within a sample were adjusted to zero. Subsequently, the average RRA per species was calculated across the three technical replicates.
Statistical analysis
To assess the effect of pond condition on amphibian richness, we first conducted a variable selection process for inclusion in a Generalized Linear Mixed Model (GLMM) with a Poisson distribution to predict amphibian species richness. The candidate predictors included the ECELS value of each pond, the TRIX trophic index, pond depth, pond area, and emersed vegetation cover. Variable selection was carried out iteratively using a stepwise procedure with the leaps R package (Lumley 2020), removing one variable at a time, and recalculating the model iteratively until the best-fitting model was identified based on the Akaike Information Criterion (AIC) (Johnson and Omland 2004). To ensure robustness, we repeated this process using the MuMIn R package (Bartón, 2024), which predicted the same variables. The final, selected set of predictors was then used to construct the GLMM with a Poisson distribution, implemented with the lme4 R package (Bates et al. 2015).
To assess the role of pond condition on the richness of protected amphibians, another GLMM was performed with the same selection process but, this time, considering the richness of amphibian species included in Annex IV of the EU Habitats Directive (1992) as a dependent variable.
Another GLMM was constructed to evaluate the effect of each ECELS component on amphibian richness by considering the amphibian species richness as a dependent variable and each of the five components of the ECELS index as predictors.
All GLMM models included the country in which a pond is located as a random effect to control for biogeographical patterns. The normality of the residuals for each model was assessed through Q–Q and observed versus predicted model residual values plots using the DHARMa package (Hartig 2022). All statistical analyses and plots were performed in R (v. 2023.12.1, R Core Team 2023).
Results
Mean local amphibian richness over the entire set of investigated ponds was 3.4 ± 1.7. Richness was significantly higher in ponds with a higher ECELS category (Fig. 2). Overall, the assessed ponds presented a good condition (Fig. 1), with an average ECELS index score of 80.3 ± 11.5, and a favourable water quality level with low eutrophication values, as assessed by the TRIX index (2.9 ± 1.1). Emergent vegetation covered approximately 36.8 ± 27.3% of the pond surface, on average (Fig. 3). A value range of these variables for the ponds in which each amphibian species has been found can be consulted in Table 1.
Fig. 2
Boxplots illustrating amphibian species richness for each ECELS category. Data for ECELS category Poor is not shown as it only consisted of one observation. Significance levels between categories were assessed using Wilcoxon tests and are indicated by the lines between the boxplots. Each boxplot displays the median (horizontal line within the box), the interquartile range (box), and the range of the data excluding outliers (whiskers)
Fig. 3
Boxplots illustrating the distribution of the assessed variables considered in this study for the assessed ponds: A Amphibian species richness, B Emersed vegetation cover in the pond, C ECELS index values, D TRIX index values, E pond area, and F pond depth. Each boxplot displays the median (horizontal line within the box), the interquartile range (box), and the range of the data excluding outliers (whiskers)
Table 1
Rounded minimum and maximum values of ECELS, TRIX, pond area (m2), pond depth (m), and cover of emersed vegetation (%) of the ponds in which each amphibian species has been found. Also, if the species is included in the Annex IV of the European Habitats directive
Species
ECELS
TRIX
Pond area (m2)
Pond depth (m)
Vegetation cover (%)
Annex IV
Anura
Alytes obstetricans
65–90
1.2–5.1
55–248
0.2–0.6
0–60
⊠
Bombina bombina
71–98
2.1–4.6
60–850
0.3–0.7
0–80
⊠
Bufo bufo
50–99
0.6–4.8
98–12,163
0.2–2.3
0–100
Bufo spinosus
58–95
1.0–5.1
65–565
0.2–0.8
0–80
Discoglossus pictus
64–82
1.0–4.7
65–55,791
0.2–0.8
20–80
⊠
Epidalea calamita
76–87
1.7–3.4
504–11,646
0.2–2.3
30–80
⊠
Hyla arborea
83–98
1.4–3.2
600–1500
0.2–0.9
20–80
⊠
Hyla meridionalis
63–100
1.0–5.1
65–55,792
0.2–1.5
20–80
⊠
Pelobates cultripes
63–100
1.0–4.7
65–55,792
0.2–1.5
20–80
⊠
Pelobates fuscus
58–100
2.6–5.0
275–2800
0.1–1.3
10–100
⊠
Pelodytes punctatus
71–95
1.2–3.3
86–367
0.2–0.4
0–60
Pelophylax bedriagae
82–95
1.1–2.9
574–3295
0.8–2.0
10–80
Pelophylax lessonae
55–95
1.5–4.9
60–3360
0.1–1.7
0–85
⊠
Pelophylax perezi
55–100
1.2–4.1
56–14,689
0.2–1.2
0–80
Pelophylax ridibundus
59–95
0.5–3.4
33–12,163
0.2–2.6
10–100
Rana arvalis
71–88
2.7–4.6
180–3770
0.3–1.5
10–35
⊠
Rana dalmatina
71–97
1.7–3.9
391–4621
0.2–1.4
0–100
⊠
Rana temporaria
59–99
0.5–4.6
64–6787
0.2–2.1
0–100
Caudata
Ichthyosaura alpestris
55–90
1.1–4.3
34–4621
0.1–2.0
0–100
Lissotriton helveticus
63–99
0.5–5.1
55–6787
0.2–2.1
0–90
Lissotriton vulgaris
55–100
1.3–5.2
33–4250
0.2–1.9
0–100
Salamandra salamandra
42–95
1.0–5.1
56–565
0.2–1.1
0–60
Triturus carnifex
80–95
1.1–2.9
33–3295
0.4–2.0
10–100
⊠
Triturus cristatus
55–100
1.1–5.5
110–6561
0.2–9.0
0–100
⊠
Triturus marmoratus
53–100
1.0–5.1
55–55,791
0.2–1.5
0–80
⊠
×
×
Twenty-five amphibian species were detected in the 154 studied ponds (Table 1). The most frequent species was Lissotriton vulgaris, which was found in 52.6% of the ponds across the studied countries, followed by Triturus cristatus (37.7%), and Bufo bufo (33.8%). 56% of the species found are listed in the annex IV of the European Habitats Directive (1992) (Table 1), with ponds from Spain presenting the most protected species (Fig. 1). All the observed species are categorized as Least concern by the IUCN Red List (2023), except for Bufo spinosus (Not assessed) and Pelobates cultripes (Vulnerable).
The variable selection to assess the effect of pond condition on amphibian species richness yielded a final model that identified ECELS value, TRIX value and pond depth as significant predictors (Table 2). The results of the GLMM show that an increasing ECELS value had a positive, significant effect on amphibian species richness, while both pond depth and TRIX value had negative effects (Fig. 4). Further analysis using a GLMM to examine the effect of each ECELS component on amphibian richness (Table 3) reveals the significance of the littoral basin morphology, with higher values for this component correlating with greater amphibian species richness. Thus, ponds with gentle marginal slopes, lacking weirs, with permeable bottoms (no pond liners) and devoid of burial, supported more species. Additionally, the stepwise variable selection to assess the effect of pond condition on the richness of protected amphibian species listed in Annex IV of the EU Habitats Directive resulted in a GLMM that identified the significant and positive effect of ECELS on the richness of protected amphibian species (Table 4, Fig. 5).
Table 2
Results of the GLMM considering the total richness of amphibian species as the dependent variable. Statistically significant values (p < 0.05) are found in bold
Variable
Estimate
Std. Error
z-value
Sig
(Intercept)
0.916
0.412
2.220
0.026**
ECELS
0.011
0.004
2.587
0.009***
Pond depth
− 0.226
0.098
− 2.320
0.020**
TRIX
− 0.139
0.052
− 2.698
0.007***
*p < 0.1; **p < 0.05; ***p < 0.01
Fig. 4
Partial residual plots that show the relationship between amphibian species richness and the ECELS conservation index value (A), pond depth (B) and TRIX index value (C), in the GLMM defined in Table 2
Table 3
Results of the GLMM considering the total richness of amphibian species as the dependent variable and each of the ECELS components as dependent variables. Statistically significant values (p < 0.05) are found in bold
Variable
Estimate
Std. Error
z-value
Sig
(Intercept)
0.112
0.586
0.192
0.848
Basin littoral morphology
0.013
0.006
1.974
0.048**
Human activity
0.010
0.009
1.217
0.224
Water characteristics
− 0.015
0.022
− 0.700
0.484
Emergent vegetation
0.021
0.017
1.245
0.213
Hydrophitic vegetation
0.015
0.009
1.765
0.078
*p < 0.1; **p < 0.05; ***p < 0.01
Table 4
Results of the GLMM considering the richness of amphibian species included in the Annex IV of the EU Habitats Directive as the dependent variable. Statistically significant values (p < 0.05) are found in bold
Variable
Estimate
Std. Error
z-value
Sig
(Intercept)
− 0.826
0.608
− 1.360
0.174
ECELS
0.015
0.006
2.253
0.024**
Pond depth
− 0.230
0.145
− 1584
0.113
*p < 0.1; **p < 0.05; ***p < 0.01
Fig. 5
Partial residual plots that show the relationship between protected amphibian species richness and the ECELS conservation index value in the GLMM defined in Table 4
×
×
Discussion
The findings of our study underscore the critical imperative of preserving pond condition and reducing anthropogenic pressures to safeguard European amphibian populations. Our results suggest that shallow ponds in better condition, characterized by a high conservation status (ECELS), good water quality and a lack of eutrophication (TRIX), harbour the highest richness of amphibian species, and are more likely to harbour protected species. The ECELS index proves to be a valuable assessment and management tool in this context. Its ease of calculation and its ability to reliably predict the conservation status of ponds make it highly usable for practitioners (Gascón et al. 2009; Della Bella and Mancini 2010; Guareschi et al. 2015). By focusing on certain components of the ECELS index, managers could effectively prioritize actions to maintain or improve pond condition, thereby supporting amphibian diversity. Our results show that general practises that reduce anthropogenic stressors and maintain permeable, weirless ponds with gentle slopes are of great benefit for European amphibians. In this regard, the PONDERFUL technical guide (Biggs et al. 2024) can provide practical guidelines for managing, restoring, and creating ponds, as well as examples of success stories.
Indeed, the ECELS component relating to the pond littoral basin morphology is highly relevant for amphibians. Preserving pond features that allow amphibian colonisation and reproduction such as gentle marginal slopes devoid of artificial structures, and maintaining a permeable substrate, are essential strategies for sustaining ponds as amphibian habitats. Keeping a smooth littoral slope facilitates the expansion of flooded areas during periods of inundation, while also fostering the creation of diverse habitats, thereby enhancing overall pond biodiversity (Provete et al. 2014; Swartz et al. 2019). According to our results, shallow ponds exhibited greater amphibian species richness compared to deeper counterparts. This can be attributed to their increased susceptibility to drying, which limits fish colonization and consequent increased predation pressure on amphibian populations (Beja and Alcazar 2003; Semlitsch et al. 2015; Burrow and Maerz 2022). Hence, our findings underscore the critical importance of prioritizing pond morphology in management practices, in line with previous studies (e.g. Miler et al. 2013; Provete et al. 2014; Swartz et al. 2019).
Our findings also highlight the importance of maintaining good water quality and minimizing eutrophication pressures to support amphibian species richness. Elevated nitrogen and phosphorus concentrations, commonly linked to agricultural runoff and livestock activity, are known to stimulate pond eutrophication (Knutson et al. 2004). This can negatively impact amphibians by reducing survival rates of eggs and larvae and increasing their vulnerability to pathogenic infections (Knutson et al. 2004; Johnson et al. 2007), ultimately leading to declines in species richness (Johnson et al. 2007; Schmutzer et al. 2008). Given that the expansion of animal agriculture and cash crops represents the most significant global threat to amphibians (Luedtke et al. 2023), implementing nutrient load management practices in ponds could enhance amphibian reproductive success and biodiversity. By addressing eutrophication, conservation efforts can mitigate a significant threat to amphibian biodiversity.
Our findings have important implications for European pond management and conservation efforts. Conservation practitioners and policymakers should prioritize measures aimed at preserving and restoring natural pond attributes that promote amphibian biodiversity. This may include implementing strategies to mitigate nutrient pollution, preserving natural hydrological processes, and minimizing anthropogenic alterations to pond morphology. Maintaining these characteristics to improve pond condition not only benefits amphibian biodiversity, but also promotes the presence of protected amphibian species listed in Annex IV of the EU Habitats Directive, which are subject to strict protection regimes by EU member states.
Despite the severe threats that ponds are facing due to anthropogenic activities, these habitats remain a low priority for national (across many countries) and international conservation policies. Addressing the amphibian extinction crisis requires international collaboration and commitment to develop effective, practical conservation and management strategies (Hill et al. 2021; Luedtke et al. 2023). While habitat protection is crucial, it alone may not suffice in addressing challenges such as disease outbreaks, overexploitation, or the impacts of climate change, particularly since many threatened amphibian species occur in protected areas (Nori et al. 2015; Luedtke et al. 2023). Therefore, selecting an adequate scale to develop accurate conservation strategies for pond amphibians assumes paramount importance (Nori et al. 2015). One of the priorities of conservation policies should be to ensure the effective management and protection of existing ponds, with a focus on enhancing their condition, to maximize opportunities for maintaining and improving amphibian diversity, as suggested by the results of the present study. Integrating ponds within the broader landscape, creating new ones prioritizing proper morphological characteristics and water quality, and ensuring connectivity is also crucial considering the current, and anticipated, global change scenarios (Sayer and Greaves 2020; Hill et al. 2021; Luedtke et al. 2023).
In summary, our study emphasizes the critical importance of improving pond condition for amphibian conservation, as European ponds in a better conservation status and with a better water quality exhibit higher species richness. Our findings underscore the urgent need for effective management strategies to mitigate anthropogenic threats such as eutrophication and habitat degradation. By prioritizing local pond conservation efforts and integrating them into broader landscape-scale initiatives, we can increase the protection of amphibian biodiversity.
Acknowledgements
We would like to show our gratitude to all the teams and individuals from the participating countries of this research for their invaluable contributions and dedication. This research has received funding from the European Union’s Horizon 2020 research and innovation programme under grant agreement N°ID 869296–The PONDERFUL project. López-de Sancha, A., Boix, D., Benejam, L., Davidson, T.A., Lemmens, P., Mehner, T. and Brucet, S. were also funded by TRANSPONDER project under grant agreement Nº Biodiversa2022-64.
Declarations
Competing interests
The authors declare no competing interests.
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Amphibian conservation in Europe: the importance of pond condition
verfasst von
A. López-de Sancha D. Boix L. Benejam L. Briggs T. A. Davidson J. C. Fahy V. Frutos-Aragón H. M. Greaves P. Lemmens T. Mehner L. Martín B. Oertli C. Sayer S. Brucet
