Amphibians

Written by Dr Andrew Smart, Conservation and Science Manager

Concern over the impact of chemicals on the environment began in the 1960s following the publication of ‘Silent Spring’ by Rachel Carson, which highlighted the risks of using pesticides such as DDT. Support for agriculture through the ongoing use of pesticides, herbicides and chemical fertilisers continues to raise concerns because of the impacts on beneficial invertebrates and lower vertebrates such as amphibians and fish, leading to ‘build-up’ within food chains.

Chemical impacts on amphibians result from terrestrial spraying and from the acute and chronic effects of chemicals being carried into ponds and wetlands. Amphibians have life cycles that involve changes of form when in an aquatic environment: from egg to larvae and larvae to adult, and then a terrestrial phase as adult, returning to wetlands to breed. Chemical pollutants that have been found to impact amphibians include pesticides, herbicides, fertilisers, de-icing salts and road materials, heavy metals and lead, and further impacts from microplastics have been identified. Little work has been undertaken on UK species, with the bulk of ecotoxicological work undertaken in the USA and Europe, on species often similar to and sometimes of the same genus as UK species of newts, frogs and toads.

A review of the impact of agricultural chemicals on amphibians in 2009[1] found that interactions between agrochemicals and other environmental factors impacted amphibians, disrupting thyroid activity and other biochemical pathways, impacting metamorphosis and sexual differentiation. Exposure to insecticides led to impaired behavioural responses, impaired growth, delayed metamorphosis and increased use of detoxification pathways which could impact the immune repose to other factors because of increased energy use. These ‘sub-lethal’ effects are the focus of much of the recent research.

In 2012[2] and 2013[3] analyses of previously published work found the overall effects of pollutant exposure included a reduction in amphibian survival body mass and an increase in the frequency of abnormalities during development and metamorphosis. The measured impacts were found to lead to as much as 14% reduction in survival, 7.5% decrease in body mass and a 5 fold increase in abnormalities. Pollution appeared to have no impact on the time from spawning to hatching or the time to metamorphosis but were again found to lead to altered behaviour, changes to metabolism, reproductive failure and increased embryonic and larval mortality. Immunotoxicity was found to generate a sub-lethal effect leading to higher parasite load and subsequent population decline. Road de-icers were more toxic than nitrogenous compounds while pesticides and wastewater pollution caused an intermediate reduction in survival.

A further meta-analysis[4] in 2013 found that pesticides and fertilisers had a significant negative effect on survival and growth across all the amphibian species studied with marked differences between chemical classes in their impact on amphibians: many inorganic fertilisers, insecticides and herbicides negatively affected amphibian survival, while some negatively affected larval growth.

 

Pesticides

Investigation in the USA[5] found complex mixtures of pesticides from wetlands including up to 8 fungicides, some previously unreported in tissue. Many studies describe wastewater contaminants as a significant threat to amphibian species based on their lethal and sub-lethal effects; amphibians can be subject to damage through skin and food ingestion[6]. Agricultural chemicals used as individual ingredients and mixed together led to sub-lethal changes in stress levels and physiological responses in amphibians[7].

A 2023 meta-analysis investigating the impact of different types of disturbance on reptiles and amphibians found the greatest impact occurred from drought, followed by invasive species and then agriculture. The review[8] found that agriculture had a moderate to large negative impact on body condition linked to low quality habitat, lack of foraging habitat and shelter on the impact of chemical contaminants. Many studies were listed indicating negative effects of pesticide exposure on embryos and developing tadpoles, including deformities, arrested development, mortality, endocrine and immune disruption, and increased disease susceptibility. Pesticide residues are broken down through processes into various ‘transformation products’[9] which have been detected in groundwater and surface water. Investigation of the effects of widely used pesticides and their transformation products in cell cultures found that approximately 50% of the transformation products exhibited stronger effects than the original pesticides.

Endosulfan, an organochlorine pesticide that is found in many ecosystems, including wetlands particularly in proximity to agriculture^[10] , has been found to have a sub-lethal effect affecting tadpole activity and survival. In amphibians, pesticide exposures have been shown to alter biochemical processes ^[11], reduce tadpole survival to < 1%, survival to 10%[12] and impairment of mobility ¹². Another pesticide, chlorpyrifos, has also been shown to alter tadpole brain development[13] .

Other pesticide compounds, also found in products including detergents, plastics, emulsifiers and cleaning products, impact newt physiology, disrupting reproduction, metamorphosis and the ability of amphibians to respond to changing environments[14] and  may also induce organ toxicity[15]. Pesticide linked compounds that increase the ability to ‘stick’ to surfaces, at sub-lethal concentrations have also been found to create physiological changes in amphibians[16] and some affect hormone systems with feminising effects on male gonad development identified in one study in the USA. [17] 

Pesticides can have other effects with disruption of pheromone communication in newts leading to a delayed response to female odours and, consequently, a reduction in mating success[18]. The impact is not restricted to larvae or aquatic systems, a study on the effects of seven pesticide products on juvenile European common frogs (Rana temporaria) in an agricultural overspray scenario found mortality ranged from 100% after one hour to 40% after seven days at the recommended label rate of currently registered products[19].

 

Non-agricultural pesticides

In the UK, chemicals that are banned for routine agricultural purposes are sold as parasiticide treatments for pets[20] and can enter the natural environment. Their active ingredients are toxic to many freshwater species and concentrations found from field studies are likely to negatively affect aquatic life, impacting food webs and amphibians in urban and semi-urban ponds and wetlands.  One study analysed water from 20 English rivers and found pesticide contamination of waterways via household drains, hypothesised to be from control of ectoparasites on pets. Seven out of 20 sites exceeded the level that would lead to chronic impact on ecosystems[21]

 

Herbicides

The use of glyphosate as herbicide varies within the environment and little is known about environmental concentrations in agricultural ponds and wetlands. The wide range of glyphosate compounds have different effects on amphibians; but the impact of direct over-spraying in terrestrial environments has been found to result in 79% mortality of Anurans[22]. Variation has been found from taxonomic group to taxonomic group with deformities appearing in larvae and one study reporting endocrine disruption, effects on development and inhibition of enzymes.  Other studies on the impact of ‘Roundup’ herbicide found that direct over-spray killed 96-100% of larval amphibians and 68-86% of post-metamorphic juvenile amphibians[23]. Additionally, herbicides have been found to indirectly increase amphibian susceptibility to trematode (parasite) infections by increasing the time spent in susceptible early developmental stages and suppressing tadpole immunity[24]. Research on common toad tadpoles found that younger tadpoles are more susceptible to glyphosate resulting in increased time to metamorphosis and reduced size of metamorphs[25]. Glyphosate has also been found to reduce tadpole survival and damage the cutaneous bacterial community[26]. Other studies have found that herbicide exposure can also disrupt amphibian immune responses¹,[27], [28] and feminization of male gonadal development has been found following the use of the herbicide atrazine¹⁷.

 

Fertilisers

Changes in rainfall and runoff can lead to increased amounts of nitrogenous compounds and agricultural ponds and wetlands¹. Ammonia and nitrite concentrations often increase after pollution incidents, but these break down to nitrates in waterbodies. A 2020 review of the impacts of nitrate on amphibians[29]  covered 46 studies and found nitrate led to a maximum decrease in activity of 79%, a decrease in growth of 29%, and can reduce survival by 62%. Nitrate exposure influenced all life stages except embryos, and nitrates in combination with other stressors can affect survival. Toxicology studies looking at ammonium nitrate[30]  and acidification of water bodies found that in the dwarf newt (a species in the same genus as the great crested newt) neither ammonium nitrate nor pH inhibited oviposition but the percentage of eggs that were ‘wrapped’ by females was lower at low pH, which could reduce survival rates.

 

Road de-icers

De-icing salts pose serious ecological risks to amphibians due to salinity increases and direct toxicity of chloride. Salts can have an extreme adverse effect on amphibians at all life stages[31], though embryonic and larval life stages are more sensitive than adults[32]. Road salt has been found to travel up to 172m from roads into wetlands and in the USA, egg mass densities of spotted salamanders and wood frogs were found to be reduced in roadside pools[33]. Road salts, as with many other pollutants, disrupt physiology and increase susceptibility to climate impact or disease. Populations exposed to salt runoff had slightly more frequent ranavirus related mass mortality events, more lethal infections, and greater pathogen environmental DNA[34]. Larvae raised in elevated salinity had 10 times more intense infections and shed five times as much virus as controls, suggesting increased transmission rates of viruses. In North America, wood frog populations living adjacent to roads had higher incidence and severity of oedema[35]  (bloating caused by subcutaneous fluid accumulation) during the breeding season, than frogs living away from the influence of roads. This was a direct impact of increased conductivity in breeding ponds, probably caused by road salt used for de-icing, and impacted movement, jumping ability and energy availability as well reducing muscle mass and causing skin damage.  Elevated salt concentrations have been found to increase both deformity frequency and severity³². Road salt (NaCl) in “low” concentrations has been shown to irreversibly disrupt the osmoregulatory ability of salamander eggs[36], [37] .

One study found that the concentration of total polycyclic aromatic hydrocarbons (PAH) from industrial waste, vehicle exhausts, oil leaks and sealants from pavement surfaces has increased while other persistent organic pollutants tended to remain stable or declined[38]. Urbanized watersheds experienced greater rises in PAH concentration compared to non-urban lakes with runoff from surfaces coated with coal–tar having higher concentrations of PAHs than runoff from asphalt-sealed or cement surfaces. Newts exposed to sediments containing coal–tar and asphalt had reduced ‘righting ability’ and diminished liver enzyme activities.

 

Metals

Some metals also have a sub-lethal effect on amphibians, raising their susceptibility to disease with an increase in evidence that lead accumulates in the tissues of fish and amphibians[39] and causes sub-lethal stress relating to haematology[40], oxidative stress, neurotoxicity and immune responses (in fish)[41] and affects metamorphosis and haematological[42]^,[43]and biochemical processes in amphibians[44].  The accumulation of lead in body tissues of these taxa will further impact predatory aquatic birds such as egrets, herons and kingfishers, feeding at the top of the food web. Heavy metal pollution effects movement and fitness of tadpoles[45] , with reduced swimming speed and disrupted swimming response suggesting a sub-lethal effect.  At a  UK Toad tunnel where amphibians cross below a busy road, seven out of eight tested metals including copper, zinc, lead and iron were in significantly greater concentrations in the tunnel than at a control site and were present in environmentally significant concentrations[46]  . Water samples also exhibited elevated concentrations of aluminium and chromium and occasionally an extreme alkaline pH, associated with leaching of portlandite in tunnel cements.

 

Microplastics

In 2019 the first record of microplastics from an amphibian stomach content (the stomach of the Italian crested newt) was recorded in a high-altitude environment in Italy[47]; an indication of the pervasive nature of microplastic pollution. Microplastics are transported by air or water and are small enough to be eaten by zooplankton and hence have a role within the food web in freshwater systems, where microplastic pollution maybe between 4 and 23 times higher than in the sea.[48].  In a 2022 review[49] investigating the impact of microplastics on amphibians found studies that indicated changes to body condition, increased susceptibility to infection or disease and where microplastics had an impact on survival and growth, bioaccumulation and toxic responses, malformation and swimming behaviour.

The extent of microplastic pollution is indicated by a 2020 study in Poland[50] which collected 201 tadpoles from 5 species at 8 different sites and found microplastics at all of the sites and in all five species; between them 26% of the tadpoles had ingested 71 different microplastic compounds. Links have been established between the number and variety of microplastics found within the larval stages of amphibians and the proximity of anthropogenic habitat to sites[51]. Where anthropogenic or ‘non-natural’ land cover was present the microplastic pollution in the larvae increased; roads have been found to be an important source of microplastic particles in the environment[52], through release of particles from tyres, road markings and polymer-modified bitumen, released through the wear and tear of tyres and the road surface.

 

Implications for amphibian metapopulations

In Scotland, a review of literature[53] found no Scottish study that has reported the effects of agrichemicals as demonstrated elsewhere, suggesting that much of the pollution is linked to agriculture that uses more agrochemicals. A 2021 study in Belgium[54]  sampled 26 amphibian breeding ponds and tested for 178 different compounds from 5 agrochemical groups to determine the frequencies of different compounds in wetlands.  Agrochemical compounds were present, with some occurring in only  1 of 26 ponds while others were in all 26. The 26 ponds were fed by runoff water and compounds found included anti-microbial drugs, anti-parasitic drugs, anthelmintics, mycotoxins, heavy metals and pesticides. 

In many amphibians, metapopulations consist of ‘source’ ponds and ‘sink’ ponds which vary year on year and in different environmental conditions.  Low annual survival of great crested newts (Triturus cristatus) is often related to mild winters and heavy rainfall, which can impact a metapopulation at the regional level[55]. A study in Kent found that some sub-populations suffered reproductive failure in most years, and recruitment to the metapopulation relied on the presence if a single ‘source’ pond. A population viability analysis at the Kent site confirmed that extinction risks increased when adult survival declined. In temperate ectotherms, mild temperatures during the winter can result in hibernating animals continuing to deplete energy reserves while being unable to feed, resulting in poor breeding condition the following spring. The ongoing sub-lethal effects of pollutants may act to exacerbate the impact of mild winters and increase the likelihood of an animals failing to breed or even failing to survive the winter.

Many of our amphibian species are in decline and based on the evidence presented above one could argue for a ‘rethink’ of our agricultural strategy to encourage the ‘re-construction’ of ponds for flood management and as reservoirs for biodiversity. The benefit of replacement of hedgerows and woodland to support pollinators and predators of insect pests will also benefit amphibians. Review of the use of pesticides and fertilisers and their impact on amphibians and on invertebrates, fish and animals further up the food chain will ensure there is minimal risk to humans and benefit to biodiversity.  This risk of acute or chronic toxicity to amphibian species from agrochemicals in our managed landscape is high and, along with:

• loss of terrestrial habitat such as hedgerows and woodland,
• loss of aquatic habitat with the ‘pondscape’ leading to reduction in pond density
• road mortality during migration
• invasive species and fish introductions
• non-native diseases
• the impact of climate change on overwintering
• climate change leading to drought events

they cause sub-lethal effects that impact reproduction, metamorphosis and resistance to parasites and disease. Action is needed now to change the way agrochemicals are used, so we can avoid the loss of nocturnal amphibian choruses and a new ‘Silent Spring’.

 

References

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