Current Biology
Magazine
smaller pieces. After the vultures’ wake,
often little remains of the carcass.
How are vultures doing? Nine of 23
vulture species (39%) are classed as
‘Critically Endangered’, i.e. on the brink
of extinction (Figure 1). An additional
three species are Endangered, four are
Near Threatened, and seven are Least
Concern. Over the past three decades,
vultures have declined catastrophically,
especially in Asia and Africa, and are
now the most threatened group of bird
in the world. Persecution, decreasing
food availability, habitat destruction,
and collision with energy infrastructure
all threaten vultures. However,
poisoning is the most imminent and
dire threat, as it is incredibly effective at
killing vultures. For example, in 2013, a
single contaminated elephant carcass
in Namibia killed 600 vultures.
Throughout Africa, vulture populations
are crashing. Over three generations,
the bearded vulture declined by 70%,
while seven other species declined
by 80% or more. Accordingly, four
African vulture species were classed
as Critically Endangered in 2015. The
deliberate poisoning of mammalian
carnivores, such as jackals, hyenas, and
lions, to avenge livestock loss, has led
to widespread unintentional poisoning
of vultures. And now, with the boom of
illegal rhino and elephant hunting across
the continent, poachers are intentionally
poisoning vultures because their
carcass circling cues can quickly lead
authorities to the scene of the crime.
The current acute situation in Africa is a
worrying déjà vu of the extreme declines
in South Asia, where populations of
three vulture species declined by >95%
between 1992 and 2007 due to poisoning
from the anti-inflammatory veterinary
drug Diclofenac. This drug, widely used
to treat pain and swelling in sacred cattle,
causes kidney failure in vultures after
ingestion. Because of the drug’s lethality
and vultures’ social foraging, only <1% of
livestock carcasses would have needed
to contain the drug to account for these
declines. Encouragingly, India, Pakistan
and Iran have banned the use of the drug
for veterinary purposes, but it remains
on the market in many other countries,
including throughout Europe.
Why should we care about vulture
declines? By quickly locating
and consuming carrion, vultures
outcompete and control problematic
facultative scavengers (like feral dogs
and rats), insects, and microorganisms.
When vulture populations decline,
carrion becomes increasingly available
to other organisms, in a form of terrestrial
eutrophication. Currently, many facultative
scavenger populations are increasing
worldwide, causing significant top-down
ecosystem effects via predation, invasion
and competition. Furthermore, carcasses
provide a reservoir and vector for many
diseases, including rabies, chronic
wasting, anthrax, bubonic plague, mad
cow, foot and mouth, etc. Vultures have
extremely acidic stomachs (pH = 1.0)
where most viruses and bacteria cannot
survive. When vultures eat carcasses,
they actively remove these pathogens
from the environment, as well as preempt
the colonization and reproduction of
pestilent insects.
Vultures offer valuable ecosystem
services and are a fascinating group
of birds highly adapted for their unique
lifestyle. They have often been portrayed
as malevolent creatures preying on
the sick and weary. But the reality
could not be further from the truth:
vultures are the “soap of the savannah”,
quickly and efficiently removing waste,
controlling pests, and preventing
disease outbreaks — all free of charge.
And, as true apex carnivores — eating
all animals in the food chain, including
lions, tigers, and bears — they are
excellent indicators of ecosystem health.
Where can I find out more?
Buechley, E.R., and Sekercioglu, Ç.H. (2016) The
avian scavenger crisis: Looming extinctions,
trophic cascades, and loss of critical ecosystem
functions. Biol. Conservat. 198, 220–228.
Markandya, A., Taylor, T., Longo, A., Murty, M.N.,
Murty, S., and Dhavala, K. (2008). Counting
the cost of vulture decline—An appraisal of the
human health and other benefits of vultures in
India. Ecol. Econ. 67, 194–204.
Mundy, P.P., Bunchart, D., Ledger, J., and Piper, S.
(1993). The Vultures of Africa (Academic Press).
Ogada, D.L., Keesing, F., and Virani, M. (2012).
Dropping dead: causes and consequences of
vulture population declines worldwide. Ann. N.Y.
Acad. Sci. 1249, 57–71.
Royet, E. (2016). Vultures are Revolting. Here’s
Why We need to Save Them. Natl. Geogr. Mag.
Available at: http://ngm.nationalgeographic.
com/2016/01/vultures-text.
Sodhi, N.S., Sekercioglu, C.H., Robinson, S., and
Barlow, J. (2011). Conservation of Tropical Birds.
Wiley-Blackwell. Oxford.
Wilson, E.E., and Wolkovich, E.M. (2011). Scavenging:
how carnivores and carrion structure communities.
Trends Ecol. Evol. 26, 129–135.
University of Utah, Department of Biology, 257 S.
1400 E. Rm. 201, Salt Lake City, UT 84112, USA.
*E-mail: e.buechley@utah.edu
Current Biology 26, R543–R576, July 11, 2016 © 2016 Elsevier Ltd. R561
Quick guide
Microbiology of
death
Jessica L. Metcalf1,2,*,
David O. Carter3, and Rob Knight2,4,5
When a mammal dies, what
happens? Decomposition happens.
When a mammal dies its immune
system shuts down, internal
temperatures change, and internal
bacteria begin to grow in ways
impossible while under the constraints
of a living host. The internal
environment then experiences another
major event: rupture — a break in the
skin that allows air, microbes, and
insects to enter, and bodily fluids to
exit. A carcass releases large amounts
of nitrogen into the environment,
mostly in the form of ammonia, as well
as carbon, phosphorous, and other
nutrients important for life. A dead
body becomes a hotspot of nutrients,
water, and ecological activity.
How do we study mammalian
decomposition? What is an
anthropological research facility?
You may have heard the term ‘body
farm’ in the news or on popular
forensic science shows like Bones
or CSI. In the scientific community,
these research centers are more
appropriately called ‘anthropological
research facilities’, and are important
for studying the anthropological,
ecological, and forensic science
implications of mammalian
decomposition. Because of the
interest in human decomposition
for anthropology and its practical
importance in forensic science, these
facilities use human donors for field
experiments to test the effects of
different variables on taphonomy — the
processes of decomposition. Some
facilities also use pigs, which are good
biological proxies for humans and
allow for more replicates and better
control over factors such as age,
weight, and sex.
What organisms are involved in
decomposition? Decomposition is
one of the most important ecosystem
processes — if it were not efficiently
 Current Biology

Magazine

Microbial decomposers Where do the microbial decomposers

Bacteria, eukaryotes (non-fungal), fungi come from? Everywhere. Inside and
Fresh out, we are surrounded by microbes
that flourish after death. Decomposer
Proteobacteria
Ascomycota Pseudomonas
microbes appear to mainly emerge
Stromatonectria Enterobacteriaceae from the rich microbial biodiversity
Unidentified Proteobacteria in soils. This is especially true for the
Death Wohlfahrtiimonas
Firmicutes Ignatzschineria microbial eukaryotic community, such
Sporosarcina Basidiomycota as the nematodes, fungi, and amoeba.
Firmicutes Lysurus
Dry remains Lactobacillales Bacteroidetes Active decay Except for some fungi, microbial
Myroides eukaryotes are usually absent during
Ascomycota
Proteobacteria
Yarrowia
decomposition unless soil is present.
Acinetobacter As a result, decomposition tends to be
Nematoda
Firmicutes Rhabditidae slower in these settings. For example,
Planococcaceae Proteobacteria mice decompose three times more
Zygomycota Pseudomonadaceae
Mortierellaceae Stramenopiles Chromatiaceae
quickly on normal soils than on soils
Plasmopara Proteus that have been sterilized.
Bacteria, in contrast, are ubiquitous.
Advanced decay Multiple decomposer bacteria
Current Biology are detectable at extremely low
abundances in many environments,
Figure 1. Succession of microbes during the decomposition of a human cadaver in Texas. including the human gut and skin,
Bacterial (blue) and microbial eukaryotic (orange, non-fungal; red, fungal) communities change in and on insects, and within soils.
composition rapidly on the skin of two decomposing human cadavers at the Sam Houston State Acinetobacter, which is highly
Southeastern Applied Texas Forensic Science Facility. We highlight a small subset of taxa that abundant during advanced decay, is
become highly abundant during decomposition, and we also show the major stages of decom-
position with which these taxa are associated: fresh (i.e. a fresh cadaver), active decay, advanced
also commonly detected on human
decay, and dry remains). The stopwatch indicates the succession of microbes over time, and the skin and in soils, although at far lower
utility of the microbial clock concept in estimating time of death. We show a photo of a fly larval abundances. Bacteria in the genera
mass under the skin during active decay, and a photo of a skull during the dry remains stage Wohlfahrtiimonas and Ignatzschineria
(photo credit: laboratory of Sibyl Bucheli). are carried in by blow flies soon after
death (Figure 1). Decomposer bacteria
accomplished by microbes, insects, as Pseudomonas. In the bacterial are likely ubiquitous taxa that are very
and vertebrate scavengers, we would family Enterobacteriaceae, Proteus good at competing for, and quickly
have a build-up of unpleasant organic mirabilis appears to play an important utilizing, rich pulses of nutrients that
waste on earth. Microbes play an role in attracting insects to bodies, become available only briefly.
important role in breaking down which facilitates decomposition.
macromolecules into more simple Next, nematodes (microscopic Can microbes be used to estimate
molecules. Many bacteria that become worms) in the family Rhabditidae the time of death? The microbiological
abundant during decay, such as become highly abundant as they changes associated with death can
taxa in the family Rhizobiaceae and consume a bumper crop of bacterial provide a vast source of biological
Chromatiaceae, are involved in the biomass. During advanced decay, the evidence for medicolegal death
nitrogen cycle, catalyzing processes microbial community is dominated investigation. It turns out that the
including denitrification and nitrate by saprotrophic fungi in the family microbial succession that occurs
reduction. Additionally, members of Mortierellaceae and bacteria in the during decomposition is quite clock-
decomposer bacterial communities genus Acinetobacter, both of which like. Several independent research
contain genes encoding components can break down a variety of organic groups have recently demonstrated
of pathways that break down amino compounds. Although Acinetobacter is that microbial succession allows
acids such as glycine, glutamate, most highly abundant during advanced for accurate estimation of the time
ornithine, and lysine. The latter two decay, it is also abundant during the since death, resulting in models that
amino acids become putrescine and onset of active decay, suggesting it can predict the time of death within
cadaverine, respectively, which smell may utilize multiple substrate types approximately 2 – 4 days during the
as good as they sound. during the decomposition process. initial 25 days after death. Therefore,
The decomposer microbial Once a cadaver has reached the a ‘microbial clock’ (Figure 1) may be
community is not a static group of dry remains phase, we detect useful for helping criminal investigators
microbes, but a rapid succession of bacteria such as Sporosarcina, which narrow the uncertainty surrounding
bacteria and microbial eukaryotes break down low molecular weight the time of death in unattended and
(Figure 1) that compete for nutrients compounds such as urea. These suspicious death scenes.
and consume each other. For example, are just a few examples of the many
initial blooms of bacteria often microorganisms and the roles they Does environment type or season
include fast-growing, metabolically contribute to the decomposition affect how a person decomposes?
diverse, opportunistic bacteria such process. Yes, indeed. Imagine a person dies

R562 Current Biology 26, R543–R576, July 11, 2016

Current Biology
Magazine
in Texas during summer and another
person dies in mid-winter in Colorado.
Both would decompose quite
differently. The corpse in Texas would
decompose relatively rapidly because
it would be used by several groups
of decomposers. Microbes, insects,
and scavengers would likely drive
the decomposition in this setting. In
contrast, the corpse in Colorado would
decompose slowly, as though it were
placed in a cooler. Insects may not be
present and the corpse could be well
preserved if it is not discovered by a
scavenger. Given these differences, is it
possible to calibrate a microbial clock
that estimates time of death across
geography and seasons? Yes, if the
clock is calibrated using a temperature-
based scale — that is, by accumulated
degree day (the product of temperature
and time) instead of calendar day.
Recent research suggests that the
microbial clock is robust regardless
of season and soil types. Research is
underway to calibrate the microbial
clock by simultaneously examining the
influence of environmental factors on
decomposition ecology across different
regions of the US during all four
seasons. Eventually, similar research
must be conducted on a global scale
to account for environments not
represented in the US.
If a body is buried or moved, can soil
microbes provide clues? Yes. Soils
have been used as evidence for over
a century, even by Sherlock Holmes!
Soil texture, mineralogy, pollen profile
and, more recently, microbial DNA
have all been used to characterize soils
as evidence. Several recent studies
employing amplicon-based sequencing
of bacteria, archaea, and microbial
eukaryotes have demonstrated, on
a small scale, that gravesoils can be
distinguished from non-decomposition
soils due to the cadaver releasing an
immense amount of organic material
into the soil. This organic material serves
as food for these microorganisms and,
because there is so much of it released,
gravesoils can be a unique habitat for
microorganisms for over a year after
decomposition. Additionally, soils from
different localities can be distinguished
from each other based on microbial
DNA. Therefore, soil can also be used as
trace evidence to link objects or people
with localities.
If you die in a forest and no one
is around to hear, will you make a
sound? Yes, it will be the sound of
microbes, insects, and scavengers
munching away at the nutritious
resource that is your corpse.
Where can I find out more?
Carter, D.O., Yellowlees, D., and Tibbett, M.
(2007). Cadaver decomposition in terrestrial
ecosystems. Naturwissenschaften 94, 12–24.
Carter, D.O., Metcalf, J.L., Bibat, A., and Knight, R.
(2015). Seasonal variation of postmortem
microbial communities. Forensic Sci. Med.
Pathol. 11, 202–207.
Finley, S.J., Pechal, J.L., Benbow, M.E.,
Robertson, B.K., and Javan, G.T. (2016).
Microbial signatures of cadaver gravesoil during
decomposition. Microb. Ecol. 71, 524–529.
Hyde, E.R., Haarmann, D.P., Petrosino, J.F., Lynne,
A.M., and Bucheli, S.R. (2015). Initial insights
into bacterial succession during human
decomposition. Int. J. Legal Med. 129, 661–671.
Lauber, C.L, Metcalf, J.L., Keepers, K.,
Ackermann, G., Carter, D.O., and Knight, R.
(2014). Vertebrate decomposition is accelerated
by soil microbes. Appl. Environ. Microbiol. 80,
4920–4929.
Jesmok, E.M., Hopkins, J.M., and Foran, D.R.
(2016). Next-generation sequencing of the
bacterial 16S rRNA gene for forensic soil
comparison: a feasibility study. J. Forensic Sci.
61, 607–617.
Metcalf, J.L., Wegener Parfrey, L., Gonzalez, A.,
Lauber, C.L., Knights, D., Ackermann, G.,
Humphrey, G.C., Gebert, M.J., Van Treuren,
W., Berg-Lyons, D., et al. (2013). A microbial
clock provides an accurate estimate of the
postmortem interval in a mouse model system.
Elife 2, e01104.
Metcalf, J.L., Xu, Z.Z., Weiss, S., Lax, S., Van
Treuren, W., Hyde, E.R., Song, S.J., Amir, A.,
Larsen, P., Sangwan, N. et al. (2016). Microbial
community assembly and metabolic function
during mammalian corpse decomposition.
Science 351, 158–162.
Pechal, J.L., Crippen, T.L., Benbow, M.E., Tarone,
A.M., Dowd, S., and Tomberlin, J.K. (2014). The
potential use of bacterial community succession
in forensics as described by high throughput
metagenomic sequencing. Int. J. Legal Med.
128, 193–205.
Young, J.M., Weyrich, L.S., and Cooper, A. (2014).
Forensic soil DNA analysis using high-
throughput sequencing: a comparison of four
molecular markers. Forensic Sci. Int. Genet. 13,
176–184.
Zheng, L., Crippen, T.L., Holmes, L., Singh, B.,
Pimsler, M.L., Benbow, M.E., Tarone, A.M.,
Dowd, S., Yu, Z., Vanlaerhoven, S.L., et al.
(2013). Bacteria mediate oviposition by the
black soldier fly, Hermetia illucens (L.), (Diptera:
Stratiomyidae). Sci. Rep. 3, 2563.
1
Department of Ecology and Evolutionary
Biology, University of Colorado, Boulder,
CO 80309, USA. 2Department of Pediatrics,
University of California, San Diego, San Diego,
CA 92037, USA. 3Laboratory of Forensic
Taphonomy, Forensic Sciences Unit, Division
of Natural Sciences and Mathematics,
Chaminade University of Honolulu, Honolulu,
HI 96816, USA. 4Department of Computer
Science and Engineering, University of
California, San Diego, San Diego, CA 92037,
USA. 5Center for Microbiome Innovation,
University of California, San Diego, San Diego,
CA 92037.
*E-mail: jessica.metcalf@colorado.edu
Current Biology 26, R543–R576, July 11, 2016 © 2016 Elsevier Ltd. R563
Primer
Climate, decay, and
the death of the
coal forests
David Hibbett1,*, Robert Blanchette2,
Paul Kenrick3, and Benjamin Mills4
After death, most of the biological
carbon in organisms (Corg) is returned
to the atmosphere as CO2 through
the respiration of decomposers and
detritivores or by combustion. However,
the balance between these processes
is not perfect, and when productivity
exceeds decomposition, carbon
sequestration results. An unparalleled
interval of carbon sequestration in
Earth’s history occurred during the
Late Carboniferous (Pennsylvanian)
and Permian Periods (ca. 323–252
Ma), when arborescent vascular
plants related to living club mosses
(Lycophytes), ferns (Monilophytes),
horsetails (Equisetophytes) and seed
plants (Spermatophytes) formed
extensive forests in coastal wetlands. On
their death, these plants became buried
in sediments, where they transformed
into peat, lignite, and, finally, coal.
The botanical origin of coal is not
disputed, but the causal factors
that determined the rate of Corg
sequestration and that limited the
extent of coal forests are matters of
debate. One theory is that abiotic
factors were solely responsible for
shifts in rates of Corg burial. Under
this view, the high rate of carbon
sequestration during the Permo-
Carboniferous was caused by unusually
widespread mire environments with
anoxic, waterlogged conditions, which
inhibited decay, and contractions in
coal forests were caused by climatic
shifts toward drier conditions.
An alternative hypothesis, proposed
by Robinson, introduced, in addition
to geological and environmental
factors, the concept that biological
interactions among organisms might
also be important in coal formation.
Specifically, the dramatic accumulation
of Corg in the Permo-Carboniferous
occurred in part because the fungi that
are able to efficiently decompose lignin
(a recalcitrant, heterogeneous plant
polymer) had yet to evolve and diversify.