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Running Heading: Flaherty; Trichinella and wildlife conservation

Title: A review of Trichinella infection and resulting behavioral changes in individual hosts:
implications for wildlife management and conservation

Author: Elizabeth A. Flaherty, Department of Zoology and Physiology, University of Wyoming,

1000 E. University Ave, Laramie, WY 82071, 307-766-4907 (phone), 307-766-5625 (fax)
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Abstract

Trichinosis, caused by nematodes in the genus Trichinella, can have a significant affect

on survival and reproduction of wildlife and domestic species. This paper provides the necessary

information, geared towards wildlife managers and biologists, to consider this parasite when

managing or studying the host populations. The paper includes a basic review of the life history,

general biology, methods for detection, both the sylvatic and domestic cycles, routes of infection,

and behavioral changes in the host species. Considerations for management and conservation

planning are included.

Key Words

Trichinella, trichinosis, Trichinella spiralis, Trichinella pseudospiralis, Trichinella nativa,

behavioral changes from parasitic infection
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Introduction

Trichinosis, caused by nematodes in the genus Trichinella, was first identified in 1835 in

humans and linked to pork consumption and disease in 1860 (Campbell 1983). It since has been

found throughout the world in a wide variety of animals primarily carnivores and scavengers.

While this disease was once of great concern to man, it has become less so due to education and

improvements in swine production. However, the parasite has continued to be quite common in

many species of wildlife worldwide.

There are 10 known genotypes of Trichinella with seven being recognized as distinct

species (Trichinella spiralis, Trichinella pseudospiralis, Trichinella nativa, Trichinella murrelli,

Trichinella nelsoni, Trichinella papuae, and Trichinella britovi) and three as uncertain taxa

(Pozio 2000). The geographic range for Trichinella spp. is widespread and covers most of the

world and is a concern to the global human population especially in parts of Russia, China, and

Argentina (Dupouy-Camet 2000). Specifically T. spiralis and T. pseudospiralis have a

cosmopolitan distribution while all others are confined to specific geographic ranges. T. nativa

has a distribution confined to the Arctic region including North America and into Europe (Pozio

2000).

Because of the importance of disease and infections in wildlife populations and because

of the impact Trichinella spp. have on their hosts, this paper provides the necessary information

to wildlife managers and biologists to consider this parasite when managing or studying the host

populations. This paper first provides a basic review of the life history, general biology, and

detection of Trichinella spp. The paper then describes the sylvatic and domestic cycles and

routes of infection for this parasite followed by a summary of the changes in behavior of infected
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individuals in the host population. Finally, I will conclude with considerations for management

and conservation planning.

Life history of Trichinella spp.

The life history of Trichinella generally begins with a host ingesting encysted,

Trichinella larvae in striated muscle tissue. The larvae are released from the cyst while in the

gastrointestinal tract of the new host and rapidly develop into adult worms involving four molts.

Adults range in size from 1.4 – 4 mm in length with the males being smaller than the females

(Smyth 1994). As immature adults, the parasites mate and invade the epithelial cells of the

intestine (Gardiner 1976). Females produce embryonic worms that then invade the circulatory

system via the lymphatic system and eventually enter striated muscle where they encyst and wait

for the muscle to be consumed by the next host.

Initial clinical signs following infection include diarrhea, vomiting, abdominal pain, and

constipation. Diarrhea is a result of the parasite infection causing an increase in the gastrin

levels in the host which stimulates gastric acid secretion, increasing gut activity, and changing

the intestinal mobility and flow of digesta (Castro et al. 1976). Following larval migration to the

muscle tissue, muscle pain, periorbital edema, and headache are the clinical signs in humans with

similar signs observed in animals. Heavy infection can lead to death if the embryonic worms

enter the cardiac tissue or the brain (Campbell 1983, Noble 1989).

Infection occurs following ingestion of uncooked or undercooked meat from an infected

animal. The infected individual becomes both the intermediate and definitive host for this

parasite (Noble et al. 1989). Infection occurs in domestic and wild mammals, including

herbivores, omnivores, and carnivores, humans, birds, reptiles, fish, and invertebrates (Pozio
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2000). Wild boar (Sus scrofa) and pork continue to be the main causes of human infection

throughout most of the world though recent infections in the United States have been a result of

consumption of undercooked game meat (Dupouy-Camet 2000). Undercooked horse (Equus

caballus) meat has resulted in human outbreaks in Europe and Mexico (Boireau et al. 2000). In

wildlife, the sylvatic cycle is maintained primarily through cannibalism and scavenging.

Detection of trichinosis is primarily through direct observation and the pooled sample

digestion method using muscle samples post mortem. Preferred sample sites include the tongue,

diaphragm, and masseter muscle. The digestion method is the best method for detecting T.

psuedospiralis because of the lack of larval cysts. Serological tests are also available and include

immunofluorescence antibody test, western blot analysis, complement fixation test,

haemagglutination test, and enzyme-linked immunosorbent assay (ELISA) with the ELISA test

being the easiest and most preferred serological test (Nöckler et al. 2000).

Trichinella cycles and routes of infection

Infection routes/cycles can be either sylvatic or domestic and depend largely on the

species of parasite. Three species are primarily involved in the sylvatic cycle in North America,

Trichinella psuedospiralis, T. nativa, and T. murrelli. T. pseudospiralis can infect both

mammals and birds and it is important to note that T. pseudospiralis does not induce capsule

formation in host muscles, a unique characteristic of this particular species (Smyth 1994). T.

nativa is cold tolerant, can be viable in the meat for as long as a year at -15° C, and has been

found in carnivores and marine mammals including seals (Phoca spp. and Erignathus spp.),

walruses (Odobenus rosmarus), and in one Beluga whale (Delphinapterus leucas; Rausch et al.

1956, Forbes 2000). This resistance to freezing and the longevity of the cysts in the hosts, which
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is usually the lifetime of the animal, has resulted in the wide distribution even when the host

population density is very low (Nelson 1990). Cannibalism and consumption of other carnivores

is likely the mechanism for maintaining high infection rates in polar bears (Ursus maritimus),

brown bears (Ursus arctos), and arctic fox (Alopex lagopus; Forbes 2000) which is the primary

cycle in the Arctic (Nelson 1990). Likewise, wolves (Canis lupis) from interior Alaska also have

a high incidence of infection of about 33-36% prevalence (Rausch et al. 1956, Zarnke et al.

1999) caused by predation on other carnivores. Marine mammals are the secondary cycle and

are infected by scavenging on the carcasses of infected carnivores that fall into the water.

Because these animals are such long-lived, the chance of infection is high even in areas with low

prevalence. In addition, larvae can be viable up to 20 years post infection. Humans and sled

dogs are at risk of acquiring this infection from consumption of game meat in the Arctic (Forbes

2000). Finally, T. murrelli is responsible for the sylvatic cycles in the temperate regions of

North America, mostly in the eastern United States (Pozio 2000).

The domestic cycle, caused by Trichinella spiralis, is primarily maintained through

domestic pig production. Domestic pigs maintain the cycle by ingestion of feces of recently

infected pigs, infected pig meat, infected rats, and through tail-biting of infected pigs. It is

important to note that infected rats have only been found on farms with infected domestic

livestock (Pozio 2000). Despite claims that wildlife were causing the infections in farms, the

farms are actually responsible for the infections in wildlife closely associated with the farms.

Carnivores in close proximity to domestic swine farms become infected with T. spiralis as a

result of eating infected rats and garbage from the farms. This was demonstrated in a study that

trapped infected skunks (Mephitis mephitis), raccoons (Procyon lotor), and opposums (Didelphis

virginiana) around a pig farm in New Jersey. Test showed that the wildlife was infected with T.
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spiralis that was genetically identical to that in the farm pigs but very different from that of a

wild fox (Murrell et al. 1987). Other small carnivores, including martens (Martes americana)

and ermines (Mustela erminea; Hoberg et al. 1990) also commonly acquire this parasite from the

farms. This species is also highly pathogenic to humans (Kapel 2000). However, T. spiralis

derived from domestic pigs can be killed with cold or heat treatment by freezing for 20 days at -

20° C or cooking to an internal temperature of 60 ° F (Nelson 1990).

Behavioral changes in wildlife infected with Trichinella

Trichinella ensure transmission from one host to another through behavioral changes in

the host leading to increased predation risk. Generally, species that have lived in close

association with a parasite for a great deal of time have evolved means to avoid infection

especially when this involves parasites that are as highly pathogenic and long-lived as

Trichinella spp. However, that does not seem to be the case for this parasite. Kuris (1997)

hypothesizes that high rates of infectivity in host populations of Trichinella spp. are because: 1.

host specificity is low (Pozio et al. 1992) because the risk of infection is spread across several

species which reduces selection pressure on individual species to avoid consuming sick prey, 2.

infection causes general weakening of prey so it is difficult for predators to differentiate between

Trichinella infection and other illnesses or injuries, 3. scavenging is common in predators and is

an important mode of transmission (Pozio et al. 1992).

Rodents, specifically mice, that become infected with Trichinella spiralis experience a

change in behavior related to daily activity. In captive studies, infected mice are less active and

reduce their exploratory bouts of locomotion (Rau 1983a). Infected wild mice and rodents may

behave similarly to domestic mice and be predated upon easily by mammalian predators thus
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transmitting the infection of this primarily domestic strain of Trichinella to predators (Poirer et

al. 1995). In contrast, mice infected with T. pseudospiralis experienced a brief decline in

locomotor activity followed by an increase in locomotor activity during the chronic phase of this

infection (Rau 1984b). This reaction is likely because T. pseudospiralis has an anti-

inflammatory potential and does not form the protective capsule around the cyst in the muscle

(Poirer et al. 1995). This increased activity makes rodents more likely to be predated upon by

avian predators that hunt by sight. Interestingly, this is the only species of Trichinella that can

infect birds. This behavioral change in rodents may work to ensure the parasites are directed to

the appropriate host (Poirer et al. 1995).

Research on the effects of Trichinella pseduospiralis in birds reported important

behavioral changes due to infection. Kestrals (Falco sparverius) infected with T. pseudospriarlis

perched closer to the ground and sometimes on the ground while uninfected birds perched much

higher. Infected kestrels also walked more (instead of flying short distances) than uninfected

birds (Saumier and Rau 1988). Because of the increase in time spent closer to and on the

ground, infected birds have a higher risk of predation.

Host behavior is not limited to changes in activity or locomotion. Behavior affecting

reproductive success is also influenced by parasite infection (Scott 1988). Because of a general

preference for healthy mates with high fitness, parasites affect reproductive success of

individuals by decreasing the chance of mating for infected individuals. In monogamous

species, individuals may prefer to choose a mate that will be able to help defend a territory, build

a nest, feed the offspring, and help with parental care. If activity of an individual is

compromised because of muscle soreness and pain, it will be less likely chosen as a mate. For

example, infected female mice are copulate less then uninfected females and males are less likely
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to mate with infected females (Edwards and Barnard 1987). However, while female voles

(Microtus ochrogaster) successfully distinguish between males infected with Trichinella spiralis

and uninfected males by olfactory cues, they show no preference in mates (Klein et al. 1999). T.

pseudospiralis infection has no effect on mate choice through courtship displays in Amercian

kestrels (Henderson et al. 1995).

Although Trichinella infection may not affect preference in mates, infection may result in

other behavioral changes affecting reproductive success. Infection of T. spiralis in mice causes

dominant males to lose their dominance position to uninfected mice (Rau 1984a). Infected mice

also assume subordinate positions when challenged by other mice (Rau 1983b). Subordinate

males generally have lower fitness, occupy less than optimal habitat, and can be more susceptible

to predation. This has implications for populations in that infection can reduce the fitness of the

hosts and facilitate transmission of the parasite through increased predation (Rau 1984).

Trichinosis can also affect the ability of females to rear young. T. spiralis infection in

mice results in lower litter size, decreased survival of progeny, and low growth rate in surviving

offspring (Weatherly 1971).

Effects of Trichinella infection on reproductive success are not limited to mammals. T.

psuedospiralis infections reduce the reproductive success of American kestrels and likely other

birds of prey. Laying of the first egg may be delayed by a week compared to uninfected females

and infected females ability to lay additional eggs if the first clutch is lost is also impaired. Egg

loss due to breaking can be considerably higher in infected birds, almost 18 times higher for

kestrels. Finally, infected kestrels produced only 25% of the young that uninfected birds

produced (Saumier et al. 1986).

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Implications for wildlife management and conservation

Trichinella spp. infections have been shown to have important affects on wildlife

behavior specifically survival and reproduction, the two main factors affecting population

growth, birth and death (Gotelli 1998). Thus high rates of infection may limit population growth

of host species in North America. This is an important factor to include in all population

monitoring programs. In fact, Trichinella has already been suspected in limiting population

density of big cats in Kruger National Park in Africa (Nelson 1990).

In areas or regions where Trichinella is a concern, there are several steps managers can

take in order to control the spread of this parasite. Because one route of infection relies on the

scavenging of infected carcasses, minimizing carnivore exposure to domestic livestock carcasses

and farm garbage could help prevent large outbreaks of T. spiralis in wildlife. Requiring the

removal and proper disposal of hunted carcasses instead of leaving the carcass in the field after

skinning, especially carcasses of carnivores, can minimize infection of other carnivores (Pozio et

al. 2001). Using carnivore carcasses for trapping should be banned in areas where Trichinella is

a concern. However, because T. nativa can exist in the cyst form for so long and no apparent

negative effects of infection have been reported for wildlife, careful carcass removal and other

management strategies are probably unnecessary for this parasite species. Finally, educating the

public about proper handling and care of game meat to avoid human infection, especially in the

Arctic region, will prevent future human outbreaks.

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