SPECIES PROFILE Black-handed Spider Monkey Ateles geoffroyi Photo: Image from Primate Info Net http://pin.primate.wisc.edu/factsheets/image/190 September 2014 Author: Mary Charrett BSc Last Updated: October 2014 1. Summary The black-handed spider monkey (Ateles geoffroyi) is a native to the Central America countries of Mexico, Belize, Colombia, Costa Rica, El Salvador, Guatemala, Honduras, Nicaragua and Panama (Hagell et al. 2013, IUCN 2008). While it is kept as a pet in some North American areas there are no established populations outside its native territory. Due to their intelligence it has been noted that a few zoos have had spider monkey escapes. All of these escapees were recaptured, most quite quickly. Ateles geoffroyi is a widespread Neotropical New World monkey with highly plastic socioecological pattern (Hagell et al. 2013). The likelihood of A. geoffroyi establishing in Tasmania is minimal, the CLIMATCH data which compares the native environs to the import region shows that the regions are not similar, A. geoffroyi would have trouble over wintering in Tasmania. Black-handed spider monkeys would have trouble finding enough nourishment in our drier environment as well as not having the tall well established trees they use to brachiate from food source to food source. Spider monkeys spend very limited time on the ground. Should the species establish in Tasmanian there would be concern from fruit farmers. Ateles geoffroyi has seven subspecies each with its own International Union for Conservation of Nature (IUCN) Red List and Convention on International Trade in Exotic Species (CITES) listing. The IUCN listing vary from Vulnerable to Critically Endangered and the CITES listing is on both Appendix I and II (CITES 2014, IUCN 2008). Tasmanians should be able to experience black-handed spider monkeys, it is a species most Tasmanian would not have to opportunity to experience in the wild and with many subspecies of Ateles geoffroyi being listed by the IUCN as critically endangered we can help the species by educating people about the problems black-handed spider monkeys face in the wild. pg. 2 2. Name and Taxonomy 2.1 Scientific Classification Kingdom: Animalia Phylum: Chordata Class: Mammalia Order: Primates Family: Atelidae Genus: Ateles Species: A. geoffroyi 2.2 Common Names Geoffroyi’s spider monkey, Mono Colorado, Black-handed spider monkey, Central American spider monkey, Atèles De Geoffroyi (French), Mico (Spanish) and Mono Araña (Spanish) (IUCN 2008). 2.3 Sub-species There is much confusion about the classification regarding the species Ateles geoffroyi. It has been stated by the International Union for the Conservation of Nature (IUCN, 2008) that the taxonomy of this species must be revised. Subspecies have been distinguished solely by pelagic colouration and facial pigmentation and hybridization has occurred in captivity (Rossan & Baerg 1977). There has been seven classified subspecies of A. geoffroyi (IUCN 2008), these include: A. geoffroyi azurensis, the Azuero spider monkey is isolated to the forested mountains of the Azuero peninsula in Ponuga. 112-116 individuals. A. geoffroyi frontatus, the Black-browed spider monkey or Red bellied spider monkey located in north-west Costa Rica and far north and west Nicaragua. 110-160 individuals. A. geoffroyi geoffroyi, the Nicaraguan spider monkey or Geoffroyi’s spider monkey is found in the coastal regions around San Juan del Norte or Martina Bay in southeast Nicaragua and possibly into Costa Rica. A. geoffroyi ornatus, the Ornate spider monkey lives in forested areas of Panama, east of the Canal Zone to central western Costa Rica. Introduced to Barro Colorado Island. Ateles geoffroyi panamensis is thought to be a junior synonym for A. geoffroyi ornatus. pg. 3 A. geoffroyi vellerosus, the Mexican spider monkeys range is the forests of Veracruz and eastern San Luis Potosí, south east through Tobasco to the highlands of Guatemala, El Salvador and Honduras. A. geoffroyi yucatanensis, the Yucatan spider monkey is found in the forests of the Yucatan peninsula, north east Guatemala, Belize and Southern Mexico. A. geoffroyi grisescens, the Hooded spider monkey, found in Panama, the authenticity of this species has been called into question, it is thought that it most likely does not exist. 2.4 Taxonomy Ateles geoffroyi is a New World Primate in the family Atelidae alongside howler monkeys, woolly spider monkeys and woolly monkeys. They are grouped as howlers and prehensile tailed monkeys, there are 24 species included in this group. Atelidae monkeys range from Mexico in Central America to Argentina in Southern America. They are characterised by their long limbs, fingers and tails which are adapted for their highly arboreal lifestyle. They have elongated limbs and are the largest New World Monkeys (EOL 2012). 3. Description Black-handed spider monkeys have no marked sexual diamorphism, the female even has a pendulous clitorus which can often be mistaken for a penis. Both sexes weigh from 6 – 9 kgs (IUCN 2008, Valero 2004). Body length measures from 305 – 630 mm and tail length is 635 – 840 mm long on average (EOL 2012). Juveniles are smaller than adults but are the same colouration and have the same skin pigmentation of the face. Infants spend most of their time being carried by mum and juveniles are independent commonly (White 1986). There is no seasonal variation. Ateles geoffroyi has colour vision polymorphism which is common in New World monkeys (Hiramatsu et al. 2005). Black-handed spider monkeys have established daily routines, they wake up around 7.30am peak foraging activity occurs at around 11.30am then they rest in the early afternoon and forage peaks again in the late afternoon arouns 5.30pm, they settle down for the night at 8pm/9pm. There is limited activity during the night (Campbell et al. 2005, Eisenberg 1976). pg. 4 Visual identification of black-handeed spider monkeys can be easily made by noting the black upper and lower limb extremities including the tail. Pelagic differences are common in subspecies but in general the fur of the body is light buff to reddish-brown in appearance and the face is hairless and unpigmented around the eyes and muzzle areas. Infants are usually completely black and as they age the colouration comes through (ARKive 2006). The name ‘ateles’ means imperfect, this is due the black-handed spider monkey not having a thumb. The thumb is greatly reduced due to evolution, this allows the monkeys to brachiate from tree to tree with great ease (ZAA n.d.). The black-handed spider monkey covers large areas of its habitat daily to get enough food, the diurnal frugivores more favoured mode of locomotion is brachiation but they can also quadrupedally and bipedally walk and run, climb, arm swing and leap (Campbell et al. 2005, Eisenberg 1976, Mittermeier & Fleagle 1976, Valero 2004). Their fully prehensile tail is often used to suspend the monkey from high branches, they get the name spider monkey from this pose, they use their tails 71% of the day on average (Covey 2005). The tail has a hairless rigged patch on one side of the tip, this is used for gripping (EOL 2012). Spider monkeys have a reduced thumb this makes brachiation easier and have a modified shoulder joint (Campbell et al. 2005, Valero 2004). Hybridization does occur in this species, viable progeny has been born from a pairing of a male A. geoffroyi panamensis and a female A. fuscieps robustus. The male offspring had a intermediate pegaic colouring. Other older spider monkeys have been found with this intermediate colouring thus concluding that hybridization is quite common in wild environs (Rossan & Baerg 1977). There are no similar looking species in Tasmania to the spider monkey. Being the largest of the New World monekys the can be easily distinguished from other monkeys around the world. pg. 5 4. Conservation and Legal Status 4.1 Conservation Status The seven subspecies of Ateles geoffroyi have been independently assessed by the IUCN. Species IUCN Listing CITES Appendix Country of origin A. g. ornatus Endangered II Costa Rica Critically Endangered II El Salvador, Guatemala, A. g. vellerosus Mexico, Belize, Honduras A. g. yucatanensis Endangered II Belize, Guatemala, Mexico A. g. azurensis Critically Endangered II Panama A. g. frontatus Vulnerable I Costa Rica, Nicaragua A. g. geoffroyi Critically Endangered II Costa Rica, Nicaragua A. g. grisescens Endangered 2000 (Data II Panama, Colombia deficient 2008) The IUCN listing was last reviewed in 2008 and the CITES listing was completed in 1975, Ateles geoffroyi frontatus is the only subspecies with an Appendix I listing, Appendix I is an animal threatened with extinction and import/export is only allowed in special circumstances. Appendix II, which covers all other A. geoffroyi subspecies, covers those not necessarily threatened with extinction, but trade must be controlled in order to avoid exploitation. Ateles geoffroyi has had a population decline of over 50% over 45 years or 3 generations (CITES 2014, IUCN 2008). It is thought that A. geoffroyi might be recovering from a bottleneck event but it has yet to be proved (Hagell et al. 2013). 4.2 Legal Status The Environment Protection and Biodiversity Conservation Act 1999 (the EPBC Act) provides the legal framework to protect and manage nationally and internationally important flora, fauna, ecological communities, and regulate the import and export of wildlife. Ateles geoffroyi is listed as a specimen ‘suitable for live import with an import permit’ issued under this Act, with the condition of import being ‘eligible non-commercial purposes only, excluding household pets’. Ateles geoffroyi is not listed as a species permitted for import into Tasmania under the Nature Conservation Act 2002 and supporting Wildlife (General) Regulations 2010. pg. 6 5. Life History The oldest living spider monkey was 52 years old when it died, generally they live between 40 to 50 years (Chapman & Chapman 1990). Spider monkeys have a low fecundity compared to other New World monkeys (Hagell et al. 2013). Black-handed spider monkeys have a gestational period of 7 – 7.5 months or 226 – 232 days (Chapman & Chapman 1990, Eisenberg 1976, IUCN 2008, RamosFernández & Wallace 2008, Turnock & Slater 2011), once they give birth the infants suckle from mum for at least 16 months and will start eating solids at 8 months, the infant can be dependent on its mother for up to 3 years. The time between births depends on length of lactation, if an infant is still born and the mother does not lactate the next birth may be in 8 - 11 months, if the mother does lactate it could be anywhere between 15 – 37 months, it seems that in captivity A. geoffroyi will reproduce quicker than in the wild (Chapman & Chapman 1990, Eisenberg 1976, IUCN 2008, RamosFernández & Wallace 2008, Turnock & Slater 2011). Ateles geoffroyi males and females do not reach sexual maturity until they are 4 – 7 years of age, when they do aggression in the monkeys heightens (IUCN, 2008, Ramos-Fernández & Wallace 2008, Turnock & Slater 2011). The female black-handed spider monkey has a cyclic uterine bleeding every 26 – 27 days which lasts for 3 – 4 days, during this time she will display a range of different postures towards the males in the group, there are few preliminaries in the build up to mating, the couple will simply move off into a secluded area (Eisenberg 1976, Muñoz-Delgado et al. 2004). Typically A. geoffroyi will only give birth to one offspring, the dominant female in the troop will give birth to either a son or daughter while the subordinate females will give birth to daughters only (MacIntosh n.d.). Alloparenting is displayed within this species, an infant, of one female may be offered to be suckled from another or may initiate a feeding from a non-parent but a non-parent will never just take an infant from the mother to feed, this starts from 7 – 10 weeks in age (Watt 1994). It has been found that in zoos the mortality rate of infants is around 25% and births are a year round event, in the wild there is no set season for birthing but generally more occur from April through to August (Chapman & Chapman 1990). It is known that in the Ateles genus hybridization does occur, it has not been found to hybridise with any other genus. The progeny of a male A. geoffroyi panamensis(ornatus) and a female A. fuscieps robustus spider monkey was found to be fertile and able to reporduce (Rossan & Baerg 1977). pg. 7 6. Habitat Requirements and Preferences Spider monkeys are primarily arboreal, they live in tropical evergreen, mangrove forest, lowland rainforest, and semi-evergreen forests. They live in undisturbed forests, they very rarely ever come to ground so they brachiate from tree to tree get around (IUCN, 2008, Turnock & Slater 2011, Valero 2004). At dusk subgroups congregate to make bigger groups at a sleeping site, a sleeping site is usually a tree that has been used before (81% of the time) they sleep on large branches, they do not create nests or sleep in hollows. Black-handed spider monkeys have high fidelity to home ranges, sleeping trees within the core habitat have a measurement of 75cm DBH (Diameter at breast height) as a minimum(Chapman 1989). The average monthly rainfall in black-handed spider monkey home ranges are about 153 mm and the average temperature in these tropical areas is 24°C (EOL 2012). The spider monkeys dependence on ripe fruit is a key limiting factor to available habitat and their arboreal lifestyle requires large areas of undisturbed forest (Ramos-Fernández & Wallace 2008). They occupy forests up to 3,000m in altitude (Hagell et al. 2013). 7. Natural Geographic Range Figure 1. Distribution of Ateles geoffroyi from southern Mexico to north-west Colombia. (Image source: http://maps.iucnredlist.org/map.html?id=2279) pg. 8 The habitat of the black-handed spider monkey is from southern Mexico through to Panama on both sides of the coast, the countries include: Belize, Colombia, Costa Rica, El Salvador, Guatemala, Honduras, Mexico, Nicaragua and Panama (Hagell et al. 2013, IUCN 2008,). The average home range of A. geoffroyi varies from different accounts but within 0.73 km² - 2.2 km² but this depends on the amount of monkeys in a troop (Valero 2004). The alternative method to calculate density of animals is individuals per km² and using this process we can get numbers as low as 2 individuals per km² and as high as 89 individuals per km² (Chaves & Stoner 2010, Fedigan & Baxter 1984, Ramos-Fernández & Wallace 2008, White 1986). As an example Chapman (1989) stated that there were 42 individuals in a home range of approximately 1.7 km² in Santa Rosa National Park, Costa Rica. Ateles geoffroyi has been introduced into the Barro Colorado Island research area. About half a century ago the area was flooded for the Panama Canal, the Smithsonian institution took control of one the newly isolated islands and set up a research facility. They released many animals into the area and A. geoffroyi was one. The release has been found successful due to the troop of monkeys reproducing and roaming the island freely (Eisenberg 1976). The home range of black-handed spider monkeys varies depending on the size of the troop, typically home ranges are from 0.73 – 1.7 km². Usually the density of animals is around 19 – 31 individuals per km² (Chapman 1989, White 1986). This species has occupied the same range throughout its history. 8. Introduced Geographic Range There is no noted releases of captive black-handed spider monkeys, there have been a few cases in the media of escapes, at such places like Dallas Zoo, Hogle Zoo, Chester Zoo and San Antonio wildlife reserve, but the cases noted have all resulted in recapture, usually by tranquilisation (Cabrero 2011, Chester Chronicle 2010, Monkey News 2010, WFAA 2011). pg. 9 9. Potential Distribution in Tasmania The Bureau of Rural Sciences (BRS 2011), Department of Agriculture, Fisheries and Forestry has developed a modelling system (CLIMATCH) so that a comparison can be made with a species native and introduced range and a specified area. In this instance we are comparing the native region of Ateles geoffroyi and Australia. Figure 2: Ateles geoffroyi source data for the CLIMATCH modelling. (Image Source - http://data.daff.gov.au:8080/Climatch/climatch.jsp) The source data in Figure 2 shows in red the data used to compare the two regions. The data in blue was not used. Figure 3 illustrates the degree of similarity between Ateles geoffroyi home range and Australia. The CLIMATCH output shows that northern parts of Australia are more comparable than southern Australia to A. geoffroyi’s home range. Tasmania’s range is from 0 – 4 thus a very low to medium comparability. This means that should A. geoffroyi escape from captivity it would struggle to establish a viable community. pg. 10 Figure 3: Ateles geoffroyi geographic distribution source data selected for CLIMATCH modelling. (Image Source: CLIMATCH - http://data.daff.gov.au:8080/Climatch/climatch.jsp) 10. Diet and Feeding Behaviour Black-handed spider monkeys are primarily generalist frugivores and secondarily folivores. Ripe fruit makes up 60 - 90% of their typical diet, leaves, flowers and young seeds make up the rest and they will sometimes eat live and decayed wood as a source of minerals such as sodium and calcium (Chaves et al. 2011, Graham et al. 2013, Schaffner et al. 2012). As well as coming to the ground for wood A. geoffroyi also seeks out water from ground sources (Campbell et al. 2005). Studies have not found Ateles sp. to consume animal protein (Valero 2004). When ripe fruit is hard to find leaves are substituted during this time spider monkeys are known to rest more frequently, spider monkeys use mental maps efficiently to remember key locations of seasonal ripe fruits these locations can be 500 meters or more apart, Ateles geoffroyi has an important role in the ecosystem as a seed disperser (Boyer et al. 2006, Chaves & Stoner 2010, Valero 2004). pg. 11 Because A. geoffroyi has a fission-fusion group dynamic it limits competition within the troop for food. Mental maps makes it easy for these smaller groups to navigate around their territories and then congregate in the evenings (Chaves & Stoner 2010). 11. Social Behaviour and Groupings Ateles geoffroyi has a rare social structure in which females will leave the troop upon reaching sexual maturity and the males in a troop are all related, most other monkey social groups would consist of related females (Hagell et al. 2013, Watt 1994). The diurnal species A. geoffroyi has a fission-fusion dynamic where the troop of up to 70 members splits up into small groups of 3 – 4 to forage in the trees, numbers in a troop depend on food availability (González-Zamora et al. 2012, Schaffner et al. 2012, Turnock & Slater 2011, Valero 2004). Females are known to have ‘core areas’ estimated to be around 259 – 388 hectares with 20 – 30% overlap with other female groups, spider monkeys are rarely seen associating with other primates (IUCN 2008). The males in a troop will be more accepting of new females than the existing females in the troop, spider monkeys can be aggressive towards each other, in the troop adult males are rarely aggressive towards each other, males and females can show aggression but most of the fighting occurs between juvenile males and an adult male, this can be serious aggression and can result in death, mood swings can be sudden and violent (Campbell 2006, Fedigan & Baxter 1984, Hines 2014, Ramos-Fernández et al. 2009). Dominant females in a troop will associate more with males than subordinate females, the reward in this is that their offspring will associate more with the males and be accepted into the troop more readily (MacIntosh n.d.). Social interaction such as grooming and grappling take place at any time, even at night. The average grooming session lasts 2 minutes, adult females do the most grooming, followed by males and juveniles. Juveniles were groomed more often than females and males. Sleeping sites of A. geoffroyi are quite easily found due to the latrines, spider monkeys defecate in the same spots and that leads to a clumped deposition of seeds (Eisenberg 1976, González-Zamora et al. 2012). pg. 12 12. Natural Predators and Disease 12.1 Natural Predators Large felids such as jaguars, ocelots and pumas are the typical predators of spider monkeys but venomous and constricting snakes, crocodilians and raptors such as harpy eagles can all pose a threat (Campbell et al. 2005, Chaves & Stoner 2010). In areas with less felids spider monkeys will spend less time scanning the environment (around 20 minutes) than in areas with known felid predators present (around 2 hours). Females show vigilance around juveniles and young, males will show vigilance when females and juvenile play (Campbell et al. 2005). By far the worst threat is humans, hunting for food and deforestation. 12.2 Disease Wild monkeys can carry many diseases. Ateles geoffroyi in the wild is a host of many diseases some of which are, Yellow fever (not in Australia), Herpesvirus ateles (HVA), Echinococcosis multilocularis which causes Alveolar echinococcosis (Northern hemisphere disease) (Borji et al 2012), which cannot be contracted unless interactions with first foxes and then rodents takes place. Monkeys play no role in transmission they can just contract it. Incubation rate of 5 – 15 years. Falciparum malaria (not in Australia). Animals entering Tasmania come from established zoos with medical records and would be checked thoroughly by professionals upon entering the state. 13. Threat to Human Safety Spider monkeys have been known to attack humans, generally speaking this is usually occurring when the monkeys are being used as a tourist prop, on a leash and people pay to pat and handle the monkey, monkeys can attack very quickly. Spider monkeys also do not like being crowded and this can often cause an attack. One case of note occurred at a Brazilian Zoo called Parque Dois Irmãos, a black-handed spider monkey escaped its cage and attacked a girl, and she was bitten on pg. 13 the face. The result was she went to hospital and they dressed the wounds, no stitches, she received a rabies shot and recovered well (Animal Planet n.d.). Another case occurred in a Brazilian zoo where an intoxicated man jumped the fence and swam across a moat to access the monkeys, before he reached the island a spider monkey gashed his arm in a couple of places, the man took a while to realise what was happening then when he did he swam back to the fence and keepers helped him out of the cage and called for help he was taken to hospital but it is not documented the action doctor undertook (The Telegraph 2011). There have been many reported escapes from zoos, including Dallas Zoo, Chester Zoo, Hogle Zoo, and a wildlife park in San Antonio (Cabrero 2011, Chester Chronicle 2010, Monkey News 2010, WFAA 2011). In every instance the monkeys have been recaptured and returned to their cages and in most instances it is not stated how the escape occurred. Of those that were noted it was usually handler error. 14. History as a Pest There is no record of this species being recognised as a pest, they do access agricultural establishments in the native territories but the impact they have is minimal (Estrada et al. 2006). People do keep spider monkeys as pets in Northern America and they are required to hold an exotic pet licence. Spider monkeys are not available in Australia as a pet. 15. Potential Impact in Tasmania The potential impacts on Tasmanian species, assets, primary industry and infrastructure would generally be minimal should Ateles geoffroyi escape from captivity, one area that may be influenced is agriculture. Spider monkeys are known to use agricultural areas in their territories as thoroughfares and sometimes to access food. Crop damage was noted by farmers in banana, citrus, mango and allspice plantations but not in cacao and coffee plantations. Spider monkeys in this study were found to frequent plantations less often than other primate species (Estrada et al. 2006). pg. 14 This species has an extended juvenile period and long inter-birth period which means that there is minimal risk of establishing a large population rapidly. They are frugivores so they consume a large amount of ripe fruit, an escapee would struggle to find enough food. Spider monkeys will turn to foliage when fruit is in short supply, the tree community generally in Tasmania is completely different to evergreen rainforests of Central America, and the small and dry native leaf material may cause a spider monkey to turn to exotic broader and fleshier leaf plants in gardens and public areas. A spider monkey on the loose could pose a threat to human safety only if it were approached and cornered. As noted in the ‘Threat to human safety’ section these animals can have violent mood swings and should this happen, people could be hurt. Tasmanian native species such as the brushtailed possum (Trichosurus vulpecula) and ringtail possum (Pseudocheirus peregrinus) both eat fruit as a main component of their diet. There would be competition between these species, A. geoffroyi is diurnal whereas T. vulpecula and P. peregrinus are nocturnal. Ateles geoffroyi does not build nests or nest in tree hollows therefor there would be no competition for sleeping areas. There would be no predators of A. geoffroyi in Tasmania should they become established. 16. Previous Risk Assessments The Vertebrate Pest Committee (VPC 2007) lists Ateles geoffroyi as 3a/Serious, this means that the threat is serious should the spider monkey escape but it is able to be kept under permit for exhibition, education, entertainment or conservation. The VPC states that a serious threat is classified as ‘These animals may be introduced and/or should be kept only in collections approved by the relevant State/Territory authority as being primarily kept for (1) public display and education purposes, and/or for (2) genuine scientific research approved by the relevant State/Territory authority, and as meeting Best Practice for the purposes of keeping the species concerned.’ pg. 15 17. Risk Management A complete Species Risk Assessment will be undertaken by the Tasmanian Department of Primary Industries, Parks, Water and Environment (DPIPWE), following the submission of this Species Profile. Utilising the Bomford (2008) Modelling System, a four-factor analysis will be applied to assess the likelihood of establishment of black-handed spider monkeys, should import of the species be permitted and an escape of release occurs. 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