Figure 2. UK distribution of the Harvest mouse (https://data.nbn.org.uk/imt/#4-

33.320,45.600,26.710,62.503!091ELC)

Nicola snow: 13111472 28/11/2014

The Role Played By Chester Zoo in the Captive Breeding and Reintroduction of the Harvest Mouse (Micromys Minutus)

Ecology & Distribution

Weighing only six grams, the harvest mouse (Micromys minutus) is the smallest mouse in Europe (Plate 1). Brown in colour, the harvest mouse can grow between 50 to 70 millimetres in length with an additional 50 to 60 millimetres just for its prehensile tail which acts as a fifth limb to provide stability when negotiating the heads of cereal crops (Leach 1990). Their diet consists primarily of grain, cereal and berries though it is supplemented with insects and young grasses (Gibson et al 2010). Harvest mice are predominantly nocturnal though they become more active in daylight hours in the winter months when food is scarce. Populations are under

increasing threat of decline due to predation by domestic cats, greater exposer to birds of prey and sudden frost (Leach1990). Typically the harvest mouse has a low average life expectancy of six months.

The harvest mouse has a historical distribution across most of Europe and some parts of Asia. Within the UK the distribution is restricted to southern England with small populations in

Chester and Yorkshire and a few fragmented populations recorded in Wales and some regions of Scotland (Figure 2) (Harris 1979). Historically, the harvest mouse was abundant within crop fields and lowland woodland with population peaks during the height of summer when food supply was plentiful (McDonald & Tattersall 2001). However, due to habitat loss and fragmentation as a result of the intensification of agriculture, the species is now largely recorded in wetlands, long grasses and hedgerows bordering crop fields (Wildlife Trust & Severn Trent Water 2010)(Wildwood Trust 2006). According to the Wildwood Trust (2006) UK population estimates are 1,425,000 with 10,000 individuals in Wales and 1,415,000 within England.

Species Status

The Harvest mouse is currently categorised as “least concern” by the IUCN (Aplin et al 2008). Taxa categorised in this way are not considered to be under any immediate threat of extinction. This means that the threat of extinction for the Harvest mouse is low, which is due to the species abundance across the globe.

Plate 1. Micromys minutus (http://www.arkive.org/harvest-mouse/micromys-minutus/ )

Nicola snow: 13111472 28/11/2014

Across Europe and most parts of Asia the Harvest mouse is common in rice fields and other wetlands, as well as any agricultural fields that aren’t maintained regularly. Currently there are no major recorded threats to its global distribution. However within the UK, decline in population size has been recorded in localised regions where loss or degradation of wetland has been observed (Macdonald & Tattersall 2003: Flowerdew 2004).

A population can be established and even thrive provided a habitat contains some quantity of long grass and wetland (Gibson 2010). As the Harvest mouse is very adaptable across a range of habitats, variation in range has been recorded throughout the globe, whilst populations within regions of Asia common amongst bamboo and rice paddies; populations within Western Europe are most common in alpine grassland, tall grass fields and the edge of humid forests (Råberg et al 2013). Throughout England, Harvest mice are most abundant within hedgerows or in landscapes where hedgerows feature as crop borders and boundaries.

Conservation

Decline of the Harvest mouse within the UK has been attributed to the increase in modern farming techniques and the advancement of agricultural technology (Toms et al 1999; Sargent 1997). In addition to this, changes in seasonal temperature and fluctuating crop yield due to the effects of increasingly turbulent weather, are impacting on the species breeding patterns which usually coincide with the abundance of cereal crops in summer (Tom et al 1999). The Harvest mouse typically nest within cereal fields, creating a nest from wheat and corn stems on the mid-area of the cereal shaft. However, due to the widespread use of agricultural machinery which limit time for escape during harvesting, the species has now adapted to dwell within the bordering hedgerows of large cereal fields to avoid nest destruction (Macdonald & Tattersall 2001). This adaptation has also led to further decline of the species due to aggressive hedgerow management. Population numbers of the Harvest mouse were found to decrease in density down to as low as 0.002 -0.76 animals per hectare in 2004 and 2006 across a number of sites in the Upper Thames tributaries region (Mammal trust UK 2007).

Conservation efforts include captive breeding and reintroduction in addition to crop margin management which involves the implantation of long grass margins along the parameter of crop fields. This provides shelter for the Harvest mouse during harvesting of the crops (Fischer & Schroder 2014).

Role of Chester zoo

Chester zoo has established a captive breeding and reintroduction programme since the 1980s in collaboration with the Cheshire Wildlife Trust; the zoo has bred the Harvest mice in controlled and monitored conditions to ensure the greatest birth rate. Litters are reared in captivity until they are between 3 and 12 months old where they are reintroduced into sites in the Cheshire countryside that have been specially selected to provide optimal habitat for the

Nicola snow: 13111472 28/11/2014

Harvest mice (Wildwood trust 2006). In 2003, 270 mice were released on land owned by Chester zoo at a sex ratio of 50:50,with a further twenty radio-tagged mice later being released (UK BARS 1999). These mice were then monitored periodically until 2006 to determine any population increase and overall success of the release.

Captive bred mice at Chester zoo are housed in a series of tanks containing small groups of two to four mice per tank. Each tank is filled with a layer of sawdust and a selection of nesting materials such as straw, leaf litter and other vegetation available to them in the wild. The mice fed on a mix of cereal, fruit and millet which is available to them throughout the day. The tanks are designed to mimic wild habitat whilst providing optimal conditions for breeding. The mice will not mate unless some degree of competition has taken place to establish a dominant female and male. Due to this, initially each tank contains four individuals which are monitored until a dominant pair has been established and conceived their first litter. Once the dominant pair is established the submissive pair is removed allowing for the remaining pair to nest without further competition for up to seven litters. Beyond seven litters the risk of death during birth increases significantly (Wildwood trust 2006).

Following the release of captive bred mice, radio tagged mice are monitored and any population increase is recorded as well as the general health and fitness of the population. Overall captive bred mice released by Chester zoo successfully integrated into wild communities with a limited number of individuals lost to predation or sickness. However minimal information is available as to the success of Chester zoo’s captive breeding programme; but continued monitoring of the released individuals over a four year period indicated that they were still present throughout the release sites but had dispersed significantly into surrounding habitats (UK BARS 1999).

Based on the methods used by Chester zoo for captive breeding and the presence of reintroduced individuals within the release sites four years after the first reintroduction; the programme can be evaluated as a success. The environmental enriched methods and breeding management effectively produced a captive population not only capable of integrating with the wild community, but thriving over generations within the release site. This is extremely crucial to the re-establishment of a stable Harvest Mouse population as it demonstrates that decline in wild populations can be offset by the release of captive bred individuals.

Nicola snow: 13111472 28/11/2014

The Role Played By Chester Zoo in the Captive Breeding and Reintroduction of the Mountain Chicken Frog (Leptodactylus Fallax)

Ecology and distribution

Leptodactylus fallax also known as the Mountain Chicken Frog due to its apparent chicken like flavour when eaten, is the world’s largest frog species and can grow up to twenty one centimetres in length. Individuals appear Brownish-orange in colour with either dark stripes or spots across its body. They have distinctive cloudy eyes commonly red in colour (Plate 3) (Kaiser 1994). The species diet consists of crickets and other insects as well as small vertebrates and crustaceans. They have also been known to eat other frogs and small mammals (Martin et al 2007). As with most other frogs the Mountain chicken also reproduces by spawning tadpoles, however their offspring are not reared in water and instead develop terrestrially in underground burrows (Gibson & Buley 2001).

The Mountain Chicken Frog has a limited global distribution and currently only natively occurs in regions of Dominica and Montserrat (Fa et al 2010). Historically the Mountain Chicken Frog was present throughout many of the western islands of Caribbean including Guadeloupe, Martinique, St Kitts and Nevis. However, due to rapid decline in population numbers the Mountain Chicken Frog now only occurs on two small island in the East Caribbean; Montserrat and Dominica (Plate 4) (Kaiser 1995). Though exact figures are not known it is estimated that numbers could be as low as 8,000 animals in the wild with only eight breeding pairs and 44 individuals currently recorded; with the species as a whole under great threat of extinction (Tapley et al 2014). The species range is greatly limited by its requirements for reproduction and its habitat preference. The species occurs in dense vegetation within or in proximity to flooded regions such as forests and gullies regularly exposed to floodwaters. As the species is nocturnal, individuals spend most of their time burrowed underground in leaf litter and soil (Daltry 1999). Soil type preference is a key factor in the restriction of the species range as soil requirements need to allow for borrowing and nesting (Gibson & Buley 2001). The Mountain Chicken Frog is in captivity in many zoos throughout the globe. These zoos are taking part in captive breeding programmes in an attempt to improve population numbers and prevent its extinction (Tapley et al 2001). This species can be found in captivity in zoos throughout Europe, America and Africa, with some zoos actively involved in its protection, research and conservation within its native environment of Dominica. The zoological Society of London, Parken Zoo (Sweden) and the North of England Zoological Society (Chester Zoo) are all partners with the “saving the Mountain chicken” campaign which is based in Dominica (Mountain chicken project 2007).

Plate 2. Leptodactylus fallaxhttp://www.arkive.org/mountain-chicken/leptodactylus-fallax/

Nicola snow: 13111472 28/11/2014

Plate 3. Distribution map of The Mountain Chicken Frog across the Caribbean (http://maps.iucnredlist.org/map.html?id=57125 )

IUCN status

According to the IUCN red list, the Mountain Chicken Frog’s global threat status is currently set at critically endangered (Fa et al 2010). The IUCN determines “critically endangered” as “… considered to be facing an extremely high risk of extinction in the wild” (IUCN 2012). This means that due to the species limited distribution and increasing rate of decline, extinction in the wild is impending unless measures are taken to protect, conserve and recover the species population numbers.

Conservation

Historically the Mountain Chicken, as the name implies, was a food source to the inhabitants of Dominica and Montserrat with between 8,000 and 36,000 individuals hunted annually (Schwartz & Henderson 1991; Malhotra et al 2007). Though hunting of the species reduced population numbers, in 2002 the population crashed. Originally, the cause of such a dramatic decline in species abundance was unclear and attributed to threats such as the brown rat (Atkinson & Atkinson 2000), increased hunting due to tourism, habitat loss due to agriculture and natural disasters such as cyclones and volcanic activity (Fisher et al 2009). However, though these threats are current and persistent it was determined by the London Zoological Society that such a significant decline in population numbers was due to an outbreak of a fungal disease known as Chytridiomycosis which affects the frog’s keratin deposits within its skin, inhibiting its ability to hydrate, breathe, osmoregulate and thermoregulate this ultimately results in a 100% mortality rate of any infected individuals (Garcia et al 2009).

Current conservation efforts include global captive breeding programmes and outreach programmes designed to research alternative methods of aiding the species recovery as well as educating local government organisations to better manage and protect this threatened species. Most notably the London Zoological Society has established a captive breeding facility and conservation reserve within Dominica in partnership with the Commonwealth of Dominica and the government of Montserrat (Martin et al 2007).

Nicola snow: 13111472 28/11/2014

Role of Chester Zoo

A number of zoos throughout the world are involved in captive breeding programmes in an attempt to help establish a so-called “safety net” population. In July 2014, the London Zoological Society and Durrell Trust successfully returned a number of individuals to the wild. Fifty-one captive bred Mountain Chicken Frogs were transported to the National Botanical Gardens in Montserrat where they were housed overnight and then later soft released with the aid of tents back into the wild. The London zoological Society and Durrell Trust have now implemented a twenty year action plan to monitor and treat all reintroduced individuals to ensure maximum survival as well as further the research and understanding into the spread of the Chytridiomycosis fungus (Durrell Trust 2008).

The Durrell Trust, London zoological Society and Chester zoo established a cooperative captive breeding programme for the Mountain Chicken Frog and outlined species management guidelines. These guidelines identify key species requirements for captive management to enable optimal breeding conditions as well as regulating exposure to the Chytridiomycosis fungus. Chester zoo, in accordance with the guidelines, photo ID all individuals keeping a catalogue of all unique markings in addition to micro-chipping via the lymph sacs beneath the frog skin. Environmental conditions of the frogs housing is monitored strictly ensuring that temperature is regulated between 24 to 28°C during the day and 19 to 13°C during the night. The temperature is also alternated to mimic natural temperature fluctuations in the wild such as seasonal temperature change. Environmental enrichment is considered right down to the frog’s substrate preference, ensuring that adults and juveniles have a good mixture of soil, bark chippings and leaf litter to maintain adequate humidity within the enclosure. Breeding is encouraged between the frogs during the month of May through to July by introduction of a female into a male’s enclosure to promote pairing and subsequently burrowing. Once the burrow is established, the pair will mate for up to 10 hours during which a foam nest is created and up to 50 small eggs are deposited. After 7 to 10 days the eggs hatch and the female frog will remain with the clutch for 6 to 8 weeks. Once the larva are 150 mm in length they will absorb their tail and leave the burrow. Chester zoo then continue to feed the clutch 4 to 5 times per week until they have reached adequate size for removal into independent enclosures. From this stage the zoo then perform health checks to establish if individuals are free from the Chytridiomycosis fungus. Once a sufficient number of individuals (usually 50 to 80) have been produced in captivity, they are transferred to the release facility in Montserrat (Durrell Trust 2001). Individuals released from the Montserrat facility are a mix of captive bred frogs from a number of different zoos participating in the captive breeding programme and regulated by the same species management guidelines. Not only does this increase the number of individuals released into the wild, it too increases genetic diversity amongst the re-established population; ensuring reduced inbreeding and consequently strengthening resilience to potentially devastating stochastic events.

Nicola snow: 13111472 28/11/2014

References

Aplin, K., Lunde, D., Batsaikhan, N., Kryštufek, B., Meinig, H. & Henttonen, H. (2008). Micromys minutus. The IUCN Red List of Threatened Species. Version 2014.3. www.iucnredlist.org. Downloaded on 07 January 2015

Atkinson, I., Atkinson, T. (2000). Land vertebrates as invasive species on islands served by the South Pa‐ cific Regional Environment Programme. Invasive Species in the Pacific: A Technical Review and Draft Regional Strategy. South Pacific Regional Environment Programme, Samoa

Daltry, J.C. 1999. Unpublished report to Montserrat Forestry and Environment Division on 1995 survey of reptiles and amphibians on Montserrat. Fauna and Flora International

Durrell Trust. (2001) Species management guidelines: Mountain Chicken Leptodactylus fallax. Durrell Wildlife Trust, Jersey zoo

Durrell Trust. (2008) Addressing a Threat to Caribbean Amphibians: Capacity Building in Dominica International Training Workshop on Prevention of Chytrid Spread and Early Surveillance Measures. Holy Redeemer Retreat House, Eggleston, Dominica

Fa, J., Hedges, B., Ibéné, B., Breuil, M., Powell, R., Magin, C. (2010). Leptodactylus fallax. The IUCN Red List of Threatened Species. Version 2014.3. www.iucnredlist.org. Visited on 08/02/2015

Fischer, C. & Schoder, B. (2014). Predicting spatial and temporal habitat use of rodents in a highly intensive agricultural area. Agriculture, ecosystems and environment, vol 189: 145-153

Fisher, M., Garner, T., & Walker, S. (2009). Global emergence of emergence of Batrachochytrium dendrobatidis and amphibian chytridiomycosis in space, time and host. Annual review of Microbiology vol 63: 291-310

Flowerdew, J. (2004) Advances in the conservation of British mammals, 1954–2004: 50 years of progress in the mammal society. Mammal review Vol 34: 169-210

Garcia, G., Lopez, J., Fa, J., Gray, G. (2009). Chytrid fungus strikes mountain chickens in Montserrat. Oryx vol 43, 323-328

Gibson, C., Elphick, J., Hume, R., Woodward, J., Dennis-Brian, K., MacKay, A., Pellant, C., Sterry, P., McGavin, G., Coombes, A., Fletcher, N., Burnie, D., Pellant, H., Pitt, J., Evans, S., Kibby, G. (2010) wildlife of Britain: RSPB pocket nature. Dorling Kindersley Ltd. Penguin company. London

Gibson, R. & Buley, K. (2001). A new mode of endotrophic reproduction in frogs ‐ evolutionary pioneering by mountain chickens. Fourth World Congress of Herpetology, Bentota, Sri Lanka.

Nicola snow: 13111472 28/11/2014

Harris, S. (1979). History, distribution, status and habitat requirements of the harvest mouse (Micromys minutus) in Britain. Mammal review. Vol 9: 159-171

IUCN. (2012). IUCN Red List Categories and Criteria: Version 3.1. Second edition.Gland, Switzerland and Cambridge, UK: IUCN

Kaiser, H. (1994). Leptodactylus fallax Catalogue of Amphibians and Reptiles. Society for the Study of Amphibians and Reptiles, vol 583:1-583

Kaiser, H. (1995) Abiotic disturbances in the Lesser Antilles. Froglog. vol 15: 1‐2Leach, M. (1990). Mice of the British Isles. Shire Natural History. Shire Publications Ltd, Aylesbury

Macdonald, D. & Tattersall, F. (2001). Britain’s Mammals: The Challenge forConservation, Mammals Trust UK

Macdonald, D. & Tattersall, F. (2003) The State of Britain’s Mammals 2003. People’s Trust for Endangered Species, London

Malhotra, A., Thorpe, R.S., Hypolite, E. & James, R. (2007). A report on the status of the herpetofauna of the Commonwealth of Dominica. Applied Herpetology vol 4: 177 - 194

Mammal Trust UK (2007). The state of Britain’s mammals 2007. WildCRU: university of Oxford

Martin, L., Morton, M., Hilton, G., Young, R., Garcia, G., Cunningham, A., James, A., Gray, G., Mendes, S. (eds) (2007). A Species Action Plan for the Montserrat mountain chicken Leptodactylus fallax. Depart‐ ment of Environment, Montserrat.

Mountain chicken project (2007) project communication stratergy. Project 18018, Montserrat

Råberg, L., Loman, J., Hellgren, O., Kooji, J., Isaksen, K., Solheim, R. (2013) The origin of Swedish and Norwegian populations of the Eurasian harvest mouse (Micromys minutus). Acta Theriologica, Vol 58: 101-104

Sargent, G. (1997) Harvest mouse in trouble. Mammal News, vol 1: 111

Schwartz, A., Henderson, W. (1991). Amphibians and Reptiles of the West Indies: Descriptions, Distributions and Natural History. The University of Florida Press, Florida

Tapley, B., Harding, L., Sultan, M., Durand, S., Burton, M., Spencer, J., Thomas, R., Douglas, T., Andre, J., Winston, R., George, M., Gaworek-michalczeniai, M., Hudson, M., Blackman, A., Dale, J., Cunningham, A.(2014) an overview of current efforts to conserve the critically endangered mountain chicken Leptodactylus fallax on Dominica. The herpetological bulletin, vol 128:9-11

Toms, M., Siriwardena, G., Greenwood, J. (1999) Developing a mammal monitoring programme for the UK. British trust for Ornithology, Vol 223

Nicola snow: 13111472 28/11/2014

UK Biodiversity Action Reporting System (1999) Monitor confirmed harvest mouse sites and captive breeding programme release sites. http://ukbars.defra.gov.uk/project/show/15497 visited on 07/02/2015

Wildlife Trust & Severn Trent Water. (2010). Water for wildlife: restoration and protection of wetland wildlife. Derbyshire wildlife trust. Peoples trust for endangered species. Derbyshire

Wildwood Trust. (2006). Captive breeding and reintroduction: the harvest mouse Micromys minutus. Wildwood trust. Kent