Croaking Science

Croaking Science: Pond Creation Works

November 29, 2022 by Roger Downie

Written by Roger Downie, Froglife and University of Glasgow

Froglife’s vision is of a world in which reptile and amphibian populations are flourishing as part of healthy ecosystems. One of the ways in which we work towards this overall aim is by transforming landscapes: increasing the availability of freshwater and terrestrial habitat suitable for amphibians and reptiles. Our ‘living water’ series of projects has addressed this by creating and repairing ponds around the UK. Producing habitats is the first part of the task, but we also need to assess how well these habitats perform in helping populations to grow. Our strategy commits us to evaluating project sites for up to 10 years after completion, with some remedial work possible if damage, such as vandalism is found.

What does the scientific literature tell us about the success of created ponds? Smith et al. (2020) reviewed 28 published studies from around the world, and concluded that pond creation is an effective, beneficial conservation action. Some of the studies concerned small numbers of ponds over a fairly short time, but others were much larger in scope e.g. a Danish study of 3446 ponds over 11 years. Now comes a major study from the Swiss canton of Aargau (Moor et al., 2022) published in the high-profile journal Proceedings of the National Academy of Sciences, USA (PNAS).

Aargau, in the north of the country on the border with Germany, is one of the most densely populated and least hilly parts of Switzerland. Although about one-third wooded, it includes many small towns and an extensive road network with much agricultural land. Following concern about 30 years ago over the decline in amphibian populations (around the time of the creation of IUCN’s Declining Amphibian Populations Taskforce- DAPTF), a pond creation programme began in 1991 and continues. Moor et al. have analysed up to 20 years of data from 856 ponds, 422 of them constructed as part of the conservation programme. The canton is home to 12 species of pond-breeding amphibians (eight anurans and four newts). The authors note that these species differ in their characteristics: life history, habitat preference, and dispersal ability.

Across the whole canton, the number of ponds occupied by amphibians increased over the period 1999-2019 for 10 of the 12 species: the number remained pretty constant for the midwife toad and declined significantly only for the natterjack toad. Results differed between regions: essentially, the more ponds constructed in a region, the more metapopulations increased and the fewer declined (‘metapopulation’ here meaning the number of ponds occupied per species). The authors detected three mechanisms at play in the effects of new ponds on metapopulation sizes. First, the increased number of ponds increases breeding habitat, particularly benefitting mobile generalist species like the common toad. Second, the constant addition of new early succession stage ponds benefits pioneer species such as natterjack toads: they prefer shallow ponds with short hydroperiods, lacking vegetation and predators; it is likely that most of the constructed ponds lacked these features, and that older ponds were losing the features suitable for natterjacks, hence this species was the only one to show a decline across the canton. Third, increased pond density enhances connectivity, a particular benefit for species with low dispersal ability, like newts.

Although new ponds were rapidly colonised by several species, populations did not always persist. This could be the result of several factors, such as eventual colonisation by predators not initially present, or successional changes that made the new ponds less suitable for early colonisers. The only species where persistence probability was higher in new than in old ponds was the tree-frog, Hyla arborea: the reasons for this are not clear, but the result was a particularly sharp increase in metapopulation size across the study from <25 to over 75 sites. Several factors mattered for the success of new ponds: surface area and shape (most often, large pond size led to more species, but one species, the yellow-bellied toad Bombina variegata preferred smaller ponds; the type of surrounding habitat (some species had positive associations with surrounding forest, but natterjack toads and smooth newts preferred less forested surroundings); roads generally had negative effects on dispersal and colonisation.

The authors made the ‘encouraging conclusion’ that ‘no effort in pond construction is really wasted’. The continuous creation of new ponds helped amphibian populations to recover despite the persistence of threats like increasing urbanisation and associated roads, the presence of non-native fish and pathogens, and the effects of agrichemicals. However, there are caveats related to the particular circumstances of this study. The canton of Aargau is 37% forested, providing abundant habitat for amphibian dispersal and shelter; contrast this with the UK at 13% (England even less at 10%). The range of species in Aargau is quite large, with their range of needs being diverse enough that different kinds of ponds can be suitable for some if not all. The authors comment particularly that pond creation in the tropics may have limited value, since so many species are not pond breeders.

Finally, the authors note that it was crucial to the success reported in their study that the authorities in Aargau responded quickly to the evidence of amphibian declines by enabling a long-term pond creation programme with associated monitoring. Froglife has often been able to find funding for pond creation projects in particular areas, but funding the monitoring has been more difficult, and persuading authorities (and funders) to think of pond creation as long-term commitment is more difficult still.

References

Moor, H. et al. (2022). Bending the curve: simple but massive conservation action leads to landscape-scale recovery of amphibians. PNAS 119, e2123070119.

Smith, R.K. et al. (2020). Amphibian Conservation. Ps 9-64, in: Sutherland, W.J. et al. (eds.) What works in conservation 2020. Open Book Publishers, Cambridge, UK.

Croaking Science: The International Trade in Reptiles and Amphibians

August 30, 2022 by Roger Downie

Part 2: Amphibians

Roger Downie, Froglife and University of Glasgow

In Croaking Science (July, 2022), I introduced the topic of the international trade in wildlife, and then focused on reptiles. This article is a companion piece, concentrating on amphibians. It will cover the frogs’ legs and pet trades, discussing their impact on wild amphibian populations, disease spread and amphibian welfare. As I was researching the topic, an excellent report on the frogs’ legs trade appeared (Altherr et al., 2022), and I have drawn heavily from it.

The existence of trade implies that people make use of amphibians. Let’s start by summarising such uses. First, amphibians as food. We may think mainly of frogs’ legs as a delicacy in French cuisine (and certainly not as a dietary essential), but amphibians form part of the diet in many cultures, with frog meat for sale in markets across Africa, Asia and Latin America. The mountain chicken (Leptodactylus fallax) was long the national dish of the Caribbean island of Dominica, until declining numbers led to a hunting ban: chytrid then nearly finished the species off, but major conservation efforts are in progress (Nicholson et al. 2020). Second, people have long been aware of the rich variety of substances in amphibian skins. Traditional healers around the world have employed concoctions from frog skin as medicines and the Amerindians of Latin America famously tip their hunting arrows with the secretions of Poison Dart Frog (dendrobatid frog) skin. Modern research is testing amphibian skin derivatives for substances of real medical benefit (see Crump, 2015: reviewed in Natterchat, Spring/Summer 2017) Third, amphibians have long played a role in scientific research: for example, Galvani and Volta’s 18^th century experiments with electrical stimulation of frogs’ legs. More recently, the African clawed frog Xenopus laevis became a fixture of hospital laboratories when it was discovered that urine from pregnant women stimulated female Xenopus to ovulate: the basis of the first reliable pregnancy test. Stimulation of ovulation then allowed Xenopus eggs to be the model of choice for studies on embryonic development. Finally, some people like to keep amphibians as ‘pets’: this often involves colourful and exotic species.

Traditional uses, such as being a small component in a local diet or in medicine, do not necessarily involve international trade, nor are such uses likely to create a conservation threat, unless exploitation becomes unsustainable, as in the case of the mountain chicken. However, the frogs’ legs and pet trades are problematic, and this article focuses on them.

Import/export of frogs as food The USA and Europe are the main importers of frogs for food. The USA imports four species: the bullfrog Lithobates catesbeianus from Mexico, Ecuador and China; the East Asian Hoplobatrachus rugulosus from Thailand and Vietnam; Forrer’s leopard frog Lithobates forreri from Mexico; and the pig frog Lithobates grylio from China. The dominant species was L. catesbeianus, with 14.5 thousand tonnes imported as live individuals or frozen meat over the period 2015-20. Frogs were both wild caught and farmed (note that this species is a USA native, but has been both released and farmed in many other countries).

During the period 2010-19, the European Union (still including the UK) imported 40.7 thousand tonnes of frogs’ legs, derived from 814 million to two billion adult frogs (a wide range because of frog size differences). The most significant importing country was Belgium (69.9%), with France second (16.7%) and the Netherlands third (6.4%). However, much of the Belgian consignments moved on to France which is the predominant consumer country. Indonesia is the main supplier (74%), followed by Vietnam (21%), Turkey (4%) and Albania (1%). India and Bangladesh were formerly major suppliers, but the relevant species were CITES listed in 1985 and exports stopped, with Indonesia becoming the main new source. The species mainly imported into Europe are not reliably known: Ohler and Nicholas (2017) used DNA sequencing to show that 99% of frogs’ legs for sale in French supermarkets were incorrectly labelled as to their species identity. This is not necessarily deliberate: it is common for collectors of wild frogs in Indonesia not to know the identity of the species, and most of the Indonesian ‘crop’ is wild caught. However, this is clearly a problem if there is a need to conserve species from over-harvesting.

The frogs’ leg trade is mainly as frozen meat, so there are no welfare issues in the transportation phase, but there may well be welfare issues during capture and killing, so far negligibly reported. The Indian trade was halted because of worries that natural populations were becoming severely depleted, but also because of a realisation of the ecological role played by healthy frog populations, especially in rice paddy fields where they help control biting insects: the use of pesticides as an alternative is an extra cost to farmers, as well as adding risks of toxicity (Propper et al. 2020). It is so far unclear whether frog harvesting in Indonesia is having similar effects, but shifts in the species make-up of frog imports suggest some impact on native populations.

Frog farming is seen by some as a means of making the frogs’ leg trade sustainable: frog farming will be discussed in a future Croaking Science article.

Amphibians in the international pet trade Tapley et al. (2011) estimated that 127 species of amphibians were on sale from UK pet shops in 2004-5, an increase of 160% from 1992-3. They argue that the pet trade can benefit source economies and provide a stimulus for conservation by providing local people with an incentive for sustainable harvesting (a similar argument is used to justify trophy hunting in countries where there is potential conflict between large mammals like lions, and local farmers). However, Tapley et al. acknowledge the problem that local people are the least likely to obtain significant financial benefit from live frog collecting. Altherr and Lameter (2020) found 352 amphibian species in the German pet trade in 2017-18. Their particular concern was the number of species offered for sale which had only recently been described by science, and whose status in the wild was usually still unknown. They found 46 species of reptiles and amphibians offered for sale that had been first described in the period 2008-17, one within 3 months of description. It was clear that collectors were able to use the locality details in the scientific description to capture individuals which could then be sold at high prices on the basis of their novelty and rarity. It was also clear that the motivation driving some hobbyists is to possess a collection of rare and exotic species: a live animal collection of this kind is therefore more similar to a collection of artefacts like paintings than it is to possessing pets which can be classed as ‘companion animals’. Auliya et al. (2016) contend that the global trade in amphibians has helped bring many species to the brink of extinction, and that trade regulation urgently needs strengthening. It is noteworthy that, while amphibians are the vertebrate group with the highest proportion of species threatened with extinction (about one third of species), only 197 species (2.1% of the total) are listed in CITES appendices 1 and 2.

Oriental fire bellied toad: a popular exotic pet

One of the causes underlying the worldwide declines in amphibian populations is the spread of chytrid disease. Schloegel et al. (2009, 2012) documented the role of the live wildlife trade in the spread of the disease: they found a prevalence of 62% for chytrid and 8.5% for ranavirus in live frogs imported into the USA. Grear et al. (2021) reported on the ban on live urodele importation into the USA, which has so far been effective in stopping the spread of the urodele-specific species of chytrid, Batrachochytrium salamandrivorans : this disease is a particular worry because of the large number of endemic urodeles in the USA. Borzee et al. (2021) note that the amphibian trade may not only have a role in the spread of amphibian diseases: by affecting insect vector populations, amphibian harvesting may contribute to the spread of diseases of humans and domestic animals.

Finally, welfare. It is likely that the risks to individual amphibians from the live animal trade are higher than to reptiles, given their stringent physiological needs, especially for water. Lambert et al. (2022) discuss the risks to amphibians inherent in the way that they are collected, transported, sold and kept. Ashley et al. (2014) reported on the police raid on the warehouse of US Global Exotics that found large numbers of amphibians in such poor condition that 44.5% died within 10 days of discovery, despite skilled efforts to help them recover.

Conclusion Both the frogs’ legs and amphibian pet trades are highly problematic and need further investigation. It is hard to argue against Auliya et al’s (2016) plea for improved regulation. It may be of interest here that in the Australian state of Victoria, only native species of amphibians and reptiles can be kept by private owners, and that they have to be licenced (Howell et al., 2020). Could such a legal framework be effective elsewhere?

References

Altherr, S. and Lambert, K. 2020. The rush for the rare: reptiles and amphibians in the European pet trade. Animals 10, 1-14.

Altherr, S. et al. 2022. Deadly dish- role and responsibility of the European Union in the international frogs’ legs trade. Pro Wildlife and Robin des Bois. Munich and Paris. Published on-line.

Ashley, S. et al. 2014. Morbidity and mortality of invertebrates, amphibians, reptiles and mammals at a major exotic companion animal wholesaler. Journal of applied animal welfare science 17, 308-321.

Auliya, M. et al. 2016. The global amphibian trade flows through Europe : the need for enforcing and improving legislation. Biodiversity and Conservation 25, 2581-2595.

Borzee, A. et al. 2021. Using the global 2020 pandemic as a springboard to highlight the need for amphibian conservation in eastern Asia. Biological Conservation 255, 108973.

Crump, M. 2015. Eye of newt and toe of frog, adder’s fork and lizard’s leg: the lore and mythology of amphibians and reptiles. University of Chicago Press, Chicago.

Grear, D.A. et al. 2021. Evaluation of regulatory action and surveillance as preventive risk-mitigation to an emerging global amphibian pathogen Batrachochytrium salamandrivorans (BSal). Biological Conservation 260, 109222.

Howell, T.J. et al. 2020. Self-reported snake management practices among owners in Victoria, Australia. Veterinary Record 187 (3), 114.

Lambert, H. et al. 2022. Frog in the well: a review of the scientific literature for evidence of amphibian sentience. Applied Animal Behaviour Science 247, 105559.

Nicholson, D.J. et al. 2020. Cultural association and its role in garnering support for conservation: the case of the mountain chicken frog in Dominica. Amphibian and Reptile Conservation 14, 133-144.

Ohler, A. and Nicholas, V. 2017. Which frog’s legs do froggies eat? The use of DNA barcoding for identification of deep-frozen frog legs (Dicroglossidae: Amphibia) commercialized in France. European Journal of Taxonomy 271, 1-19.

Propper, C. et al. 2020. Role of farmer knowledge in agroecosystem science: rice farming and amphibians in the Philippines. Human-Wildlife Interactions 14, 273-286.

Schloegel, L. et al. 2009. Magnitude of the US trade in amphibians and presence of Bd and ranavirus infection in imported North American bullfrogs. Biological Conservation 142, 1420-1426.

Schloegel, L. et al. 2012. Novel, panzootic and hybrid genotypes of amphibian chytridiomycosis associated with the bullfrog trade. Molecular Ecology 21, 5162-5177.

Tapley, B. et al. 2011. Dynamics of the trade in reptiles and amphibians within the UK over a ten year period. Herpetological Journal 21, 27-34.

Croaking Science: The international trade in reptiles and amphibians

July 21, 2022 by Roger Downie

Part 1: Reptiles

Roger Downie, Froglife and University of Glasgow

You can read part 2 of this series here.

Froglife recognises that some people derive their interest in and enthusiasm for reptiles and amphibians through keeping them, and that most such hobbyists do their utmost to provide the best conditions they can for the animals in their care. Nevertheless, Froglife’s view is that the life of these animals in captivity rarely meets their needs, especially in the case of animals which have been captured in the wild and then transported over long distances, prior to their sale and eventual residence in an enthusiast’s home. There are three fundamental issues facing the international trade in reptiles and amphibians. First, what impact does the trade have on the conservation status of these species, especially when we consider that amphibians are recognised as the most threatened of the terrestrial vertebrates (and reptiles may not be so different)? Second, to what extent does international trade in live wild animals contribute to the spread of diseases, both of wildlife and of humans? Third, how does the trade impact on the animals’ welfare? In two Croaking Science articles we will examine the international wildlife trade: first, reptiles.

Since 1975, the international trade in wildlife has been partially regulated by the Convention in International Trade in Species (CITES) of wild flora and fauna, which most countries (180+) have ratified. CITES regulates trade in species where trade might threaten their survival. Species are listed under three Appendices: 1- species threatened by extinction: only non-commercial trade under exceptional circumstances is permitted; 2- trade is regulated in order to avoid utilization incompatible with survival; 3- species threatened in a single country which therefore wishes to limit trade. Currently, 6.6% of reptile species (875 of 13,283) are on Appendices 1 and 2, including all crocodilians, sea turtles and boas/pythons.

Analysis of CITES data on the reptile trade by Marshall et al. (2020) shows that five genera (Alligator, Caiman, Python, Crocodylus, Varanus) comprise 84% of legally traded items. Most of this is skins for the fashion industry, and about 50% of this is not wild caught: i.e. it is derived from farmed animals. However, Marshall et al. also show that CITES regulations only cover a small proportion of internationally traded reptile species. Many animals are traded using the internet, mostly as part of the exotic pet trade: their estimate is that at least 36% of all reptile species are traded to some extent (compared to only 6.6% of species being CITES listed). To give a feel for the numbers involved, Auliya et al. (2016) calculated that the EU alone legally imported 20.8 million live reptiles over the period 2004-14. These numbers are certainly underestimates of the full trade. Sung et al. (2021) have shown that many freshwater and terrestrial chelonians are sold without regulation via social media sites (Hong Kong has one of the largest markets), and that much of this involves illegally harvested specimens. Worse, Stringham et al. (2021) report that a proportion of such trade does not occur on ‘observable sections of the internet’ i.e. it happens on the dark web. Vamberger et al. (2020) report that around 100,000 star tortoises are illegally collected and exported from India each year: many are confiscated and released, but the lack of data on where they were collected means that they are released in inappropriate locations, contributing to loss of local adaptations. Harrington et al. (2021) analysed information held by Facebook on wild animal exports from Togo, an important trade hub in west Africa. Of 187 species traded, 102 were reptiles, most of them not evaluated for the IUCN Red List, nor on CITES appendices. Can et al. (2019) found Peru to be the biggest contributor to the trade in live reptiles, 1.7 million individuals over 5 years.

The number of described species of reptiles increases by about 200 each year (see the on-line Reptile Database). One of Marshall et al.’s more disturbing findings is that recently-described species are being traded soon after their formal identification and well before their ranges, ecology and conservation status can be properly assessed. Altherr and Lameter’s (2020) analysis of the live amphibian and reptile trade in Germany (2017-18) found that 46 of the species traded had only been described by science in the previous decade, with most still lacking IUCN assessments: they concluded that for some hobbyists, a major motivation is the rarity and novelty of the animals.

So, is the international trade in reptiles a threat to their survival? One argument is that a well-regulated sustainable trade (i.e. based only on animals which can be harvested without damaging the state of wild populations) can provide an income for people who live in poverty in tropical countries that are rich in wildlife: the income gives an incentive to manage the wildlife resources well, rather than destroying them (Tapley et al. 2011). This is an extension of the idea that big game hunting helps conserve populations of charismatic large mammals in Africa. It is problematic in several ways: for example, do the poor people get much of the income flowing from wildlife harvesting, and which examples show human populations are capable of long-term sustainable wildlife harvesting (certainly not fishing)? For reptiles, Marshall et al. argue that we need a new basis for regulation founded on the precautionary principle: i.e. populations should be shown to be sustainable before any harvesting is permitted. Macdonald et al. (2021) agree: their analysis of the wildlife trade identifies ‘ten tricky issues’ inherent in both the legal and illegal trades, and concludes that the onus should be on traders to demonstrate that their trade is sustainable, humane and safe (with respect to disease and ecological invasion risks). The covid pandemic has concentrated concerns that international movements of wildlife contribute to disease spread (Can et al., 2019), but reptiles have not so far been focused on. And it is well known that exotic species of reptiles are often found in the wild, having been released as no longer wanted pets: depending on their origins, they may be able to establish populations.

Next, issues of welfare. As noted above, most of the trade regulated by CITES is in reptile skins. So any welfare issues relate to how the skins are harvested and how the animals are kept, if farmed (a future Croaking Science will investigate welfare conditions on reptile and amphibian farms). However, the larger reptile trade by species numbers is in live animals for the exotic pet trade. Welfare issues arise during the capture, transport and retail phases of this trade, as well as at the final location that the animals live. Not surprisingly, evidence on welfare in the illegal wildlife trade is hard to come by, but this is true even of the legal trade. Baker et al. (2013) reviewed 292 published papers on the live wildlife trade and found that only 17% included any reference to welfare, and these mainly applied to mammals. Wyatt et al.’s (2022) more recent review shows that this lack of information remains the case, and they argue that welfare issues ought to be at the forefront of discussions on how to reform the live wildlife trade. They quote an EU study that estimated that 70% of animals die within six weeks at commercial animal supply houses, and that 75% of pet reptiles and amphibians die within their first year, as a result of inappropriate care. Ashley et al. (2014) reported on what might seem an extreme case: the entire stock (26,400 animals from 171 species) held by the US company Global Exotics in Texas was confiscated following an inspection which showed 80% of the animals were grossly sick, injured or actually dead, with the remainder judged as in sub-optimal condition. During the 10 days following the confiscation, the mortality rate of the reptiles was 42%. Contributory factors were poor hygiene, poor food, inadequate water and heat provision, high levels of stress, over-crowding and poor or minimal environmental enrichment. In the subsequent court case, the company claimed that their mortality rates were similar to the industry standard! Harrington et al.’s work on the Togo wildlife trade also found welfare standards to be poor: no enrichment; poor shelter provision; inadequate space and water. The complexity and flexibility of reptile behaviour is increasingly being appreciated: see Lambert et al.’s (2019) review on reptile sentience and Downie (2021) on welfare and enrichment in captive reptiles.

In summary, the international trade in live reptiles may be contributing to biodiversity decline and is certainly causing suffering to a huge number of animals, especially when the trade is illegal and unregulated. What can be done? Restricting supply is the approach generally advocated, through attempts to stop poaching and by improved customs checks, but these suffer from poor resources in the countries where the animals live, and most emphasis tends to be on charismatic mammals like elephants and rhinos, rather than on reptiles. Thomas-Walters et al. (2021) focus on the factors that generate demand for wildlife: as noted above, some people are motivated by novelty, or rarity, so possessing a species few others have, rather like rich people who own expensive paintings. Thomas-Walters et al. identified five general motivations: experiential, social, functional, financial and spiritual, and discussed ways of reducing demand in each category. A UK government initiative, the Illegal Wildlife Trade Challenge Fund provides significant funding for projects aimed at combatting the illegal trade in wildlife, mostly in mammals, but projects on reptiles have been supported. Another angle is to focus on improving welfare. This is a tricky argument if one’s basic contention is that keeping captive wild reptiles should be stopped, since improved welfare standards might reduce the force of that overall aim. However, given that keeping wild reptiles in captivity is unlikely to stop soon, it is at least reasonable to urge for improved welfare standards. Williams and Jackson (2016) surveyed information available on welfare standards for reptiles in the UK pet trade, in the context of the UK’s Animal Welfare Act (2006) which provides guidance for the welfare of common companion animals, but not for reptiles. They found that some pet shops provided excellent advice on reptile care, but that many did not: e.g. only 8% gave advice on signs of ill health. The Federation of British Herpetologists has published ‘Good Practice Guidelines, 2015’ for private keepers of reptiles and amphibians, but Warwick’s review (on-line) is very critical of many of its claims, while accepting that some of the advice is helpful.

You can read part 2 of this series here.

References

Alterr, S. and Lameter, K. 2020. The rush for the rare: reptiles and amphibians in the European pet trade. Animals 10, 1-14.

Ashley, S et al. 2014. Morbidity and mortality of invertebrates, amphibians, reptiles and mammals at a major exotic companion animal wholesaler. Journal of applied animal welfare science 17, 308-321.

Auliya, M. et al. 2016. Trade in live reptiles, its impact on wild populations, and the role of the European market. Biological Conservation 204, 103-119.

Baker, S.E. et al. 2013. Rough trade; animal welfare in the global wildlife trade. Bioscience 63, 928-938.

Can, O.E. et al. 2019. Dealing in deadly pathogens: taking stock of the legal trade in live wildlife and potential risks to human health. Global Ecology and Conservation 17, e00515.

Downie, J.R. 2021. Environmental enrichment and welfare in captive reptiles. Natterchat 23, 6-9.

Harrington, L.A. et al. 2021. Live wild animal exports to supply the exotic pet trade: a case study from Togo using publicly available social media data. Conservation Science and Practice 3, e340.

Lambert, H.S. et al. 2019. Given the cold shoulder: a review of the scientific literature for evidence of reptile sentience. Animals 9, 821.

Macdonald, D.W. et al. 2021. Trading animal lives: ten tricky issues on the road to protecting commodified wild animals. Bioscience 71, 846-860.

Marshall, B.M. et al. 2020. Thousands of reptile species threatened by under-regulated global trade. Nature Communications 11, 4738.

Stringham, O.C. et al. 2021. A guide to using the internet to monitor and quantify the wildlife trade. Conservation Biology 35, 1130-1139.

Sung, Y-H. et al. 2021, Prevalence of illegal turtle trade on social media and implications for wildlife trade monitoring. Biological Conservation 261, 109245.

Tapley, B. et al. 2011. Dynamics of the trade in reptiles and amphibians within the UK over a ten year period. Herpetological Journal 21, 27-34.

Thomas-Walters, D. et al. 2021. Motivation for the use and consumption of wildlife products. Conservation Biology 35, 483.

Vamberger, M. et al. 2020. Already too late? Massive trade in Indian star tortoises might have wiped out its phylogenetic differentiation. Amphibia-Reptilia 41, 133-138.

Warwick, C. (on-line). Review: ‘Good practice guidelines for the welfare of privately kept reptiles and amphibians (2015).

Williams, D. and Jackson, R. 2016. Availability of information on reptile health and welfare from stores selling reptiles. Open Journal of Veterinary Medicine 6, 59-67.

Wyatt, T. et al. 2022. The welfare of wildlife : an interdisciplinary analysis of harm in the legal and illegal wildlife trades and possible ways forward. Crime, Law and Social Change 77, 69-89.

The Ecological Importance of Small Freshwater Bodies and Riparian Habitats

May 9, 2022 by Kathy Wormald

Summary
Small Freshwater Bodies include ponds, lochans, ditches, springs, seepages and flushes. All of these
provide huge ecological benefits, supporting a wide range of aquatic species and offsetting some of the
negative impacts of many environmental issues facing us such as climate change, flooding, chemical and
noise pollution. Riparian habitats are the terrestrial sites in close proximity to the freshwater habitats and
provide critical habitats for insects, amphibians and other wildlife, and make valuable contributions to our
natural capital.

What are they?
Ponds support an extraordinary two thirds of all freshwater species including Common frog, Common
toad, Teal, Pond mud snail, Tadpole shrimp, Northern damselfly, Broad-leaved pondweed, Great Crested
Newt, Grass snake, Pillwort, and Medicinal leech. Ponds are also used by a wide range of other wildlife
as a source of drinking water including hedgehogs and birds.

One third of ponds are thought to have disappeared in the last fifty years or so and of those that remain
more than 80% are considered to be in ‘poor’ or ‘very poor’ condition (Freshwater Habitat Trust). This
has had an enormous impact on aquatic wildlife.

Creating clean new ponds is one of the simplest and most effective ways to protect freshwater wildlife.
Where it is not a viable option to create new ponds, restoring existing depleted ponds is greatly
beneficial.

Ditches are man-made waterbodies that are used mainly to drain the land. They are distinguished from
streams in that they are usually straight and follow linear field boundaries; they show little relationship
with natural landscape contours. There are over half a million kilometres of ditches in the British
landscape. They are found in a wide range of habitat types from lowlands to hills and can have as much
biodiversity as some of our best rivers. In addition, they often support temporary water specialists which
are often not found in other freshwater habitats.

As ditches drain land, what lives in them is dependent on how polluted they are, on their gradient and
how often they flow. Unpolluted, high quality ditches are in the minority, with perhaps only 10% of the
UK ditches qualifying (Freshwater Habitat Trust).

Springs are places where underground water emerges at the surface. They may turn into tiny seepages
and become flushes, or they may be the beginning of substantial water courses. They are found all over
the country in all landscapes and are dominated by small animals and plants such as mosses and
liverworts, cold water flatworms, caddis flies and the larvae of two-winged flies. Many of these species
are found very close to the start of springs and seepages. If the spring is permanent it may also be used
by fish.

Seepages and flushes are areas where water from underground flows out onto the surface to create an
area of saturated ground. Flushes vary from open, stony ground with sparse plant cover to dense cover
of flowering plants, usually sedges or rushes, with mosses and liverworts forming a ground layer under
the canopy. They are found all over the country and support a wide variety of wetland plants,
invertebrates and other uncommon smaller wildlife.

The ecological benefits of riparian areas are huge. They provide habitat for many species such as water
vole and create habitat corridors by linking fragmented and isolated habitats through which species can
migrate. They are also a great food source for many species, particularly invertebrates.

Why are they important?
Small freshwater and riparian habitats are biodiversity hotspots, collectively acting as small ecosystems
and supporting a massive range of wildlife species.

They are also remarkably good carbon sinks. Carbon sinks are reservoirs that absorb and store
atmospheric carbon through physical and biological processes. Ponds in particular are more active in
nearly all of these processes than larger lakes, marine ecosystems and terrestrial ecosystems (Downing,
2010). Small ponds sequester 79-247g of organic carbon per square metre annually, a rate 20-30 times
higher than woodlands, grasslands and other habitat types (Taylor et al., 2019). Céréghino et al., (2014)
suggested that some 500m² ponds may even be capable of sequestering up to 1000kg of carbon per
year. Although ponds take up only 0.0006% of land area in the UK, a tiny proportion compared to the
36% of grasslands (Carey et al., 2008), their high rates of carbon burial suggest that their overall
contribution is significant.

Biological processes carried out by aquatic vegetation are pivotal in carbon sequestration.
Photosynthesis contributes to the sequestration of carbon dioxide by turning it into oxygen and
biomass. One kilogram of algae uses an average of 1.87 kilograms of carbon dioxide a day (Anguselvi et
al., 2019). Algae in ponds also contribute to reducing additional greenhouse gases such as nitrous oxide
(N2O). Nitrogen is a key component in chlorophyll and thus used in farm fertiliser. Excess nitrogen could
react with oxygen in the air to become N2O. The presence of algae in farm ponds to capture this excess
can prevent this reaction from occurring and limit emission of greenhouse gas. A study found that two
thirds of farm ponds act as N2O sinks (Webb et al., 2019), making them an important contributor to
combating climate change, particularly as N2O traps heat at 300 times the rate of CO2.

Freshwater habitats and soft ground act as flood defences and with flood incidence increasing they can
make a huge contribution to offsetting the environmental and social damage that is caused by flooding.

Finally Freshwater habitats absorb noise and can offset noise pollution in highly populated noisy urban
environments.

What needs to happen?
We need to accelerate the implementation of both strategic and specific actions to manage small
freshwater bodies in ways that reduce freshwater pollution and improve water quality. We need an
ongoing funded programme to undertake restoration works on existing smaller freshwater bodies.
This needs to be a rolling programme to avoid the current trend of small freshwater body succession at
such a late stage that restoration is no longer an option and the body becomes defunct for biodiversity
benefits. In order to address the estimated 50% loss in small freshwater bodies we need investment to
create new smaller freshwater bodies.

These interventions will both support nature’s recovery, and help the freshwater environment become
more resilient to the impacts of climate change. Nature-based solutions to climate change are
increasingly recognised as an essential approach to water management and we must restore smaller
freshwater bodies in ways that promote ecosystem processes. Restoring and creating new smaller
freshwater bodies is a key nature-based solution to climate change, with the scope to lock up carbon,
benefit biodiversity and enhance human well-being. However, nature-based solutions are not yet
sufficiently incorporated into strategic and project plans.

Next steps for the Scottish Parliament:
With the scrutiny of the Scottish Government’s proposals for the fourth National Planning Framework
(NPF4) currently underway by parliament, there are a number of areas where the protections and
regulations relating to freshwater bodies could be improved. LINK members urge MSPs to consider the
following measures:

● Seize the opportunity to align nature-based solutions to flood management with NPF4,
Scottish Planning Policy and the Land Use Strategy. The ‘mainstreaming’ of nature-based
solutions across government policies is a key step in tackling the climate and nature
emergencies.
● Focus on the restoration of natural processes as the most sustainable footing for biodiversity
recovery. Such habitats must also include smaller water bodies including ponds, ditches, springs
and wetlands. Both cost and technical feasibility have limited action in these waters to date; to
counter this, natural ecosystem function should underpin a ‘no-regrets’ approach to restoration.
● Preference must be given to schemes which utilise nature-based solutions/natural flood
management wherever possible. It will not always be possible to adapt to climate change and
the pressure to implement hard engineering solutions in order to attempt to do so must be
resisted; we must instead think in terms of mitigating the impacts of a changing climate and
select solutions which work with nature. Working with natural processes is now more readily
considered but there remain questions that concern some stakeholders, such as around long-term maintenance, liabilities and so on, which would benefit from resolution.
● As our understanding of such techniques grows, findings must be widely communicated
amongst stakeholders, particularly to Local Authorities, to ensure that all involved in Flood Risk
Management are able to draw upon techniques that work with natural processes in the widest
sense.
● Small water bodies must be given the same priority as other important habitats, given their
important contribution to Scotland’s environment, wildlife and tourism sectors.
● Connectivity is a key attribute required for healthy, functioning ecosystems. Habitat restoration
and creation, planned and prioritised through a spatially mapped national Nature Network in
NPF4. Informed by local knowledge, this could be used to enhance connectivity, as well as by
considering the quality of connected habitats. Mapping of priority wetland habitats would also
identify existing areas of good-quality habitat as well as opportunities for restoration and allow
the identification of areas where habitat restoration or re-creation will be valuable to support
biodiversity delivery.
● Habitat restoration and creation should be funded by a combination of sources including
Water Framework Directive, Scottish Rural Development Programme payments, the Nature
Restoration Fund from government, Flood Risk Management funding, Scottish Water
investment programme and other sources. Together, this spatial planning and framework
integration can deliver the “urgent step change in effort” that the biodiversity crisis demands.
● Improving joint working, including via the sharing of information so that stakeholders are
clearer on the contributions that they could make to improving the state of estuarine and
coastal waters by undertaking work further up the catchment.Funding criteria for catchment based projects should include an assessment of whether they have incorporated actions which will contribute to improvements.
● Finally, it is important to monitor our progress towards addressing loss of our smaller freshwater
bodies. A target should be developed, and progress towards meeting that target should be
reported on a regular basis as part of the Scottish Government’s Environment Strategy.

Where property development is essential due diligence must be awarded to existing freshwater bodies.
These bodies are crucial habitats for many species such as amphibians and invertebrates. With much
smaller ranges than some other species, they are unable to travel a great distance to populate new
habitats. Associated infrastructure, such as roads, railways and cycle tracks need to take into account
species migration routes. Mortality of wildlife in the country as a result of habitats being fragmented by
infrastructure is a huge issue. Species such as toads, which use hereditary migration routes, can suffer
huge mortality rates crossing roads.

Can frogs, salamanders and lizards show us the way to limb regeneration?

April 26, 2022 by Roger Downie

Roger Downie

Froglife and University of Glasgow

Limb loss in humans is a very significant source of disability and distress. One estimate is that in the USA alone, 3.6 million people will be affected by 2050, as a result of war and other traumatic injuries, or after diabetes-related amputation (Ziegler-Graham et al. 2008). There are two possible routes to the treatment of these losses. Until recently, the most hopeful way forward was advances in prosthetic limb development, related to robotic and micro-electronic engineering progress. Encouraging regeneration of the lost limb seemed less likely, despite many years of research. This is because organ regeneration in mammals is extremely limited in nature. However, recent work based at Tufts University in the USA, using the African clawed frog Xenopus laevis, suggests that limb regeneration in mammals could be stimulated with the right interventions (Murugan et al. 2022).

The ability to repair tissue damage is very widespread in the animal kingdom. In ourselves, the most obvious example is wound healing, with a complex sequence of events following an injury: local cessation of blood flow; blood clotting and formation of a scab to prevent entry of micro-organisms; mobilisation of surrounding cells to close the wound; tissue remodelling below the skin to tidy up the damage, sometimes involving formation of scar tissue. However, some animals have the capacity to replace complete and functional organs if they are lost. In amphibians and reptiles, this capability has an odd distribution.

Some species of lizards show autotomy, the deliberate loss of part or all of the tail in response to predator attack (autotomy also happens elsewhere in the animal kingdom: starfish, stick insects etc.). In these lizards, muscles in the tail on the body side contract, severing a line of weakness built into the vertebrae, and the predator is left with the twitching end of the tail, while the rest of the lizard escapes. The tail stump then heals, and the tail regenerates, but not as before. The regenerate is mis-shapen and its skeletal core is a stiff rod of tissue, rather than a set of vertebrae. If the lizard is attacked again, autotomy can only occur in the part of the tail containing the original structures. The costs and benefits of tail autotomy in lizards are finely balanced, and this ability has been lost and evolved many times in different lineages (Clause and Capaldi 2006). Where the tail is important in balance, as in fast-running species, or in social signalling, as a sign of quality as in Uta species (Fox 1998), autotomy tends to be rare or does not occur at all. Cooper et al. (2004) showed that selection related to predation pressure could influence the occurrence of autotomy in different populations of a single lizard species.

In newts and salamanders, adults can regenerate a range of complex organs: parts of the eye, brain, and heart, as well as limbs and tail. This does not involve autotomy, and unlike the case of lizard tails, regeneration results in the re-formation of a normal, functional limb or tail. Limb regeneration follows an orderly sequence: closing of the wound is followed by the formation of a ‘blastema’- a mass of tissue with the characteristics of tissue at the distal end of an embryonic developing limb. Somehow, the blastema ‘knows’ how much of the limb has been lost, and it reforms only the missing elements in order, from proximal to distal ends. As the process progresses, nerves grow into the regenerate, and these provide signalling molecules essential for full regeneration. The ability to regenerate limbs is somewhat variable between species, with larger species and individuals generally having less regenerative capacity than smaller ones (Joven et al. 2019).

In frogs and toads, regeneration of larval tails and early-stage limb buds occurs, but limb regeneration in adults hardly at all. In some families (pipids, discoglossids, hyperoliids), a blastema forms and a partial regenerate grows from the stump, a bit like the regenerated tails of lizards, but it never approaches the size and complexity of the original limb. In bufonids and ranids, wound healing occurs, but no regeneration at all (Scadding 1981). Mammals are like adult amphibians, with no limb regeneration at all.

This is where the new results from Murugan et al. are revelatory. After some years of technique development, they now report substantial hindlimb regeneration in experimentally-amputated Xenopus laevis adults ( X. laevis has a long history as a laboratory species for biological research following its early 20^th Century use in human pregnancy testing). The method involves applying a temporary ‘collar’ (called a ‘Biodome’) to the limb stump following amputation. The collar is made of silicone and silk fibres, impregnated with a solution containing a mix of five molecules known to act as signals during normal limb development (such as growth hormone and retinoic acid). It therefore provides a moist environment for the stump tissue, including limb development molecules that would not normally be present there in damaged adult Xenopus limbs. The collars were left in place for only 24 hours, then removed, and the frogs then followed for 18 months to assess how well the amputated limbs regenerated. After decades of failure in such experiments, the results were spectacular.

The regenerates formed went well beyond the mis-shapen spikes usually formed by Xenopus stumps. There was long-term growth, including formation of bones and other normal tissues, neuromuscular repair so that the limbs could move, and the formation of digit-like projections at the distal ends: the animals were able to use their repaired limbs for more or less normal movements. Murugan et al. comment that while regeneration was not perfect in their experiment, the set-up provides considerable scope for alteration of the details: the mix and concentration of the signalling molecules, the duration of their application; also, the possible addition of electrical stimulation, which has shown some positive effects in other experiments. The authors are hopeful that, if regeneration can be stimulated in Xenopus, similar methods may work for mammals, including humans.

The occurrence and distribution of organ regeneration has long intrigued biologists (Bely 2010). For example, why should complete regeneration occur in newt and salamander adults, but not at all in frogs and toads? One theory concerns the period of impairment while the limb is regenerating, which can take months. Newt locomotion can remain effective in the absence of a functional limb (in many species, the limbs are greatly reduced and even absent in some), whereas the absence of a frog hindlimb for some months would be disastrous. The argument from this is that limb regeneration in frogs would be too slow to be effective, and therefore that it does not occur. This argument can be extended to mammals: the high demand for food in warm-blooded animals means that a period of immobility while a limb regenerates would not be useful (Elder 1979). Most discussion of limb regeneration assumes that the benefit follows limb loss after predation, as in lizards, but there are very few studies investigating the ecological role of regeneration in newts and salamanders.

Finally, a comment on ethics. Those opposed to any animal experimentation will not approve of Murugan et al.’s studies. Those with a more utilitarian outlook, will hope that the discomfort and death of a hundred or so Xenopus will lead eventually to new treatments that could benefit millions of people (and even some other animals). Those who prioritise animal welfare will study the conditions under which the Xenopus lived and look to see that the experimental protocols minimised any pain and discomfort. However, there is another ethical aspect: on behalf of Tufts University, where the experiments have been done, patents for the methodology have been applied for. I find it distressing that scientists should seek to make profit from advances in medical research, especially when it has been publicly funded. The notion that, in the future, victims of war should have to pay a royalty to Tufts so that their limbs can be repaired, is distasteful. But then we are all used these days to noticing that some companies have done very well financially out of the Covid pandemic.

References

Bely, A.E. 2010. Evolution of animal regeneration: re-emergence of a field. Trends in Ecology and Evolution 25, 161-170.

Clause, A.R. and Capaldi, E.A. 2006. Caudal autotomy and regeneration in lizards. Journal of Experimental Zoology 305A, 965-973.

Cooper, W.E. et al. 2004. Ease and effectiveness of costly autotomy vary with predation intensity among lizard populations. Journal of Zoology 262, 243-255.

Elder, D. 1979. Why is regeneration capacity restricted in higher organisms? Journal of Theoretical Biology 81, 563-568.

Joven, A. et al. 2019. Model systems for regeneration: salamanders. Development 146, dev167700.

Murugan, N.J. et al. 2022. Acute multidrug delivery via a wearable bioreactor facilitates long-term limb regeneration and functional recovery in adult Xenopus laevis. Science Advances 8 (4).

Scadding, S.R. 1981. Limb regeneration in adult amphibia. Canadian Journal of Zoology 59, 34-46.

Ziegler-Graham et al. 2008. Estimating the prevalence of limb loss in the United States, 2005-2050. Archives of Physical Medicine and Rehabilitation 89, 422-429.

Croaking Science: The benefits of green spaces and nature on mental health

March 29, 2022 by Briony Nesbitt

“In every walk with nature, one receives far more than he seeks” – John Muir

As well as the conservation work Froglife does for amphibians and reptiles across the UK, we also run projects that promote education amenities and research activities for the benefit of the public. We run wildlife projects for disadvantaged young people and those with dementia, such as our Green Pathways, Green Pathways for Life and Leaping forward for Dementia projects. A common issue amongst our participants is mental health, especially coming out the other side of the COVID-19 pandemic. Our Eco therapy style project is based on scientific research that suggests being outdoors and connecting with nature, have hugely positive effects on individuals.

As countries become increasingly urbanised, the world’s population is spending increasingly less time exposed to natural environments (Cox et al, 2018). It has been reported that 55% of the world’s population live in urban areas and this is expected to increase to 68% by 2050 (United Nations, 2018). Unfortunately, urbanisation not only means spending less time in natural environments but more time destroying them and reducing the number of green spaces around the globe (Collins, 2014). Aside from the detrimental environmental effects of this, loss of these green spaces and time spent in them could have hugely negative effects on people’s mental health and well-being.

There is growing evidence to suggest that being in nature has positive effects on people’s mental health. Studies have shown that green spaces can lower levels of stress (Wells et al, 2003) and reduce rates of depression and anxiety, reduce cortisol levels (Park et al, 2010) and improve general well-being. Not only can a simple walk in nature boost your mood but also improve your cognitive function and memory (Berman et al, 2012). Green spaces can provide a buffer against the negative health impacts of stressful life events. A Dutch study showed that residents with a higher area of green spaces within a 3km radius had a better relationship with stressful life events (Van den Berg et al, 2010) which was soon to be increasingly important in recent years with the effects of COVID-19.

So what is it about natural environments that are good for mental health and wellbeing?

Positive Physiological effects

Something as simple as exposure to natural environments can be physiologically restorative (Conniff et al, 2014). This means that being in a natural outdoor environment can have positive mental health effects due to the physical processes elicited in the body. A Japanese study showed that viewing and walking in forest environments can promote lower concentrations of cortisol, lower pulse rates and blood pressure when compared to city environments (Park et al, 2010). These physiological effects are all a counter to the physical effects stress causes in the body and are what happens when you relax. A recent study found that those who had access to natural spaces during the COVID-19 lockdowns had lower levels of stress and those that could view nature from home had reduced psychological distress (Ribeiro et al, 2021).

There are multiple psychological theories as to how nature helps our mental well-being. The two common prevailing theories on how nature brings about these positive effects are the Stress Reduction Theory (SRT) coined by Ulrich (1981) and Kaplan et al’s (1989) Attention Restoration Theory (ART). SRT suggests that nature promotes recovery from stress and that urban environments have the opposite effect. Ulrich proposes that being in unthreatening natural environments (a green space you would consider safe) activates a positive emotional response. That being in nature produces this as a universal innate connection, promoting the physiological effects of lower blood pressure, heart rate and increases attention which in turn blocks negative thoughts and emotions (Ulrich et al, 1991). Kaplan et al’s ART works around the idea that we have different types of attention: voluntary or involuntary, and that the latter requires no effort. After using voluntary attention we experience ‘attention fatigue’, reducing our cognitive abilities and increasing mental fatigue. According to Kaplan et al, when we use our involuntary attention it gives us time to restore our voluntary attention. From this, Kaplan et al have suggested that what nature provides acts as a restorative power by providing four processes:

Being away – an opportunity to distance from routine activities and thoughts.
Soft fascination – nature holds attention effortlessly: think about the sunsets, sound of water, leaves blowing in the wind all-natural phenomena allowing your voluntary attention to rest.
Extent – nature provides an immersion experience, engaging the mind and rest from concerns.
Compatibility – a setting that is well matched to human needs and desires, providing a feeling of being in harmony with a greater whole.

These two theories have much in common: they focus on cognitive vs autonomic processes and both support a change in attention and stress load when an individual interacts with the natural environment (Gregory N. Bratman, 2012). However, they differ in how they suggest the primary mechanisms work. The effects the theories suggest are blurred in the sense of cause and effect: does a reduction in stress levels allow someone to concentrate better or does replenished direct attention help reduce stress?

Both these assertions are controversial in the field of environmental psychology, yet much research falls under either both or one of these theories.

Mental Health and Nature Policy

To what degree these theories influence policy is debated but it is clear that in recent years, especially after the recent pandemic, that nature spaces are becoming an increasing priority for mental health provision. Research has evidenced that we need to shift our attention from focusing on people visiting green spaces to how we interact and connect with nature close to home through simple activities (Mental Health Foundation, 2021). The Mental Health Foundation suggests from their research findings that we need to focus on six main areas in policy:

Facilitating connection with nature
Protecting the natural environment and restoring biodiversity
Improving access to nature
Making green spaces safe for all
Using the planning system and urban design to improve the visibility of nature in every local area
Developing a life – long relationship with nature.

Through our projects at Froglife we provide ways for people to interact with the environment instead of simply just being in it.

Promotion of Physical activity

Green spaces such as nature reserves, wilderness environments and urban parks also promote certain behaviours, such as encouraging physical activity within the space, which is a pro-mental health behaviour. Experimental studies have shown that not only do green spaces promote experience but they may be better for mental health than activity in other environments. Those that perform exercise in natural environments once a week are at about half the risk of poor mental health as those that don’t (Mitchell, 2013). Participation and involvement in nature is often tied to physical activities such as gardening or farming, trekking or running: the evidence of the benefits of this promotes the idea that green spaces should be seen as an essential health resource (Pretty, 2004).

There are many more benefits associated with natural green spaces. However, in terms of mental well-being, greener areas have been associated with a sustained improvement in mental health, highlighting the significance of green spaces, especially in urban areas. They provide not only a habitat for wildlife but also sustainable public health benefits (Alcock et al, 2014). Many studies have shown that more time spent in nature is associated with better mental health, independent of culture and climatic contexts, as well as the promotion of physical activity.

In addition to the wildlife and environmental benefits of conserving nature spaces, especially in urban areas, we also benefit in many ways from these natural spaces. This gives us even more reason to continue to protect our wildlife and conserve our natural areas and green space.

References

Alcock, I, et al., 2014. Longitudinal Effects on Mental Health of Moving to Greener and Less Green Urban Areas. Environmental Science & Technology , 48, 1247-1255.

Berman, M.G, et al., 2012. Interacting with nature improves cognition and affect for individuals with depression. Journal of Affective Disorders, 140, 300-305.

Bratman, M.G, et al., 2012. The impacts of nature experience on human cognitive function and mental health. Annals of the New York Academy of Sciences (Issue: The Year in Ecology and Conservation Biology), 1249, 118-136.

Collins, A.M., 2014. Destruction of urban green spaces: A problem beyond urbanization in Kumasi city (Ghana). American Joural of Environmental Protection, 3, 1-9.

Conniff, A, et al., 2016. A methodological approach to understanding the wellbeing and restorative benefits associated with greenspace. Urban Forestry & Urban Greening, 19, 103-109

Cox, D.T.C, et al., 2018. The impact of urbanisation on nature dose and the implications for human health. Landscape and Urban Planning, 179, 72-82.

Kaplan, R, et al., 1989. The Experience of Nature: A Psychological Perspective. New York: Cambridge University Press.

Mental Health Foundation, 2021. Nature- How Connecting with nature benefits our mental health. Published on-line.

Mitchell, R., 2013. Is physical activity in natural environments better for mental health than physical activity in other environments? Social Science & Medicine, 91, 130-134.

Park, B.J, et al., 2010. The physiological effects of Shinrin-yoku (taking in the forest atmosphere or forest bathing): evidence from field experiments in 24 forests across Japan. Environmental Health and Preventative Medicine, 15, 18-26.

Pretty, P. J., 2004. How nature contributes to mental and physical health. Spirituality and Health International, 5, 68-78.

Ribeiro, A.I, et al., 2021. Exposure to nature and mental health outcomes during COVID-19 lockdown. A comparison between Portugal and Spain. Environment International, 154 article 106664.

Ulrich, R. S., 1981. Natural Versus Urban Scenes: Some Psychophysiological Effects. Environment and Behavior 13, 523-556.

Ulrich, R. S., et al., 1991. Stress recovery during exposure to natural and urban environments. Journal of Environmental Psychology, 11, 201-230.

Van den Berg, A. E, et al., 2010. Green space as a buffer between stressful life events and health. Social Science & Medicine, 70, 1203-1210.

Wells, N.M. & Evans, G.W., 2003. Nearby Nature: A Buffer of Life Stress among Rural Children. Environment and Behavior, 35, 311-330.

Croaking Science

Footer

Contact us