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Croaking Science: Alternative strategies for amphibians – neoteny and overwintering

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Written by Dr Andrew Smart, Head of Science and Research at Froglife

People often wonder why they occasionally find tadpoles in their ponds over the winter.  This is an example of delayed metamorphosis, which can be advantageous to some individuals, particularly in northern latitudes. In newts we find overwintering larvae and also examples of neoteny when the larval form is retained and, in some cases, mature and reproduce.

The classic case of neoteny in amphibians is the axolotl, which retain their feathery gills into adulthood, becoming enlarged larvae that develop reproductive organs and can produce large numbers of fertile eggs. Axolotls evolved to live in two lakes in Mexico where the water levels were stable and food levels high, enabling animals, lacking the thyroid hormone that triggers metamorphosis, to survive and evolve a life-strategy that was more effective than having a terrestrial stage.

The classic case of neoteny in amphibians is the axolotl, which retain their feathery gills into adulthood.

In frogs and toads, there are a range of reasons why tadpoles might be found in a pond in the winter months. The first to rule out is the risk of the invasive species Lithobates catesbeianus, the American bullfrog, which has a larval stage than can be anything from 1 to 4 years.  Overwintering of this large, predatory species has been found to have a neutral or negative impact on other amphibians in introduced populations in the USA[1]. Thankfully, the bullfrog appears to have been eradicated from the UK since 2015[2].

If you have other ‘normal sized’ tadpoles in your pond, the chances are that a number of things may have happened: in some northern latitudes, frog and toad tadpoles have been shown to adopt different strategies[3], with some animals metamorphosing early while others delay metamorphosis, remaining in the pond to be able to exploit resources early in the spring , outcompeting a new cohort of smaller tadpoles[4].  As well as food availability and temperature, other unknown factors lead to this strategy[5]. This enables them to produce larger metamorphosed froglets or toadlets which have a better chance of survival through the winter. 

So why don’t all anurans follow this strategy?  It can be high risk; extreme temperatures could kill animals during hibernation or ponds could dry out before the end of the late summer period and kill all the ‘delaying’ tadpoles.  Most Anurans have developmental cues that trigger metamorphosis, linked to the proximity of other tadpoles and to reduction in water level; [6] in the case of ‘drying ponds’ reducing water depth[7],[8] leads to faster metamorphosis and smaller froglets.

Anurans that develop into ‘large’ tadpoles do have the capacity to develop gonads but in the case of Xenopus (the African clawed toad) ‘giant tadpoles’ that occur develop gonads but struggle to release eggs and sperm[9] and in any case, a ‘giant tadpole’ would be an unlikely animal to participate in amplexus. A similar situation occurs in Pseudis paradoxa, the paradoxical frog, which has evolved a ‘giant tadpole’ that metamorphoses into an adult rather than a froglet.[10] The tadpoles have developed gonads that are close to maturity but the authors point out that life stages in Anurans are very different and that the opportunity for full neoteny is unlikely because of the need for behavioural changes to enable successful reproduction.

African Clawed Frog - Xenopus laevis
In the case of Xenopus (the African clawed toad) ‘giant tadpoles’ that occur develop gonads but struggle to release eggs and sperm.

What about Caudata? There is evidence that some individuals, usually young adults, may move into ponds in the autumn and overwinter[11].  Examples of palmate newts overwintering in ponds in Scotland are well recorded[12],[13], again a strategy to enable a more robust metamorph emerging in the summer to face colder winters. 

There are now several well recorded cases of neoteny in smooth newts – in a Norfolk swimming pool, numbers of neotenous newts were found, resembling female smooth newts but with feathery gills[14].  Two of these animals were  removed for examination and very quickly metamorphosed to adult newts.  The authors of the study suggested a number of possible outcomes suggesting that a change in water quality (increase in iodine) or change in water depth could have triggered the change.

Examples of delayed metamorphosis and also total neoteny have also been recorded at a site in Cambridgeshire, where newt larvae have been seen in large numbers in autumn and early spring, after presumably hibernating in the pond. One of the newts was taken to captivity and laid fertile eggs[15]. This animal did rise to the surface for air,  a behaviour not normally linked with neotenous newts, which have fully functioning gills. As in many cases of neoteny, the records were incidental and unable to be investigated in detail.

So overwintering tadpoles and newt larvae may be a way of amphibians having two different life strategies within a population, some animals taking the risk in the pond, some taking the risk overwintering as a smaller sized individual. Neotenous individuals may be taking advantage of a stable environment with significant food sources and low levels of competition as an alternative strategy, but to really investigate this further we need more information on the habitats where these animals are found.  If you know of a site with neotenous animals, please let us know by emailing: info@froglife.org

References

[1] Boone, M.D., Little, E.E. and Semlitsch, R.D., 2004. Overwintered bullfrog tadpoles negatively affect salamanders and anurans in native amphibian communities. Copeia, 2004(3), pp.683-690

[2] New strategy launched to protect biodiversity and economy from non-native species – GOV.UK (www.gov.uk)

[3] Tattersall, G.J. and Ultsch, G.R., 2008. Physiological ecology of aquatic overwintering in ranid frogs. Biological Reviews, 83(2), pp.119-140.

[4] McNeill, D.C. and Downie, J.R., 2017. Overwintering of smooth and palmate newt larvae in the Gartcosh Nature Reserve, Scotland. The Glasgow Naturalist, 26.

[5] Walsh, P.T., Downie, J.R. and Monaghan, P., 2008. Larval over‐wintering: plasticity in the timing of life‐history events in the common frog. Journal of Zoology, 276(4), pp.394-401..

[6] Walsh, P.T., Downie, J.R. and Monaghan, P., 2008. Larval over‐wintering: plasticity in the timing of life‐history events in the common frog. Journal of Zoology, 276(4), pp.394-401.

[7] Merilä, J., Laurila, A., Pahkala, M., Räsänen, K. and Timenes Laugen, A., 2000. Adaptive phenotypic plasticity in timing of metamorphosis in the common frog Rana temporaria. Ecoscience, 7(1), pp.18-24.

[8] Laurila, A. and Kujasalo, J., 1999. Habitat duration, predation risk and phenotypic plasticity in common frog (Rana temporaria) tadpoles. Journal of Animal Ecology, 68(6), pp.1123-1132.

[9] Rot-Nikcevic, I. and Wassersug, R.J., 2004. Arrested development in Xenopus laevis tadpoles: how size constrains metamorphosis. Journal of Experimental Biology, 207(12), pp.2133-2145.

[10] Downie, J.R., Sams, K. and Walsh, P.T., 2009. The paradoxical frog Pseudis paradoxa: larval anatomical characteristics, including gonadal maturation. The Herpetological Journal, 19(1), pp.1-10.

[11] Beebee, T. & Griffiths, R. , 2000, Amphibians and Reptiles: A Natural History of the British Herpetofauna: Book 87 (Collins New Naturalist Library), Harper Collins, London

[12] McNeill, D.C. and Downie, J.R., 2017. Overwintering of smooth and palmate newt larvae in the Gartcosh Nature Reserve, Scotland. The Glasgow Naturalist, 26.

[13] Walker, G., Fairclough, B. and Paterson, E., 2019. Winter presence of adult male palmate newts (Lissotriton helveticus) in a pond in Scotland. Herpetological Bulletin, 149, pp.24-27.

[14] Allain, S.J. and Phillips, N., 2023. Observations of a neotenous population of Smooth NewtsLissotriton vulgaris from Norfolk. Trans. Norfolk Norwich Nat. Soc, 56(1).

[15] Leeke, C. 1990, An occurrence of neotenous sooth newts (Triturus vulgaris) in Cambridgeshire. Bulletin of the British Herpetological Society 31,

What our animals are doing this month…

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Late spring or early summer is a good time to be on the lookout for tadpoles! You might spot common frog or common toad tadpoles or, if you are lucky and on the coast, you might even spot natterjack toad tadpoles!

You might have spotted a few tadpoles already as frogs can lay their frogspawn as early as January and it can take two to four weeks for tadpoles to hatch out. As the tadpoles grow, they become faintly speckled with gold/brown and will slowly grow back and front legs!

Common toads breed a little later than common frogs, laying double strings of spawn and wrapping it carefully around vegetation. Again, it will take two to four weeks for the tadpoles to hatch out. To tell the difference between frog and toad tadpoles, you simply have to look at their colour. Toad tadpoles remain jet black and can also form shoals so can be easier to spot.

Common frog tadpoles
Common toad spawn
Natterjack toad spawn. Credit: Matt Wilson

 

The natterjack toad is confined to just a handful of sites on the coast in the UK and is only found on the Solway Coast in Scotland. Breeding for natterjack toads takes place in March/April but can continue into the early summer. So, depending on the natterjacks in your area, you may see males waiting by the pond edge (making loud rasping noises to attract the females), natterjack toad spawn or even some tadpoles!  Natterjack toad spawn is laid in single strings with their tadpoles being smaller than common toad tadpoles and sporting a grey spot on their throat.

Always remember to record your amphibian and reptile sightings on our FREE Dragon Finder app. All of the data collected is sent to the National Biodiversity Network Atlas. You can download the app here.

#StopSpawnSales- What you can do to help

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Froglife run our annual #StopSpawnSales social media campaign during March to tackle the illegal practice of selling wild-caught amphibian spawn and tadpoles online. 

As most of us are aware, we are now in the peak of amphibian breeding season as our species are laying their eggs in ponds and pools across the country. This time of year also sees an unfortunate sharp rise in sales of wild-caught amphibian spawn (and even tadpoles) on online selling sites. 

One of the biggest reasons for people buying spawn/tadpoles online is to stock their ponds at home. However, if there is no spawn or tadpoles in your garden pond, then there is a good reason for this. Either your pond hasn’t had time to establish or the pond/ surrounding environment is unsuitable and this could result in the bought spawn failing or the tadpoles that develop from it to die. 

Another reason for people buying spawn/ tadpoles is to use them as an educational tool and watch them develop at home. We aren’t party poopers! We know how fascinating it can be to take spawn home, watch it grow and release the tadpoles/froglets back into the wild, but we want people to do this legally and safely! Not only is there a massive risk of spreading amphibian disease and viruses, invasive plants and invertebrates, but the sale of wild-caught spawn or tadpoles is an offence under The Wildlife and Countryside Act 1981. 

What you can do to #StopSpawnSales:

  • Never buy wild-caught spawn/tadpoles online! If you decide to raise frogspawn, it is crucial that all tadpoles/froglets/toadlets are released to the ponds where they were found to prevent spreading disease and invasive species
  • If you see wild-caught spawn/tadpoles for sale on social media or online marketplaces, please report it to the marketplace itself in the first instance
  • If further action is needed (i.e the posts aren’t taken down), please report it to your local Police’s Wildlife Crime Officer (with screen shots of the advert if possible)
  • Spread the word! like and share our social media posts and encourage those around you to #StopSpawnSales
Photo Credit: David Palmer

Further resources:

FSC Guide to Keeping Common Frog Tadpoles

Amphibian FAQs

Information on UK Amphibians

Just Add Water guide (a guide for creating wildlife ponds)

Wildlife at Home (guides on how to make your gardens more wildlife friendly) 

#pawsagainstponds Campaign

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During April, we will be running our #pawsagainstponds campaign! Britain is a nation of dog lovers, there are over 12 million in the UK and here at Froglife we love our furry friends, in fact many of our staff and volunteers are dog owners themselves. However, dogs swimming in ponds can have negative impacts on wildlife and we want to focus on reducing this and raising awareness of the issue.

Keeping dogs out of ponds used by amphibians for breeding is important for three reasons:

  • Dogs swimming and paddling in ponds can stir up sediment, blocking out valuable sunlight for aquatic plants and spawn/tadpole development.
  • Trampling spawn, tadpoles and froglets/toadlets
  • Spot-on flea treatments can have a devastating impact on aquatic ecosystems. If dogs go into ponds shortly after treatment, the powerful pesticides can kill the insect life within the pond. You can find further information on the British Veterinary Association’s webpage here. 

There can also be negative impacts on dogs including:

  • Illness and risk of death from blue-green algae. Please read the British Veterinary Association’s article on the subject (with advice on what you can do to prevent your dog from becoming ill) here
  • Injuries from hidden hazards below the water
  • Infections from existing cuts and injuries or ones sustained whilst in the water  

If you see a pond that is well planted and appears to be a designated wildlife habitat, try to keep your dogs away or even better, on a lead, particularly in spring when amphibians will be breeding and in the summer when young amphibians will be leaving their ponds for terrestrial habitats.

Ziggy being a very good girl!

What alternatives are there?

We still want dogs to enjoy water, but we want to keep wildlife as well as the dogs themselves safe when doing so. There are some brilliant alternatives to swimming in wild water including:

  • ‘Dog swim days’ You can check outdoor pools in your area to see if they provide this service. There are some great suggestions here. 
  • Head for the beach! Remember to check if dogs are allowed on your chosen beach before travelling
  • Sourcing an old paddling pool or sandpit and making a doggy pool in the comfort of your own garden
  • Play with sprinklers- hook one up to your hosepipe and watch your dog enjoy it- you could even join in with them! (be aware of local hosepipe bans in the summer months before doing this)
  • Give them an outdoor bath- if you’ve been on a walk and your doggo is a bit dusty/dirty you can bathe them in the garden. Make it fun by adding their favourite toys and don’t forget a nice treat for afterwards

 What you can do to help the #pawsagainstponds campaign:

  • When walking your dog near wild water, please keep them on a lead
  • Use alternatives to swimming in wild water (mentioned above)
  • When building a wildlife pond, consider creating natural fencing (hedges, willow fencing) to prevent your dog from taking a swim. More info here
  • Spread the word! Please share our social media posts and tell your family and friends about the campaign

Further reading:

Here are some useful articles on dogs in ponds

 

The astonishing diversity of reproductive modes in amphibians: a new classification

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Written by Roger Downie, Froglife Trustee and University of Glasgow

In the UK, we are accustomed to amphibians breeding in the spring and depositing their eggs in freshwater bodies, usually ponds rather than streams or lakes. Frogs deposit their eggs as a clump of jelly; toads as strings; and newts wrap theirs individually in folded leaves. The embryos hatch as larvae and feed in the water until they are ready to metamorphose into juvenile versions of the adult form. The adults spend no time with their eggs after deposition. So far, so familiar. But, when we look beyond our UK species, we find a wide diversity of reproductive modes. How many, and what are they like?

The term ‘reproductive mode’ (RM) was coined by Breder and Rosen (1966) to help them make sense of reproductive diversity in fish. Later, Salthe and Duellman (1973), in the context of amphibians, defined RM as a set of characters including oviposition site, ovum and clutch characteristics, rate and duration of development, stage and size of hatchlings, and type of parental care, if any. Without using the term RM, Boulenger (1886) had identified 10 amphibian modes. A hundred years later, Duellman and Trueb’s (1986) textbook recognised 29 RMs in anurans, seven in urodeles and two in caecilians. Haddad and Prado (2005) extended this to 39 modes for all amphibians, and there have been a few additions since. However, Nunes-de-Almeida et al. (2021) have now published a new classification, identifying 74 RMs in amphibians, almost a doubling of the 2005 list. How and why?

Their method is to divide the reproductive process into a set of eleven characters where each species can be assigned to one of two (occasionally more) states. The characters are:

  1. Reproduction type: oviparity (egg-laying) or viviparity (eggs not laid: the female gives birth to larvae or juveniles). Viviparity is common in caecilians, but also occurs in a few frogs and salamanders.
  2. Oviposition macrohabitat: eggs are deposited into the environment or they develop in or on the body of either the female or the male parent.
  3. Spawning type: the distinction here is between cases where eggs are immersed in froth, or not. Froth is made from oviduct secretions in two ways: either a foam is generated by beating movements of the adults’ limbs; or bubbles are made by the female’s jumping movements.
  4. Oviposition substrate: either in water, or not in water: on the ground, or in vegetation, or attached to a parent.
  5. Medium surrounding the eggs: the main distinction here is between two kinds of aquatic habitat: lentic (still water, like a pond) or lotic (flowing waters, such as streams). The medium can also be air, as in eggs deposited on the ground, or attached to a parent’s body.
  6. Nest construction: a constructed nest is defined as a place to deposit eggs which the parents have made by digging, or cleaning, or building in some way. ‘Froth’ nests are excluded from this category (I’m not sure this exclusion is fully justified). Constructed nests can be burrows, or depressions, or cleared areas on the forest floor, or leaves folded around the eggs.
  7. Oviposition microhabitat: here, Nunes-de Almeida and colleagues find 15 variables: eggs on the surface of water, at the bottom of a pool, on the ground, on a leaf, on a rock, in a bromeliad tank etc.

The remaining characters distinguish different patterns of development:

  1. Embryonic development: can be indirect, with a larval stage, or direct – lacking a distinct larval form, and progressing directly from embryo to juvenile.
  2. Embryonic nutrition: all amphibians have yolky eggs, and the yolk provides the nutrients needed for embryonic development, but in some cases the mother provides additional nutrients. Where all nutrients derive from the yolk, development is termed lecithotrophic; where the mother provides extra, it is matrotrophic.
  3. Larval and newborn nutrition: when embryos hatch and become free-living, we consider them as larvae. Generally, this marks the stage when they begin to forage for food, although they still have some of the egg-yolk left. However, some species do not feed as larvae, but obtain their nutrition from their large remaining yolk reserves: these are termed endotrophic. Most larvae are exotrophic, obtaining most of their nutrition from external food sources. In a few cases, parents provide this nutrition. For example, so-called trophic eggs, unfertilised eggs deposited by females to feed their hatched larvae. Another example is the feeding of some caecilian young on their mother’s skin secretions.
  4. Place of larval development: mostly this occurs either in a pool (lentic) or a stream (lotic), but there are also cases of larval development on land, or attached to a parent’s body.
Credit: Julia Page

Overall, the authors reviewed RMs in 2171 species on which they could find adequate information: this is 26 % of all amphibians (8393 species, November 2021). Anurans showed 71 of the 74 RMs; urodeles 16 and caecilians seven. Most species showed a single RM, but some fitted up to four of the modes.

Nunes-de-Almeida and colleagues have made a valiant effort to classify the rich diversity of amphibian RMs, but it is not without some problematic aspects. One omitted feature is fertilisation mode: internal or external. This is a crucial feature in research on reproductive strategies relating to certainty of paternity and male competition. Another aspect largely omitted is parental care behaviour. Parental care can be defined as non-gametic investments in offspring that incur a cost to the parent, but which provide a benefit to the offspring. Parental care in amphibians is discussed in Croaking Science (date to come). The new RM classification  explicitly excludes parental care on the grounds that parental care information is lacking for too many species. However, many kinds of parental care are actually included: for example, the provision of trophic eggs to larvae (character 10 above); while others such as larval transportation by adults are omitted. Another omitted feature which I find surprising is the differences in anuran spawn characteristics: single non-adhesive eggs, eggs in clumps, eggs in strings. It is likely that these differences are evolved characteristics important to reproductive success, so should be included in a classification of RMs. Another omission is the diversity of larval forms: there is huge diversity in tadpole form and behaviour, related to the habitats they live in: this may go beyond the usual definition of an RM, but is an important aspect of reproductive success. There are also occasional inconsistencies: phyllomedusine tree frogs wrap their egg clutches in leaves, and this is classed as a constructed nest (character 6 above); newts wrap their eggs individually in leaves, but this behaviour is not acknowledged as a kind of nest construction.

One excellent point made by the authors is about plasticity: i.e. individuals within a species may vary their RM, depending on circumstances. One example I’ve observed is the giant tree frog Boana boans. These frogs generally construct nests, as basins in gravel or sand (character 6 above), just beyond the edge of streams. However, where there is no suitable ‘beach’, the eggs are deposited at the water surface amongst emergent vegetation.

I’m sure that this new RM classification will stimulate discussion and research, and that later versions will include more species and modes. The authors hope that their work will stimulate the development of RM classifications for other taxa: how about reptiles?

References

Breder and Rosen (1966). Modes of Reproduction in Fishes. Natural History Press, New York.

Duellman and Trueb (1986). Biology of Amphibians. Johns Hopkins University Press, Maryland.

Haddad and Prado (2005). Reproductive modes in frogs and their unexpected diversity in the Atlantic forest of Brazil. Bioscience 55, 207-217.

Nunes-de-Almeida et al. (2021). A revised classification of the amphibian reproductive modes. Salamandra 57, 413-427.

Salthe and Duellman (1973). Quantitative constraints associated with reproductive modes in anurans. Pp 229-249 in: Vial (ed.) Evolutionary biology of the anurans. University of Missouri Press, Columbia.

Parental care in amphibians: research findings from 1705 to the present day

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Writen by Roger Downie, University of Glasgow and Froglife

Croaking Science does not usually urge its readers to study a particular scientific paper, but this is an exception. The paper is Schulte et al.’s (2020) review of research into amphibian parental care, a fascinating and essential read for all amphibian enthusiasts. Parental care is usually defined as ‘non-gametic investments in offspring that incur a cost to the parent’ and which provide some benefit to the offspring. Common examples are egg-guarding, and provisioning of young after hatching. Although some authors restrict discussions of parental care to actions that occur after fertilisation, others include activities like nest-building in preparation for egg laying. For example, we generally consider UK amphibians as lacking parental care: they deposit their eggs in water, then leave. But Schulte et al include the behaviour of female newts that wrap their eggs individually in leaves: this behaviour takes a substantial amount of time, so is costly to the female, and contributes to offspring survival by reducing predation.

Research into parental care tends to focus disproportionately on birds and mammals. Stahlschmidt (2011) in a review of what he termed ‘taxonomic chauvinisn’ found amphibian and reptile parental care much less studied than cases from birds, mammals and even fish. Schulte at al. redress this situation through a vast historically-based review, identifying 685 studies spanning the period 1705-2017. Early studies were mainly simply descriptive, but since 1950, there has been a greater focus on the investigation of explanations: what does parental care achieve, and what does it cost?

The paper’s Table 1 lists each of the parental care modes so far described: four in Caecilians; eight in Urodeles; 28 in Anurans. Some modes occur in all three Orders e.g. terrestrial egg guarding; others occur in only one Order e.g. wrapping of individual eggs in leaves by newts; foam-nest construction by many frogs. Overall, parental care is known from 56 (74%) of the amphibian Families. It is not really surprising that more parental care modes occur in the Anurans than in the other two Orders, since anuran species diversity is so high (Frost, 2021 lists 7406 anurans, 768 urodeles and 212 caecilians).

The first known report of parental care in an amphibian, remarkably, was by a German female natural historian and artist, Maria Sibylla Merian in 1705. Her book was mainly devoted to meticulous drawings of the insects she observed in Suriname, but she also included an illustration and observations on an aquatic frog, later named the Suriname toad (Pipa pipa), which incubates its eggs in individual pockets on its back: she saw the metamorphosed juveniles emerging from the pockets. I was lucky, on my first visit to Trinidad, to see this for myself. We captured a ‘pregnant’ female and the babies later hatched into the water, some still with tail stumps, others fully metamorphosed. Female biologists have been prominent in the study of amphibian parental care: in addition to Maria Sibylla Merian, Martha Crump (1996) and Bertha Lutz (1947) come to mind, as well as the four authors of the review under discussion.

Suriname Toad

Among the 500 or so papers that Schulte et al. cite, I was pleased to see two from the work we have done in Trinidad (Downie et al., 2001; Downie et al., 2005). These are about the Trinidad stream frog Mannophryne trinitatis (see Croaking Science September 2020), where the fathers guard the eggs on land then transport hatchlings on their backs to a pool where they can complete development to metamorphosis. Tadpole transportation is a common aspect of parental care in the neotropical families Dendrobatidae and Aromobatidae. We found that the fathers are choosy over where to deposit their tadpoles, avoiding pools that contain potential predators, and therefore contributing to their survival. The search could take up to four days. We wondered how costly this might be to fathers: to our surprise, transporting a relatively heavy load of tadpoles did not appear to reduce the fathers’ jumping ability, nor did it prevent them from finding food. However, four days away from their territory must count as at least some cost in terms of lost mating opportunities.

A male Trinidad stream frog, Mannophryne trinitatis transporting his tadpoles (photo credit: Joanna Smith)

Schulte et al. conclude with a timely plea for a revival of teaching and research in natural history. As they say, natural history observations – on the distribution, numbers and habits of organisms- form the basis of all new ideas and hypotheses in ecology and evolutionary biology. They note that there remain many amphibian species whose habits are poorly known and that many novel observations have been made on parental care in recent years. They therefore expect that much could be discovered, as long as effort is put into new field work. Over 20 years ago, I wrote lamenting the modern status of natural history (Downie 1997, 1999), and Schulte et al. report that the loss of organism-based teaching and research is widespread. In the UK, there are moves to create a natural history curriculum, to complement biology in schools. I feel that it is much needed.

References

Crump (1996). Parental care among the amphibia. Advances in the Study of Behaviour 25, 109-144.

Downie (1997). Are the naturalists dying off? The Glasgow Naturalist 23 (2), 1.

Downie (1999). What is natural history, and what is its role? The Glasgow Naturalist 23 (4), 1.

Downie et al. (2001). Selection of tadpole deposition sites by male Trinidadian stream frogs (Mannophryne trinitatis; Dendrobatidae): an example of anti-predator behaviour. Herpetological Journal 11, 91-100.

Downie et al. (2005). Are there costs to extended larval transport in the Trinidadian stream frog (Mannophryne trinitatis, Dendrobatidae)? Journal of Natural History 39, 2023-2034.

Frost (2021). Amphibian species of the world : an online reference. Version 6.1 (accessed 29/9/21). Electronic database accessible at http://amphibiansoftheworld.amnh.org/index.php. American Museum of Natural History, New York, USA.

Lutz (1947). Trends towards non-aquatic and direct development in frogs. Copeia 1947, 242-252.

Schulte et al. (2020). Developments in amphibian parental care research: history, present advances, and future perspectives. Herpetological Monographs 34, 71-97.

Stahlschmidt (2011). Taxonomic chauvinism revisited: insight from parental care research. PLoS ONE 6, e24192.