This is the final post in three-part series. Read part one → Read part two →

Introduction

Previously, I wrote about approaches to studying wild animals’ causes of death, with the goal of making work in this field maximally useful for understanding wild animal welfare. Cause of death has not received sufficient research attention relative to its significance to wild animal welfare. The overwhelming majority of the research that does exist is focused on land-dwelling mammals and birds, and primarily on cases where understanding what animals are dying from is instrumental to preventing the extinction of their species. Here, I will give an overview of what research in this field has taught us so far about how wild animals die and highlight gaps that seem especially important for welfare biology.

Cause of death in wild terrestrial vertebrates

Collins and Kays (2011) conducted the first systematic review of cause-specific mortality rates in mammals, selecting only studies that used small radio trackers to monitor animals and document their deaths in a timely manner. They also limited their analysis to adult animals, due to a serious lack of data on juvenile mortality causes. This review found that, overall, predation was the most common cause of death for small-bodied mammals, while human-caused deaths, including hunting and vehicle collision, were the most common causes of death in larger mammals. 

In 2019, Hill et al. expanded on this review with a vast amount of new data, including data from juveniles and non-mammalian vertebrates. They found that natural causes of death (predation, disease, starvation), especially predation, were common among juvenile animals irrespective of their species’ typical adult body size. For mammals and reptiles, predation was roughly twice as frequent in juveniles as in adults, with predation accounting for more than 95% of documented deaths of juvenile reptiles (Figure 1). Birds, on the other hand, exhibited very similar cause-specific mortality rates between juvenile and adult age classes. 

The authors note that their dataset probably still greatly underestimates natural causes of death, considering that these deaths are often harder to detect. Although smaller animals exhibit the highest natural mortality rates, they are harder to monitor. Research to date has also focused on populations that come into conflict with or are used by humans.  These factors combine to make the most numerous deaths in the wild the least understood.

Hill et al. provide an excellent summary of mortality causes, but many of these categories — especially predation, accident and disease — encompass a huge degree of variation in experience. For example, 18% of New Zealand sea lions die from tuberculosis, while 24% die as a result of violence from other sea lions (Lenting et al. 2019). Similarly, approximately half of American black bears die as cubs, often as a result of attacks by older male bears (LeCount 1987). In their study area of northern Pennsylvania, Alt (1984) estimated that 5% of cubs drowned in their winter dens as a result of flash flooding. This was 3-5 times more likely to occur when dens were made in root cavities or excavated soil. Juvenile bears also frequently die from disease (e.g. Chomel et al. 1998). For example, a grizzly cub suffering from canine hepatitis died live on camera in Katmai National Park beside their bewildered mother and siblings. Welfare interventions will need to account for all this variation in individual wild animals’ experiences of death.

Much of the data on birds’ deaths comes from urban wildlife hospitals, where traumatic injury is often the apparent leading cause of death among adult birds, while disease and malnutrition is responsible for the majority of juvenile deaths (e.g. Stenkat et al. 2013). However, these statistics are certain to be biased by the kinds of birds and causes of death that people are most likely to come into contact with. For example, although many traumatic injuries are attributable to domestic cats, birds attacked by predatory raptors are rarely admitted (c.f. Palma et al. 2006). Studies of radio-tagged wild birds report predation and hunting as the leading causes of death (Hill et al. 2019). Some disease mortality can also be linked to hunting practices, as the importation of birds to stock hunting grounds can contribute to outbreaks (Buenestado 2009). Migratory birds present a special challenge for researchers, since many of their deaths occur in transit over long distances, where it may be impossible to recover their corpses. For example, out of 51 probable deaths among satellite-tracked migratory raptors, Klaasen et al. (2014) were only able to confirm 10, among which the leading causes of death were collision with man-made structures and exhaustion during migration.

The progress made in the last decade of cause-specific mortality research is encouraging, but there is much more to be learned, especially about more numerous, smaller-bodied animals. Little is known about the causes of death among prairie dogs, for instance, except that predation is common and plague occasionally wipes out entire colonies (Crosby and Graham 1986; Stapp et al. 2004). Studies of wild reptiles, especially snakes and turtles, consistently indicate road traffic accidents as a leading cause of death (e.g. Himes et al. 2002), although most juveniles are killed by predators (e.g. Butler and Sowell 1996). These gaps in our knowledge of wild animal mortality seem likely to be filled as radio tracking devices are made smaller, lighter and more resilient over the next decade (Kays et al. 2015). 

Cause of death in wild fish

Among vertebrates, the most neglected group in the current body of cause-specific mortality research is wild fish. Of the papers that do touch on causes of death in wild fish, many are case reports focusing on the risks of disease outbreaks to human health or the fishing industry. Case reports can be valuable for demonstrating the presence of specific risks that some number of fish do die from (Krkošek 2017). For example, Sterud et al. (2007) detected an outbreak of the parasite Tetracapsuloides bryosalmonae in an Atlantic salmon population that appeared to be their most common cause of death during the study period. This parasite is probably in constant circulation among the fish, and outbreaks have been documented in many other populations, but it is impossible to say whether these results are a representative snapshot of the parasite’s effect on mortality or what alternative causes of death occur in the population. 

Most effective studies of terrestrial animals’ cause of death rely on recovering the corpses of tagged individuals, as discussed in my previous post. However, this is clearly more challenging to do with fish. Radio signals for tracking individuals are relatively ineffective underwater, and corpses are much less likely to be recovered (c.f. Benelli and Pozzebon 2013). Several studies have cleverly taken advantage of avian predators naturally retrieving radio-tagged fish from the water and depositing their eaten corpses on shore. For example, Koed et al. (2006) estimated that 39% and 12% of juvenile salmon and brown trout, respectively, were preyed upon by cormorants in the estuary where their study was set. Approximately a further 10% of salmon and trout were killed by cormorants in the adjoining river, while 3-6% were preyed upon by pike, a predatory fish. A similar study by Dieperink et al. (2001) recorded that 65% of juvenile trout were eaten by cormorants and herons while migrating downstream to the Baltic Sea. Fritts and Pearsons (2004) used another predator-based approach to quantify predation, analyzing the stomach contents of smallmouth bass to estimate their annual consumption of salmon. Taken at face value, their results suggested that smallmouth bass accounted for only around 4% of salmon mortality in this system, though the authors noted that this was probably an underestimate. Despite the special challenges involved in recovering the corpses of wild fish, it is at least possible to study the impact of specific predators on fish populations.

Technological progress is proving especially important for studying cause of death in the marine environment. In one recent study, fish were implanted with acoustic transmitters that enabled the researchers to detect predation events occurring within range of their underwater receiver array (Weinz et al. 2020). They inferred that approximately one third of tagged fish were preyed upon over the four months following their release. Several factors could be confounding this result, in both directions. For one, the invasive procedure required to implant the fish with acoustic transmitters could have made these particular fish more susceptible to predation than average. This would be consistent with other studies showing that fish caught and released are more vulnerable due to physical injuries or stress (e.g. Raby et al. 2013). On the other hand, some predation events were likely missed because they occurred out of range of the acoustic array. As the range of underwater tracking improves and the size of transmitting devices decreases so as to cause less harm to the tagged individuals, we should expect to see much more data on the lives and deaths of fish and other marine animals.

Cause of death in insects

Insects are among the most numerous and diverse animals, but also the smallest. Their diversity and size makes them especially difficult to monitor on an individual level. At the same time, some insect species are viewed as pests, and so there is commercial interest in understanding their natural causes of death to devise more effective management strategies (Roux and Baumgärtner 1998). This has motivated a handful of studies reviewing the causes of death of agriculturally relevant insects (Table 1). 

Some of these studies use a combination of field observations and population modeling to estimate by how much the population’s overall mortality rate would be reduced if a given cause of death could be eliminated. For example, if predators disproportionately target weak or sick prey, then even if many individuals ultimately die from predation, eliminating their predators may have only a small effect on the overall mortality rate because the same individuals who are vulnerable to predation are also vulnerable to dying soon from disease or starvation.

Determining the significance of competing mortality risks

Future interventions seeking to improve wild animal welfare should account for how actions to protect animals from specific causes of death could influence population sizes, lifespans, and alternative causes of death. Compensatory mortality, where mortality due to a certain cause is replaced by mortality due to another cause when the first is removed, has been noted in many diverse species and ecosystems. For example, Hostetter et al. (2012) reported that cormorants along the Columbia River in Oregon selectively predate poorer-condition juvenile steelhead salmon en route to the sea. Had they not been killed by cormorants, these same individuals would likely have been among the first to succumb to harsh conditions and competition during their first winter in the ocean (Hurst 2007). Similarly, in a classic study on mule deer, Bartmann et al. (1992) found that removal of coyotes over winter reduced the rate of mule deer deaths by predation, but did not increase their overall survival rates, as the researchers observed increased mortality due to starvation. Diseased mule deer are also selectively preyed upon by mountain lions (e.g. Krumm et al. 2009), which suggests that some of this predator-caused mortality is compensatory.

On the other hand, some cause-specific mortality really is irreplaceable. Achhami et al. (2020) demonstrated this for plant chemical defenses against wheat stem sawflies, while Cooley et al. (2009) showed that other causes of death are not reduced in populations of mountain lions hunted by humans. Bergman et al. (2015) proposed that the degree to which mortality due to a particular cause is compensatory depends on ecological context. For example, if chronic illness made animals less effective at competing for food in a dense population, death by starvation may occur first and compensate for some disease-related mortality in this hypothetical population. If food later became more accessible, we might observe an apparent increase in mortality caused by diseases that are now able to run their course. In addition to studying mortality dynamics in a snapshot of a population’s present conditions, research should model how mortality risks compete under different conditions (Siler 1979) (Figure 2).

Conclusions

A relatively comprehensive snapshot of cause of death in the wild is emerging for terrestrial mammals, birds, and reptiles, thanks to mainstream research in ecology and conservation (Hill et al. 2019). For example, we can see that predation is the leading natural cause of death, especially in juveniles (Figure 1). However, this account is still likely to be heavily biased, since most studies focus on adults and large-bodied species. The focus on large animals could be inflating the number of deaths caused by hunting rather than vehicle collisions, for instance, given that accidents involving small animals often go unreported (Sáenz-de-Santa-María and Tellería 2015). More research on juveniles and small mammals is needed (Table 2). We are also at the stage of considering interventions to improve the welfare of some wild mammals and birds, ranging from pigeon fertility control to reducing feral cat predation. To make these interventions as effective as possible, it would be valuable to understand the replaceability of different sources of mortality.

Fish and juvenile amphibians are still seriously lacking in data on cause-specific mortality, especially relating to juveniles. Research on both of these groups is challenged by the fact that they spend some or all of their lives underwater, but biologging technologies — including pop-up satellite archival tags (PSATs) (Tolentino et al. 2017) and acoustic telemetry (Weinz et al. 2020) — could enable more research on cause of death in aquatic environments, especially related to predation.

A surprising amount is known about cause-specific mortality in insects regarded as agricultural pests (Table 1). However, very little research has been done on the deaths of insects with less agricultural relevance. From the existing research, it is clear that insects face challenges that would surprise us. For example, Asiimwe et al. (2006) found that many whiteflies died as a result of poorly understood developmental abnormalities, such as failure to complete metamorphosis. Drowning during rainy weather was one of the foremost causes of death among the moths of Pereira et al. (2007), and plant chemical defenses were responsible for a majority of the deaths of wheat stem sawflies monitored by Acchami et al. (2020).

As many challenges as we know that animals face in the wild, some may yet be masked by the urgent threats they face from humans through hunting, fishing, extermination, and competition for resources. Humans should leave more space for wildlife, and try not to make their existence harder than it already is, but we should also be willing to go further. Learning more about cause-specific mortality in different populations and environmental contexts can inform plans for the most effective actions to improve wild animal welfare.

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