Antagonism in nature: Interspecific conflict

This text is about interspecific antagonism in nature. Another text discusses fighting between animals of the same species, and another one deals with sexual conflicts. For information about other ways in which animals in the wild suffer, see our general section on the situation of animals in the wild.

In nature, the ecosystemic relations in which one organism benefits by causing harm to another are called “antagonistic relationships.” Antagonistic relationships arise because organisms have conflicting interests. For example, a tick might have an interest in feeding off the blood of a deer because this provides nourishment to the tick and thereby benefits him. This conflicts with the interests of the deer because part of her energy is siphoned off to feed the tick, and this can harm her by weakening her physical condition. The main examples of antagonistic relations are those in which one organism nourishes themself by harming another organism, in particular by parasitism or predation.

There can also be antagonistic relationships within species, when the interests of individuals of the same species conflict. For example, in environments with limited resources, animals will fight to secure territory, mates, or social status within a group. Some animals eat members of their own species, including siblings and children. We’ll discuss these kinds of relations in the text on intraspecific conflict. There can also be antagonistic relations between males and females within a species.

Two main cases of interspecies antagonistic relations are parasitism and predation. Predators are generally bigger or around the same size as the animals they prey upon, while parasites are usually much smaller.1 Predators usually kill several or many animals in their lifetimes, and their interactions with each are short-lived, usually consisting only of the chase and the kill. Parasites generally spend their whole lives within a single host, who they usually don’t kill. The exception to this are parasitoids that only interact with one host who they eventually kill. An example is the Ichneumonidae wasp family whose females lay their eggs in a live host such as a caterpillar. The larvae subsequently consume their host, who they only kill when they are about to abandon the body.

 

Parasitism and parasitoidism

Parasitism is extremely common.2 Most wild animals harbor a variety of parasites. Many of them are microbial pathogens such as viruses that can harm their hosts by causing disease. Others are larger organisms, even animals.

Some parasites cause little harm to the animals they infest. Some, however, cause pain and weaken them. Parasitoids ultimately kill the animals they infest. There are also indirect types of harm. For example, the actions of a parasite can cause fatigue, making it harder for the host to find food and avoid predators.

Some parasites castrate their hosts, leaving their other systems intact so that the host can survive, diverting the energy that would have gone into reproduction into sustaining the parasite.3

Some parasites cause behavioral changes in their hosts (particularly intermediate hosts) that make them more susceptible to predators (final hosts).4 Intermediate hosts provide an environment for the immature parasite to develop and grow. Final hosts are where sexually mature parasites reproduce. For example, the parasitic flukes Dicrocoelium dendriticum reproduce inside of the final host, grazing ruminants like cows or sheep, and the eggs are excreted in the host’s feces. The first intermediate host is a common snail, who consumes the feces and becomes infested by the larval parasites. The snail forms cysts around the parasites, which he then excretes. These cysts are consumed by the second intermediate host, an ant. The parasite is able to take control of the ant’s behavior, forcing him to climb to the top of a blade of grass where he will be eaten by a grazing animal, where the now mature parasite can reproduce.5

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 the host’s 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.

It is rare for an animal in the wild not to have multiple parasites of a variety of species at any given time. It has been estimated that parasites outnumber other animals by four to one.6 Parasites may be host-specific or generalistic, the latter usually limited to a taxonomic group, such as fishes, birds, or mammals.

Some parasites are called hyperparasites because they feed on other parasites. They are not to be confused with superparasites, which live in large populations within a single host (as with wasps whose larvae are parasites of caterpillars).7 The following are some examples of parasites prevalent among wild animals.

 

Parasites suffered by mammals

Trichinella

Trichinella is a nematode (parasitic roundworm) found worldwide among wild animals, mostly reported in wild boars and other mammals.8 It is responsible for Trichinellosis, a disease caused by the ingestion of microbial cysts. Once the larvae reach the small intestine, they reproduce and enter the bloodstream, affecting various organs such as the retina, myocardium, and skeletal muscle cells, causing edema, muscle pain, fever, and weakness. In severe cases, it can be fatal, leading to myocarditis, encephalitis, or pneumonia.

 

Echinococcus spp.

Echinoccus spp. is a cestode (parasitic tapeworm) transmitted between ungulates (white-tailed deer, moose, caribou and elk), small mammals (mice, voles, and rats), and larger predators (wolves, coyotes, foxes, cats, and hyenas) through the trophic chain. The worm lives in cysts in the internal organs (e.g. the lungs) of the intermediate host and are passed to the definitive host’s intestine after the final host eats the intermediate host. The ingestion of the definitive host’s feces leads to a new cycle of infestation in animals who are intermediate hosts. Echinococcosis, the resultant disease, causes bodily weakness, impairment of movement, and organ damage.

 

Leishmania

Leishmania is a flesh eating parasite responsible for the disease leishmaniasis, transmitted to wild canids9 when they are bitten by a sand fly. The fly becomes infested by sucking on the blood of an already contaminated animal. The fly passes it on to another host through saliva by biting. The severity of symptoms varies from sores on the site of the bite to leprosy-like lesions and tissue damage to the 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.10 The infestation causes an allergic reaction to the mite, resulting in intense scratching and biting, leading to crusted skin and bloody lesions. It may cause blindness and deafness. Infected animals often become very weak and the symptoms have been shown to be intensified when combined with food deprivation and other diseases. A severe form of the disease affecting foxes has been responsible for high mortality rates among European foxes. Foxes are 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,11 and this combination of parasites aggravates the debilitating effects of the sarcoptic mite.

 

Babesia

Babesia is a protozoan parasite prevalent in wild mammals, particularly wild ungulates12 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 shared by mammals and birds

Common parasites who infest mammals often afflict other species. Toxoplasma gondii, for example, is a protozoan parasite widespread among wild mammals and birds. It is primarily found in cats; however, it has been shown to affect other species such as starlings and species of rodents. Toxoplasmosis, the corresponding disease, has been reported as a cause of mortality for hares, Australian marsupials, lemurs, and other small primates.13 Even though the parasitic infestation may be asymptomatic in some cases, in weakened individuals it can cause encephalitis and affect the eyes, heart, and liver.

Another example is Giardia lamblia, a protozoan parasite that causes giardiasis, a disease prevalent among beavers, various ungulates, and water birds.14 The disease is acquired through waters contaminated with cysts from feces of infected animals. Intestinal symptoms are usually associated with the infestation, such as chronic diarrhea, abdominal cramps, nausea, dehydration, and weight loss.

 

Parasites suffered by birds

Trichomonosis

Wild birds commonly suffer from trichomonosis, a disease caused by the parasite Trichomonas. It is a debilitating disease which usually affects the mouth, oesophagus, crop, and glandular stomach of birds as well as other organs such as the liver. The severity of the disease varies from a mild condition up to death shortly after infestation. The frequency of trichomonosis in wild birds varies by species, ranging from frequent in pigeons and doves, common in falcons and hawks, occasional in owls, to rare in songbirds.15

The video below shows birds exhibiting symptoms of trichomonosis, including damaged beaks, difficulty swallowing, drowsiness, and inattention.

 

Haemosporida

Haemosporida is a microscopic, intracellular parasitic protozoan transmitted from infested to non-infested birds by fly bites. Of over 3,800 species of birds examined, more than 68% were hosts for the parasite, including ducks, geese, and swans. Wild turkeys and pigeons also show high rates of infestation. Animals with these parasites develop anaemia and weight loss, among other symptoms. It is a cause of mortality for young birds.16

 

Sarcocystis

Another debilitating parasitic protozoan found in wild birds (mostly waterfowl) is Sarcocystis. The bird becomes infested after ingestion of food or water contaminated with feces containing cysts. The parasite then develops in the intestine of the bird before reaching the bloodstream, where it produces new cysts. The infestation results in loss of muscle tissue which, among other debilitating effects, increases the host’s susceptibility to predation.

 

Worms

Both land and water birds are also frequently parasitized by different types of worms. Depending on the severity of the infestation, birds may experience a range of symptoms, from minor weakness to gross body lesions. Eustrongylidosis, for example, a disease caused by various genera of roundworm, results in large visible tunnels in the stomach or intestine of the infested 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. In response, infested birds usually cough, sneeze, and shake their heads trying to dislodge the parasites. They may lose body mass, display anemia, and often die of starvation.17 A similarly debilitating worm is the heartworm, reported among swans and geese. It is responsible for a general lethargic condition.

 

Common parasites among reptiles and amphibians

Protozoan infections

Haemoproteus, a protozoan parasite transmitted by blood sucking insects, has been reported in various species of reptiles and amphibians, mostly turtles and tortoises.18 It has debilitating effects on skeletal muscles and other organs such as the liver. Other parasitic infestations include Entamoeba invadens, a protozoan that causes colitis, abscesses of the liver and other organs, and sometimes death;19 and spirochid trematodes (turtles and snails)20 affecting major arteries and the heart.21 Other parasitic infections include cryptosporidiosis, reported in a variety of reptiles, mostly snakes and lizards, causing regurgitation, diarrhea, weight loss, and swelling of the gastric mucosa.22

 

Parasitism among invertebrates

Ichneumonidae and Braconidae wasps

Among the best known example of parasitism among invertebrates is the case of Ichneumonidae and Braconidae wasps. These animals lay their eggs in the bodies of other insects, such as caterpillars and ants. When the eggs hatch, the larvae start to eat their host alive, leaving the host’s vital organs intact until the end. Only when the edible nonvital parts of the host have been eaten is the host finally killed. Some of these wasps are hyperparasites, laying their eggs in the bodies of other parasite wasps.23

The video below shows wasp larvae emerging from the body of their caterpillar host.

 

Predation

One of the causes of suffering among wild animals is predation. At its most basic level, predation is an antagonistic relationship whereby one organism (the predator) obtains their energy by consuming another organism (the prey), in which the prey is alive when the predator attacks them.24 One of the standard definitions describes predation as a process through which a certain animal captures and kills another animal and then eats a part or all of that animal’s body.25

 

How do animals who are preyed upon die?

Animals who are preyed upon are killed and eaten in varied ways. The amount of time it takes before the victim is killed also varies. Some are killed by their predators before the predators eat their bodies. Some predators routinely eat the animals alive. 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 may not be as bad as it first appears due to the release of endorphins which reduce the perception of pain and stress. However, it is important not to underestimate the pain that is experienced by animals when they are attacked, and the fear and distress they may undergo while being chased and from living in fear of predators.

 

Invertebrates

By far the most numerous animals are invertebrates. It has been estimated, for example, that there are 10 quintillion individual insects alive at any one time,26 about 200 million insects for every human being.27 The invertebrate class also includes the rest of the arthropods (arachnids, crustaceans, myriapods); mollusks (octopuses, squids, snails, etc.); annelids (earthworms and leeches) and cnidarians (jellyfishes, sea anemones, etc.). Among them, we can find deadly predators such as the meat ant, and the blue ringed octopus, as well as animals who are preyed upon by others such as crabs, fruit flies, and bees. Some predators, such as meat ants and certain spiders, also eat vertebrates such as toads, small birds, and mammals. Epomis beetles paralyze their prey with venom (sometimes frogs or other large animals) and then eat them alive, as seen in the video below.

The vast majority of animals who are preyed upon are invertebrates. Below we will look at some of the ways invertebrates are preyed upon.

Bees are preyed upon by a range of animals including insects, birds, and mammals. Some species of hornets attack bees and either eat them themselves or bring their bodies to their nests to feed them to their larvae. The video below shows a beewolf wasp stalking and attacking a honeybee. While the bee is distracted feeding on nectar, the wasp pounces on her, then injects her with a deadly venom. The bee struggles against her attacker, but her stinger cannot penetrate the wasp’s armor. The wasp drinks nectar directly out of the mouth of her dead victim, then carries the bee’s body back to her nest to feed her own grub.

Other species of hornets storm beehives in order to eat the bee larvae within. In the video below, 30 Japanese giant hornets attack a beehive. The bees outnumber the hornets a thousand to one, yet they have no effective defenses against the giant hornets, one of which can kill up to 40 bees a minute. After killing all the honeybees, the hornets enter the hive and eat the flesh of the bee larvae within.

Some birds prey on bees too, rubbing off the stinger before eating the contents of the abdomen, including the honey stomach.28 It has been estimated that birds consume between 400 and 500 million tons of insects every year.29 That is tens or hundreds of billions of individual animals every year.

The video below shows wrens and thrushes, as well as a toad and a lizard, eating a swarm of cactus bees. As the male bees fight each other for females, the birds are able to pick them off with ease.

Spiders prey on insects, other spiders, and sometimes birds and lizards. There are over 48,000 known species of spider, all but one of which are predators. It has been estimated that spiders kill between 400 and 800 million tons of animals each year, the vast majority of which are arthropods.30 The most well known method is building webs and waiting for animals to fly into them and become stuck. Spiders are very sensitive to vibration, and, waiting at the center of their web, they can detect a trapped animal by the vibrations he makes. Usually the spider will wait for the trapped animal to become tired from his struggles to escape, then she moves in for the kill. Spiders have sharp fangs, and the majority use them to inject venom into the body of the animal they have captured, either killing or paralyzing them. Some spiders then wrap the animal in a silk cocoon. Finally, they excrete digestive enzymes which start to break down the animal’s body into a liquid form which they are able to consume. Depending on the kind of venom and the size and species of the captured animal, he may still be alive and capable of feeling pain during this process.

The video below shows a spider killing a fly caught in her web. The fly struggles a great deal but she is overpowered by the spider. After killing the fly, the spider begins to wrap her body in silk in preparation to consume her.

Other spiders will hunt and pounce on their victims instead of using webs. Below we can see a British Zebra Jumping spider hunt a greenbottle fly.

Some spiders can also kill and eat much larger animals such as birds, frogs, and bats.

Spiders are not only hunters; they are hunted too. Portia is a genus of jumping spider that specializes in hunting other spiders, particularly web building ones. They can adapt their hunting methods to hunt animals that neither they nor their ancestors have encountered before, suggesting a level of intelligence. Spiders are also eaten by birds, toads, and lizards. The video below shows one of the hunting techniques employed by the Portia spider against other spiders.

Octopuses eat crustaceans such as crabs and prawns, other molluscs such as whelks and clams, fishes, and other cephalopods, including other octopuses. Bottom dwelling octopuses move along the sea floor across rocks and crevices. When an octopus spots a crab, she propels herself rapidly towards him and pulls him towards her mouth with her strong arms. She then injects the crab with a paralyzing agent before tearing him apart with her beak. When they attack shelled molluscs, octopuses either force the shells apart or they drill a small hole into the shell and inject a nerve toxin that kills the animal, thus relaxing her muscles and allowing the octopus to remove the soft tissue. It can take around three hours to drill the hole into the shell.31

In the video below, we can see an octopus springing from a rock pool to catch a crab, then dragging him back under the water to eat him.

Cuttlefish also prey on crabs and fishes. They are capable of changing their skin color, either for camouflage or to hypnotize small animals like crabs with pulsing displays of color.32 In addition to their eight arms, they have two specialized tentacles with suckers which they can deploy extremely rapidly to catch crabs and fishes and pull them into their sharp beaks, which can break through crab shells. The video below shows a cuttlefish catching a crab.

Despite their intelligence and their capacity for camouflage, cephalopods are vulnerable to predators such as sharks, dolphins, and other cephalopods. The video below shows a Moray eel catching an octopus. The octopus attempts to cling to a rock with her tentacles, but the eel is too strong for her. They struggle for about ninety seconds before the eel manages to pull the octopus out of her hiding place and carries her back to his lair to eat.

 

Medium sized animals

When we think of predators, we tend to think of large animals. They are the ones we see in nature documentaries, wild animal parks, the media, and children’s books. They can also pose a threat to human beings. They are in the minority, however, even when we just consider vertebrates. The vast majority of vertebrate predators are much smaller than lions, crocodiles, and wolves. There are around 170,000 Jaguars,33 70,000 leopards, 30,000 cougars, 20,000 lions,34 7,000 cheetahs, and 3,000 tigers.35 Taken together, the most common species of big cat comprise fewer than 300,000 individuals. Smaller cats, by contrast, have a global population somewhere between 200 and 600 million, including approximately 100 million wild/feral animals. In the United States alone, domesticated cats kill between 6.3 and 22.3 billion mammals and 1.3 to 4 billion birds every year.36 As anyone who has witnessed a cat killing a mouse can attest, these are not quick deaths. Often domestic cats will “play” with the animals they capture until they finally succumb to their injuries.

Although cats are cute and usually harmless to humans, they are powerful and dangerous predators to mice. To put this in perspective, we must think about the relative size and weights of the animals in question.

We can see this if we consider the difference in size and weight between a human and a lion. An adult male lion weighs around 190 kg and may be up to 2.5 meters in length.37 Consider a human male who weighs 83.6 kg and is 1.75 meters tall.38 This puts the lion at less than 2.5 times the weight and 1.5 times the length/height of an adult man. In contrast, average adult domesticated cat weights between 4 and 5 kg, standing at 25 cm in height and 46 cm in length (excluding the tail), while an adult house mouse can be up to 10cm long (excluding tail) and can weigh up to 45 grams. This means a typical domesticated cat is around 100 times heavier and 4-5 times longer than a mouse. Being attacked by a cat may be significantly worse for a mouse than being attacked by a lion is for a human being. The lesson here is that the small size of a predator from a human viewpoint is irrelevant when considering the experiences of the animals they attack. We must be careful not to underestimate the fear and pain endured by prey animals at the claws and teeth of “small” predators.

Other animals of medium size and small vertebrates are predated by fishes or birds. Pikes, for example, eat fishes, frogs, small mammals, and birds, as well as invertebrates. Pikes have a distinctive method of devouring their victims: they catch them sideways in their jaws, then turn the animal around and swallow them whole, head first. For larger animals, they will first drown them before carrying them off to eat them. The video below shows a pike catching a duckling.

Some birds also prey upon a variety of other animals. Large ones include herons, who are freshwater and coastal birds found in every continent other than Antarctica. They eat fishes, amphibians, reptiles, crustaceans, small birds, and mammals. These birds typically swallow the animals they prey upon whole, often while they are still alive, although sometimes they drown them first. The first video shows a heron swallowing a chipmunk whole while he is still alive.

The second video sees a heron eating a rabbit who he appears to have killed by submerging her under the water until she drowned.

Large vertebrates

Predators of large animals are better known, but they are much less numerous than predators of small animals. Big cats are among the most familiar predators to many people. To give an idea how it feels for animals to be attacked by them, 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.39

The video below shows lions killing a zebra by asphyxiation. She is still alive when the lions begin eating her flesh.

 

It isn’t easy to establish the number of animals killed by lions each year, but we can make some reasonable estimates based on known facts. Based on the global lion population, we estimate that about 280,000 animals are killed by lions each year.40

Other large animals who typically come to mind when we think of predators are crocodiles. Large species, such as adult Nile or Saltwater crocodiles, can kill large mammals such as wildebeests, zebras, and giraffes. They are ambush predators, which means they conceal themselves near the edge of a watering hole and strike suddenly when an animal they are targeting comes within range. When multiple crocodiles attack a single animal, they typically kill her by tearing her apart. When a single crocodile attacks a large animal such as a zebra, they will either drown her by holding her under the water, clamped helplessly in their powerful jaws, or they will break her neck by violently thrashing around in the water. It is estimated that there are between 250,000 and 500,000 Nile or African crocodiles, between 200,000 and 300,000 Saltwater crocodiles and over a million American alligators in the world.41 Below are some videos of crocodiles and alligators killing their prey. The first video shows a group of crocodiles killing a wildebeest.

The second shows a crocodile ambushing a giraffe at a watering hole. After the kill, lions move in to claim the body.

The final video shows an American alligator capturing and drowning a wild pig in a New Orleans swamp.

Val Plumwood, who survived an attack by a Saltwater crocodile in Kakadu National Park in Australia, recounts here the moments after the crocodile has spotted her when she unsuccessfully attempts to make her escape:

I had a blurred, incredulous vision of great toothed jaws bursting from the water. Then I was seized between the legs in a red-hot pincer grip and whirled into the suffocating wet darkness.

She then describes the experience of the Crocodile submerging her in the “death roll”:

Few of those who have experienced the crocodile’s death roll have lived to describe it. It is, essentially, an experience beyond words of total terror. The crocodile’s breathing and heart metabolism are not suited to prolonged struggle, so the roll is an intense burst of power designed to overcome the victim’s resistance quickly. The crocodile then holds the feebly struggling prey underwater until it drowns. The roll was a centrifuge of boiling blackness that lasted for an eternity, beyond endurance, but when I seemed all but finished, the rolling suddenly stopped. My feet touched bottom, my head broke the surface, and, coughing, I sucked at air, amazed to be alive. The crocodile still had me in its pincer grip between the legs. I had just begun to weep for the prospects of my mangled body when the crocodile pitched me suddenly into a second death roll.

After the second death roll, she manages to grab onto a branch. She decides to cling on and allow herself to be torn to pieces rather than be pulled under the water again:

I grabbed the branch, vowing to let the crocodile tear me apart rather than throw me again into that spinning, suffocating hell.

Finally, she recounts the injuries she suffered at the crocodile’s jaws:

I did not remove my clothing to see the damage to the groin area inflicted by the first hold. What I could see was bad enough. The left thigh hung open, with bits of fat, tendon, and muscle showing, and a sick, numb feeling suffused my entire body. I tore up some clothing to bind the wounds and made a tourniquet for my bleeding thigh, then staggered on.42

 

Large animals can also be eaten alive

Some predators prefer to eat other animals while they are still alive instead of killing them first. Hyenas and African wild dogs often do this, frequently either disemboweling them or eating their genitals first. In the first video below, an impala fights back against a pack of wild dogs even after they have already torn her guts out. They overpower her and eat her alive.

In the second video, a hyena pins a wildebeest to the ground and eats him alive.

The following testimony is by a photographer who witnessed an elephant being eaten alive. The comment refers to the image depicted here.

This scene is probably the most shocking and emotionally difficult scene I have ever witnessed in nature. This young elephant got stuck in mud and was abandoned by his parents. Hyenas found it and started to eat it alive. The calf could obviously not move and the hyenas started at the trunk and ate it and most of the head skin and meat, before we finally convinced a ranger to put the calf to sleep, obviously against all rules and regulations not to intervene. It suffered for many hours before it was finally released of his tragic fate.

We only found the elephant at a time when the trunk was already eaten and I could only “handle” to take a few photographs. At this stage, it was already too late for the calf. But it did not let go…. About 2 hours later the elephant was still alive and at that time the hyenas had already eaten the eyes and skinned his skull completely. The calf kept fighting and continuously called for help.

Komodo dragons have also been known to eat their prey alive as the below video shows.

In the video below, we see a bear eating an elk calf while she is still alive.

 

Other ways animals suffer

Animals who avoid being captured and eaten also suffer in a variety of ways from the presence of predators in their environment. When they share an environment with predators, they may suffer from psychological distress, poor nutrition, loss of young, and injury. The following is a brief description of a few of the ways surviving prey animals suffer from predation.

 

Psychological distress

A number of studies have demonstrated the effects on behavior caused by fear of predators.43 Songbirds have shown to reduce their production of offspring by 40% when they perceive predation risk.44

It is sometimes assumed that the fear experienced by animals in the presence of a predators is “necessarily acute and transitory”,45 meaning that the fear response lasts only long enough for them to cope with the situation before returning to normal. The assumption for this is that since lasting effects of fear diminish the reproductive fitness of animals who are preyed upon, such long term effects must be maladaptive.46

This view is no longer tenable, however, because a growing number of studies have demonstrated that predator-induced fear has long lasting effects on wild animals.47 Chronic fear in wild animals who are preyed upon is an adaptive evolutionary response to the predatory environments in which they have evolved. That is, since animals who are hunted by predators are in constant danger of being killed, the fear responses they exhibit are adaptive, because they are necessary to stay alive. Though doubtless unpleasant for the individual animals who exhibit such PTSD like behavior, from an evolutionary perspective these responses are a necessary trade-off to ensure the animal survives long enough to reproduce.48 Given the similarities between predator-induced stress in animals and PTSD and chronic stress in humans, as well as the well-documented behavioral and neurological effects of exposure to predators, it seems likely that chronic fear causes great distress.

 

How predators suffer

The harmful nature of predation is not a one-sided affair, with the animals preyed upon enduring all the harms and the predatory ones reaping all the benefits. The lives of predators are also filled with hardships, many of which are the direct or indirect results of their reliance on a predatory mode of life.

 

Starvation

One of the most obvious harms faced by predatory animals is the risk of starvation. It is common for predators to starve to death either because there aren’t enough animals for the predator population to hunt or because they have become too old, injured, or sick to successfully hunt. Older male lions are particularly vulnerable to starvation as they are driven out of their prides by younger lions. Typically, the female lions in a pride do most of the hunting. A solitary older male is often unable to secure enough food to sustain himself. It can take several weeks for a lion to starve to death.

Even lions hunting together as a pride can face starvation. The video below shows a pride starving.

Mother octopuses starve to death while protecting their eggs, even when food is available to them. The behavior seems to be caused by the release of hormones from octopuses’ optical gland. It isn’t known why this self-destructive behavior has been selected for, though it has been speculated that it might be a mechanism for avoiding cannibalism of the babies.49

How often do predators starve to death? This is a complicated question without a simple answer. It varies by species, local environment, by year, and by prey populations. One thing we do know is that in many ecosystems the relative populations of predator and prey are not stable; rather their numbers rise and fall in cycles. As prey populations increase, so do the number of predators because there are so many of the animals they prey upon. However, as predator populations rise, they hunt so many animals that the prey population starts to fall again. Once the prey population falls, the predator population falls too as predators starve to death. Then once the predator population has dropped, the prey population starts to rise yet again. The unstable, cyclical nature of predator-prey populations means that starvation must be a common experience for predators.

 

Injury

Hunting is a dangerous activity. It is common for predators to be injured while hunting, either by the defenses of the animal they are attacking, by other predators who attack them to take the killed animal for themselves, or simply by losing their footing in high speed chases over difficult terrain. If the injury is severe enough to prevent a predator from hunting or eating, then he may die of starvation. Sometimes the hunter is killed outright by his intended prey. Here are two videos of lions being injured by buffalos. In the first, video the lion is impaled by the buffalo’s horn, an injury she would be unlikely to survive.

In the second, she is stomped to death by a herd of buffalos.

The below picture is the skull of a wolf who was born and died in Yellowstone National Park. Wolves in the park are closely monitored and studied, so we have a good idea of what his life was like. He was born in April 2010. He left his birth pack as a yearling, found a mate, and started a new pack, which he led for several years. In that first year, he bred with his mate. The following year, his mate died, along with all their cubs. By April 2016, he was in noticeably bad shape. He had lost weight, started limping and was not always with his pack. In September, he was witnessed attacking and killing a female elk, alone. He must have been driven to this rash action by desperation, as it normally requires at least four wolves to tackle a healthy elk. Soon afterwards, a rival pack killed him and took the elk’s body for themselves. An autopsy was performed and it was discovered that his jaw was broken, and had been for months, likely as a result of a kick from an elk or bison. He must have been in a great deal of pain, and the injury apparently impacted his ability to feed himself – he weighed 2/3 his normal weight. The injury was severe, and despite the extensive calcification (the body’s method of healing broken bones), the wound could never heal correctly.50

To conclude, antagonistic relationships such as parasitism and predation are ubiquitous in nature. They occur at every level, from insects to giant mammals, and in every habitable environment.

For information about other ways in which animals in the wild suffer see the situation of animals in the wild. For information about other kinds of antagonistic relationships see discusses fighting between animals of the same species and sexual conflict.


Further readings

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: Biological Sciences, 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 [2011]) 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 Mathematical Biology, 52, pp. 595-612.

Faria, C. (2016) Animal ethics 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: Biological Sciences, 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].

Marrow, P.; Dieckmann, U. & Law, R. (1996) “Evolutionary dynamics of predator-prey systems: An ecological perspective”, Journal of Mathematical 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 , November 22 [accessed on 4 April 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].

Schumacher, J. (2006) “Selected infectious diseases of wild reptiles and amphibians”, Journal of Exotic Pet Medicine, 15, pp. 18-24.

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.


Notes

1 Minelli, A. (2008) “Predation”, in  Jørgensen, S. E. (ed.) Encyclopedia of ecology, Amsterdam: Elsevier, pp. 2923-2929.

2 Marine ecologist Kevin Lafferty calls parasitism “the most popular lifestyle on Earth,” noting that approximately half of all species of animals and plants are parasitic at some stage in their lifecycle, and few, if any, species are not infested by any parasites. Lafferty, K. D. (2008) “Parasites”, in Jørgensen, S. E. (ed) Encyclopedia of ecology, op. cit., pp. 2640-2644.

3 Poulin, R. & Randhawa, H. S. (2015) “Evolution of parasitism along convergent lines: From ecology to genomics”, Parasitology, 142 (suppl. 1), pp. S6–S15 [accessed on 4 December 2019].

4 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.

5 Otranto, D. & Traversa, D. (2002) “A review of dicrocoeliosis of ruminants including recent advances in the diagnosis and treatment”, Veterinary Parasitology, 107: pp. 317-335.

6 Zimmler, C. (2003) Parasite Rex: Inside the bizarre world of nature’s most dangerous creatures, New York: Atria.

7 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.

8 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.

9 Ibid.

10 Ibid. Martin, A. M.; Fraser, T. A.; Lesku, J. A.; Simpson, K.; Roberts, G. L.; Garvey, J.; Polkinghorne, A.; Burridgeand, C. P. & Carver, S. (2018) “The cascading pathogenic consequences of Sarcoptes scabiei infection that manifest in host disease”, Royal Society Open Science, 5 (4) [accessed on 13 December 2019].

11 Simpson, V. R. (2002) “Wild animals as reservoirs of infectious diseases in the UK”, The Veterinary Journal, 163, pp. 128-146.

12 Ibid.

13 Ibid.

14 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].

15 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 [accessed on 4 August 2020].

16 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].

17 Ibid.

18 Ibid.

19 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.

20 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.

21 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.

22 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.

23 Weng, J. L., & Barrantes Montero, G. (2007) “Natural history and larval behavior of the parasitoid Zatypota petronae (Hymenoptera: Ichneumonidae)”, Journal of Hymenoptera Research, 16, pp. 327-336; Komatsu, T. & Konishi, K. (2010) “Parasitic behaviors of two ant parasitoid wasps (Ichneumonidae: Hybrizontinae)”, Sociobiology, 56, pp. 575-584.

24 Begon, M.; Townsend, C. R. & Harper, J. L. (2006) Ecology: From individuals to ecosystems, Oxford: Blackwell, p. 266.

25 Minelli, A. (2008) “Predation”, in S. E. Jørgensen (ed.) Encyclopedia of ecology, op. cit.

26 National Museum of Natural History & Smithsonian Institute (2018) “Numbers of insects (species and individuals)”, Information Sheet, 18 [accessed on 20 July 2019].

27 Pedigo, L. & Rice, M. (2009 [1989]) Entomology and pest management, 6th ed., Long Grove Illinois: Waveland, p. 1.

28 Bumblebee.org (2019) “Predators of bumblebees”, Bumblebee.org [accessed on 12 December 2019].

29 Nyffeler, M.; Şekercioğlu, Ç. H. & Whelan, C. J. (2018) “Insectivorous birds consume an estimated 400–500 million tons of prey annually”, The Science of Nature, 105 [accessed on 2 December 2019].

30 If we take the weight of an average housefly (12mg) as the average weight of an animal preyed on by spiders, and divide this into the lower estimate of 400 million tons of animals killed each year we get a staggering figure of 33.2 quadrillion animals killed by spiders every year.

31 Carefoot, T. (2011) “Learn about octopuses and relatives”, A Snail’s Odyssey [accessed on 23 September 2019].

32 How, M. J.; Norman, M. D.; Finn, J.; Chung, W. S. & Marshall, N. J. (2017) “Dynamic skin patterns in cephalopods”, Frontiers in Physiology, 8 [accessed 28 July 2019]

33 Jędrzejewski, W.; Robinson, H. S.; Abarca, M.; Zeller, K. A.; Velasquez, G.; Paemelaere, E. A. D.; Goldberg, J. F.; Payan, E.; Hoogesteijn, R.; Boede, E. O.; Schmidt, K.; Lampo, M.; Viloria, Á. L.; Carreño, R.; Robinson, N.; Lukacs, P. M.; Nowak, J. J.; Salom-Pérez, R.; Castañeda, F.; Boron, V. & Quigley, H. (2018) “Estimating large carnivore populations at global scale based on spatial predictions of density and distribution – Application to the jaguar (Panthera onca)”, PLOS ONE, 13 (3) [accessed on 14 November 2019].

34 Cougar Network (2015) “Cougar facts”, Cougar Network [accessed on 28 September 2019].

35 Goodrich, J.; Lynam, A.; Miquelle, D.; Wibisono, H.; Kawanishi, K.; Pattanavibool, A.; Htun, S.; Tempa, T.; Karki, J.; Jhala, Y. & Karanth, U. (2014) “Tiger: Panthera tigris”, The IUCN Red List of Threatened Species, 20 April [accessed on 28 November 2019].

36 For an estimate of the cat population of the United States see 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 [accessed on 2 November 2019]. For estimates of the global population see Migiro, G. (2018) “How many cats are there in the world?”, worldatlas.com, November 7 [accessed on 14 November 2019].

37 Bradford, A (2019) “Lions: The uniquely social ‘king of the jungle’”, Live Science, August 19 [accessed on 24 October 2019].

38 BBC News Services (2010) “Statistics reveal Britain’s ‘Mr and Mrs Average’”, BBC News, 13 October [accessed on 30 October 2019].

39 McGowan, C. (1997) The raptor and the lamb: Predators and prey in the living world, New York: Henry Holt, pp. 12-13.

40 The global wild lion population is estimated to be around 20,000 individuals. On average, an adult lion requires around 8 kg of meat per day. 8 kg multiplied by 365 gives us a yearly minimum of 2,920 kg of meat per lion per year. Most of the animals they eat weigh between 50 and 300 kg. Erring on the high side, we might estimate 200kg of edible meat per kill. This means that every adult lion will kill approximately 14 animals per year. Multiplying these 14 kills per year by the number of lions gives us a figure of 280,000 animals killed by lions per year. See McCarthy, E. M. (2008) “What do lions eat?”, Online Biology Dictionary [accessed on 26 November 2019]; Packer, C. (2015) “Frequently Asked Questions”, Driven to Discover [accessed on 29 November 2019]; WWF (2016) “The magnificent lion: The symbol of Africa”, wwf.org.uk [accessed on 4 November 2019].

41 Crocodiles of the World (2015) “Conservation status”, Crocodiles of the World [accessed on 13 November 2019].

42 Plumwood, V. (2012) “Prey to a crocodile”, Imagining Other [accessed on 19 November 2019].

43 Adamec, R. E. & Shallow, T. (1993) “Lasting effects on rodent anxiety of a single exposure to a cat”, Physiology and Behavior, 54, pp. 101-109.

44 Zanette, L. Y., White, A., Allen, M. C. & Clinchy, M. (2011) “Perceived predation risk reduces the number of offspring songbirds produce per year.”, Science, 334, pp. 1398-13401.

45 Ibid.

46 Schulkin, J. (2003) Rethinking homeostasis, Cambridge: MIT Press. Sheriff, M. J.; Krebs, C. J. & Boonstra, R. (2009) “The sensitive hare: Sublethal effects of predator stress on reproduction in snowshoe hares”, Journal of Animal Ecology, 78, pp. 1249-1258 [accessed on 5 December 2019].

47 Suraci, J. P.; Clinchy, M.; Dill, L. M.; Roberts, D. & Zanette, L. Y. (2016) “Fear of large carnivores causes a trophic cascade”, Nature Communications, 7 [accessed on 6 December 2019]. Zanette, L. Y.; White, A.; Allen, M. C. & Clinchy, M. (2011) “Perceived predation risk reduces the number of offspring songbirds produce per year”, Science, 334, pp. 1398-13401.

48 Clinchy, M.; Schulkin, J.; Zanette, L. Y.; Sheriff, M. J.; McGowan, P. O. & Boonstra, R. (2011) “The neurological ecology of fear: Insights neuroscientists and ecologists have to offer one another”, Frontiers in Behavioral Neuroscience, 5 [accessed on 30 November 2019].

49 Wang, Z. Y. & Ragsdale, C. W. (2018) “Multiple optic gland signaling pathways implicated in octopus maternal behaviors and death”, Journal of Experimental Biology, 221 [accessed on 6 November 2019].

50 For a full account of his story see Smith, W. D. (2019) “My time with ‘male 911’: This Yellowstone wolf was safe from people, but not from nature”, The Washington Post, 31 May [accessed on 19 July 2019]; National Park Service (2017) “The hard life of a Yellowstone wolf”, nps.gov [accessed on 19 July 2019].

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