A Summer Carrion Study of the Baby Pig Sus Scrofa Linnaeus

Author(s): Jerry A. Payne

Source: Ecology, Vol. 46, No. 5 (Sep., 1965), pp. 592-602
Published by: Ecological Society of America
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592

JERRY

A. PAYNE

. 1953a. The settlement of Ophelia bicornis Savigny larvae. The 1951 experiments.
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A SUMMER CARRION STUDY OF THE BABY PIG SUS SCROFA LINNAEUS

JERRY

A.

PAYNE

Radiation Ecology Section, Health Physics Division

Oak Ridge National Laboratory,1 Oak Ridge, Tennessee
Abstract. A carrion study of the baby pig, Sus scrafa Linnaeus, was conducted during the
summers of 1962 and 1963 in a mixed mesophytic hardwood-pine community at Clemson,
South Carolina. Six stages of decomposition were delimited for carrion exposed to arthropods: fresh, bloated, active decay, advanced decay, dry, and remains. Five stages were recognized for carrion protected from arthropods: fresh, bloating and decomposition, flaccidity and
dehydration, mummy, and desiccation and disintegration. Carrion free of insects decomposed
and dried very slowly, retaining its form for many months, while 90% of the carrion open to
insects was removed in 6 days. Carrion temperature during the bloated through advanced
decay stages differed widely from that of air or soil.
A definite ecological succession occurred among the fauna of carrion. Each stage of decay
was characterized by a particular group of arthropods, each of which occupied a particular
niche. Their activities were influenced by physical properties of carrion, rapidity of putrefaction, time of day, and weather. A total of 522 species representing 3 phyla, 9 classes,
31 orders, 151 families, and 359 genera were collected from decomposing pigs. Four orders of
arthropods (Coleoptera, Diptera, Hymenoptera, and Araneida) accounted for 78%o of the
carrion fauna. Two coleopterous families, Histeridae and Staphylinidae and three dipterous
families, Sarcophagidae, Calliphoridae, and Muscidae, represented 26%o of the fauna.

nite series of changes, much the same as do decomposing

logs or feces. One of the objectives of this
"A neglected microsere is that of carrion. Decomposing
bodies of fishes washed ashore, and the remains of dead research was to outline the various recognizable
reptiles, birds, and mammals, are especially well suited
stages through which a pig carcass passes as it
for research in this connection. Associated with changes
decomposes. In addition, the faunistic succession
in the chemistry of the flesh are numerous problems inresulting from the summer exposure of the carvolving bacterial activities, carrion biocoenoses, and the
casses of newborn pigs was given special attention.
microseral succession of the carrion fauna."
Previous workers have neglected the study of
Allee, et al. (1949: 570)
carcasses isolated from insects when studying carMuch of the work done on carrion has been rion microcommunities. A very important aspect
confined largely to the habits and life histories of of this summer carrion study concerned the stages
various carrion insects, the taxonomy of certain of decomposition of pigs protected from insects.
groups, and problems of economic importance such Previous carrion workers also have neglected deas the screw-worm and the sheep blow fly; a few cay rates. The rates of removal of the two types
have been concerned with carrion succession. of pig carrion (open to insects and insect free)
These studies provided much needed information were investigated. It is hoped that this study will
necessary for a better understanding of the ecology show vividly the role of certain fauna as scavengers
of carrion. However, many aspects of the carrion and will contribute knowledge about the processes
microcommunity have been neglected.
which redistribute the matter in a dead body back
Many excellent works have been published on to the parent community.
carrion subjects but few have been concerned with
THE STUDY AREAS
the actual process of decomposition of the carcass.
As a carcass decomposes it passes through a defiThe field study for this summer carrion research
was conducted at a locality about 1 mile south
' Operated by Union Carbide Corporation for the U. S.
southeast of the city limits of Clemson. South
Atomic Energy Commission.
INTRODUCTION

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Late Summer

1965

CARRION

STUDY

Carolina, on Clemson College property. Coordinates of research location are 1,453,100(E)614,690(N), based on the South Carolina plane
coordinate system.
Clemson College is located in northwestern
South Carolina in Oconee and Pickens Counties.
The college is approximately 20 miles from the
foothills of the Blue Ridge Mountains in the Piedmont Section. The average elevation is 800 ft
above sea level.
To facilitate daily observations of carrion, the
study area chosen was located within walking distance of the college insectary. Laboratory procedures involved in the research were conducted at
the insectary. The study area was selected for
uniformity with respect to cover, sunlight, and
drainage. Two areas with essentially the same
composition of flora and fauna were selected adjacent to each other. Each area consisted of a
40-ft square, with a caged carcass located at each
corner. A wooden utility building with a sheetmetal roof located in one of the study areas housed
the equipment necessary for the field work. A
Berlese funnel was located outside the entrance to
the building for collection of soil insects and for
large-scale collections of carrion arthropods.
The areas were located in a mixed mesophytic hardwood-pine community near the top of a hill with slight
slope. The cover formed by the trees was of medium
density. The canopy was composed mainly of short-leaf
pine, Pings echinata Mill.; southern red oak, Quercus falcata Michx.; tulip poplar, Liriodendron tulipifera L.; and
scarlet oak, Quercus coccinea Muench. The principal
trees of intermediate height were sourwood, Oxydendrum
arboreum (L.) D.C.; black gum, Nyssa sylvatica Marsh.;
black oak, Quercus velutina Lam.; pignut hickory, Carya
glabra (Mill.) Sweet; dogwood, Cornus florida L.; and
mockernut hickory, Carya tomentosa Nutt.
The chief constituents of the ground cover, which was
of medium density, were seedlings and sprouts of yellow
poplar, Liriodendron tulipifera L.; sourwood, Oxydendron
arboreum (L.) D.C.; black gum, Nyssa sylvatica Marsh.;
mockernut hickory, Carya tomentosa Nutt.; blackberry,
Rubus sp.; and wild grape, Vitis rotundifolia Michx.
Other ground cover consisted of a few scattered sprouts
and seedlings of black cherry, Prunus sero tina Ehrh.,
willow oak, Quercus phellos L.; green briar, Smilax sp.;
huckleberry, Gaylussacia sp.; and wild ginger, Asarutm
sp. Few herbs and grasses were present.
The forest floor was covered by a 1-inch layer of leaf
litter comprised chiefly of deciduous leaves and pine
needles. In some few spots the mineral soil was exposed.
Carcasses in both areas were sometimes shaded for rather
long intervals, but all received nearly the same amount
of direct and indirect sunlight.

OF THE

BABY

593

PIG

cauda), cotton rats (Sigmodon hispidus), and

eastern chipmunks (Tamias striatus). In the beginning of these practice studies, all arthropods
(especially insects) were collected and identified
until a large reference collection was established.
Some difficulty was encountered in observing
the arthropods present chiefly because of the fast
rate of decay and the small size of the study animals. The various stages of decay (microseral
stages) were hardly recognizable in these small
animals.
Larger carrion was tried including dogs, cats,
squirrels, rabbits, chickens, birds, and pigs. Dogs
and cats were not selected because of the difficulty
in getting enough specimens of uniform size.
Chickens and other birds were eliminated because
feathers caused problems in estimating and sampling insects. Dead rabbits and squirrels were
collected from the highways and streets. However, they were not used because of the problem
involved in estimating the time of death and in
getting sufficient numbers of intact specimens.
These preliminary studies served to emphasize
several points: (1) the need for animals of uniform and relatively large size, (2) the difficulty
of recovering or observing carrion insects in
feathers, and (3) the need for thorough and frequent examination of carcasses.
Baby pigs, Sus scrafa Linnaeus, were finally
selected as research animals. They were collected
in plastic bags within 2 hours of death and
placed in a freezer until used. These pigs were
either dead at birth or crushed by the mother
shortly thereafter. Most of these pigs weighed
between 1,000 and 1,400 g.
In the preliminary studies dogs, cats, opossums,
humans, and birds examined and disturbed the
carcasses. Sometimes the carcasses were partly
eaten, were missing from the area, and, on one
occasion, were buried. For these reasons cages
were a necessity throughout the study.
CAGES

The pigs were placed in three types of cages:

first, an observation cage, 4 X 4 X 2 ft, used solely
for collection and observation of insects. This
cages was merely an enclosure of 2 X 6 in. welded
woven wire, open at the bottom. To reduce the
danger of disturbance by vertebrates, traps were
placed at intervals around this cage. Second,
cages designed toi permit the entrance of insects
AND METHODS
MATERIALS
In the spring and early summer of 1962 a series were 2 X 2 X 2 ft and covered with 52-in. galof preliminary carrion studies were undertaken, vanized hardwarde cloth. Third, cages designed
using frogs (Rana), toads (Bufo), white-footed to exclude insects were of the same dimension as
mice (Peromyscus leucopus), house mice (Mus the second group, but covered with two layers of
musculus), short-tailed shrews (Blarina brevi- 14- X 18-mesh screen. Rubber strips tacked in-

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594

JERRY

Ecology, Vol. 46, No. 5

A. PAYNE

side the plywood tops gave added protection

against the entry of insects. Frames for all cages
were of pine, and access was provided by hinged
plywood tops. The bottom of each cage had complete contact with the soil.
FIELD

TECHINIQUES

Ten pigs were used for each series of observations. They were handled as follows:
1. Eight pigs uniform in weight and physical
condition were taken from the freezer. Eight
nylon screens were selected and weighed.
2. Pigs were weighed on an autopsy balance
and placed on a nylon screen in their respective
cages. These screens were used throughout the
experiment for handling the pigs when weights
were taken. The pigs in the decay stages could
not be weighed unless screens for containing them
were used.
3. Each pig's physical condition was noted and
recorded.
4. Insects present around the cages at the beginning of each experiment were also recorded.
5. Each pig was weighed on a schedule of S-hr
intervals (8 AM, 4 PM, and 12 midnight). This
schedule was maintained for 8 to 13 days depending on the rate of decomposition.
6. The two remaining pigs were placed in the
observation cage.

FIG. 1.

Twelve-channelthermistor-actuatedtelethermometer with interchangeableprobes.

MICROCLIMATOLOGIC

METHODS

Records of the carrion and environmental temperature were obtained with a thermistor-actuated
thermometer (Fig. 1) Six interchangeable probes
made it possible to obtain simultaneous records at
six separate points. The interchangeable probes
were A8 in. in diameter and were attached to a
meter by 10-ft, vinyl-covered flexible leads with
phone plugs. The six positions were read merely
bv switching from channel to channel.
Two pigs were used in each experiment. It was
discovered earlier in the research that penetration
of the skin with the thermometer provided another
entrance point for dipterous larvae. Consequently,
At each 8-hr interval the physical condition of a
centigrade thermometer was forced into each
each carcass was noted, especially with regard to animal
by way of the mouth, which already served
the extent of bloating, amount of fluid, characteris- as a
natural entrance, to take internal temperatic odors, and amount and location of decomposi- tures. Skin
temperature probe no. 1 was placed
tion. Much care was taken in moving the ex- under the
left ear of the pig for taking air temtremely bloated animals to the autopsy balance, peratures above the
pig, and no. 2 was placed unand in containing the fluids which were present der the pig
between the nylon screen and the pig's
during the various decay stages. In the case of abdomen for
taking temperatures under the pig.
carcasses exposed to insects, particular care was
Corresponding temperatures were also taken on
taken not to disturb the attracted fauna until it the other
pig with probes no. 3 and no. 4. Probe
could be observed. At no time were collections no. 5 was
placed on the top of the litter to record
made from the carcasses in the cages exposed to air
temperature.
No. 6 was placed beneath the
insects.
litter to measure the soil temperature.
Carcasses in the observation cage were examThe thermometer was in operation from August
ined both day and night at intervals more frequent
13 to August 19, 1962. On August 19 the pig
than the 8-hr routine observed for other specicarrion reached the dry stage, and carrion tenmmens. These carcasses, as well as others not in
perature became equal to environmental temperathe observation cage, provided the source of all
ture. The carcasses were so disintegrated by this
collections. Occasionally a Berlese funnel was
time that the locations "internal," "above," and
used to extract insects from a carcass. Frequently
"below" no longer had meaning.

excavations beneath the carrion were searched

thoroughly by using a gardener's tool. These
RESULTS AND DISCUSSIONS
operations could not be performed on carrion in
Stages of decomposition
other cages because of the possibility of altering
the successional pattern. Detailed methods for
While pig decomposition is a continuous process
collection and preservation are described elsewhere without discrete stages, for discussion purposes
it is convenient to divide the decomposition se(Payne 1963; Payne and Crossley 1965).

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Late Summer 1965

CARRION

STUDY

quence into six stages. Reed (1958) divided his

dog carcass seres into only four stages. Howden
(1950) recognized two major phases in the decomposition of carrion. She established her system on the presence or absence of maggots and
their predators. Fuller (1934) separated the
process of putrefaction into three stages. Megnin
(1894) divided cadaveronic decomposition into
eights stages covering over 3 years.
A better definition of the carrion decomposition
sequence could be made by placing dead baby pigs
of approximately the same size in two separate
sets of cages (insect-proof and open to insects).
Carrion open to insects was described on the basis
of physical conditions, odors, and characteristic
insects present. Carrion free from insects had
fewer distinguishing points.
Carrion open to insects

1. Fresh stage.-The fresh stage (F'ig. 2) commenced when the frozen animals were taken from
the freezer and continued until bloating was evident. Odors, when present, were those of straw
and pig mash.

FIG. 2.

Fresh stage, first day of placement.

W\ith~inl 5 minutes after the fresh-frozen pigs

were placed on the nylon screens within each cage,
sarcophagids were observed on the carcasses.
Droplets of water were forming on the head and
abdomen. Calliphorids, chiefly Cochliomyia macella~ria,(F.), arrived at the pig within 10 ruin after
placement and began feeding at the umbilical cord
and mouth. These body areas thawed very
quickly. Shortly thereafter yellow jackets, Ves(Buyss.), were seen on the carpula, mna-culifrons
casses. They fed on the liquids present and also
captured calliphorid adults. Other calliphorid
species were present at the carcass 1 hour after
placement.
Eggs were deposited by the Sarcophagidae and
Calliphoridae adults while the carcasses were

OF THE

FIG.

BABY

595

PIG

3. Bloated stage with egg masses, two days after

placement.

still partially frozen. Some carcasses required as

much as 6 hours to thaw. Several species of
ants were found feeding on the lips and noses of
the pigs and carrying other insect eggs from the
carcasses during this period of thawing.
Insect activity declined appreciably during the
first night. No calliphorids, sarcophagids, or yellow jackets were present. Ants were confined
to the eyes and mouth. Several species of Phalangida (daddy longlegs) were observed feeding on
the juices present.
2. Bloated stage.-Pigs were beginning to bloat
by the second day (Fig. 3). The first visible
signs included a slight inflation of the abdomen,
and in male pigs the scrotum became inflated.
Bubbles of blood were beginning to form at the
nose and anus. Calliphorids of several species
arrived in great numbers early in the morning of
the second day. Sarcophagids, muscids, and calliphorids continued to deposit eggs. Mating pairs
of Diptera were often captured by yellow jackets.
Piophilidae and Lonchaeidae were observed on
the carcasses for the first time. They usually
appeared when the pigs were showing indications
of bloat.
Two species of Scarabaeidae, Onthophagts
hecate (Panzer) and Ateuchits histeroides \Vleb..
arrived at dusk on the second day. They immediately buried themselves in the wet soil beneath
the abdomen of the carcass. Very few histerids
visited the carcasses while they were still cool and
fresh.
During the night the scarabs occasionally ventured from beneath the carcass and fed on the
bloated carrion. They constructed tunnels in the
soil in which they remained during the daylight
hours. Ants were very busy at the carcass site.
Prenolepsis imparis (Say) and Camponotus aniericanus Mayr were the dominant species.
On the third day the skin on the abdomen and

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5%9

JERRY

A. PAYNE

between the hind legs began to tighten, giving the

pig the appearance of a taut, black balloon. Odors
of decay became noticeable during these conditions,
probably from the juices and gases bubbling from
the nose and anus. Juices were even seeping
into the soil from the bloated animal. Histerids
and small staphylinids made their appearance at
the carcass for the first time. They remained hidden beneath the carcass. Yellow jackets returned
again and took their share of fluids and dipterous
adults. Drosophilidae, Coreidae, and Stratiomyidae were seen walking on the carcasses.
By late afternoon a smell of decay permeated
the entire study area. Freshly hatched dipterous
larvae were beginning to feed on the pig carrion.
Their feeding activity was confined to the mouth,
nostrils, ears, umbilical cord, anus, and between
the legs. The puncture of the skin and release of
gases was probably aided by the early feeding
activity of maggots.
Activity as usual declined at dusk. Diptera
began to leave the carcasses as the sun set. Histerids, scarabs, small staphylinids, coreids, and
ants were active at night. Only the ants were
present in large numbers. Many more dipterous
larvae were hatching. Histerids would occasionally prey upon these masses of small larvae.
3. Active decay stage.-Penetration of the skin
by larvae had usually occurred by the fourth day
(Fig. 4). Staphylinids and histerids had increased

FIG. 4.

Active decay stage, four days af ter placement.

in numbers overnight. The adult calliphorid and

muscid populations had fallen off, but many were
still present feeding on the carrion. No mating
was recorded among the M.\uscidae,Sacrophagidae,
and Calliphoridae at this late date. Sepsidae and
Otitidae were observed on the carrion for the first
time. The first silphid to make an appearance at
the carrion was Silpha, amtericana Linnaeus, the
large black and yellow silphid.
Dipterous larvae had now begun to feed actively
upon the carrion. They were concentrated in

Ecology, Vol. 46, No. 5

those areas of the body which offered least resistance to penetration, such as the eyes, ears, nose,
mouth, and anus. Histerids and staphylinids were
eating these small larvae. Specimens of the large
black and white staphylinid, Staphylinus maxillostts L., were beginning to discover the carcass.
They were usually very active during the daytime,
entering the decomposing flesh and feeding on the
maggots. Yellow jackets were very abundant on
the fourth day.
Activity of diptera declined at dusk. Histerids,
staphylinids, silphids, and scarabs continued their
feeding. Euspilotuts assinmilis (Payk.) was the
most abundant species of Histeridae. Several species of Staphylinidae and Scarabaeidae were present. Ants, roaches (Parcoblatta sp.), and Phalangida were among the arthropods gathered at the
carrion.
The adult Diptera returned the next morning.
By midday Tachinidae, Syrphidae, and Sphaeroceridae were recorded as new in the succession.
Honey bees, Apis mellifera L., and bumble bees,
Bombus impatiens Cr., occasionally fed on the
fluids present on the carrion and ground. Calliphorid activity had declined appreciably. Muscidae, predominantly Fannia sp., and Sarcophagidae
were still abundant, however. Several braconid
wasps were observed among the many insects at
the carrion.
All of the flesh from the head and an area
around the anus and umbilical cord had been removed from the carcass by this time. Only
skin and bones remained on the head. All portions of the carcass except the head had a characteristic wet appearance. Liquefaction and disintegration became noticeable. Odors of decay
were strong and stinking.
Larvae were now crowded in the thoracic and
abdominal regions of the carcass. Necrodes surinainensis (F.) (Silphidae), Staphylinus macidosus Grav. (Staphylinidae), and Geotrtpes sp.
(Geotrupidae), made their first appearances as
carrion inhabitants. Coleoptera were the dominant adult insects present; maggots the dominant
immature forms.
Insect activity declined at night. Moths were
recorded for the first time in the succession. They
sucked up fluids which had collected in the decomposing carcasses. Ants, roaches, histerids,
staphylinids, silphids, carabids, and scarabs were
also busy.
4. Advanced decay stage.-In this stage (Fig.
5) most of the flesh had been removed from the
carcass; however, some flesh still could be found
in the abdominal cavity. Odors of decay were
beginning to fade.
Mainy changes began to occur on the sixth (lay.

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Late Summer

*l

1965

CARRION

STUDY

OF THE

BABY

PIG

597

-~~~~~~~~~~~~~4
I.~~~~~~~~.

FIG. 5.

Advanced decay stage, six days after placement.

Dipterous larvae were beginning to. migrate from

the carcass. Very few calliphorids, muscids, or
Diptera as a group were present. Sphaeroceridae,
Leptocera sp.; Drosophilidae, Drosophila aflinis
Sturtevant; and Otitidae, Euxesta sp. were the
dominant Diptera present. Many of the silphid
and scarab species were leaving. Staphylinids and
histerids were still present in medium numbers.
Trogids, especially Trox monochus Herbst and
Trox aasper (LeConte), had entered during the
night and hidden beneath the carcass. Occasional
dermestids, Dermestes caninus Germar and Derdoestes marontratus Say, were observed entering
the carcass. Staphylinids and histerids remained
under the carcass throughout most of the day.
During the night of the sixth day more staphylinids and histerids left the carcass, and dermestids,
trogids, and nitidulids entered the carcass. Numbers of ants and roaches also decreased. Many of
the remaining histerids buried themselves in the
wet soil beneath the pig carrion. Many of the
smaller species of staphylinids and scarabs reiained in the soil at the carcass site. Excavations
and tunnels were extremely abundant in the soil.
The carcass was beginning to dry by the seventh
day. Some calliphorid larvae could be found
feeding on the remaining scraps. Dermestids and
nitidulids were active during the daytime, while
trogids remained sheltered from the light beneath
the carcass. Muscid larvae (Fannia sp.) took
their position on the carrion where the last remaining scraps were to be found. They were
never present in numbers comparable to the calliphorid larvae, and larval stages of the two families very seldom occurred at the same time. The
remaining staphylinids and histerids were not observed feeding on Fannia larvae.
5. Dry stage.-By the eighth day only dry skin,
cartilage, and bones remained (Fig. 6). Odors
ranged from that of dried animal skin to that of
wet fur. During the eighth, ninth, and tenth days

FIG.

6. Dry stage, eight days after placement.

there was a gradual movement of new species to

the carcass with many of the formerly dominant
carrion fauna leaving. The histerids, many staphylinids, silphids, and most adult Diptera left the
carrion. Centipedes, millipedes, isopods, snails,
and roaches took positions beneath the carrion.
Leptodirids, trogids, dermestids, nitidulids, clerids,
ants, and mites occupied the dried carrion. Dipterous larvae (Fannia sp.) were sometimes observed even on the dried remains. During this
stage larval staphylinids and larval silphids were
observed. Since no readily available food was
present, these insects could not complete their
development. Some of the soil-inhabiting carrion
insects such as the small beetles probably fed on
the carrion media which had adhered to the soil
particles. Ants were often observed carrying these
bits of carrion scraps.
During the next 10 days there was a considerable overlapping of soil and carrion insects. The
trogids and dermestids began to leave the bleached
bones and masses of matted hair and skin. Other
noncarrion insects entered and established a cryptozoic habitat. In a few instances, the remains
became wet and odoriferous after a summer

FIG.

7. Remains stage, four weeks after placement.

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598

JERRY

Ecology, Vol. 46, No. 5

A. PAYNE

shower, and Sphaeroceridae, Drosophilidae, Pso- in the cage. All pigs were extremely bloated by
cidae, Trogidae, Nitidulidae, and several other the end of the third day. The carcasses were befamilies were again attracted to the remnants.
ginning to become oily and greasy by this time.
6. Remains stage.-It was almost impossible to Strong putrefactive odors were present by the
indicate when the dry stage ended and remains fourth and fifth days. Fluids were constantly
stage (Fig. 7) began. Odors present were that escaping by way of mouth and anus. Pig carcasses
of litter and soil. All the skin and flesh had been had to be handled carefully by the sixth day beremoved from the pigs. Only hair, bits of skin, cause of the danger of rupturing the carcass while
bones, and teeth remained of the original pig. No taking the weights. Bubbles were beginning to
typically carrion-feeding or visiting insects were form under the skin on the seventh and eighth
present. Insects present were assumed to be those days. The underlying blood and decomposing
which normally inhabited the area. However, juices gave the skin a very black appearance.
stratiomyid larvae, silphid pupae, and trogid larvae Fluids were beginning to dry in the cage by the
were occasionally taken from the soil. The bound- eighth and ninth days. The odors from the dearies and fauna of this stage are largely unknown. composing pig were becoming tolerable.
The carcasses were soft but still bloated by the
Carrion free from insects
tenth day. The various smells of decay were no
The decomposition and disintegration of pigs longer objectionable; however, they were still presfree from insects was very different from that of ent. This stage lasted approximately 8 days.
3. Flaccidity and dehydration.-The average
pigs exposed to insects. When arthropods were
excluded from the carcasses it was very difficult duration of this stage (Fig. 9) was 6 days. The
to divide decomposition of the carcass into welldefined stages. Five stages were recognized with
some certainty in all carcasses.
1. Fresh stage.-This stage (Fig. 2) began
when the pigs were taken from the freezer and
ended when the first signs of bloating were detected. No insect activity was observed except
for the occasional penetration of ants into the cage.
This stage lasted approximately one and onehalf days. It was noticed that the fresh stage of
carrion free from insects was always longer than
that of carrion open to insects. The author has
assumed that insects probably aid in the dissemination of bacteria.
2. Bloating and decomposition.-Carcasses were FIG. 9. Flaccidity and dehydration stage, three weeks
after placement in insect-proof cage.
beginning to show visible evidence of bloating by
the end of the second day (Fig. 8). Inflation of
the carcass proceeded rapidly. Bubbles of blood carcasses were beginning to lose their bloated
and other body fluids were forced from the mouth, appearance and their remaining fluids. As the
nose, and anus by the third day after placement gases and fluids escaped, the pigs became soft and
flabby. All carcasses had to be carried in a level
position. If a carcass were slightly tilted or inclined, semifluids would escape from the mouth.
Odors of this stage were almost identical to that
of fermenting fruit juices.
Deflation proceeded gradually. The belly was
the last area to deflate, probably due to pockets
of gas trapped in the loose skin of the abdomen.
By the thirteenth day, the pig carcass had become
'';S''sS'SD
;;.:.D~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~.
.................
.......
leatherlike, and all fluids had escaped by the end
of this stage. Colonies of fungi were formed on
the semisolid fluids within the cage.
4. Mummy stage.-Dehydration (Fig. 10) proceeded very slowly. The pig carcasses gradually
and flatter. Loss of fluids was very
FIG. 8. Bloating and decompositionstage, one week after became drier
retained this mummified appearance
Pigs
in
slight.
placement insect-proof cage.
. ... ... ., .

R........

...

.....

.... .

..........
......

.. ......

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Late Summer

1965

CARRION

STUDY

OF THE

BABY

599

PIG

UNCLASSIFIED
ORNL-DWG 63-4390
--

SC

___

Mummy stage, five weeks after placement in

insect-proof cage.

as long as 2 months. During this time there

was a gradual loss of moisture from the remaining
tissues. The numerous colonies of fungi which
had developed on the carcass gave the pig a
speckled or mottled appearance. In the latter
part of this stage the outline of the bones could
be seen, indicating that most of the tissues had
decomposed. The odors present ranged from a
stale or musty odor to that of dry skins. After a
rain the odors became somewhat more noticeable
but never strong and stinking.
5. Desiccation and disintegration.-The begin. ~~~~~~~~~~~~~~~~~~~~~~~~~~~Z
ning of this stage (Fig. 11) was extremely hard
to determine, but the rupture of skin and exposure
of tissue and bone were selected as its start. The
exposure of the skull was the next step. As the
carcass gradually shrank more bones were exposed. Very little moisture could be detected in
the remaining tissue. Body form was still well
defined after 3 months. The duration of this stage
is unknown.
Carrion tem~peratusre
In the temperature studies conducted on carrion
the temperature of the carrion was determined

::H

stage 100 days

FIG. 11. Desiccation and disintegration
after placement in insect-proof cage. Note the large cottony colony of fungi in the neck region

__

FRESH sBLOATED ACTIVEDECAY

3 ADVANCED
4DECAY

NOON

FIG. 10.

SOI
CTEMPERTUR

40
Z3 S

PIG TEMPERATURE

NOON

NOON
NOON
NOON
TIME AFTER PLACEMENT(days)

DRY

NOON

NOON

FIG. 12. Comparison of average pig carrion temperature with soil temperature during each stage of carrion
decomposition.

from the average of the three readings obtained

for each pig. Since air temperature for the observational period fluctuated greatly, soil temperature
was used in all comparisons. The temperature of
the carrion during the bloated stage was found
to be slightly higher than the soil temperature.
However, the active and advanced decay carrion
temperatures were considerably higher than the
soil temperature and even higher than the surrounding air temperature (Fig. 12). Heat from
the decomposing pigs in advanced decay could
actually be felt on the skin. The mean daily
temperatures for the pig carrion from August 14
to August 17, 1962 (bloated and decay periods)
was 28.70C, whereas the mean daily soil temperature for the same period was 26.10C. When animals reached the dry stage, animal temperature
and soil temperature were essentially the same.
Additional readings were made to verify this
finding.
The difference between carcass temperature and
soil temperature was probably due to the high
metabolic rates of the bacteria and dipterous larvae
present. On one occasion during advanced decay
a temperature of 37.70C was recorded in the carcass and air temperature outside was only 220C.
This aspect of increased temperature perhaps could
be used in estimating the age of a carcass-as
Megnin ( 1894) used insects- if consideration is
taken of external environmental factors.
Environmental temperature
The activities of insects were more influenced
by temperature than by any other environmental
factor. Decomposition and removal of carrion
was slower on cool, cloudy days. Calliphorid
adults and larvae appeared to be sluggish during
such days. Graham-Smith (1916) also reported
that flies are usually very inactive on cloudy days.
Fuller ( 1934) observed that high temperature and

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600

JERRY

Ecology, Vol. 46, No. 5

A. PAYNE

very low humidity caused more rapid desiccation

of the carrion, which made most of the food unavailable to maggots. This condition was never
seen in any of the pig carcasses studied. Instead,
high temperatures promoted intense insect activity
which resulted in rapid depletion of the softer
parts of the carcass. Environmental temperature
was most critical during the fresh and dry stages
of carrion. It may be noted at this point that
seasonal observations on carrion would yield other
aspects of the temperature relationship.
Moisture
Excessive moisture and extremely high temperature had a pronounced effect on the succession. The microseral stages were completed so
quickly that some insect groups did not appear or
failed to complete their larval development. In
many instances larval silphids and staphylinids
failed to complete their development because the
pig carrion was dry and void of the dipterous larvae which are their prey.
Cochliomyit and Calliphora larvae left pig carrion in which excess fluids had collected. The
skin was relatively intact and was collecting fluids
which normally would have seeped into the soil.
Some carrion fauna have a preference for moister
conditions. Histeridae, Silphidae, Vespidae, and
certain Lepidoptera were observed in abundance
on very soupy carrion. In contrast, Nitidulidae,
Mycetophagidae, and Dermestidae preferred the
'dried remains. Moisture content of a carcass may
be an indication of what insects are present and the
stage of decomposition. Graham-Smith (1916)
reported that the larvae of many species of flies
migrated in wet weather, even when the food
supply was abundant. Brannon (1934) stated
that maggots of the sheep blow fly were very sensitive to excess moisture.
Carcasses in the dry and remains stages had
very little or no insect activity. Sudden summer
rains caused a partial repetition of succession.
Histeridae, Staphylinidae, and some small Diptera
were attracted again to the wet remains. The
dermestids and nitidulids sought refuge beneath
the dried carrion scraps. The succession usually
returned to the former state within 2 days. These
short summer showers were detected when the
carrion was weighed because of the increase in
carrion weight.
Decay rates
A very important aspect of the summer carrion
study concerned the rate of removal of the two
types of pig carrion (open to insects and insectfree). Decay curves were constructed by plotting
against time the per cent of original animal weight

UNCLASSIFIED
ORNL-DWG 63-4392

,100

80

EXPERIMENT2A
EXPERIMENT4A

o400

20

TIME AFTER PLACEMENT(days)

FIG. 13. Decay curve showing the loss _ of weight of

pig carrion when exposed to insects during the summer
of 1962. Each experiment consisted of four pigs.
-J60_

'2

UNCLASSIFIED
ORNL-DWG 63-4391

----

a0.20

16=
~~~~EXPERIMENT

loo

14

EXPERIMENT36
-----------

--

~~~~80~

10

20
5
3
5 25 4
TIME AFTER PLACEMENT(days)

TM

- - --

AFEXPERIEMENT 66ys

FIG. 14. Decay curve showing the loss of weight of

pig carrion when free from insects during the summer of
1962. Each experiment consisted of four pigs.

remaining (Figs. 13 and 14). As shown in these

graphs the process of decomposition (carrion removal) and the resulting decay curve shapes were
mainly dependent on the presence of insects. A
protected carcass ( Fig. 14) underwent quite a
different type of decomposition from an unprotected carcass (Fig. 13). Following the first 4
days of exposure the weight of the pigs maintained
free of insects was considerably greater than the
pigs exposed to insects.
During the fresh- stage and the onset of the
bloated stage (first 2 days) the two curves were
very much alike. After this the two type of
carrion underwent their characteristic stages of
decomposition. Carrion free of insects decomposed and dried very slowly. The loss of weight
was gradual and thus gave a gently sloping curve.
Even after 100 days 20% of the original carrion
remained in the form of a mummified pig. Ninety
per cent of the carrion open to insects was removed
in 6 days.

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Late Summer

1965

CARRION

STUDY

OF THE

BABY

PIG

601

Araneida-accounted for 78% of the carrion

fauna.
Thirty-eight Coleoptera families were collected.
Two coleopterous families, Histeridae and Staphylinidae, contained 92 species or 42% of the total
Coleoptera collected. The members of these two
families were almost exclusively predaceous and
fed upon the dipterous larvae present. Three dipterous families out of the 27 present Sarcophagidae, Calliphoridae, and Muscidae-contained 43
species or 42% of the total Diptera collected.
Larvae (maggots) of these families were the only
dipteran larvae which fed upon the carrion media.
These 43 dipterous species played predominantly
scavenger roles and were primarily responsible
for the removal of carrion. The three Diptera and
two Coleoptera families, containing 135 species,
accounted for 26% of the carrion fauna. Furthermore, members of these five families were found
in abundance in most of the collections. Most of
the reliable indicators of the stage of decomposition are found among these families.
The order Hymenoptera was the third most
numerous order, containing 54 species. Three
families-Formicidae, Braconidae, and Ichneumonidae-out of the 16 families contained 21 species or 40% of the total hymenopteran species.
Most of the species of Hymenoptera were repreThe organisms concerned
sented by only a few individuals, except for some
A total of 522 species representing 3 phyla, 9 formicids and vespids. Most of the 34 species of
classes, 31 orders, 151 families, and 359 genera the fourth most numerous order, Araneida, were
were collected and identified from the five stages seldom present in numbers. However, a few speof pig carrion decomposition during the summers cies were present in moderate numbers during
of 1962 and 1963. Of this total 422 were insect active and advanced decay when insect activity
species representing 11 orders, 107 families, and was at a maximum.
283 genera.
Carrion fauna was found to be very diverse and
The organisms visiting the carcasses fall into quite variable. Many species were collected and/
five groups: those only scavenging on the carcasses or recorded for the first time for carrion. Four
(necrophagous species), those parasitic and pre- species are new to science and are being described
daceous on various arthropods and scavengers of by the appropriate specialists. A definite ecological
the carrion also (omnivorous species), those feed- succession occurred among the fauna of carrion.
ing on arthropods only (predators and parasites), The nature of the succession was determined by
those which used the carcass for shelter or con- the chemical and physical properties of the carrion,
cealment, and those whose presence is accounted type and rapidity of putrefaction, time of day,
for only by chance (accidental species). The and weather. Each stage of decomposition was
systematic list of all the species associated with characterized by a particular group of organisms,
the various stages of decomposition of the carrion, each of which occupied a particular niche. There
their food habits, and their approximated succes- was a gradual change in the number of individuals
sional distribution is too extended to be reproduced and species beginning with the flesh feeders and
here, but has been published separately (Payne ending with the skin eaters. The greatest number
and Crossley 1965). Copies of the report are of species inhabiting the carcass at a given time
available from the authors upon request.
occurred during the late decay stages (Table I).
Two orders of insects, Coleoptera and Diptera, Those species which occurred earlier in the succomprised 60%oof the total fauna collected from cession were predominantly dependent on the carcarrion. From this total of 522 species 217 were rion as a direct source of food. These insects
beetles and 108 were flies. Four orders of arthro- usually completed their feeding and/or developpods-Coleoptera, Diptera, Hymenoptera, and ment while the carrion was still moist and soft.
The data obtained from decay curves are applicable in biological control and medico-legal entomology. Previous workers have stated that x
species or x family of parasite or predator gave an
x per cent reduction in the dipterous larvae of
carrion. These theories could be checked by comparing the curves of a carcass seeded with dipterous larvae and protected from parasites and
predators with an exposed carcass under similar
conditions. Medico-legal advice is sometimes desired in estimating the time of death of human
bodies found in protected places in which the
system of calculating the time of death by insects
would be inapplicable. The decay curve of a protected body would be of some aid. The effects of
season and various physical factors on decay may
be explored through this technique.
Insects undoubtedly hasten liquefaction and disintegration by dissemination of bacteria, by the
digestive juices they secrete, and by the mechanical processes of tunneling and burrowing through
the carcasses (Fuller 1934). The author's observations are in agreement with the above. This
combination of actions plus necrophagous insects
and the environmental temperature accelerated the
rate of decomposition and removal of carrion.

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602

JERRY
TABLE I.

Ecology, Vol. 46, No. 5

A. PAYNE

Total number and per cent of species attracted in abundance to the various stages of decay

Stage of decomposition
Fresh .17
Bloated .48
Active decay .255
Advanced decay ...........,..
Dry .211

Total no. of
species attracted
to each stage
of decomposition

426

Very few of these species remained until the dry

stage. From the 522 species collected only 13
were collected in all five stages of decomposition
and 17 were collected in only one of the five stages
of decomposition. Those species which occurred
in the succession after the fresh and bloated stages
usually remained until the early part of the dry
stage. Many of these arthropods which occurred
latest were unable to complete a life cycle at the
carrion. Adults of Dermestidae, Trogidae, Nitidulidae, and Mycetophagidae appeared in numbers
late in the succession. Very few of their larvae
were able to complete development before the
remains stage.
Table I lists the total number of species attracted
in abundance to each stage of decomposition and
the per cent of those species also attracted in
abundance to another decay stage. This table is
essentially a summary of the similarities of the
attractive powers of the different stages. These
data show that there is some overlapping of odors
from protein and fat decomposition during the adjoining stages. This is particularly pronounced
during the active decay and advanced decay stages.
Of the 255 species present during active decay,
98%oof these occurred in advanced decay. Superficially this would seem to indicate an unwarranted
division of decomposition into active decay and
advanced decay stages; however, 171 additional
species were attracted in abundance to carrion in
advanced decay.
Additional research should be conducted on
odors of putrefaction from decomposing carcasses.
Odors undoubtedly attract the appropriate fauna
to the carrion. Many of the insects collected from
carrion have also been collected from flowers,
feces, garbage, and decaying fruits and fungi.
This would seem to be evidence indicating an overlap of odors. .No attempt has been made to construct a food web for the carrion-frequenting fauna.
The carrion microsere was found to be extremely
complex. This fauna which was borrowed from
the major community, including some necrophagous species, shares other niches in the parent community. The use of radioactive carcasses may

Per cent of species attracted

to another stage of decomposition:
Fresh

Bloated

Active
decay

Advanced
decay

Dry

100
33
6
3
0

94
100
19
10
<1

94
100
100
59
16

76
90
98
100
76

0
2
13
38
100

enable one to construct a reliable food web and

should certainly be of aid in describing energy
flow from the carrion microhabitat.
ACKNOWLEDGMENTS

The author is indebted to E. W. King, Clemson College, for his interest, invaluable suggestions, and assistance
during the planning and development of this research
and manuscript; to P. B. Dunaway, Oak Ridge National
Laboratory, for the editorial advice and assistance given
by him during the preparation of the manuscript; and to
Frances McAlister, Clemson College, for her aid in
the preparation of the specimens for identification. In
addition, I wish to express sincere appreciation to the
54 specialists who identified specimens; to Ben Oswald,
Allendale County, South Carolina, and D. L. Handlin,
Clemson College, for providing baby pigs for the research.
This investigation was supported in part by a National
Defense Graduate Fellowship; this aid is gratefully
acknowledged. Part of the work reported in this paper
was submitted in a thesis to the Graduate School of
Clemson College for the M.S. degree in entomology. I
wish to express gratitude to my graduate committee and
especially the chairman, J. K. Reed. The sponsorship
and support of the Department of Entomology and Zoology, Clemson College, is appreciated.
LITERATURE

CITED

Allee, W. C., A. E. Emerson, 0. Park, T. Park, and

K. P. Schmidt. 1949. Principles of animal ecology.
837 p.
W. B. Saunders Co., Philadelphia.
Brannon, C. H. 1934. Observations on the blow-fly
Lucilia sericatta Meig. J. Parasitol. 20: 190-194.
Fuller, M. E. 1934. The insect inhabitants of carrion,
a study in animal ecology.
Austral. Council Sci.
Indus. Res. Bull. 82: 5-62.
Graham-Smith, G. S. 1916. Observations on the habits
and parasites of common flies. Parasitol. 8: 440-546.
Howden, A. T. 1950. The succession of beetles on
carrion. M.S. Thesis, North Carolina State College,
Raleigh. 83 p.
Mdgnin, P. 1894. La Fauna des Cadavres. Application de L'entomologie a la medicine legale. Gauthier.
Paris: Villars et Fils. 214 p.
Payne, J. A. 1963. A summer carrion study of the
baby pig, Sus scrofa Linnaeus. M.S. Thesis, Clemson
College, Clemson, South Carolina. 123 p.
Playne, J. A. and D. A. Crossley, Jr. 1965. Animal
species associated with pig carrion. ORNL report
(In press).
Reed, H. B. 1958. A study of dog carcass communities
in Tennessee, with special reference to the insects.
Am. Midland Naturalist 59: 213-245.

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