Erysipelas in the critically endangered kakapo (Strigops habroptilus)

Abstract

This paper describes the effect of a disease outbreak on the success of a translocation for conservation management in a critically endangered species. Three juvenile kakapo from a group of 19 translocated birds died within 72 h of transport between New Zealand offshore islands. Clinical findings, gross necropsy changes, cytology, histopathology and bacterial culture confirmed systemic disease caused by Erysipelothrix rhusiopathiae. On the island from which the kakapo were sourced, positive cultures of E. rhusiopathiae were obtained from the medulla of the ulna from 10 out of 15 seabird carcasses examined, suggesting that this could be the source of infection for the kakapo. Immediately after the diagnosis, all of the translocated birds were re-captured and treated with antibiotics. A vaccination programme has commenced using a commercial killed bacterin developed for turkeys. The disease outbreak has had costly implications for the population and conservation management of the species. This is the first report of erysipelas in wild parrots, and the first report of the management of erysipelas in a critically endangered wild population of birds.

L'érysipèle chez des strigops kakapo (Strigops habroptilus) en voie d'extinction

Dans cet article il est décrit l'effet d'un cas pathologique sur le succès du transfert d'une espèce en voie d'extinction pour parvenir à sa conservation. Trois jeunes strigops kakapo, appartenant à un groupe de 19 oiseaux qui ont été transférés, sont morts au cours des 72 heures de transport entre les îles proches du littoral de Nouvelle Zélande. Les observations cliniques, les lésions macroscopiques, la cytologie, l'histopathologie et la culture bactérienne ont confirmé la présence d'une maladie systémique causée par Erysipelothrix rhusiopathiae. Sur l'île d'où provenaient les strigops kakapo, E. rhusiopathiae a été isolé par culture à partir de la moelle du cubitus de 10/15 carcasses d'oiseaux marins examinés suggérant qu'ils pouvaient être la source de l'infection des strigops kakapo. Immédiatement après le diagnostic, tous les animaux transférés ont été de nouveau capturés et traités aux antibiotiques. Un programme de vaccination a commencé en utilisant le vaccin inactivé commercial développé pour les dindes. Ce cas pathologique, a eu des répercussions coûteuses pour la population et la réussite de la conservation de l'espèce. C'est le premier rapport d'un cas d'érysipèle chez des perroquets sauvages et le premier rapport de la gestion de l'érysipèle chez une population sauvage d'oiseaux en voie d'extinction

Rotlauf bei stark vom Aussterben bedrohten Eulenpapgeien (Strigops habroptilus)

Diese Veröffentlichung beschreibt die Auswirkung eines Krankheitsausbruchs auf den Erfolg eines Umsiedlungsprogramms als Erhaltungsmaßnahme bei einer bedrohten Tierspezies. Drei juvenile Eulenpapageien aus einer Gruppe von 19 umgesiedelten Tieren starben innerhalb von 72 Stunden Transportzeit zwischen den vor der Küste gelegenen Inseln Neuseelands. Klinik, Pathologie, Zytologie, Histopathologie und bakteriologische Kultivierung bestätigten Erysipelothrix rhusiopathiae als Ätiologie der systemischen Erkrankung. Auf der Insel, von der die Eulenpapageien stammten, wurde E. rhusiopathiae aus der Medulla der Ellenbogenknochen bei 10 von 15 Seevogelkarkassen isoliert, die in der Annahme untersucht wurden, dass sie die Infektionsquelle für die Eulenpapageien gewesen sein könnten. Unmittelbar nach der Diagnose wurden alle umgesiedelten Vögel wieder eingefangen und antibiotisch behandelt. Ein Vakzinationsprogramm unter Verwendung eines kommerziellen für Puten entwickelten Totimpfstoffs wurde begonnen. Dieser Krankheitsausbruch hatte kostspielige Auswirkungen auf die Population und das Erhaltungsprogramm für diese Spezies. Dies ist die Erstbeschreibung von Rotlauf bei wildlebenden Papageien und der erste Bericht über eine Rotlaufbekämpfung in einer vom Aussterben bedrohten Wildvogelpopulation.

Erisipelas en el kakapo (Strigops habroptilus) en peligro de extinción

Este artículo describe el efecto de un brote de enfermedad que ocurrió durante el traslado por motivos de conservación de una especie en peligro de extinción. Tres kakapos juveniles de un grupo de 19 aves que fueron trasladadas murieron durante las 72 horas de transporte entre islas (off shore islands) en Nueva Zelanda. Los hallazgos clínicos, las lesiones macroscópicas a la necropsia, las citologías, histologías y el cultivo bacterológico confirmaron que la enfermedad sistémica fue causada por Erysipelothrix rhusiopathiae. En la isla de la que provenían los kakapos, se obtuvieron cultivos positivos de E. rhusiopathiae de la médula de la ulna de 10 de 15 cadáveres de aves marítimas examinadas, lo que sugirió que ésta podría ser la fuente de infección de los kakapos. Inmediatamente tras el diagnóstico, todas las aves trasladadas fueron capturadas y tratadas con antibióticos. Se ha iniciado un programa de vacunación con una bacterina comercial desarrollada para pavos. El brote de enfermedad tuvo implicaciones costosas para la población y para el manejo y conservación de la especie. Esta es la primera descripción de brote de erisipelas en loros salvajes, y también es la primera descripción el manejo de esta enfermedad en una población de aves salvajes en peligro de extinción.

Introduction

Infection in animals with the bacteria Erysipelothrix rhusiopathiae is known as erysipelas (Bricker & Saif, 1997; Shimoji, 2000). Erysipelas in birds is characterized by either acute, fulminating infections or, more rarely, chronic infections causing infertility in male birds and reduced egg production in females (Bricker & Saif, 1997). Erysipelas infections in poultry, particularly turkeys, have been recognized since at least the turn of the century (Bricker & Saif, 1997; Hafez, 2003). Outbreaks of erysipelas causing deaths have occurred in many other bird species, including albatross, crows, pheasants, ducks, geese, guinea fowl, chukars, grebes, malleefowl, tawny frogmouths, budgerigars and waterfowl (Gerlach 1994; Bricker & Saif, 1997; Wobeser, 1997; Swan & Lindsey, 1998; Blyde & Woods, 1999; Brooke & Riley, 1999; Parvanta, 1999; Work et al., 1999; Weimerskirch, 2004).

Studies of the control of avian erysipelas are based on experiences with poultry (Gerlach, 1994; Bricker & Saif, 1997; Wobeser, 1997; Hollifield et al., 2000; Hafez, 2003) and isolated reports of the control of outbreaks in emu and malleefowl (Swan & Lindsey, 1998; Blyde & Woods, 1999). The current recommendation for management of outbreaks in poultry flocks (reviewed by Bricker & Saif, 1997) is to administer antibiotics to all birds in the affected flock as soon as the diagnosis is established and to vaccinate all members of the flock. Vaccination recommendations are for two doses of the adjuvanted killed bacterin vaccine 4 weeks apart (Anonymous, no date). Live vaccines are now becoming available for poultry and have been used in pigs for 30 years (Bricker & Saif, 1997; Yamamoto et al., 2000; Lacave et al., 2001).

The kakapo (Strigops habroptilus) is a critically endangered parrot endemic to New Zealand. It is a giant, flightless, nocturnal parrot, and the only representative of its subfamily (Strigopinae) (Clout & Merton, 1998; Higgins, 1999). Kakapo are extinct throughout their natural range and are currently maintained on three offshore islands where they have been translocated since 1997 (Clout & Merton, 1998; Higgins, 1999). The goal of the New Zealand Department of Conservation is “to establish at least one viable, self-sustaining, unmanaged population of kakapo” and “two or more other populations which may require ongoing management” (Cresswell, 1996). Currently the three populations require intensive management to be sustainable (Cresswell, 1996; Clout & Merton, 1998; Higgins, 1999). One of the management tools used to enhance the chances of successful reproduction in adult birds is translocating juvenile birds to less productive islands (Clout & Merton, 1998; Cresswell, 1996; Higgins, 1999).

This paper describes the effect of a disease outbreak on the success of a translocation for conservation management in this species. It is the first report of a mortality outbreak caused by infection with E. rhusiopathiae in kakapo, and is also to the best of our knowledge the first paper to report the management of the disease in a critically endangered wild population of birds.

Case History

The New Zealand Department of Conservation translocated 18 young birds and one adult male from Codfish Island to Chalky Island on 8 July 2004 in the southern hemisphere winter. Pre-translocation health screening was carried out on 20 birds consisting of physical examinations, complete blood counts and faecal cultures for the bacterial species Yersinia, Salmonella, and Campylobacter as outlined by Brangenberg et al. (2003). One bird was excluded from the transfer because of an ulcerative cloacitis but the remaining 19 showed no significant abnormalities. The birds were shifted in two batches approximately 5 days apart. They were kept in clean plastic transport boxes or housed in small pens overnight prior to translocation. During the translocation they were held in clean transport cages and did not come in physical contact with each other.

All birds were monitored using radio-transmitters following translocation. Immediately after release, five birds were noted to have a lower level of activity than is commonly seen post-translocation. The first mortality occurred in the 2 to 4 days after transport of the first batch, and following this a bird from the second batch died 1 day after its transfer and a third bird died 3 days after transfer. The other two birds that had been noted to be slow in moving improved during this period.

The dead birds were transported individually by refrigerated courier to the diagnostic laboratory at the New Zealand Wildlife Health Centre, Massey University.

Results and Discussion

The gross, cytological, and histopathological changes and the results of bacterial cultures were similar in all three birds. All showed a congested, slightly swollen and mottled liver (Figure 1) and a congested and swollen spleen together with a variable degree of enteritis. This ranged from mild hyperaemia of the small intestine with fluid small intestinal contents in two birds, to severe hyperaemia of the intestines with severe watery diarrhoea in one bird. All birds were in good body condition with good fat reserves and food still present in the crop. The gross findings were suggestive of a bacterial septicaemia.

Figure 1.  In situ appearance of the swollen and mottled liver (L) of a kakapo after infection with E. rhusiopathiae. Adjacent is the heart (H) and abdominal and subcutaneous fat deposits (F). Scale bar = 2 cm.

Impression smears of liver, routinely stained with Wrights and Gram stains, showed low numbers of inflammatory cells, mainly macrophages, with a few heterophils and small lymphocytes and very occasional eosinophils. There were large numbers of bacilli present in the background of the smears but also heterophils and macrophages with the same bacteria in their cytoplasm. Impression smears of the spleen showed high numbers of small lymphocytes with occasional large lymphoblasts, reactive lymphocytes and macrophages. Very occasional heterophils and eosinophils were present. In a moderate number of macrophages the cytoplasm was full of bacilli and lesser numbers of organisms were present in the background. Heart blood smears showed an estimated white cell count of approximately 10×10⁹/l. The majority of cells were monocytes with lower numbers of reactive lymphocytes. Heterophils were very rare. Erythrocytes and thrombocytes appeared normal. There were bacilli in the background and in the cytoplasm of some monocytes. The spleen and liver cytology was consistent with a bacterial infection, and although there was presumably some postmortem bacterial overgrowth, the majority of organisms were intracellular. This was supported by the low to normal white cell counts and profound heteropaenia consistent with a peracute bacterial infection.

Tissues were routinely processed for histological examination and stained with haematoxylin and eosin and Gram's stain. Histologically, the livers were diffusely congested and contained irregular focal infiltrations of lymphocytes and plasma cells around many blood vessels. The cytoplasm of the majority of Kupffer cells throughout the livers was distended with large, Gram-positive, pleomorphic bacterial rods. Similar organisms were also present in the cytoplasm of some endothelial cells (Figure 2). The spleens showed diffuse lymphoid hyperplasia and contained numerous clumps of large histiocytes filled with similar Gram-positive organisms. The lungs showed a mild generalized increase in the numbers of circulating mononuclear cells. Many alveolar endothelial cells were laden with similar Gram-positive bacteria. The kidney showed a moderate early interstitial nephritis with peri-glomerular mononuclear cell infiltration and similar bacterial accumulations in many endothelial cells (Figure 3). A few endothelial cells in the hearts, proventriculus and small intestines contained similar bacteria. The histological findings confirmed the macroscopically suggested bacterial septicaemia.

Figure 2.  Photomicrograph of a Gram-stained section of liver of a kakapo after infection with E. rhusiopathiae, showing the cytoplasm of Kupffer cells (K) and endothelial cells (E) distended with large, Gram-positive, pleomorphic bacterial rods. Adjacent hepatocytes (H) are unaffected. Scale bar = 15 µm.

Figure 3.  Photomicrograph of a Gram-stained section of kidney of a kakapo after infection with E. rhusiopathiae, showing moderate early interstitial nephritis with peri-glomerular mononuclear cell infiltration (N). Scale bar = 10 µm.

E. rhusiopathiae was isolated from the liver, kidney and spleen of all three birds using standard culture and identification methods (Quinn et al., 1994). Antibiotic sensitivity testing showed the organisms to be resistant to penicillin but sensitive to amoxycillin/clavulanic acid, tetracycline and enrofloxacin. Antigen testing for Chlamydophila psittaci (Clearview Chlamydia test; Unipath Ltd, Bedford, UK) on a swab of fresh liver was negative in all three birds.

At the time of the mortality in the kakapo in July, there were no fresh seabird carcasses available so 15 desiccated seabird carcasses were collected from different areas of Codfish Island and sent to the diagnostic laboratory at the New Zealand Wildlife Health Centre, Massey University. The ulna was removed from each carcass and the bone marrow of the medulla was swabbed and cultured. Ten of the 15 seabirds sampled grew E. rhusiopathiae from the ulna bone marrow.

In birds, erysipelas is generally an acute fulminating infection and the characteristic diamond-shaped epidermal lesions common in mammals are rarely seen (Bricker & Saif, 1997; Wobeser, 1997; Amass, 1999; Blyde & Woods, 1999; Brooke & Riley, 1999; Ganière et al., 2001). Many different vertebrate species are affected worldwide, and outbreaks of deaths occur rarely but in a wide range of species and locations (Bricker & Saif, 1997).

Seabirds were considered to be the most probable source of infection for the kakapo in this mortality event as both Codfish and Chalky Islands have a diverse fauna of marine and terrestrial birds. The most numerous birds on the island are nesting seabirds from the family Procellariidae such as shearwaters (Puffinus spp.) and petrels (Pterodroma spp.). During the seabird breeding season in the southern hemisphere summer (October to December) there is an annual mortality of juvenile birds, and these carcasses are regularly found on the island. In wild birds, deaths due to erysipelas have been reported in a range of terrestrial birds and seabirds (Gerlach, 1994; Wobeser, 1997; Blyde & Woods, 1999; Parvanta, 1999; Work et al., 1999; Weimerskirch, 2004). Further microbiological studies, including DNA typing of the various isolates, will be necessary to confirm the source of infection. Other potential sources and vectors of erysipelas include fish (Fidalgo et al., 2000; Lehane & Rawlin, 2000), marine mammals (Kinsel et al., 1997), human handlers (Boo et al., 2003; Brooke & Riley, 1999; Maestre et al., 2001) and ectoparasites (Chirico et al., 2003). Surveillance of local birds and ectoparasites is recommended in order to learn more about the epidemiology of the disease.

The environmental factors that contribute to infections are only partially understood (Gerlach, 1994; Bricker & Saif, 1997; Brooke & Riley, 1999; Fidalgo et al., 2002). In many species, outbreaks are associated with rainy, cold weather. Sources of the organism may be contaminated feed, soil, or decaying matter; infected carrier birds within the flock; ectoparasites; or infected rodents (Gerlach, 1994; Bricker & Saif, 1997; Brooke & Riley, 1999; Fidalgo et al., 2002; Chirico et al., 2003).

The infection has zoonotic potential. In humans, infection with E. rhusiopathiae is generally characterized by a local infection (erysipeloid) but can occasionally be manifest as septicaemic disease, which may be fatal (Brooke & Riley, 1999; Lehane & Rawlin, 2000; Maestre et al., 2001; Boo et al., 2003). Infections are generally via a cut in the skin and are common in fish handlers, butchers, kitchen workers, veterinarians and turkey growers (Brooke & Riley, 1999; Lehane & Rawlin, 2000; Maestre et al., 2001; Boo et al., 2003).

Despite dealing with this disease in intensive conditions for the past century, in commercial turkey flocks there are no effective management strategies that do not rely on vaccination (Bricker & Saif, 1997; Swan & Lindsey, 1998; Blyde & Woods, 1999). Vaccination using the killed bacterin has been used in a wide range of avian species without significant side effects (Bricker & Saif, 1997; Swan & Lindsey, 1998; Blyde & Woods, 1999). Two doses of the commercial bacterin have been reported to give good immunity in field conditions where unvaccinated animals suffered between 6% and 10% mortality (Swan & Lindsey, 1998). Annual vaccination is currently recommended in high-risk flocks of turkeys, emu and mallee-fowl, although long term studies of the length of immunity induced are lacking (Bricker & Saif, 1997). It should be noted that none of the avian species studied so far are as long lived as kakapo.

There is a rare risk of anaphylactic reaction to vaccination (Anonymous, no date; Bricker & Saif, 1997). To mitigate this risk, animals should be observed immediately after vaccination. Treatment of acute allergic reactions involves using adrenaline intravenously or intratracheally and providing supplemental oxygen.

While the outbreak of erysipelas in kakapo has killed only young birds exposed to the stress of translocation, little is known of the epidemiology of the disease in the wild. Further work is required to elucidate the degree of exposure of the rest of the flock, the likelihood and method of spread between affected animals, and whether kakapo may become carriers of the bacteria or chronically infected. Given these uncertainties, it is difficult to suggest management practices other than vaccination that will reliably reduce the risk of fresh outbreaks of disease.

The subcutaneous route of vaccination is recommended and used safely in a wide range of bird species (Anonymous, no date; Bricker & Saif, 1997; Swan & Lindsey, 1998; Blyde & Woods, 1999). Given the relatively short neck and location of the boom sacs in kakapo, the neck should be avoided and the vaccination given under the skin of the inguinal flap between the leg and the abdomen.

Extrapolating from the reports of the behaviour of erysipelas in other species, if vaccination is not carried out it is probable that there will be further outbreaks of disease and deaths in the kakapo. This may occur in this season or in subsequent years. Animals that are not vaccinated should be considered at risk.

Translations of the abstract in French, Germany and Spanish are available on the Avian Pathology website.

The authors wish to thank the members of the Kakapo Recovery Team for all their work, Pat Davey and Evelyn Lupton for histological processing, and Nicola Smith for proof-reading.