Rewriting ecological succession history: did carrion ... · cited in Rennie 1810; Dureau de la Malle 1825; Hult 1885, 1887; Warming 1891) helped mark the birth of ecology. Accord-ing

REWRITING ECOLOGICAL SUCCESSION HISTORY: DID CARRIONECOLOGISTS GET THERE FIRST?

Jean-Philippe MichaudSerious Crimes Branch, Royal Canadian Mounted Police

Calgary, Alberta T2E 8A2 CanadaDepartement de biologie, Universite de MonctonMoncton, New Brunswick E1A 3E9 Canada

e-mail: [email protected]

Kenneth G. SchoenlyDepartment of Biological Sciences, California State University, Stanislaus

Turlock, California 95382 USA


Gaetan MoreauDepartement de biologie, Universite de MonctonMoncton, New Brunswick E1A 3E9 Canada


keywordssuccession, facilitation, carrion ecology, plant ecology, paradigm shift,

community assembly, decay stages, multiple independent discovery, forensicentomology, decomposition ecology

abstractEcological succession is arguably the most enduring contribution of plant ecologists and its origins

have never been contested. However, we show that French entomologist Pierre Megnin, while collab-orating with medical examiners in the late 1800s, advanced the first formal definition and testablemechanism of ecological succession. This discovery gave birth to the twin disciplines of carrion ecologyand forensic entomology. As a novel case of multiple independent discovery, we chronicle how thedisciplines of plant and carrion ecology (including forensic entomology) accumulated strikinglysimilar parallel histories and contributions. In the 1900s, the two groups diverged in methodology andpurpose, with carrion ecologists and forensic entomologists focusing mostly on case reports andobservational studies instead of hypothesis testing. Momentum is currently growing, however, todevelop the ecological framework of forensic entomology and advance carrion ecology theory. Research-

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ers are recognizing the potential of carcasses as subjects for testing not only succession mechanisms(without assuming space-for-time substitution), but also aggregation and coexistence models, diversity-ecosystem function relationships, and the dynamics of pulsed resources. By comparing the contribu-tions of plant and carrion ecologists, we hope to stimulate future crossover research that leads to ageneral theory of ecological succession.

Introduction

MULTIPLE independent discovery(Lamb and Easton 1984) has occurred

sporadically in science throughout its recenthistory. Some of these discoveries were simul-taneous or almost so, while others occurred inmutual isolation, sometimes many years apart(Merton 1961). In the ecological sciences, ex-amples include (but are not limited to) thetheory of evolution by natural selection (Dar-win 1858, 1859; Wallace 1859), the equilib-rium theory of island biogeography (Munro1948; MacArthur and Wilson 1963; Brownand Lomolino 1989), and allometric scalingof population variance with mean body size(Marquet et al. 2005; Cohen et al. 2012).Ecological succession, the change in speciescomposition in communities over time (asdefined by Cain et al. 2008), is arguably theoldest and most enduring concept in ecol-ogy (Cherrett 1989). Modern general ecol-ogy textbooks repeatedly identify Cowles(1899), Clements (1916, 1936), and Gleason(1917, 1926, 1939)—in various combina-tions—as succession’s earliest theorists (e.g.,Stiling 2002; Cain et al. 2008; Krebs 2009;Smith and Smith 2012; Molles 2013). Hence,the origin of ecological succession theory hasnever been questioned. However, here weshow that French veterinarian and entomol-ogist Pierre Megnin, while collaborating withmedical examiners to document the succes-sion of insects on exhumed and exposedhuman corpses (Megnin 1883, 1887, 1894),advanced the first formal definition and test-able mechanism of ecological succession.This discovery gave birth to carrion ecologyand its applied cousin, forensic entomology,which uses thermal development and succes-sional timetables of insects on corpses to es-timate time since death of the deceased incriminal investigations (Byrd and Castner2010).

The fields of plant and carrion ecologyoriginated and developed independently,

and given their disparity in subject matter,training, and institutional structures, weshow that these two groups were unaware ofeach other’s publications. Nevertheless, thesegroups accumulated strikingly similar paral-lel histories and contributions, which wealso chronicle below. One difference is,however, obvious. Breakthroughs in plantecology, notably the paradigm shift fromthe Clementsian school (Clements 1916,1936) to the Gleasonian school (Gleason1917, 1926, 1927, 1939) and the introduc-tion of testable models and mechanisms(Horn 1975; Connell and Slatyer 1977; Hillet al. 2004; Solow and Smith 2006), shapedthe theoretical development of succession.By contrast, carrion ecology and forensicentomology diverged from basic ecologicalthinking about succession due to their em-phases on insect taxonomy and observa-tional studies throughout the 20th century(Michaud et al. 2012). Mechanisms devel-oped for plant and marine communities(Connell and Slatyer 1977) carried over tocarrion succession without empirical support(Connell and Slatyer 1977; Schoenly andReid 1987; Smith and Baco 2003) and, as aresult, little is known about the mechanismsthat drive succession on carrion as well asother ephemeral and patchy resources (e.g.,dung, leaf litter, fallen fruits, rotting logs).

In this paper, we chronicle the indepen-dent discovery and formalization of plantand carrion-arthropod succession, and ex-amine the paradigm shifts that redirectedplant ecology and the twin disciplines of fo-rensic entomology and carrion ecology intowhat they are today. Such comparisons, wehope, will stimulate future crossover re-search that leads to a general theory of eco-logical succession.

Paradigms of Plant SuccessionEarly documentation of plant communi-

ties by European naturalists (De Luc 1806 as

46 Volume 90THE QUARTERLY REVIEW OF BIOLOGY


cited in Rennie 1810; Dureau de la Malle1825; Hult 1885, 1887; Warming 1891)helped mark the birth of ecology. Accord-ing to Clements (1916), De Luc (1806; ascited in Rennie 1810) was the first naturalistto coin the word “succession,” Hult (1885,1887) conducted the first systematic study ofvegetation development and established theconcept of a climax assemblage, and Warm-ing (1891) was the first to give a consistentaccount of succession on sand dunes. EarlyEuropean botanists also provided the neces-sary observations that plant ecologists wouldlater build upon to formalize a conceptualframework of plant succession.

One of the first naturalists to apply theterm “succession” and offer a functional ex-planation was American naturalist HenryDavid Thoreau (1860). Through his own ob-servations, Thoreau also refuted old think-ing that seeds spontaneously generate or laydormant for centuries and showed insteadthat they become dispersed by wind and an-imals. Thoreau described a particular caseinvolving pine trees and oaks, and how everytime a pine tree was cut down an oak treesprung up, and vice versa. When pines werecut down, conditions became favorable forthe oaks and the latter grew larger. After afew years, the area became unfavorable forthe oaks and, in turn, pines were again al-lowed to grow. Thoreau called this trend“forest succession.” Likewise, Darwin (1859)proposed that cleared forests eventually sup-ported the same species as surrounding forestsand, later, Douglas (1875, 1889) chronicledthe fate of pioneer species in burnedforests.

Despite the early accounts of Thoreau,Darwin, and Douglas, a decade passed be-fore succession was formalized as an eco-logical concept in North America. Cowles(1899) described the coastal region of LakeMichigan, its various dune formations, andvegetation, including the transition frombeach to mesophytic forest. Cowles also usedthe term “climax” to describe the last, mostmature stage of vegetation within a geo-graphic area. Subsequently, Cowles (1901)defined the mesophytic forest as a climaxassemblage, but this time for inland andcoastal environments. Cowles described the

order of succession and how plant commu-nities replaced each other when conditionschanged, a phenomenon driven mostly byclimate, and he assumed that changes inspace mirrored those in time, known todayas space-for-time substitution (Pickett 1989).Cowles wrote:

The various plant societies pass in a seriesof successive types from their original con-dition to the mesophytic forest, which maybe regarded as the climax or culminatingtype . . . stages may be slow or rapid . . . stagesmay be direct or tortuous (Cowles 1901:80-81).

Thus, Cowles (1899, 1901) was the firstecologist to define succession as a sequentialand directional process ending in a climaxcommunity. Tansley later wrote:

It is to Henry Chandler Cowles that we owe,not indeed the first recognition or even thefirst study of succession, but certainly the firstthorough working out of a strikingly com-plete and beautiful successional series . . .Cowles did far more than any one else tocreate and to increase our knowledge ofsuccession and deduce its general laws(Tansley 1935:284).

Research by pioneering botanists such asHult (1885, 1887), Warming (1891), andCowles (1899, 1901) helped to usher in ecol-ogy as a distinct discipline. By the early1900s, Frederic E. Clements (1916, 1936)had developed his monoclimax theory ofsuccession, which became ecology’s first par-adigm (Simberloff 1980). The premise ofClements’ work, based loosely on Cowles’ideas, was that succession behaved like anorganism, developing from different unsta-ble stages called seres, to a final stable serecalled a climax, all under control of the re-gional climate. In his youth, Clements saw aboom-and-bust cycle of agricultural expan-sion play out on the Midwestern prairies bypioneer homesteaders whose poor farmingand grazing practices brought drought andfamine (Tobey 1981). Clements and his fel-low grassland ecologists, who included hismentor Charles E. Bessey and Roscoe Poundat the University of Nebraska, championed adynamic version of plant ecology in the early1900s that depended on quadrats (including

March 2015 47REWRITING ECOLOGICAL SUCCESSION HISTORY


permanent and denuded versions), experi-mental and graphical methods, and quanti-tative approaches (Worster 1994; Kingsland2005). Using the quadrat method, Poundand Clements ([1898] 1977) found that veg-etation along the slope of the Great Plainsvaried more than expected, “even though tothe eye there was no change” (Tobey 1981:71). By comparing vegetation in roadwayswith those in right-of-way enclosures (fencedoff by the railroad), Clements showed whatthe prairie landscape, when left undisturbed,looked like (Kingsland 2005). These percep-tions and observations developed into theClementsian school that emphasized theclosed-ended, sequential, directional, andpredictable nature of succession and identi-fied facilitation as its chief mechanism (i.e.,pioneer colonizers modify their environ-ment, making it unsuitable for themselvesbut suitable to others). Clementsian succes-sion, which was considered dogma in thefirst half of the 20th century, neverthelessoffered an experimental approach for study-ing succession (Tobey 1981; Kingsland 2005)and stimulated a groundswell of researchthat still finds applications today (Pickett etal. 2009).

The second view, based on field studies ofHenry Gleason (1917, 1926, 1927, 1939) andLeonty Ramensky (1924), shifted attentionaway from the superorganism view to onethat emphasized the community’s depen-dence on environmental gradients, life his-tories of individual species, stochastic events,and variable arrival times of colonizers. Theindividualistic concepts of Gleason and Ra-mensky were deeply rooted in extensive flo-ristic studies they had conducted in theirhome countries of America and Russia, re-spectively. Like Clements, Gleason employedquadrats and they were among the earliestecologists to use them to study the distribu-tion and frequency of individual terrestrialplants (McIntosh 1985). In his landmark1926 paper, Gleason concluded:

it may be said that every species of plant is alaw unto itself, the distribution of which inspace depends on its individual peculiari-ties of migration and environmental re-quirements (Gleason 1926:26).

In opposition to Clements, Gleason arguedfor a more flexible view of succession andrejected Clements’ notion of irreversibly di-rected seres and the monoclimax. Gleason’spapers, however, had little impact on hiscontemporaries, and were largely ignored.Even before Gleason published his last paperon succession in 1939, he had decided toleave ecology to pursue plant taxonomy forwhich he had a long and distinguished ca-reer (McIntosh 1975). Although the Gleaso-nian view was overlooked for decades, by the1950s the contributions of John T. Curtis(i.e., ordination) and Robert H. Whittaker(i.e., gradient analysis) had persuaded manyplant ecologists that Gleason’s individualisticconcept was valid (Gurevitch et al. 2006). By1949, the first American textbook on animalecology (Allee et al. 1949) had at least citedGleason’s papers on the individualistic con-cept (McIntosh 1975); however, it took an-other decade for Gleason’s succession modelto carry over into animal ecology (McIntosh1995).

Today, modern ecology textbooks con-tinue to portray the Clementsian and Glea-sonian schools as a dichotomy from whichfew ecologists have diverged; the few that didincluded Cooper (1926), Tansley (1935),Whittaker (1953), Horn (1975), and Pickett(1976). These slightly divergent approaches,however, never quite caught on. McIntosh(1975) provocatively asked to what extentthe power of place, namely, the Nebraskagrassland for Clements and the prairie-forestborder of Illinois for Gleason, informedtheir views on plant succession that led themto reach different conclusions. Likewise, Ra-mensky worked in meadows near the OskilRiver region of Voronezh Province in Russia,arrived at similar conclusions as Gleason,and was also dismissed by his peers (McIntosh1983, 1985). Today, most plant ecologiststake an intermediate position between theClements-Gleason (Ramensky) dichotomy(Gurevitch et al. 2006) and acknowledgethat the methods used to sample vegetationalso affects the nature of the plant associa-tion (Barbour et al. 1987). Plant ecologistsstill disagree, however, on the relative impor-tance of biotic and abiotic factors and therole of stochastic events in shaping plant



community structure (Barbour et al. 1987;Gurevitch et al. 2006).

Although the 1960s saw the introductionof mathematical models for plant succession(McIntosh 1999), testable hypotheses of dif-ferent successional mechanisms did not ap-pear until Connell and Slatyer (1977). Intheir influential paper, Connell and Slatyer(1977) described three mechanisms and of-fered examples for each from the literatureand experimental criteria required for hy-pothesis testing. Briefly, in the facilitationmodel, only pioneer species are able to col-onize. Those species modify their environ-ment, eventually making it more suitable forthe establishment of later-succession speciesand less suitable for other early colonists. Intime, pioneer species are eliminated. In thetolerance model, any species has the poten-tial to colonize. Those species modify theenvironment, eventually making it less suit-able for early colonists but the ability of later-succession species to colonize is not affected.In time, pioneer species are eliminated. Inthe inhibition model, any species has thepotential to colonize. Those species modifythe environment, eventually making it lesssuitable for early colonists, but also inhibit-ing the ability of later-succession species tocolonize. According to Connell and Slatyer(1977), studies on newly exposed substratesand marine benthic environments providedevidence for facilitation, whereas studies onterrestrial plants and marine organisms pro-vided evidence for the inhibition model. Nostudy was found to support the tolerancemodel. Just as the views of Clements andGleason stimulated much debate 50 yearsearlier, the mechanisms of succession pro-posed by Connell and Slatyer (1977) under-went rapid scrutiny and refinement (e.g.,Tilman 1985; Pickett et al. 1987; Farrell1991). These developments initiated the sec-ond paradigm shift in plant succession,which continues today (e.g., Maggi et al.2011; Marleau et al. 2011; Prach and Walker2011).

What Cowles and his European predeces-sors and colleagues did was document thefirst successional series, apply the word “suc-cession,” and provide a general framework ofthe mechanism involved. Coincidentally, a

veterinarian-entomologist and his medicalexaminer colleagues in France were studyingthe same phenomenon, but in a more ma-cabre context.

Paradigms of Forensic Entomologyand Carrion Ecology

Forensic (or medicolegal) entomologyemerged out of the much older and largerdiscipline of forensic medicine whose ori-gins date back to Egypt nearly 3,000 yearsago (Smith 1951). According to Greenbergand Kunich (2002), the earliest recordeduse of insects in a legal case dates back to10th century China in which a murder in-vestigation was recorded, set between 907and 960 ad (Cheng 1890, cited by Green-berg and Kunich 2002). A coroner had in-terviewed a distraught woman who said herhusband was killed by fire, but the coronerfound aggregations of flies on the victim’shead. At autopsy, investigators found an em-bedded projection in the wound. Whenconfronted with the evidence, the womanreportedly confessed that she and an accom-plice had murdered her husband (Cheng1890). Another first for China was the pub-lication of the earliest training manual fordeath scene investigators, Hsi Yuan Chi Lu(“The Washing Away of Wrongs”), writtenby Sung Tz’u in the 13th century (translatedinto English by Giles 1924 and McKnightin Sung 1981). Although Sung’s medicalknowledge was considerable, he was trainednot as a physician, but as a jurist. Neverthe-less, his “Instructions to Coroners” (Giles1924) was unrivaled in detail and coveragefor his day (Gwei-Djen and Needham 1988)and contained many observations, methods,tests, and collections of selected cases, in-cluding one case involving insects. A manhad been found dead by the roadside withnumerous head wounds that resembledthose made by a sickle. After the coronerordered 70 of the local villagers to assemblewith their sickles on the ground, he noticedflies aggregating on only one, indicatingthat it had residual traces of blood and tis-sue. When confronted with the evidence,the villager reportedly confessed (Giles 1924:77; Sung 1981:69-70). Elsewhere in the man-ual, Sung revealed his knowledge of fly life



cycles, their appearance in decomposingbodies in different seasons of the year, andobservations on their infestation in the ninenatural orifices and wounds of the body(Giles 1924:68-69; Sung 1981:86–87).

In Europe, the coroner system (i.e.,coroners being responsible officials of theCrown) was established in the late 12th cen-tury, whereas expert testimony in death in-vestigations was formalized in the 13thcentury (Sung 1981). When English colo-nists came to America, they brought theircoroner system with them (Hanzlick 2007).Coroners were often elected officials with nomedical training. The earliest American leg-islation to require elected coroners to havemedical training did not occur until the1870s, which eventually led to a gradual shifttoward the medical examiner system (Han-zlick and Combs 1998). Currently, 31% ofthe counties in the U.S. are served by medi-cal examiners (Hanzlick 2007).

One of the earliest known documenta-tions of the role of insects in decompositionoriginated in Europe and was used to refutespontaneous generation when Italian physi-cian Francesco Redi (1668) experimentallydemonstrated, using meat, small carcasses,and proper controls, that maggots comefrom adult flies. Redi also documented thesuccessive emergence from the substrate ofdifferent types of adult flies. He did not usethe term “species” as his work preceded Lin-naeus (1767), but his descriptions matchedthose of Calliphoridae (two or three spe-cies), Sarcophagidae and/or Muscidae, andprobably Sepsidae. However, Redi did notmonitor visitation or oviposition behavior ofdifferent fly species, and as such did not al-lude to any successional process. From hisfield observations and taxonomic treatmentof carrion-breeding flies, Linnaeus wrote acentury later:

Three flies consume the corpse of a horseas quickly as a lion did (Linnaeus 1767:990).

Over the succeeding decades, Europeanphysicians, while conducting autopsies, alsoencountered (but largely ignored) carrioninsects. Although Orfila and Lesueur (1831)suspected that insects could play a role in

legal medicine, they did not include a discus-sion of insect succession or how insects couldbe used in such investigations. Bergeret(1855) used insects to solve a homicide in-volving a mummified infant found in anapartment’s chimney in March 1850. Theautopsy revealed the presence of pupae andmaggots of the flesh fly Musca carnaria (nowSarcophaga carnaria; Diptera: Sarcophagidae)and a moth (named “Papillon des mites”;most likely Lepidoptera: Tineidae), an earlyand late colonizer, respectively. Bergeretused his limited knowledge of entomology asa tool to estimate time of death and con-cluded that investigators should focus theircase on previous tenants of the apartment.Although Bergeret (1855) misinterpretedthe life cycles of some of the insects in thiscase (Goff 2000; Benecke 2008), it was thefirst time entomology was used to estimatetime of death and also the first documentedcase in which succession was described. Theterm “succession,” however, was never used.Three decades later, the German physicianHermann Reinhard (1882), conducted thefirst taxonomic survey of the fauna of ex-humed corpses, identifying seven arthropodtaxa (i.e., coffin flies, braconid wasps, latrineflies, millipedes, rove beetles (two species),and graveyard beetles).

The first biologist to provide a compre-hensive account of succession, to make useof the term, and to hypothesize on its under-lying mechanisms was French army veterinar-ian and entomologist Pierre Megnin (1883,1887, 1894) who collaborated with PaulBrouardel, a French medical examiner(Brouardel 1879) who also worked on tuber-culosis and vaccination (Benecke 2008). Me-gnin, who started his collaboration withBrouardel in 1878 by identifying mites froma mummified body (Benecke 2008), recog-nized the predictability of carrion-arthropodsuccession and its forensic potential. Whilerealizing the enormous challenge posed bytime-since-death estimation, Megnin noted:

This problem seemed insoluble. However,Brouardel suggested to me that perhaps wecould use as its solution the remnants thatthe numerous legions of insects, succeed-ing each other with remarkable regularity,



leave behind on a cadaver (translated byJ.-P. Michaud; Megnin 1883:480).

Megnin (1883) also described three of hiscases in which his estimates of time sincedeath were corroborated by suspect confes-sions. Megnin later noted that:

The oviposition by insects does not occurat the same time for all; they each chose adegree of decomposition . . . that momentis so constant for each species and the suc-cession of their apparition is so regular thatwe can state the age of the cadaver (trans-lated by J.-P. Michaud; Megnin 1887:948).

In his classic text, Megnin (1894) summa-rized his case histories dating back to 1879and expanded on his time-since-death meth-odology:

For a long time a fact, which we were thefirst to observe, marked us: the insects thatcolonize cadavers, or death workers, arrivein succession and always in the same order.We counted a dozen periods betweendeath and the complete destruction of thecadaver, and in each of those always appearthe same insects . . . putrefaction occurs ina series of fermentations, and the productof each is better suited to a group of deathworkers than the other, which explainstheir regular succession (translated by J.-P.Michaud; Megnin 1894:13).

Megnin was referring to the action of bac-teria that produced different odorous gasesthat became attractive to certain insects. Me-gnin (1894) also described eight “squads” ofarthropods (insects, mites) that succeededeach other at different times during decom-position and within each squad a distinctarthropod assemblage formed (Figure 1). Inaddition, Megnin (1894) acknowledged thatthe arthropods in each squad could changedepending on site and season. In the secondhalf of his book, Megnin (1894) described 19case reports (spanning 30 years), includinghis own cases (some with Brouardel) be-tween 1879 and 1890, for which he offeredexpert testimony. Megnin also briefly collab-orated with another French physician, G. P.Yovanovitch, of the Faculty of Medicine inParis, who published a thesis based on Me-gnin’s succession tables (Yovanovitch 1888).However, without consulting Megnin, Yovano-vitch added a table at the end of his thesis

that listed insect occurrences spanning fiveyears when instead Megnin’s observations in-cluded at most 24 months. Megnin (1889)pointed out that Yovanovitch had mistaken“periods” for “years” and asked for the tableto be retracted from the thesis. Another phy-sician inspired by Megnin (1894) was EduardRitter von Niezabitowski, a medical exam-iner at the Medico-Legal Institute at KrakowUniversity. Niezabitowski (1902) conducteda two-year observational study of arthropodsuccession using stillborn human remainsand carrion from several mammal species(i.e., cat, fox, rat, mole, and calf) deployed inand around the institute’s grounds and innearby fields and forests. He collected andidentified carrion-associated species belong-ing to several fly and beetle families and ag-gregated his data in a succession table thatspanned 14 days of observations. Niezabi-towski observed a faster rate of soft-tissue de-cay during summer than fall and winter,negligible preference by carrion insects forhuman remains over (other) animal re-mains, and habitat preferences of certain in-sects for human settlements, fields, andforests. Based on these seasonal and site dif-ferences, Niezabitowski (1902) warned thatMegnin’s eight-squad classification systemwas neither regular nor universal in its chro-nology and concluded that his theory, whichwas based mostly on concealed remainsfound inside closed rooms, had limited fo-rensic value for outdoor situations.

In North America, Wyatt Johnston andGeorges Villeneuve, two Canadian physi-cians inspired by Megnin, applied their ob-servations of insect succession on corpsesfrom several of their cases to estimate time ofdeath (Johnston and Villeneuve 1897), butcautioned against applying Megnin’s rules toother countries and climates. The authorsconcurred with Megnin (1894) as to the suc-cessional sequence and the rules governingit. American physician Murray G. Motter,working as a volunteer for the U.S. Bureau ofAnimal Industry (now the U.S. AgriculturalResearch Service), also tested the applicabil-ity of Megnin’s squads in a study of 150 ex-humed corpses in the Washington, DC, area(Motter 1898). His results included detailedannotations on corpse-associated arthropods



Figure 1. Fauna of Dead Bodies Exposed to the AirMegnin’s (1894) eight “squads” reflecting his view that distinct arthropod faunas succeed one another on a

human corpse at different times in a deterministic order (Megnin 1894:24–95). Megnin’s succession-basedthinking preceded the parallel theories of Clements (1916) and Gleason (1917) by two decades. Figurereprinted from Johnston and Villeneuve (1897).



as well as tabulated data on the soil type,grave depth, and moisture content associ-ated with each exhumed corpse. He chal-lenged Megnin’s view that squads replaceeach other in an orderly sequence at precisemoments throughout decomposition andcautioned against making generalizations.

Megnin and his colleagues essentially re-produced what Cowles’ predecessors andcolleagues did: they observed and describedsuccessional seres, coined “succession,” andprovided a general framework of the mech-anism involved. Both groups originated inEurope in the late 1800s. By the turn of thecentury, European scientists had introducedsuccession concepts to North America wherehigh importance was assigned to seres (orsquads) and to the role of climate in shapingsuccessional outcomes.

Despite these promising beginnings, sci-entific progress and popularity in forensicentomology languished in the first half ofthe 20th century, except when a high-profilemurder case that involved insects surfaced(Goff 2000; Benecke 2008). Over the sametime period and for the rest of the century,carrion ecology remained mired in a descrip-tive era, notable for its many observationalstudies that exposed animal carcasses to dif-ferent seasons and environments (e.g., Mor-ley 1907; Jaques 1915; Illingworth 1926;Fuller 1934; Bornemissza 1957; Reed 1958;Payne 1965; Nabaglo 1973; Johnson 1975;McKinnerney 1978; Abell et al. 1982; Earlyand Goff 1986; Tantawi et al. 1996). Al-though these (and many other) reports pro-vided detailed species lists, graphs, and tablesof succession, and descriptions of decompo-sition, no mechanisms were proposed for thesuccessional patterns observed.

One study in the 1960s by Jerry A. Payne, agraduate student at Clemson University,stands out for its originality and impact. First,Payne (1965) used cages with different meshsizes to provide open and closed access toinsects to study day-to-day changes in carcassdecomposition, a comparison that previousresearchers had not subjected to a tandemfield test; Fuller (1934) studied insect-protected carrion in an insectary. Paynefound that carcasses protected from insectsmummified, keeping their integrity for

months, whereas, carcasses exposed to in-sects lost 90% of their starting weight in justsix days. This result showed that carrion de-composition, based on weight loss measure-ments, accelerated in the presence of insects.Second, after trying carrion of different sizesand from different vertebrate species (i.e.,amphibians, mammals, and birds), Payne(1965) settled on domesticated pigs becausehe knew when they died and could acquirethem in large numbers of uniform sizeand age. He also found that their rela-tively hairless skin and lack of feathersmade insect sampling easier. Third,Payne (1965) published his study, not inan entomology journal, but in an ecologyjournal, which guaranteed a wider audi-ence. Since this study, the domestic pighas become the model corpse for carrionresearch (Catts and Goff 1992; Goff1993). Payne went on to publish severalother papers from his groundbreakingwork, including reports of arthropodsfrom buried and submerged carcasses(Payne et al. 1968; Payne and King 1972).

Beginning in the 1940s, several forensicpractitioners, including Marcel Leclercq,Pekka Nuorteva, Bernard Greenberg, andM. Lee Goff, began to publish their casereports that identified promising insect taxafor estimating the postmortem interval indeath investigations (Leclercq and Quinet1949; Nuorteva et al. 1967; Greenberg 1985;Goff and Odom 1987; Goff et al. 1988).These forensic developments gave renewedpurpose to carrion research, including thecreation (in 1980) of the first outdoor labo-ratory for human decomposition research(Shirley et al. 2011), but no study had testedecological mechanisms for the successionpatterns observed. Over the next 75-plusyears, however, carrion would become thefocus or model for investigating other eco-logical concepts and theories, such as detritalfood webs (Reed 1958; Cornaby 1974;McKinnerney 1978; Schoenly and Cohen1991), successional dynamics (Beaver 1977;Schoenly and Reid 1987; Boulton and Lake1988; Moura et al. 2005), energetics of an-imal decomposition (Putnam 1978a,b),spatial dynamics (Kneidel 1985; Hanski1987; Ives 1991; Fiene et al. 2014), re-



source pulses (Yang 2006), nutrient cy-cling (Carter et al. 2007; Parmenter andMacMahon 2009), and landscape hetero-geneity (Barton et al. 2013).

It was also during the 20th century that thestage-based paradigm emerged in carrionecology and forensic entomology. Succes-sional timetables, which displayed the namesand occurrences of different insect speciesand their life stages over time, included de-cay stages that were named according to ob-served physical and chemical changes in thecarcass. In these early ecological studies,stage descriptions varied in both numberand duration. For example, Fuller (1934)described three stages, Reed (1958) de-scribed four, Bornemissza (1957) describedfive, and Payne (1965) described six. Onewidely held belief was that the onset of eachstage was marked by abrupt changes in insectcomposition (Schoenly and Reid 1987), sim-ilar to Megnin’s (1894) notion of “squads”and Clements’ (1916) “seres.” For example,Fuller wrote:

It has become obvious, as Megnin [1894]pointed out, that each stage of decomposi-tion is characterized by a particular groupof insects, but the process of decomposi-tion itself is largely dependent on the pres-ence of the insects (Fuller 1934:24).

Some carrion researchers even used theterms “microsere” and “microseral stages”from plant succession studies to documentdecomposition progress (e.g., Reed 1958;Johnson 1975). The stage-based paradigmwas first challenged by Schoenly and Reid(1987) who demonstrated that succession in11 published studies (largely) followed acontinuum of gradual changes, verifying theexistence and timing of authors’ decay stagesin only a minority of cases. Those conclu-sions were later corroborated by Boultonand Lake (1988) and Moura et al. (2005).Despite these findings, and a reminder byPeters (1991) that decay stages represent ty-pological thinking, their use has spread inthe forensic literature (i.e., entomology, an-thropology, taphonomy). Practitioners haveused them as “convenient descriptors” for sum-marizing postmortem changes (e.g., Mann etal. 1990; Anderson and VanLaerhoven

1996; Tibbett and Carter 2009) or as “refer-ence points” for educating judges and juriesin the courtroom (Goff 2000). Moreover,just like the individualistic and continuumviews for plant communities championed byGleason and Ramensky, the richness, abun-dance, and distribution of chemical com-pounds emanating from a decomposingcarcass interact in complicated ways, are de-pendent on the physical environment, andrarely coincide with established decay stages,yielding limited use as indicators of decom-position (Vass et al. 1992; Vass 2012). Al-though some authors who have used decaystages have acknowledged their artificiality,using them still evokes a stepwise (and nec-essarily abrupt) view of carcass decay thatmisinforms the more continuous process.The widespread adoption and uncritical ac-ceptance of decay stages in carrion researchhas unfortunately diverted attention fromempirical testing of ecological mechanismsand models.

The descriptive era brought increasedecological attention to carrion (e.g., Eltonand Miller 1954) but did little to advanceunderstanding of temporal dynamics. Foren-sic entomology and carrion ecology continueprimarily as descriptive disciplines (Michaudet al. 2012), although a shift has begun to-ward a more hypothesis-driven framework(see below).

Connections Between Plant andCarrion Succession Theory

multiple independent discoveriesMultiple independent discoveries, accord-

ing to Lamb and Easton (1984), have oc-curred in every branch of science andinvolve researchers working in different lab-oratories and countries who were unawareof each other’s contributions. In addition,multiple discoveries are often dependent oncommon precursors, such as the theory ofevolution by natural selection in which Dar-win and Wallace were inspired by the eco-nomic theories of Thomas Malthus (Lamband Easton 1984). In the case of ecologicalsuccession, we show that carrion successiontheorists (i.e., medical examiners and foren-sic entomologists) of the late 1800s (i.e.,



Megnin, Yovanovitch, Johnston, Villeneuve,Motter, Niezabitowski) preceded plant suc-cession theorists (i.e., Cowles, Clements,Gleason, Ramensky) by two decades in for-malizing and testing this concept. Inspec-tion of the footnotes and bibliographies ofthe papers on succession by Cowles and col-leagues do not include the papers andbooks of Megnin and colleagues. Moreover,the papers from Cowles and colleagues re-ferred only twice to carrion-related termi-nology or succession in carrion. In oneinstance, Cowles used “corpses” to describeonce buried and resurfaced pine trees inretreating dunes (Cowles 1899:298). In thesecond, Clements linked “cadavers” withseres when describing examples of “minia-ture successions that run their short butsomewhat complex course within the con-trol of a major community” (Clements 1936:280), but provided no citation with thisdescription. Despite carrion and plant ecol-ogists having different historical roots (i.e.,forensic medicine and plant geography,respectively), they did depend on com-mon precursors that could have providedbuilding blocks for developing parallelsuccession concepts. For example, bothgroups cited studies that refuted sponta-neous generation, namely, Redi (1668)by carrion ecologists and Thoreau (1860)by plant ecologists. Also, both groups de-pended on the binomial classification sys-tem of Linnaeus (and the work of othersystematists) and benefited from the emer-gence of specialized subdisciplines withinbotany and zoology (Farber 1982) to de-scribe temporal and spatial changes in spe-cies composition. Unlike Mendel’s paper onparticulate inheritance that went unnoticedfor 35 years until it was rediscovered in 1900,we found no evidence that the papers andbooks of Megnin and colleagues were redis-covered (i.e., cited) by plant ecologists gen-erations later. This result is not surprisinggiven a persistent divide that has existed fordecades between plant and animal ecologists(McIntosh 1985).

Among the first plant ecologists to drawattention to animal-driven succession wasWhittaker when he wrote:

The most effective demonstrations of themanner in which populations succeed oneanother are in such short-range, small-scalesuccessions as those of infusions . . ., car-rion . . ., rotting logs and stumps . . ., dung. . ., etc. (Whittaker 1953:43).

At the time, carcasses were already an over-looked ecological unit (Allee et al. 1949; El-ton and Miller 1954) and for the most partwere ignored by plant ecologists. Similarly,post-1950s carrion researchers, while intro-ducing or reviewing succession, rarely in-cluded the contributions of Cowles andcolleagues (but see Schoenly and Reid 1987;VanLaerhoven 2010; Villet 2011). But per-haps most tellingly is that carrion succes-sion’s pioneers went uncited by prominentecology and environmental historians suchas Tobey (1981), Egerton (1983, 1985, 2008,2013, 2014), McIntosh (1985), Worster (1994),and Kingsland (2005). Likewise, medical his-torians did not cite the contributions of Me-gnin and colleagues among the pioneers offorensic medicine and death investigation inEurope and North America (e.g., Smith1951; Fisher and Platt 1993; Clark and Craw-ford 1994; Jentzen 2009). Consequently, al-though common precursors likely contributedto parallel thinking on ecological successionby carrion and plant ecologists, we found noevidence that either group was aware of theother’s contributions, at least until the mid-1900s.

Despite having common precursors, wehypothesize that different academic culturesand institutional structures kept carrion andplant ecologists apart. Up to the mid-1700s,scientists (i.e., natural philosophers) couldconceptualize grand syntheses of knowledgeabout the entire world, particularly if theywere ambitious, disciplined, and well placed(Farber 1982). This was especially true ofnaturalist-physicians, such as Linnaeus,whose broad training in the natural andmedical sciences (Blunt 2001) allowed himto investigate living systems across taxonomicand ecological boundaries. By the 19th cen-tury, the volume of information (includingcollected specimens) had exploded, favoringthe proliferation of natural history museumsand outlets for publishing (Farber 1982). Inthis era, “ecology,” as coined by Haeckel in



1866, had progressed to become a fusion ofnatural history and physiology (Farber 1982;McIntosh 1985) and, together with Darwin’stheory of evolution in 1859, should haveforged robust and lasting collaborations be-tween carrion and plant ecologists. But bythe turn of the 20th century, when carrionand plant ecologists were investigatingsuccession, the acceleration of scientific in-formation led to specialization and compart-mentalization of professions and institutions(Smith 1951; Farber 1982; McIntosh 1985).In North America, the birthplaces for ecol-ogy developed around botany programs,such as the Carnegie Institution of Washing-ton’s Desert Botanical Laboratory and theNew York Botanical Garden that pursuedmostly plant taxonomy, genetics, and eco-physiology (Kingsland 2005), land-grant uni-versities in Nebraska, Iowa, and Kansas(among others) that trained generations ofgrassland ecologists (Tobey 1981), and pri-vate universities such as the University of Chi-cago that trained both plant and animalecologists (McIntosh 1985). Consequently,in the early 1900s, American ecologists mostlysaw themselves as botanists and zoologists(Kingsland 2005) and rejected attempts bytheir leaders to embrace a broader researchagenda (Huntington 1920; Moore 1920; Cle-ments 1935) that included human-centereddisciplines (e.g., public health and urbanecology; Kingsland 2005). Following thistrend, the journal Ecology became more nar-rowly focused on botanical topics through the1920s (Kingland 2005). Over the same timeperiod, but independently of these develop-ments, the emergence of forensic pathology,as a medical specialty, into death investiga-tion had begun in America in the late 1800s(Fisher and Platt 1993). But even before thistime, the coroner system, made up of electedpersons who typically had no medical train-ing to investigate untimely deaths, was legis-lated into American colonial governments asearly as 1777 (Hanzlick 2007). By the early1900s, the modern medical examiner systemhad been established, and a trend to replaceuntrained coroners with physician medicalexaminers (expertly trained to performdeath investigations and autopsies) had be-gun (Hanzlick and Combs 1998). However,

conflicts continue today between medicalexaminers and coroners, and with politi-cians and law enforcement, resulting in apatchwork of death investigation systemsat state and local levels (Hanzlick 2007;Jentzen 2009). Consequently, as a resultof specialization and compartmentalization,newly established American institutions andcurricula in ecology and medicine did muchto weaken the potential for interdisciplinarycollaboration, not just between plant andcarrion ecologists, but between plant andanimal ecologists. As Lamb and Easton(1984) have observed, most scientists donot pursue interests or advance theoriesbeyond their cultural boundaries, but in-stead adopt the values of the society ofwhich they are part.

Finally, we hypothesize that carrion andplant ecologists had different objectives andmotivations that worked against mutualrecognition and exchange of ideas on eco-logical succession. First, plant ecologists havemostly studied succession prospectively(Kingsland 2005) as a forecasting tool to pre-dict future changes in community composi-tion, whereas carrion ecologists (particularlythose who did casework) studied successionretrospectively, backtracking egg laying byadult flies and beetles to estimate time ofdeath of the deceased (Byrd and Castner2010). This may partly explain why Markovchain models of succession, used mostly byplant ecologists for analyzing future succes-sional states, have found little appeal amongcarrion ecologists (i.e., “the forward prob-lem”; Solow and Smith 2006). Second, plantsuccession is a concept embedded within theecosystem (Tobey 1981; McIntosh 1985;Kingsland 2005); as such, most early plantecologists held that ecosystems (throughtheir communities) exhibited large-scale ho-mogeneity and long-term stability, rooted inthe “balance of nature” assumption that pre-vailed for centuries (Wu and Loucks 1995).In contrast, carrion was viewed and studiedin isolation of the larger ecosystem, provok-ing early animal and carrion ecologists to usethe terms “microsere,” “microseral stage,”and “microcommunity” to describe thesehabitat patches (Allee et al. 1949; Reed 1958;Payne 1965; Johnson 1975). Despite these



different perceptions, a few early and far-sighted plant ecologists (McIntosh 1985)recognized the linkage between ecosys-tem heterogeneity and scale multiplicity(i.e., hierarchical patch dynamics; Wuand Loucks 1995). One was William S.Cooper, who concluded after mappingand aging trees in Isle Royale, Lake Su-perior, that the forest is a:

mosaic or patchwork [that] changes con-tinually in a manner that may almost becalled kaleidoscopic when long periods oftime are considered (Cooper 1913:36).

Decades later, Alexander S. Watt, while ex-panding on this framework, introduced theterm “gap phase” when describing patches offorest (Watt 1947:12) and cited insect inhab-itants of decaying walnuts, logs, and dung asanimal examples (Watt 1947:20). Third,most 20th-century plant and animal ecolo-gists chose to study “pristine” environmentsthat were largely (although never entirely)removed from human activities (Kingsland2005); whereas, many carrion ecologistsconducted their field work in and aroundhuman-managed landscapes (e.g., agri-cultural experiment stations, urban andsuburban areas, landfills). Fourth, most ac-ademic ecologists have historically shunned in-volvement in environmental litigationbecause they perceived it to be unprofes-sional, claimed it diluted their objectiv-ity, and found it brought few academicrewards (Willard 1980). In contrast, many car-rion ecologists (i.e., forensic entomolo-gists, anthropologists, taphonomists) haveroutinely assisted law enforcement and testi-fied as expert witnesses (e.g., Haglund andSorg 1997; Greenberg and Kunich 2002; Du-pras et al. 2006). Tellingly, these ideologicaland motivational differences are reflected intextbook comparisons that show a conspicu-ous lack of environmental litigation coveragein general ecology textbooks (even cases in-volving plant succession and biodiversity; seeWillard 1980), compared to whole-chaptercoverage of litigated casework, expert witnesstestimony, and/or courtroom practices inmany forensic entomology, anthropology,and taphonomy textbooks (e.g., Haglund

and Sorg 1997; Greenberg and Kunich 2002;Burns 2013).

To sum up, the available evidence showsthat carrion and plant ecologists of the late19th and early 20th centuries, despite havingcommon precursors, advanced ecologicalsuccession theory in isolation and developeddifferent academic cultures, motivations,and objectives that kept them apart. It istempting to speculate whether the originand history of this theory would have un-folded differently if specialization and com-partmentalization of the natural and medicalsciences in the late 19th century had beendelayed, or if early plant and animal ecolo-gists and their founding institutions in theearly 20th century had coalesced and broad-ened their scope, or if plant and carrionecologists in the mid-20th century hadshared similar views of the ecosystem and inthe way they studied succession. Althoughthese alternate histories will remain thoughtexperiments, it seems clear that the originand development of ecological successiontheory unfolded as a series of missed oppor-tunities for cross-collaboration between itstwo groups of pioneers and successors.

carrion insect succession: aclementsian or gleasonian process?Since the theoretical framework of carrion-

insect succession does not provide many an-swers with regard to community assembly, itis tempting to draw information from plantecology. Carrion use by insects appears toevoke agreement, in part, with both Clem-entsian and Gleasonian succession. From aClementsian view, carrion-insect successionis directional in nature and is relativelypredictable within a given ecosystem of abiogeographic zone (e.g., Anderson 2010),two traits that are required for time-since-death estimation. Although decompositionis marked by statistically predictable stagesor “seres” (Michaud and Moreau 2011),boundaries between stages (Schoenly andReid 1987; Boulton and Lake 1988; Mouraet al. 2005) and between ecosystems (Mi-chaud et al. 2010) rarely correspond toabrupt changes in arthropod composi-tion. For that reason, carrion-insect suc-cession also evokes comparison with



Gleasonian succession. Another Gleaso-nian trait is interannual variation in in-sect arrival and departure times thatoccur when carcasses are exposed in thesame seasons and environments in differ-ent years (e.g., Archer 2003; Michaudand Moreau 2009). Also, some insect spe-cies that frequent carrion have a randomoccurrence pattern and do not appear tofollow the predicted successional sequence(Michaud and Moreau 2009).

Plant and carrion-insect succession alsodiffers in major and obvious ways. Carrionfunctions as a nonequilibrium island (Beaver1977) that is without primary production ora climax assemblage because its successionalendpoint is recycling of the remains intogravesoil (Poole 1974; Braack 1987; Begon etal. 1996; Carter et al. 2007). In her analysis ofturnover rates, Anderson (2007) examinedsuccessional data sets from both plant andcarrion communities and found that themain drivers of succession were competition,abiotic limitation, and dispersal limitation,and concluded that her results were moreconsistent with a Gleasonian approach forplants but could not come to any conclusionwith respect to carrion-insect succession. Ev-idence from dispersal studies on sapropha-gous Diptera and Coleoptera, however, showthat they have wide dispersal ranges thatspan several kilometers (see references inMichaud et al. 2012). Moreover, competitionamong fly larvae on carrion, dung, andfallen fruit has been well documented(e.g., Valiela 1974; Denno and Cothran1975; Atkinson and Shorrocks 1984;Kneidel 1984; Hanski 1987; Ives 1988);however, the net effect of competition onthe rest of the insect community remainsunknown. Although these studies pro-vided important insight on how commu-nity assembly proceeds on ephemeraland divided resources, none directly ex-plored mechanisms of succession. Morefield studies will be needed to reach aconclusion about whether carrion-insectsuccession fits the Gleasonian model, theClementsian model, or if it is a uniqueprocess deserving its own conceptualframework.

Future Questions in Carrion Ecologyand Forensic Entomology

what mechanisms underlie carrion-insect succession?

The Gleason versus Clements debate islikely to persist for many years to come. Thisis because these concepts are rooted in the-ory rather than empirical data, which defiesstraightforward testing. Connell and Slatyer(1977) attempted to resolve the testabilityissue by proposing three mutually exclusivemechanisms of succession (facilitation, inhi-bition, and tolerance) for plants and sessileaquatic animals. Facilitation has been pro-posed as a likely mechanism for animal suc-cession on carrion (Connell and Slatyer1977; Schoenly and Reid 1987), althoughno empirical evidence was offered to sup-port this claim. Connell and Slatyer wrote:

The mechanisms of the facilitation modelprobably apply to most heterotrophic suc-cessions of consumers feeding on car-casses, logs, dung, litter, etc. . . . Noexperimental investigation has been car-ried out to demonstrate the details of theprocess, but the evidence seems to supportthe application of this model (Connell andSlatyer 1977:1124).

Later, Schoenly and Reid wrote:

The species replacement patterns . . . areconsistent with Connell and Slatyer’s (1977)“facilitation” mechanism (model 1) of com-munity succession . . . We stress, however,that the available data sets are inappropriatefor testing the facilitation hypothesis. Cor-roboration of this hypothesis will require fur-ther field and/or laboratory trials (Schoenlyand Reid 1987:199).

Over a decade later, Smith and Baco(2003) stated in their review of whale falls atthe deep-sea floor that facilitation was thedominant mechanism in community assem-bly, although again the hypothesis was notdirectly tested. Researchers working onother degradative habitats where facilitationhas been demonstrated, such as rottingwood (Renvall 1995; Weslien et al. 2011) anddung (Slade et al. 2007), also hinted thatfacilitation may occur on carrion. However,as Schoenly and Reid (1987; see above)pointed out almost 30 years ago, further test-



ing will be required to better understandhow applicable to carrion facilitation (or anyother mechanism) truly is.

Another untested assumption dates backto Megnin (1883, 1887, 1894) and his con-cept of “squads” in which he proposes thatcarrion-insect succession is driven byphysical-chemical changes in cadaver decay(Figure 1). In other words, different waves ofinsects are attracted to specific odors as theyare released sequentially during decomposi-tion. A few studies have identified many com-pounds that are released during carcassdecomposition (e.g., Vass et al. 1992; Vass2012) and the response of carrion-associatedinsects to certain compounds has beenshown (e.g., Frederickx et al. 2012; von Ho-ermann et al. 2012; Johansen et al. 2014);however, we are aware of no study that hasestablished a link between chemical succes-sion and insect succession in carrion. In-deed, Vass (2012) has proposed an “odorsignature” for human decomposition thatmay have many potential benefits for theforensic sciences. However, such a concept,if it can be linked with corpse-insect succes-sion, will require further experimentation incontrolled settings.

Succession is a leading concept in ecology(Cherrett 1989) and its predictability in car-rion is a basic premise behind forensic ento-mology. Focusing more time and effort onmechanisms of succession is likely to in-crease our understanding of communityassembly and improve the theoretical frame-work of both carrion ecology and forensicentomology. Despite these knowledge gaps,researchers cite the potential of carcasses toilluminate ecological principles, in largepart, due to their discrete and ephemeralnature and ease with which they can be ac-quired, replicated, manipulated, and sam-pled (Braack 1987; Schoenly and Reid 1987;Finn 2001). Because carrion communi-ties assemble from a regional speciespool, they offer realistic diversity gradi-ents (and endless community combina-tions) for investigating diversity-ecosystemfunction relationships (Finn 2001). More-over, the hotly disputed space-for-time substitu-tion (Pickett 1989; Johnson and Miyanishi2008; Walker et al. 2010) does not apply, giving

carrion a clear advantage as a model system forinvestigating mechanisms of succession andother ecological processes.

developing the ecologicalframework of forensic entomologyHistorically, the forensic sciences were

held in high regard by the public and thecourts throughout most of the 20th cen-tury. However, the landmark paper by Saksand Koehler (2005) and the long-anticipated,congressionally mandated National Re-search Council (NRC 2009) report, Strength-ening Forensic Science in the United States: APath Forward, drew attention to many sci-entific inadequacies of the forensic iden-tification disciplines (e.g., fingerprinting,toolmarks, ballistics). Among the 13 re-commendations in the NRC report was theneed to:

develop tools for advancing measurement,validation, reliability, information sharing,and proficiency testing in forensic scienceand to establish protocols for forensic ex-aminations, methods, and practices (NRC2009:214; Recommendation 6).

Although forensic entomology was not atarget of the report, a paradigm shift to cor-rect methodological shortcomings and de-velop theoretical models had started beforethe report was published. For example, fo-rensic entomologists had anticipated theneed to incorporate null models and MonteCarlo methods in hypothesis testing (Schoenly1991, 1992; Schoenly et al. 1996), developprobability-based estimates of time sincedeath (Wells and LaMotte 1995; LaMotteand Wells 2000; Michaud and Moreau 2009),test the reliability of pig carcasses as modelcorpses (Schoenly et al. 2007), and conductblind validation tests of time-since-deathmethodology (VanLaerhoven 2008). Afterthe report was published, researchers in thefield realized the need to design better fieldexperiments (Michaud et al. 2012; Michaudand Moreau 2013) and improve and fieldtest their statistical models (Michaud andMoreau 2011; Basque and Amendt 2013;Perez et al. 2014). Carrion ecologists, in turn,have vowed to develop the ecological frame-work of forensic entomology by proposing a



strategy that unifies basic and applieddecomposition research (Tomberlin et al.2011a,b). Similarly, carrion ecologists havehighlighted the importance of decomposingcarcasses in the larger ecosystem in an at-tempt to advance carrion ecology theory. Forexample, Parmenter and MacMahon (2009)examined the decomposition rate of severalvertebrate species for different seasons andmicrosites and also measured energy and nu-trient loss through nutrient cycling and com-pared these loss rates to plant-litter studies.Yang et al. (2008) proposed that pulsed re-sources, such as carrion, influence ecologicalprocesses at the individual, population, andcommunity levels. Barton et al. (2013) devel-oped a framework of carrion dynamics thatweds succession theory with aggregation andcoexistence theory (e.g., Atkinson and Shor-rocks 1984; Ives 1988) and suggested refo-cusing future research on carrion’s impactson biodiversity and ecological processes atdifferent spatial scales. Pechal et al. (2014)showed how insect access to carrion, if de-layed by biophysical or forensic factors, canshift community structure and arrival pat-terns, and slow decomposition rates. Al-though much work needs to be done toelucidate mechanisms of carrion-insect as-sembly, armed with this new paradigm, car-rion ecologists and forensic entomologistshave the momentum, tools, and ecologicalmindset to accomplish it.

ConclusionAt a time when most ecologists believed

that plants directed succession, Elton (1927)warned plant ecologists that they should notignore animals, and offered examples ofhow activities of animals (e.g., eating, dis-persing, trampling, and destroying vegeta-tion) could influence successional outcomes(Cain et al. 2008). Today, authors of ecologytextbooks feature examples of both auto-genic (plant) and heterotrophic (marine,degradative) succession, but often ignorecarrion-arthropod succession as an exampleof the latter (but see Begon et al. 1996;Krebs 2009). Here we showed that not onlydid early forensic entomologists advance

and test the first formal definition andmechanism of ecological succession (Me-gnin 1883, 1887, 1894; Yovanovitch 1888;Johnston and Villeneuve 1897; Motter 1898;Niezabitowski 1902), but that their his-tory and contributions paralleled those ofearly plant ecologists. For example, bothgroups originated in Europe, used succession-related concepts to refute the theory ofspontaneous generation, and introducedsuccession to colleagues in North America.Both groups also initially placed greatimportance on typological concepts (i.e.,“seres” in plant ecology, “squads” in carrionecology), the role of site and climate inshaping successional outcomes, and offereda qualitative framework of the mechanismsinvolved. Afterward, for nearly a century,empirical testing of succession mechanismsin carrion went underexplored, due in largepart to an emphasis on insect taxonomy andobservational studies (Michaud et al. 2012)and to the lingering, untested claim thatfacilitation was the sole mechanism (Connelland Slatyer 1977; Schoenly and Reid 1987;Smith and Baco 2003). Today, the Clemen-tsian (i.e., stage-based) view remains domi-nant in carrion ecology and in severalforensic disciplines (i.e., entomology, an-thropology, taphonomy), and momentum isgrowing to put these disciplines on a moreecological (and empirical) footing. We ex-pect that the theoretical framework of theseforensic disciplines will benefit greatly fromecology-based (i.e., mechanistic) thinking,much in the same way modern ecology willbenefit from increased understanding ofsuccessional dynamics on carrion.

acknowledgments

We are grateful to Dale Bottrell, Jim Brown, Joel E.Cohen, Michael Fleming, Franck Gandiaga, andParyse Nadeau for references and comments on anearlier version of this manuscript. We also thankChristian Fromme for translating the Niezabitowski(1902) article from German to English and Tim Heldfor help with the article’s content and grammar. Wealso thank two anonymous reviewers for their manyhelpful recommendations, which have greatly im-proved the quality of this manuscript.



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Rewriting ecological succession history: did carrion ... · cited in Rennie 1810; Dureau de la Malle 1825; Hult 1885, 1887; Warming 1891) helped mark the birth of ecology. Accord-ing