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Inr. Zoo Yb. (1991) 30: 68-75 0 The Zoological Society of London

Captive- breeding programme for the Red-kneed bird- eating spider

at London Zoo Euathlus smithii

DAVE CLARKE Senior Keeper, Invertebrate Conservation Centre, The Zoological Society of London, Regent’s Park, London NWI 4RY, Great Britain

The Red-kneed bird-eating spider Euath- lus (Brachypelma) smithii, sometimes erroneously called a ‘tarantula’, is an ideal species for zoos and private collections because of its relative ease of main- tenance, longevity, docile nature, large size and attractive markings. Its popu- larity has led to its being collected from the native habitat in fairly substantial numbers giving rise to concern for the status of the species in the wild. Although the spider is represented in many zoolo- gical collections, the majority are simply maintained as individual exhibits and until recently little breeding had taken place. Certainly no co-ordinated captive- breeding programme has been formu- lated, although the loaning of mature 66 for pairing and some dissemination of juveniles has occurred.

The breeding of this species in captivity has now been shown to be a practical exercise and because most of the adult specimens of E. smithii now in collections are wild caught (Clarke, 1991) and therefore probably not closely related, we are in an excellent position to establish a co-ordinated approach towards the propagation of the species.

SPECIES DESCRIPTION Euathlus smithii is probably the best known of the bird-eating spiders (Thera- phosidae). An adult 0 measures some 6 cm from chelicerae to spinnerets with an overall leg-span of 17 cm; 65 tend to be slightly smaller in body size but have

proportionally longer legs. Most thera- phosids are shades of brown or grey but Euathlus species often have bright red markings on the legs or abdomen. Euath- lus smithii has bands of bright orange-red alternating with black on the legs, the cephalothorax is black with a tan pubes- cence on the outer edge and the abdomen is a deep black with intermittent longer white-tipped hairs over the legs and abdomen (Smith, 1986).

It has been reported that coloration may vary in different regions of its range and given the relatively large distribution of the species, and the apparently frag- mented populations in the wild, the occur- rence of regional variation is possible. However, one published report of colour dimorphism (Smith, 1986) appears to be based on a misinterpretation of Baerg (1958), who compares the ‘unique’ colour pattern of E.srnithii, which he calls the ‘golden-banded tarantula’, to other species in different regions which are more uniform in colour.

The species was originally described in 1897 from Guerrero, Mexico (Pickard- Cambridge, 1899). In the wild it is confined to Mexico, although there is one unconfirmed report of its occurrence in Costa Rica (Baerg & Peck, 1970). Previous reports have given locations in the states of Nayarit, Colima, Mexico, Guerrero and Chiapas (Baerg, 1958), with possible sightings on the west coast north to Sonora (Wells et al., 1983).

The generic name has been quoted at

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various times as Eurypelma or Aphono- pelma and was recently revised from Brachypelma to Euathlus (Raven, 1986).

STATUS IN THE WILD Euathlus smithii has been listed by the IUCN for several years in the category ‘Insufficiently Known’ (Wells et al., 1983; IUCN, 1990). A recommendation in the 1983 report that trade in the species should be controlled, was put into effect in 1985 when it was added to Appendix I1 of CITES, which requires parties to the convention to monitor trade in the species. Although Mexico is not party to CITES, there are national restrictions on the movement of wildlife, and collection or export of E. smithii is forbidden except under licence. It appears, however, that this is not strictly enforced, partly due to lack of resources (Smith et al., unpubl.).

In 1988 an expedition from Cambridge University, in collaboration with Dr N. M. Collins of IUCN, attempted to collect population data on the species in the wild (Smith et al., unpubl.). Colonies were located at four sites, one in Oja de Agua in Michoacan and three close together on the coast of Guerrero. There were local reports of a large distribution on the south-west coast, but as local inhabitants may have confused species, the accuracy of the information was ques- tionable. The report states that large areas of western Mexico remain uncultivated and provide apparently suitable habitat in which the species could still occur rela- tively undisturbed. Because disturbance of the habit appears to be limited and collec- tions from the wild are on relatively small scale, the main conclusion of the report was that E. smithii, as yet, is not seriously threatened (Smith et al., unpubl.).

In order to validate the status of E.smithii in the wild, we made contact with American and Mexican arachnolo- gists to determine whether anyone is currently working with the species, parti- cularly in relation to aspects of distribu- tion, variability (genetic and morpho- logical), present status, breeding and

conservation. It appears that no-one is working on E. smithii at present, although the need for study has been emphasized by a Mexican biologist and the National University of Mexico (L. Jiminez, pers. comm.; D. Stimpson, pers. comm.).

CAPTIVE BREEDING In attempting to assess the need and feasi- bility of a breeding programme for E. smithii, we have considered various aspects of the species’ distribution and biology: (1) the status of the species in the wild requires validation in order to review the necessity for conservation strategies in captive culture, which should always be allied to protection of the species in its natural habitat; (2) the breeding beha- viour must be studied and applied to captive-breeding programmes so that successful culture methods can be developed; (3) a protocol to maintain genetic diversity within the captive popu- lation needs to be formulated and inte- grated into the breeding programme.

Breeding of E. smithii in collections has become more frequent partly owing to the availability of maturing adult 88 either from recent importations of immature spiders from Mexico or from earlier captive-bred stocks and partly because data on successful breeding are becoming available (Clarke, 1991). A brief sum- mary of pairing and egg production is given here.

Male E.smithii usually mature at around five years of age and can be recog- nized by the fully developed intromittent organs on the end of the pedipalpi and by the body shape. Approximately two weeks after the maturing moult the 8 produces the first of several sperm webs, to transfer spermatozoa to the palpi in preparation for mating. The 99 normally mature at about seven years of age and are most receptive to mating if well fed. A 9 is selected for mating when no growth moult is expected because spermatozoa are stored in the exoskeleton and would be lost if she shed before egg laying. The 8 is introduced to the 0 in a large

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container with a flat, stable substrate and, since 99 may become aggressive, the mating process is monitored. The 6 signals to the 9 and if his approaches are accepted, the mating embrace takes place. During sperm transfer, the 8 raises the 9’s body, using hooks on the front pair of legs to hold her fangs, while he reaches forward underneath to insert the palpi into her genital opening. The actual mating normally takes only a minute or so and afterwards the 8 cautiously but quickly withdraws from the Q; he is then removed. The same 8 may be mated with the 9 again a few days later, to guarantee insemination. The 6 E.smithii will live only a short while after maturing, perhaps less than one year, therefore it is impor- tant to ensure a good mating in one season (Clarke, 1991).

One or two months after a successful pairing the egg sac, a large ball of silk, c. 35mm wide and containing up to a thousand eggs, is produced. Although it may be left with the 0, it has been known

for 99 to eat their egg sacs, particularly if disturbed. Artificial incubation also allows closer monitoring especially as, after about one month, an inspection ‘flap’ can be carefully cut into the silk to view development. The spiders hatch and moult once within the sac. Emergence of the young, which can number in excess of 700, takes place some two to three months after laying.

Newly emerged spiderlings remain close together but after their first moult outside the egg sac, within one month of emer- gence, they will commence feeding and we normally separate them to avoid canni- balism. The spiderlings grow slowly and moult approximately once a month in the first six months; frequency of moults declines over time. One-year-old spiderl- ings at London Zoo have an average cephalothoracic length of 4mm. It takes some five to seven years for E. smithii to reach adult size.

At London Zoo, most newly emerged spiderlings are separated into individual

Plate 1. A 9 Red-kneed birdsating spider Euarhlus smifhii depositing her eggs into the silk sheet that Will form the egg sac. D. Clarke.

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Plate 2. Euathlus smithii spiderlings emerging from an artificially incubated egg sac. D. Clarke.

cylindrical containers, 4.5 cm tall by 45cm diameter (60cc). The substrate is slightly dampened, fine-grade vermiculite and a small ball of soaked cotton wool is used to provide drinking water. By one year of age larger containers are necessary and adults are maintained in individual plastic boxes 28 x 15 x 10 cm high with a similar substrate and 4 cm diameter water dishes.

Initially the spiderlings are fed on single first instar crickets Gryllus bimaculatus every other day; as they develop the frequency of feeds decreases and the size of the food items offered increases. Mature E. smithii will accept a variety of live food and are even capable of over- powering an adult mouse. At London, they are fed on adult crickets and locusts. Like adults, spiderlings are not fed before or shortly after moults.

GENETIC PROTOCOL The only invertebrates for which a genetic protocol has been established in a breeding programme are the Moorean

tree snails Partulu spp. The protocol was devised in 1987 by G. Mace, B. Clarke & J. Murray with the aim of maintaining as much genetic diversity in the captive population as possible, given the limited captive gene pool (see Tonge & Bloxam, this volume). Following this protocol, which is based on principles relevant to all endangered species, it should be possible, theoretically, to retain 98% genetic diver- sity. We had to assess how a programme for E. smithii, a species which produces a large number of young at one time, would compare with that for Partulu.

Little is known about the genetic varia- tion of the current captive population (Clarke, 1991). As it is possible for 99 to live for 28 years in captivity (Russell, 1987), individuals from most of the wild collection sites may still be in culture. Some preliminary studies, using protein electrophoresis, are being made to deter- mine some baseline data on the pedigrees of E. smithii in the London Zoo collection and freshly dead adult spiders, after pathological examination, are frozen for

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storage, in anticipation of future investi- gation. A small number of newly hatched spiderlings from egg sacs produced in cap- tivity have been culled for the same purpose. When the data from the parents of this stock are analysed, it is hoped that it will be possible to compare the geno- types of one generation to the next. Also, preliminary work to extract genetic material from preserved specimens and moulted skins is being pursued both at the Zoo and the Arachnid Department of the British Museum (Natural History).

Because of the reasonably large number of E.smithii in captivity there is a basis for a captive-breeding programme. In 1987, 55 adult E.smithii were held in British Zoo Federation collections (Col- lins et d., unpubl.); currently London Zoo holds ten adults and over 500 young.

A prototype genetic protocol has been developed at the Zoo after discussion with Dr G. Mace. A foundation of, ideally, ten unrelated viable eggs sacs is needed to provide the initial required diversity and adult E. smithii in captivity, believed to be unrelated, will be paired to produce egg sacs. Each animal will be coded to retain individual identity and once a spider has contributed its genes to the next genera- tion it will not be used again; whenever possible individual genetic information will be stored. Assuming successful production of young, a minimum of 40 spiderlings from each of the ten founder eggs sacs will be kept specifically for the breeding programme. It is presumed, for the purpose of the genetic protocol, that 20 of these young will survive to become adult and of these ten will be suitable for breeding purposes. It is from these ten

groups of ten adults that the next genera- tion would be produced.

The basic format of this breeding protocol is applicable to various arachnid species taking into account production of large numbers of young from a single mating. However, E. smithii is somewhat unusual in having such a long life cycle and the majority of arachnid species live no more than a year or two (Savory, 1977) so turnover of generations in cap- tivity would normally be much quicker.

GENETIC MANAGEMENT AT LONDON ZOO An essential requirement in any planned breeding programme is, of course, identi- fication of individuals. At London Zoo, all sub-adult and adult E. smithii are allo- cated an individual identification number; egg sacs and young are identified by the mother’s code followed by a further iden- tifying letter until are they are separated and assigned an individual code. Thus, the first egg sac of spider ‘ZSLE.s.9’ is labelled ‘ZSLE.s.9A’ with a change of the last letter for any future egg sacs.

In 1988, two successful matings of un- related E. smithii were achieved (Table 1). One of the $6 was on breeding loan from a private collector, the other 1.2 animals matured in the collection. Both egg sacs were removed for artificial rearing. The majority of the nearly 700 young which emerged from ZSLE.s.9A, in April 1989, were isolated into individual containers within the first month after their post- emergence moult. For the first six months 300 of these separated young were organ- ized into three groups with different feeding methods and notes made on moulting rates. Although limited staff

P 3 MATED 2nd EGG SAC DATE YOUNG 1st SEPARATED MATING OPENED EMERGED MOULT’

E.s.9 E.s.25 29 Nov 88 5 Feb 89 19 Mar 89 20 Apr 89 2 May 89 21-28 May 89 E.s.10 E.s.22 7 Nov 88 10 Nov 88 24 Apr 89 13 Jul 89 20 Jul 89 12 Aug 89 2C-31 Aug 89 E.s.20 E.s.19 8 Dec 89 8 Feb 90 16 Mar 90 May 1990 May 1990

‘Outside egg sac. Table 1. Red-kneed bird-eating spider Euathfus smithii egg sacs produced at London Zoo in 1989 and 1990.

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time prevented us from extending this study beyond the six-month period, the individuals retain the identity of their group and maturation dates can be recorded. Young from the second egg sac, ZSLE.s. 10A, emerged in July 1989. As an experiment, only a proportion of these were separated into individual containers, the remainder being kept in communal groups of 25 spiderlings to a 28 x 16 x 10 cm high container. They were given a substrate of thick sphagnum moss to offer ample hiding places and live food was liberally provided. Even so, after six months to one year, only a single larger than average spider had survived in each of eight containers. The sheer number of spiderlings from each egg sac permitted the efficiency of rearing methods to be assessed, while allowing several hundred animals to be disseminated amongst other collections.

The egg sac of a third pairing was left with the which was found ripping the

silk open just over one month after laying. Although there were a small number of living young, most of the eggs were decomposing. The 15 surviving spider- lings were separated and continued to develop normally.

Groups of spiderlings from London Zoo have been distributed to other collec- tions, notably Glasgow, Chester and Amsterdam Zoos, and the amateur arach- nologist group the British Tarantula Society (BTS) are assisting with rearing the remainder. Other zoos and societies have also successfully produced young and juveniles have already been exchanged between London and Chess- ington Zoos. At time of writing another egg sac is expected from a recent mating between a 6 at London Zoo and a 0 owned by a member of the BTS.

CONCLUSION One of the most important factors in the success of a captive-breeding programme

Plate 3. Adult $2 E. smithii, E.s.10, with spiderlings. The young have been through their first moult outside the egg sac and will soon be put into individual containers. D. Clarke.

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is the establishment of unrelated founder stock, and the availability and successful mating of unrelated animals. With a large group of animals being maintained between several institutions, the prob- ability of success with E.smithii is increased. The breeding season, which is linked to the maturation of the $3, occurs in mid- to late summer in Mexico (Wells et al., 1983). At London, $ E. smithii have usually matured in October or November and egg sacs have been produced in January to March of the following year. Maintaining the timing of the breeding season in tandem with the wild popula- tion should be considered if re-introduc- tion programmes are envisaged. Long- term effects of captive culture, such as temperature, food and photoperiod, may already be influencing the natural cycle and more study is required into the neces- sity to control seasonal changes in the captive environment.

Typically, $$ mature at approximately five years of age, with 99 not reaching breeding condition until two or three years later (Wells et al., 1983). This is possibly a natural defence against inbreeding which could be used to advan- tage in a captive programme, since 99 from egg sacs laid earlier in the breeding programme could be mated with 88 from later broods. Euazhlus smizhii is a long- lived species and it will be several years from one generation to the next. The recent improvement in techniques for sexing theraphosids (Hancock & Hancock, 1989) along with the ability to manipulate the growth rate of individuals by adjusting temperature and food supply (Savory, 1977) means that, if necessary, spiderlings can be brought to maturity in the sex ratios required for the next stage of the breeding programme. The possibili- ties of sperm and egg storage, should also be investigated for the storage of such material could help overcome the prob- lems which might arise because of different maturation times of the sexes, the relatively short adult lives of $6 and inbreeding.

Ironically, the success of the captive culture of E. smithii produces its own problems. In the wild mortality rates can be as high as 98% (Baerg, 1958); in cap- tivity they may be as low as 2%. With more than 700 spiderlings from each mating, huge numbers could be produced yet for the proposed programme only some 40 individuals are needed. A certain number of animals could be housed in other zoologicaI institutions, possibly for display only, but we are left with the question of whether the surplus animals should go into the pet trade. Trade in invertebrates in Britain appears to be on the increase, with a distinct rise in the number of private individuals keeping exotic pets. Would providing captive-bred animals to the trade create an even bigger demand? Would morc be kept in unsuit- able conditions? Is culling of juveniles an ethical alternative? The question of what to do with surplus captive-bred stock will have to be faced and solved.

Even if the situation in the wild should deteriorate further, E. smithii’s popularity as a captive animal and the present success in captive breeding should ensure the survival of the species. However, a co- ordinated breeding programme is essen- tial and the captive population needs to be managed genetically and demographi- cally. The experiences gained with this species may be applied to other threat- ened arachnids, such as the No-eyed big- eyed wolf spider Adelocosa anops (IUCN Endangered), perhaps not as charismatic but certainly no less deserving of the attentions of captive breeding.

ACKNOWLEDGEMENTS

My thanks to Paul Hillyard of the British Museum (Natural History) and Derek Stimpson of the British Entomological and Natural History Society for help with contacts abroad, and also Georgina Mace of the Institute of Zoology, The Zoological Society of London, for her work on genetics. Also we thank Chris Andrews, Paul Pearce-Kelly and Matthew Robertson for checking the text. Most important, thanks to the many dedicated people who over the past few years have painstakingly looked after the seemingly endless numbers of baby red-knees!

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REFERENCES Araneida. In Biologia Centrali-Americana: 1 4 0 . BAERG, W. J. (1958): The tarantula. Lawrence: University of Kansas Press. BAERG, W. J. & PECK, W. B. (1970): A note on the longevity and molt cycle of two tropical theraphosids. Bull. Br. arachnol. Soc. 1: 107-108. CLARKE, D. (1991): Captive breeding of arachnids. In Arachnida ’87: Proceedings of a one-day symposium on spiders and their allies. Cooper, J. E., Pearce-Kelly, P. & Williams, D. L. (Eds). Keighley, W Yorks: Chiron Publications Ltd. COLLINS, N. M., COOPER, J. E. & HUGHES, D. G. (Unpublished): Survey of invertebrates in Federation Collections. Unpublished report 1987. HANCOCK, K. & HANCOCK, J. (1989): Sex determination of immature theraphosid spiders from their cast skins. K. & J. Hancock, 28 Pump Mead Cl., Southminster CMO 7A0. Private publication. IUCN (1990): 1990 IUCN red list of threatened

London: Godman &- Salvin. RAVEN, R. J. (1986): The spider infraorder Mygalomorphae (Araneae): cladistics and systematics. Bull. Am. Mus. nat. Hist. 182 1-180. RUSSELL, A. (Ed.) (1987): Guinness book of records (1987). Beccles: W. Clowes. SAVORY, T. (1977): Arachnida (2nd edn). London, New York: Academic Press. SMITH, A. (1986): The tarantula: classification and identification guide. London: Fitzgerald Publishing. SMITH, R., SLEEMAN, J., BATCHELOR, J. & HAWORTH, R. (Unpublished): Report of the Cambridge Tarantula Project 1988. Report to the University of Cambridge, 1990. WELLS, S. M., F’YLE, R. M. & COLLINS, N. M. (1983): The IUCN invertebrate red data book. Gland, Cambridge: IUCN.

animals.’Gland, Cambridge: IUCN. PICKARD-CAMBRIDGE, F. 0. (1899): Arachnida Manuscript submitted 15 February 1991

Int. Zoo Yb. (1991) 30: 75-79 0 The Zoological Society of London

The project to rescue the Italian ground beetle Chrysocarabus olympiae

J. C. MALAUSA’ & J. DRESCHER? ‘Institut National de la Recherche Agronomique and ?Ofice pour I’ Information Eco- entomologique, c /o Laboratoire de Biologie des Invertibris, Insectarium ‘Emile Biliotti’. 1382 route de Biot, F-06560 Valbonne, France

Since its discovery in 1854 the story of the beautiful and rare Italian ground beetle Chrysocarabus olympiae has become almost a legend, intriguing several genera- tions of entomologists. A number of published works have been devoted to it, with the first complete monograph on behaviour and biology appearing almost a 100 years after its discovery (Sturani, 1947). Later came a comprehensive update on the biology and phylogeny of the species, with a review of its history and concrete proposals for its protection (Malausa et al., 1983).

Recent developments in captive

breeding and rearing techniques have increased our knowledge of the genetics and phylogeny of the species (Allemand & Malausa, 1984; Braun, 1988) and have led to the initiation of programmes for its conservation. For over ten years conser- vation studies have continued in an insec- tarium (Malausa, 1978) and the expansion of the population through captive breeding enabled trials to begin on the reintroduction of the species into protected areas with the aim of creating new populations (Malausa & Drescher, 1987).

In this paper we report on the progress