Chapter 11 Disease Management in Ex-Situ Invertebrate Conservation Programs
Animal conservation programs have traditionally been dominated by “charismatic” vertebrate species.18 The International Union for the Conservation of Nature (IUCN) has evaluated the conservation status of 100% of the 9932 avian species it currently recognizes and 99% of the 4842 mammalian species, but less than 0.3% of the over 1 million currently described invertebrate species have been evaluated. Although most authorities believe that the real number of invertebrate species is likely 6 to 10 million,15,24 others estimate the number may be as high as 80 million.56,57 Whatever the actual figure, we may not even be certain to within an order of magnitude of the true number of these species.22,23
Conservation is usually defined as the “preservation of biodiversity,”24 and the World Conservation Strategy17 proposed this as one of the three basic objectives of conservation. Ignoring invertebrate species in zoo programs could reduce the meaning of our work in fulfilling the definition of conservation. It is hoped that zoos will continue to expand their captive conservation programs to include a broader cross section of the animal kingdom, including invertebrates.35
Although the educational use of invertebrates to illustrate the importance of preserving biodiversity probably remains their main contribution at present, zoos are also involved with some captive breeding of endangered invertebrate taxa for potential future reintroduction programs.13,36–38 Invertebrate captive breeding may be more economical than breeding of vertebrates because they have a shorter generation interval and higher yield. Therefore, invertebrates may be a convenient means of boosting a zoologic institution’s captive breeding contribution for minimal cost. Unfortunately, maintaining viable, self-replicating captive colonies is often not sufficient to ensure the success of reintroduction programs.13,18
Also, it remains to be seen how this definition of conservation, as the preservation of biodiversity, will affect wildlife veterinarians when dealing with parasites that may be even more endangered than their more charismatic hosts. There has already been debate on lethal side effects of relatively nonspecific treatments, such as the macrocyclic lactones, on minimally pathogenic but often extremely host-specific parasites, such as avian Mallophaga lice,35 not to mention nontarget species such as endangered dung beetles. In the future the conservation biology community may criticize veterinarians’ sometimes indiscriminate use of these treatments.
In regard to zoo-based invertebrate conservation programs, unfortunately, disease risk assessment, screening, and management lag behind vertebrate programs. Therefore, zoo veterinarians need to develop increased interest and involvement in maintaining the health of this significant portion of the animal kingdom.
Recognition of the specific extinction threat causing a population to decline in its native habitat is essential to the success of any invertebrate captive breeding and reintroduction program. Conservation plans, captive management, and pathogen risk limitation need to be planned with this in mind. The most important threats are habitat loss or change, overkill, exotic species invasions, chains of extinction (decline in one species leading to declines or extinction in a host of other interdependent species), and nontarget pesticide effects.26 Most conservation entomologists believe that habitat loss or change is the main global threat to inverte-brate biodiversity. Therefore, to be successful, captive breeding programs for reintroduction must be coupled with habitat conservation or modification programs.
As in charismatic megavertebrates such as elephants or rhinoceroses, unsustainable harvesting, or overkill, has also played a key role in the decline of a number of invertebrate species. Lepidoptera are particularly affected. Unfortunately, the more endangered the species, the more desirable it is to collectors. The British subspecies of the large copper butterfly (Lycaena dispar dispar) was collected to extinction by 1848. The numerous reintroduction attempts at sites in Britain and Ireland all have ultimately failed.9,26
The black-veined white butterfly (Aporia crataegi) became extinct in the United Kingdom (U.K.) in the 1920s, but the reason for its decline could not be established. Although many reintroductions have been attempted, all these have again ultimately failed. This highlights the fact that Captive breeding and reintroduction may be ineffective unless the underlying problem is identified and then corrected. Of the four species of butterfly to become extinct in the U.K. in the last 200 years, only the large blue butterfly (Maculinea arion), extinct in 1979, has been successfully reintroduced since 1983 using stock from Sweden. This butterfly has specific habitat requirements. Its larvae initially feed on the flower heads of wild thyme (Thymus polytrichus), but after the fourth instar, they feed on ant grubs within the nests of Myrmica red ants.59 Accurate identification of the factors causing its extinction, as well as management of its habitat requirements as part of the reintroduction, has been essential to its success.
We are likely to see the increasing influence of genetically modified crops in the future, as well as the more well-documented effects of some pesticides on nontarget species. Genetically modified corn pollen has been shown to affect monarch butterfly larvae (Danaus plexippus) feeding on neighboring milkweed.21 Crops genetically modified to produce Bacillus thuringiensis toxins are likely to increasingly affect some nontarget invertebrate species, mainly those with a particularly alkaline midgut pH.58
The introduction of exotic species has devastated some localized species, such as the Polynesian Partula species tree snails, many of which were decimated by the poorly conceived introduction of Euglandina rosea predatory snails, released as a postulated biologic control measure for introduced giant African land snails (Achatina fulica), which had become crop pests. Inadvertent introduction of a novel invertebrate pathogen into an already-threatened, naive wild population could be just as disastrous.6
As with vertebrate captive breeding and reintroduction programs, careful disease-screening measures are essential before invertebrate reintroductions.62 It would be irresponsible for zoologic collections to undertake breeding and release programs without pathogen risk assessments and screening to prevent the introduction of diseases into the wild population.1 It is generally accepted that deliberate or accidental introduction of exotic organisms or diseases into ecosystems by humans has been one of the major causes of extinctions and loss of biodiversity in recent years.27 Unfortunately, pathogen evaluations are often limited to investigation once an epizootic occurs. The IUCN guidelines for reintroductions14 and translocations16 are as relevant to invertebrates as to vertebrates.
One useful captive husbandry principle is to avoid having enclosures of species with high conservation priority adjacent to exhibit species of low importance. An example would be an endangered weta species (Deinacrida) enclosure next to a desert locust (Schistocerca gregaria) exhibit, a species that is often infected, even if subclinically, with eugregarines.36 Although these parasites are usually regarded as fairly host specific, both insect species are members of the Orthoptera, and it would be sensible to keep these separated. Because some Eugregarines do not cause increased mortality and may only cause subtle signs such as reduced fecundity and reduced growth rates, monitoring of dead individuals may not be sufficient to detect infection in the population. Pooled feces in ethanol could be examined for spores. Infection may not clearly affect captive population with optimum environmental conditions and surplus food but could significantly impact the survival probability of the same species in its natural habitat. Implementation of similar principles is also recommended with different taxa, such as gastropod snails.
Marine invertebrates are often not quarantined or screened before introduction by aquarists, but introduction of pathogens by this route is well recorded.53 Once introduced, disease control may be extremely difficult, with the complications of filtration systems and the sensitivity of exhibit invertebrates to many therapeutic agents.
Pathogen introduction risks are not only important to endangered invertebrate populations, but also to economically important insects. These include honey bees (Apis mellifera) and silkworms (Bombyx mori), as well as crop pollinator species. Some crops depend on a single insect species for their pollination, such as oil palms (Elaei guineensis) pollinated by the weevil Elaeidobius kamerunicus.
Additionally, novel infections are emerging in captive populations kept for conservation reasons.8 An invertebrate example is the recently described oral Panagrolaimidae nematode infection of tarantula spiders (Theraphosidae).† Brachypelma spp. such as the Mexican redknee B. smithi (listed in CITES Appendix 1) are popular zoo exhibit species. This fatal infection has been noted in captive bred terrestrial and arboreal species from the Americas, Asia, and Africa, including Brachypelma and Poecilotheria spp. The mode of transmission is unknown, but collections have reported spread of infection between separate enclosures in the same rooms, where spiders are obviously housed individually. Attempts at clinical treatment with benzimidazoles and antibiotics for concurrent bacterial infections have not prolonged survival.
The zoonotic potential of some related nematode species is also cause for concern. Mammalian infections have occurred as infections of deep wounds and are difficult to treat. Large species such as the Goliath bird-eating spider (Theraphosa blondi) may have fangs up to 3 cm in length, making infection of human bites a possibility. Because of the zoonotic risk and unsuccessful treatment attempts, euthanasia of affected spiders is strongly advised. With the emergence of this infection, it has been suggested that until the mode of transmission has been elucidated, veterinarians dealing with Theraphosidae spiders in zoologic collections institute a minimum quarantine period of newly acquired spiders, in a separate room, of at least 30 days. This should be prolonged in anorexic spiders approaching ecdysis (shedding), until resumption of normal feeding behavior after ecdysis has been observed.† This problem may adversely affect any future efforts at reintroduction and warrants further investigation.
The field of entomopathology is extremely well developed,2,19,58 but it has remained almost entirely focused on control of agricultural pest species and on human and domestic animal disease vectors. Modern techniques are often not applicable or affordable for disease screening in zoologic collections.51 The histologic basis of entomologic pathology research52,54,55 has now given way to molecular techniques, with the result that few entomologists are able to help with histopathologic queries.37 Zoo veterinarians may be familiar with disease screening in a large variety of vertebrate species but are usually limited in experience with invertebrate diseases and pathology.* Many of the most useful texts to a veterinary invertebrate pathologist are thus those from before this change in direction of entomologic pathology research.19,52,54,55
The well-recorded extinction in captivity of the last Partula turgida Polynesian snails, has been claimed to be the first proven case of extinction by infection, with a Steinhausia species microsporidian infection implicated.7 Unfortunately, because no initial disease screening or archiving of wild individuals’ tissues for later examination was performed, before captivity the true significance of this organism is by no means clear. It may have been present in the original wild population, even if at a low level.36,37
A similar situation is infection with the entomopathogenic fungus Metarhizium anisopliae var. anisopliae of captive stock of the endangered Frégate Island giant tenebrionid beetle (Polposipus herculeanus). This beetle was listed as critically endangered after the introduction of rats to its home island in the Seychelles.10 The rats have since been eradicated, but the beetle still has a restricted range, making the population vulnerable to a stochastic threat. Although adult beetle mortality rates appear to be low,10 approximately 30% of all dead adults examined postmortem demonstrated infection. This isolate appears to have a relatively low pathogenicity in adult beetles, but it is unknown whether this agent occurs naturally on Frégate Island or in beetles in their natural habitat. It is thus impossible to determine sensibly the level of intervention and disease control needed in captivity. Although the risk of introducing a novel pathogen into a naive wild population is to be avoided at all costs, rigorous isolation, culling, and time-intensive husbandry techniques would be counterproductive should this agent occur naturally in the wild population. Further research is therefore essential before the reintroduction of any captive bred beetles could be considered.
The diagnosis of pathogens is also complicated by the occurrence of normal entomosymbiont organisms. These may be intracellular or extracellular and may occur in specific regions, such as the digestive tract, or may be free in the hemolymph. These entomosymbionts may be found in highly developed structures or mycetomes,55 which have specific physiologic, organlike functions in some species. Mycetomes may contain a combination of several different organisms. Blattaria spp. such as the commonly kept Madagascan hissing cockroach (Gromphaorhina portentosa) have mycetomes associated with their adipose bodies. These are believed to be bacterial and rickettsial in nature. Elimination of the symbionts leads to abnormal protein metabolism, shortened survival rate, and reproductive failure.58 Partula spp. Polynesian tree snails appear to have large numbers of normal flagellates, which do not appear to be associated with disease.48 If pathologists are not familiar with the species, these may be erroneously diagnosed as pathogens.