This article was downloaded by: [Aston University]On: 11 January 2014, At: 13:20Publisher: Taylor & FrancisInforma Ltd Registered in England and Wales Registered Number: 1072954 Registered office: Mortimer House,37-41 Mortimer Street, London W1T 3JH, UK

Journal of Vertebrate PaleontologyPublication details, including instructions for authors and subscription information:http://www.tandfonline.com/loi/ujvp20

On the Eocene cichlids from the Lumbrera Formation:additions and implications for the NeotropicalichthyofaunaMaria C. Malabarba a , Luiz R. Malabarba a & Hernán López-Fernández b ca Departamento de Zoologia , Universidade Federal do Rio Grande do Sul , 91501-970 , PortoAlegre , Rio Grande do Sul , Brazilb Department of Natural History , Royal Ontario Museum , 100 Queen's Park, Toronto ,Ontario , M5S 2C6 , Canadac Department of Ecology and Evolutionary Biology , University of Toronto , 25 WillcocksStreet, Toronto , Ontario , M5S 3B2 , CanadaPublished online: 07 Jan 2014.

To cite this article: Maria C. Malabarba , Luiz R. Malabarba & Hernán López-Fernández (2014) On the Eocene cichlids fromthe Lumbrera Formation: additions and implications for the Neotropical ichthyofauna, Journal of Vertebrate Paleontology,34:1, 49-58, DOI: 10.1080/02724634.2013.830021

To link to this article: http://dx.doi.org/10.1080/02724634.2013.830021

PLEASE SCROLL DOWN FOR ARTICLE

Taylor & Francis makes every effort to ensure the accuracy of all the information (the “Content”) containedin the publications on our platform. However, Taylor & Francis, our agents, and our licensors make norepresentations or warranties whatsoever as to the accuracy, completeness, or suitability for any purpose of theContent. Any opinions and views expressed in this publication are the opinions and views of the authors, andare not the views of or endorsed by Taylor & Francis. The accuracy of the Content should not be relied upon andshould be independently verified with primary sources of information. Taylor and Francis shall not be liable forany losses, actions, claims, proceedings, demands, costs, expenses, damages, and other liabilities whatsoeveror howsoever caused arising directly or indirectly in connection with, in relation to or arising out of the use ofthe Content.

This article may be used for research, teaching, and private study purposes. Any substantial or systematicreproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in anyform to anyone is expressly forbidden. Terms & Conditions of access and use can be found at http://www.tandfonline.com/page/terms-and-conditions

Journal of Vertebrate Paleontology 34(1):49–58, January 2014© 2014 by the Society of Vertebrate Paleontology

ARTICLE

ON THE EOCENE CICHLIDS FROM THE LUMBRERA FORMATION:ADDITIONS AND IMPLICATIONS FOR THE NEOTROPICAL ICHTHYOFAUNA

MARIA C. MALABARBA,*,1 LUIZ R. MALABARBA,1 and HERNAN LOPEZ-FERNANDEZ2,3

1Departamento de Zoologia, Universidade Federal do Rio Grande do Sul, 91501-970 Porto Alegre, Rio Grande do Sul, Brazil,mariacslm@hotmail.com; malabarb@ufrgs.br;

2Department of Natural History, Royal Ontario Museum, 100 Queen’s Park, Toronto, Ontario M5S 2C6, Canada;3Department of Ecology and Evolutionary Biology, University of Toronto, 25 Willcocks Street, Toronto, Ontario, M5S 3B2, Canada,

hlopez fernandez@yahoo.com

ABSTRACT—The Lumbrera Formation is an Eocene unit cropping out in northwestern Argentina from which three cichlidspecies were recently described and represent the oldest Neotropical cichlid records: Proterocara argentina, Gymnogeophaguseocenicus, and Plesioheros chauliodus. The fossils come from a level interpreted as a perennial, low-energy, freshwater lakesurrounded by low relief and sporadically flooded vegetated areas. Sedimentological, paleontological, and absolute U/Pb zir-con dating studies suggest a lower Eocene age (∼48.6 Ma). Phylogenetic analyses place these cichlids as nested in the modernGeophagini and Heroini clades and attest to early differentiation from the basal cichlid lineages and a morphological con-servatism since at least the early Eocene (∼48.6 Ma). Molecular phylogenies calibrated with the Lumbrera Formation fossilssuggest that the age of cichlids may be considerably older than the minimum age provided by currently known fossils. In com-bination with well-established family-level phylogenetic relationships compatible with Gondwanan fragmentation, the originof the Cichlidae likely dates back to the Cretaceous. The occurrence of Eocene cichlid fossils in the same geographical areaas that of related modern lineages suggests that patterns of distribution and endemism of the Neotropical Cichlidae have anancient history. Here we describe additional cichlid specimens from the Lumbrera assemblage and evaluate their implicationsfor cichlid phylogeny and paleobiogeography.

INTRODUCTION

Cichlids are teleost fishes found chiefly in freshwaters thatform one of the largest vertebrate families and one of the mostspecies-rich percomorph clades, with more than 1600 species(Eschmeyer and Fong, 2012; Near et al., 2012). Due to thisremarkable diversity and associated ecological, morphological,and behavioral diversification, cichlids constitute a model forstudying evolution. Recent estimates report more than 600species of Neotropical cichlids, many of them still undescribed(Kullander, 2003; Lopez-Fernandez et al., 2012). Contrasting withthe diversity of modern forms is a limited fossil record. Fossilcichlids are known from Africa, Europe, South America, theCaribbean, and the Near East (Eocene to Pliocene), but mostlyas fragmentary remains. The most notable African cichlid fossilsbelong to the Eocene genus Mahengechromis (Murray, 2000).In South America, cichlids are recorded for the Oligocene toMiocene of Brazil and the Eocene to Miocene of Argentina.

In recent years, a proliferation of phylogenetic studies, mainlyusing molecular data sets (e.g., Farias et al., 2000; Lopez-Fernandez, Honeycutt, Stiassny, et al., 2005; Lopez-Fernandez,Honeycutt, and Winemiller, 2005; Chakrabarty, 2006a; Concheiro-Perez et al., 2007; Musilova et al., 2008; Rıcan et al., 2008; Smithet al., 2008; Hulsey et al., 2010; Lopez-Fernandez et al., 2010;Chakrabarty and Albert, 2011) and new fossil discoveries(Murray, 2000; Malabarba et al., 2006, 2010; Malabarba andMalabarba, 2008; Perez et al., 2010), have elevated interest

*Corresponding author.

in the geological age and historical biogeography of cichlids.Although the fossil record extends to the early Eocene of SouthAmerica and Africa (Murray, 2000; Malabarba et al., 2006;Malabarba et al., 2010; Perez et al., 2010), phylogenetic analysesreveal reciprocal monophyly of the Neotropical and Africancichlid assemblages, which in turn are sister to an Indo-Malagasyradiation, suggesting that diversification among major cichlidlineages is compatible with vicariant divergence during Gond-wanan fragmentation in the Cretaceous. And although someanalyses that use fossils to calibrate molecular phylogenies havesuggested a Cretaceous or even late Jurassic age for the family(e.g., Genner et al., 2007; Azuma et al., 2008; Lopez-Fernandezet al., 2013), there is still ample discussion on the subject(e.g., Murray, 2001; Vences et al., 2001; Schwarzer, 2009; Nearet al., 2012; Wainwright et al., 2012). In this context, continuedcharacterization of the cichlid fossil record is paramount infurthering our understanding of the evolutionary history of thefamily.

The cichlid fauna from the level known as Faja Verde in theLumbrera Formation (northwestern Argentina) plays an interest-ing role for understanding the evolution and diversification timesof the Cichlidae. Considering its location and age (Eocene, ∼48.6Ma), detailed study and accurate phylogenetic assignment of thesefossils provide essential calibrations for dating the divergence ofcichlids (e.g., Lopez-Fernandez et al., 2013). These well-preservedfossils also complement our understanding of the evolution of ci-chlid ecomorphology by offering a window into the environmentsin which modern lineages may have originated.

Three cichlid species have been described from the Lumbr-era Formation: Proterocara argentina Malabarba, Zuleta, and Del

49

Dow

nloa

ded

by [

Ast

on U

nive

rsity

] at

13:

20 1

1 Ja

nuar

y 20

14

50 JOURNAL OF VERTEBRATE PALEONTOLOGY, VOL. 34, NO. 1, 2014

Papa, 2006, Gymnogeophagus eocenicus M. Malabarba, L. Mal-abarba, and Del Papa, 2010, and Plesioheros chauliodus Perez,Malabarba, and Del Papa, 2010, whose phylogenetic positionswere found (Malabarba et al., 2006, 2010; Smith et al., 2008; Perezet al., 2010) to be relatively derived within the Neotropical Cichli-nae (sensu Smith et al., 2008). The examination of new materialfrom this same level has revealed the presence of more cichlidfishes, confirming cichlids as a major component of this ichthy-ofauna. In this paper, we describe an additional specimen of G.eocenicus and a new cichlid specimen possibly also assigned to theGeophagini, and discuss the implications of this early fauna for thecichlid phylogeny, paleobiogeography, and evolutionary diversifi-cation.

MATERIALS AND METHODS

The two fossil specimens described here are both preserved asimpressions in lateral view, presenting some distortion and crush-ing. They were collected in the Faja Verde of the Lumbrera For-mation at the Alemania locality in northwestern Argentina (Fig. 1)and are deposited in the collection of the Universidad Nacionalde Salta (CNS-V), in Salta, Argentina. The Faja Verde levels aremade up of greenish shales deposited in a lacustrine environment(see below; Del Papa et al., 2002).

The specimens were cleaned using brushes and needles undera stereomicroscope. Anatomical illustrations were prepared usinga camera lucida and a digital camera attached to a dissecting mi-croscope. To optimize the observation and interpretation of theanatomical structures, silicone peels were made. Peels and fossilswere sprinkled with ammonium chloride (NH4Cl) to improve thevisualization of the described structures.

Measurements were made using a digital caliper with the datarecorded to 0.1 mm. Measurements follow Reis and Malabarba

FIGURE 1. Map showing the location of the collecting site (blacksquare).

(1988) and Casciotta and Arratia (1993). Fin spines are indicatedby upper case Roman numerals and soft rays by Arabic numer-als. General osteological terminology follows Reis and Malabarba(1988) and Kullander and Nijssen (1989). The terminology, mea-surements, and angles adopted for jaw descriptions follow Cas-ciotta and Arratia (1993). The term ‘coulter area’ (Casciotta andArratia, 1993a) indicates the portion of the suspensorium formedby the base of the anguloarticular and the retroarticular. Sys-tematic nomenclature follows Smith et al. (2008), with Neotrop-ical cichlids referred to as the subfamily Cichlinae, which includesseven tribes: Astronotini, Chaetobranchini, Cichlasomatini, Cich-lini, Geophagini, Heroini, and Retroculini. Also following Smithet al. (2008), for informal suprageneric names we use the suffixes-ine(s) for subfamilies (e.g., ‘cichlines’ for Cichlinae) and -in(s) fortribes (e.g., ‘heroins’ for Heroini).

Institutional Abbreviations—CNS, Universidad Nacional deSalta, Salta, Argentina; MCP, Fish collection, Museu de Cienciase Tecnologia, Porto Alegre, Brazil.

Comparative Material—†Gymnogeophagus eocenicus, holo-type, CNS-V10024; †Proterocara argentina, holotype, CNS-V10020A/B; †Plesioheros chauliodus, holotype, CNS-V10026.Cleared and stained extant specimen: Gymnogeophagus sete-quedas, MCP 11903.

SYSTEMATIC PALEONTOLOGY

TELEOSTEI Muller, 1845CICHLIDAE Gill, 1872

GEOPHAGINI Haseman, 1911GYMNOGEOPHAGUS EOCENICUS

(Figs. 2–4)

Gymnogeophagus eocenicus M. Malabarba, L. Malabarba, andDel Papa, 2010 (description and phylogeny, Lumbrera Forma-tion in Argentina).

Material—CNS-V10027, an articulated almost complete speci-men, lacking parts of dorsal, anal, and caudal fins.

Description

Morphometric data for CNS-V10027 are summarized in Ta-ble 1. CNS-V10027 is a small (44 mm SL), elongate cichlid, withgreatest body depth (42.97% SL) in the region of pelvic fin inser-tion. The lateral profile is more convex dorsally than ventrally. Theskull is roughly triangular in lateral view, slightly deeper than long.The predorsal contour is steep, straight ascending to the supraoc-cipital crest, which contributes significantly to the skull height.Posterior to this point, the contour is gently arched until the dor-sal fin origin and descends along the dorsal fin base. The caudalpeduncle profile is not observable. The ventral contour, from thelower jaw to the anal fin origin, is only slightly curved; anal fin baseascending, slightly convex.

Neurocranium—The skull is preserved as an impression inlateral view, but distortion and crushing precludes clear interpre-tation of several bones. On the skull roof, a shallowly, completelypreserved, grooved frontal bears four sensory canal foramina(NLF 0–3); the frontal ridges are divergent anterior to NLF 0.Posteriorly, the frontal contacts the parietal laterally and thesupraoccipital medially. The supraoccipital bears a relatively highcrest, which extends anteriorly to the level of the posterior borderof the orbit. A conspicuous frontoparietal crest begins medial tothe NLF 3 and continues caudally over the parietal to the epioticfacet of the posttemporal. The slightly rotated preservationallowed us to identify the bones in the otic region, but the detailedanatomy was lost. The pterosphenoid has a small and pointed ros-tral oriented projection. The sphenotic-pterotic canal is short and

Dow

nloa

ded

by [

Ast

on U

nive

rsity

] at

13:

20 1

1 Ja

nuar

y 20

14

MALABARBA ET AL.—EOCENE NEOTROPICAL CICHLID FAUNA 51

TABLE 1. Morphometrics and meristics of G. eocenicus CNS-V10027and CNS-V10024 (holotype) and the geophagin CNS-V10029.

CNS- CNS- CNS-Character V10027 V10024 V10029

Standard length (mm) 48.54 56.84 45.24Percent standard length

Greatest body depth 40.77 38.52 37.64Head length 39.47 41.39 34.39∗Head depth 39.14 37.15 —Snout to anal fin origin 70.16 65.05 62.51Snout to dorsal fin origin 37.74 42.81 —Snout to pelvic fin origin 47.96 47.36 37.33Anal fin base length 19.46 17.11 18.98Caudal peduncle length 12.66 14.21 17.86Caudal peduncle depth 15.36 15.28 15.64Pelvic fin length — 25.19Pectoral fin length — 25.66 25.81Basipterygium 12.60 —Pelvic spine 13.61 12.03 15.47

Percent head length

Snout length 30.65 33.86 —Eye diameter 21.63∗ 21.94 20.37∗Preorbital length 36.40Postorbital length 45.35 48.40 61.05Ascending arm of premaxilla 34.25∗ 35.38 —Dentigerous arm of premaxilla 22.32 22.76 12.72Anguloarticular length 27.79 30.91Anguloarticular depth 24.31Coulter area depth 11.58 17.73Coulter area width 10.90 8.54

Counts

Dorsal fin spines >11 14 >9Dorsal fin soft rays 11–12 12Anal fin spines 3 3 3Anal fin soft rays 9 9Pectoral fin rays 13 13Vertebrae abdominal/caudal 12/15 12–13/15 >10/15Lateral line scales upper/lower sections 15–16/13

Asterisks indicate approximated values.

angled. A slender lateral commissure in the prootic is preservedas well as the trigeminal and hyomandibular nerve foramina. Thehyomandibular shell is elongated and weakly concave. The ba-sisphenoid is narrow, with no laminar expansions, and articulateswith the parasphenoid. Anteriorly, the supraorbital sensory canal(NLF 1) is followed by a tubular nasal with a lateral wing.

The preorbital region is badly damaged with dislocated andmissing bones, which prevent us from determining outline of theorbit. Therefore, although we can identify a mesethmoid, and awell-developed lateral ethmoid, their position and relation withother bones cannot be accurately determined.

Infraorbital Series—The lachrymal is slightly deeper than wideand bears four sensory canal pores; there is a deep anterodorsalincision for articulation with the process of the lateral ethmoid.Only two infraorbital elements are preserved: the most anterior isadjacent to lachrymal and the other is attached to the sphenotic.

Jaws and Suspensorium—Upper and lower jaws are reasonablywell preserved. The premaxilla is robust, with its ascending anddentigerous arms forming a nearly right angle. The ascending armof the premaxilla is wide at its base, with an oval-shaped rostralforamen; its dorsal tip is not visible, preventing us from deter-mining its length. The dentigerous arm is long and slightly curved.There are no teeth preserved on the premaxilla, but two rows ofalveoli can be seen along the two-thirds of its oral border. Themaxilla is relatively long, with a well-developed anterior end andshort ventral process.

The two lower jaw rami are preserved. The left ramus is en-tirely visible in lateral view; the ventral region of the right ramus isseen in mesial view, below the left one. The articulation betweenthe quadrate and the lower jaw is roughly below the midpoint ofthe orbit. There are five mandibular canal foramina on the den-tary, and impressions of two small unicuspid teeth (0.8 mm) inits symphyseal region. The sharp and narrow primordial processis slightly anteriorly directed. The coulter area is almost as deepas long, bearing an elongate postarticular process adjacent to thequadrate articular facet. The alpha angle is 95◦.

The hyomandibular has a long shaft that expands dorsally andbears three articulation facets. The metapterygoid is large, with a

FIGURE 2. CNS-V10027, Gymnogeophagus eocenicus, as preserved. Scale bar equals 5 mm.

Dow

nloa

ded

by [

Ast

on U

nive

rsity

] at

13:

20 1

1 Ja

nuar

y 20

14

52 JOURNAL OF VERTEBRATE PALEONTOLOGY, VOL. 34, NO. 1, 2014

very irregular anteroventral border; its dorsal border is concealedby a dislocated fragment of the parasphenoid. The quadrate hasthe typical triangular shape, with a strong and elongate condyle.Its anterior border is attached to the ectopterygoid, which has anarrow rostral projection for articulation with the palatine. Onlypart of the palatine maxillary process can be seen anterior to thelachrymal.

Opercular Apparatus—The opercle is roughly triangular, withsome impressions of cycloid scales over it. The preopercle is ‘L’-shaped, with the vertical arm much longer than the horizontal,forming a rounded right angle. The preopercular sensory canal hastwo terminal and four medial pores; only the third pore from theanterior-most forms a distinct branch. The opercular bones havesmooth borders.

Hyoid Series—Remains of the urohyal and a ceratohyal are pre-served as impressions below the interopercle. The urohyal showsthe anterior part of a dorsocaudally directed process. A small por-tion of the anterior ceratohyal showing the symphyseal articulararea is preserved, along with a few detached branchiostegals.

Vertebrae—Twenty-eight vertebrae can be counted: 13 abdom-inal and 15 caudal. There is no sign of supraneurals. Because thenape is well preserved, it is assumed that CNS-V10027 lacks supra-neural bones.

Fins and Supports—All fins are incompletely preserved. Onlythe anterior 12 spines of the dorsal fin are observable; they in-crease in length from the first to the fifth. The first dorsal ptery-giophore has a blunt, anteriorly directed process adjacent to thebase of the spine (Fig. 4). The pectoral girdle is represented byparts of the posttemporal, supracleithrum, cleithrum, coracoid,and scapula, the latter bearing a median foramen; pectoral fin rayscannot be counted. Both pelvic fins are preserved in ventral view,partly overlapping. The basipterygia are triangular, with short andnarrow median processes; pelvic fin rays I+5. The base of the analfin is missing, including the articulation between the first pterygio-phore and its spine; anal fin rays III+8. The caudal fin is poorlypreserved.

Scales—Impressions of moderately large cycloid scales are scat-tered over some regions of the head and body. The lateral lineis divided into two segments: the upper segment begins next tosupracleithrum region and extends posteriorly, ascending gradu-ally and terminating at the vertical between the third and fourthcaudal vertebrae. The lower section of the lateral line begins im-mediately below the sixth caudal vertebra and passes posteriorlyclose to the vertebral column until entering the caudal peduncle; itcontinues crossing the hypurals and appears to terminate betweenrays D1 and D2. The quality of the preservation does not allowlateral line scales to be counted.

Remarks—Amongst cichlids, the absence of supraneurals israre and considered a derived character state (Cichocki, 1976;

← FIGURE 3. CNS-V10027, G. eocenicus, skull in lateral view. A, orig-inal fossil; B, cast in latex (reversed) sprinkled with ammonium chloride;C, interpretative drawing. Abbreviations: br, branchiostegal rays; ca, coul-ter area of the right anguloarticular; ce, ceratohyal; ec, ectopterygoid; en,endopterygoid; ep, epioccipital; ex, exoccipital; f, frontal; fp; first dorsalfin pterygiophore; h, hyomandibular; i6, infraorbital 6; io, interopercle; l,lachrymal; la, anguloarticular; lc, left cleithrum; ld, left dentary; le, lateralethmoid; m, maxilla; mc, foramina of the mandibular canal in the dentary;mt, metapterygoid; n, nasal; np1–3, neurocranial lateral line pores 1–3; op,opercle; pa, parasphenoid; pl, palatine, pm, premaxilla; po, preopercle; pp,posttemporal; pr, prootic; ps, pterosphenoid; pt, pterotic; q, quadrate; ra,retroarticular; rc, right cleithrum; rd, right dentary; s, sympletic; sc, supra-cleithrum; sn, sphenotic; so, subopercle; sp, scapula; st, supraoccipital; ur,urohyal. Scale bar equals 2 mm.

Dow

nloa

ded

by [

Ast

on U

nive

rsity

] at

13:

20 1

1 Ja

nuar

y 20

14

MALABARBA ET AL.—EOCENE NEOTROPICAL CICHLID FAUNA 53

FIGURE 4. Predorsal region in species of†Gymnogeophagus. A, †Gymnogeophaguseocenicus holotype, CNS-V10024; B, †G.eocenicus, CNS-V10027, identified in this paper(reversed); C, the extant G. setequedas. Ante-rior to right. Abbreviations: ds, dorsal fin spine;fsd, forward spine in the first dorsal pterygio-phore; ns, first neural spine; soc, supraoccipitalcrest.

Stiassny, 1991; Kullander, 1998). Lack of supraneurals and thepresence of a rostral projection in the first dorsal fin pterygio-phore, as observed in this specimen, are two synapomorphies thatdefine the genus Gymnogeophagus (Fig. 4; Gosse, 1976; Reis andMalabarba, 1988; Kullander, 1998, Lopez-Fernandez, Honeycutt,Stiassny, et al., 2005). Although not diagnostic, the presence ofcycloid scales on the operculum is also congruent with conditionin Gymnogeophagus (Lopez-Fernandez, Honeycutt, Stiassny,et al., 2005).

The specimen CNS-V10027 was compared with the holotype(CNS-V10024) of G. eocenicus. The two counts available for com-parison, number of vertebrae and anal fin spines, are equal in bothspecimens. Also, the morphometric data of both specimens arevery similar (Table 1), with only a small variation between themthat may be expected among individuals of the same species (com-pare with morphometric variation among individuals of sevenspecies of Gymnogeophagus described in table 3 of Reis and Mal-abarba, 1998; data therein expressed as ratios instead of percent-ages). These similarities and the lack of characters to support thatthey belong to different species lead us to assign the specimenCNS-V10027 to †G. eocenicus.

GEOPHAGINI Haseman, 1911Gen. et sp. indet.

(Figs. 5, 6)

Material—CNS-V10029, an articulated individual preserved asimpression in lateral view, which it is missing (unpreserved) theanterodorsal region of the head, including part of the snout andskull roof.

Description

Morphometric data of CNS-V10029 are presented in Table 1.CNS-V10029 has an elongated body that reaches 45.24 mm in stan-dard length (SL). The greatest body depth is at the most anteriorpreserved point of the dorsal fin. From this point, the dorsal con-tour curves downward towards the caudal peduncle. The caudalpeduncle is longer than deep, with the dorsal and ventral edgesstraight and equal in length. The ventral body contour is slightlycurved in the gular region, becoming almost straight towards thecaudal fin.

Skull—The anterodorsal region, including snout, skull roof,supraoccipital crest, and dorsal fin origin, is missing. Although it isnot possible determine the shape and details of these parts, based

on the remaining elements (mainly the mandible), it is possible toinfer that the specimen had a very short head. The mouth is smalland terminal. Based on the preserved portion of the orbit, which isonly the posterior half, the orbit is large, measuring approximately5.3 mm in diameter.

The parasphenoid is narrow, with no expansion of the dorsalwing. Of the frontal, only the ventroposterior portion contactingthe parietal and pterosphenotic can be observed; a well-developedparietal crest is partially preserved. The sphenotic-pterotic canal isslightly inclined.

Infraorbital Series—There is a single lachrymal only partiallyvisible. It appears to be rectangular, wider than deep. Three open-ings are preserved in the lachrymal and in contact with infraor-bital 1, but not extended over it. Posteriorly to the lachrymal, thereare four infraorbitals; the anterior two with ventral laminar expan-sions. Infraorbital 2 is slightly curved with a central pore.

Jaws and Suspensorium—The mouth is ventrally located, ter-minal, and small. Because the anterior part of the snout is missing,it is not possible to determine if the jaws are equally sized or toestablish the anatomy of their symphysial regions. The dentiger-ous arm of the premaxilla is slightly curved ventrally. No teeth arepreserved.

The dentary is very short and deep, with the coronoid pro-cess partially concealed by the maxilla. It bears five mandibularcanal openings. The anguloarticular is nearly as deep (4.54 mm)as it is long (4.81 mm), with the primordial process pointed andprojecting slightly forward. The coulter area is rectangular, al-most as deep (2.23 mm) as wide (2.93 mm). The section of themandibular canal in the anguloarticular is short and slightly in-clined. The posterior border of the coulter area is slightly curved,with the retroarticular forming the ventral border. There are sometooth impressions in the oral border of the dentary, indicating thatteeth were conical, small, robust, and arranged in more than onerow.

The hyomandibular has a clear vertical crest and is dorsallyexpanded; it is ventrally sutured to the metapterygoid. Themetapterygoid is large, with irregular borders and surface. It isdorsally and posteriorly articulated with the hyomandibular. Theendopterygoid is mainly roundish with its border projected overthe quadrate. The quadrate is typically triangular, with the ante-rior border articulating with the ectopterygoid. The condyle of thequadrate articulates with the mandible at the level of the posteriorthird of the orbit. Only the posterior portion of the palatine, wherethe dermal splint contacts the ectopterygoid, is preserved.

Dow

nloa

ded

by [

Ast

on U

nive

rsity

] at

13:

20 1

1 Ja

nuar

y 20

14

54 JOURNAL OF VERTEBRATE PALEONTOLOGY, VOL. 34, NO. 1, 2014

FIGURE 5. CNS-V10029, Geophagini from the Lumbrera Formation as preserved. Scale bar equals 5 mm.

Opercular Apparatus—The preopercle is narrow, with the hor-izontal arm meeting the much longer vertical arm at a slightly ob-tuse angle. It is crossed longitudinally by the preopercle sensorycanal with two terminal and four medial pores, which is the condi-tion of most derived Neotropical cichlids (Kullander, 1986, 1998).The opercle is trapezoid, with a round posteroventral angle. Thesubopercle is narrow, with a long process projecting between theopercle and preopercle. The interopercle is partially concealedand displaced; its anterior margin bears an anterodorsal projec-tion. All opercle elements have smooth surfaces and borders and,except for the preopercle, they have impressions of cycloid scalescovering their surfaces.

Vertebrae—The nape and origin of the dorsal fin are missing,rendering it impossible to determine whether supraneurals arepresent or to count the exact number of precaudal vertebrae. Thevertebral column is slightly curved, with 27 vertebrae: 11 precau-dal and 16 caudal, but one or two anterior precaudal vertebraemay be missing.

Paired Fins and Girdles—Most of the pectoral girdle and fin ispreserved. Dorsally in the girdle, there are parts of the posttem-poral, the proximal (medial) extrascapular next to neurocranium,and supracleithrum all bearing sensory canals. The supracleithrumhas smooth margins. The cleithrum contours the opercle and sub-opercle, bearing a rounded and expanded lamina for the postclei-thrum articulation. The postcleithra are not visible, concealed bythe pectoral fin rays. The scapula and coracoid are barely visiblebut remain articulated to each other and to the four rectangularradials. The pectoral fin has 14 soft rays with a rounded outline;fifth and sixth rays are the longest.

Of the pelvic fin, only part of the basipterygium and first spine(15.47% SL) are preserved; it is not possible to determine theshape of the fin, but the longest rays reach the anal fin origin.

Median Fins—Because the most anterior dorsal fin spines aremissing, we cannot determine their exact number. There are atleast nine spines, followed by 12 branched rays; the spiny and softportions are continuous. The first three preserved spines are ofequal length; posteriorly they increase gradually in size and incontinuity with the soft portion until the eighth ray, forming apoint.

The caudal skeleton is concealed by the squamation, allowingonly the observation of the vertebral centra and uroneural. Theposterior border of the caudal fin is emarginated, with the lowerlobe slightly longer (29.35% SL) than the upper. There are 16 prin-cipal caudal rays (8+8); D8 and V8 rays are simple, whereas theinner rays are branched. Four dorsal procurrent rays are present.The caudal peduncle is very long containing eight vertebrae.

The anal fin has an acuminate margin, with the first soft raysthe longest; rays iii+9. The first two pterygiophores seem to forma single element that contacts the hemal spine of the first caudalvertebra dorsally and articulates with the two most anterior spinesventrally. The three anal fin spines increase in length caudally.

Squamation—The entire body is covered by large, mostly cy-cloid scales, with some ctenoid scales in the supratemporal regionand anteroventrally on the abdomen, below the pectoral fin. Thereare smaller cycloid scales on the dorsal and anal fins, arrangedmainly over the membranes between the soft rays. The caudal finis scaled at the base with small interradial scales. There are eightscale rows in the caudal peduncle. The opercle and subopercle arecovered with variably sized cycloid scales.

Lateral Line—As typical in cichlids, the lateral line in CNS-V10029 is divided in two segments: upper (anterior) and lower(posterior). The upper segment begins next to the supracleithrumand it extends caudally to approximately the level of the sixth softray. The lower section of the lateral line starts at about the seventhcaudal vertebra (approximately under the eighth soft dorsal ray),following close to the vertebral column to the caudal fin. Thereis no overlap of the upper and lower sections. There are 15–16tubed scales (impressions) in the upper and 13 in the lower lateralline section. Scale rows between upper lateral line and dorsal finare three anteriorly, one and one-half posteriorly; one horizontalscale series between lateral line sections.

Remarks—Although important characters are missing in CNS-V10029, it is distinguished from the other Lumbrera cichlid fossilsin being elongate with a very long caudal peduncle. Additionally,it can be unambiguously distinguished from other cichlids bythe combined meristic and morphometric attributes. We havetentatively ascribed this fossil to the tribe Geophagini based onthe presence of more than three procurrent caudal fin rays (char.

Dow

nloa

ded

by [

Ast

on U

nive

rsity

] at

13:

20 1

1 Ja

nuar

y 20

14

MALABARBA ET AL.—EOCENE NEOTROPICAL CICHLID FAUNA 55

84 of Kullander, 1998), and of five lateralis canal openings in thedentary, as opposed to the four generally observed in the tribesCichlasomatini and Heroini (Kullander 1986, 1998). Additionally,the presence of a first postlacrhymal infraorbital with a ventrallydirected laminar expansion is compatible with some clades ofGeophagini (see Lopez-Fernandez, Honeycutt, Stiassny, et al.,2005). Although these attributes are not sufficient for an unam-biguous diagnosis of Geophagini, the absence of synapomorphiessupporting other clades leaves Geophagini as the most parsi-monious interpretation of the fossil. Nevertheless, none of thesynapomorphies previously defined for Geophagini (Kullander,1998; Lopez-Fernandez, Honeycutt, Stiassny, et al., 2005; Smithet al., 2008) could be verified in CNS-V10029 and our assignmentmay warrant revision if additional specimens become available.

DISCUSSION

Geological Evidence: Age of the Lumbrera Formation

The Lumbrera Formation is the upper unit of the Salta Group,consisting of 300–500 m of continental deposits exposed in north-western Argentina (Fig. 1). An omission surface (20–30 cm thick)representing a sedimentary discontinuity horizon was recognizedand used to divide this formation into two informal members:lower and upper Lumbrera. The cichlid fauna discussed herecomes from the upper section of the lower Lumbrera, known asFaja Verde. Its greenish shales were deposited in a lacustrine envi-ronment. Sedimentological data from the Faja Verde section (DelPapa, 2006) support the interpretation of a lake of low energy, offreshwater chemistry and surrounded by low relief vegetated areassubject to sporadic flooding.

Traditionally, the Lumbrera Formation has been dated asCasamayoran South American land mammal age (SALMA) age,estimated primarily on the basis of the mammalian fossil record.Radiometric ages for the Casamayoran, which is divided in Va-can and Barrancan, are rare and controversial and it is conven-tionally regarded as early Eocene (Kay et al., 1999). This datingfor the Lumbrera Formation is mainly based on the similarities ofits mammal association with that of the Casamayoran in Patago-nia; however, there are no common taxa between these regions.The discontinuity recognized between upper and lower Lumbreramembers is also seen in the mammalian fossil associations: noneof the mammals recorded for the lower Lumbrera persists into theupper Lumbrera section (Del Papa et al., 2010).

However, recently, Del Papa et al. (2010) provided strong dat-ing evidence by identifying and dating radiometrically a continu-ous, white, 25-cm-thick layer of crystal tuff near the top of the up-per Lumbrera section. The calculated age for this layer is 39.9 ±0.4 Ma and serves as a minimum age for the end of the formation’sdeposition. Stratigraphically, this crystal-tuff layer is located 240 mabove the fossiliferous level (Del Papa et al., 2010). Additional in-direct evidence for dating the fossil layer comes from paleoclimaticinferences based on the study of alluvial paleosol horizons in the

← FIGURE 6. CNS-V10029, Geophagini, skull in lateral view. A, origi-nal fossil; B, cast in latex (reversed) sprinkled with ammonium chloride; C,interpretative drawing. Abbreviations: aa, anguloarticular; bp, basiptery-gium; br, branchiostegal rays; cl, cleithrum; d, dentary; ec, ectopterygoid;en, endopterygoid; ex, exoccipital; et, extrascapular; f, frontal; h, hy-omandibular; i2–5, infraorbital 2–5; ic, interclar; io, interopercle; l, lachry-mal; le, lateral ethmoid; m, maxilla; mc, foramina of the mandibular canalin the dentary; mt, metapterygoid; n, nasal; op, opercle; pm, premaxilla; q,quadrate; pa, parasphenoid; po, preopercle; pr, prootic; ps, pterosphenoid;pt, pterotic; q, quadrate; ra, retroarticular; s, sympletic?; sc, supraclei-thrum; sn, sphenotic; so, subopercle; v, vomer. Scale bar equals 2 mm.

Dow

nloa

ded

by [

Ast

on U

nive

rsity

] at

13:

20 1

1 Ja

nuar

y 20

14

56 JOURNAL OF VERTEBRATE PALEONTOLOGY, VOL. 34, NO. 1, 2014

Lumbrera Formation, where a stratigraphic fluvial section correl-ative to the Faja Verde Lake has been preliminarily assigned tothe Early Eocene Climatic Optimum (EECO; White et al., 2009).In conjunction, the evidence points to a lower Eocene, more pre-cisely upper Ypresian–lower Lutetian (∼48.6 Ma) age for the FajaVerde of the Lumbrera Formation (Perez et al., 2010).

Paleontological Evidence: The Lumbrera Cichlid Fauna

To date, the cichlid fauna from the Lumbrera Formation isknown from five articulated individuals from the Faja Verde lev-els, representing at least three species and two tribes of Cichlinae:the Geophagini and Heroini.

†Proterocara argentina, represented by a complete specimenpreserved as part and counterpart, was phylogenetically assignedto a basal position as sister group of the clade formed by thecichlasomatins, heroins, and geophagins, when described (Mal-abarba et al., 2006), based on the inclusion and analysis of the fos-sil species in the morphological matrix of Kullander (1998). Smithet al. (2008) further included Proterocara in their total evidenceanalysis, and the fossil species was recovered in an apical positionin the Geophagini, in a branch along with Crenicichla and Teleoci-chla.

†Gymnogeophagus eocenicus exhibits the synapomorphies ofthe genus Gymnogeophagus: lack of supraneurals associated witha forward-directed spine at the distal tip of the first dorsal ptery-giophore. Additionally, two characters observed in †G. eoceni-cus, the presence of 15 caudal vertebrae, and extended softdorsal fin rays (characteristic of mature males of some extantspecies), were mapped in a Gymnogeophagus phylogeny (Wim-berger et al., 1998), in order to assess its relationships amongthe extant species of the genus (Malabarba et al., 2010). The ob-tained results supported †G. eocenicus as more closely related tothe G. gymnogenys clade than to the G. rhabdotus clade. TheG. gymnogenys clade contains all mouth-brooding species of thegenus. To date, available evidence supports G. eocenicus as a stembranch of the G. gymnogenys clade, not allowing us to predictunambiguously the presence of a mouth-brooding habit for thespecies. †Gymnogeophagus eocenicus is known from two speci-mens, the holotype (Malabarba et al., 2010) and the specimen de-scribed in this paper.

The recently described species from Lumbrera, †Plesioheroschauliodus, was included in the Heroini (Perez et al., 2010) basedon the presence of canines much larger than the other teeth, andthe presence of a lingual subapical cusp on the outer anteriorteeth of the oral jaws (Kullander, 1996). This assignment was cor-roborated in a phylogenetic analysis that recovered †Plesioheros,closely related to Australoheros and to the deep-bodied SouthAmerican heroins (Perez et al., 2010).

The Lumbrera Fossils and the Patterns and Times of Divergenceof Neotropical Fishes

The Lumbrera Formation ichthyofauna, containing the oldestcichlid record, extends back the minimum age for the family, pre-viously set at the middle Eocene (46 Ma) based on Tanzanian ci-chlid fossils (Murray, 2000), to 48.6 Ma. As such, it plays an essen-tial role in understanding the evolutionary history of Neotropicalcichlids, and of the family as a whole. Moreover, considering thelocation of the fossils, their age, and the fact that they are morpho-logically modern, their insertion in a phylogenetic framework pro-vides valuable information for understanding the evolution and di-versification times of the Cichlidae. Recent methods allow for thetemporal calibration of molecular phylogenetic hypotheses usingfossil data (e.g., Drummond et al., 2006; Yang and Rannala, 2006;Ho, 2007; Inoue et al., 2010), and the Lumbrera fossils providekey calibration points for the dating of cichlids. Unlike other ci-

chlid fossils of comparable age (Murray, 2000), the Lumbrera fos-sils are assigned to extant clades. In particular, the assignment of†G. eocenicus to the living genus Gymnogeophagus is an extraor-dinary circumstance based on the presence of the two synapomor-phies that characterize the genus (see above). This assignment isalso supported, albeit indirectly, by the congruence between themodern distribution of the genus (restricted to the La Plata basinand the Atlantic slopes of southern Brazil, Uruguay, and northernArgentina) and the location of the fossil-bearing Lumbrera For-mation. Along with †Gymnogeophagus, the identification of Ple-sioheros chauliodus as a lineage nested within the modern cichlidtribe Heroini (Perez et al., 2010) and dating of the Faja Verde levelprovide minimum ages of divergence for the two most diverseclades of Neotropical cichlids, and arguably the two strongest in-ternal calibrations for the family. In addition, the Brazilian fossilsof the genus †Tremembichthys (34 Ma; Malabarba and Malabarba,2008) provides a calibration point for the Neotropical tribe Cichla-somatini, and Nandopsis woodringi from the Miocene of Hispan-iola (Chakrabarty, 2006b) potentially provides a second internalcalibration for Heroini.

The Lumbrera fossils provide novel insight into the ageof cichlids. A study by Lopez-Fernandez et al. (2013) used†Gymnogeophagus eocenicus, †Plesioheros chauliodus, and†Tremembichthys garciae to calibrate the 166-taxa phylogenypresented by Lopez-Fernandez et al. (2010), finding the originof cichlids to be middle Jurassic to early Cretaceous. This result,the oldest age for cichlids found through molecular studies todate, assumed that the origin of cichlids predates the separationof Gondwana, as suggested by various recent phylogenetic hy-potheses (e.g., Stiassny, 1991; Farias et al., 2000; Sparks, 2004;Chakrabarty, 2006a; Concheiro-Perez et al., 2007; Smith et al.,2008; Lopez-Fernandez et al., 2010). Despite some differences,all these analyses recover the major geographic cichlid assem-blages as monophyletic (African, Neotropical, Malagasy-Indian),supporting a vicariance model to explain the modern cichliddistribution. Although the ages recovered by Lopez-Fernandezet al. (2013) are not incompatible with some previous studies (e.g.,Genner et al., 2007; Azuma et al., 2008), younger dates for cichlidshave also been recently proposed (e.g., Genner et al., 2007; Santiniet al., 2009). Near et al. (2012) recovered an Oligocene–earlyMiocene age for the Malagasy-India clade, a result incompatiblewith the Gondwanan hypothesis assumed by Lopez-Fernandezet al. (2013). A more recent study of Heroini diversification(Rıcan et al., 2012) using the Lumbrera heroin †Plesioheroschauliodus found Heroini to be 39.9–48.6 Ma, an age at odds withthe original stratigraphic description that proposed 48.6 Ma asthe absolute minimum age for the fossil. The differences betweenthese estimates could be due to a variety of causes, including thefossil calibrations used or the assumptions underlying differentdating analyses (e.g., Ho, 2007; Inoue et al., 2010), as well asdifferences in rates of molecular evolution among loci used indifferent studies (e.g., Lukoschek et al., 2012;). Clearly then,and despite a number of recent studies, the time of origin ofcichlids remains unclear. Because of their excellent preservation,well-supported phylogenetic placement, and their early age, thecichlids of Lumbrera provide an extraordinary addition to thefossil record that should play a central role in furthering ourunderstanding of the age of cichlids.

The essentially modern status of the Lumbrera fossils requiresthat most of early cichlid evolutionary history occurred before48.6 Ma, as old as the early Eocene. The 46-Ma cichlids fromTanzania are also derived forms, probably closely related to mod-ern haplochromins or hemichromins (Murray, 2000; Sparks, 2004).Because their phylogenetic position has not been strongly estab-lished, they could be potentially closer to the root of the Africancichlid tree than the Lumbrera ones are in the Neotropical tree.

Dow

nloa

ded

by [

Ast

on U

nive

rsity

] at

13:

20 1

1 Ja

nuar

y 20

14

MALABARBA ET AL.—EOCENE NEOTROPICAL CICHLID FAUNA 57

Altogether, the derived position of these fossils suggests that thefamily is much older than implied by the current fossil record (andsee Lopez-Fernandez et al., 2013). In combination, the fossil agesand the higher-level phylogeny of the Cichlidae suggest a Creta-ceous age for the family, congruent with the timing and sequenceof the hypothesized vicariant events that associate cichlid diversi-fication with the Gondwanan fragmentation. Nevertheless, the ac-tual age of cichlids is far from clearly established and further studyis required.

Phylogenies based on molecular and total evidence analyses re-sulted in short branches at the base of the Geophagini and Hero-ini, suggesting the hypothesis that those groups underwent anearly and rapid adaptive radiation (Lopez-Fernandez, Honeycutt,Stiassny, et al., 2005; Lopez-Fernandez, Honeycutt, and Wine-miller, 2005; Lopez-Fernandez et al., 2010). Analysis of lineagediversification and phenotypic disparity through time stronglysupported an “ancient adaptive radiation” of the South Ameri-can Geophagini, with more recent increased phenotypic diversi-fication of Heroini in Central America (Lopez-Fernandez et al.,2013:1334). Because Gymnogeophagus is an ecomorphologicallyspecialized invertebrate feeder (Lopez-Fernandez et al., 2012), theLumbrera fossils also support the idea of early, adaptive evolu-tionary divergence among Neotropical cichlids.

A particularly interesting aspect of the Lumbrera fossils is theirmodern facies, suggesting that at least in some lineages certainmorphological attributes have been conserved for at least 50 mil-lion years. Although this evolutionary stasis seems unlikely, theoccurrence of the extant genus Corydoras (C. revelatus Cockerell,1925; but see Reis, 1998) in the Paleocene (∼65–55 Ma) MaızGordo Formation attests to an even longer period of stasis forother Neotropical fish lineages. Underlying the Lumbrera Forma-tion in this same region, the sediments of Maiz Gordo Forma-tion (Del Papa and Salfity, 1999) bear abundant, though invari-ably disarticulated, Corydoras remains (M.C.M., pers. observ.).The mid-Eocene Tanzanian cichlids, which are morphologicallynearly indistinguishable from modern African cichlids, representanother example of morphological conservatism dating to 46 Ma(Sparks, 2004). Widespread morphological stasis among cichlidsand other freshwater fish lineages suggests that adaptive traits andecological interactions that define the structure of modern tropicalfish communities were acquired much earlier than the establish-ment of modern fluvial environments (Lundberg, 1998; Lundberget al., 2011; Reis, 1998; Lopez-Fernandez and Albert, 2011; Lopez-Fernandez et al., 2012).

The cichlids from Lumbrera Lake rival those from Tanzania’sMahenge crater lake in age (46 Ma; Murray, 2000). In both places,the species are in some respects morphologically modern andphylogenetically derived. However, whereas in Lumbrera thereare different lineages represented, cichlid species in Tanzania areplaced in a single genus, suggesting that they already had the abil-ity to form species flocks (Murray, 2000). Species flock evolutionis common to the cichlids of the African lakes and have beenhypothesized to occur only in the geophagine Crenicichla amongNeotropical lineages (Kullander et al., 2010).

ACKNOWLEDGMENTS

The authors thank O. Zuleta for collecting the material of theLumbrera Formation presented here, and C. Del Papa (UNC)for loaning the material and for the critical reading of a previousversion of this paper. This work was partially funded by CNPq(M.C.M. and L.R.M.) grants. H.L.F. was supported by a Discov-ery Grant from the National Sciences and Engineering ResearchCouncil of Canada. Comments by P. Chakrabarty and an anony-mous reviewer helped to significantly improve the manuscript.

LITERATURE CITED

Azuma, Y., Y. Kumazawa, M. Miya, K. Mabuchi, and M. Nishida. 2008.Mitogenomic evaluation of the historical biogeography of cichlids to-ward reliable dating of teleostean divergences. BMC EvolutionaryBiology 8:215.

Casciotta, J., and G. Arratia. 1993. Jaws and teeth of American cichlids(Pisces: Labroidei). Journal of Morphology 217:1–36.

Chakrabarty, P. 2006a. Systematics and historical biogeography ofGreater Antillean Cichlidae. Molecular Phylogenetics and Evolution39:619–27.

Chakrabarty, P. 2006b. Taxonomic status of the Hispaniolan Cichlidae.Occasional Papers of the Museum of Zoology University of Michi-gan 737, 20 pp.

Chakrabarty, P., and J. S. Albert. 2011. Not so fast, a new take on theGreat American Biotic Interchange; pp. 293–305 in J. S. Albert andR. E. Reis (eds.), Historical Biogeography of Neotropical FreshwaterFishes. University of California Press, Berkeley, California.

Cichocki, F. P. 1976. Cladistic history of cichlid fishes and reproduc-tive strategies of the American genera Acarichthys, Biotodoma andGeophagus. Ph.D. dissertation, University of Michigan, Ann Arbor,Michigan, 356 pp.

Cockerell, T. D. A. 1925. A fossil fish of the Family Callichthyidae. Science62:697–698.

Concheiro-Perez, G. A., O. Rıcan, G. Ortı, E. Bermingham, I. Doadrio,and R. Zardoya. 2007. Phylogeny and biogeography of 91 species ofheroine cichlids (Teleostei: Cichlidae) based on sequences of the cy-tochrome b gene. Molecular Phylogenetics and Evolution 43:91–110.

Del Papa, C. 2006. Estratigrafıa y paleoambientes de la Formacion Lum-brera, Grupo Salta, noroeste argentino. Revista de la Asociacion Ar-gentina de Geologıa 61:15–29.

Del Papa, C., and J. A. Salfity. 1999. Non-marine paleogene se-quences, Salta group, Northwest Argentina. Acta Geologica Hispan-ica 34:105–121.

Del Papa, C., V. Garcıa, and M. Quattrocchio. 2002. Sedimentary faciesand palynofacies assemblage in Eocene perennial lake, LumbreraFormation, northwest Argentina. Journal of South America EarthSciences 15:553–569.

Del Papa, C., A. Kirschbaum, J. Powell, A. Brod, F. Hongn, and M. Pi-mentel. 2010. Sedimentological, geochemical and paleontological in-sights applied to continental omission surfaces: a new approach forreconstructing Eocene foreland basin in NW Argentina. Journal ofSouth American Earth Sciences 29:327–345.

Drummond, A. J., S. Y. W. Ho, M. J. Phillips, and A. Rambaut. 2006. Re-laxed phylogenetics and dating with confidence. PLoS Biol 4:e88.

Eschmeyer, W. N., and J. D. Fong. 2012. Species by Fam-ily/Subfamily. Available at http://research.calacademy.org/research/ichthyology/catalog/SpeciesByFamily.asp. Accessed October 18,2012.

Farias, I. P., G. Ortı, and A. Meyer. 2000. Total evidence: molecules, mor-phology, and the phylogenetics of cichlid fishes. Journal of Experi-mental Zoology 288:76–92.

Genner, M., O. Seehausen, D. Lunt, D. Joyce, P. Shaw, G. Carvalho, andG. Turner. 2007. Age of cichlids: new dates for ancient lake fish radi-ations. Molecular Biology and Evolution 24:1269–1282.

Gill, T. N. 1872. Arrangement of the families of fishes, or classes Pisces,Marsipobranchii, and Leptocardii. Smithsonian Miscellaneous Col-lections 247:1–49.

Gosse, J. P. 1976. Revision du genre Geophagus (Pisces, Cichlidae). Mem-oires de l’Academie Royale des Sciences d’Outre-Mer, Classe desSciences Naturelles et Medicales 19(3):1–173.

Haseman, J. D. 1911. Descriptions of some new species of fishes and mis-cellaneous notes on others obtained during the expedition of theCarnegie Museum to central South America. Annals of the CarnegieMuseum 7:315–328.

Ho, S. Y. W. 2007. Calibrating molecular estimates of substitution ratesand divergence times in birds. Journal of Avian Biology 38:409–414.

Hulsey, C. D., P. R. Hollingsworth Jr., and J. A. Fordyce. 2010. Tempo-ral diversification of Central American cichlids. BMC EvolutionaryBiology 10:279.

Inoue, J., P. C. J. Donoghue, and Z. Yang. 2010. The impact of the rep-resentation of fossil calibrations on Bayesian estimation of speciesdivergence times. Systematic Biology 59:74–89.

Dow

nloa

ded

by [

Ast

on U

nive

rsity

] at

13:

20 1

1 Ja

nuar

y 20

14

58 JOURNAL OF VERTEBRATE PALEONTOLOGY, VOL. 34, NO. 1, 2014

Kay, R. F., R. H. Madden, M. G. Vucetich, A. A. Carlini, M. M. Mazzoni,G. H. Re, M. Heizleri, and H. Sandeman.1999. Revised geochronol-ogy of the Casamayoran South American Land Mammal Age: cli-matic and biotic implications. Proceedings of the National Academyof Sciences of the United States of America 96:13235–13240

Kullander, S. O. 1986. Cichlid Fishes of the Amazon River drainage ofPeru. Swedish Museum of Natural History, Stockholm, Sweden, 431pp.

Kullander, S. O. 1996. Heroina isonycterina, a new genus and species ofcichlid fish from Western Amazonia. Ichthyological Exploration ofFreshwaters 7:148.6–172.

Kullander, S. O. 1998. A phylogeny and classification of the South Ameri-can cichlid (Teleostei: Perciformes); pp. 461–498 in L. R. Malabarba,R. Reis, R. P. Vari, Z. M. Lucena, and C. A. Lucena (eds.), Phylogenyand Classification of Neotropical Fishes. Edipucrs, Porto Alegre, RioGrande do Sul, Brazil.

Kullander, S. O. 2003. Family Cichlidae (cichlids); pp. 605–654 in R. E.Reis, S. O. Kullander, and C. J. Ferraris Jr. (eds.), Check List of theFreshwater Fishes of South and Central America. Edipucrs, PortoAlegre, Rio Grande do Sul, Brazil.

Kullander, S. O., and H. Nijssen. 1989. The Cichlids of Surinam. E.J. Brill,Leiden, The Netherlands, 256 pp.

Kullander, S. O., M. Noren, G. B. Friðriksson, and C. A. S. de Lucena.2010. Phylogenetic relationships of species of Crenicichla (Teleostei:Cichlidae) from southern South America based on the mitochondrialcytochrome b gene. Journal of Zoological Systematics and Evolution-ary Research 48:248–258.

Lopez-Fernandez, H., R. L. Honeycutt, and K. O. Winemiller. 2005.Molecular phylogeny and evidence for an adaptive radiation ofgeophagine cichlids from South America (Perciformes: Labroidei).Molecular Phylogenetics and Evolution 34:227–244.

Lopez-Fernandez, H., K. O. Winemiller, and R. L. Honeycutt. 2010. Mul-tilocus phylogeny and rapid radiations in Neotropical cichlid fishes(Perciformes: Cichlidae: Cichlinae). Molecular Phylogenetics andEvolution 55:1070−1086.

Lopez-Fernandez, H., J. H. Arbour, K. O. Winemiller, and R. L. Hon-eycutt. 2013. Testing for ancient adaptive radiations in Neotropicalcichlid fishes. Evolution. 67:1321–1337.

Lopez-Fernandez, H., R. L. Honeycutt, M. L. J. Stiassny, and K. O. Wine-miller. 2005. Morphology, molecules, and character congruence inthe phylogeny of South American geophagine cichlids (Perciformes,Labroidei). Zoologica Scripta 34:627−651.

Lopez-Fernandez, H., K. O. Winemiller, C. G. Montana, and R. L. Hon-eycutt. 2012. Diet-morphology correlations in the radiation of SouthAmerican geophagine cichlids (Perciformes: Cichlidae: Cichlinae).PLoS ONE 7:e33997.

Lundberg, J. G., M. H. Sabaj-Perez, W. M. Dahdul, and O. A. Aguilera.2010. The Amazonian Neogene fish fauna; pp. 281–300 in C. Hoornand F. P. Wesselingh (eds.), Amazonia, Landscape and Species Evo-lution: A Look into the Past. Blackwell Publishing, Chichester, WestSussex.

Lundberg, J. G., L. G. Marshall, J. Guerrero, B. Horton, M. C. Malabarba,and F. Wesselingh. 1998. The stage for Neotropical fish diversifica-tion: a history of tropical South American rivers; pp. 13–48 in L. R.Malabarba, R. Reis, R. P. Vari, Z. M. Lucena, and C. A. Lucena(eds.), Phylogeny and Classification of Neotropical Fishes. Edipucrs,Porto Alegre, Rio Grande do Sul, Brazil.

Malabarba, M. C., and L. R. Malabarba. 2008. A new cichlid Tremem-bichthys garciae (Actinopterygii, Perciformes) from the Eocene-Oligocene of eastern Brazil. Revista Brasileira de Paleontologia11:59–68.

Malabarba, M. C., L. R. Malabarba, and C. del Papa. 2010. Gymnogeoph-agus eocenicus (Perciformes: Cichlidae), an Eocene cichlid from theLumbrera Formation in Argentina. Journal of Vertebrate Paleontol-ogy 30:341–350.

Malabarba, M. C., O. D. Zuleta, and C. del Papa. 2006. Proterocara ar-gentina, a new fossil cichlid from the Lumbrera Formation, Eoceneof Argentina. Journal of Vertebrate Paleontology 26:267–275.

Murray, A. M. 2000. Eocene cichlid fishes from Tanzania, East Africa.Journal of Vertebrate Paleontology 20:651–664.

Murray, A. M. 2001. The fossil record and biogeography of the Cichlidae(Actinopterygii: Labroidei). Biological Journal of the Linnean Soci-ety 74:517–532.

Musilova, Z., O. Rıcan, K. Janko, and J. Novak. 2008 Molecular phylogenyand biogeography of the Neotropical cichlid fish tribe Cichlasomatini.Molecular Phylogenetics and Evolution 46:659–672.

Muller, J. 1845. Uber den Bau und die Grenzen der Ganoiden und uberdas naturliche System der Fische. Abhandlungen der KoniglichenAkademie der Wissenschaften 1845 (for 1844):117–216.

Near, T. J., R. J. Eytan, A. Dornburg, K. L. Kuhn, J. A. Mooreb, M. P.Davis, P. C. Wainwright, M. Friedman, and W. L. Smith. 2012. Reso-lution of ray-finned fish phylogeny and timing of diversification. Pro-ceedings of the National Academy of Sciences of the United States ofAmerica 109:13698–13703.

Perez, P. A., M. C. Malabarba, and C. del Papa. 2010. A new genus andspecies of Heroini (Perciformes: Cichlidae) from the early Eocene ofsouthern South America. Neotropical Ichthyology 8:631–642.

Reis, R. E. 1998. Systematics, biogeography and the fossil record of theCallichthyidae: a review of the available data; pp. 351–362 in L. R.Malabarba, R. Reis, R. P. Vari, Z. M. Lucena, and C. A. Lucena(eds.), Phylogeny and Classification of Neotropical Fishes. Edipucrs,Porto Alegre, Rio Grande do Sul, Brazil.

Reis, R. E., and L. R. Malabarba. 1988. Revision of the Neotropical genusGymnogeophagus Ribeiro, 1918, with descriptions of two new species(Pisces, Perciformes). Revista Brasileira de Zoologia 4:259–305.

Rıcan, O., L. Pialek, R. Zardoya, I. Doadrio, and J. Zrzavy. 2012. Biogeog-raphy of the Mesoamerican Cichlidae (Teleostei: Heroini): coloniza-tion through the GAARlandia land bridge and early diversification.Journal of Biogeography 40:579–593.

Schwarzer, J., B. Misof, D. Tautz, and U. Schliewen. 2009. The root of theEast African cichlid radiations. BMC Evolutionary Biology 9:186.

Smith, W. L., P. Chakrabarty, and J. S. Sparks. 2008. Phylogeny, taxon-omy, and evolution of Neotropical cichlids (Teleostei: Cichlidae: Ci-chlinae). Cladistics 24:625–641.

Sparks, J. 2004. Molecular phylogeny and biogeography of the Malagasyand South Asian cichlids (Teleostei: Perciformes: Cichlidae). Molec-ular Phylogenetics and Evolution 30:599−614.

Sparks, J. S., and W. L. Smith. 2004. Phylogeny and biogeography of cichlidfishes (Teleostei: Perciformes: Cichlidae). Cladistics 20:501–17.

Stiassny, M. L. 1991. Phylogenetic intrarelationships of the family Cich-lidae: an overview; pp. 1–35 in M. H. A. Keenleyside (ed.), Cich-lid Fishes. Behaviour, Ecology and Evolution. Chapman and Hall,London.

Vences, M., J. Freyhof, R. Sonnenberg, J. Kosuch, and M. Veith. 2001.Reconciling fossils and molecules: Cenozoic divergence of cichlidfishes and the biogeography of Madagascar. Journal of Biogeography28:1091–1099.

White, T., C. del Papa, and R. Brizuela. 2009. Paleosol-based paleocli-mate reconstruction of Late Paleocene through Middle Eocene Ar-gentina. Geological Society of America, Abstracts with Programs 41:567.

Wiley, E. O., and G. D. Johnson. 2010. A teleost classification based onmonophyletic groups; pp. 123–182 in J. S. Nelson, H.-P. Schultze, andM. V. H. Wilson (eds.), Origin and Phylogenetic Interrelationships ofTeleosts. Verlag Dr. Friedrich Pfeil, Munich.

Wainwright, P. C., W. L. Smith, S. A. Price, K. L. Tang, J. S. Sparks, L.A. Ferry, K. L. Kuhn, R. I. Eytan, and T. J. Near. 2012. The evolu-tion of pharyngognathy: a phylogenetic and functional appraisal ofthe pharyngeal jaw key innovation in Labroidei and beyond. System-atic Biology 61:1001−1027.

Wimberger, P. H., R. E. Reis, and K. Thornton. 1998. Mitochondrial phy-logenetics, biogeography, and evolution of parental care and matingsystems in Gymnogeophagus (Perciformes: Cichlidae); pp. 509–518 inL. R. Malabarba, R. Reis, R. P. Vari, Z. M. Lucena, and C. A. Lucena(eds.), Phylogeny and Classification of Neotropical Fishes. Edipucrs,Porto Alegre, Rio Grande do Sul, Brazil.

Yang, Z. H., and B. Rannala. 2006. Bayesian estimation of species di-vergence times under a molecular clock using multiple fossil cal-ibrations with soft bounds. Molecular Biology and Evolution 23:212–226.

Submitted August 6, 2012; revisions received January 23, 2013;accepted February 24, 2013.Handling editor: Matt Friedman.

Dow

nloa

ded

by [

Ast

on U

nive

rsity

] at

13:

20 1

1 Ja

nuar

y 20

14