Ehret et-al.-2012 carcharodon-hubbelli

ORIGIN OF THE WHITE SHARK CARCHARODON

(LAMNIFORMES: LAMNIDAE) BASED ON

RECALIBRATION OF THE UPPER NEOGENE PISCO

FORMATION OF PERU

by DANA J. EHRET1* , BRUCE J. MACFADDEN2 , DOUGLAS S. JONES2 ,

THOMAS J. DEVRIES3 , DAVID A. FOSTER4 and RODOLFO SALAS-GISMONDI5

1Monmouth University, West Long Branch, NJ, 07764, USA; e-mail: [email protected] Museum of Natural History, University of Florida, Gainesville, FL 32611, USA; e-mails: [email protected], [email protected] Museum of Natural History and Culture, University of Washington, Seattle, WA 98195, USA; e-mail: [email protected] of Geological Sciences, University of Florida, Gainesville, FL 32611, USA; e-mail: [email protected] de Paleontologia de Vertebrados, Museo de Historia Natural Javier Prado, Universidad Nacional Mayor de San Marcos, Lima 11, Peru;

e-mail: [email protected]

*Corresponding author.

Typescript received 21 October 2009; accepted in revised form 22 August 2012

Abstract: The taxonomic origin of the white shark, Car-

charodon, is a highly debated subject. New fossil evidence

presented in this study suggests that the genus is derived

from the broad-toothed ‘mako’, Carcharodon (Cosmopolito-

dus) hastalis, and includes the new species C. hubbelli sp.

nov. – a taxon that demonstrates a transition between

C. hastalis and Carcharodon carcharias. Specimens from the

Pisco Formation clearly demonstrate an evolutionary mosaic

of characters of both recent C. carcharias and fossil C. has-

talis. Characters diagnostic to C. carcharias include the pres-

ence tooth serrations and a symmetrical first upper anterior

tooth that is the largest in the tooth row, while those indic-

ative of C. hastalis include a mesially slanted third anterior

(intermediate) tooth. We also provide a recalibration of

critical fossil horizons within the Pisco Formation, Peru

using zircon U-Pb dating and strontium-ratio isotopic anal-

ysis. The recalibration of the absolute dates suggests that

Carcharodon hubbelli sp. nov. is Late Miocene (6–8 Ma) in

age. This research revises and elucidates lamnid shark evo-

lution based on the calibration of the Neogene Pisco For-

mation.

Key words: Carcharocles, Cosmopolitodus, geochronology,

Miocene, Isurus, strontium.

Neoselachians are well represented in the fossil

record worldwide during the Neogene and most of the fos-

sil material found consists of isolated teeth. Shark teeth are

shed by the thousands over an individual’s lifetime and

have an enameloid crown that acts as a protective layer

during fossilization. The cartilaginous skeleton of chondri-

chthyans does not typically preserve except in rare instances

where calcified vertebral centra, portions of the neurocrani-

um and fin rays have been described (Uyeno et al. 1990;

Shimada 1997; Siverson 1999; Gottfried and Fordyce 2001;

Shimada 2007; Ehret et al. 2009a). The lack of more com-

plete specimens of most fossil taxa has led to conflicting

interpretations about the taxonomy and anatomy of many

species. Such problems have caused much confusion in the

nomenclature (including generic and specific names) and

terminology (i.e. dental homologies) of fossil neosela-

chians.

One of the most debated enigmas within the neosela-

chians focuses on the evolution and taxonomic placement of

the white shark, Carcharodon carcharias (Linnaeus, 1758),

within the Lamniformes. There are two distinct hypotheses

regarding the evolution of C. carcharias that have been pro-

posed in the literature. The first hypothesis places all large,

serrated megatoothed sharks within the genus Carcharodon,

including C. carcharias as well as those species referred to as

Carcharocles, for example, Carcharocles megalodon (Jordan

and Hannibal, 1923) and its related taxa. Based on this tax-

onomy, the lineage of C. carcharias branched off as smaller

forms of the megatoothed sharks and co-evolved alongside

the truly large taxa, such as C. megalodon (Applegate and

Espinosa-Arrubarrena 1996; Gottfried et al. 1996; Purdy

1996; Gottfried and Fordyce 2001; Purdy et al. 2001).

The second hypothesis proposes that C. carcharias evolved

from the broad-toothed ‘Oxyrhina’ (Cosmopolitodus)

[Palaeontology, Vol. 55, Part 6, 2012, pp. 1139–1153]

ª The Palaeontological Association doi: 10.1111/j.1475-4983.2012.01201.x 1139

hastalis (Agassiz, 1843–1844) while the megatoothed sharks

belong to a separate family, the Otodontidae, within the

Lamniformes (Casier 1960; Glikman 1964; Cappetta 1987;

Ward and Bonavia 2001; Nyberg et al. 2006; Ehret et al.

2009a). C. hastalis was originally assigned to the genus

Oxyrhina and later to Isurus. However, based on affinities

with C. carcharias, Glikman (1964) suggested the reassign-

ment of all unserrated forms within the Carcharodon line-

age to the genus Cosmopolitodus to reflect this relationship

(Siverson 1999; Ward and Bonavia 2001). Under this

hypothesis C. hastalis and C. carcharias represent chrono-

species as C. hastalis is replaced by C. hubbelli and finally

C. carcharias in geological time through a gradation. Fur-

thermore, the teeth of C. hastalis do not share all characters

with Isurus but instead are more similar to C. carcharias

exhibiting triangular crowns that are labiolingually flat-

tened, a flat labial face, a lingual face that is slightly convex

and a root that is flat and quite high (Cappetta 1987). As

such, the genus Carcharodon (Smith in Muller and Henle,

1838) is the senior synonym of Cosmopolitodus (Glikman,

1964) the proper genus name for C. hastalis. Fossil material

collected from the Late Miocene and Early Pliocene of the

Pacific Basin including Peru (specifically the Pisco Forma-

tion), Chile, CA, USA, and Japan provide further evidence

of this relationship (Muizon and DeVries 1985; Long 1993;

Tanaka and Mori 1996; Stewart 1999, 2002; Yabe 2000;

Suarez et al. 2006; Nyberg et al. 2006; Ehret et al. 2009a).

The recent description of an articulated specimen of

this intermediate form of Carcharodon recorded from the

Pisco Formation presents important new insights into the

evolutionary history and taxonomy of the genus (Ehret

et al. 2009a). The described specimen was collected from

Sud Sacaco (West), a locality referred to the Pliocene

(c. 4.5 Ma) by Muizon and DeVries (1985). However, iso-

topic calibration of fossil horizons exposed at Sud Sacaco

(West), using strontium and zircon dating, allows us to

reassess the age of the Carcharodon specimen. Based on

the calibration of these horizons, it is our conclusion that

the specimen should be referred to the Late Miocene

rather than the Early Pliocene.

The purpose of this paper is to present (1) a reassess-

ment of the ages of some horizons within the Pisco For-

mation, (2) formally describe a new species of the white

shark and (3) relate changes in age and taxonomy to the

evolution of the white shark within the Pacific Basin.

METHODS AND MATERIALS

Numerous studies indicate the Miocene Epoch was char-

acterized by rapidly increasing 87Sr ⁄ 86Sr in the global

ocean; therefore, it is especially amenable to dating and

correlating marine sediments using strontium isotope

chemostratigraphy (Hodell et al. 1991; Miller et al. 1991,

Hodell and Woodruff 1994, Oslick et al. 1994, Miller and

Sugarman 1995, Martin et al. 1999, McArthur et al.

2001). We analysed three fossil marine mollusc shells

from each of five localities to determine the ratio of87Sr ⁄ 86Sr in the shell calcium carbonate. When compared

with the global seawater reference curve, these data allow

us to estimate the age of the fossil molluscs for each

locality (Table 1).

For isotopic analyses, we first ground off a portion of

the surface layer of each shell specimen to reduce possible

contamination. Areas showing chalkiness or other signs of

diagenetic alteration were avoided. Approximately 0.01–

0.03 g of aragonite or low-magnesium calcite powder was

recovered from each fossil sample. The powdered samples

were dissolved in 100 ll of 3.5 N HNO3 and then loaded

onto cation exchange columns packed with strontium-

selective crown ether resin (Eichrom Technologies, Inc.,

Lisle, IL, USA) to separate Sr from other ions (Pin and

Bassin 1992). Sr isotope analyses were performed on a

Micromass Sector 54 thermal ionization mass spectrome-

ter equipped with seven Faraday collectors and one Daly

detector in the Department of Geological Sciences, Uni-

versity of Florida. Sr was loaded onto oxidized tungsten

single filaments and run in triple collector dynamic mode.

Data were acquired at a beam intensity of about 1.5 V for88Sr, with corrections for instrumental discrimination

made assuming 86Sr ⁄ 88Sr = 0.1194. Errors in measured87Sr ⁄ 86Sr are better than ±0.00002 (2r), based on long-

term reproducibility of NIST 987 (87Sr ⁄ 86Sr = 0.71024).

Age estimates were determined using the Miocene portion

of Look-Up Table Version 4:08 ⁄ 03 associated with the

strontium isotopic age model of McArthur et al. (2001).

Zircons were extracted from samples using standard

crushing, density separation and magnetic separation

techniques. The zircons were hand picked, mounted in

epoxy plugs along with the reference zircon FC-1 (Paces

and Miller 1993) and analysed using laser ablation multi-

collector inductively coupled plasma mass spectrometry

TABLE 1 . Strontium chemostratigraphic analyses of fossil mar-

ine mollusc shells from the Pisco Formation.

Fossil Horizon Mean87Sr ⁄ 86Sr

Age

estimate (Ma)

95% CI (Ma)

El Jahuay 0.7089424 7.46 9.03–6.51

Montemar 0.7089468 7.30 8.70–6.45

Sud Sacaco

(West)

0.7089659 6.59 10.77–2.50

Sud Sacaco

(West)

0.7089978 5.93 6.35–5.47

Sacaco 0.7090005 5.89 6.76–4.86

Ages and confidence intervals (CI) determined from McArthur

et al. (2001).

1140 P A L A E O N T O L O G Y , V O L U M E 5 5

(LA-MC-ICP-MS). We used a Nu Plasma mass spectrom-

eter fitted with a U-Pb collector array at the Department

of Geological Sciences, University of Florida. 238U and235U abundances were measured on Faraday collectors

and 207Pb, 206Pb and 204Pb abundances on ion counters.

The Nu Plasma mass spectrometer is coupled with a New

Wave 213 nm ultraviolet laser for ablating 30–60 lm

spots within zircon grains. Laser ablation was carried out

in the presence of a helium carrier gas, which was mixed

with argon gas just prior to introduction to the plasma

torch. Isotopic data were acquired during the analyses

using Time Resolved Analysis software from Nu Instru-

ments. Before the ablation of each zircon, a 30 s peak

zero was determined on the blank He and Ar gases with

closed laser shutter. This zero was used for online correc-

tion for isobaric interferences, particularly from 204Hg.

Following blank acquisitions, individual zircons under-

went ablation and analysis for c. 30–60 s. The analyses of

unknown zircons were bracketed by analysing an FC-1

standard zircon.

GEOLOGICAL SETTING

The shallow-water, marine Pisco Formation of southwest-

ern Peru consists of materials that accumulated during

Late Miocene to Early Pliocene (c. 11.6–3.6 Ma); it is well

known for its wealth of vertebrate fossils including elas-

mobranchs, teleosts, chelonians, shore birds, seals, dol-

phins, whales and aquatic sloths (Hoffstetter 1968;

Muizon and DeVries 1985; Muizon and McDonald 1995;

Muizon et al. 2002; Amiot et al. 2008; Ehret et al. 2009a).

In addition to the presence of complete vertebrate skele-

tons, the area also contains the partial remains of fossil

sharks including associated tooth sets, vertebral centra

and preserved cartilage of the jaws and neurocrania. The

Pisco Formation also preserves the transition from Car-

charodon hastalis to C. carcharias as demonstrated in the

shark fossils recovered from localities within the forma-

tion. Another taxon that exhibits intermediate characters

between the two species, previously referred to as Car-

charodon sp., is also abundant at some localities (particu-

larly Sud Sacaco West and Sacaco) of the region (Muizon

and DeVries 1985; Ehret et al. 2009a, b).

The Pisco Formation crops out on the coastal plain of

southern Peru from the town of Pisco south to Yauca

(Fig. 1). The sediments include tuffaceous and diatoma-

ceous sandstone and siltstone, ash horizons, bioclastic

conglomerate (including the marine mollusc beds sampled

in this study) and phosphorite, representing shallow mar-

ine environments. These preserve cyclic marine transgres-

sive and regressive events spanning the Middle Miocene

(c. 13 Ma) through the Late Pliocene (c. 4 Ma; Muizon

and DeVries 1985; DeVries 1998; Amiot et al. 2008).

Around the region of Sacaco, Muizon and DeVries

(1985) identified a composite section for the Pisco For-

mation in the Sacaco area (which is not fully exposed in

the region) consisting of five localities: El Jahuay (also

known as Alto Grande), Aguada de Lomas, Montemar,

Sud Sacaco (West) and Sacaco (Fig. 2). In addition to the

exposed stratigraphy, these localities are also distinguished

by a high diversity of fossilized vertebrate and inverte-

brate species that found in numerous horizons (Marocco

and Muizon 1988).

El Jahuay is designated as the lowermost section of the

Pisco Formation in the Sacaco area (Muizon and DeVries

1985). The lowest tuff bed at El Jahuay is also the oldest

in the Sacaco Basin and has been dated to 9.5 Ma (K-Ar

dating, late Miocene; Muizon and DeVries 1985; Muizon

and Bellon 1986). Below this bed, sediments are com-

prised of a rounded boulder conglomerate (Muizon and

DeVries 1985). In the 15 m exposed above this tuff, the

section contains two shelly sandstone beds that are mixed

with a bioturbated fossiliferous sandstone (Muizon and

DeVries 1985). This layer had been designated as the El

Jahuay vertebrate level (Fig. 2). Fossil selachians of inter-

est to this study within the El Jahuay fossil level are iden-

tified as C. hastalis and C. megalodon.

14º

F IG . 1 . Map of Peru with localities within the Southern

section of the Pisco Formation.

E H R E T E T A L . : W H I T E S H A R K E V O L U T I O N 1141

At Aguada de Lomas, two tuffs were analysed using K-

Ar isotopes and dated to 8 and 8.8 Ma, respectively

(Fig. 2; Muizon and DeVries 1985; Muizon and Bellon

1986). The sequence of these tuff layers and rounded

boulder conglomerates at Aguada de Lomas led Muizon

and Bellon (1986) to conclude that the lower section of

this locality might have been produced by similar pro-

cesses or even contemporaneous with the El Jahuay sec-

tion (Muizon and DeVries 1985). Above these tuff beds,

fine sandstone is the dominant lithology for the next

80 m of the section (Muizon and Devries 1985). The fos-

sil horizon presents at Aguada de Lomas caps these sand-

stone layers and is comprised of cross-bedded sandstone,

Skolithos burrows, and well-preserved vertebrate remains

(Fig. 2; Muizon and DeVries 1985).

The third exposed section of the Pisco Formation in

the southern Pisco Basin can be found at Montemar

(Fig. 2; Muizon and DeVries 1985). Sediments are com-

prised of coarse and fine sandstone, siltstone and gypsum,

along with mixed vertebrate and invertebrate fossils. The

fossil horizon is considered to be uppermost Miocene

(7.3–7.0 Ma) based on the co-occurrence of transitional

Carcharodon teeth (Carcharodon hubbelli n. sp. of this

study) and several molluscan species (Muizon and DeV-

ries 1985). This fossil horizon is also noted for the pres-

ence of articulated skeletons of baleen whales, penguins

and sloths (Muizon and DeVries 1985).

At Sud Sacaco (West), the Pisco Formation is repre-

sented by a fossil horizon that is identified by the pres-

ence of fossilized barnacle debris and shell beds that

contain a diverse assemblage of molluscs (e.g. Dosinia

(Scopoli, 1777)) and vertebrates (Fig. 2). These shell beds

are capped by thick vertebrate-bearing tuffs, fining

upward cycles of brachiopod-bearing sandstone, which

contain serrated C. carcharias-like teeth (Muizon and

DeVries 1985). Based on the stratigraphy and palaeontol-

ogy, Muizon and Bellon (1980) concluded that the shell

beds of the Sud Sacaco (West) fossil horizon were situ-

ated stratigraphically below the vertebrate-bearing tuff

bed dated at 3.9 Ma (i.e. Pliocene), and younger than the

Miocene horizons present at El Jahuay and Montemar

(Muizon and DeVries 1985).

Finally, the youngest section within the southern

Sacaco Basin is exposed at Sacaco. Sediments are mainly

comprised of fine sandstone interbedded with a pebbly

sandstone layer and two mollusc layers. The horizon also

contains interbedded tuffs and cross-bedding is common.

This horizon is considered to be above the vertebrate-

bearing tough bed (3.9 Ma), which is exposed at Sud Sac-

aco (West), and would indicate an Early Pliocene age

(Fig. 2; Muizon and Bellon 1980; Muizon and DeVries

1985). Additional sampling of invertebrate fossils and the

tuff beds taken from El Jahuay (Alto Grande), Montemar,

Sud Sacaco (West) and Sacaco during the summer of

2007 were analysed for 87Sr ⁄ 86Sr isotopes and zircon

U-Pb and will be discussed below.

OVERVIEW OF TAXONOMY ANDFOSSIL RECORD OF CARCHARODON

As previously discussed, the evolutionary history of Car-

charodon has been a contentious subject. To elucidate our

current knowledge of the subject, it is important to

review the hypotheses that have been previously pro-

posed. We will then compare and incorporate the mate-

rial from Peru into these paradigms. The taxonomy of

F IG . 2 . Stratigraphic log of the Pisco Formation (based on

Muizon and DeVries 1985). Abbreviations: AGL, Aguada de

Lomas vertebrate horizon; ELJ, El Jahuay vertebrate horizon;

MTM, Montemar vertebrate horizon; SAS, Sud Sacaco (West)

vertebrate horizon; SAO, Sacaco vertebrate horizon.


the megatoothed sharks (including Otodus and Carcharo-

cles) beyond their relationship to C. carcharias is not

within the scope of this paper and will only be addressed

to the extent necessary.

The first hypothesis places the megatoothed sharks (Oto-

dus and Carcharocles) and C. carcharias within the Lamni-

dae. The serrated-toothed forms of the megatoothed sharks

are assigned to the genus Carcharodon (referred to as Car-

charocles here), while the unserrated form is recognized as

being related and has been given a separate generic name,

Otodus (Agassiz, 1833–1844; Applegate and Espinosa-Arru-

barrena 1996; Gottfried et al. 1996; Purdy 1996; Purdy

et al. 2001). It should be noted that a recent shift in para-

digm recognizes Otodus as a chronospecies, thereby placing

all species of Carcharocles into the genus Otodus, with the

exception of megalodon, which has been referred to the

genus Megaselachus (Glikman, 1964) (Casier 1960; Zhe-

lezko and Kozlov 1999; Ward and Bonavia 2001). For the

purpose of this discussion, however, we refer all serrated

megatoothed sharks to Carcharocles based on the accepted

taxonomy in the literature at the present time.

The grouping of megatoothed sharks with Carcharodon

carcharias was based on a number of dental characters

including: (1) a symmetrical second anterior tooth; (2)

large third anterior (intermediate) tooth that is inclined

mesially; (3) upper anterior teeth that have a chevron-

shaped neck on the lingual surface; (4) an ontogenetic

gradation whereby the coarse serrations of a juvenile

C. carcharias shift to fine serrations in the adult, the latter

serrations resembling those of C. megalodon; (5) morpho-

logical similarity between the teeth of young C. megalodon

and adult C. carcharias (Gottfried et al. 1996; Gottfried

and Fordyce 2001; Purdy et al. 2001; Ehret et al. 2009a).

Following this hypothesis, C. carcharias is either the result

of dwarfism from a larger megatoothed taxon or evolved

via cladogenesis from a large megatoothed shark species

sometime during the Palaeocene and coevolved alongside

the other species (Gottfried et al. 1996; Martin 1996; Pur-

dy 1996; Purdy et al. 2001).

This taxonomy, however, does not truly reflect the fos-

sil record. The characters listed above as diagnostic, unit-

ing the megatoothed sharks and C. carcharias, are a result

of individual variation, interpretation and homoplasy

(Hubbell 1996; Shimada 2005). Variation and pathologic

abnormalities within individual teeth can lead to the

incorrect interpretation and identification of specimens.

As an example, USNM 336204 has been described as lat-

eral tooth of Carcharodon sp. (Purdy 1996) or C. carcha-

rias (Gottfried and Fordyce 2001) from the Middle

Miocene of the Calvert Formation of Maryland (Fig. 3).

However, re-analysis of this specimen reveals that it is a

small C. megalodon, based on the presence of a chevron-

shaped neck, the thickness of the crown and the serration

type. While the serrations are somewhat coarse for

C. megalodon and could be misleading, the presence of

the other characters listed above make this identification

more plausible. Furthermore, the reconstruction of dental

patterns of extinct sharks based on isolated teeth or disar-

ticulated tooth sets is misleading when extant taxa are

used as a template for interpretations (Shimada 2006,

2007). Finally, the presence of serrations in both the

megatoothed and white sharks is a result of homoplasy

rather than a diagnostic character uniting the two taxa. A

comparison of the serrations shows that they are in fact

very different, with the Carcharocles exhibiting very fine

and regular serrations while those of Carcharodon are

coarse and irregular (Fig. 4).

The second hypothesis keeps C. carcharias and the

broad-toothed ‘makos’ within the Lamnidae while the

megatoothed sharks are reclassified into their own family,

the Otodontidae within the Lamniformes. This hypothesis

proposes that Carcharodon hastalis gave rise to the ser-

rated-toothed Carcharodon carcharias during the Late

Miocene or Early Pliocene (Casier 1960; Glikman 1964;

Muizon and DeVries 1985; Cappetta 1987; Ward and Bo-

navia 2001; Nyberg et al. 2006; Ehret et al. 2009a). This

hypothesis would suggest that the lamnid and otodontid

sharks last shared a common taxon in the Cretaceous

(Casier 1960). Casier (1960) proposed that C. hastalis is

ancestral to Carcharodon citing characters of dentition

(although he did not list these characters) and offering

as a possible transition between the taxa, Isurus escheri

(Agassiz 1833–1843), which exhibits weak, fine crenula-

tions (not true serrations) on the cutting edges of its teeth.

It should be noted that Agassiz (1833–1844) separated

the broad-toothed ‘makos’ into numerous separate

F IG . 3 . Carcharocles megalodon tooth, USNM 336204. Scale

bar represents 10 mm.


morphotypes, two of the most prominent were originally

referred to Carcharodon (Oxyrhina) hastalis and Isurus

(Oxyrhina) xiphodon (Agassiz, 1833–1844). His differenti-

ation of the two taxa was based on C. hastalis having a

noticeable flattening of the lingual crown foot and nar-

rower tooth crowns compared to I. xiphodon but admit-

ted that the latter was too weak of a character for

identification (Agassiz 1833–1844; Purdy et al. 2001). Ler-

iche (1926) included I. xiphodon in the synonymy of

C. hastalis and noted the uncertainty of the origin of the

types, which have since been lost (Ward and Bonavia

2001). The species was recognized by Glikman (1964) and

Purdy et al. (2001), who attributed specimens of C. has-

talis from Peru, North Carolina and Belgium; the new

species from Peru described herein; and I. escheri from

Belgium to I. xiphodon based solely on the broadness of

their crowns. Ward and Bonavia (2001) regarded I. xiph-

odon as a nomen dubium based on the arguments of Leri-

che (1926), the absence of any type specimens, and an

unlikely provenance. Recent morphometric analysis of

broad-toothed ‘mako’ specimens by Whitenack and Gott-

fried (2010) supports a morphological difference based on

the broadness of the crown in broad-toothed ‘makos’.

While this study might accurately separate these species,

this could also represent sexual dimorphism or ontoge-

netic changes in tooth morphology in one taxon. There

may be a true delineation between broad- and narrow-

crowned broad-toothed ‘makos’; however, based on the

arguments of Leriche (1926) and Ward and Bonavia

(2001), we agree that the name I. xiphodon is inappropri-

ate and use C. hastalis for all forms of broad-toothed

‘makos’ at the present time.

The species I. escheri was originally placed in the genus

Oxyrhina and later Isurus as a variant of C. hastalis (Agas-

siz 1833–1844; Leriche 1926; Casier 1960). Specimens

have been reported from the late Middle Miocene

through the Early to Middle Pliocene (c. 14–4 Ma) of the

northern Atlantic (including Germany, Belgium, the

Netherlands and Denmark) with materials ranging from

isolated teeth to an associated set of teeth and vertebrae

from northern Germany (Agassiz 1833–1843; Leriche

1926; Van den Bosch et al. 1975; Nolf 1988; Mewis and

Klug 2006; Mewis 2008). The crenulations on the cutting

edges of the teeth are much finer than the serrations of

C. carcharias specimens found in the Pacific basin and

tend to be along the entire cutting edge of the tooth (Ler-

iche 1926; Van den Bosch et al. 1975; Nolf 1988). In

addition to crenulations, some specimens may exhibit 1–3

pairs of lateral cusplets, which are more pronounced in

the lower teeth (Mewis 2008).

The crown shape of I. escheri is less dorsoventrally flat-

tened and thinner anterodorsally with a stronger distal

inclination than either C. hastalis or Carcharodon (Fig. 5).

This inclination is a result of a marked change in direction

A B C

D

E

F IG . 4 . Comparison of serration types. A, Carcharodon hastalis (UF 57267). B, Carcharodon hubbelli (UF 226255). C, Isurus escheri

(UF 245058). D, Carcharocles megalodon (UF 217225). E, Carcharodon carcharias (G. Hubbell collection). Scale bar represents 10 mm.


of the distal cutting edge of the tooth crown and appears

to be more pronounced in lateral teeth. The roots of the

upper teeth also appear to be more lobate and angular

than either C. hastalis or Carcharodon, which have very

square, rectangular roots (Ehret et al. 2009a). The teeth of

I. escheri appear to have stronger affinities with a more

narrow-toothed form of C. hastalis, whereas the vertebral

centra reported from Germany appear to have the typical

amphicoelous lamniform morphology that is not diagnos-

tic for refined taxonomic assessment above the ordinal

level (Mewis and Klug 2006; Mewis 2008).

While the latter hypothesis more accurately portrays

the evolutionary history of Carcharodon, the designation

of I. escheri as a sister taxon to C. carcharias based on cla-

distic analysis of dental characters by Mewis (2008) could

be misleading. Shimada (2005) has shown that cladistic

analysis combining both dental and nondental characters

of extant and fossil shark taxa generates considerable phy-

logenetic noise. Comparisons of consensus trees using

dental characters versus trees combining dental and all

other morphological characters result in different topolo-

gies. Tree statistics for the cladogram just using nondental

characters were better than those combining dental and

nondental characters (Shimada 2005). Shimada did

acknowledge, however, that patterns indicated that dental

characters are important for at least some phylogenetic

signal. A review of the analysis by Mewis (2008) reveals

that three of the synapomorphies uniting I. escheri and

C. carcharias relate to the presence of serrations, which

have evolved numerous times in the Lamniformes, while

two others are dependent on correct tooth position

assignment of disarticulated specimens. Additionally, the

restricted fossil distribution of I. escheri to the Northern

Atlantic and Mediterranean does not support the earliest

Pliocene occurrences of C. carcharias in the Pacific, while

appearances of the white shark are slightly later in the

Atlantic.

In contrast to I. escheri, the evolution of the white shark

in the Pacific during the Late Miocene and Early Pliocene

(c. 10–4 Ma) is well documented in the fossil records of

Peru, Japan, California, Australia and Chile (Muizon and

DeVries 1985; Kemp 1991; Long 1993; Tanaka and Mori

1996; Stewart 1999, 2002; Yabe 2000; Nyberg et al. 2006;

Ehret et al. 2009a). Based on the rich fossil record and the

rejection of I. escheri as a sister taxon to C. carcharias, we

agree more with the second origin hypothesis outlined

above but propose a Pacific Basin origin for the genus

Carcharodon with C. hastalis as a closely related taxon.

Furthermore, we designate a new species of Carcharodon

from the Pacific basin that represents an intermediate

form between C. hastalis and C. carcharias.

Institutional abbreviations. UF, Florida Museum of Natural His-

tory (FLMNH) University of Florida; USNM, United States

National Museum; MUSM, Museo de Historia Natural Javier

Prado, Universidad Nacional Mayor de San Marcos, Lima, Peru.

Terminology and anatomical abbreviations. Following Cappetta

(1987) and Siverson (1999), specifically we define intermediate

teeth as those that form on the intermediate bar, vary in number

and are less than one half the crown heights of the anterior

teeth.

SYSTEMATIC PALAEONTOLOGY

Class CHONDRICHTHYES Huxley, 1880

Subclass ELASMOBRANCHII Bonaparte, 1838

Order LAMNIFORMES Berg, 1958

Family LAMNIDAE Muller and Henle, 1838

Genus CARCHARODON Smith in Muller and Henle, 1838

Remarks. Glikman (1964, p. 104) placed the genera Car-

charodon and Cosmopolitodus within the Carcharodontidae

(Gill, 1893; mis-cited as 1892 in Glikman) based on the

A

C D

B

F IG . 5 . Isurus escheri from the Delden Member (Early

Pliocene), the Netherlands. A–B, Upper Anterior tooth, UF

245058. A, Labial view. B, Lingual view. C–D, Upper Lateral

tooth, UF 245059. C, Labial view. D, Lingual view. Scale bar

represents 10 mm.


following characters: teeth broad and blade-like, crowns of

upper lateral teeth dorsoventrally flattened, neck very small,

roots short, base of the tail with keels. The idea of the Car-

charodontidae was also raised separately by Whitley (1940)

and supported by Applegate and Espinosa-Arrubarrena

(1996), who cited anatomical evidence including fin posi-

tions (but did not explicitly list the characters) and the pres-

ence of serrations and lateral denticles as synapomorphies.

However, the characters of the Carcharodontidae listed by

Glikman (1964) are not synapomorphies specific to Car-

charodon. Furthermore, the separation of the Otodontidae

from the Lamnidae and the presence of a weakly crenulated

I. escheri do not restrict serrations and lateral cusplets to

the Carcharodontidae, and therefore, the family is not

supported. Glikman (1964) also differentiated the genus

Cosmopolitodus from Carcharodon based on the absence of

serrations and lateral cusplets.

Carcharodon hubbelli sp. nov.

Figure 6

Derivation of name. Named in honour of Dr. Gordon Hubbell

of Gainesville, Florida, in recognition of the substantial contribu-

tion he has made to the field of shark palaeontology.

Holotype. UF 226255 (Fig. 6), an articulated dentition including

222 teeth, 45 vertebral centra, portions of the left and right Mec-

kel’s cartilages and palatoquadrates, and neurocranium.

Type locality. Sud Sacaco (West) (15�33¢S, 74�46¢W), 5 km east

of Lomas, Arequipa Region, Peru. Nearly 20–40 cm above the

vertebrate-bearing tuff bed, Pisco Formation; Upper Miocene.

Referred specimens. Upper teeth (UF 245052–245057; Fig. 9).

These teeth were recovered from the type locality (Sud Sacaco

West), above the vertebrate-bearing tuff bed.

Diagnosis. A lamnid shark that differs from all other

lamnids by the following unique combination of dental

characteristics: (1) An A3 tooth distally inclined; (2) an

A1 tooth that is the largest tooth in the dentition and is

symmetrical; (3) an A2 tooth that is slightly larger than

the a2 tooth; (4) serrations present but not fully devel-

oped.

Description. The mandibular arch of UF 226255 is partially pre-

served, making it not possible to distinguish some features of

the jaws. The left and right palatoquadrates are preserved anteri-

orly along with the symphysis. The symphysis of both palatoqua-

drates is square and deep. The upper dental bullae are also

preserved in both palaquadrates. Within these bullae, the upper

F IG . 6 . Carcharodon hubbelli, UF

226255 (holotype). Scale bar represents

10 cm.


anterior teeth are found within a hollow, with an intermediate

bar, or a labiolingual constriction of the cartilage, present

between the third anterior tooth and the first lateral tooth. The

distal portions of both palatoquadrates are not preserved, and

the medial and lateral quadratomandibular joints are not dis-

cernable due to the dorsoventral flattening of the specimen.

The Meckel’s cartilages are much deeper than the palatoqua-

drates. The posterior portions of both are highly fragmented,

making the original shape impossible to discern. The lower sym-

physis is preserved; however, it is less deep than the symphysis

of the palatoquadrates. The Meckel’s cartilages are situated much

lower than the palatoquadrates, suggesting a subterminal mouth.

Portions of the neurocranium are preserved; however, the

structure is not discernable due to the dorsoventral flattening of

the specimen. The occipital hemicentrum consists of the poster-

ior half of a calcified double-cone centrum, which articulates

with the anteriormost centrum of the vertebral column. Other

portions of sheet-like cartilage are preserved within the gape of

the jaws; however, it is not identifiable. Based on the position

and preservation, they most likely represent the basal plate of

the neurocranium. Other openings within these fragments of

cartilage could represent foramina; however, due to the preserva-

tion, they probably represent areas of weathering.

The dentition of C. hubbelli is represented by 222 teeth

located on the palatoquadrates and Meckel’s cartilages. The teeth

are flattened labiolingually, and triangular in shape (Fig. 7). The

crowns have a slight convex curve lingually. There are five to six

tooth series present for each tooth position. The teeth are weakly

serrated, with anterior teeth averaging more than 30 serrations

per side for anterior to no serrations for the distal-most laterals.

Of the teeth that do have serrations, there is an average of 8–12

serrations per centimetre on both edges of each tooth. Basal ser-

rations on the teeth are larger than the other serrations on the

edges.

There are three anterior teeth present in each palatoquadrate.

The A1 is symmetrical, and it is the largest in the tooth in the

dentition. The A2 is also symmetrical and is slightly larger than

the a2, while the A3 is distally inclined. The upper lateral teeth

are also inclined distally (with L1 having the greatest inclination)

and get progressively smaller towards the distal edge of the jaw.

The roots of the teeth are relatively flat and rectangular in shape.

In the Meckel’s cartilages, there are three anterior teeth pres-

ent. Overall, the lower teeth have crowns that are more slender

than those of the uppers. There is very little inclination seen in

any of the lower teeth. As in the uppers, the teeth of the Mec-

kel’s cartilages are progressively reduced distally. The roots of

the lower teeth have a deep basal concavity and are thicker than

those of the upper teeth, being somewhat lobate.

There are 45 vertebral centra of UF 226255 preserved in the

holotype. These centra are laterally compressed and are com-

posed of two calcified cones connected by radiating calcified

lamellae within the intermedalia (Fig. 8). These centra are as-

terospondylic. The articular surfaces are concave and show clear,

calcified lamellae as well as pits in the centre that represent the

A

B

C

D

F IG . 7 . Functional tooth series of Carcharodon hubbelli, UF 226255 (holotype). Scale bar represents 5 cm.


notochordal constricture (Ridewood 1921; Gottfried and Fordyce

2001). In UF 226255, the occipital hemicentrum followed by the

first 45 centra, which get larger in size in ascending order.

Remarks. Carcharodon hubbelli is an intermediate form

between Carcharodon hastalis and Carcharodon carcharias

and demonstrates a mosaic of characters from both spe-

cies. Tooth crowns of C. hubbelli are convex and curve

lingually similar to the crowns of C. hastalis. The serra-

tions of C. hubbelli are enlarged basally but weaker overall

than those of C. carcharias (but stronger than those seen

in I. escheri) and appear to be intermediate between the

unserrated C. hastalis and the coarsely serrated C. carcha-

rias (Fig. 4). The A2 is symmetrical and is slightly larger

than the a2, which are characters also seen in C. carcha-

rias (Compagno 2001). Whereas the A3 is distally

inclined, a character is found in C. hastalis. Therefore, the

taxa may be useful as chronospecies, because they are

diagnostically distinguishable by dental characteristics and

are beneficial for biostratigraphy. Specimens collected in

Upper Miocene deposits throughout the Pacific basin

exhibit morphological gradation of dental characteristics

from Carcharodon hastalis to C. hubbelli, and finally

C. carcharias in the Early Pliocene. The observable transi-

tion of species through geologic time is denoted here by

the designation of C. hastalis and C. hubbelli to the genus

Carcharodon (Smith in Muller and Henle, 1838), which is

given precedence over Cosmopolitodus (Glikman 1964).

Furthermore, the diagnosis of Cosmopolitodus by Glikman

is misleading since some Late Miocene C. hastalis teeth

may have basal serrations.

DISCUSSION

Geology and stratigraphy. The new absolute ages obtained

from molluscs recovered at many of the localities of the

Pisco Formation suggest that deposition of the strata,

now referred to the Pisco Fm, occurred earlier than

thought previously. The results have direct bearing on the

age of the holotype for C. hubbelli sp. nov. and evolution

of white sharks in the Pacific basin.

Previous dating of the tuff bed at Alto Grande within

the El Jahuay vertebrate horizon resulted in an age of

9.5 Ma based on K-Ar dating (Muizon and Bellon 1986;

Muizon and DeVries 1985). Analysis of 55 zircon grains

collected from the tuff bed at Alto Grande yielded 54 that

gave ages that were Neoproterozoic through Cretaceous,

which are obviously inherited or mixed detritus. One

grain gave a concordant crystallization age of 10 ± 1 Ma,

which could also be inherited and should be treated as an

upper limit for the horizon. The strontium ages of the

shell layers overlying the tuff bed yielded an age range of

9.03–6.51 Ma with a mean of 7.46 Ma (Fig. 2), which are

younger than those for the ash layer. However, the upper

limits of these ages are within the range for the other dat-

ing methods making these age estimates congruent with

previously published dates.

Mollusc samples analysed from the Montemar horizon

yield 87Sr ⁄ 86Sr dates of 8.70–6.45 Ma with a mean of

7.30 Ma. These ages are congruent with the estimation of

Muizon and DeVries (1985) based on the vertebrate and

invertebrate faunas (Fig. 2). While the resolution of the

A B

F IG . 8 . Vertebral centrum of Carcharodon hubbelli, UF 226255 (holotype). Scale bar represents 10 mm.


strontium data is not more precise than the estimate

based on the molluscan fauna, it does confirm a Late

Miocene age (Table 1). A Late Miocene (c. 8.7–6.5 Ma)

age based on the correlation of gypsum beds with Aguada

de Lomas, fossiliferous sandy siltstone with Sud Sacaco

(West) and calibration of molluscan fauna was postulated

by Muizon and DeVries (1985).

Both geochemical methods, zircon U-Pb and strontium

isotopic data, yield ages for the Sud Sacaco (West) level that

are 1–2 million years older than reported previously by

Muizon and DeVries (1985) and Tsuchi et al. (1988). Thus,

making a change of age for the Sud Sacaco (West) horizon

from the Early Pliocene to the Late Miocene (Gradstein

et al. 2004). At Sud Sacaco (West), a thick Dosinia bed was

sampled for strontium (Fig. 2). 87Sr ⁄ 86Sr dates for the bed

ranged from 10.77 to 2.50 Ma with a mean of 6.59 Ma

(Table 1). Additionally, the vertebrate-bearing tuff dis-

cussed in Muizon and DeVries (1985) was located and sam-

pled for zircon data. In total, 35 zircon grains were

analysed with a majority being inherited or mixed detrital

grains. Of the Oligocene and Miocene zircons identified,

the youngest grain is 7 ± 1 Ma and is probably the youn-

gest age of the depositional range for the tuff. It should also

be noted that the in situ holotype of Carcharodon hubbelli

(UF 226255) was recovered 20–40 cm above the base of the

vertebrate-bearing layer (Ehret et al. 2009a).

On the east side of Sud Sacaco (West) horizon,

approximately 10 m above the vertebrate-bearing tuff

layer, a shell bed containing abundant Ophiomorpha

(Lundgren, 1891) burrows was sampled for strontium

and yielded an age range of 6.35–5.47 Ma, with a mean

of 5.93 Ma (Fig. 2). Previous methods of calibrating the

Sud Sacaco (West) level include correlation of molluscs

with white shark (Carcharodon) fossils. Furthermore, the

reassignment of the shark fossils from C. carcharias

(Early–Middle Pliocene) to C. hubbelli (Late Miocene–

Early Pliocene) also correlates with the older age for the

horizon.

For the Sacaco horizon, mollusc samples were collected

near the Museo de Sacaco and yielded 87Sr ⁄ 86Sr dates of

6.76–4.86 Ma, with a mean of 5.89 Ma. This age is much

older than the underlying tuff bed dated at 3.9 Ma by

Muizon and Bellon (1980). Additional unpublished Ar–Ar

data from the Sacaco ash bed located on the floor of east-

ern side of Quebrada Sacaco (locality DV 514-2 Snee)

below the unconformity that separates Sacaco shell beds

from upper portion of sequence on the hillsides of Sacaco

yielded an age of 5.75 ± 0.05 Ma (Lawrence Snee, USGS,

sample collected 1987). These new Sr and Ar data are in

disagreement with and much older than the 3.9 Ma age

of Muizon and Bellon (1980). Therefore, the horizons

exposed at the Sacaco locality appear to be older than

previously recorded.

Taxonomy and evolution of Carcharodon. The taxonomic

evolution and placement of Carcharodon is a complex

A

G H I J K L

B C D E F

F IG . 9 . Individual upper teeth demonstrating the gradation of serrations from the Pisco Formation, Peru. Upper teeth from left to

right, UF 245052–245057. A–F, labial view; G–L, lingual view. Scale bar represents 10 mm.


subject that has been compounded by the lack of more

complete specimens and high levels of homoplasy in the

tooth morphology of many species. While a C. hastalis-

origin hypothesis has gained popularity in recent years,

the timing and transition from one taxon to the other

have remained unresolved. It is generally accepted that

C. carcharias is directly related to Carcharodon hastalis

and not the megatoothed sharks as previously discussed.

Isurus escheri from the Middle Miocene through Early

Pliocene of the Northern Atlantic has been suggested as a

possible sister taxon to C. carcharias, based mainly on the

presence of crenulations on the cutting edges of the teeth

(Fig. 4). However, these fossils are restricted to the

Northern Atlantic and Mediterranean and become extinct

just prior to or as a result of the appearance of C. carcha-

rias in the Atlantic by the mid-Pliocene. This species

likely evolved from an Atlantic population of slim-

toothed C. hastalis or hastalis-like taxon in the early Mio-

cene. Meanwhile, materials from the Miocene Pacific

Basin clearly demonstrate an intermediate form between

C. hastalis and C. carcharias that is significantly different

from I. escheri. The discovery and description of C. hub-

belli from the Late Miocene of Peru and the recalibration

of the Pisco Formation demonstrate the presence of ser-

rated forms in the Miocene and early Pliocene of the

Pacific, while there is general lack of specimens from the

Atlantic at the same period.

The distinction of C. hubbelli from I. escheri is vali-

dated by the morphological differences exhibited in UF

226255 and specimens of I. escheri examined from the

Delden Member (Early Pliocene), the Netherlands (UF

245058 and UF 245059) and the description of an associ-

ated specimen from Germany (Mewis and Klug 2006;

Mewis 2008). I. escheri has been identified from the Mid-

dle Miocene (c. 14 Ma) to at least the Early Pliocene

(c. 5–4 Ma) throughout Northern Europe. Van den Bosch

(1978, 1980) differentiates I. escheri from the late Miocene

as weakly crenulate and early Pliocene teeth as strongly

crenulate types. However, this difference was not quanti-

fied or figured in either of the studies and is inconsistent

with our Early Pliocene samples that demonstrate weak

crenulations (Fig. 5). C. hubbelli teeth show a progressive

increase in the number and overall coarseness of serra-

tions on their cutting edges from the Late Miocene to the

Early Pliocene that are distinctively different and appear

to evolve separately from I. escheri (Figs 4, 9). Addition-

ally, the in situ dentition of UF 226255 demonstrates a

mixture of characters expressed in both C. hastalis and

C. carcharias, supporting our revised C. hastalis-origin

hypothesis.

Isurus escheri, on the other hand, appears to be a sepa-

rate taxon more closely related to a narrow-crowned

C. hastalis or hastalis-like taxon. Tooth serrations (or in

this case crenulations) have evolved independently

numerous times throughout the evolution of the sela-

chians (Casier 1960; Cappetta 1987; Frazzetta 1988).

Based on the living mako sharks, their tooth shape and

overall body size, it is hypothesized that species within

the genus Isurus were piscivorous (Applegate and Espin-

osa-Arrubarrena 1996; Purdy et al. 2001; Aguilera and de

Aguilera 2004). The evolution of serrations or crenula-

tions would be advantageous for competition with other

piscivorous shark taxa (C. hastalis, Galeocerdo (Muller

and Henle, 1837)), Hemipristis (Agassiz, 1833–1843) and

Carcharhinus (Blainville, 1816). Therefore, it is not sur-

prising that more than one form would acquire serra-

tions.

The evolution of the white shark in the Pacific Basin is

validated by the presence of weakly to moderately serrated

teeth in the fossil deposits from the Late Miocene and

Early Pliocene of North and South America, Asia and

Australia (Muizon and DeVries 1985; Kemp 1991; Long

1993; Tanaka and Mori 1996; Yabe 2000; Stewart 1999,

2002; Nyberg et al. 2006; Ehret et al. 2009a). While many

of these specimens from the Pacific represent different

degrees of evolution between C. hastalis and C. carcharias,

it is not possible to separate these based on isolated teeth.

A complete tooth set, exhibiting more definitive charac-

ters, would be required to differentiate potentially differ-

ent forms. Therefore, these teeth are assigned to the

species Carcharodon hubbelli; previous identifications as

I. escheri (Kemp 1993), Carcharodon sp. (Nyberg et al.

2006; Ehret et al. 2009a) or C. carcharias (Muizon and

DeVries 1985; Long 1993; Tanaka and Mori 1996) should

be amended to reflect this new assignment.

Additional research on C. hubbelli has shed light on the

palaeobiology of this species (Ehret et al. 2009a, b). Incre-

mental growth analyses of the vertebral centra of UF

226255 have revealed annular growth patterns that relate

to the life history of this specimen. Growth rings visible

using X-radiography appear to represent annual periodic-

ity based on the calibration of oxygen and carbon isotope

analysis within the rings. Counts of the growth rings

using the X-radiographs provide an age estimate of at

least 20 years. The overall length of the specimen was

estimated using the averages of both crown height and

vertebral centrum diameter regressions from previously

published studies of C. carcharias. Resulting data provide

total length estimates between 4.89 and 5.09 m. for the

specimen. Based on growth curves of modern C. carcha-

rias, UF 226255 appears to have been growing at a slower

rate than white sharks today.

Further palaeobiological information about C. hubbelli

includes a partial mysticete whale mandible from the SAS

layer containing a partial tooth crown MUSM 1470,

housed in the collection of the Museo de Historia Natural

Javier Prado, Universidad Nacional Mayor de San Mar-

cos, Lima, Peru (MUSM), described by Ehret et al.


(2009b). This specimen represents direct evidence of feed-

ing behaviour of the species in the Late Miocene. The

presence of tooth serrations and MUSM 1470 provides

definitive proof that C. hubbelli was adapted for taking

marine mammals as prey as early as c. 6.5 Ma.

CONCLUSIONS

The recalibration of fossil horizons within the Pisco For-

mation finds ages are older than previously published

(Muizon and Bellon 1980; Muizon and DeVries 1985;

Muizon and Bellon 1986). While these changes are not

exceptionally large, it does directly relate to the evolution-

ary history of the genus Carcharodon. The discovery and

description of an outstanding specimen from the Pisco

Formation further elucidate the taxonomy and palaeobi-

ology of the white sharks. The hypothesis that I. escheri is

a sister taxon of C. carcharias is refuted based on the

Miocene and Pliocene distribution of Carcharodon fossils

from the Pacific Basin and tooth morphology. The genus

name Carcharodon is proposed for the species hastalis,

hubbelli and carcharias based on dental characters shared

between the taxa discussed above, and our interpretation

of the C. hastalis-hubbelli-carcharias transition as an

example of chronospecies. Palaeobiological information

from UF 226255 reveals that this specimen grew at a rate

comparatively slower than modern white sharks. MUSM

1470 confirms that the diet of C. hubbelli was at least par-

tially comprised of marine mammals as early as the Late

Miocene. Continued research of these specimens and

newly discovered materials from the Pisco Formation and

other fossil localities will only further advance our knowl-

edge of the fossil lamnid sharks.

Acknowledgements. This research is supported by National Sci-

ence Foundation grants EAR 0418042 and 0735554. We espe-

cially thank Gordon Hubbell from Jaws International,

Gainesville, Florida, for donating UF 226255 to the Florida

Museum of Natural History as well as access to his collection

and his wealth of knowledge of fossil sharks. We thank M. Stuc-

chi from the Museo de Historia Natural of Lima, Peru, who

provided assistance in the field in 2007. We also thank M. Siver-

son from the Western Australian Museum, Welshpool, Western

Australia, and J. Bourdon of http://www.elasmo.com for discus-

sions and constructive suggestions for the improvement of this

manuscript. Thanks to E. Mavrodiev from the Florida Museum

of Natural History for assistance with Russian translations. We

also appreciate the comments from J. Bloch, R. Hulbert and J.

Bourque from the Florida Museum of Natural History and two

anonymous reviewers towards the improvement of this manu-

script. This is University of Florida Contribution to Paleobiology

627. Any opinions, findings, conclusions or recommendations

expressed in this paper are those of the author and do not nec-

essarily reflect the views of the National Science Foundation.

Editor. Adriana Lopez-Arbarello

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