In nature, the ecosystemic relations in which an organism causes a harm to another one for his or her own benefit are called antagonistic ones. The main example of antagonistic relations are those in which one organism nourishes by harming another one, in particular by eating it. The two main instances of these relations are parasitism and predation.
The term “parasite” is sometimes used to mean all kind of organisms that interact with another host organism in a way that is positive for the parasite and negative for the host organism. In other cases, a distinction is made between parasitism and parasitoidism. Both parasites and parasitoids have a similar life history in that they spend a great part of their life obtaining nourishment from a host. But parasitoids, unlike parasites, ultimately sterilize or kill, and sometimes consume, their host. So sometimes a distinction is made between parasites and parasitoids, while in other cases the term “parasite” is used broadly to name all kind of organisms that nourish from a host, including parasitoids.
Most wild animals harbor different types of parasites. Many of them are microbial pathogens such as viruses, though the harms that cause are often commonly considered as diseases. But others are larger organisms. Sometimes they are animals too.
The victims of parasites are not only harmed because of the direct pain and distress parasites cause them, or because they kill them (in the case of parasitoids). They are also harmed in other, indirect ways. Their capacity to act is also affected by it. Some parasites have been even shown to cause behavioral alterations in their hosts (particularly intermediate hosts) such that the susceptibility to predators (final hosts) is significantly increased.1
Parasites have a relatively long period of interaction with the host organism, unlike the relatively short interaction between predator and prey during predation, due to which the harm they inflict to their victims can be significantly higher. We will now see some different forms of parasitism.
Parasites may be endoparasites or ectoparasites. Endoparasites live inside the host’s body: in the blood, tissues, body cavities, digestive tract and other organs, consuming and reproducing from internal resources. Common types include protozoa (single celled organisms) and helminths (multicellular worms: cestodes, nematodes and trematodes). Ectoparasites also live off the host’s resources but they do it from outside the body, usually living on its surface (skin or fur). Some common types are arthropods, such as ticks and mites.
In addition, another distinction can be made between microparasites and macroparasites. The former are those that can be seen by the naked human eye, while the latter can be seen with the use of a microscope or special lens.
It is rare for a free-living organism in the wild to not have multiple parasites from a variety of species at any given time. It has been estimated that parasites may outnumber free-living species by four to one.2 Parasites may be host-specific or generalistic, the latter usually limited to a taxonomic group, such as fish, birds or mammals.
Some parasites are called hyperparasites because they feed on other organisms that are also parasites themselves. They are not to be confused with superparasites, which are those that live in large populations within a single host (this happens in particular in the case of wasps larvae that are parasites of caterpillars).3 The following are some examples of prevalent parasites among wild animals.
Trichinella is a nematode (parasitic roundworm) found worldwide among wild animals, mostly reported in wild boars and other mammals.4 It is responsible for Trichinellosis, a disease caused by the ingestion of cysts hosted in a prey. As the larvae get to the small intestine, they reproduce and enter the blood stream, affecting various organs such as the retina, myocardium and skeletal muscle cells, causing edema, muscle pain, fever, and weakness. In its more severe versions, it can be fatal, leading to myocarditis, encephalitis or pneumonia.
Echinoccus spp. is a cestode (parasitic tapeworm) transmitted between ungulates (white-tailed deer, moose, caribou, elk), small mammals (mice, voles, and rats) and carnivores (wolves, coyotes, foxes, cats, hyenas) through the trophic chain. The worm lives in cysts in the internal organs (e.g. the lungs) of the intermediate host which are then passed, after consumption, to the definitive host’s intestine. The accidental ingestion of the definitive host’s feces leads to a new cycle of infection by the intermediate hosts. Echinococcosis, the resultant disease, is responsible for bodily weakness, impairment of movement and organ damage.
Leishmania is a parasite responsible for the disease l eishmaniasis, transmitted to wild canids5 by the bite of sandflies. The fly becomes infected by sucking on the blood of an already contaminated animal and becomes a vector of the disease. It then passes it on to another host through infected saliva during the bite process. The severity of its symptoms vary from sores on the bite’s site to leprosy-like lesions and tissue damage to nose and mouth. In its more severe forms it may lead to death.
Sarcoptes scabiei canis
The canine sarcoptic mite is an ectoparasite responsible for the Sarcoptic mange disease abundant in wild mammals such as cats, pigs, horses and various other species.6 The infection causes an allergic reaction to the mite, resulting in intense scratching and biting. The general condition of infected animals is often very weak and its symptoms have been shown to be intensified by the combination with food deprivation and other diseases. A severe form of the disease affecting foxes has been responsible for causing high rates of mortality to foxes in Europe. Foxes are usually a common definitive host of many other parasites, such as several genus of Taenia (cestode), Crenosoma (lung worms) and Filaroides (respiratory tract), among many others,7 which aggravates their debilitating condition.
Babesia is a protozoan parasite prevalent in wild mammals, particularly wild ungulates8 responsible for babesiosis, a disease very similar to malaria. The parasite is passed on to the host through saliva released during the bite of a mite. Once it reaches the red blood cells, the parasites reproduce and multiply, causing, among its most severe effects, hemolytic anemia, jaundice and hemoglobinuria. It is a potentially fatal disease.
Common parasites harbored by mammals are often shared with other species. Toxoplasma gondii, for example, is a protozoan parasite widespread among wild mammals and birds. It is primarily harbored by felids, however, it has been shown to affect other species such as starlings and rodents. Toxoplasmosis, the corresponding disease, has been reported as a cause of mortality for hares, Australian marsupials, lemurs and small primates.9 Even though the parasite may be asymptomatic in some cases, for those individuals with a general weak condition, it can cause encephalitis and affect eyes, heart and liver.
Another example is Giardia lamblia, a protozoan parasite that causes giardiasis, a prevalent disease among beavers, various ungulates and waterfowl.10 The disease is acquired through waters contaminated with cysts from feces from infected animals. Intestinal symptoms are usually associated with the infection, such as chronic diarrhea, abdominal cramps, nausea, dehydration and weight loss.
Wild birds commonly suffer from trichomonosis, a disease caused by the parasite Trichomonas. It is a debilitating disease which usually affects mouth, oesophagus, crop and glandular stomach of birds as well as other organs such as the liver. The disease varies from a mild condition to death shortly after infection. The frequency of trichomonosis in wild birds also varies according to the species, ranging from frequent in pigeons and doves, common in falcons and hawks, occasional in owls to rare in songbirds.11
Haemosporida is a microscopic, intracellular parasitic protozoan transmitted from infected to noninfected birds by biting flies. More than 68% of over 3,800 species of birds examined were hosts of the parasite, including ducks, geese and swans. Wild turkeys and pigeons also present high rates of infection. Animals with parasites present with anemia and weight loss, among other symptoms. It is a cause of mortality for young birds.12
Another debilitating parasitic protozoan found in wild birds (mostly, waterfowl) is Sarcocystis. The bird becomes infected after ingestion of food or water contaminated with carnivore cysted feces. The parasite then develops in the intestine of the bird and manages to reach the bloodstream where it produces new cysts. The resultant condition is the loss of muscle tissue which, among other debilitating effects, increases the host’s susceptibilty to predation.
Both land and water wild birds are also frequently parasitized by different types of worms. Depending on the severity of the infection, birds may experience from minor weakness to gross body lesions. Eustrongylidosis, for example, a disease caused by various genus of roundworms, results in large visible tunnels on the stomach or intestine of the infected birds, with bacterial peritonitis and secondary infections as well as thick-walled granulomas.
Other extensively reported parasites in birds are tracheal worms. These obstruct the trachea and bronchi, resulting in major respiratory distress. As a response, infected birds usually cough, sneeze and shake their heads trying to resist the parasites. As a result, they may loose body mass, display anemia and often die of starvation.13 A similarly debilitating worm is the heartworm, reported among swan and geese, it is responsible for a general lethargic condition.
Haemorpoteus, a protozoan parasite, transmitted by blood sucking insects, has been reported in various species of reptiles and amphibians, mostly turtles and tortoises,14 debilitating skeletal muscles and other organs, such as the liver. Other parasitic infections include Entamoeba invadens, a protozoan that causes colitis, abscesses of the liver and other organs, and sometimes even death15 and spirochid trematodes (turtles and snails)16 affecting major arteries and the heart.17 Other parasitic infections include cryptosporidiosis, reported in a variety of reptiles, mostly in snakes and lizards, causing regurgitation, diarrhea, weight loss and hypertrophy of the gastric mucosa.18
Ichneumonidae and Braconidae wasps
Among the best known cases of parasitism among invertebrates there is the case of Ichneumonidae and Braconidae wasps. These animals lay their eggs in the bodies of other insects, such as caterpillars or ants. When the eggs hatch, they start to eat their host alive, respecting the host vital organs until the end. Only when the edible non vital parts of the host has been eaten the host is killed. Some of these wasps are hyperparasites that lay their eggs in the bodies of other parasite wasps.19 The case of these parasitoids, together with that or predator prolonging the agony of their victims, famously led Charles Darwin to claim:
There seems to me too much misery in the world. I cannot persuade myself that a beneficent and omnipotent God would have designedly created the Ichneumonidae with the express intention of their feeding within the living bodies of Caterpillars, or that a cat should play with mice.”20
Predation is responsible for some of the greatest suffering wild animals experience in nature. Although some animals have evolved defenses against predators, most studies of predator-prey interactions show that large numbers of animals are killed by predators.21
The methods by which predators kill and consume their prey are diverse. The amount of time it takes before the prey is killed also varies. Some predators kill their prey before eating their bodies. Other predators, such as hyenas, routinely eat their prey while the prey animal is still alive. Crocodiles clamp onto their prey and submerge them underwater until they drown. Some animals, such as herons and some species of snakes, swallow their prey whole and digest them alive.
It’s difficult to estimate the suffering undergone by animals while they are being hunted and killed. It’s possible that the suffering may not be as bad as it first appears due to the release of endorphins which reduce the perception of pain and stress. However, we don’t want to underestimate the pain that is experienced by animals when they are chased and attacked.
The following gives a vivid account of a female lion killing a zebra:
The lioness sinks her scimitar talons into the zebra’s rump. They rip through the tough hide and anchor deep into the muscle. The startled animal lets out a loud bellow as its body hits the ground. An instant later the lioness releases her claws from its buttocks and sinks her teeth into the zebra’s throat, choking off the sound of terror. Her canine teeth are long and sharp, but an animal as large as a zebra has a massive neck, with a thick layer of muscle beneath the skin, so although the teeth puncture the hide they are too short to reach any major blood vessels. She must therefore kill the zebra by asphyxiation, clamping her powerful jaws around its trachea (windpipe), cutting off the air to its lungs. It is a slow death. If this had been a small animal, say a Thomson’s gazelle (Gazella thomsoni) the size of a large dog, she would have bitten it through the nape of the neck; her canine teeth would then have probably crushed the vertebrae or the base of the skull, causing instant death. As it is, the zebra’s death throes will last five or six minutes.”22
Animals have evolved a great array of defenses against predators, showing predation is a powerful selecting force in nature. Examples of these defenses are chemical defenses, warning coloration, camouflage, and mimicry. An example of a prey species that has a chemical defense is the bombardier beetle. This beetle ejects a hot spray of noxious chemicals at attackers. Warning coloration is coloration that prey species have evolved that show off an organism’s bad taste. Camouflage is coloration that organisms have evolved to better blend in to their surrounding and thereby reduce the risk of being eaten by a predator. Mimicry involves looking like another species. This can occur when multiple toxic species undergo convergent evolution to look alike or when a palatable species evolves to look like an unpalatable species. Even more defenses exist than were mentioned here, all pointing to predation as a strong selecting force. Despite these defenses, suffering and death due to predation is still prevalent, as has been documented through nearly 1,500 predator-prey studies that ecologists have carried out, in which 72% showed a large reduction in the number of prey animals due to the action of predators.23
This is also evident from the manner in which prey and predator populations oscillate in a predator-controlled system where the size of the prey population is determined by predation.
Many people believe ecosystems have some perfect balance at which predators kill a certain number of prey, keeping both populations at stable levels. In this picture, there are no disturbances or alterations (at least until humans appear). This is far from the truth, though. Predation leads to cycles in the numbers of predators and their prey that causes animals of both types to die through time. This happens as follows. Predation reduces the prey population. As a result, the predators have fewer animals to hunt. Therefore, some predators will starve and die, so their own numbers will be reduced. With fewer predators, the prey population increases again. As a result, there will be more prey animals than the existing predators can hunt, so the number of predators will grow. This will increase predation, causing the prey population to dwindle. The cycle will then repeat.24
These processes are well known and occur among many different animals. In population dynamics, this is explained by Lotka-Volterra models.25 These models deal with how animal populations vary, and they show that predator-prey interactions affect how their populations vary through time.
These are called stable predator-prey interactions (even though, as we have seen, they are not really so stable when we consider the animals involved). Unstable predator-prey interactions sometimes occur, too, in which predators eventually exterminate their prey.26
There may be other factors that affect the animals. For instance, the predators may have other prey, there may be other predators that kill the same prey, or there may be other predators that kill the predators. There may be additional limiting factors such as a lack of food for the prey, harmful temperature or other weather conditions, or lack of water. The Lotka-Volterra models together with these other factors explain why suffering and death are found not only among prey but also among predators.
As explained in Population dynamics and animal suffering, the basic reason that there is so much suffering and death in the wild is the fact that, while many animals come into existence, there are limiting factors that impede the population growth of a particular species in a particular area. Factors such as climate and food availability cause many animals to die, probably in most cases in pain. There is often an interaction between predation and these other factors.
For instance, it has been well documented that when there are predators in a certain area, animals that can be hunted by the predators may become more cautious and take few risks when looking for food. Because of this, they may become malnourished or even starve to death.27 This is known among ecologists as the “ecology of fear”, and the landscapes where this occurs are “landscapes of fear.”
Predators have a variety of adaptations that enable them to catch their prey, including speed, camouflage, and advanced senses. Adaptations to kill prey include sharp teeth and claws, venom, stingers, and powerful jaws. There are many ways that prey animals are killed. Large mammals are some of the most well-known predators, partly because their effects are so visible. Wolves may kill their prey by tearing at the rectum or genitalia and allowing the animals to bleed profusely until sufficiently weakened, at which point the wolf will begin to eat them alive. Alternatively, they may disembowel the prey animal. Coyotes bite the legs of their prey as they chase them, until the prey is weakened enough to be killed. Coyotes sometimes kill their prey faster than some other predators, either by suffocating them or ripping their throats out. Suffocation is, of course, a slow death, but it’s faster than being disembowel or eaten alive. However, coyotes don’t always kill their prey immediately, leaving them to die of shock, blood loss, or infection. Cougars also kill their prey by suffocating them. Cougars an other predators may also kill their prey by puncturing the prey’s throat or crushing the skull. Bobcats and lynxes tackle their prey to the ground and claw at them and bite them on their windpipes, causing them to die of suffocation or shock. Bears maul their prey and bite them many times along the spine, which means it takes a long time for their prey to die. Komodo dragons and hyenas have been seen eating their prey alive.
Insects sometimes eat much larger animals, and this is likely to be a particularly painful death, since the process is so slow. Beetles can eat much larger animals, such as frogs. The beetle first bites the frog, causing a violent reaction that suggests severe pain. After paralyzing the frog with poison by biting her, the beetle eats the frog from the legs up over the course of several hours. Praying mantises have been known to eat small birds.Centipedes have been seen to kill and eat rodents such as mice similarly, by using their poison to paralyze them. Spiders can also eat larger animals such as birds, snakes, frogs, lizards, mice, and bats. They first inject their prey with venom. Next they may grind up and eat the prey with their fangs. Alternatively, they may inject the prey with proteins that liquefy their internal organs, and suck out the liquid. In other cases, animals get trapped in spider webs and die of exhaustion, starvation, dehydration, or excessive heat.
Snakes often swallow their prey alive, and the prey animals die in the snakes’ mouths or in their digestive tracts.
Sometimes predators eat parts of the bodies of animals without killing them, a phenomenon similar to parasitism. Animals raised by humans for food are often the victims of this, but there is no reason to believe this does not also occur in the wild. Coyotes eat the tails, genitals, and hindquarters of live cattle, particularly calves. Coyotes and bears eat the udders of live cows. Birds often peck out the eyes of animals smaller than themselves.
Some animals will eat animals that are not typically part of their diets if given the opportunity. For example, turtles and fishes will eat birds, and some frogs will eat mice. There have even been examples of cows eating baby chickens.
Finally, carnivorous plants drown their victims or kill them with chemicals. In most cases they trap insects or other invertebrates, although some of them may also catch small vertebrates such as frogs, rats, lizards or small birds.
Abrams, P. A. & Matsuda, H. (1993) “Effects of adaptive predatory and anti-predator behaviour in a two-prey one-predator system”, Evolutionary Ecology, 7, pp. 312-326.
Animals eating animals (2010-2014) Animals eating animals: Nature at its finest can be a thing of beauty. Here’s images of the carnage that results, animalseatinganimals.com [accessed on 30 May 2014].
Beddington, J. R. & Hammond, P. S. (1977) “On the dynamics of host-parasite-hyperparasite interactions”, Journal of Animal Ecology, 46, pp. 811-821 [accessed on 16 December 2016].
Biro, P. A.; Abrahams, M. V.; Post, J. R. & Parkinson, E. A. (2004) “Predators select against high growth rates and risk-taking behaviour in domestic trout populations”, Proceedings of the Royal Society London B, 271, pp. 2233-2237 [accessed on 3 March 2014].
Blamires, S. J.; Piorkowski, D.; Chuang, A.; Tseng, Y.-H.; Toft, S. & Tso, I.-M. (2015) “Can differential nutrient extraction explain property variations in a predatory trap?”, Royal Society Open Science, 2 [accessed on 22 March 2015].
Boesch, C. (1991) “The effect of leopard predation on grouping patterns by forest chimpanzees”, Behaviour, 117, pp. 220-142.
Bonta, M.; Gosford, R.; Eussen, D.; Ferguson, N.; Loveless, E. & Witwer, M. (2017) “Intentional fire-spreading by “firehawk” raptors in Northern Australia”, Journal of Ethnobiology, 37, pp. 700-718.
Brooker, R. J.; Widmaier, E. P.; Graham, L. E. & Stiling, P. D. (2012 ) Biology: For Bio 211 and 212, 2nd ed., New York: McGraw-Hill.
Brown, J. S.; Laundre, J. W. & Gurung, M. (1999) “The ecology of fear: Optimal foraging, game theory, and trophic interactions”, Journal of Mammalogy, 80, pp. 385-399.
Bunke, M.; Alexander, M. E.; Dick, J. T. A.; Hatcher, M. J.; Paterson, R. & Dunn, A. M. (2015) “Eaten alive: Cannibalism is enhanced by parasites”, Royal Society Open Science, 2 [accessed on 22 March 2015].
Cressman, R. (2006) “Uninvadability in N-species frequency models for resident-mutant systems with discrete or continuous time”, Theoretical Population Biology, 69, pp. 253-262.
Cressman, R. & Garay, J. (2003a) “Evolutionary stability in Lotka-Volterra systems”, Journal of Theoretical Biology, 222, pp. 233-245.
Cressman, R. & Garay, J. (2003b) “Stability in N-species coevolutionary systems”, Theoretical Population Biology, 64, pp. 519-533.
Cressman, R. & Garay, J. (2006) “A game-theoretic model for punctuated equilibrium: Species invasion and stasis through coevolution”, Biosystems, 84, pp. 1-14.
Edmunds, M. (1974) Defence in animals: A survey of anti-predator defences, New York: Longman.
Eisenberg, J. N. S.; Washburn, J. O. & Schreiber, S. J. (2000) “Generalist feeding behaviour of Aedes sierrensis larvae and their effects on protozoan populations”, Ecology, 81, pp. 921-935 [accessed on 12 April 2014].
Eshel, I.; Sansone, E. & Shaked, A. (2006) “Gregarious behaviour of evasive prey”, Journal of Mathetical Biology, 52, pp. 595-612.
Faria, C. (2016) Animal ethis goes wild: The problem of wild animal suffering and intervention in nature, Barcelona: Universitat Pompeu Fabra, pp. 75-85.
Fiksen, Ø.; Eliassen, S. & Titelman, J. (2005) “Multiple predators in the pelagic: Modelling behavioural cascades”, Journal of Animal Ecology, 74, pp. 423-429 [accessed on 14 January 2014].
Godfray, H. C. J. (2004) “Parasitoids”, Current Biology, 14 (12), R456.
Hochberg, M. E. & Holt, R. D. (1995) “Refuge evolution and the population dynamics of coupled host-parasitoid associations”, Evolutionary Ecology, 9, pp. 633-661.
Hofbauer, J. & Sigmund, K. (1998) Evolutionary games and population dynamics, Cambridge: Cambridge University Press.
Holbrook, S. J. & Schmitt, R. J. (2002) “Competition for shelter space causes density-dependent predation mortality in damselfishes”, Ecology, 83, pp. 2855-2868 [accessed on 30 October 2013].
Holt, R. D. (1977) “Predation, apparent competition, and structure of prey communities”, Theoretical Population Biology, 12, pp. 197-229.
Holt, R. D. (1985) “Population dynamics in two-patch environments: Some anomalous consequences of an optimal habitat distribution”, Theoretical Population Biology, 28, pp. 181-208.
Holt, R. D. & Lawton, J. H. (1994) “The ecological consequences of shared natural enemies”, Annual Review of Ecology and Systematics, 25, pp. 495-520.
Hopla, C. E.; Durden, L. A. & Keirans, J. E. (1994) “Ectoparasites and classification”, Revue scientifique et technique (International Office of Epizootics), 13, pp. 985-1017.
Huffaker, C. B. (1958) “Experimental studies on predation: dispersion factors and predator-prey oscillations”, Hilgardia, 27, pp. 343-383.
Hughes, R. N. & Taylor, M. J. (1997) “Genotype-enviromental interaction expressed in the foraging behaviour of dogwhelks, Nucella lapillus (L.) under simulated environmental hazard”, Proceedings of the Royal Society London B, 264, pp. 417-422 [accessed on 2 January 2014].
Internet Center for Wildlife Damage Management (2005) “Livestock and animal predation identification”, icwdm.org [accessed on 4 June 2013].
Jervis, M. A. & Kidd, N. A. C. (1986) “Host-feeding strategies in hymenopteran parasitoids”, Biological Reviews, 61, pp. 395-434.
Leeuwen, E. van; Jansen, V. A. A. & Bright, P. W. (2007) “How population dynamics shape the functional response in a one-predator-two-prey system”, Ecology, 88, pp. 1571-1581 [accessed on 13 March 2014].
Loss, S. R.; Will, T. & Marra, P. P. (2013) “The impact of free-ranging domestic cats on wildlife of the United States”, Nature Communications, 4, 1396.
Marrow, P.; Dieckmann, U. & Law, R. (1996) “Evolutionary dynamics of predator-prey systems: An ecological perspective”, Journal of Mathetical Biology, 34, pp. 556-578.
McMahan, J. (2010a) “The meat eaters”, The New York Times (online), 19 September [accessed on 23 March 2013].
McMahan, J. (2010b) “Predators: A response”, The New York Times (online), 28 September [accessed on 12 May 2013].
McNamara, J. M. & Houston, A. I. (1992) “Risk-sensitive foraging: A review of the theory”, Bulletin of Mathematical Biology, 54, pp. 355-378.
Mnaya, B.; Wolanski, E. & Kiwango, Y. (2006) “Papyrus wetlands a lunar-modulated refuge for aquatic fauna”, Wetlands Ecology and Management, 14, pp. 359-363.
Olivier, D. (2016) “On the right of predators to life”, David Olivier’s blog, April 30 [accessed on 16 December 2016].
Pielou, E. C. (1977) Mathematical ecology, New York: Wiley.
Ray, G. (2017) “Parasite load and disease in wild animals”, Wild-Animal Suffering Research [accessed on 24 November 2017].
Roemer, G. W. & Donlan, C. J. (2004) “Biology, policy and law in endangered species conservation: I. The case history of the Island Fox on the Northern Channel Islands”, Endangered Species UPDATE, 21, pp. 23-31.
Roemer, G. W.; Donlan, C. J. & Courchamp, F. (2002) “Golden eagles, feral pigs, and insular carnivores: How exotic species turn native predators into prey”, Proceedings of the National Academy of Sciences of the USA (PNAS), 99, pp. 791-796 [accessed on 26 December 2013].
Ruxton, G. D. (1995) “Short term refuge use and stability of predator-prey models”, Theoretical Population Biology, 47, pp. 1-17.
Saleem, M.; Sadiyal, A. H.; Prasetyo, E. & Arora, P. R. (2006) “Evolutionarily stable strategies for defensive switching”, Applied Mathematics and Computation, 177, pp. 697-713.
Sapontzis, S. F. (1984) “Predation”, Ethics and Animals, 5, pp. 27-38 [accessed on 21 February 2013].
Schutt, B. (2017) Cannibalism: A perfectly natural history, Chapel Hill: Algonquin Books of Chapel Hill.
Sih, A. (1987) “Prey refuges and predator-prey stability”, Theoretical Population Biology, 31, pp. 1-12.
Vincent, T. L. & Brown, J. S. (2005) Evolutionary game theory, natural selection and Darwinian dynamics, Cambridge: Cambridge University Press.
Voigt, K. & Voigt, S. (2015) Cats and wildlife, Wight: Wight Nature Wildlife Rescue and Rehabilitation.
Williams, T. M.; Kendall, T. L.; Richter, B. P.; Ribeiro-French, C. R.; John, J. S.; Odell, K. L.; Losch, B. A.; Feuerbach, D. A. & Stamper, M. A. (2017) “Swimming and diving energetics in dolphins: A stroke-by-stroke analysis for predicting the cost of flight responses in wild odontocetes”, Journal of Experimental Biology, 220, pp. 1135-1145 [accessed on 2 May 2017].
Ylönen, H.; Pech, R. & Davis, S. (2003) “Heterogeneous landscapes and the role of refuge on the population dynamics of a specialist predator and its prey”, Evolutionary Ecology, 17, pp. 349-369.
1 Gopko, M.; Mikheev, V. N. & Taskinen, J. (2017) “Deterioration of basic components of the anti-predator behavior in fish harboring eye fluke larvae”, Behavioral Ecology and Sociobiology, 71, 68.
2 Zimmler, C. (2003) Parasite Rex: Inside the bizarre world of nature’s most dangerous creatures, New York: Atria.
3 Sullivan, D. J. & Völkl, W. (1999) “Hyperparasitism: Multitrophic ecology and behaviour”, Annual Review of Entomology, 44, pp. 291-315. Van Alphen, J. J. & Visser, M. E. (1990) “Superparasitism as an adaptive strategy for insect parasitoids”, Annual Review of Entomology, 35, pp. 59-79.
4 Gortázar, C.; Ferroglio, E.; Höfle, U.; Frölich, K. & Vicente, J. (2007) “Diseases shared between wildlife and livestock: A European perspective”, European Journal of Wildlife Research, 53, pp. 241-256.
7 Simpson, V. R. (2002) “Wild animals as reservoirs of infectious diseases in the UK”, The Veterinary Journal, 163, pp. 128-146.
10 Martin, C.; Pastoret, P. P.; Brochier, B.; Humblet, M. F. & Saegerman, C. (2011) “A survey of the transmission of infectious diseases/infections between wild and domestic ungulates in Europe”, Veterinary Research, 42 [accessed on 21 October 2016].
11 Graczyk, T. K.; Fayer, R.; Trout, J. M.; Lewis, E. J.; Farley, C. A.; Sulaiman, I. & Lal, A. A. (1998) “Giardia sp. cysts and infectious Cryptosporidium parvum oocysts in the feces of migratory Canada geese (Branta canadensis)”, Applied and Environmental Microbiology, 64, pp. 2736-2738.
12 Cole, R. A. & Friend, M. (1999) Parasites and parisitic diseases (field manual of wildlife diseases), sec. 5, Lincoln: University of Nebraska [accessed on 16 April 2014].
15 Jovani, R.; Amo, L.; Arriero, E.; Krone, O.; Marzal, A.; Shurulinkov, P.; Tomás, G.; Sol, D.; Hagen, J.; López, P.; Martín, J.; Navarro, C. & Torres, J. (2004) “Double gametocyte infections in apicomplexan parasites of birds and reptiles”, Parasitology Research, 94, pp. 155-157.
16 Bradford, C. M.; Denver, M. C., & Cranfield, M. R. (2008) “Development of a polymerase chain reaction test for Entamoeba invadens”, Journal Zoological Wildlife Medicine, 39, pp. 201-207.
17 Tkach, V. V.; Snyder, S. D.; Vaughan, J. A. (2009) “A new species of blood fluke (Digenea: Spirorchiidae) from the Malayan Box turtle, Cuora amboinensis (Cryptodira: Geomydidae) in Thailand”, Journal of Parasitology, 95, pp. 743-746.
18 Chen, H.; Kuo, R. J.; Chang, T. C.; Hus, C. K.; Bray, R. A. & Cheng, I. J. (2012) “Fluke (Spirorchiidae) infections in sea turtles stranded on Taiwan: Prevalence and pathology”, Journal of Parasitology, 98, pp. 437-439.
19 Schumacher, J. (2006) “Selected infectious diseases of wild reptiles and amphibians”, Journal of Exotic Pet Medicine, 15, pp. 18-24.
20 Spencer, H. (1926) “Biology of the parasites and hyperparasites of aphids”, Annals of the Entomological Society of America, 19, pp. 119-157. Vinson, S. B. (1976) “Host selection by insect parasitoids”, Annual Review of Entomology, 21, pp. 109-133. Gauld, I. D. (1988) “Evolutionary patterns of host utilization by ichneumonoid parasitoids (Hymenoptera: Ichneumonidae and Braconidae)”, Biological Journal of the Linnean Society, 35, pp. 351-377. Godfray, H. C. J. (1994) Parasitoids: Behavioral and evolutionary ecology, Princeton: Princeton University Press.
21 Darwin, C. (2007 ) “Charles Darwin to Asa Gray, May 22nd 1860”, in Darwin, F. (ed.) The life and letters of Charles Darwin, vol. II, Middleton: The Echo Company, pp. 431-432.
22 McGowan, C. (1997) The raptor and the lamb: Predators and prey in the living world, New York: Henry Holt and Company, pp. 12-13.
23 Brooker, R. J.; Widmaier, E. P.; Graham, L. E. & Stiling, P. E. (2010) Biology, New York: McGraw-Hill, ch. 57.2.
25 Lotka-Volterra equations are first-order differential equations which can be presented as follows:
dx/dt = x (A – By)
dy/dt = –y (C–Dx)
where t represents time; x is the number of the animals killed as prey of a certain species (such as, say, hares);y is the number of the predators of a certain species (such as, say, linxes); A represents the growth rate of the prey animals; B is the rate at which the predators of the species under study kill the prey; C is the death rate of the predators; and D is the rate of growth of the predators due to the fact that they kill the prey under study. They therefore study how the populations of the animals killed as prey and the predators vary through time, under the assumption that the factors that affect this are the one represented by A, B, C and D.
See Lotka, A. J. (1920) “Analytical note on certain rhythmic relations in organic systems”, Proceedings of the National Academy of Sciences Of the USA (PNAS), 6, pp. 410-415 [accessed on 12 February 2013]; Volterra, V. (1931) “Variations and fluctuations of the number of individuals in animal species living together”, in Chapman, R. N. (ed.) Animal ecology, New York: McGraw-Hill, pp. 3-51.
26 These processes have been studied in different places and with different species of animals. A well known case is that of the hunt of moose by wolves on Isle Royale in Lake Superior, USA, which has been studied continuously since 1959. See Peterson, R. O. (1999) “Wolf-moose interaction on Isle Royale: The end of natural regulation?”, Ecological Applications, 9, pp. 10-16.
27 Horta, O. (2010) “The ethics of the ecology of fear against the nonspeciesist paradigm: A shift in the aims of intervention in nature”, Between the Species, 13 (10), pp. 163-87 [accessed on 21 October 2013].