The dead of winter

24 January 2014 by Malcolm Campbell, posted in Biology, Science

In winter, nature is a cabinet of curiosities, full of dried specimens, in their natural order and position.” from A Winter Walk by Henry David Thoreau (1817-1862)

They were a surprising thing to find on an early winter’s walk. A tiny troupe of beautiful two-toned mice. The trio was lying peacefully on the gravel track, no more than a hand’s width apart.

They were a handsome group. Each had sleek coats – tan on top, with white bellies and feet. Their colours gave them away as deer mice – members of the genus Peromyscus. deadmau51

They might have been “proper” deer mice, of the species Peromyscus maniculatus, but they also could have been the closely related white-footed mice, Peromyscus leucopus. It’s hard to tell the species apart visually, and they lead very similar lives – active in open spaces, from grasslands to woods, making their way along pathways as opposed to closed burrows.

Despite the strange location for resting, in the midst of a path, and the timing, on a frigid, early-winter morning, the three mice appeared to be in the deepest of slumbers. Closer inspection revealed that the threesome was in a far deeper rest.

All members of the little entourage were deceased.

Each tiny little body was entirely motionless. No inhaling. No exhaling.

They were casualties of an early winter. The cold had come fast and hard.

At the time of the year the deer mice died, it is not uncommon for the siblings of the last litter of the year to strike out on their own – leaving the nest of their birth to establish new nests. As deer mouse litters typically have three to five pups, it may be that the trio were indeed nestmates departing to make new homes for themselves. Perhaps they got caught by the biting cold as they made their way – there was no sign of any struggle – no indication that they had fallen prey to any predator – more like they had lain down and fallen asleep in the midst of a journey, like victims of hypothermia.

Possibly they were weakened by poor diet. As opportunistic omnivores, deer mice eat what is available. During the autumn and winter months, when vegetation is in short supply, up to a third of their diet may be insects and other invertebrates. The cold snap ensured that such foodstuffs were in short supply – killed by the temperature, or inaccessible in the frozen ground. It would have made for a tough start to the winter for the deer mice. They might have succumbed to the combination of factors brought about by winter’s early arrival.

Of course, they might have met a more nefarious end – sickened by a lethal illness, or poisoned by something they encountered in their travels.

Regardless of how they came to their fate, the diminutive corpses were melancholy inducing. It was difficult to imagine these attractive creatures meeting an early end – an end to their inquisitive scurrying and exploratory scampering as they went about their lives in their miniature world.

Death seemed so final. Particularly so with the force of winter bearing down. It was difficult to imagine the trio as anything but emblematic of a very definitive finish to life. deadmau52

But this is wrong-minded thinking. To think of death in nature as a chapter closed loses track of a much grander, much more impressive story . A story of continuity. Of life supporting life. Endlessly.

Because the deer mice were not merely deer mice. Sure, they bore all the outward trappings of deer mice – the product of mouse cells working together to make a mouse form – but they were much more than that.

The deer mice were ships laden with cargo that would carry their legacy far into the future.

What was the legacy-making cargo that they bore?

Microbes.

Each deer mouse was made up of billions of deer mouse cells. For comparison, recent estimates suggest that humans are made up of 37.2 trillion human cells. Deer mice will likely have fewer cells, but still many, many billions.

But we, and the deer mice, are much more than just our own cells. We carry with us a whole host of microbes. For humans, it’s been estimated that we are host to 100 trillion microbial cells. We, and the deer mice, have more microbial cells than we do our own cells. We are walking trellises for microbes.

Microbes are unicellular organisms with which most people have some familiarity. For instance, there’s the ubiquitous Escherichia coli, or E. coli, a bacterial denizen found in our guts, commonly in our lower intestines. There are a variety of different types, strains, of E. coli, some of which are helpful, some of which are benign, and others that are problematic.

Like E. coli, other species of bacteria reside in our guts. Yet others take up residence on our skin, others in our mouth, others in our ears, and so on. What’s more, each location in our body is like a different ecosystem. Just as some ecosystems harbour different species from other ecosystems – consider a rainforest versus a desert for example – our bodies host different collections of bacteria in different locations. Some bacteria like places that are relatively free from oxygen, like our intestines, while others prefer to be awash in oxygen, on our face.

In addition to different bacterial species, we also have different fungal species, like yeasts, that come along for the ride. Like bacteria, different fungi take up residence in preferred locations, adding to the biodiversity found in each of your body’s “ecosystems”.

The collection of microbes residing in a particular location at a particular time is known as the microbiome. Each microbiome consists of a specific set of microbes. If you imagine each microbiome being represented by a pie chart, where each microbe is represented by a different coloured slice of the pie, then each microbiome is characterised by both the slice colour palette and the size of the slice for each colour in the chart.

Like us, deer mice also carry diverse microbiomes. When they die, their microbiomes still remain. What’s more, when a deer mouse dies, these microbiomes become more dynamic. They become powerful agents of change, They transform the corpse. They decompose it, returning its constituents to the earth. They shape the future. deadmau53

We know a good amount about what happens to microbiomes after a mouse dies. Elegant research conducted by Jessica Metcalf, Rob Knight and their colleagues have explored the shift in microbe populations as a mouse corpse decomposes. In controlled experiments using 20 mouse corpses, they examined the composition of microbiomes over time. They examined the microbiomes of the skin and the abdominal cavity, as well as the gravesoil, the soil that lies beneath the corpse.

Shifts in the composition of the microbiome were determined by tallying genetic fingerprints. Each species and strain of microbe has a distinctive genetic makeup. This makeup can be identified using a diagnostic gene – a specific stretch of DNA that provides a signature, a fingerprint, for the microbial species and strain in question.

Recall that DNA is written in a four-letter code. If we look at a gene that is found in all microbes, any difference in the four-letter code enable us to distinguish between individuals, strains and species. If we examine the DNA extracted, say, from a swab taken from the skin, looking at variation in the four-letter code of DNA for a given gene, the variants we observe reflect the presence of different strains and species. As we have already determined which variant belongs to which strain and species, we can determine the species composition of a sample simply by looking at which DNA sequence variants are present. By tallying the number of these variants, we get a measure of the relative abundance of each of the corresponding species and strains in the sample. This is precisely what Jessica Metcalf and her colleagues did – looking at samples obtained from the mouse corpse and the gravesoil over time.

What they found was amazing.

The fresh corpse had microbiomes of the living mouse. The skin microbiome favoured oxygen-utilising bacteria, known as aerobes, while the abdominal cavity favoured anaerobes, microbes that work in the absence of oxygen. But then the corpse began to change. First it became discoloured. The corpse then went through the distinctive stages of decomposition. This began with a process of active decay, starting with noticeable discolouration; followed by purging of decomposition fluids out of eyes, nose, or mouth; then bloating of neck and/or face. During these stages the corpse became bloated, after which is ruptured purging the decomposition fluids. These stages were followed in turn by advanced decay, which progressed from sagging, to sinking, then caving in of flesh. The process concluded with mummification. During these stages, the microbiomes undergo sweeping changes.

As the corpse undergoes decay, anaerobes take over the body cavity. Any aerobes within the body cavity are now deprived as oxygen, as it no longer flows with breathing and is passed through the body in the blood. Instead the body cavity becomes depleted in oxygen, favouring aerobes that are normally found in the gut. With no food being ingested, these active digesters start to work on the mouse body, digesting fats and proteins – putrefying the inside of the corpse – producing liquid and gas that causes the cavity to swell. As the digestion breaks down membranes, eventually the body cavity bursts, releasing its putrefied constituents. deadmau54

When the body cavity bursts, the anaerobes that had taken over the cavity are now exposed to oxygen, and their numbers drop. They are supplanted by aerobes found on the skin, particularly the skin of the belly, and finally by aerobes found in the soil below.

The release of the body cavity fluid has a profound effect on the gravesoil microbiome. The fluid is rich in nutrients, especially ammonia, and is relatively  alkali in pH. As such it provides a boon to opportunistic microbes that can make use of those nutrients. Simultaneously, it is a detriment to any microbes that favour acidic soil conditions. Consequently, the bursting of the body cavity is accompanied by a rapid shift in the soil microbiome – losing acid-loving microbes, and increasing high-nutrient-favouring aerobes.

The decomposition of the corpse ushers in waves of microbiome changes. If one was to look at the pie charts corresponding to each of the microbiomes, one would see a flux in the colour palette, involving the loss of some coloured pieces of the pie, expansion of some pieces, contraction of others, and the appearance of new colours in the pie.

In essence, the tiny corpse creates microbiome kaleidoscopes.

In turn, each kaleidoscope changes the environment in which it resides – ultimately returning the chemical constituents of the mouse to the soil. The entire process takes a mere 48 days. Just 48 days to convert a life of 48 months to soil.

Evidence to date suggests that the interplay between the corpse and these shifting microbiomes, the process of decomposition, can have a greater, albeit localised, effect on soil ecosystems than plants or faeces. Far from being a static end to existence, the decomposition process creates a lasting legacy of a lives well-lived. Of lives that gave back what they took during their brief existence.

But what of the winter deaths of the trio of deer mice? Did this process play itself out with these wintry corpses? The answer is yes…but slowly.

The process of decomposition is influenced by a number of factors. Moisture level is an important determinant of the speed and extent of the process. Similarly, temperature plays a key role in determining the rate of decomposition.

Under the low temperatures of winter, decomposition occurs. Slowly. The clock of conversion is slowed down. As opposed to 48 days, decomposition will be stretched over months. It will be arrested by sub zero temperatures, and re-initiated when temperatures rise again. Like anything placed in deep freeze, certain biological processes will be frozen in time also. But still they will progress. deadmau55

In winter, the kaleidoscope of microbiome changes will run in slow motion. There will be days when the kaleidoscope is masked by snow or ice, but still the pie chart moves – with the ecosystem of microbes shifting to convert the corpse to soil. Like a glacier creeping across the landscape, the dance macabre of the microbes and the corpse moves in tinier increments under the weight of deep winter. But still it moves.

So don’t look at the deer mice with heavy heart. They support trillions of other lives. They will support many more times that in the future. They will feed the soil, and the plants that live in that soil. The plants in turn will feed and shelter generations of deer mice to come.

The deer mice were here with us briefly, but their legacy will stay with us so much longer. In their deaths there is, and will be, so much life. The dead of winter are needed to realise the promise of summer.

Images: All photographs by Malcolm M. Campbell.

References:

Bianconi E, Piovesan A, Facchin F, Beraudi A, Casadei R, Frabetti F & Canaider S (2013) An estimation of the number of cells in the human body. Annals of Human Biology 40: 463-471

Carter DO, Yellowlees D & Tibbett M (2007) Cadaver decomposition in terrestrial ecosystems. Naturwissenschaften 94: 12-24

Carter DO, Yellowlees D & Tibbett M (2008) Temperature affects microbial decomposition of cadavers (Rattus rattus) in contrasting soils. Applied Soil Ecology 40: 129-137

Carter DO, Yellowlees D & Tibbett M  (2010) Moisture can be the dominant environmental parameter governing cadaver decomposition in soil. Forensic Science International 200: 60-66

Hyde ER, Haarmann DP, Lynne AM, Bucheli SR & Petrosino JF (2013) The Living Dead: Bacterial community structure of a cadaver at the onset and end of the bloat stage of decomposition. PLOS ONE 8(10): e77733

Metcalf JL, Wegener Parfrey L, Gonzalez A, Lauber CL, Knights D, Ackermann G  & Knight R (2013) A microbial clock provides an accurate estimate of the postmortem interval in a mouse model system. eLife 2: e01104

Meyer J, Anderson B, & Carter D O (2013) Seasonal variation of carcass decomposition and gravesoil chemistry in a cold (dfa) climate. Journal of Forensic Sciences 58: 1175-1182

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6 Responses to “The dead of winter”

  1. Chris Buddle Reply | Permalink

    Great post, Malcolm! I'm always keeping an eye out for 'dead things' in the yard, park or ditch. One thing that amazes me is that arthropod scavengers/decomposers play a 'mixed' role in decomposition - I don't have literature on my fingertips, but arthropods aren't the main decomposers, but rather are facilitators of the process, speeding things up by increasing surface area to allow increased microbial / fungal activity. So, I guess the point is that there's a wonderful interplay between the 'actors' in decomposition and the 'facilitators' and I don't know of great studies that really combine both effectively (although I admit I haven't done an exhausted literature search, and your citation by Carter et al. seems to sort of get at this).

    As another aside, I use decomposition of roadkill as an analogy to discuss successional concepts in ecology - fascinating because the 'end point' is a something that is completely transformed, yet you still have faunal turnover. Now I'll have to revise that lecture to focus more on microbial activity, thanks to your post!

    • Malcolm Campbell Reply | Permalink

      Thank you for the kind feedback, Chris! You are absolutely correct - there's also an important invertebrate component to decomposition. I left it out of this post in the interest of keeping this particular story simple - but there's a risk that this misleads folks into thinking that decomposition is all about microbes. Let this serve as a correction in that regard. Invertebrates play a big role in decomposition. There's a huge literature on blowfly larva and cadavers alone. In fact, what is known about blowfly larva activity on corpse is so extensive that it is used as a forensic indicator for time of death. This would be a great subject for a future post - although perhaps better done by a legitimate entomologist! ;)

      Your comment about using decomposition to illustrate concepts of succession in ecology is excellent. There are several changing "ecosystems" in play in a decomposing corpse (e.g., skin, body cavity, & soil), and they eventually converge in the gravesoil. There's an amazing story to be told based about the population dynamics of the organisms in those locations. Hopefully a glimpse into that story was captured in the post here!

      • Chris Buddle Reply | Permalink

        Yes, the forensic entomology literature is vast! But, I think ignores the microbial/fungal components, in the same way some of the microbial/fungal work ignores the arthropod component. I think there's a real need for an integrated approach to decomposition of cadavers! (btw, yes, a future post on time of death & entomology is a GREAT idea!).

        • Malcolm Campbell Reply | Permalink

          Entirely in agreement, Chris! Hopefully the post highlights some of the microbial work. For what it's worth, the paper by Jessica Metcalf and colleagues does explore changes in the nematode population. Not arthropods of course, but at least inclusion of dynamics that extend beyond bacteria and fungi. A harbinger for good things to come!

  2. Jim Woodgett Reply | Permalink

    Is the average life of a field mouse 48 months (made for a nice mirror with the decay of 48 days). I think their lives are likely a lot more brief. Even a "pampered" lab mouse only has an expectancy of of 24-28 months (no predators, ad libitum food, warmth, etc).

    This Winter, my son witnessed a rather more accelerated dissemination when a local hawk snatched up a mouse or small rat that was scurrying across the snow in our back yard. It's microbiome is now melded with that of the hawk's although there is no doubt residue dropped somewhere that may have since found its way into the nests of another rodent sheltering from the cold.

    • Malcolm Campbell Reply | Permalink

      Great question, Jim! As mice go, the genus Peromyscus is remarkable in its lifespan. Under laboratory conditions, mice of the genus Peromyscus can live for up to 8 years! The genus Peromyscus has even been proposed as a gerontological model for this reason.

      This said, you are absolutely correct that, under "real world" conditions, the lives of these mice are likely to be much shorter. For example, one study worked with a natural population of white-footed mice (Peromyscus leucopus) where the average lifespan was a mere 3-4 months. In most other studies, the lifespan seems to be around 1-2 years - due to predation and other environmental factors, including cold. This said, 48 months is thought to be the average achievable lifespan, based on the mouse's own constitution.

      I hope that this clears up the rather brief consideration of the deer mouse's longevity above. MC.

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