Southern African Seabird Colony Disease Risk Assessment – December 2016

Recommended citation:

Parsons, NJ, Vanstreels, RETV, 2016. Southern African Seabird Colony Disease Risk Assessment – December 2016. Southern African Foundation for the Conservation of Coastal Birds, Cape Town, South Africa.

Cover photos:

Top left – Incinerator used to burn bird carcasses during an avian cholera outbreak on Dyer Island (South Africa), with black bags of dead birds in the foreground. Source: Waller & Underhill (2007). Top right – African penguin colony at Mercury Island (Namibia). Bottom left – Leucocytozoon tawaki in the blood smear of an African penguin. Bottom right – Post-mortem examination of a Cape gannet.

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Contents

1. Introduction ...... 6 2. Risk assessment ...... 7 2.1 Assumptions, limitations and acceptable risk ...... 7 2.2 Identification of disease hazards ...... 7 2.3 Assessing the risk of each disease hazard ...... 7 2.4 Disease hazards of high concern ...... 12 3. Management options ...... 12 3.1 Captive environment ...... 12 Biosecurity ...... 12 Prophylaxis ...... 13 Health screening ...... 13 Management of stress ...... 14 Period of quarantine ...... 14 3.2 Wild environment ...... 14 Carcase disposal ...... 14 Removal of sick birds for rehabilitation ...... 15 Disinfection ...... 15 Human disturbance ...... 16 Environmental management ...... 16 Release environment ...... 17 4. Monitoring and review ...... 17 5. Contingency planning ...... 17 6. Conclusion ...... 18 Acknowledgments ...... 18 References ...... 19

Appendix A. Summary of diseases affecting southern African seabirds ...... 22 1. Viral diseases ...... 22 Avian Pox ...... 22 Avian Herpesviruses ...... 23 Newcastle Disease ...... 24 Avian Influenza ...... 25 West Nile Disease ...... 26

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Eastern Equine Encephalitis ...... 26 Avian Reovirus ...... 27 Infectious Bursal Disease ...... 27 Other viruses ...... 28 2. Bacterial diseases ...... 28 Avian Cholera ...... 28 Chlamydiosis ...... 29 Mycoplasmosis ...... 30 Relapsing Fever Borrelia ...... 31 Lyme Disease Borrelia ...... 32 Bacterial Airsacculitis and Pneumonia ...... 32 Bacterial Gastroenteritis and Colitis ...... 33 3. Fungal diseases ...... 34 Aspergillosis ...... 34 Candidiasis ...... 35 4. Protozoal diseases ...... 36 Avian Malaria ...... 36 Babesiosis ...... 37 Leucocytozoonosis ...... 38 Haemoproteosis ...... 38 Toxoplasmosis ...... 39 Intestinal Coccidiosis ...... 40 Cryptosporidiosis ...... 41 5. Parasites ...... 42 Stomach Nematodes ...... 42 Intestinal Trematodes ...... 42 Intestinal Cestodes ...... 42 Tracheal Nematodes ...... 43 Renal Trematodes ...... 43 Ticks ...... 43 Fleas ...... 43 Lice ...... 43 Mites ...... 43 6. Toxins ...... 44

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Avian Botulism ...... 44 Marine Biotoxins ...... 44 7. Miscellaneous conditions ...... 45 Feather-loss Disorder ...... 45

Appendix B. Detailed risk assessment scoring sheets ...... 47 1. Penguins ...... 47 2. Cormorants ...... 48 3. Gannets ...... 49 4. Terns ...... 50 5. Gulls ...... 51 6. Pelicans ...... 52

Appendix C. List of controlled and notifiable animal diseases ...... 53

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1. Introduction

The African penguin Spheniscus demersus has a breeding range extending from southern Namibia to KwaZulu-Natal and is listed as Endangered due to a 60% decline in the population over the last three generations (BirdLife International 2016). Other seabirds breeding on the mainland or offshore islands of southern Africa that are also at risk of extinction are: the Cape cormorant Phalacrocorax capensis (Endangered), the Bank cormorant Phalacrocorax neglectus (Endangered), the Cape gannet Morus capensis (Vulnerable) and the Crowned cormorant Microcarbo coronatus (Near threatened) (BirdLife International 2016).

A biodiversity management plan was gazetted with the aim of establishing guidelines around African penguin conservation and consolidation of existing conservation work (Department of Environmental Affairs 2013). Action 4.5.4.3 states “Conduct a disease risk assessment for seabird breeding islands. Assessment to include documentation highlighting diseases already recorded, activities which may influence disease, ranking of importance of disease of concern”.

In a Disease Risk Analysis, the likelihood and consequences of disease occurring in a population are taken into consideration (Jakob-Hoff et al 2014). Steps involved in this process are 1) describing the problem with the assumptions, limitations and acceptable level of risk, 2) identification of the hazards, 3) assessing the risk for each hazard of concern, 4) evaluation of management options and risk reduction and 5) formulation of action plans with monitoring and review of actions as well as contingency planning (Jakob-Hoff et al 2014).

The goal of this document is to provide information on the different documented diseases in southern African seabirds along with an evaluation of their risk to the bird populations as well as management actions that can be taken to mitigate the effects of disease. In many cases, a disease outbreak is unavoidable, but contingency planning and intervention may allow the reduction of its population-level impacts. This document focuses solely on diseases caused by infectious and parasitic organisms or toxins; morbidity or mortality caused by predation, trauma or climatic events were not considered in the scope of this document.

Disease surveillance is necessary to manage diseases and pathogens to minimise the risk of diseases further reducing seabird populations. It is vital to continue conducting disease surveillance work to add to the information known about the occurrence of all these potential disease hazards. See document entitled “Disease surveillance in southern African seabird colonies” also prepared for the African Penguin Biodiversity Management Plan and the practical documents “Diseases seen in seabird colonies” and “Collecting carcases in penguin colonies” distributed to the African penguin working groups and colony managers, all prepared by Nola Parsons. This improved knowledge will enable better risk evaluations of the disease hazards in the seabird populations and therefore better management of the disease and of the risk of disease.

Disease is a major ecological force that has the potential to cause significant effects especially in threatened populations (Friend et al 2001) and Heard et al (2013) showed that the threat of disease increases with the level of extinction risk in all species. However, there is limited knowledge on the effects of disease on population dynamics of seabirds (Lewison et al 2012) or even for the role of disease as a major threat to species at risk of extinction (Heard et al 2013). While a single disease

6 outbreak could decimate a population, the true cost of disease may be associated with chronic attrition of the population (Friend et al 2001) and thereby influence metabolic rate, life history traits and social status (Barbosa & Palacios 2009).

2. Risk assessment

2.1 Assumptions, limitations and acceptable risk

A comprehensive disease risk analysis has been completed for the diseases known to infect southern African seabirds although there is often not much data available on the epidemiology and pathology of these diseases in these species. This document therefore incorporates, along with published information, personal experience and information based on other species and/or from other geographical areas, which implies a degree of subjectivity in the resulting risk analysis of some diseases. Some of the diseases evaluated in this document are uncommon and/or have not been recorded in the species concerned in South Africa, however they are considered in the analysis because an outbreak could potentially have dire consequences. It is also likely that there are diseases not listed due to lack of diagnostic testing and surveillance and therefore are unknown to occur in southern African seabird species. This is the best representation of our current knowledge.

The disease hazards are compared against each other and not against other hazards occurring in the wild population; caution is therefore warranted not to compare these relative disease risks to other conservation threats which may be more frequent and impactful (for example: competition with fishery resources, predation, oiling). Acceptable risk has not been evaluated although it may generally be considered lower for threatened species and higher for species of lower concern. It is also reasonable to expect that acceptable risk could vary over the year depending on management of the colony as a whole (ie: what species are breeding at certain times, what is the impact of disturbance from an intervention at a given time, etc).

Both captive and wild environments were borne in mind throughout this document, especially in treatment and quarantine (captive), prevention and control (both) and in the management options discussed below.

2.2 Identification of disease hazards

These are listed extensively and in detail in Appendix A based on current knowledge to date.

2.3 Assessing the risk of each disease hazard

Qualitative risk assessments were done for the African penguin, cormorant species, Cape gannet, gull species, tern species and the great white pelican (all species occurring on mainland South Africa and Namibia as well as offshore islands) (Table 1). Although there is data lacking in order to determine a numerical score for all of the disease hazards in all target species, the process of evaluating a numerical risk assessment is intended in assisting the detection and adjustment of inherent perception biases involved in the assessment. All disease hazards were evaluated on a score of 0-3 under the following criteria: species susceptibility, probability of exposure, inter-annual variability, potential to spread, chick survival/breeding impact, juvenile/adult survival impact and the

7 zoonotic potential (Table 2). The results of the assessment are summarised in Table 3, and the detailed scoring sheets are provided in Appendix B.

When no information was available for the target species (i.e. all species within the group, as listed in Table 1), the score was extrapolated from the closest related species in which the pathogen or disease is known to occur. When species sucsceptibility was scored as zero, the remaining scores were also considered zero and the pathogens and diseases were not evaluated for that seabird species.

For each pathogen or disease, a probability of occurrence score (POS) was calculated based on species susceptibility, probability of exposure and inter-annual variability. Similarly, an outbreak impact score (OIS) of each pathogen or disease was calculated based on potential to spread from bird to bird, chick survival/breeding impact and juvenile/adult survival impact. Both of these scores are expressed in values ranging from 0 to 10, and were further categorised as: low (lower than 4), medium (equal to or greater than 4 and lower than 7), or high (equal to or greater than 7).

POS = [ SS + (2 × PE) + IV ] ÷ 1.2

OIS = ( TO + IC + IA ) ÷ 0.9

Table 1. List of seabird species evaluated in the disease risk assessment. Group Species Common name Conservation status Penguins Spheniscus demersus African penguin Endangered Cormorants Microcarbo africanus Reed cormorant Least concern Microcarbo coronatus Crowned cormorant Near threatened Phalacrocorax capensis Cape cormorant Endangered Phalacrocorax carbo lucidus White-breasted cormorant Least concern Phalacrocorax neglectus Bank cormorant Endangered Gannets Morus capensis Cape gannet Vulnerable Terns Hydroprogne caspia Caspian tern Least concern Sterna dougallii Roseate tern Least concern Sternula balaenarum Damara tern Near threatened Thalasseus bergii Swift tern Least concern Gulls Larus cirrocephalus Gray-hooded gull Least concern Larus hartlaubii Hartlaub’s gull Least concern Larus dominicanus Kelp gull Least concern Pelicans Penecanus onocrotalus Great white pelican Least concern

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Table 2. Criteria used to score each disease/pathogen for each seabird group. Category Score Criteria Species susceptibility (SS) 3 Recorded in the target species.

(is there reason to believe the target 2 Recorded in the family of the target species. species is susceptible to the pathogen or 1 Presumed to infect/occur in most avian species. disease?) 0 Never recorded in target species or its family and not presumed to infect/occur in most avian species. Probability of exposure (PE) 3 Numerous cases recorded in target species in South Africa.

(how likely is it that the target species will 2 Few cases recorded in target species in South Africa. come into contact with the pathogen or 1 Recorded in other species in South Africa and/or serological evidence in target species in South Africa. disease in South Africa?) 0 Never recorded in South Africa Interannual variability (IV) 3 Regular occurrence in target species (cases are recorded almost every year).

(how consistently has the pathogen or 2 Occasional/sporadic occurrence in target species (cases are recorded a few times every 2-5 years). disease been recorded in the target 1 Rare occurrence in target species (cases are recorded scarcely every 5-10 years). species in South Africa?) 0 Extremely rare in target species (only a few cases have been historically recorded). Transmission in outbreaks (TO) 3 High (pathogen is air-borne and/or transmitted through direct bird-to-bird contact).

(how effectively can the pathogen or 2 Medium (pathogen or toxin is water, food or arthropod-borne). disease be spread to birds during an 1 Low (pathogen is an omnipresent opportunist or is rarely transmitted through direct contact). outbreak?) 0 None or very low (pathogen or disease has limited ability to spread among birds). Impact on chick survival and/or 3 High (substantial morbidity and/or mortality occur even in otherwise healthy individuals). breeding physiology (IC) 2 Medium (morbidity and/or mortality occur predominantly in weak or compromised individuals).

(how significant is the pathogen or 1 Low (morbidity and/or mortality are uncommon, even in weak or compromised individuals). disease to the survival of chicks or to the 0 None or very low (morbidity and/or mortality are extremely uncommon). reproductive physiology of adults?) Impact on juvenile/adult survival (IA) 3 High (substantial morbidity and/or mortality occur even in otherwise healthy individuals).

(how significant is the pathogen or 2 Medium (morbidity and/or mortality occur predominantly in weak or compromised individuals). disease to the survival of juveniles or 1 Low (morbidity and/or mortality are uncommon, even in weak or compromised individuals). adults?) 0 None or very low (morbidity and/or mortality are extremely uncommon). Zoonotic potential (ZP) high High (widely established zoonotic risk, with substantial lethal risk to humans).

(how significant is the pathogen or med Medium (widely established zoonotic risk, without substantial lethal risk to humans). disease to human health?) low Low or very low (possibly zoonotic but low risk of infection from seabird sources, minor disease effects). - None (no record of zoonotic infection).

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Table 3. Outcomes of the disease risk assessment for southern African seabird colonies.

Pathogen or disease Penguins Cormorants Gannets Terns Gulls Pelicans Zoonotic POS OIS POS OIS POS OIS POS OIS POS OIS POS OIS potential Viral diseases Avian pox 10 5.6 3.3 3.3 - - 3.3 3.3 3.3 3.3 - - - Herpesvirosis (S. African strain) 6.7 3.3 ------Herpesvirosis (S. American strain) 1.7 10 ------Herpesvirosis (cormorant strain) - - 1.7 2.2 ------Newcastle disease 5.8 10 6.7 10 2.5 10 3.3 10 3.3 10 6.7 10 low Avian influenza (high pathogenicity) 2.5 10 2.5 10 2.5 10 5.8 10 5.8 10 2.5 10 high Avian influenza (low pathogenicity) 3.3 3.3 3.3 3.3 3.3 3.3 4.2 3.3 5.8 3.3 3.3 3.3 med West Nile disease 4.2 6.7 3.3 6.7 2.5 5.6 2.5 5.6 3.3 4.4 3.3 5.6 med Eastern equine encephalitis 2.5 6.7 1.7 6.7 0.8 6.7 0.8 6.7 1.7 6.7 0.8 6.7 med Avian reovirus 3.3 4.4 ------3.3 4.4 - - - Infectious bursal disease 3.3 5.6 ------Bacterial diseases Avian cholera 6.7 7.8 8.3 10 6.7 10 6.7 10 6.7 7.8 1.7 10 low Chlamydiosis 3.3 7.8 3.3 7.8 3.3 7.8 3.3 7.8 3.3 7.8 3.3 7.8 high Mycoplasmosis 4.2 5.6 ------3.3 5.6 10 4.4 - Relapsing fever Borrelia 6.7 5.6 2.5 5.6 5.8 5.6 2.5 4.4 2.5 4.4 2.5 4.4 med Lyme disease Borrelia 1.7 2.2 0.8 2.2 0.8 2.2 0.8 2.2 0.8 2.2 0.8 2.2 high Bacterial airsacculitis and pneumonia 10 5.6 10 3.3 10 3.3 6.7 3.3 10 3.3 6.7 3.3 med Bacterial gastroenteritis and colitis 10 5.6 10 3.3 10 3.3 6.7 3.3 10 3.3 6.7 3.3 med Fungal diseases Aspergillosis 10 5.6 8.3 4.4 8.3 4.4 6.7 4.4 10 5.6 6.7 4.4 med Candidiasis 10 2.2 3.3 2.2 2.5 2.2 2.5 2.2 3.3 2.2 3.3 2.2 low Legend: POS – Probability of occurrence score, OIS – Outbreak impact score. Colours: green – low, yellow – medium, orange – high.

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Table 3 (cont). Outcomes of the disease risk assessment for southern African seabird colonies. Pathogen or disease Penguins Cormorants Gannets Terns Gulls Pelicans Zoonotic POS OIS POS OIS POS OIS POS OIS POS OIS POS OIS potential Protozoal diseases Avian malaria 9.2 8.9 7.5 8.9 7.5 8.9 2.5 8.9 3.3 6.7 2.5 8.9 - Babesiosis 10 5.6 10 5.6 9.2 4.4 - - 5.8 4.4 - - - Leucocytozoonosis 6.7 3.3 7.5 3.3 ------Haemoproteosis 3.3 2.2 ------10 2.2 - - - Toxoplasmosis 4.2 6.7 2.5 6.7 2.5 6.7 3.3 6.7 3.3 6.7 2.5 6.7 med Intestinal coccidiosis 7.5 3.3 6.7 8.9 2.5 3.3 3.3 3.3 2.5 3.3 3.3 3.3 - Cryptosporidiosis 10 4.4 3.3 3.3 3.3 3.3 3.3 3.3 3.3 3.3 3.3 3.3 low Parasites Stomach nematodes 10 3.3 10 3.3 10 3.3 2.5 2.2 3.3 2.2 10 2.2 - Intestinal trematodes 10 3.3 10 2.2 10 2.2 2.5 2.2 3.3 2.2 3.3 2.2 - Intestinal cestodes 10 3.3 5.8 3.3 3.3 3.3 7.5 3.3 10 3.3 3.3 3.3 - Tracheal nematodes 10 3.3 10 3.3 10 3.3 2.5 2.2 3.3 2.2 3.3 2.2 - Renal trematodes 10 2.2 10 2.2 10 2.2 7.5 2.2 3.3 2.2 3.3 2.2 - Ticks 10 5.6 6.7 5.6 3.3 5.6 3.3 5.6 3.3 5.6 3.3 5.6 low Fleas 10 3.3 6.7 3.3 3.3 3.3 2.5 3.3 2.5 3.3 3.3 3.3 low Lice 10 3.3 10 3.3 10 3.3 10 3.3 10 3.3 10 3.3 - Nasal mites 1.7 4.4 - - - - 1.7 2.2 1.7 2.2 - - - Feather mites 1.7 3.3 1.7 3.3 1.7 2.2 1.7 2.2 1.7 2.2 1.7 2.2 - Subcutaneous mites - - 6.7 3.3 3.3 2.2 - - - - 3.3 2.2 - Toxins Avian botulism 2.5 8.9 3.3 8.9 2.5 8.9 3.3 8.9 10 8.9 10 8.9 med Marine biotoxins 3.3 8.9 6.7 8.9 3.3 8.9 6.7 8.9 6.7 8.9 3.3 8.9 med Miscellaneous conditions Feather-loss disorder 6.7 2.2 ------Legend: POS – Probability of occurrence score, OIS – Outbreak impact score. Colours: green – low, yellow – medium, orange – high.

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2.4 Disease hazards of high concern

Based on the probability of occurrence and the outbreak impact scores, and disease hazards of high concern were identified and categorised in three levels: (a) high outbreak impact and medium/high probability of occurrence, (b) high outbreak impact and low probability of occurrence, (c) medium outbreak impact and high probability of occurrence.

Table 4. The disease hazards of high concern for each seabird group. Pathogen or disease Penguins Cormorants Gannets Terns Gulls Pelicans Avian pox ™ Herpesvirosis (S. American strain) ˜ Newcastle disease ˜ ˜ ˜ ˜ ˜ ˜ Avian influenza (high pathogenicity) ˜ ˜ ˜ ˜ ˜ ˜ Avian cholera ˜ ˜ ˜ ˜ ˜ ˜ Chlamydiosis ˜ ˜ ˜ ˜ ˜ ˜ Mycoplasmosis ™ Bacterial airsacculitis and pneumonia ™ Bacterial gastroenteritis and colitis ™ Aspergillosis ™ ™ ™ ™ ™ Avian malaria ˜ ˜ ˜ ˜ ˜ Babesiosis ™ ™ ™ Coccidiosis ˜ Cryptosporidiosis ™ Ticks ™ Avian botulism ˜ ˜ ˜ ˜ ˜ ˜ Marine biotoxins ˜ ˜ ˜ ˜ ˜ ˜ Legend: ˜ – High outbreak impact score with medium/high probability of occurrence; ˜ – High outbreak impact score with low probability of occurrence; ™ – Medium outbreak impact with high probability of occurrence.

3. Management options

3.1 Captive environment

Biosecurity Measures to prevent the transmission of disease within captive environments: • Provide a barrier to prevent the exposure of seabirds to synantropic (living close to human habitation and benefitting from humans, often considered pests) and wild birds, to prevent transmission of diseases such as Newcastle disease, avian influenza, chlamydiosis and avian pox. • Provide a barrier to prevent the exposure of seabirds to insects that serve as vectors of disease, such as mosquitoes and flies. • Separate groups of seabirds according to their stages of development and symptoms/illnesses so that immune-compromised individuals are not exposed to new pathogens. Ensure that personnel and equipment involved in the handling of these different groups do not move between groups and thus act as mechanical vectors.

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• Ensure that strict protocols are in place with regards to cleaning and disinfection of the pens and all equipment that comes into contact with the seabirds under care. Disinfectant products to be used should ensure that there is no build-up of resistant pathogens in the environment (for example: avian pox, Cryptosporidium). • Ensure the use of personal protective gear and hygiene routines in order to prevent the spread of pathogens from bird to bird.

Prophylaxis Prophylactic treatments to reduce the risk of transmission of pathogens or parasites: • Dust birds with an insecticide powder on admission to the centre to prevent the admission of external parasites into the facility. This can be repeated if parasites are observed while birds are under care. • Deworm birds on admission to the centre to prevent the admission of internal parasites into the facility. This can be repeated at regular intervals since reinfection may occur while birds are under care due to the presence of worms in fish. • Mosquito repellent measures can be used for individual birds as well as for pens holding birds to limit numbers of mosquitoes near to the seabirds. • Other insect repellent or killing devices and products can be installed to limit overall numbers of insects near to the seabirds. • Prophylactic treatments can be given to prevent the potential spread of disease between birds or when the likelihood is high that disease may be contracted by susceptible individuals, for example antibiotics, antifungals and nebulisation treatment. This should be done at the discretion of the veterinarian and will differ depending on the health condition of the birds and the particulars of each facility and situation.

Health screening Regular screening for disease and parasites forms the basis of the veterinary diagnostic work in terms of treating and caring for sick individuals in the centre. This also acts as a passive disease surveillance programme and signals when potential problems may occur within the captive and wild populations. This is applicable during the stay in the captive environment and also before release into the wild. • Haematocrit and the plasma protein provide a rapid and valuable assessment of the health status of the bird, and allow for the identification of the most compromised individuals that can guide rehabilitation and husbandry protocols. • Blood smears should be examined on a regular basis to detect blood parasites and haematological changes indicative of inflammatory response, allowing for treatment to be started at an early stage. • Faecal smear examination and wet preparations should be conducted periodically or on sick birds to evaluate the presence of worm eggs, coccidia, cryptosporidia, other protozoa, yeast or the overgrowth of bacteria. • Post mortem examination of all birds deceased while under care is essential to determine the cause of death and identify potential outbreaks as early as possible. • More advanced diagnostic tools such as full blood counts, biochemistry, histopathology, bacteriology, virology, endoscopy and ultrasound examination can be used in cases to determine more specific causes of disease.

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Management of stress Captivity alters the birds’ normal behaviour and therefore causes psychological and physical stress. Crowding, handling, exposure to unusual pathogens, unsanitary conditions and malnutrition are all stress factors (Ritchie et al 1994). Stress causes a change in metabolism towards the consumption of fat and protein reserves, which further debilitates the bird. Furthermore, stress hormones have an immunosuppressant effect, and as a result stressed birds are more susceptible to infectious diseases. It is therefore ideal to remove or minimise the stress factors (visual stimulation, loud noises, unnecessary handling, overcrowding of enclosures, uncomfortable ambient temperature, exposure to species potentially perceived as predators, etc.) in order to improve the birds’ ability to overcome the threat of disease while under care.

Period of quarantine It is impossible to set a specific quarantine period to rule out the presence of all pathogens before birds are released into the wild, as the incubation period can vary broadly depending on the pathogen and the health status of the birds. A period of two weeks is considered minimum in terms of evaluating a minimum of two health screening tests (blood smears, faecal smears and wet preparations, weight and physical examination) before release or translocation. It is thought that clinical signs of disease should become apparent within two weeks and also that two weeks would be sufficient time after signs of disease disappear, or treatment is discontinued, to confirm that no new clinical signs are seen. A two-week period is also recommended when captive bred individuals come into contact with conspecifics that are being rehabilitated as a way of introducing them to wild bird behaviour as well as possible exposure to microorganisms that may be present in the wild that the bird has not be exposed to before.

3.2 Wild environment

A seabird colony does not generally only house one animal species, but is a complex ecosystem including marine and terrestrial plant, insect, bird and mammal species. As a result, these interacting species need to be managed as a whole and although the management recommendations provided in this document refer only to controlling the occurrence of disease, or minimising the impacts of a disease outbreak, they must also be borne in mind with the other parts of the ecosystem that may also be affected by the disease or by the control measures implemented. In case of infectious disease outbreaks or large-scale intoxication events, it is worthwhile to monitor scavenging bird species (such as kelp gulls and great white pelicans) as these species may act as mechanical vectors, transferring infectious agents from rubbish dumps or poultry farms to seabird colonies (Assunção et al 2007) and/or may become collateral victims of the pathogen/toxin.

Carcase disposal Wildlife that have died from infectious disease are often a primary source of infection, hence the removal of these carcases is an important strategy to prevent disease transmission to other animals and to prevent the build-up of the pathogen in the environment. Carcases must be handled and transported in a manner that prevents them from releasing infectious agents into the environment or jeopardising the health of personnel (see associated document “Collecting carcases in penguin colonies” for correct handling techniques and use of protective gear). The same principles apply to both small scale and mass mortality events.

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While removing carcases, it is important to collect as much information as possible so that the extent of the mortality event can be documented, as well as collecting fresh carcases for post- mortem examination and diagnostic work. A fresh carcase can be identified by the body appearing fresh, possibly still in rigor mortis, the eyes partially sunken but not completely sunken or dried out. Carcases for post mortem examination should not be frozen but placed in the fridge and sent for examination within three days of death (preferably less than eight hours).

Heavy-duty plastic bags are required for carcase removal. Waller & Underhill (2007) provide a good example of the management of a mass mortality event in southern Africa and Friend & Franson (1999) provide detailed examples of several different methods of disposal. If local authorities or organisations have specific protocols on how to deal with carcases (especially diseased carcases), such protocols should be followed. Disposal techniques include the following options: burying at a suitable location (as determined by the organisation), incineration at the location, incineration by an approved company specializing in animal carcases, disposal by a suitable disposal company to an approved animal waste disposal site. When a controlled disease is suspected (see Appendix C), follow state veterinary protocols.

It is important that personnel do not act as mechanical vectors of a disease agent. During a mass mortality event, it is important to limit the number of people moving into the contaminated area and walking around the colony. Outer clothes (including boots and gloves) must be worn while working in the colony, and need to be removed before leaving the contaminated area. After use, these clothes can be disposed of or bagged and removed to an area where they can be washed and disinfected before re-use. In the latter case, care should be taken that the residues from disinfecting clothing and gear does not constitute a source of environmental contamination.

Removal of sick birds for rehabilitation Removing sick birds out of the area is also a management intervention that will likely decrease the amount of disease agent in the environment, as does the removal of carcases. There may be implications related to bird biology, for example: a chick with avian pox may completely recover in the wild environment without intervention, so evaluating removal (to decrease the spread of pox virus to other chicks) must be borne in mind against the parents’ pair bond relating to the success of the breeding attempt. This decision may be easier to make if the birds are in poor condition and not likely to survive. However, if removal of sick birds causes high levels of disturbance to the colony, causing increased abandonment and predation, then removal may not be the best option.

Disinfection It is good practice to routinely disinfect boots, clothing, gloves and equipment during routine monitoring work in the colony, as well as to have extra gloves used exclusively to handle carcases. Personnel should shower and change clothes before visiting another colony and should remove colony boots before driving. Visiting researchers should also be expected to follow the same protocols. In the event of a mass mortality event, disinfection of all clothing, boots and equipment is vital to limit the spread of disease as mentioned above. If an infectious disease is suspected, it is also necessary to limit the movement of people in the colony.

It is not possible to disinfect the environment except perhaps in a catastrophic event when all birds have died or have been removed. The potential impact on other species using the area should be carefully considered. State veterinary advice is likely to be needed in this eventuality.

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Human disturbance Humans may contribute to disease occurrence through causing chronic stress, acting as mechanical vectors through transporting infectious agents (clothing, boots and equipment) and disturbance causing parents not to provision their chicks adequately (causing malnourished chicks that are more prone to disease). Disturbance may very well cause disruption to the breeding cycle and increased predation that probably has much more significant impacts on the population than disease (at least in the short-term period).

It is not recommended that tourists visit a protected seabird colony except when walking on specific pathways or boardwalks. Magellanic penguins seem to habituate to tourist visitation as long as the visits are controlled (Yorio & Boersma 1992) whereas Humboldt penguins seem to be very sensitive to human presence highlighting the need for species-specific visitor management (Ellenberg et al 2006). The two mainland African penguin breeding colonies in South Africa (Stony Point and Boulders Beach) have high levels of visiting tourists on boardwalks, to which the penguins seem mostly tolerant. However, in the event of a disease outbreak, restricting or interrupting public visitation may be particularly important to prevent the spread of infectious pathogen as well as to minimize the risk of human exposure to zoonotic pathogens.

Monitoring and research activities also cause disturbance to birds for the same reasons listed above but acting as mechanical vectors may be more important due to the close contact that they have with the birds and access to more remote parts of the colony. Disinfection procedures as discussed above are therefore critical. It is recommended that each colony develops specific visitation guidelines that consider all species of seabirds breeding or roosting at the colony and bears in mind:

• Hours of visitation, • Numbers of people in the colony, • Physical access to seabirds, • Disinfection protocols, • Ability to act as mechanical vector, and • Speed and noise of visitors.

Environmental management Environmental management may or may not be possible, depending on the colony. The most important environmental management option is the removal of carcases that is discussed above. It may be necessary to analyse specific areas in a colony where disease consistently occurs (monitoring is very important to identify such patterns) and to evaluate what may be contributing to disease outbreaks in this area. Here are some ideas that may decrease the chance of disease outbreaks or decrease the occurrence of insect vectors.

• Management of poorly drained soil (to prevent damp nesting conditions), • Management of the use of burrows (some may promote the build-up of ectoparasites), • Planting of indigenous plants that may have insecticidal or mosquito repellent properties (for example, see Maharaj et al 2010 and Chalannavar et al 2013), • Clearing out of nest material in nests between breeding attempts in heavily parasitized nests, • Management of poor ventilation, • Management of the build-up of moisture and faeces,

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• The controlled use of insecticidal powder in heavily parasitized nests, • Control of standing water, especially over the summer months (breeding of mosquitoes and other insects), or treatment of the water to prevent the breeding of insects, • Prevention of decaying organic material in water bodies, and • Prevention of organic pollution (especially waste management) of water bodies.

Release environment The release environment of birds that have been rehabilitated, hand-reared or captive reared also needs to be considered in terms of what pathogens and parasites may be present that may be new to naïve individuals as well as what the environment may hold, in terms of vectors, that have the potential to spread any pathogens or parasites that the released birds may be carrying. No release site will be perfect in all aspects, but pathogen, parasite and vector considerations should be borne in mind with other factors such as age of birds and time of year.

The ongoing monitoring of birds in the release area is important to evaluate whether there has been any introduction or re-emergence of infectious diseases. Bear in mind that clinical signs may be non- specific and sometimes the only indication of disease is the death of some animals. It is critically important to monitor the number of deaths and to submit fresh carcasses for post-mortem examination to determine the cause of death, which will assist in determining possible intervention or mitigation strategies.

4. Monitoring and review

This is the ongoing process by which the disease surveillance and management measures are continuously monitored to evaluate whether results are being achieved (Jakob-Hoff et al 2014). A risk management strategy must be devised with measurable criteria against which to base decisions to continue or to modify. In general, with diseases, this monitoring revolves around continued disease surveillance and feedback from this as to the occurrence of disease and evaluation of any changes to the status quo. It is also important to realise that there is still much unknown and the discovery of “new” pathogens or an apparent increase in the frequency with which a pathogen is recorded may be related to an increased research effort or improved diagnostic technology rather than an actual disease emergence or re-emergence. In this context, the risk posed by “new” diseases must be evaluated by the different stake-holders as to interpret their relative importance (i.e. seabird colony managers, rehabilitation centres, state veterinarians, management authorities and government departments).

5. Contingency planning

Disaster management contingency planning is vital for all seabird colonies and includes contingency planning for oil spills, predation events, fire outbreaks and disease occurrence. Friend & Franson (1999) list detailed plans and lists for disease control operations that can be used to formulate these plans. Amongst others, plans should include:

• Protective gear in storage for immediate use, • Heavy duty bags and plastic containers for carcase removal,

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• Training and supervision of staff for working in a disease outbreak, especially for correct handling of carcases and disinfection protocols, • Disinfection protocols easily accessible for implementation, • Portable incinerators, if possible, or access to incineration services, • List of organisations and contacts for advice, rehabilitation centres, personnel supply and equipment needed in the event of an outbreak, and • Contact details for state veterinarians in the event of a controlled disease outbreak.

6. Conclusion

This document represents a first attempt to compile relevant information on the different pathogens and diseases that may pose a threat to seabird colonies in Southern Africa, aiming to provide a broad assessment of their risk to the bird populations and management actions that can be taken to mitigate the effects of disease. It is important to re-iterate that this is based on our best current knowledge, and is therefore limited by the existing gaps in disease research and surveillance in these species. Disease surveillance is vital to continue to diagnose causes of morbidity and mortality in different seabird species in order to continuously re-assess the risk posed by these diseases. As a result, future reviews of this document will be necessary to incorporate novel knowledge and adjust the risk assessment accordingly, as well as management mitigation measures.

Acknowledgments

NJP would like to acknowledge the fact that this document represents many years of veterinary and disease work on seabirds based at SANCCOB and in collaboration with many people involved with southern African seabird colonies and/or disease. My co-author Ralph Vanstreels has provided invaluable skills, knowledge and support in the preparation of this document. SANCCOB provided the opportunity to conduct this research especially helped by the leadership of Venessa Strauss, Margaret Roestorf and Stephen van der Spuy. This work would of course not be possible without the involvement of the conservation authorities that manage the seabird colonies; CapeNature (especially Lauren Waller, Deon Geldenhuys, Cuan McGeorge, Johan Visagie), SANParks (especially Monique Ruthenberg, Guy Padayachee, Anè Oosthuizen), City of Cape Town and Robben Island Museum (especially Mario Leshoro, Sabelo Madlala, Phakamile Zungu) as well as the Department of Environmental Affairs (especially Rob Crawford, Newi Makhado, Bruce Dyer, Leshia Visagie). Thanks to all the veterinarians and pathologists who have contributed to this large body of work: Mike Cranfield, Dave Allright, Tertius Gous, Ralph Vanstreels, Rick Last, Stephen van der Spuy, Jeanette Engelbrecht, Lindy McGregor, Natasha Ayres, Allison Tuttle, Tonya Clauss, Ellen Bronson and collaborators: Mike Peirce, Michael Yabsley, Adam Schaefer, Natasha Fleming, Venessa Strauss, Lisa Nupen, Dirk Bellstedt, Elizabeth Horne, Olivia Kane, Richard Sherley, Les Underhill. Many thanks to the many staff, interns and volunteers that helped with sample collection both at SANCCOB and in the field from SANCCOB, Mystic Aquarium and Georgia Aquarium as well as from the conservation authorities listed above. The main funders of this work over the years have been International Fund for Animal Welfare (IFAW), Hans Hoheisen Charitable Trust, National Lottery Distribution Fund, Sea Research Foundation (Mystic Aquarium), Georgia Aquarium, Leiden Conservation Foundation, National Research Foundation, Bayworld Centre for Research and Education and SANCCOB.

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Appendix A. Summary of diseases affecting southern African seabirds

This is not a definitive list of diseases affecting southern African seabirds, but a collation of knowledge from published papers including comprehensive reviews and texbooks (Clarke & Kerry 1993, Ritchie et al. 1994, Friend & Franson 1999, Thomas et al. 2007, Atkinson et al. 2008, Barbosa & Palacios 2009), a recent extensive health survey of wild African penguins (Parsons et al 2016, in press) as well as unpublished data from work conducted at SANCCOB over the last 16 years. References used are listed in the main document.

To shorten the text below, it is agreed that for the treatment and quarantine section, the following applies to all disease hazards unless otherwise stated: The health of the animal should be determined through basic tests such as haematology and physical examination before release back into the wild.

1. Viral diseases

Avian Pox Disease/pathogen and transmission: Viruses of the Avipoxvirus genus cause a variety of diseases in many different bird species and there are several different strains; some infect groups of birds while some are species specific. Transmission is through direct contact with infected birds (generally through traumatic injury) as well as biting arthropods (mosquitoes may serve as the primary vector). Presence in captive and wild populations: Avian pox has been noted in African penguins in the wild and in rehabilitation centres. Lesions have varied from mild to severe with some mortality, however most individuals recovered and the lesions resolved, some with treatment during rehabilitation and some left without treatment in the colony. There are no records of avian pox in other southern African seabird species, but the disease has been seen in seabird species worldwide. Epidemiology: Avian pox viruses penetrate damaged epithelium and cause hyperplasia of the epithelium. Infection may be limited to the epithelium or a viraemia with spread to other organs may occur. Latent pox infections can be activated by stress conditions. Rehabilitation centres may facilitate the spread of this disease through close contact of infected birds but if the lesions are treated in time to prevent secondary infection, the lesions heal well and the bird develops limited immunity. Birds may become carriers of the disease after recovery. Clinical signs: Most lesions seen in the African penguin are the mild to moderate cutaneous form with nodular lesions on the eye, beak, flipper and feet. Severe lesions may cause blindness, scarring of the eyelids and deformities and nodular lesions in the face and beak. Some birds may develop the diptheritic form of the disease, where white-yellowish plaques form in the mouth. Secondary bacterial infections are common and may cause more damage than the initial pox lesions. Diagnosis: Diagnosis is made through histologic examination of lesions as well as culture or PCR for the identification and characterisation of the virus. Treatment and quarantine: Antibiotic and supportive treatment can be given to treat secondary infections however the mild cutaneous lesions are usually self-limiting and will completely resolve if the bird can feed. It is possible that recovered birds will become carriers of the

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disease but this does not seem to be a risk due to the existence of the virus in the wild population. Prevention and control: Removal of birds with lesions to rehabilitation centres can help to limit the disease in the wild population by diminishing the source of virus for the vector population. Prevention is through vector control, separating infected and non-infected birds and decontamination of infected material with specific disinfectants aimed at killing the resistant pox virus. Vector control in the natural environment may be difficult. Zoonotic potential: There is no record of avian pox viruses successfully infecting or causing disease in humans.

Avian Herpesviruses Disease/pathogen and transmission: Avian herpesviruses have a worldwide distribution, affecting many different bird species and isolated from diseased as well as apparently healthy individuals. Transmission is through direct contact with infected birds through saliva, nasal discharge, urine, faeces and feathers. Presence in captive and wild populations: Three distinct herpesviruses are known to infect seabirds: the South African penguin strain, the South American penguin strain, and the cormorant strain. The herpesvirus-like infection documented in African penguin chicks during hand- rearing was determined to be present in the wild; diagnosis is challenging and prevalence in the wild population is unknown, with only a few confirmed cases in rehabilitated and wild carcases. There have been no reports of any herpesvirus-like deaths in other southern African seabirds. The South American penguin herpesvirus was documented at a rehabilitation centre in South America, but the source of infection remains unknown and it is possible that it could have originated from terrestrial birds. The South American strain has never been documented in South Africa and its phylogenetic relationship to the South African strain is not known. The cormorant strain was identified only once from a cormorant in Australia. Epidemiology: The viruses cause a variety of disease conditions with prolonged latent infections and concomitant infections, stress or environmental factors activating overt disease. The virus is labile in the environment and inactivated by common disinfectants. After infection, however, this virus is able to integrate with the host’s DNA and can enter latency for an indefinite period of time, which is why it is virtually impossible to consider a bird negative once it has been infected. Birds kept in captivity during rehabilitation are more likely to have outbreaks than wild populations, most likely due to stress and immune suppression caused by other diseases. Clinical signs: The lesions caused by the South African penguin strain were all related to the respiratory system and it was unclear whether the virus was a primary or secondary factor in the death of the individuals. Respiratory lesions were seen in live birds and on post-mortem examination, and only one case showed the haemorrhagic lesions that are traditionally seen in chickens with infectious laryngotracheitis. The lesions caused by the South American penguin strain were predominantly on the upper respiratory tract, with birds exhibiting marked dyspnoea with extreme discomfort. After the onset of the clinical signs, the birds refused food and did not appear to sleep or rest, dying within few days. Severe haemorrhagic and/or suppurative tracheitis, secondary bacterial airsacculitis and/or pneumonia also occurred in many cases. The cormorant strain was not associated with lesions.

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Diagnosis: Diagnosis is difficult due to lack of antibody production for serological testing as well as difficulty in viral culture and isolation from penguins in chicken eggs. Diagnosis in African penguins was based on histopathology examination and electron microscopy although no specific virus was isolated for identification. Traditional PCR testing designed for gallid herpesvirus fails to detect the infection in penguins; hence negative tests should not be relied upon. However, PCR tests using primers targeting highly-preserved sequences succeeded in identifying the virus in Magellanic penguins. Treatment and quarantine: Treatment is based on supportive antibiotic and anti-fungal treatment as well as nebulisation for birds showing respiratory signs as there is no diagnosis possible in live birds. Extra caution should be taken to isolate birds showing clinical signs once a diagnosis has been made on deceased individuals. Birds should not be released if showing any signs of disease. A quarantine period of 30 days is recommended for birds suspected of being infected with any herpesviruses. Prevention and control: In other avian herpesvirus infections, sick birds shed virus into the environment and control is aimed at “depopulation”, however, there is indication that the South African penguin strain naturally circulates in wild populations and therefore such measures would be too aggressive. More conservatively, it is recommended that sick birds are removed for rehabilitation. Prevention protocols include thorough disinfection of the premises and limiting contact of susceptible birds with possibly infected birds. Outbreaks causing mortality are possible in the wild and establishing cause of death is priority as well as decontamination/quarantine of the area. Zoonotic potential: There is no record of avian-infecting herpesviruses successfully infecting or causing disease in humans.

Newcastle Disease Disease/pathogen and transmission: Newcastle disease is caused by an avian paramyxovirus-1 virus with different strains of the virus causing different severity of disease. The virus is transmitted by inhalation or ingestion of contaminated material and is highly contagious. Mechanical vectors such as wind, insects, equipment and humans may help to spread the virus. Presence in captive and wild populations: The Newcastle disease virus is capable of infecting a wide range of avian species and is seen worldwide. Antibodies to the virus have been seen in African penguin, Cape gannet and cormorant species in southern Africa and the virus has been isolated in Cape cormorant and African penguin carcases although no large mortality events have been described. The virus is therefore present in the wild, probably at low prevalence in multiple seabird species. Epidemiology: There have been several large-scale illness and mortality events reported especially in cormorant breeding colonies in North America and in captive or pet birds worldwide. In an outbreak, morbidity may affect 100% of the colony but mortality is generally lower. Clinical signs: Sick birds may present sudden death, neurological lesions (seizures, torticollis, ataxia and paralysis), greenish diarrhoea or respiratory disease. There are only non-specific lesions on post-mortem examination and histologic lesions are largely variable. Diagnosis: Tracheal and cloacal swabs can be taken from live birds and swabs from organs can be taken from dead birds. The first step in diagnosis is running a screening PCR test for the virus, if this is positive then further PCR tests can be done to determine virulence and then virus isolation, culture and sequencing need to be done to fully characterise the virus isolated.

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These tests are done at a state veterinary laboratory and determine whether the strain of virus poses a risk for poultry. Treatment and quarantine: Newcastle disease is generally only diagnosed on death and therefore treatment is not given. The state veterinarian needs to be consulted before birds that are serologically positive are released back into the wild. Prevention and control: The disease is a controlled disease in South Africa (due to the economic importance in the poultry industry) and a state veterinarian must be notified on occurrence. Large amounts of virus are shed in the faeces of infected birds and contaminate the environment. It is vital that carcases are removed and incinerated and that there are strict measures to prevent human spread of the virus. If birds were sent for rehabilitation and diagnosed after death, then follow up with the areas where they were found is important. Zoonotic potential: Newcastle disease can cause a self-limiting conjunctivitis and mild flu-like symptoms in humans.

Avian Influenza Disease/pathogen and transmission: Type A influenza viruses generally cause an inapparent viral infection of wild birds maintained by the faecal-oral route of transmission. There are different subtypes of the virus with two main types of antigens: haemagglutinin (H) and neuraminidase (N). Subtypes H5 and H7 can be classified as “high pathogencity avian influenza” (HPAI) depending on the amino-acid sequence of the haemagglutinin cleavage site; H5 and H7 without the specific cleavage site and the remaining subtypes (H1-H4, H6 and H8-H13) are classified as “low pathogenicity avian influenza” (LPAI). Presence in captive and wild populations: There were no positive cases when testing for H5 and H7 in a serological health survey of African penguins, Cape cormorants and Cape gannets between 2010 and 2013, nor have there been any positive cases on seabirds under care or carcases submitted to SANCCOB for post-mortem examination in recent years. There are no records of HPAI infecting seabirds worldwide to date, however LPAI is widely distributed and known to occur in humans and poultry in South Africa. Epidemiology: There are many different virus subtypes found worldwide that have differing virulence in different bird species. Shorebirds, ducks and teals play a key role in the maintenance of LPAI, serving as asymptomatic carriers. Because different strains of the virus can reorganize their genome and mutations are common, however, the potential exists for a sudden shift of a LPAI strain into an HPAI strain. Clinical signs: LPAI are thought to be non-pathogenic to seabirds. In domestic birds, HPAI can cause rapid and severe outbreaks of respiratory disease, with secondary effects on the enteric or reproductive tracts. There are no specific post-mortem lesions. Diagnosis: Tracheal and cloacal swabs can be taken from live birds and swabs from organs can be taken from dead birds for virus isolation and PCR determination of the virus and subtype. Pathogenicity of the virus is determined through inoculation tests. These tests are done at a state veterinary laboratory and determine whether the subtype of virus poses a risk for poultry. Treatment and quarantine: HPAI is generally only diagnosed on death and therefore treatment is not given. The state veterinarian needs to be consulted before birds that are serologically positive are released back into the wild.

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Prevention and control: The disease is a controlled disease in South Africa and a state veterinarian must be notified on occurrence. This is mainly important to determine the effect on the poultry industry. Control of the disease in the wild bird population is not possible due to the widespread prevalence of many different serotypes. Zoonotic potential: Most influenza strains circulating in human do not cross-transmit to wild birds, and most LPAI strains are not of significant concern to human health. HPAI strains, however, can cause severe respiratory disease, with high lethality.

West Nile Disease Disease/pathogen and transmission: West Nile virus is a mosquito-borne virus that circulates among birds and is transmitted by mosquitoes, especially Culex species, but other arthropods may also be involved. Presence in captive and wild populations: Wild birds are the main reservoir hosts for west Nile virus. It has mostly been reported in passeriformes, shorebirds, hawks, eagles and owls although not all birds show clinical signs. There have been some reports of disease in seabird species such as cormorants, gulls and pelicans but not in southern Africa although it has been reported in ostriches in South Africa. Epidemiology: Birds are the primary hosts but mosquitoes can transmit the virus to mammals (mostly horses and humans). Some birds may shed the virus in the faeces but the virus does not persist in the environment. Clinical signs: A variety of clinical signs have been reported with anorexia, lethargy, neurological signs (ataxia, paralysis, blindness) as well as sudden death or no clinical signs. Multi-organ haemorrhages, splenomegaly, hepatomegaly are seen on post mortem examination while histological lesions seen are non-specific inflammatory reactions in the different organs. Diagnosis: Serology can detect the virus in live birds (not confirmed that this test is available in South Africa). Virus culture and isolation as well as molecular methods (PCR) are recommended from carcases. Treatment and quarantine: No treatment is available but birds can recover if given supportive care. There is an incubation period of 5 days in birds so a quarantine period of two weeks should be adequate. Prevention and control: Control measures should prevent exposure to mosquitoes: repellents, fans, screening or netting, insecticides, elimination of standing water, etc. Zoonotic potential: West Nile disease is a serious disease in people and presents as a fever with flu- like symptoms or a neurological disease with encephalitis, meningitis or paralysis. Both forms can be life-threatening. It is considered an endemic disease in humans in South Africa.

Eastern Equine Encephalitis Disease/pathogen and transmission: Eastern equine encephalitis is caused by a togavirus that is transmitted by mosquitoes and is maintained among wild birds. Presence in captive and wild populations: This virus infects a wide range of wild birds and has been reported in gull species but no other seabird species worldwide. It has been recorded in captive African penguins. Epidemiology: This is an endemic disease in a mosquito-wild bird cycle usually associated with freshwater marshes and mortality has generally been limited to captive-rearing situations. Horses are highly susceptible to the virus and they often die from the infection.

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Clinical signs: Clinical signs include depression, tremors, paralysis and ataxia. Gross pathology lesions include ascites, hepatomegaly, splenomegaly and visceral gout. Histology shows an inflammatory response in the brain. Diagnosis: Serology can be done on live birds (not confirmed that this test is performed in South Africa) and virus isolation can be done from bird carcases. Treatment and quarantine: No treatment is available but birds can recover if given supportive care. The incubation period in birds is unknown but clinical signs are seen in humans 5-10 days after being bitten by the infected mosquito. Prevention and control: Control measures should prevent exposure to mosquitoes: repellents, fans, screening or netting, insecticides, elimination of standing water, etc. Zoonotic potential: Humans generally get infected after horses have been infected. It can be a severe disease with a high mortality rate and often causes permanent neurological disorder in patients that recover. However, seabirds are probably unlikely to become significant sources of infection.

Avian Reovirus Disease/pathogen and transmission: Reovirus infections are ubiquitous in poultry flocks worldwide, mainly causing an arthritic disease and spread through vertical and horizontal transmission. Presence in captive and wild populations: Reoviruses are seldom reported in wild birds but are ubiquitous in the poultry industry. A reovirus was reported in captive African penguins but it was unclear what role the virus played in the deaths of the birds. There have been seropositive results for this virus in African and rockhopper penguins. Epidemiology: Both vertical (through the egg) and horizontal transmission (bird to bird) are recognised. The virus is spread mainly through the faecal-oral route but can also spread through the respiratory tract and through broken skin. Chicks are more susceptible than older birds. Clinical signs: In chickens, the main lesion is swelling of the hock joints causing lameness. There is low morbidity and mortality. African penguins that died in a zoo were found to be positive with reovirus but it is unclear what role the virus played in their deaths. Diagnosis: Serology is routinely performed in the poultry industry and virus isolation and molecular methods (PCR) can confirm the presence of the virus. Treatment and quarantine: There is not enough known about the disease in wild birds to formulate treatment and quarantine regimes. Chickens show viraemia 30hours after inoculation. Prevention and control: The virus is ubiquitous in the poultry industry and control is aimed at vaccination, good management and biosecurity measures. Prevention and control in seabirds would be to prevent access to domestic birds, especially chickens and to ensure adequate biosecurity between poultry farms and seabird colonies. Zoonotic potential: There is no record of avian reoviruses successfully infecting or causing disease in humans.

Infectious Bursal Disease Disease/pathogen and transmission: Infectious bursal disease is caused by a birnavirus and is widespread in the poultry industry. There are two serotypes of the virus with serotype 1 causing disease in chickens and serotype 2 recorded in captive penguins that died. Mode of transmission is primarily through faecal oral route, with aerosol spread considered to be less important.

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Presence in captive and wild populations: Infectious bursal disease is widespread in the poultry industry but is also reported in other gallinaceous wild birds, crows, sparrows and pigeons. There have been reports of seropositive African penguins as well as other penguin species. African penguins captive in a North American zoo died with birnavirus isolated from the carcases. Epidemiology: The disease is subclinical in wild birds and they act as reservoirs of the virus. The disease is highly contagious in chickens. Clinical signs: In chickens, the virus causes immunosuppression and mortality in chicks. The main clinical signs are watery diarrhoea, lethargy and anorexia. Post-mortem lesions include numerous ecchymotic haemorrhages on the muscles and enlarged, turgid bursa of Fabricius with haemorrhages present and, in some cases, the bursa may be completely haemorrhagic. African penguins that died in a zoo were found to be positive with birnavirus but it is unclear what role the virus played in their deaths with none of the characteristic lesions present. Diagnosis: The combination of characteristic signs and post-mortem lesions are indicative of this disease but laboratory confirmation can be carried out by serology and molecular methods (PCR). In the absence of such tests, histological examination of the bursa may be helpful. Treatment and quarantine: In wild birds the disease reported has been subclinical and therefore no treatment is necessary. In the event of positive cases showing clinical signs, treatment would be supportive, especially to prevent secondary infection due to immunosuppression. There is an incubation period of 2-3 days in chickens; therefore a quarantine period of two weeks is sufficient. Prevention and control: Prevention and control in seabirds would be to prevent access to domestic birds, especially chickens and to ensure adequate biosecurity between poultry farms and seabird colonies. Zoonotic potential: There is no record of birnaviruses successfully infecting or causing disease in humans.

Other viruses Even though seropositve results were obtained for African penguins tested for Avian Encephalomyelitis Virus (Tremovirus) and Infectious Bronchitis Virus (Gammacoronavirus), there is no evidence to indicate that these agents are successful infecting penguins or other seabirds, and therefore they were not included in the assessment.

2. Bacterial diseases

Avian Cholera Disease/pathogen and transmission: Avian cholera, or pasteurellosis, is caused by the bacterium Pasteurella multocida, of which there are several different serotypes and variants. Environmental contamination from diseased birds is the primary source for infection and is transmitted through ingestion, bird-to-bird contact, aerosol transmission and in the water. Presence in captive and wild populations: Avian cholera is well known to cause severe mortality events in southern Africa especially in Cape cormorant populations, but also affecting other seabird species in smaller numbers. Large-scale mortality of ducks, skuas and penguins due to avian cholera has also been documented elsewhere. It is not seen in captive populations apart from a few cases seen in seabirds undergoing rehabilitation. It is likely that most cases are

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serotype 1 but pathogenicity is determined by evaluation of surface proteins and determining strains has not been done in South Africa. Epidemiology: The bacterium is highly infectious and persists in the environment but it is not always evident why there are outbreaks in some years and not in others. Outbreaks generally occur during the breeding season when large numbers of birds are in close contact and the infection spreads rapidly throughout the colony. It is unclear whether nutritional stress and infection with other bacteria plays a part in the severity of an outbreak or not. Clinical signs: Avian cholera is generally identified when there are higher than average deaths in a colony, especially of birds in good or breeding condition. Clinical signs seen are mostly neurological with lethargy, “tameness”, convulsions and throwing head back before death. Post-mortem lesions include good body condition, haemorrhages on the heart, pale spots on the liver, generalised congestion and haemorrhages. In some cases, however, no post-mortem lesions may be apparent at all. Diagnosis: Fresh carcases sent for post-mortem examination and bacterial culture is needed to confirm a diagnosis. Serotyping can be done at the ARC Onderstepoort Veterinary Institute however it is unknown whether any laboratory in South Africa is doing PCR evaluation of the surface proteins to characterise different strains. Treatment and quarantine: In acute outbreaks, birds normally die within 24 hours of showing symptoms and therefore treatment is not an option. Disposal of the carcases is important to limit the spread of the disease. It is possible that some birds become disease carriers but show no symptoms and it is therefore difficult to identify these individuals. Prevention and control: Carcase collection and incineration is the best control of the disease as well as to prevent further losses. Removing carcases prevents environmental contamination as well as decreasing the amount of scavenging of infected carcases. If the outbreak seems to be confined to areas near freshwater bodies, hazing and deterrence techniques may be used to restrict the access of birds. It is important to be aware of disturbance of other species of birds in the colony during management of an avian cholera outbreak. Zoonotic potential: Although humans can be infected by Pasteurella multocida, it is largely established that the serotypes involved in seabird infections are not the same as those that cause disease in humans. Skin infections may result from bites and scratches and respiratory infections may result from confined spaces and limited air movement.

Chlamydiosis Disease/pathogen and transmission: Chlamydiosis, or psittacosis, is caused by the bacterium Chlamydophila psittaci. There are different strains of this bacterium and different bird species have different levels of susceptibility. The organism is excreted in faeces and nasal discharges (remaining infective for several months) and infection occurs through direct contact with infected birds as well as through inhalation of infected exudates, faecal matter or dust. Presence in captive and wild populations: This pathogen has been occasionally recorded in pet birds in South Africa, but its occurrence in wild populations of southern African seabirds has yet to be recorded. However, outbreaks in North American zoos demonstrate that African penguins are susceptible to this disease and it is frequently recorded in waterbird species and occasionally recorded in gulls and terns. Epidemiology: Chlamydiosis is seen in birds worldwide and is a serious disease especially in captive parrots. There are healthy carriers and latent infections within bird populations with any form

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of stress (particularly in captivity) or concurrent infections triggering the onset of clinical signs and causing shedding of the bacterium, potentially leading to an outbreak of disease. Clinical signs: The disease may be inapparent or show acute, subacute or chronic infection and may be fatal in susceptible species. Clinical signs include weakness, anorexia, ruffled feathers, purulent eye and nare discharges, diarrhoea and laboured breathing. There may be cases of mortality with birds in poor condition. Hepatomegaly and splenomegaly may be seen on post- mortem examination. Diagnosis: Diagnosis is through isolation or culture of the pathogen from tissues of infected birds. A PCR test is available in South Africa for use on swabs taken from infected tissues. Treatment and quarantine: Long-term treatment with tetracyclines is necessary in acutely ill birds; however the antibiotics are not effective against latent infections. It is unknown whether antibiotic treatment completely clears the infection and therefore releasing birds back into the wild may not be recommended. There is an incubation period of at least 40 days but may extend for much longer, which makes determining a quarantine period virtually impossible. Prevention and control: Birds showing clinical signs should be removed from the colony and sent for rehabilitation. Chlamydiosis is a controlled disease in South Africa and a state veterinarian should be notified on the occurrence and diagnosis of disease. Prevention in captivity is achieved through the separation of infected birds and thorough disinfection of equipment and facilities coming into contact with them. During an outbreak, collection and incineration of carcases will help to limit the spread of the organism. Zoonotic potential: Chlamydiosis is a relevant disease to humans, leading to respiratory disease that can be potentially severe and even cause death. The bacterium is spread through inhaling airborne avian faecal material and in the event of the disease occurring, masks or respirators should be worn by personnel and dusty areas with bird droppings can be wetted down with a bleach solution.

Mycoplasmosis Disease/pathogen and transmission: Mycoplasmosis is caused by Mycoplasma bacteria, in particular Mycoplasma gallisepticum and M. synoviae although there are many different species and different strains. Transmission occurs through bird-to-bird contact, aerosol transmission via dust or droplets, contact with contaminated surfaces and through the egg. Presence in captive and wild populations: Serological testing of wild African penguins and Cape gannets has shown antibodies to M. gallisepcticum and M. synoviae. Mycoplasma spp. have also been reported in the faeces of the great white pelican although the clinical significance of these strains is not clear. There are no records of deaths attributed to Mycoplasma infections in southern African seabirds. Epidemiology: Mycoplasmosis is mostly seen in chickens and other gallinaceous bird species although it has been isolated in a wide range of bird species worldwide. The importance of the majority of strains is unknown. Infection often occurs through contact with an infected carrier bird causing disease outbreaks, especially in species that form large breeding colonies or roost together in large flocks. Clinical signs: In domestic birds, mycoplasmosis may lead to lethargy, respiratory distress (sinusitis, airsacculitis, laboured breathing), decreased egg production and death; however other bird species also show arthritis and synovitis. Sinusitis, airsacculitis and pneumonia may be seen on post-mortem examination but no distinct lesions are seen histologically.

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Diagnosis: Culture of the bacterium is difficult and swabs from eyelids or sinuses should be inoculated on selective media in the laboratory. Treatment and quarantine: Treatment with erythromycin, spectinomycin and clindamycin is recommended with treatment designed to allow birds to recover, not to eliminate the bacterium. Birds surviving the infection may become carriers of the infection and therefore release back into the wild may not be recommended. It is therefore vital that a positive diagnosis is made. If release is considered, a quarantine period of three weeks is recommended after treatment has stopped (incubation period of MG in poultry species varies from 1-3 weeks). Prevention and control: Birds showing clinical signs should be removed from the colony and sent for rehabilitation. Prevention is through separation of infected and non-infected birds and thorough disinfection in captivity. Zoonotic potential: There is no record of M. gallisepticum or M. synoviae successfully infecting or causing disease in humans.

Relapsing Fever Borrelia Disease/pathogen and transmission: The relapsing fever Borrelia species are blood spirochaetes that have been described in several species including the African penguin. The parasite is tick- borne and generally spread by soft ticks, and Carios capensis is particularly relevant for seabirds. Presence in captive and wild populations: There is a low prevalence of Borrelia in African penguins being seen more commonly in chicks and juveniles compared to adults. The spirochaete may be noticed in birds in rehabilitation but is also present and spread in the wild population, especially in areas with high tick burdens. There is likely also low prevalence in other seabird species with records in Cape gannets and southern giant petrels. Epidemiology: Seabird ticks (especially the soft tick) are found together at all southern African seabird colonies, providing the opportunity for inoculation of seabird species with this bacterium. The pathogenicity in the endemic seabird species is unknown but it may contribute to morbidity with concurrent infections, especially in immune-suppressed individuals. Clinical signs: Clinical signs may be inapparent with non-specific signs such as lethargy, anaemia, fever and neurological signs. Post-mortem lesions of splenomegaly and hepatomegaly can be seen and confirmed with histological findings. Diagnosis: Diagnosis can be made of the spirochaete on blood smear evaluation; however determining whether this is causing clinical disease is difficult. Histopathology may confirm whether borreliosis/spirochaetosis is the cause of death. Specific diagnosis of the spirochaete species can be done using molecular methods (PCR). Treatment and quarantine: Treatment of birds showing clinical signs can be given with penicillins or tetracyclines; although treatment should not be given with a high parasitaemia as the sudden liberation of spirochaetal degradation products can cause mortality. Control of all ecto- parasites with insecticide on birds admitted for rehabilitation will limit further exposure. Prevention and control: Management control of ecto-parasite load may be justified in the colonies, if there is cause for concern; this may entail use of insecticide powder, evaluation of burrows and the use of vegetation to minimise the levels of ecto-parasites. Zoonotic potential: Relapsing fever is a significant disease for humans, however it is currently unknown whether the species occurring in southern African seabirds can infect humans or if

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different strains are involved. Nonetheless, precautions should be taken in the field to limit exposure to tick bites. Symptoms of relapsing fever include fever, headache, fatigue, skin rash, muscle pain and joint pain.

Lyme Disease Borrelia Disease/pathogen and transmission: The Lyme disease Borrelia species are blood spirochaetes that have been described in several species of mammals and birds. The parasite is tick-borne and generally spread by hard ticks, and Ixodes uriae is particularly relevant for seabirds. Presence in captive and wild populations: Seabirds are known to play a key role in the long-term maintenance of Lyme disease Borrelia. It has been recorded in seabirds worldwide, but has yet to be recorded in seabirds in South Africa. Epidemiology: Hard ticks are found occasionally at southern African seabird colonies, providing the opportunity for inoculation of seabird species with this bacterium. Clinical signs: Lyme disease Borrelia species do not appear to cause clinical disease in seabirds. Diagnosis: Diagnosis can be made through serological testing or through molecular testing (PCR) of blood or tissues. Treatment and quarantine: The disease is not significantly pathogenic to seabirds, and there is no need to treat them. However, eliminating ticks with insecticide powder and treatment of birds with penicillins or tetracyclines may be an option to reduce the risk of human exposure. Prevention and control: Management control of ecto-parasite load may be justified in the colonies, if there is cause for concern; this may entail use of insecticide powder, evaluation of burrows and the use of vegetation to minimise the levels of ecto-parasites. Zoonotic potential: Lyme disease is a significant pathogen for humans, and the strains carried by seabirds are genetically compatible with those causing disease in humans. Symptoms of Lyme disease include fever, headache, fatigue, skin rash, muscle pain and joint pain. Precautions should therefore be taken in the field to limit exposure to tick bites.

Bacterial Airsacculitis and Pneumonia Disease/pathogen and transmission: Several bacteria species can cause acute to chronic respiratory disease. Many of these bacteria are commensal gastrointestinal bacteria that can become opportunistic pathogens in immune-compromised individuals. Presence in captive and wild populations: Bacterial airsacculitis and pneumonia is a significant cause of mortality in abandoned African penguin chicks admitted for hand-rearing at rehabilitation centres. It is also a common cause of mortality seen in seabird carcases admitted from the colonies for post-mortem examination. Epidemiology: Birds may be immunocompromised due to their age (chicks) and poor condition (abandoned, nutritional stress, arrested moult) in the wild and when admitted for rehabilitation, they face additional handling stress. Clinical signs: Birds with respiratory infections show laboured or heavy breathing (panting) (especially when the weather is not excessively hot) and occasional coughing; however clinical signs may be non-specific such as delayed growth, poor appetite or reclusive behaviour. Deaths are normally seen in individual cases rather than mass mortality, however many deaths may be seen when birds are in poor condition. Carcases may be found in a stretched out position with the neck extended and beak open. Infection with exudate in the airsacs and/or severe pneumonia is apparent on post-mortem examination.

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Diagnosis: Clinical signs are indicative of infection and can be confirmed with auscultation of the chest or radiographic evaluation. Large numbers of monocytes and/or toxic heterophils in blood smears may be considered suggestive. However, often sick birds may successfully hide all clinical signs and the diagnosis will only be made on post mortem examination. Bacterial culture and identification is possible with tracheal swabs or swabs of air sacs or lungs, allowing for the causative agent to be identified; an antibiogram may also be valuable to select the best antibiotic for treatment and identify antibiotic-resistant strains. Treatment and quarantine: Treatment of positive cases should be attempted with antibiotic treatment and nebulisation. Concurrent treatment with antifungals to prevent the establishment of aspergillosis is also recommended. If the bird has been treated for a respiratory infection, there should be at least two weeks after the treatment was concluded in which there are no clinical signs and the bird is healthy in all other aspects so that it can be considered fit for release. Prevention and control: Prevention is dependent on reducing the predisposing stress factors; in captive environments these may include overcrowding, malnutrition, poor ventilation and poor cleaning. Thorough disinfection of enclosures and handling equipment is important, with regular environmental audits done to determine the presence of problem bacteria. Prevention in the natural environment may need some analysis of the areas affected with an increased occurrence of disease and an evaluation of why these areas are problematic. Possible causes could be poor drainage of soil and poor ventilation with build-up of moisture and faeces, especially in nesting areas. In particular, nest type and material (including artificial nests) should be evaluated in terms of their ventilation and drainage. Removal of sick birds to rehabilitation centres will limit the spread of any contagious disease in the natural environment. It is important that health checks are done on rehabilitated birds before release back in the wild in order to control any introduction of a pathogenic or resistant strain of bacteria. Release sites should be monitored for increased mortality. Zoonotic potential: Many of the opportunistic bacteria that cause airsacculitis and/or pneumonia in birds may also cause significant respiratory disease in humans, especially in immune- compromised individuals.

Bacterial Gastroenteritis and Colitis Disease/pathogen and transmission: Several bacteria species can cause acute to chronic infection. Many of these bacteria are commensal gastrointestinal bacteria that become opportunistic pathogens in immune-compromised individuals. Presence in captive and wild populations: Bacterial gastro-enteritis is a significant cause of mortality in abandoned chicks admitted for hand-rearing at rehabilitation centres. It is also a cause of mortality seen in seabird carcases admitted from the colonies for post-mortem examination. Epidemiology: Birds may be immunocompromised due to their age (chicks) and poor condition (abandoned, nutritional stress, arrested moult) in the wild and when admitted for rehabilitation, they face additional handling stress. They then become susceptible to bacteria that are opportunists or contaminants in the natural environment as well as increased bacterial load in the artificial environment. If an animal is immune compromised, normal intestinal bacteria may become pathogenic. Clinical signs: Birds with gastro-intestinal disease may show diarrhoea (watery or smelly faeces instead of thicker, pasty, brown to green faeces with watery white urates), regurgitation and

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fouling of feathers around the cloaca; however clinical signs may be non-specific such as delayed growth, poor appetite or reclusive behaviour. Deaths are normally seen in individual cases rather than mass mortality, however many deaths may be seen when birds are in poor condition. Lesions in the gastro-intestinal system may or may not be apparent on post mortem examination. Diagnosis: Cilinical signs are indicative of infection and a faecal smear may show an overgrowth of bacteria. Bacterial culture and identification is possible with faecal samples or post-mortem intestinal swabs, allowing for the causative agent to be identified; an antibiogram may also be valuable to select the best antibiotic for treatment and identify antibiotic-resistant strains. Treatment and quarantine: Treatment of positive cases should be attempted with antibiotic treatment and supportive treatment. If the bird has been treated for a gastro-intestinal infection, there should be at least two weeks after the treatment was concluded in which there are no clinical signs and the bird is healthy in all other aspects so that it can be considered fit for release. Prevention and control: Prevention is dependent on reducing the predisposing stress factors; in captive environments these may include overcrowding, malnutrition and poor cleaning. Thorough disinfection is important, with regular environmental audits done to determine the presence of problem bacteria. It is unlikely that prevention is possible in the natural environment. Removal of sick birds to rehabilitation centres will limit the spread of any contagious disease in the natural environment. It is important that health checks are done on rehabilitated birds before release back in the wild in order to control any introduction of a pathogenic or resistant strain of bacteria. Release sites should be monitored for increased mortality. Zoonotic potential: Many of the opportunistic bacteria that cause gastro-intestinal infections in birds may also cause significant gasto-intestinal disease in humans, especially in immune- compromised individuals.

3. Fungal diseases

Aspergillosis Disease/pathogen and transmission: The fungi Aspergillus fumigatus (most frequent) and Aspergillus flavus (uncommon) are responsible for a predominantly respiratory disease that can be peracute, acute or chronic. The fungus grows in damp soils, decaying vegetation and organic debris and releases spores that are inhaled and then disseminated from the respiratory system to other parts of the body. Presence in captive and wild populations: Fungal airsacculitis and pneumonia, most likely caused by Aspergillus spp., is a significant cause of death in rehabilitation and permanent captivity. There is a high prevalence in rehabilitation as the birds are compromised due to oiling, injury, concurrent disease or chicks being hand-reared. Fungal infection is also a common cause of mortality in seabird carcases admitted from the colonies for post-mortem examination. Epidemiology: The organism is ubiquitous in the environment and infections mainly occur secondarily to an immunosuppressive event but can also occur due to high levels of spores present in the natural environment. It is likely to affect young or old birds, particularly in moist or dusty, poorly ventilated and overcrowded areas.

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Clinical signs: In chronic cases, the bird is emaciated and shows laboured breathing and lethargy. In acute cases, there may be no symptoms other than sudden death of individuals. Post-mortem examination shows typical lesions of plaques, fungal growth and in systemic cases, disseminated nodules are seen in parenchymatous organs. There can be destruction of adjacent tissue including bone and blood vessels (often with extensive haemorrhage). Diagnosis: Fungal infection is apparent on post-mortem examination but definitive diagnosis is based on fungal culture (from a specific lesion) and/or histopathology. Nasal swabs may be taken from a live bird but a positive culture is not diagnostic as the organism is ubiquitous in the environment. Treatment and quarantine: Treatment of positive cases should be attempted with anti-fungal treatment, nebulisation and possible surgical debridement. A quarantine period is difficult to define due to a variable incubation period (several days to months), vague clinical signs and often a lack of a definitive diagnosis. Prevention and control: Prevention is dependent on reducing the predisposing stress factors; in captive environments these may include overcrowding, malnutrition, poor ventilation, antibiotic therapy, respiratory irritants, concomitant disease and moist nesting material. Careful cleaning and disinfection is also important. Prevention and control in the wild is dependent on management of nest sites with perhaps supplying artificial burrows and management of damp areas and the presence of organic debris. Zoonotic potential: Humans are also susceptible to aspergillosis, which manifests itself as a severe respiratory infection; however, it is generally limited to severely immune-compromised individuals.

Candidiasis Disease/pathogen and transmission: Candidiasis is caused by the yeast Candida albicans and is a common environmental organism and normal inhabitant of the gastro-intestinal system. It is transmitted through ingestion of food and water. Presence in captive and wild populations: The occurrence of disease in wild populations is unknown but it is seen in chicks (African penguins and cormorant species) being hand-reared in captivity. Disease likely occurs in immune-compromised individuals in the wild. Epidemiology: C. albicans is a normal inhabitant of the gastro-intestinal system and only causes disease secondarily to an immuno-suppressive event or in immune-compromised chicks. It can be a primary cause of infection or it can be a secondary pathogen that takes advantage of a damaged gastro-intestinal epithelium. Clinical signs: Chicks show stunted growth and ruffled feathers with circular, raised, ulcerative lesions in the mouth and oesophagus. It is generally restricted to birds in poor condition and/or those that have concurrent disease. Diagnosis: Faecal smears and impression smears of lesions showing the presence of yeasts is not diagnostic but large numbers of budding yeasts are presumptive for candidiasis. Histologic evaluation of biopsy or post-mortem samples is necessary to confirm that the yeast is causing pathologic changes. Treatment and quarantine: Affected birds need supportive treatment to resolve predisposing factors as well as anti-fungal treatment. The symptoms may clear up with supportive treatment and improvement in the bird’s overall condition even without anti-fungal treatment.

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Prevention and control: The occasional occurrence of the disease does not warrant control. Prevention, especially during hand-rearing is to reduce the predisposing stress factors such as overcrowding, malnutrition, antibiotic therapy and concomitant disease as well as thorough disinfection. Zoonotic potential: Immune-compromised humans can also develop candidiasis, however it is unlikely that birds should be significant sources of infection since this fungus is ubiquitous and the development of the disease is primarily related to the immune status rather than to exposure to the pathogen.

4. Protozoal diseases

Avian Malaria Disease/pathogen and transmission: Avian malaria is caused by the protozoan Plasmodium species and the vector is the Culicine species mosquito. Presence in captive and wild populations: High prevalence and mortality of African penguins due to avian malaria has been recorded in captivity and mortality occurs in different seabird species during rehabilitation. There is lower prevalence of avian malaria in the wild African penguin population and Plasmodium infections have also been recorded in wild Cape cormorants and Cape gannets. Research still needs to be done to determine the different species of Plasmodium occurring in wild populations of southern African seabirds. Avian malaria is likely to be present at any seabird colony where there are culicine mosquito species. Epidemiology: Most Plasmodium species are generalist parasites, and may have many competent mosquito hosts as well as many competent avian hosts. Some bird species are very susceptible to Plasmodium infections, for example penguins, possibly due to the fact that these species did not evolutionarily coexist and therefore did not develop natural immunity. Avian malaria does not generally cause mass mortality in seabird colonies but is more likely to cause individual mortality related to the occurrence of mosquitoes (temperature and rainfall conditions), level of immunity of the avian hosts and recrudescence of a latent infection. Clinical signs: Signs of illness are mostly absent except in susceptible species, but may include lethargy, anorexia, regurgitation and convulsions. Often the only sign of disease is sudden death. Post-mortem examination shows generalised congestion, with marked splenomegaly, lung congestion and often hydropericardium. Diagnosis: Blood smear evaluation is the standard diagnostic tool for diagnosing Plasmodium in a live animal although there is the possibility of a false negative diagnosis. Post-mortem lesions (hydropericardium, hepatomegaly, splenomegaly) are fairly specific and can be confirmed with histopathology evaluation and tissue impression smears. It may be difficult to differentiate this parasite from Haemoproteus in blood smears; the key difference is that Plasmodium presents erythrocytic meronts whereas Haemoproteus does not.Other diagnostic tools such as molecular diagnostic work and gene sequencing are currently only used for research purposes in South Africa. Treatment and quarantine: Treatment is given in rehabilitation and captive centres (primaquine, chloroquine and trimethoprim-sulfonamides) reducing morbidity and mortality but does not clear latent tissue parasites. There is a pre-patent period of at least 5-7 days in most Plasmodium species from inoculation by the infected mosquito to the emergence of the first erythrocytic parasites. It is therefore reasonable to have a quarantine period of at least two

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weeks with blood smears being evaluated for parasites at the end of each week, in order to detect new and relapsing/recrudescing infections. Prevention and control: Prevention of contact between natural avifauna, mosquitoes and susceptible birds is necessary. It is recommended that all seabirds in open air enclosures (especially penguin species) are kept in netted enclosures to minimise this contact. Fans, or windy conditions (interfering with mosquito flight), mosquito repellents and prophylactic treatment are other methods to use in captive environments. Contact between mosquitoes and seabirds is impossible to prevent in the wild. As long as there is standing water and other bird species in or near to a seabird colony, the threat of exposure to Plasmodium exists. Once diagnosis is confirmed in carcases from a colony, the only management option is to try and limit the presence of mosquitoes through eliminating any standing water. Zoonotic potential: There is no record of avian-infecting Plasmodium successfully infecting or causing disease in humans.

Babesiosis Disease/pathogen and transmission: Babesia spp. are tick-transmitted piroplasm parasites. There are 16 recognized species in different bird species, among which B. peircei has been described in penguins, B. ugwidiensis in cormorants and B. bennetti in gulls. The species infecting gannets has not been characterised yet, but is likely to correspond to B. poelea, the species that occurs in boobies (Sula spp.). It is not clear the relative roles that the hard tick Ixodes uriae and the soft tick Carios capensis play in the transmission of the parasite. Presence in captive and wild populations: Babesia species occur endemically in various seabird species in southern Africa. Babesia infections are seen at high prevalence especially in the African penguin and Cape cormorant and with lower prevalence in the Cape gannet and other cormorant species. It may contribute to morbidity and mortality in chicks and juveniles and immune-compromised individuals, whether in captivity, rehabilitation or the wild population. Epidemiology: Seabird ticks (especially the soft tick) are found together at all southern African seabird colonies, explaining the endemic distribution of these parasites. It is not clear if different seabirds can serve as reservoirs of infections for other species of seabirds as genetic research of Babesia species needs to clarify the species found in different seabird species. Clinical signs: Non-specific signs such as anaemia, pale mucus membranes and poor condition (especially in chicks and juveniles) are seen but are hard to determine whether caused by Babesia, concurrent disease or general debilitation. Carcases appear to be pale, occasionally pale yellow, with watery blood but diagnosis as to cause of death would need to be considered with histopathology evaluation. Diagnosis: The presence of Babesia parasites on blood smear evaluation does not necessarily indicate babesiosis; the level of parasitaemia should be borne in mind together with the intensity of clinical signs when considering treatment of live birds. Identification can be confirmed with histopathology evaluation; however determining primary cause of disease may be subjective. Treatment and quarantine: Insecticide treatment should be given to all birds entering rehabilitation to remove all ecto-parasites to prevent unnecessary exposure. Treatment with primaquine can be given to positive birds in a captive environment however quarantine is not necessary as the parasite is endemic in most of our seabirds. Imidocarb dipropionate is used for the

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treatment of Babesia infection in raptor species. Quarantine may be justified for the pelagic and sub-Antarctic seabird species if present in captivity or rehabilitation. Prevention and control: Management control of ecto-parasite load may be justified in the colonies, if there is cause for concern; this may entail use of insecticide powder, evaluation of burrows and the use of vegetation to minimise the levels of ecto-parasites. Zoonotic potential: There is no record of avian-infecting Babesia successfully infecting or causing disease in humans.

Leucocytozoonosis Disease/pathogen and transmission: Leucocytozoon tawaki has been recorded in the African penguin and Leucocytozoon ugwidi was described from cormorants, both of which are transmitted by simulid flies. Presence in captive and wild populations: Leucocytozoon species are seen at low prevalence in Southern African seabirds in rehabilitation centres in South Africa and likely occur at a low prevalence in these species in the wild. Parasites are seen more commonly in chicks and juveniles. Leucocytozoon can be highly pathogenic in other bird species. Epidemiology: Leucocytozooids are not transmitted between different bird families and therefore other bird species do not serve as a reservoir. It is unknown what species of fly transmits Leucocytozoon in southern Africa but the distribution of the vector will be important to determine the geographical area where this disease is likely to occur. Clinical signs: It does not seem to cause any clinical disease in these seabird species but may contribute to morbidity with concurrent infections. Mortality due to Leucocytozoon infection occurred in the yellow-eyed penguin causing disseminated petechial haemorrhage, hepatomegaly, splenomegaly and hydropericardium. Diagnosis: The parasite can be detected through blood smear evaluation or histopathology. Further work can be done using molecular methods to determine species. Treatment and quarantine: Treatment with metronidazole can be given. The pre-patent period (from inoculation by the infected insect to the emergence of the first blood parasites) tends to be relatively long (15-30 days). It is therefore reasonable to have a minimum quarantine period of two weeks, preferably four weeks, with blood smears being evaluated for parasites at the end of each week, in order to detect new and relapsing/recrudescing infections. Prevention and control: In captive environments, prevention of contact between natural avifauna, mosquitoes and susceptible birds is necessary. This may be achieved by keeping birds in netted enclosures to minimise this contact; fans, or windy conditions (interfering with simuliid flight), mosquito repellents and prophylactic treatment are other methods to use in captive environments. More research is needed on the epidemiology of the Leucocytozoon parasite as well as the vector to determine methods of control in the natural environment. In the event of a mortality event, the presence of similid flies should be investigated. Zoonotic potential: There is no record of Leucocytozoon successfully infecting or causing disease in humans.

Haemoproteosis Disease/pathogen and transmission: Haemoproteus spp. parasitise exclusively birds with approximately 150 recognised species. Haemoproteus lari has been described in gulls, and Haemoproteus skua has been described in the Sub-Antarctic skua. These parasites are transmitted by biting midges Culicoides spp.

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Presence in captive and wild populations: Only one individual Sub-Antarctic skua has been recorded historically, however Haemoproteus parasites are commonly seen in blood smears from Kelp and Hartlaub’s gull species. The occurrence of this parasite in the African penguin is unknown due to the higher frequency and similarities in basic morphology of Plasmodium species. Epidemiology: The distribution of biting midges overlaps with that of seabirds breeding in Namibia and South Africa, possibly providing opportunities for Haemoproteus inoculation. Infections may cause problems if the birds are stressed, immunocompromised or suffering from concurrent infections. There have been no records of infection causing mortality and therefore it seems unlikely that these parasites pose a significant threat for seabird conservation. Clinical signs: It does not seem to cause any clinical disease in these seabird species but may contribute to morbidity with concurrent infections. Anaemia, splenomegaly, hepatomegaly and pulmonary oedema have been seen in other bird species with pathogenic infections. Diagnosis: The parasite can be detected through blood smear evaluation or histopathology. It may be difficult to differentiate this parasite from Plasmodium; the key difference is that Plasmodium presents erythrocytic meronts whereas Haemoproteus does not. Further work can be done using molecular methods to determine species. Treatment and quarantine: Treatment with antimalarial drugs can be given although this does not seem necessary unless the individual is showing signs of illness. Because the parasite is widespread within gull species, a quarantine period is not justified and birds may be released with positive blood smears. However, in the case of morbidity or mortality resulting from a Haemoproteus infection, then a quarantine period of at least two weeks with blood smears being evaluated for parasites at the end of each week is recommended. Prevention and control: No prevention or control measures are warranted, other than the treatment of individuals presenting clinical signs of disease. Zoonotic potential: There is no record of Haemoproteus successfully infecting or causing disease in humans.

Toxoplasmosis Disease/pathogen and transmission: Toxoplasma gondii is an intracellular protozoan parasite that is transmitted horizontally through the ingestion of oocysts. Only the definitive host (exclusively felids) can shed oocysts in the faeces. Presence in captive and wild populations: T. gondii has a worldwide distributionwith wild and domestic cats being the definitive host while other mammals (including humans) and birds are intermediate hosts. T. gondii has been described in many domestic and wild bird species including gulls and terns (no clinical disease seen) and in captive penguin species and a red- footed booby admitted for rehabilitation (diagnosed on death). There have been no reports in wild southern African seabirds. It is reasonable to suspect the occurrence of this protozoan in seabird colonies that are near to domestic or wild cat species. Epidemiology: Wild and domestic cats excrete the Toxoplasma oocysts in the faeces which then contaminate food and water sources. Intermediate hosts become infected by ingestion of contaminated food and water or through the ingestion of tissue cysts. Scavenging species are high risk candidates for becoming intermediate hosts. Clinical signs: In captive African penguins, clinical signs such as ataxia followed by death were seen with hepatomegaly, splenomegaly, congested and haemorrhagic lungs and hyperaemic and

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thicked meninges seen on post-mortem examination. Histology confirmed the presence of the protozoan. Diagnosis: Diagnosis can be made with serologic, histopathologic, immunohistochemical and molecular methods. Most cases are diagnosed through histopathological examination of tissues from carcases, and can be aided by immunohistochemical staining of samples. Treatment and Quarantine: Diclazuril is described for the treatment of toxoplasmosis in birds but it is likely that diagnosis is only made after death and therefore no treatment would be necessary. However, in the event of a disease outbreak, the possibility of treatment would need to be investigated. There is an incubation period of 1-3 weeks after exposure to the organism in humans but is undocumented in bird species. Prevention and Control: Prevention of contact between cats and seabirds is recommended although this may be unavoidable in the case of wild cats near to mainland colonies; however the impact of predation from these cats may be far higher than the contamination of especially water sources. Management of water sources is also important to limit any sewage contamination as this was found to be an impotant link in gull exposure. Zoonotic potential: Toxoplasmosis is widespread in the human population, mostly as a sub-clinical disease with clinical signs only seen in immune-compromised individuals. Mothers can also pass the infection onto a foetus. Symptoms are generally flu-like although there can also be neurological and eye lesions. There is a very low risk of the disease spreading from bird to human, unless an infected carcase is eaten.

Intestinal Coccidiosis Disease/pathogen and transmission: Coccidiosis is mainly caused by protozoa Eimeria spp. or Isospora spp. but other species may also be involved. They are spread through ingestion of oocysts from the faeces of an infected bird or from a contaminated environment and have a direct life-cycle. Oocysts can be transmitted mechanically by equipment, insects, other birds and humans. Presence in captive and wild populations: In general, disease is not common in wild bird species. The prevalence is unknown in wild southern African seabirds but is seen occasionally in rehabilitation and the potential exists for a disease outbreak in the wild. Epidemiology: The severity of disease varies greatly and some immunity develops after exposure, especially with treatments that do not eliminate the infection. Stress causes an increase in the occurrence of the disease. In other bird species, contamination in the environment and the possibility of increasing coccidial infections with the release of hand-reared birds are concerns. Clinical signs: Coccidia occur in the gastro-intestinal tract but can also affect other organs, such as the liver and kidney. They may occur without causing illness. Clinical signs are non-specific such as lethargy, unthrifty appearance, weight loss, watery diarrhoea and death. Enteritis is seen on post mortem examination with possible granulomas within the body cavity. Diagnosis: Faecal smears can be analysed for the presence of oocysts but results must be evaluated together with clinical symptoms. Confirming coccidiosis as the cause of death involves histopathology examination and identification of the species. Treatment and quarantine: A conclusive diagnosis can only be made on post-mortem examination and therefore treatment may not be feasible. In the event of an outbreak, anti-coccidial drugs can be used to minimise mortality. The objective of treatment is not to eliminate the infection

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as light infections result in high levels of immunity and can prevent outbreaks with high mortality. The quarantine period should be at least two weeks as the life cycle is completed in the host in this time before shedding oocysts. Prevention and control: Prevention includes treatment of infected birds to minimise the build-up of oocysts in the environment, thorough disinfection and good husbandry to prevent contamination of food in the captive environment. In colony situations, control is impossible as oocysts will contaminate the breeding area in colony breeding birds. Zoonotic potential: There is no record of avian-infecting coccidia successfully infecting or causing disease in humans.

Cryptosporidiosis Disease/pathogen and transmission: Cryptosporidium spp. are protozoa that cause respiratory, gastro-intestinal or renal disease. There are several different species that infect many different bird species. The protozoan oocysts are present in the environment or are excreted by infected individuals and infect new birds through direct contact via ingestion or inhalation. Presence in captive and wild populations: There have been no recognised die-offs in wild bird populations from cryptosporidiosis. It is likely that there is widespread exposure to Cryptosporidium in wild African penguins but disease is probably limited to immune- compromised individuals. It is occasionally seen in penguin chicks admitted for hand-rearing as well as penguin carcases from the wild. It has not been recorded in other southern African seabird species. Epidemiology: Cryptosporidiosis may cause primary disease or it may be a secondary pathogen with concurrent disease. In most situations it only causes severe disease in immune-compromised hosts, especially chicks. Clinical signs: In African penguin chicks, the affected birds presented with smelly diarrhoea, not thriving, poor weight gain and susceptibility to other bacterial and fungal infections. Post- mortem lesions were non-specific. Diagnosis: Diagnosis is difficult, especially in live birds, due to the lack of specific clinical signs, difficulty in identifying the small oocysts in faecal smears, different staining techniques and use of expensive alternative techniques. Diagnosis can be made with histopathology examination but tissues need to be obtained from multiple tissue sites to minimise false negatives. In the African penguin, lesions were most commonly seen in the small intestine and the bursa of Fabricius. Treatment and quarantine: There is no specific treatment for Cryptosporidium infections but there is likely immunity developed after exposure. Birds should not be released if showing any signs of disease. Prevention and control: Specific disinfectants are required to disinfect against Cryptosporidium if there is an outbreak within a captive environment. The organism is resistant to many disinfectants. Prevention protocols include thorough disinfection of the premises as well as disinfection of everything that comes into contact with infected birds, specifically targeted at Cryptosporidium spp. In colony situations, control is impossible as oocysts will contaminate the breeding area in colony breeding birds. Zoonotic potential: Cryptosporidiosis may cause self-limiting diarrhea in healthy people, particularly children, and severe disease (potentially lethal) in immune-compromised people.

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5. Parasites

Endo and ecto-parasites can also cause problems and disease conditions within captive and wild populations. Some species have been identified in the African penguin, however most species found in other seabird species have not been identified. It is therefore difficult to determine or know the epidemiology of these species. The presence of parasites does not infer cause of death; the parasites may be incidental or may have contributed to mortality.

Endo-parasites may contribute to morbidity by causing inflammation and necrosis, enteritis, nutritional impacts and decreased vigour as well as predisposing to other diseases. Mortality may be caused by blood loss and severe malnutrition, especially in chicks. The life-cycle of different endo- parasites may be complex or direct and is often dependent on an intermediate host. Diagnosis of endo-parasites can be made by faecal evaluation of the eggs, visualisation of the worms in regurgitation or guano and post-mortem examination, however, the identification of species needs to be done by specialists. Regular deworming treatment seems to control the problem in rehabilitation and captive environments. There are no prevention or control measures in the wild, since the diet (fishes and squid) are the reservoirs of infection.

Ecto-parasites act as vectors that transmit pathogens to birds but they can also contribute directly to morbidity and mortality through blood loss, reduced growth, feather damage, skin damage, mange and depression, especially in chicks. Ticks are easily killed on the bird through treatment with insecticide, although environmental control is debatable. Furthermore, ecto-parasites can transmit certain pathogens such as Avipoxvirus (fleas, mosquitoes and possibly ticks), Babesia (ticks), Borrelia (ticks) and Plasmodium (mosquitoes).

Stomach Nematodes Contracaecum variegatum is commonly seen in the African penguin and stomach nematodes (presumably Contracaecum sp.) are commonly seen in other seabird species. On post-mortem examination, the nematodes can be seen to cause stomach ulcers and inflammation and can cause peritonitis if the stomach wall is perforated. It is unlikely that the nematodes cause mortality, except if causing peritonitis, but may cause nutritional impacts and decreased vigour. Aberrant migration of nematodes through other organs may cause lethal inflammation and infection although this is rarely seen.

Intestinal Trematodes Cardiocephaloides physalis is commonly seen in the proximal intestine (duodenum) of the African penguin and intestinal trematodes are occasionally seen in other seabird species. This species has been implicated in the deaths of African penguin chicks in the Eastern Cape with severe infestations causing destruction of the intestinal mucosa. In less severe infestation, intestinal trematodes likely contribute to morbidity and mortality through impaired absorption of food, especially if the bird is immune-compromised or has concurrent infection.

Intestinal Cestodes Tetrabothius lutzi and T. eudyptidis are occasionally seen in the stomach and small intestine of the African penguin. Intestinal cestodes are commonly seen in other seabirds, especially gull

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species. They do not seem to cause severe lesions but severe infestations likely impair digestion of food.

Tracheal Nematodes Cyasthoma phenisci is seen occasionally in the respiratory system of the African penguin (prevalence rate of approximately 15%). Tracheal nematodes are occasionally seen in other seabird species. The nematode does not seem to cause much pathology but may contribute to bacterial and fungal respiratory tract infection as well as airway obstruction.

Renal Trematodes Renicola sloanei commonly occurs in cyst-like structures in the kidney of the African penguin but generally little tissue reaction is seen on histopathology examination. Kidney trematodes are commonly seen in cormorant species and occasionally seen in other seabird species. It is unclear whether this worm causes any clinical problems and whether it is controlled through basic deworming treatment.

Ticks The argasid tick Carios capensis is commonly seen on African penguins and many seabird species. The ixodid tick Ixodes uriae is recorded as commonly seen on various southern African seabird species but was not collected at all during a recent health survey (2010-2013). Ticks are haematophagous and act as vectors for various parasites and pathogens. In severe infestations they can also cause severe anaemia and death in small chicks.

Fleas Parapsyllus humboldti is is commonly collected from African penguins and is also found on other penguin species. Fleas of unknown species are also found on other seabird species. It is unknown what the impact the fleas have on their hosts, but they can be haematophagous and therefore could also act as vectors of parasites and pathogens, they often occur in large numbers, especially on chicks and can cause irritation of the skin.

Lice Many different species of lice have been recorded on southern African seabirds and are commonly recorded on all species. There may be several species of lice on each bird species. There are biting lice that move around the body and chewing lice that are adapted to specific feather types. It is unknown what impact the louse has on the host but likely causes skin irritation and feather loss.

Mites A subcutaneous mite, likely Knemidocoptes spp., has been recorded in southern African seabirds (cormorants and gannets) but there are likely other feather mites also present in seabird species. The infestations do not seem to cause clinical disease, but in other bird species these mites can cause hyperkeratotic lesions on the feet and beak. Knemidocoptes spp. can be treated with topical ivermectin. Nasal mites have been recorded in other species of penguins and may be associated with mild to moderate sinusitis, but have yet to be recorded in African penguins.

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6. Toxins

Avian Botulism Disease/pathogen and transmission: Avian botulism occurs when birds ingest toxins produced by the bacterium Clostridium botulinum. There are different types of toxin produced but it is unknown what toxin causes botulism in southern African seabirds. Presence in captive and wild populations: Botulism is seen commonly in scavenging seabird species such as gulls and pelicans and is rarely seen in birds that only eat live fish. It is also commonly seen in many waterbird species, especially those that eat maggots. Epidemiology: C. botulinum is an anaerobic bacterium that persists in the environment in dormant spores. These spores are resistant to heat and dry conditions and can remain viable for years. The spores are found in wetland sediments as well as in many aquatic insects, crustacea and vertebrates. The spores germinate and the bacterium grows, multiplies and produces the toxin. The timing of botulism outbreaks is generally determined by environmental conditions such as temperature (generally above 25°C), season (generally summer), presence of decaying material and shallow water. The birds may ingest the toxin in decaying material or the toxin may be transferred to invertebrates that have eaten decaying material, and then eaten by birds. Clinical signs: The first signs are paralysis especially of the legs and wings followed by paralysis of the neck muscles and inability to hold the head up. In an outbreak, there may be a lot of carcases often close to a water source. There are no specific lesions seen on post-mortem examination but haemorrhage of the cerebrum may be indicative of toxicity. Diagnosis: A presumptive diagnosis is made on a combination of clinical signs, field conditions and the absence of lesions on post-mortem examination; however these may all indicate other toxic causes. Diagnosis can be confirmed with an ELISA test and water or decayed material can also provide diagnostic samples. Treatment and quarantine: Treatment is symptomatic and supportive, with activated charcoal given to adsorb any remaining toxin. There is an anti-toxin but it might not be available for treatment of seabirds in South Africa. Recovery is fast with gradually less severe lesions but birds with more severe lesions may die, often from aspiration pneumonia. After full recovery, there is no need for quarantine before release back into the wild. Prevention and control: Botulinum spores are resilient and ubiquitous in a wetland environment; it is not feasible to eliminate them. Control measures should focus on mitigating the environmental conditions such as reducing the chance of decaying material in water sources (for example removal of fish or bird carcases), prompt and thorough carcase disposal (burial or burning) and prevention of disposal of sewage and other waste water into water sources. Zoonotic potential: Humans are susceptible to botulism, however it seems highly unlikely that handling seabirds could result in human exposure to the toxin. Affected individuals may present weakness, trouble seeing, feeling tired, trouble speaking, difficulty to breathe and death.

Marine Biotoxins Disease/pathogen and transmission: Periodic blooms of algae and microorganisms (dinoflaggelates and cyanobacteria) have been recorded in marine and freshwater bodies throughout the

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world. Depending on the species involved, different toxins that kill shellfish, fish, birds and humans may be produced. Presence in captive and wild populations: There is little knowledge on the effects of marine biotoxins to seabirds in South Africa due to diagnostic testing difficulties, although the occurrence of red tides with invertebrate and fish mortality has been documented. There have occasionally been mass bird mortality events, especially of flying species such as terns, gulls, cormorants and gannets but with no definitive diagnosis made. There are no records of biotoxins causing mass mortality in captive populations. Epidemiology: Algal blooms are a natural phenomenon but occurrence may increase with pollution of the water body and increased phosphorus and nitrogen in the water causing favourable conditions for the growth of algae. Marine toxins are magnified in the food chain by fish and shellfish, which are in turn, eaten by birds. Harmful algal blooms may also cause deaths of fish and lead to avian botulism, which may be difficult to distinguish from algal toxicity in the bird. Clinical signs: The toxins seem mainly to affect the nervous system and the liver. Clinical signs therefore include neurological signs such as muscle tremors, weakness, paralysis and death. Other signs such as vomiting or regurgitation can be seen. There are no specific lesions seen on post-mortem or histologic examination. Diagnosis: A presumptive diagnosis can be made on a mass bird mortality event after the occurrence of an algal bloom, with supportive clinical symptoms and the absence of lesions on post- mortem examination; however these may also indicate other toxic causes. Toxins can be tested from the water sample or from the gastro-intestinal contents and tissues of affected birds. Treatment and quarantine: Treatment is symptomatic and supportive, with activated charcoal given to adsorb any remaining toxin. A live bird showing signs of illness should be treated as in an avian botulism case. After full recovery, there is no need for quarantine before release back into the wild. Prevention and control: Control measures would be directed at identification of the conditions that trigger harmful algal blooms, particularly through management of pollution and waste management of the water bodies. Zoonotic potential: The biotoxins are generally only harmful if ingested; therefore exposure during handling seabirds is unlikely. However, it is possible that humans may absorb toxins through skin lesions when handling carcases, thus care should be taken to prevent this.

7. Miscellaneous conditions

Feather-loss Disorder Disease/pathogen and transmission: This disorder has been described in African and other penguin chicks although the aetiology has not been determined. Presence in captive and wild populations: It is documented in wild and hand-reared African penguin chicks, although it is more common in the hand-reared chicks. It has not been seen in seabird species other than penguins. Epidemiology: The aetiology is currently unknown and therefore its epidemiology is poorly understood. It is only seen in chicks and those chicks that survive grow normal plumage. If the chick loses the emerging juvenile feathers, then the feathers that grow through are in the

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adult plumage pattern. This disorder does not seem to be related to malnutrition and does not seem to be contagious, however the occurrence and severity does vary from year to year. Clinical signs: There are patches of exposed skin from relatively sudden feather-loss; these can vary from small patches typically on the head and neck to almost complete loss of plumage and the birds remain feather-less for a few weeks until the new plumage grows. It must be differentiated from feather-loss caused by manual rubbing or plucking of the feathers or from peck wounds. The loss of feathers is not associated with any skin lesions, irritations or the presence of ecto-parasites. The feather-loss may affect the second coat of down or emerging juvenile feathers. Feather-loss may result in slower growth and smaller fledglings and may contribute to mortality, especially in the wild where the chicks are unable to thermoregulate with an incomplete feather layer. Diagnosis: Diagnosis is made purely on clinical signs especially with the history of rapid feather loss. Treatment and quarantine: Treatment is supportive, giving the chicks time to grow back their feathers. There is no need for quarantine; the bird can be released once it has re-grown it’s plumage and tested waterproof for release. Prevention and control: It is debatable whether feather-loss chicks should be removed from the wild for rehabilitation in order to prevent possible mortality due to slower growth and exposure, or if they should be left to resolve the issue in the colony. The body condition of the chicks and other signs of illness could be borne in mind when making this decision as well as the competency of the parents to raise the chick. Monitoring should be done to record the incidence of the feather-loss disorder so that it can be further understood. Zoonotic potential: The aetiology is unknown and therefore zoonotic risk cannot be determined, however it seems unlikely to pose a significant threat to human health.

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Appendix B. Detailed risk assessment scoring sheets

1. Penguins

Pathogen or disease SS PE IV TO IC IA POS IOS Avian pox 3 3 3 2 2 1 10 5.6 Herpesvirosis (S. African strain) 3 2 1 1 2 0 6.7 3.3 Herpesvirosis (S. American strain) 2 0 0 3 3 3 1.7 10 Herpesvirosis (cormorant strain) 0 ------Newcastle disease 3 2 0 3 3 3 5.8 10 Avian influenza (high pathogenicity) 1 1 0 3 3 3 2.5 10 Avian influenza (low pathogenicity) 2 1 0 3 0 0 3.3 3.3 West Nile disease 3 1 0 2 2 2 4.2 6.7 Eastern equine encephalitis 3 0 0 2 2 2 2.5 6.7 Avian reovirus 2 1 0 2 1 1 3.3 4.4 Infectious bursal disease 2 1 0 3 1 1 3.3 5.6 Avian cholera 3 2 1 3 2 2 6.7 7.8 Chlamydiosis 2 1 0 3 2 2 3.3 7.8 Mycoplasmosis 3 1 0 3 1 1 4.2 5.6 Relapsing fever Borrelia 3 2 1 2 2 1 6.7 5.6 Lyme disease Borrelia 2 0 0 2 0 0 1.7 2.2 Bacterial airsacculitis and pneumonia 3 3 3 1 2 2 10 5.6 Bacterial gastroenteritis and colitis 3 3 3 1 2 2 10 5.6 Aspergillosis 3 3 3 1 2 2 10 5.6 Candidiasis 3 3 3 1 1 0 10 2.2 Avian malaria 3 3 2 2 3 3 9.2 8.9 Babesiosis 3 3 3 2 2 1 10 5.6 Leucocytozoonosis 3 2 1 2 1 0 6.7 3.3 Haemoproteosis 2 1 0 2 0 0 3.3 2.2 Toxoplasmosis 3 1 0 2 2 2 4.2 6.7 Intestinal coccidiosis 3 2 2 2 1 0 7.5 3.3 Cryptosporidiosis 3 3 3 2 2 0 10 4.4 Stomach nematodes 3 3 3 0 2 1 10 3.3 Intestinal trematodes 3 3 3 0 2 1 10 3.3 Intestinal cestodes 3 3 3 1 1 1 10 3.3 Tracheal nematodes 3 3 3 0 2 1 10 3.3 Renal trematodes 3 3 3 0 1 1 10 2.2 Ticks 3 3 3 2 2 1 10 5.6 Fleas 3 3 3 2 1 0 10 3.3 Lice 3 3 3 2 1 0 10 3.3 Nasal mites 2 0 0 2 1 1 1.7 4.4 Feather mites 2 0 0 2 1 0 1.7 3.3 Subcutaneous mites 0 ------Avian botulism 1 1 0 2 3 3 2.5 8.9 Marine biotoxins 2 1 0 2 3 3 3.3 8.9 Feather-loss disorder 3 3 3 0 2 0 6.7 2.2 Legend: SS – Species susceptibility, PE – Probability of exposure, IV – Interannual variability, TO – Transmission in outbreaks, IC – Impact on chick survival and/or breeding physiology, IA – Impact on juvenile/adult survival, POS – Probability of occurrence score, OIS – Outbreak impact score.

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2. Cormorants

Pathogen or disease SS PE IV TO IC IA POS IOS Avian pox 2 1 0 2 1 0 3.3 3.3 Herpesvirosis (S. African strain) 0 ------Herpesvirosis (S. American strain) 0 ------Herpesvirosis (cormorant strain) 2 0 0 1 1 0 1.7 2.2 Newcastle disease 3 2 1 3 3 3 6.7 10 Avian influenza (high pathogenicity) 1 1 0 3 3 3 2.5 10 Avian influenza (low pathogenicity) 2 1 0 3 0 0 3.3 3.3 West Nile disease 2 1 0 2 2 2 3.3 6.7 Eastern equine encephalitis 2 0 0 2 2 2 1.7 6.7 Avian reovirus 0 ------Infectious bursal disease 0 ------Avian cholera 3 3 1 3 3 3 8.3 10 Chlamydiosis 2 1 0 3 2 2 3.3 7.8 Mycoplasmosis 0 ------Relapsing fever Borrelia 1 1 0 2 2 1 2.5 5.6 Lyme disease Borrelia 1 0 0 2 0 0 0.8 2.2 Bacterial airsacculitis and pneumonia 3 3 3 1 1 1 10 3.3 Bacterial gastroenteritis and colitis 3 3 3 1 1 1 10 3.3 Aspergillosis 3 2 3 1 2 1 8.3 4.4 Candidiasis 2 1 0 1 1 0 3.3 2.2 Avian malaria 3 2 2 2 3 3 7.5 8.9 Babesiosis 3 3 3 2 2 1 10 5.6 Leucocytozoonosis 3 2 2 2 1 0 7.5 3.3 Haemoproteosis 0 ------Toxoplasmosis 1 1 0 2 2 2 2.5 6.7 Intestinal coccidiosis 3 2 1 2 3 3 6.7 8.9 Cryptosporidiosis 2 1 0 2 1 0 3.3 3.3 Stomach nematodes 3 3 3 0 2 1 10 3.3 Intestinal trematodes 3 3 3 0 1 1 10 2.2 Intestinal cestodes 3 2 0 1 1 1 5.8 3.3 Tracheal nematodes 3 3 3 0 2 1 10 3.3 Renal trematodes 3 3 3 0 1 1 10 2.2 Ticks 3 2 1 2 2 1 6.7 5.6 Fleas 3 2 1 2 1 0 6.7 3.3 Lice 3 3 3 2 1 0 10 3.3 Nasal mites 0 ------Feather mites 2 0 0 2 1 0 1.7 3.3 Subcutaneous mites 3 2 1 2 1 0 6.7 3.3 Avian botulism 2 1 0 2 3 3 3.3 8.9 Marine biotoxins 3 2 1 2 3 3 6.7 8.9 Feather-loss disorder 0 ------Legend: SS – Species susceptibility, PE – Probability of exposure, IV – Interannual variability, TO – Transmission in outbreaks, IC – Impact on chick survival and/or breeding physiology, IA – Impact on juvenile/adult survival, POS – Probability of occurrence score, OIS – Outbreak impact score.

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3. Gannets

Pathogen or disease SS PE IV TO IC IA POS IOS Avian pox 0 ------Herpesvirosis (S. African strain) 0 ------Herpesvirosis (S. American strain) 0 ------Herpesvirosis (cormorant strain) 0 ------Newcastle disease 1 1 0 3 3 3 2.5 10 Avian influenza (high pathogenicity) 1 1 0 3 3 3 2.5 10 Avian influenza (low pathogenicity) 2 1 0 3 0 0 3.3 3.3 West Nile disease 1 1 0 2 2 1 2.5 5.6 Eastern equine encephalitis 1 0 0 2 2 2 0.8 6.7 Avian reovirus 0 ------Infectious bursal disease 0 ------Avian cholera 3 2 1 3 3 3 6.7 10 Chlamydiosis 2 1 0 3 2 2 3.3 7.8 Mycoplasmosis 0 ------Relapsing fever Borrelia 3 2 0 2 2 1 5.8 5.6 Lyme disease Borrelia 1 0 0 2 0 0 0.8 2.2 Bacterial airsacculitis and pneumonia 3 3 3 1 1 1 10 3.3 Bacterial gastroenteritis and colitis 3 3 3 1 1 1 10 3.3 Aspergillosis 3 2 3 1 2 1 8.3 4.4 Candidiasis 1 1 0 1 1 0 2.5 2.2 Avian malaria 3 2 2 2 3 3 7.5 8.9 Babesiosis 3 3 2 2 1 1 9.2 4.4 Leucocytozoonosis 0 ------Haemoproteosis 0 ------Toxoplasmosis 1 1 0 2 2 2 2.5 6.7 Intestinal coccidiosis 1 1 0 2 1 0 2.5 3.3 Cryptosporidiosis 2 1 0 2 1 0 3.3 3.3 Stomach nematodes 3 3 3 0 2 1 10 3.3 Intestinal trematodes 3 3 3 0 1 1 10 2.2 Intestinal cestodes 2 1 0 1 1 1 3.3 3.3 Tracheal nematodes 3 3 3 0 2 1 10 3.3 Renal trematodes 3 3 3 0 1 1 10 2.2 Ticks 2 1 0 2 2 1 3.3 5.6 Fleas 2 1 0 2 1 0 3.3 3.3 Lice 3 3 3 2 1 0 10 3.3 Nasal mites 0 ------Feather mites 2 0 0 1 1 0 1.7 2.2 Subcutaneous mites 2 1 0 1 1 0 3.3 2.2 Avian botulism 1 1 0 2 3 3 2.5 8.9 Marine biotoxins 2 1 0 2 3 3 3.3 8.9 Feather-loss disorder 0 ------Legend: SS – Species susceptibility, PE – Probability of exposure, IV – Interannual variability, TO – Transmission in outbreaks, IC – Impact on chick survival and/or breeding physiology, IA – Impact on juvenile/adult survival, POS – Probability of occurrence score, OIS – Outbreak impact score.

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4. Terns

Pathogen or disease SS PE IV TO IC IA POS IOS Avian pox 2 1 0 2 1 0 3.3 3.3 Herpesvirosis (S. African strain) 0 ------Herpesvirosis (S. American strain) 0 ------Herpesvirosis (cormorant strain) 0 ------Newcastle disease 2 1 0 3 3 3 3.3 10 Avian influenza (high pathogenicity) 3 2 0 3 3 3 5.8 10 Avian influenza (low pathogenicity) 3 1 0 3 0 0 4.2 3.3 West Nile disease 1 1 0 2 2 1 2.5 5.6 Eastern equine encephalitis 1 0 0 2 2 2 0.8 6.7 Avian reovirus 0 ------Infectious bursal disease 0 ------Avian cholera 3 2 1 3 3 3 6.7 10 Chlamydiosis 2 1 0 3 2 2 3.3 7.8 Mycoplasmosis 0 ------Relapsing fever Borrelia 1 1 0 2 1 1 2.5 4.4 Lyme disease Borrelia 1 0 0 2 0 0 0.8 2.2 Bacterial airsacculitis and pneumonia 2 2 2 1 1 1 6.7 3.3 Bacterial gastroenteritis and colitis 2 2 2 1 1 1 6.7 3.3 Aspergillosis 2 2 2 1 2 1 6.7 4.4 Candidiasis 1 1 0 1 1 0 2.5 2.2 Avian malaria 1 1 0 2 3 3 2.5 8.9 Babesiosis 0 ------Leucocytozoonosis 0 ------Haemoproteosis 0 ------Toxoplasmosis 2 1 0 2 2 2 3.3 6.7 Intestinal coccidiosis 2 1 0 2 1 0 3.3 3.3 Cryptosporidiosis 2 1 0 2 1 0 3.3 3.3 Stomach nematodes 1 1 0 0 1 1 2.5 2.2 Intestinal trematodes 1 1 0 0 1 1 2.5 2.2 Intestinal cestodes 3 2 2 1 1 1 7.5 3.3 Tracheal nematodes 1 1 0 0 1 1 2.5 2.2 Renal trematodes 3 2 2 0 1 1 7.5 2.2 Ticks 2 1 0 2 2 1 3.3 5.6 Fleas 1 1 0 2 1 0 2.5 3.3 Lice 3 3 3 2 1 0 10 3.3 Nasal mites 2 0 0 1 1 0 1.7 2.2 Feather mites 2 0 0 1 1 0 1.7 2.2 Subcutaneous mites 0 ------Avian botulism 2 1 0 2 3 3 3.3 8.9 Marine biotoxins 3 2 1 2 3 3 6.7 8.9 Feather-loss disorder 0 ------Legend: SS – Species susceptibility, PE – Probability of exposure, IV – Interannual variability, TO – Transmission in outbreaks, IC – Impact on chick survival and/or breeding physiology, IA – Impact on juvenile/adult survival, POS – Probability of occurrence score, OIS – Outbreak impact score.

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5. Gulls

Pathogen or disease SS PE IV TO IC IA POS IOS Avian pox 2 1 0 2 1 0 3.3 3.3 Herpesvirosis (S. African strain) 0 ------Herpesvirosis (S. American strain) 0 ------Herpesvirosis (cormorant strain) 0 ------Newcastle disease 2 1 0 3 3 3 3.3 10 Avian influenza (high pathogenicity) 3 2 0 3 3 3 5.8 10 Avian influenza (low pathogenicity) 3 2 0 3 0 0 5.8 3.3 West Nile disease 2 1 0 2 2 1 3.3 4.4 Eastern equine encephalitis 2 0 0 2 2 2 1.7 6.7 Avian reovirus 2 1 0 2 1 1 3.3 4.4 Infectious bursal disease 0 ------Avian cholera 3 2 1 3 2 2 6.7 7.8 Chlamydiosis 2 1 0 3 2 2 3.3 7.8 Mycoplasmosis 2 1 0 3 1 1 3.3 5.6 Relapsing fever Borrelia 1 1 0 2 1 1 2.5 4.4 Lyme disease Borrelia 1 0 0 2 0 0 0.8 2.2 Bacterial airsacculitis and pneumonia 3 3 3 1 1 1 10 3.3 Bacterial gastroenteritis and colitis 3 3 3 1 1 1 10 3.3 Aspergillosis 3 3 3 1 2 2 10 5.6 Candidiasis 2 1 0 1 1 0 3.3 2.2 Avian malaria 2 1 0 2 2 2 3.3 6.7 Babesiosis 3 2 0 2 1 1 5.8 4.4 Leucocytozoonosis 0 ------Haemoproteosis 3 3 3 2 0 0 10 2.2 Toxoplasmosis 2 1 0 2 2 2 3.3 6.7 Intestinal coccidiosis 1 1 0 2 1 0 2.5 3.3 Cryptosporidiosis 2 1 0 2 1 0 3.3 3.3 Stomach nematodes 2 1 0 0 1 1 3.3 2.2 Intestinal trematodes 2 1 0 0 1 1 3.3 2.2 Intestinal cestodes 3 3 3 1 1 1 10 3.3 Tracheal nematodes 2 1 0 0 1 1 3.3 2.2 Renal trematodes 2 1 0 0 1 1 3.3 2.2 Ticks 2 1 0 2 2 1 3.3 5.6 Fleas 1 1 0 2 1 0 2.5 3.3 Lice 3 3 3 2 1 0 10 3.3 Nasal mites 2 0 0 1 1 0 1.7 2.2 Feather mites 2 0 0 1 1 0 1.7 2.2 Subcutaneous mites 0 ------Avian botulism 3 3 3 2 3 3 10 8.9 Marine biotoxins 3 2 1 2 3 3 6.7 8.9 Feather-loss disorder 0 ------Legend: SS – Species susceptibility, PE – Probability of exposure, IV – Interannual variability, TO – Transmission in outbreaks, IC – Impact on chick survival and/or breeding physiology, IA – Impact on juvenile/adult survival, POS – Probability of occurrence score, OIS – Outbreak impact score.

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6. Pelicans

Pathogen or disease SS PE IV TO IC IA POS IOS Avian pox 0 ------Herpesvirosis (S. African strain) 0 ------Herpesvirosis (S. American strain) 0 ------Herpesvirosis (cormorant strain) 0 ------Newcastle disease 3 2 1 3 3 3 6.7 10 Avian influenza (high pathogenicity) 1 1 0 3 3 3 2.5 10 Avian influenza (low pathogenicity) 2 1 0 3 0 0 3.3 3.3 West Nile disease 2 1 0 2 2 1 3.3 5.6 Eastern equine encephalitis 1 0 0 2 2 2 0.8 6.7 Avian reovirus 0 ------Infectious bursal disease 0 ------Avian cholera 2 0 0 3 3 3 1.7 10 Chlamydiosis 2 1 0 3 2 2 3.3 7.8 Mycoplasmosis 3 3 3 3 1 0 10 4.4 Relapsing fever Borrelia 1 1 0 2 1 1 2.5 4.4 Lyme disease Borrelia 1 0 0 2 0 0 0.8 2.2 Bacterial airsacculitis and pneumonia 2 2 2 1 1 1 6.7 3.3 Bacterial gastroenteritis and colitis 2 2 2 1 1 1 6.7 3.3 Aspergillosis 2 2 2 1 2 1 6.7 4.4 Candidiasis 2 1 0 1 1 0 3.3 2.2 Avian malaria 1 1 0 2 3 3 2.5 8.9 Babesiosis 0 ------Leucocytozoonosis 0 ------Haemoproteosis 0 ------Toxoplasmosis 1 1 0 2 2 2 2.5 6.7 Intestinal coccidiosis 2 1 0 2 1 0 3.3 3.3 Cryptosporidiosis 2 1 0 2 1 0 3.3 3.3 Stomach nematodes 3 3 3 0 1 1 10 2.2 Intestinal trematodes 2 1 0 0 1 1 3.3 2.2 Intestinal cestodes 2 1 0 1 1 1 3.3 3.3 Tracheal nematodes 2 1 0 0 1 1 3.3 2.2 Renal trematodes 2 1 0 0 1 1 3.3 2.2 Ticks 2 1 0 2 2 1 3.3 5.6 Fleas 2 1 0 2 1 0 3.3 3.3 Lice 3 3 3 2 1 0 10 3.3 Nasal mites 0 ------Feather mites 2 0 0 1 1 0 1.7 2.2 Subcutaneous mites 2 1 0 1 1 0 3.3 2.2 Avian botulism 3 3 3 2 3 3 10 8.9 Marine biotoxins 2 1 0 2 3 3 3.3 8.9 Feather-loss disorder 0 ------Legend: SS – Species susceptibility, PE – Probability of exposure, IV – Interannual variability, TO – Transmission in outbreaks, IC – Impact on chick survival and/or breeding physiology, IA – Impact on juvenile/adult survival, POS – Probability of occurrence score, OIS – Outbreak impact score.

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Appendix C. List of controlled and notifiable animal diseases

Pathogens that may be associated with birds are indicated with black dots.

South Africa controlled and notifiable animal diseases (Act 35 of 1984)

l Any animal disease or infectious agent ¡ Foot and mouth disease (FMD) that is not known to occur in South Africa ¡ Glanders ¡ African horse sickness (AHS) ¡ Haemorrhagic septicaemia (in fish) ¡ African swine fever (ASF) ¡ Johne’s disease (in sheep, cattle and l Anthrax goats) ¡ Aujeszky’s disease ¡ Nagana (Trypanosomiasis) ¡ Bacterial kidney disease (in fish) l Newcastle disease ¡ Bovine contagious pleuropneumonia l Notifiable avian influenza (CBPP) ¡ Porcine reproductive and respiratory ¡ Bovine spongiform encephalopathy (BSE) syndrome (PRRS) l Brucellosis (in animal species) l Psittacosis ¡ Classical swine fever (CSF) l Rabies ¡ Contagious equine metritis (CEM) ¡ Rinderpest ¡ Contagious haemopoieitic necrosis (in l Salmonella Enteritidis fish) l Salmonella Gallinarum ¡ Contagious pancreatic necrosis (in fish) l Salmonella Pullorum ¡ Corridor or Buffalo disease (Theilerioses) ¡ Scrapie ¡ Dourine ¡ Sheep scab ¡ East coast fever ¡ Skin conditions in sheep ¡ Equine infectious anaemia (EIA) ¡ Swine vesicular disease ¡ Equine influenza (EI) l Tuberculosis (in all animal species) ¡ Equine viral arteritis (EVA)

South Africa notifiable animal diseases (Act 35 of 1984)

¡ Bovine malignant catarrhal fever ¡ Rift valley fever (Snotsiekte) ¡ Strangels ¡ Bluetongue ¡ Swine erysipelas ¡ Lumpy skin disease

OIE-listed avian diseases, infections and infestations in force in 2016

l Avian chlamydiosis l Infection with avian influenza viruses l Avian infectious bronchitis l Infection with influenza A viruses of high l Avian infectious laryngotracheitis pathogenicity in birds other than poultry l Avian mycoplasmosis (Mycoplasma including wild birds gallisepticum) l Infection with Newcastle disease virus l Avian mycoplasmosis (Mycoplasma l Infectious bursal disease (Gumboro synoviae) disease) l Duck virus hepatitis l Pullorum disease l Fowl typhoid l Turkey rhinotracheitis

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