A matter of life and... energy?

Death is absolutely fundamental to behaviour, ecosystems and evolution. Lewis Halsey asks if biologists need to look more closely at how and why animals die

The Biologist 65(2) p18-21

Animals are not subject to tax regimes, so for them there is just one certainty in life – death. During the many conversations I have had with fellow behaviourists and physiologists about the species they study, I have often asked what their species' primary cause of morbidity is. The response is usually a furrowed brow.

Do most simply starve when they get too old to forage? Do they get eaten before they keel over? Does disease get them before age? It seems that this macabre yet fundamental aspect of their subject species' existence is rarely the focus of detailed study.

Biologists instinctively focus on how animals live, not on how they die. Yet death is, of course, a main cog in the machine that drives evolutionary change, whereby inferior individuals are removed from the population, along with their opportunity to replicate. Death is clearly central to biology.

What new angles of thought might arise by bringing death to the forefront of conversations in the fields of animal behaviour and physiology? We are all aware of the aphorism that the antelope evades the lion through camouflage, fleetness of foot and herd behaviour. However, what factors weaken the efficacy of these adaptations, indirectly making the antelope vulnerable? If antelope can succumb to infections that compromise their evasive capacities, then is their immune system as much the target of lion-driven Darwinian selection as is the colouring of their fur and the anatomy of their leg?

We need a strong understanding of what environmental factors can contribute to an animal's death, and how these environmental factors disproportionately affect different genotypes and phenotypes.

This article makes a foray into the subject of animal morbidity, focusing on several 'starter' questions designed to generate momentum in thinking about the topic. For any given animal, how important is predation as a driver of morbidity? How important is the availability of energy, in the form of food, as a driver of morbidity? And what impact do other potential insults such as disease or misadventure have? These factors often interact, creating a network of influences on animal mortality.

To start, the main factors that directly cause death in wild animals are listed below (see 'What do animals die from?'). Why animals die might sound more complicated, but below I argue that these causes of mortality can be categorised quite simply, making some sense of the intricacy. I will highlight some key questions yet to be asked about patterns of animal mortality, based on these categorisations, including the most straightforward one yet to be answered for many species: what are the common causes of death?

What do animals die from?
For wild animals, we can categorise causes of death into four types: predation, disease, misadventure and starvation. First, let's look at some examples of each, with more detail about the fourth one because I believe it has particular importance.
Broadcast spawners that shed their gametes into seawater, such as mussels, are highly vulnerable to mass predation during the early stages of their life cycle. Death by predation can also be prevalent in species with high levels of parental care – for example, the high mortality rates in cheetah cubs are mostly via predation by other felid species, and predation also has a strong influence on deer demographics. Human predation can be extreme – for example, fisheries can decimate populations of both targeted and non-targeted marine species.
In some populations of New Zealand sea lions, the majority of pups succumb to hookworm combined with a bacterial epizootic. Dampwood termites often die from natural exposure to fungal conidia within the microbial communities of their own nest.
Other species experience massive mortality from abiotic factors such as extreme weather – insects can die en masse from a loss of favourable shelter from the elements. Antarctic fur seal pups succumb to skull damage purposefully inflicted by other pups' mothers or liver damage accidentally inflicted by males that crush the pups while displaying.
Starvation is a key factor of morbidity for many species5 and a case study about penguins provides an insightful example. Colonies of emperor penguins live around the periphery of Antarctica. The majority of chicks do not survive to adulthood – the growing chicks often do not receive sufficient food from their parents to supply the necessary growth. Emaciation can also seal the fate of chicks that survive to fledging once the parents have stopped feeding them. At this testing time, the chicks must rely on their own energy reserves until they become successful foragers. While fledgling emperor penguins are learning their foraging trade, both the duration and depth of their dives are less than those of experienced adults.6 They are probably energetically inefficient hunters, putting further strain on their body's energy reserves. This has also been documented in the king penguin, which when juvenile is both an inefficient hunter in terms of the rate it captures prey and the rate it expends energy while diving.

Lack of food as an indirect cause of morbidity

Energy is essential for an organism to survive, and in turn energy demarcates the states of life and death. Through this article, I make the argument that low energy availability (most commonly in terms of a lack of food ingestion) often plays a role in death, even if indirectly.

There is good empirical evidence that for many species, energy is a central driver of mortality. For example, many studies report high mortality rates of wild animals during winter, with necropsy indicating that at death they had negligible fat stores under the skin, implicating emaciation as the final death knell[1]. Furthermore, drivers of mortality often cause and feed back on one another, such that in many instances where energy availability is not the final cause of death, it is a background factor.

For instance, in situations where animals need to feed for longer in order to obtain sufficient sustenance, perhaps because food is sparsely available, they are also exposing themselves to predators for longer. Furthermore, they may be in a weakened state due to emaciation and thus less able to flee predation.

Conversely, animals that are injured, perhaps from a confrontation with a predator, may struggle to forage due to physical damage, septicaemia or tetanus, inviting the onset of emaciation. There are many published reports of predators capturing substandard individuals disproportionately[2]. For example, grey squirrels that were captured by hawks had both considerably higher parasite loads and much less adipose tissue than normal.

Animal Morb homepage

Classifying pathways to mortality

Death can be caused by a plethora of bottom-up and top-down factors, often interlinking, and in some cases acting on an animal over extended periods of time before death ensues (see 'Pathways to mortality', below). However, we can categorise these interacting factors, defined by the presence of a 'background' (ultimate) cause and a 'final' (proximate) cause, and by whether energy availability plays a role or not, thus providing some clarity to processes of mortality.

First, and most simply, the death of an animal can be due to a single event or process that is entirely unconnected with its energy reserves (A, below). For example, hares are predated on by both birds and mustelids regardless of their physical condition, and insect larvae die from desiccation often owing to weather conditions. Australian macropods such as wallabies are often killed on roads by cars and lorries, while Northern right whales suffer fatal collisions with fishing vessels.

Physical or physiological deterioration due to an event not associated with energy availability can leave the animal debilitated (B). This exposes it to a subsequent deleterious factor also not associated with its energy reserves, and that is the final cause of its eventual moribund state.

For example, zebra mussels with damaged shells or byssus threads are more susceptible to predation by rusty crayfish, and codling moths are vulnerable to cannibalism if temporarily incapacitated during moulting. The males of dasyurids, a marsupial family native to Australasia, typically live for just a year and experience immune system breakdown during the mating season resulting in organ failure and then death from a host of direct causes such as gastrointestinal haemorrhage, vehicle impact or predation.Beluga whales in the St Lawrence estuary that die after stranding (final cause) are usually diagnosed with a respiratory or gastrointestinal infection, or cancer.

Physical or physiological deterioration, again due to factors not associated with energy reserves, debilitate an animal (background cause), but this time the debilitation leads to death by starvation (C). For example, along the East Lothian coast in Scotland, oystercatchers with damaged limbs often then die of emaciation.1 More generally, during a period when food is scarce, animals that are less capable foragers are more likely to reach a moribund state of emaciation before the season changes.

Low energy uptake can be the background cause of deterioration, which then makes the animal vulnerable to death from a final cause other than lack of energy reserves (D). Most obviously, animals weakened from a loss of tissue mass are likely to be targeted by predators. Snowshoe hares lose body mass over winter due to limited food supply and those with less marrow fat are more likely to be predated by lynx and coyote.

Finally, low energy uptake can be both the background and final cause of death (E). Low food availability, or reduced access to food due to conspecific competition or predator presence, can cause a deterioration of body condition in a fully grown animal or poor growth rates in a developing animal. Then, continued low food availability or a consequent reduction in foraging ability further progresses the animal's decline and eventually it cannot escape a spiralling deterioration.

Pathways to mortality
A) Death from non-energy related (background) cause – for example, vehicle impact or viral infection kills the animal directly.
B) Background – physical or physiological deterioration results in reduced capabilities.
Final – increases the chances of death by predation/infection/misadventure.
Example: muscle atrophy due to ageing reduces the chances of being able to escape predators.
C) Background – physical deterioration results in poor foraging capabilities.
Final – leads to emaciation/death by starvation.
Example: cancer reduces the ability to compete for food.
D) Background – physical deterioration due to low energy uptake.
Final – increases vulnerability to death from a background cause not related to lack of energy.
Example: low food availability leads to increased chance of predation.
E) Low energy uptake drives the initial (background) and subsequent (final) deterioration. Example: low food uptake causes an animal to not survive migration or hibernation.

Of course, this categorisation of processes leading to animal mortality cannot detail the intricate inter-relationships between the often multiple final and background causes that definitively describe an animal's demise. However, aside from providing some clarity, these categories elucidate the fundamental ways in which energy availability and body energy reserves influence, either directly or indirectly, deterioration to a moribund state, as well as the scenarios where it has no part to play.

Animal Morb pinginos

The goal of animals is arguably to maximise the viable offspring they have. To achieve this, their strategy could include maximising the energy that they expend on reproduction over their lifetime[3] while focusing that expenditure on rearing the most promising offspring (and staying alive for a good many reproductive cycles). Perhaps for this reason, theories of and studies into animal optimality focus on adult animals striving to breed – sexually mature animals optimise their harvesting of energy through foraging and their allocation of that energy to reproduction. However, this disregards the reproductive aspirations of still immature individuals. Death, of course, is catastrophic for these juvenile individuals' reproductive fitness: they return a lifetime fecundity score of zero and often with low energy availability a key culprit.

In most species, breeding individuals reproduce many more times than necessary to replace themselves, yet long-term population sizes tend to hold. The main explanation for this is that most of the progeny perish before reaching sexual maturity. Studying the breeding success of solely mature adult animals and relating this to their adaptations and energy allocations therefore focuses on only the fortunate few, and is not indicative of a population's general struggle for survival both in the present generation and into the next. What factors predominantly drive the lifetime reproductive success of an entire species may skew from those that most influence the fecundity of its sexually active adults, and those factors can include energy availability. While energy availability will be incidental to the fatalities of many animals, for many more individuals a loss of energy reserves is pivotal to their demise.

This classification of pathways to mortality highlights the role of energy availability. Each classification (except A) is based on a general background (ultimate) and then also a general final (proximate) driver of mortality.

Future research

Some impressive field studies have been published documenting the rates of and reasons for mortality in particular species across a plethora of taxa[4]. In particular there is a preponderance of life tables for insects. Together, these available data may be sufficient to investigate key remaining questions about the mortal susceptibilities of different species. For example, how do the categories of mortality change in prey and/or predator species inhabiting environments that become anthropogenically disturbed?

Within species, how do levels of cognition relate to longevity and category of death? Are r-selected species proportionately more likely to die from abiotic factors and k-selected species from biotic factors? And how do parental care, juvenile growth rates and metabolism describe those species that live and die under the spectre of insufficient energy?

For many species studied, however, the key cause of death is undocumented – individuals in a population simply disappear. As I have argued, this blind spot is unsatisfactory when we are pursuing a better understanding of an animal's behavioural and physiological adaptations to life. Perhaps, then, in part this essay can serve as a call to arms for researchers who I have convinced can better understand the life of their study animal by also understanding its death.

Lewis Halsey is a reader in environmental physiology at the University of Roehampton in London. He studies energy expenditure in a diversity of species from lobsters to penguins, including humans.

  1. Whitfield, D. Raptor predation on wintering waders in southeast Scotland. The Ibis 127, 544–558 (1985).
  2. Temple, S. A. Do predators always capture substandard individuals disproportionately from prey populations? Ecology 68 669–674 (1987).
  3. Brown, J. et al. Toward a metabolic theory of ecology. Ecology 85, 1771–1789 (2004).
  4. Severtsov, A. & Shubkina, A. Predator-prey interaction between individuals: 1. The role of predators in natural selection. Biology Bulletin 42, 633–642 (2015).
  5. McCue, M. D. Starvation physiology: reviewing the different strategies animals use to survive a common challenge. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 156, 1–18 (2010).
  6. Ponganis, P. et al. Development of diving capacity in emperor penguins. Journal of Experimental Biology 202, 781–786 (1999).

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