Naturwissenschaften

, Volume 93, Issue 11, pp 557–564 | Cite as

Hyperdisease in the late Pleistocene: validation of an early 20th century hypothesis

Original Article

Abstract

The hypothesis of disease-related large mammal extinction has new support. A unique pathologic zone of resorption was first noticed in a Hiscock Mammut americanum metacarpal. The pathognomonic zone of resorption was present in fifty-nine (52%) of 113 skeletons with feet available for examination. Metacarpals and metatarsals were most commonly affected. Associated rib periosteal reaction is highly suggestive of tuberculosis and the foot lesions were identical to that documented in Bison as pathognomonic for tuberculosis. Recognizing that only a portion of animals infected by infectious tuberculosis develop bone involvement, the high frequency of the pathology in M. americanum suggests that tuberculosis was not simply endemic, but actually pandemic, a hyperdisease. Pandemic tuberculosis was one of several probable factors contributing to mastodon extinction.

Keywords

Tuberculosis Hyperdisease Mastodon Pleistocene Erosive disease Bison Infection 

Introduction

Hyperdisease is offered as one of three major theories for late Pleistocene extinction of megafauna (Alroy 2001; Grayson 1984; Jepsen 1964; Martin and Wright 1967; MacPhee and Marx (1997), predicated upon the existence of a pandemic disease (affliction of the majority of the population). Evidence proved elusive, until recognition that more than half of Western Hemisphere mastodon (but the other major Pleistocene proboscidean branch, mammoths were not afflicted) examined in the current study were afflicted with the same pathologic alteration (articular surface undermining characteristic of tuberculosis) first recognized in a mastodon metacarpal (BMS E27191) from the late Pleistocene Hiscock Site in Western New York (Rothschild 2003).

Systematic macroscopic evaluation of North American collections of Mammut americanum foot bones was conducted to establish whether the disease was a virulent terminal Pleistocene event (to which demise of the species could be attributed) or if it had been long present. The latter would suggest that it weakened, rather than killed, making mastodons more susceptible to the climatic and human “influences” of the terminal Pleistocene.

Materials and methods

Postcranial large fossil mastodon bones were systematically examined macroscopically for surface abnormalities in the collections of the American Museum of Natural History, New York City (AMNH); Bergen County Museum, Trenton, NJ (BCM); Brigham Young University, Provo, Utah (BYU); Buffalo Museum of Science, Buffalo, NY (BMS); Carnegie Museum of Natural History, Pittsburgh, PA (CM); Children’s Museum of Indianapolis, Indianapolis, IN (CMI); Cleveland Museum of Natural History, OH (CMNH); Columbiana Historical Society, Columbiana, OH (CHS); Cornell University, Ithaca, New York (CU); Denver Museum of Natural History, CO (DMNH); Field Museum of Natural History, Chicago (FMNH); Florida Museum of Natural History, Gainesville, FL (FLMNH); George C. Page Museum, Los Angeles, CA (LACMHC); Idaho Museum of Natural History, Pocatello, ID (IMNH); Illinois State Museum, Springfield (ISM); Indiana State Museum, Indianapolis (INSM); Joseph Moore Museum of Natural History, Earlham College, Richmond, IN (JMM); Kent State University, Salem, OH (KSU); Louisiana State University, Baton Rouge, LA (LSU); Mastodon State Historic Site (MSHS), Imperial MO; McKinley Museum of History, Science and Industry, Canton, OH (MMH); Michigan State University, East Lansing, MI (MSU); National Museum of Natural History, Washington, DC (USNM); New Brunswick Museum, Saint John, New Brunswick, Canada (NBMG); New Mexico Museum of Natural History, Albuquerque (NMMNH); New York State Museum, Albany (NYSM); Nova Scotia Museum of Natural History, Halifax, Nova Scotia (NSMNH); Orange County Community College, NY (OCCC); Orton Geologic Museum and Ohio State University, Columbus, OH (OSU); Paleontologic Research Institute, Ithaca, New York (PRI); Pratt Museum of Natural History, Amherst College, Amherst, MA, (ACM); Pubic Museum of Grand Rapids, Grand Rapids, MI (PMGR); Rochester Museum and Science Center, NY (RMSC); Royal Ontario Museum, Toronto, Canada (ROM); State Museum of Pennsylvania, Harrisburg (SMP); University of Michigan, Ann Arbor (UM); University of Nebraska, Lincoln (UNSM); University of Kansas Museum of Natural History, KS (KU); University of Utah Museum of Natural History, Salt Lake City, Utah (UMNH); and Yale Peabody Museum, New Haven, CT (YPM).

Infectious disease (nonspecific infection) was recognized on the basis of abscesses or filigree (microbubbly or aero candy-like) reaction on the bone surface (Rothschild and Martin 1993). Specific diagnosis of tuberculosis was hypothesized on the basis of subchondral joint surface undermining, with relative sparing of the actual joint (subchondral) surface, pathognomonic for that diagnosis (Resnick 2002; Rothschild and Martin 1993). Normal subchondral bone articular surface is smooth, whereas tubercular infection excavates under this region (rather than through it). This tubercular excavation is distinct from the fronts of resorption noted in erosive spondyloarthropathy, which actually disrupt the joint (subchondral) surface (Rothschild and Martin 1993; Rothschild and Woods 1991). Zones (rather than fronts) of resorption have been related to tuberculosis in humans (Hershkovitz et al. 1998; Hong et al. 2001; Rothschild and Martin 1993) and documented as Mycobacterium tuberculosis by DNA extraction in Pleistocene bison (Rothschild et al. 2001). The characteristic erosions of tuberculosis are also distinguishable from rheumatoid arthritis and spondyloarthropathy on the basis of location. Whereas the erosions in all three disorders can be marginal in distribution, characteristic erosions of tuberculosis spare the actual subchondral bone (the bone underneath the joint cartilage). These will be henceforth referred to as classic erosions in this paper. Conversely, rheumatoid arthritis and spondyloarthropathy erosions invade that subchondral bone (Rothschild and Martin 1993; Rothschild and Woods 1991). The classic erosions of tuberculosis are easily distinguished from other granulomatous diseases, which do not spare the subchondral bone (Hershkovitz et al. 1998). Nonclassic erosion of joints also occurs in tuberculosis and may have specificity in identifying an infectious disease, but not which one (Resnick 2002; Rothschild and Martin 1993). Therefore, classic erosions were sought to allow specific diagnosis.

Selected pathologic specimens were examined radiologically in the anatomical position in which they would be viewed during in vivo radiology. Computerized tomography (Pickard 600 computerized tomography equipment) was performed in axial and transverse longitudinal planes using 1-mm-thick slices on three specimens to confirm excavation (erosion) as opposed to natural variation.

Chi-square and Fisher exact tests were utilized to assess relationship of rib periosteal reaction to undermined articular surfaces and other signs of infection. Accession numbers and dates are provided where they could be derived.

Results

Bacterial infection

Twenty-five of 113 individuals (22%) had bone destruction with filigree remodeling and/or abscesses characteristic of bacterial infection. This included three occurrences in metacarpals III, IV (one of each bilateral), and V, two occurrences in metacarpals I and II, unspecified incomplete metatarsal and cuneiform, and one each in scaphoid, magnum, astragalus, cuboid, and pedal proximal phalanges II, III, and IV.

Tuberculosis

A zone of resorption, undermining the articular surface (Fig. 1), was noted in 59 (52%) of 113 individuals available for examination (Tables 1 and 2). Computerized tomographic evaluation confirmed undermining of the articular surface (Fig. 2), as opposed to the buildup of reactive bone which could simulate bone excavation. Metacarpals (57) and metatarsals (48) were most commonly affected, with less frequent involvement of phalanges (eight manus, four pes), carpals (13 bones), and tarsals (19 bones).
Fig. 1

Erosions, granulomatous masses, and abscesses in mastodon feet. Posterior view of metatarsals (a UMNH 36.63, d BMSE 27191, and e PRI 1182), metacarpals (f PRI 1182 and h UF 137891), astragalus (b LSU 2290 and j UM 37881) and phalanges (c FLMNH 50225E and i KU), and anterior view of carpal metacarpal articulation (g DMNH 1924). Large erosions undermine articular surfaces in a, b, e, f, and g, with more subtle erosions in c, d, and h (arrow). Granulomatous mass effect in f and i (left image, noting right normal) with abscesses in i and j

Table 1

Distribution of resorption zone and rib lesions in Mammut americanum with age, sex, and butchering assessment provided where known

Site

Number

Available dating

Feet

Rib

Stress fxa

Ageb

Sexb

Butcheredb

Nova Scotia, Canada

NSMNH 92GF220

 

+

    

Hillsborough, NB, Canada

NBMG 3906

 

+

    

Arborio, NY

NYSM V102

 

+

0

    

Pirello, NY

NYSM 29668

 

0

0

    

Temple Hill, NY

NYSM V100

 

+

0

    

Hiscock, NY

BMS E27191

 

+

+

+

   

Doerfel, Springfield, NY

BSA E2SW

 

+

+

    

Museum Village, Monroe, NY

MV exhibit

 

0

0

 

26

Male

 

Dwarskill, NY

BCM no #

 

0

    

Sugar Loaf, NY

OCCC exhibit

9,860 +/−225

0

0

+

21

Male

 

Gilbert, Chemung Cty, NY

CU 42440

14,500

+

0

+

   

Hyde Park, Dutchess, NY

PRI 1182

1,500

+

+

    

Farview, Livingston, NY

RMSC 94.07.01

10,600

+

+

    

East Bloomfield, NY

RMSC 94.83.01

 

+

+

    

Seneca, NY

ACM 1172

 

+

    

Otisville, NY

YPM VP 012600

 

0

0

    

Scottsburgh, NY

YPM VP 011714

 

0

    

North Java, NY

PRI 1260

 

+

0

    

Warren, NY

AMNH 9951

 

0

0

    

Hackensack, NJ

BCM no #

 

0

    

Bojak/Liberty Cty, NJ

NJSM 11267

10,995+/−750

+

0

+

21–2

Female

 

Sparta, Sussex, NJ

NJSM 11268

12,730+/−360

0

0

    

Ohberg Vernon County, NJ

NJSM 11907

10,890+/−200

0

0

 

20–1

Female

 

Monroe, PA

SMP-VP 13

12,000

 

0

0

   

Saltville Cty, VA

CM 3949

 

0

    

St. Helena Island, SC

ACM 1181

 

+

0

    

Shipyard Creek, Georgia

USNM 494405

 

+

    

Moffit Cty, FL

CM 340

 

0

    

Taylor County, FL

ROM 34741

 

+

    

Taylor, County, FL

FLMNH 137891

 

+

+

    

Taylor County, FL

FLMNH 103618

 

+

    

Alachua County, FL

FLMNH 50225E

 

+

    

Alachua County, FL

FLMNH 50225E—2nd animal

 

0

    

Alachua County, FL

FLMNH 50225E—3rd animal

 

0

    

Sarasota County, FL

ROM 33702

 

+

    

Florida

USNM 11620

 

0

    

Angola Parish, LA

LSU VL429

 

0

    

Ward Creek Baton Rouge Parish, LA

LSU V586

 

+

    

Tunica Creek W. Feliciena Parish, LA

LSU 3390

 

0

    

Tunica Hills W. Feliciena Par, LA

LSU V854

 

0

    

Adams, Mississippi LSU V536

  

+

    

Bony Springs Lick, KY

ISM 39BS68

16,580+/−220

+

    

Bony Springs Lick, KY

ISM 154BS68

16,580+/−220

+

    

Bony Springs Lick, KY

ISM 130BS71

16,580+/−220

+

    

Bondo Betty, Stark, OH

McKinley Mus

12,000–15,000

0

0

    

Conway Mastodon, OH

OSU 23119

 

+c

0

+

   

Licking, OH

CMNH 10001

 

+

0

    

Hartley, Columbiana, OH

CMNH 2001-35

 

+

+

    

Firestone Farms, Columbiana, OH

Columbiana Co Hist Soc Exhibit

 

0

    

Christensen Site, Hancock, IN

CMI no #

12,500

0

0

    

Richmond, IN

JMM VP2

 

+

0

    

Waterloo, IN

CM 67

 

+

+

+

24

Male

 

Gums Farm, Port, IN

INSM 71.3.173

 

0

0

    

Marshal, IN

INSM 71.3.146

 

0

0

    

Darrow; LaGrange, IN

INSM 71.3.26

 

0

0

    

Hamlet Quad, IN

INSM 71.983.74

 

+

+

    

Stark, IN

INSM 71.980.50

 

0

    

Beusching, IN

IPFW no #

 

+

+

+

   

Argos, IN

UNSM 28-2-33

 

+

+

    

Kalb, IN

DMNH 1924

 

+

+

+

   

Indiana

PM 1173

 

0

    

Indiana

PM 3945

 

0

    

Indiana

PM 39231

 

0

    

Indiana

PM 26267

 

+

0

    

Indiana

UMNH 36.63

 

+

0

    

Indiana

USNM 8881

 

+

    

Illinois

USNM 8204

 

+

+

    

Grandville, MI

PMGR no #

11,320+/−140

+

0

  

Male

Yes

Mannington, Salem Cty, MI

UM no #

 

0

    

Somsel–Toledo, MI

UM 13909

 

0

0

    

Eldridge, MI

UM 50675

11,000

0

0

+

  

Yes

Taylor, MI

UM 61246

 

+

0

  

Male

No

Kuhl, MI

UM 59936

 

+c

+

 

45

Male

No

Van Sickle, MI

UM 58028

 

0

0

 

26

Male

Yes

New Hudson, MI

UM 57856

 

0

  

Female

Yes

Pleasant Lake, MI

UM 57705

10395+/−100

+

0

+

36

Male

Yes

Vincent, MI

UM 44432?

 

0

0

    

Russell Farm I, MI

UM 37811

 

+

0

 

28

Male

Yes

Bloomfield, MI

UM 8394

 

0

    

Tecumseh, MI

UM 3484

 

0

0

    

Tecumseh, MI

UM 3483

 

0

0

+

   

Brennan, MI

UM 10627

 

+

    

Winameg, MI

UM 11230

 

0

0

 

34

Male

Yes

Krugler, MI

UM no #

 

+

0

    

Powers, MI

West Mich Univ

 

0

 

39

Female

No

Owosso, MI

UM 23498

 

0

0

 

39

Female

No

Jonio, Conklin, MI

MSU VP 1289

 

+

+

    

Keith, MI

MSU VP 1112

 

0

0

    

South Michigan

PM 25125

 

+

0

    

Michigan

MSU VP 1290

 

0

0

    

Michigan

UM 11731

 

0

0

    

Michigan

UM 10375

 

0

    

Michigan

UM 3488

 

+

    

Welland City, Ontario

ROM 65

 

+

0

    

Wellandport, Ontario

ROM 4184

 

+

    

Rodney, Ontario

ROM 1792

 

0

    

Tuppenville, Ontario

ROM 3272

 

+

    

Barnhart, Jefferson Co, MO

MSHS no #

 

+

0

    

Lynch, Boyd, NE

UNSM 1430

 

0

    

Nebraska

AMNH AINS 142

 

0

    

Nebraska

AMNH AINS 50

 

0

    

Madison Valley, MT

CM 1361

 

0

    

Idaho

IMNH 17248

 

+

0

    

Idaho

IMNH 17269

 

0

    

Idaho

IMNH 730

 

0

    

Spring Creek, NV

NV S2631

 

+

    

Wasatach Mountains, UT

BYU 4379

 

0

0

    

Rancho LaBrea, CA

LACMHC 60232/1

13,900

0

    

Rancho LaBrea, CA

LACMHC 81769

 

+

    

Rancho LaBrea, CA

LACMHC 85218/21

12,200

+

    

Rancho LaBrea, CA

LACMHC 81785

 

+

    

Rancho LaBrea, CA

LACMHC 81036

 

0

    

Rancho LaBrea, CA

LACMHC 105557

 

0

    

Rancho LaBrea, CA

LACMHC 81039

34-38,000d

+

    

Rancho LaBrea, CA

LACMHC 95319

 

0

    

Rancho LaBrea, CA

LACMHC 127574

 

+

0

    

Panama

USNM 494404

 

+

    

Insertae

ACM 2219

 

+

    

No # Indicates purchase/curation in process, so numbers not available.

aFracture

bDerived from references Martin and Wright 1967, Palfi et al. 1999, Resnick 2002, and Rothschild 2003.

cAssociated with draining sinus and fused vertebrae with filigree reaction.

dThis specimen from 14 ft depth of pit 9. Wood below 10 ft from this pit was dated between 34,000–40,000 years before present (Marcus and Berger 1984).

Table 2

Zone of resorption, undermining the articular surface

Affected bone

Number affected

Forelimb

 

 Radius

1

 Pisiform

2

 Magnum

2

 Lunar

2

 Scaphoid

4

 Unciform

1

 Metacarpal I

4

 Metacarpal II

16, bilateral in 2

 Metacarpal III

13, bilateral in 3

 Metacarpal IV

14, bilateral in 5

 Metacarpal V

7

 Phalanx II-1a

2

 Phalanx III-1

1

 Indeterminate

5

Hindlimb

 

 Astragalus

7

 Navicular

2

 Cuboid

1

 Entocuneiform

2

 Ectocuneiform

4

 Calcaneum

3

 Metatarsal I

4

 Metatarsal II

10

 Metatarsal III

15, bilateral in 3

 Metatarsal IV

16, bilateral in 1

 Metatarsal V

2

 Phalanx II

2

 Phalanx III

1

 Phalanx IV

1

aWith draining sinus

Fig. 2

CT slice in lateral projection of mastodon BMSE 27191 metatarsal. Arrow points to erosion

Fifteen (25%) of 60 individuals with manus/pes undermined articular surfaces and associated ribs had periosteal reaction on the pleural surface of several of those ribs. Rib periosteal reaction was found only among individuals with undermined articular surfaces [Chi-square (1 df)=17.143, p<0.001]. Rib lesions correlated with other signs of infection (e.g., abscess or filigree reaction) (Fisher exact test, p=0.0066).

Tuberculosis demographics

Occurrence of articular surface undermining was independent (Table 1) of season of death or evidence of butchering (as defined, documented, and determined by Fisher (1984, 1987, 1990) and Kapp et al. (1990). It was also independent (Table 1) of age at death (being found in individuals with unfused epipiphyses, as well as mature individuals). Affliction of half of the largest animals (Temple Hill and Warren mastodons) mirrors that of the smaller. If size is considered a rough surrogate for maturity or age, no relationship to size is demonstrable. Examining geographic distribution also revealed no variation in frequency [e.g., west (California, Nevada, and Utah), north (New Brunswick and Nova Scotia), midwest (Indiana and Michigan), and south (South Carolina, Florida, and Georgia), even documenting its occurrence as far south as Panama).

Discussion

Tuberculosis is evidenced in Pleistocene M. americanum. Rib periosteal reaction is highly suggestive of tuberculosis, although other pulmonary infections could be responsible (Kelley and Micozzi 1984). Abscess cavities and other signs of bone infection were clearly present, but also are not specific for tuberculosis (Rothschild and Martin 1993; Rothschild and Woods 1991). It is the articular lesions that provide specificity. This undermined surface, present in 52% of observed individual M. americanum, has been documented in bison as caused by M. tuberculosis (Rothschild et al. 2001). The pathology is easily distinguished from that of other infectious and inflammatory diseases (Hershkovitz et al. 1998; Rothschild and Martin 1993; Rothschild and Woods 1991). The correlation of rib lesions with those documented in other species as pathognomonic and definitive for tuberculosis (Rothschild et al. 2001) strongly supports the contention that the etiologic agent is a member of the M. tuberculosis complex, if not M. tuberculosis itself.

Given the frequency of bone involvement among mastodons affected with tuberculosis, it seems likely that the entire population of mastodons (all animals, at least in the Americas) was afflicted with what has been termed the “white plague” tuberculosis. Recognizing that only a portion of humans and other animals infected by tuberculosis actually develop bone involvement, the high frequency of classic pathology in M. americanum suggests that tuberculosis was not simply endemic, but actually pandemic—a hyperdisease in that species, present from coast to coast (e.g., California to Nova Scotia to Florida) with equal frequencies.

An intriguing aspect of this hyperdisease is its persistence in the fossil record, present as recently as 10,000 years ago and identifiable in bones dated at a minimum of 34,000 years (Fisher 1984, 1987, 1990; Marcus and Berger 1984; Sullivan and Randall 1996). This and analysis of Pleistocene bovids (Rothschild and Martin 2006) firmly establish presence of the disease in the late Pleistocene.

However, there is a difference between infection and mortality. An accommodation may have been reached (Giraud et al. 2001), wherein the infection was pandemic, but not fatal. This contrasts with “endemic stability” (Coleman et al. 2001, p. 1284), “in which clinical disease is sparse despite high levels of infection in the population”. The latter requires that the disease be more likely or more severe in older individuals and that the initial infection decreases the probability of subsequent infection or clinical effect. That is the converse of tuberculosis in humans, in which [BCG (bovine tuberculosis derived) vaccination aside] there is no selective immunity.

We hypothesize the possibility that tuberculosis played a role in the extinction of the mastodon at the end of the Pleistocene. The evidence presented above suggests a latency or accommodation of tuberculosis in the American mastodon, at least in the Late and possibly for most of the Pleistocene. In humans, this tuberculosis latency is lost when the host is stressed (Chan et al. 2002; Palfi et al. 1999). Stress has also been demonstrated as a source of extinction in recent times (Schoener et al. 2001). Because the end of the Pleistocene was a time of great stress (Alroy 2001; Jepsen 1964; Martin and Steadman 1999; Martin and Wright 1967; Stuart 1999), we suggest that loss of latency of tuberculosis in the mastodon may have increased mortality to the point that the population was no longer able to sustain itself. Documenting high frequency of tuberculosis in terminal Pleistocene mastodons is one aspect of this hypothesis-documenting that hyperdisease did exist in the Late Pleistocene. Its persistence in that period, however, suggests that it cannot be invoked as the terminal event.

Notes

Acknowledgements

Appreciation is expressed to Laura Marie Abraczinskas, Warren Allmon, Joe Bopp, Kenneth Carpenter, John J. Chiment, Margery Coombs, George Corner, Shelley M. Cox, Denny Diveley, Dallas Evans, Daniel Fisher, Mary Flynt, Robert C. Glotzhober, Dale Gnidovec, Mike Gottlieb, Brian Hockett, Robert Hunt, Logan Ivy, Brian Iwama, Spencer Lucas, Gay Malin, Peggy Mathias, Cheryl Mattevi, George McIntosh, Lorrie McWhinney, Lyn Murray, David Parris, William H. Peks, Art Poyer, Robert Purdy, Ronald Richards, Tracy M. Rozelle, Nora Salmen, Scott Sampson, Jeff Saunders, Kevin Seymour, Chris Shaw, Greg Sheehan, James M. Sherpa, William Simpson, Deborah Skilliter, Kenneth Stadtman, Robert Sullivan, Mike Voorhees, Ray Wilhite, and Michael Williams for facilitating access to the collections they curate and especially to John Chiment, Kenneth Carpenter, Daniel Fisher, and Jeff Saunders for balancing perspectives.

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Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  1. 1.Arthritis Center of Northeast OhioYoungstownUSA
  2. 2.Northeastern Ohio Universities College of MedicineRootstownUSA
  3. 3.Carnegie Museum of Natural HistoryPittsburghUSA
  4. 4.University of Kansas Museum of Natural HistoryLawrenceUSA
  5. 5.Buffalo Museum of ScienceBuffaloUSA

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