Biological Journal of the Linnean Society (2001), 74: 517-532. With 4 figures doi:10.1006/bijl.2001.0599, available online at http://www.idealibrary.com on IDEM®

The fossil record and biogeography of the Cichlidae (: Labroidei)

ALISON M. MURRAY*

Redpath Museum, McGill University, 859 Sherbrooke St West, Montreal, QC, H3A 2K6, Canada

Received 20 March 2001; accepted for publication 17 July 2001

The family Cichlidae is a large group of tropical fishes in the order , with an estimated number of living species exceeding 1400. The modern distribution of the family Cichlidae is predominantly in fresh waters of Central and South America, , Madagascar, India and the Middle East, with fossil members known from Africa, Saudi Arabia, the Levant, Europe, South America and Haiti. Many authors have referred to the distribution as being Gondwanan and have postulated that originated over 130 million years ago, in the Early Cretaceous. However, the suggested evidence for an Early Cretaceous origin of cichlids is equally or more compatible with a much younger age of origin. Based on the biology and distribution of modern and fossil cichlids, it is more probable that they arose less than 65 million years ago, in the Early Tertiary, and crossed marine waters to attain their current distribution. © 2001 The Linnean Society of London

ADDITIONAL KEY WORDS: Africa - Asia - dispersal - Europe - Neotropics - palaeobiogeography - salinity tolerance.

INTRODUCTION 1300 (Nelson, 1994), 1400 (Kullander &Nijssen, 1989), or more, with the majority being the species that have Two schools of thought regarding the origin of disjunct radiated rapidly in the East African Great Lakes. distributions dominate in the literature. On the one The Early Cretaceous origin for the family Cichlidae hand are those biogeographers who suggest that dis- suggested by Stiassny (1987, 1991) was in part based peral across a barrier allowed organisms to exploit upon the assertion that the distribution of cichlids new areas and speciate, while on the other are those conformed to a Gondwanan pattern, and therefore who attribute disjunct distributions to the splitting of must have originated before the breakup of the con­ a larger ancestral distribution by a vicariant event. tinents. Although Greenwood (1983) had previously Although vicariant events may explain many dis­ suggested that cichlids may have undergone marine tributions, dispersal events also have been significant dispersals and were unlikely to have been present in for some current distributions of organisms (e.g. on “Gondwana times”, and Stiassny & Raminosoa (1994) oceanic islands). The current distribution of cichlids later stated that the presence of cichlids in Madagascar has been attributed to vicariant events, leading to might be best explained by a post-rift (i.e. marine an extremely lengthy history for the family being or land bridge) dispersal, the suggested ‘Gondwanan’ postulated (e.g. Stiassny, 1987, 1991; Zardoya et al., distribution of the Cichlidae and their implied Early 1996; Farias, Schneider & Sampaio, 1999). Cretaceous origin is reiterated in the literature (e.g. Extant cichlids are found in Central and South Greenwood, 1994; Leveque, 1997). Farias et al. (1999) America (with one species reaching into Texas), the also stated that cichlids had an “ancestral Gondwana- West Indies, Africa, Madagascar, the Levant, Syria, wide range” and that “a simple vicariant hypothesis” Sri Lanka, coastal India and Iran (Fig. 1). The number explained the distribution of this family, based on their of Recent species in the family is estimated at about phylogeny in which the South American and African cichlids form reciprocal monophyletic sister groups (but see Stiassny, 1991 for an alternate opinion in which the African cichlids are polyphyletic). The as­ * Current address: Research Division, Canadian Museum of Nature, P.O. Box 3443, Station D, Ottawa, ON K1P6P4, sumed age of origin has been further lengthened by Canada. E-mail: [email protected] Zardoya et al. (1996), Streelman et al. (1998) and 517 0024-4066/01/120517 + 16 $35.00/0 © 2001 The Linnean Society of London 518 A. M. MURRAY

Figure 1. Distribution of fossil and modern cichlids. Shaded areas are current distribution and lighter grey area indicates disjunct water bodies within the area. Modified from Stiassny (1991: fig. 1.1) with information from Coad (1982). Numbers refer to fossil specimens and localities listed in Table 1.

Farias et al. (1999), who have suggested a history of are often related to the geographical position of con­ over 130 million years (Myr) for the Cichlidae, based tinental land masses at certain points in their geo­ on the separation of Madagascar from the Gondwanan logical history. In the early part of the Mesozoic, most continent by a marine barrier. This extremely remote of the earth’s land mass was coalesced in a single origin of cichlids is not supported by the fossil record. continent. This single continental mass had split into The earliest known cichlids are about 45 Myr old a northern part, Laurasia, separated by the Tethys (Murray, 2000b), which would suggest a gap in the Sea from the southern part, Gondwana, by the end of fossil record of more than 80 Myr if the age of origin the Middle Jurassic, about 160 million years ago (Mya) suggested by Farias et al. (1999) were correct. Such a (Smith, Smith & Funnel, 1994). Gondwana included gap is not evident in the fossil records of two other the lands of South America, Africa, India, Madagascar, fish groups, the freshwater osteoglossomorphs and ch- Australia, Antarctica and Arabia. These land masses aracoids. The former has a fossil record from the Jur­ maintained at least minor connections until roughly assic (Li & Wilson, 1996) and the latter from the 120 Mya, by which time Gondwana had split into Late Cretaceous (Murray, 2000a), with representatives three masses: (1) Africa/Arabia + South America, (2) known from all the following epochs. Madagascar + India, and (3) Australia + Antarctica. Furthermore, the phylogenetic relationships and Cichlids are found in the two former, but not Australia/ current distribution of the Cichlidae can be equally Antarctica. well interpreted based on dispersal events. Hypotheses If cichlids truly had a Gondwanan distribution 130 of an Early Cretaceous origin of cichlids rests on two Mya, they should also have been in Australia, which questionable assumptions: that the distribution of cich- was at a similar latitute to India/Madagascar. Al­ lids conforms to a Gondwanan pattern and that cichlids though the freshwater fish fauna of Australia is de­ are incapable of dispersal through salt waters. pauperate and highly endemic (Morgan, Gill & Potter, 1998), it does share some taxa with Africa (e.g. Os- teoglossomorpha, Galaxiidae, and lungfishes), all of GONDWANAN DISTRIBUTION which have a fossil record dating from the Cretaceous The distributions of modern organisms, particularly or earlier. However, neither living nor fossil cichlids those that are terrestrial or confined to fresh waters, are known from Australia. Furthermore, if cichlids BIOGEOGRAPHY 519 were confined to a strictly Gondwanan distribution, Democratic Republic of the Congo, and O. amphimelas they would not now be in the West Indies which did of lakes Manyara and Eyasi, which have high pro­ not rise above sea level until the late Miocene (Smith portions of sodium chloride (Trewavas, 1983). Clearly et al., 1994) perhaps 7 or 8 Mya. Clearly, the dis­ there are many examples of salinity tolerance in cichlid tribution oi the Cichlidae does not include some oi the fishes, and consequently there is no reason to believe Gondwanan land mass, but does include lands that that salt water was a barrier to cichlid dispersal in were not part oi Gondwana, so it cannot be described the past. as strictly Gondwanan. Cichlids found in Madagascar and India are thought to be some of the most primitive species of the family (Fig. 2). Reinthal & Stiassny (1991) listed three of SALINITY TOLERANCE the nine endemic Madagascan cichlids as euryhaline. Implicit to interpreting the distribution oi cichlids Several of these species are not only tolerant of brack­ based on vicariant events is the assumption that cich- ish waters, but live in estuarine environments (Nor­ lids are obligate ireshwater fishes, unable to disperse man & Greenwood, 1975) and are occasionally found across marine barriers that separate the land masses in marine waters (Banarescu, 1990). Two species of the in which they now live. They therefore have been Indian/Sri Lankan Etroplus are salt-tolerant, assumed to have an origin predating the breakup oi living preferentially in brackish waters (Kiener & the continents on which they are found. Over fifty Mauge, 1966; Loiselle, 1994). This suggests that high years ago, Myers (1949: 318) pointed out that the salinity tolerance was a feature of the first cichlids, an Cichlidae are not limited by salinity and therefore hypothesis consistent with the fact that the perciform cannot be used as evidence of past land connections. families considered most closely related to the Cich- Myers (1949) was one of the first to separate fresh­ lidae (Stiassny, 1991) - the Embiotocidae, Labridae, water fishes into several divisions based on tolerance and - are all marine groups. to salt waters. Freshwater fishes of the primary di­ Despite the evidence to the contrary, current lit­ vision are the only ones that are strictly intolerant erature shows an acceptance of a Gondwanan dis­ to salt water. Cichlid fishes are secondary division tribution circumscribed by the inability of cichlids to freshwater fishes (Norman & Greenwood, 1975; Lowe- tolerate salt water. Clearly, cichlid distribution is not McConnell, 1975, 1987; Banarescu, 1990), which are strictly Gondwanan, nor must cichlid distribution be at least ‘less intolerant’ of salt water. explained solely in terms of vicariant events because Members of the tilapiine lineage not only tolerate dispersals through marine waters are possible. Thus, but occasionally breed in salt waters, and some vicariant events cannot be used to infer a minimum have been maintained in sea water for 7 years (Myers, time of origin for this family. However, fossils can 1949). A species of Oreochromis has established a contribute information on the age of origin by providing population in the sea (Greenwood, 1994), and Tilapia minimum ages at which a lineage inhabited a par­ guineensis and Sarotherodon melanotheron are eu- ticular geographical place. This information, along ryhaline and capable of reproducing in brackish or salt with the distribution of modern cichlids can be used coastal waters (Reid, 1996). Miyazaki et al. (1998) to indicate modes and patterns of dispersal for cichlid found that Oreochromis mossambicus can breed in lineages. either fresh or salt water, and there is no mortality of embryos and larvae transferred directly from one to FOSSIL EVIDENCE the other. In West Africa, hemichromine cichlids have been collected from salt and brackish waters (Gras, An Early Cretaceous origin of cichlids has wider im­ 1961; Boeseman, 1963). Even some Neotropical cichlids plications - it requires that the more inclusive clades have been caught in brackish water (Kullander, 1983). containing cichlids must necessarily have originated Other cichlids are known to tolerate high levels of prior to this time. Yet there is no fossil evidence to sodium chloride, and other minerals, in streams and support this. The family Cichlidae is placed in the lakes. hormuzensis inhabits highly saline suborder Labroidei of the acanthomorph order Per- rivers and streams (Coad, 1982). Danakilia franchettii ciformes. Acanthomorph fishes first appear in the fossil is found in Lake Afrera which has high sodium and record in the Cenomanian, at the beginning of the Late chlorine concentrations (Trewavas, 1983). Oreochromis Cretaceous (Patterson, 1993). Perciform fishes, also alcalicus grahami inhabits highly saline peripheral absent from the Early Cretaceous, first appear in the lagoons in Kenya (Maina, 2000), and Oreochromis al- Campanian, 20-25 Myr after the first acanthomorphs calicus alcalicus is in Lake Natron, which is rich in (Nolf & Dockery, 1990; Patterson, 1993). Hence, the salts, particularly sodium (Trewavas, 1983). Two other oldest acanthomorphs and perciforms known at pres­ species of Oreochromis are also found in saline waters, ent are from Late Cretaceous deposits. O. salinicola, in the saline springs of the Mwashia, Palaeontological data, as Banarescu (1990: 16) 520 A. M. MURRAY

Figure 2. Relationships and distribution of lineages of the Cichlidae. Composite tree created using the method of Baum (1992) from cladograms of Stiassny (1991: fig. 1.20), Lippitsch (1995: fig. 2), Nishida (1991: fig. 3) and Meyer et al. (1994: fig. 4, 1996: fig. 6).

noted, are the only data which prove that a given & Arratia, 1993). This fossil is now considered part of lineage or species was present during a given geological an extant genus (as priscus; Casciotta & period in a given area. Similarly, Lundberg (1998: 52) Arratia, 1993) and the deposits have been listed as noted that fossils provide the only direct evidence of Miocene or questionably Pliocene in age (Frickhinger, prior distributions of ancient taxa. In addition, al­ 1995; Schaeffer, 1947). though a lack of fossils is not necessarily evidence that Oligocene cichlids are known from Africa and Saudi a particular was not present in a given place Arabia (Van Couvering, 1982; Casciotta & Arratia, at a given time, complete absence of a particular animal 1993; Micklich & Roscher, 1990; Lippitsch & Micklich, from beds that would be expected to contain it is strong 1998). The African species (Macfadyena dabanensis, circumstantial evidence that the absence reflects a and four indeterminate forms from Somalia) are ques­ true absence of the animal, not just absence of fossilized tionably Oligocene, in that they occur in the Middle remains. Deposits of a suitable nature are known and Upper Daban Series of Somalia between beds in the Cretaceous (Murray, 2000a), yet no remains dated as upper Eocene marine deposits and possible attributable to a cichlid have been recovered. lower Miocene deposits (Van Couvering, 1982). The The oldest confirmed cichlids, of Eocene age (Table Oligocene Saudi Arabian cichlids represent at least 1), are five species of Mahengechromis from deposits three different lineages of cichlids, possibly related to dated as 45 Mya in Tanzania (Murray, 2000b). An Heterochromis, tilapiines and haplochromines (Lip- Eocene fossil from Italy, reported in a popular book, pitsch & Micklich, 1998). was tentatively identified as a cichlid (Frickhinger, Recently, remains identified as Cichlidae were re­ 1995), but this identification cannot be confirmed. A ported from Early Oligocene deposits in the Sultanate cichlid from Brazil, Macracara prisca, was originally of Oman (Thomas et al., 1999). Unfortunately, none of recorded as early Tertiary (Woodward, 1939) which the remains were illustrated or described, although was later interpreted to mean Eocene (e.g. Casciotta the authors gave the impression that they are pre- Table 1. Fossil remains attributed to the Cichlidae

Age/Country Locality Identification References Notes Map#

PLEISTOCENE Zaire (DRC) Ishango, L. Edward several Tilapiini* Greenwood, 1959 a 17 sites

?LATE PLEISTOCENE Ghana Lake Bosumtwi Tilapia fossilis White, 1937; Greenwood, 1974 a 6 T. melanopleura ( = T. zilli) i Kenya Kangototha (west of Tilapiini* Greenwood, 1974; Thomson, 1966 i 21 L. Turkana)

LATE PLEISTOCENE Egypt along the sp. Van Neer, 1986 i, 1 25 Chad several sites Tilapia sp. Rivallain & Van Neer, 1984 i, 1 7 Zaire (DRC) Ishango, L. Edward and 'KJreochromis Greenwood & Howes, 1975 i, 2 17 Upper Semliki Sudan two sites Tilapiini* Greenwood, 1968b 24 Tanzania Mumba Cave Tilapiini* and possibly a Greenwood, 1957, 1974 11 Haplochromis type Mauritania Yegai Arenga Cichlidae Daget, 1961; Greenwood, 1974 5 Zaire (DRC) Ishango, L. Edward Cichlidae Stewart, 1990 i 17

MID-LATE PLEISTOCENE Kenya Rawe beds, Kanam Tilapia cf. T. nigra Trewavas, 1937, 1983; Greenwood, 1974 a 14 (Lake Victoria) ( = Oreochromis spilurus)

MIDDLE PLEISTOCENE Kenya West Natron Tilapiini* unpublished data in Greenwood, 1974 ?i Egypt Bir Tarfawi, Eastern Sahara Tilapiini Van Neer, 1993 i 26

EARLY PLEISTOCENE

Kenya Omo, west of Lake Turkana Tilapia crassipina Arambourg, 1947; Greenwood, 1974 a, 3 21 521 BIOGEOGRAPHY CICHLID Tanzania Olduvai Gorge Cichlidae Greenwood, 1974; Greenwood & Todd, 1970; i, 3 12 Stewart, 1996

EARLY PLEISTOCENE OR PLIOCENE Zaire (DRC) Ishango, L. Edward and Sinda Tilapiini* Greenwood, 1959, 1974; Greenwood & Howes, i, 4 17 Mohari ?Cichlidae 1975 i, 2, 3

PLIO-PLEISTOCENE Kenya eastern Turkana Cichlidae spp. Stewart, ms i 19

PLIOCENE Kenya Lothagam, Nachukui Fm Tilapiini Stewart, ms i 20 Muruongori and Kaiyumung members

continued 2 A M MURRAY M. A. 522

Table 1 - continued

Age/Country Locality Identification References Notes Map#

PLIOCENE Jordan Valley two Cichlidae, one similar Avinimelech & Steinitz, 1951 i 28 to Tilapia zilii Mallorca ?Cichlidae Casciotta & Arratia, 1993 i, 5 34 Haiti Cichlasoma woodringi Cockerell, 1923; Casciotta & Arratia, 1993 a 1 Brazil Sao Paulo Acara sp. Aequidens Casciotta & Arratia, 1993; Schaeffer, 1947 a 3 pauloensis Malawi Chiwondo Beds Cichlidae Murray & Stewart, in press i 8 Ethiopia Middle Awash Oreochromis harrisae Murray & Stewart, 1999 a 22 Egypt Wadi Natrun Cichlidae Greenwood, 1972 i, 6 27

EARLY PLIOCENE Tanzania Manonga, Lower Tinde Cichlidae Stewart, 1997 i 10 Member

?PLIOCENiyMIOCENE Brazil Maranhao Geophagus priscus Woodward, 1939 a, 7 4 ( = Macracara prised)

LATE MIOCENE Tanzania Manonga, Inole Member Cichlidae Stewart, 1997 i 10

MIOCENE Argentina Salta Aequidens saltensis Casciotta & Arratia, 1993 a 2 Palaeoeiehla longirostrum ( =Aeoronia) cf. Crenicichla cf. Cichlidae

LATE MIOCENE Tunisia Bled ed Douarah ?Cichlidae Greenwood, 1973, 1974 i 32 (lower faunal level) Italy Romagna and Marche Tilapiini Landini & Sorbini, 1989 a 36 Kenya Ngorora Fm Sarotherodon martyni Van Couvering, 1982; Murray & Stewart, a 13 ( = Oreochromis martyni) 1999 Kenya Mpesida beds Cichlidae Van Couvering, 1982 ?i 13 Algeria Seybouse Valley, near Guelma Palaeochromis daresti, Van Couvering, 1982 a 33 P. rousseleti

continued T a b le 1 - continued

Age/Country Locality Identification References Notes Map#

’ MIDDLE MIOCENE Kenya Kirimun Beds Cichlidae spp. (groups A and B) Van Couvering, 1982 i 13 ’ EARLY MIOCENE Kenya Turkana Grits and Basalts near Cichlidae Van Couvering, 1982 i 18 Loperot EARLY THROUGH LATE MIOCENE Europe Germany, Moravia and Eurotilapia Gaemers, 1989 i 38, 39, 40 Switzerland EARLY MIOCENE Uganda “Lamitima Beds” east of Bukwa cf. Pelmatochromis Van Couvering, 1982 i 16 Kenya Rusinga Island, Kulu Formation ?Tilapia, Cichlidae Greenwood, 1974; Van Couvering, 1982 a, i 15 Palaeofulu kulensis Kalyptochromis hamulodentis Nderechromis cichloides UPPER OLIGOCENE OR MIOCENE Jordan North of Shobak, eastern rim of Cichlidae Weiler, 1970 i, 8 20 Wadi Araba Graben OLIGOCENE Somalia Dab an Fm Macfadyena dabanensis Van Couvering, 1982 a 23 Cichlidae Saudi Arabia Ad Darb Fm ?Astatotilapia Micklich & Roscher, 1990; Lippitsch & a, 9 30 THeterochromis Micklich, 1998 ?Tilapiini Oman Thaytiniti and Taqah ?cichlid remains Thomas et al., 1999; Otero & Gayet, 2000 ?i, 10 31 Ashawq Fm EARLY OLIGOCENE Egypt Fayum cf. Tylochromis Murray, in press EOCENE Tanzania Mahenge Mahengechromis Murray, 2000b a, 1 19 Italy Vicenza ?Cichlidae Frickhinger, 1995 a 37 IHI BOEGAH 523 BIOGEOGRAPHY CICHLID * Indicates material referred to Tilapia sp., prior to the split of this genus into Tilapia, Oreochromis and Sarotherodon. Notes: (а) Remains are body fossils or articulated material. (i) Remains are isolated elements, usually fin spines or teeth. (1) Remains are associated with hominid zooarchaeology sites. (2) Remains were considered to resemble Sarotherodon niloticus; this species is now in the Oreochromis. (3) Casciotta & Arratia (1993) listed these sites as late Pliocene. (4) Remains may be from younger deposits (Greenwood, 1959). (5) Confirmation of this record (given in Casciotta & Arratia, 1993) was not found; see text. (б) Casciotta & Arratia (1993) listed Tilapia (Upper Miocene) of Wadi el Natrum; this may be the same material. (7) This material has previously been given an Eocene date; see text. (8) Casciotta & Arratia (1993) listed these remains only as Cenozoic. (9) Van Couvering (1982) previously noted the presence of ‘cf. Tilapia’ at this site which she listed as Tertiary. (10) Remains may not exist; see text. (11) These fish have been previously listed as Miocene, Tertiary and Oligocene (and are listed twice in Casciotta & Arratia, 1993), but have now been dated as Eocene (see Murray, 2000b). 524 A. M. MURRAY dominantly isolated bones and teeth. Otero & Gayet predominantly based on large size. Because this genus (2001) reviewed the ichthyofauna from this area, but has been split into three (Tilapia, Sarotherodon and did not mention any cichlid remains being present, Oreochromis), material previously identified as Tilapia implying that Thomas et al. (1999) may have erred in might better be considered as ‘tilapiine’ only. Similarly, their identification. Weiler (1970) reported cichlids of the concept of ‘haplochromine’ has changed con­ indeterminable genus and species from freshwater siderably over the years, and remains identified as deposits in Jordan, dated as Late Oligocene or Miocene. such may not belong to Haplochromis or closely related Miocene cichlids are known from a larger number of genera. Isolated elements, predominantly fin spines, localities. Early Miocene remains from Uganda include pterygiophores and vertebral centra, are known from isolated elements representing two or more species Pleistocene deposits in the Democratic Republic of the referred to Pelmatochromis, and articulated skeletons Congo, Egypt, Tanzania, Mauritania, Sudan, Chad, from Kenya were described as Palaeofulu kuluensis, and several localities in Kenya particularly around Nderechromis cichloides and Kalyptochromis hamu- Lake Turkana. Pleistocene articulated skeletons have lodentis (Van Couvering, 1982). Isolated elements of been described from Omo, west of Lake Turkana (Til- indeterminate cichlids have also been recovered from apia crassipina, Arambourg 1947; although Trewavas Kenya and dated as possibly Early and Late Miocene (1983) considered this fossil to be indistinguishable (Van Couvering, 1982). Late Miocene African cichlids, from the modern form, Oreochromis niloticus vulcani, some formally named, are also known from deposits in Lake Turkana), from Lake Victoria (assigned to the in Tanzania, Kenya (Oreochromis martyni), Algeria extant Oreochromis spilurus, Trewavas 1937, 1983), (Palaeochromis daresti and P. rousseliti) and Tunisia and from Ghana (Tilapia fossilis and T. melanopleura (Van Couvering, 1982). The oldest European and South (a synonym of T zilli) White, 1937). American cichlids are of Miocene age (Table 1), with Cichlid remains are common in deposits ranging articulated skeletons recovered from Argentina (Ca- from their first appearance in the Eocene right through sciotta & Arratia, 1993) and Italy (Landini & Sorbini, to the Holocene. Although the lack of remains in earlier 1989). Otoliths and jaw fragments reported as cichlids deposits maybe a factor of non-discovery, there is no a have also been recovered from Early through Late priori reason to assume cichlids originated significantly Miocene deposits in Switzerland, Moravia and Ger­ earlier, but did not leave a trace in deposits of the many (Eurotilapia; Gaemers, 1989). Cretaceous. Therefore, it is reasonable to believe, as Casciotta & Arratia (1993) listed Pliocene remains of did Lundberg (1998), that in the case of cichlids, the indeterminate cichlids from Mallorca. Unfortunately, absence of fossils in the Cretaceous may be evidence although they cited Bauza Rullan (1958) in their table of absence, and that cichlids had not yet evolved by as the authority for that information, the full citation that point in time. What the fossil record clearly dem­ was not given, and the only paper I found on fossil onstrates is that cichlids have been in Africa at least otoliths from Mallorca by Bauza Rullan (1958) did not since the Eocene, were in Arabia in the Oligocene, and refer any material to the Cichlidae. Isolated teeth reached the Neotropics and Europe at the latest by and spine fragments identified as having belonged to the Miocene. cichlids were recovered from Pliocene deposits in the Jordan Valley (Avinimelech & Steinitz, 1951). Pliocene deposits with isolated cichlid elements are also known in Kenya, Malawi, and Egypt (Greenwood, AGE OF ORIGIN FOR THE FAMILY 1972; Murray & Stewart, in press; Stewart, ms). Oreochromis harrisae, from the Pliocene of Ethiopia, It is reasonable to assume that the origin of a lineage is represented by specimens preserved as three-di­ predates its first appearance in the fossil record. Al­ mensional articulated portions of the body complete though there is no set length of time for this gap, with scale covering (Murray & Stewart, 1999). Whole some Recent cichlids are known to speciate extremely body fossils are also found in the Pliocene deposits of quickly (e.g. Owen et al., 1990), and it is unlikely that Sao Paulo, Brazil (Casciotta & Arratia, 1993), and the gap would comprise more than a fraction of the Cockerell (1923) reported several specimens from Haiti known geological history of the family. The earliest which he placed in an extant genus as Cichlasoma known fossils are about 45 Myr old; it is hardly neces­ (Parapetenia) woodringi. Although the Haitian locality sary to postulate a gap of 85 Myr since the origin of was considered Miocene by Cockerell, Casciotta & the family. The only reason to concede these minimum Arratia (1993) listed it as questionably Pliocene. ages for cichlids is if salt water is a barrier to their Pleistocene cichlid remains are mainly isolated bones dispersal, which, as shown above, it is not. Given and fragments of indeterminate species, or are more this, and based on the fossil record, an early Tertiary complete remains referable to a Recent species. Many (perhaps Palaeocene) origin for cichlids is more plaus­ isolated elements have been identified as Tilapia sp., ible. CICHLID BIOGEOGRAPHY 525

CENTRE OF ORIGIN AND DISPERSAL indicate it was once above sea level. Although a land ROUTES: PROPOSED SCENARIO bridge would not be necessary for salt-tolerant cichlids, the Davie Ridge ‘stepping stone’ and surrounding shal­ Although several authors have previously mentioned lower water would have resulted in shorter migrations in passing the possibility of marine dispersal for cich- across deep water for these fishes to reach East Africa. lids (e.g. Greenwood, 1983; Lundberg, 1993), the idea Taquet (1982) noted that a regression in the Senonian was not developed and has been largely ignored in the prior to the Maastrichtian transgressive might have literature. If the unfounded limitation of dispersal only made this route more accessible, but even lower sea through fresh waters is removed, and an age of origin levels occurred during regressions in the Upper Pa- after the separation of the Gondwana land masses is laeocene and Early Eocene (Haq, Hardenbol & Vail, accepted, a biogeographic reconstruction can be pro­ 1987). Thus, conditions in the Early Tertiary would posed that is in agreement with the biology, fossil have been favourable for the migration of cichlids from record and phylogeny of cichlids. Madagascar to Africa. Without a knowledge of the relationships among the taxa under study, biogeographic hypotheses cannot be meaningful (Greenwood, 1983; Humphries & Parenti, 1986). Although the lower level relationships of many DISPERSAL TO INDIA AND SRI LANKA FROM cichlids are not well known, the relationships of the MADAGASCAR higher lineages within the family (Fig. 2) are reason­ The Indian and Sri Lankan cichlids (Etroplus) are ably well supported (Farias etal., 1999; Stiassny, 1990, most closely related to a subset of the Madagascan 1991; Streelman & Karl, 1997). The reconstruction of genera (Fig. 2), again indicating that a single lineage the biogeographic history of cichlids presented below from Madagascar dispersed from there to the east, is based on a composite of several phylogenies available invading the waters of India and Sri Lanka. Flores for part or all of the family (Fig. 2), created using the (1971) suggested that Indian and Madagascar only method described by Baum (1992). separated at the end of the Cretaceous-beginning of From this phylogeny, assumptions can be made re­ the Tertiary, but more recent information (Smith et garding dispersal of lineages. When confronted with al., 1994) indicates that Madagascar and India had two land masses, one inhabited by a monophyletic separated from one another by the Coniacian (88 Ma). group and the other by a polyphyletic group, it is more The Indian land mass then remained isolated until it parsimonious to assume that the single lineage of collided with central Asia in the Maastrichtian (Rage the monophyletic group dispersed, rather than that & Jaeger, 1995), Late Palaeocene (Mattauer, Matte & multiple lineages dispersed. This reasoning is used in Olivet, 1999), Early Eocene (Krause & Maas, 1990) or the following reconstruction of dispersal events. Late Oligocene (Smith et al., 1994). Goldstein (1973) suggested that the species of Etro- MADAGASCAR AS THE CENTRE OF ORIGIN plus (or their ancestor) travelled to India and Sri Based on current phylogenies, the most primitive cich- Lanka from eastern Africa (although dispersal from lids (Fig. 2) occur in Madagascar. Although Kiener & Madagascar, not East Africa, is more likely based on Mauge (1966) noted that an ancestor to the cichlids the phylogeny) sometime in the Tertiary, possibly by of Madagascar could have reached Madagascar from a progressive dispersal ofpopulations through brackish Africa across the Mozambique channel, it is more waters of river mouths along the coastline of the Ara­ consistent with the phylogeny of the family, in which bian plate. The only cichlids known from Saudi Arabia the two Madagascan lineages form a paraphyletic are of Oligocene age; however, these fossils have been group, to suggest that the opposite happened: cichlids identified as belonging to three separate lineages (Lip- arose in Madagascar then representavites of one lin­ pitsch & Micklich, 1998) none of which are closely eage crossed the channel to invade Africa. Cichocki related to the Indian cichlids. Furthermore, no cichlids (1976) argued that dispersal through the sea probably currently inhabit this area, therefore, if a coast-wise has not contributed to the current distribution of cich- dispersal over generations along the Arabian Plate lids because there is no evidence that cichlids currently occurred, the populations later became extinct and left disperse across the relatively narrow Mozambique no record. Alternatively, it is possible that cichlids Channel between East Africa and Madagascar. At migrated directly across marine waters from Ma­ present, the narrowest part of the channel is about dagascar to India. There are no fossils known from 400 km wide, with most of that distance being over either India or Sri Lanka, so no minimum date of water that is 1000 or more metres deep. However, arrival in those places can be assigned. Sri Lanka was Taquet (1982) noted the occurrence of continental de­ below sea level in the Tertiary until the Pliocene (map posits on the Davie Ridge (100 km from Africa and in Smith et al., 1994), suggesting that cichlids only 300 km from Madagascar) in the Mozambique channel invaded the island after that point in time. 526 A. M. MURRAY

DISTRIBUTION WITHIN AFRICA in the rainy season from a coastal habitat in West Prior to the Miocene, Africa probably was a stable land Africa out to sea. Clearly, two or more individuals mass with a shared continental hydrography (Reid, would have to cross the ocean and arrive in a habitable 1996). Many authors have noted a pre-Miocene pan- area at roughly the same time, but ocean currents African ichthyofauna (e.g. Greenwood, 1983) which and shallow water areas were available to aid cichlid included cichlids. Fossil remains of cichlids are known dispersal. Palaeoreconstructions of ocean currents from East, West and North Africa, and apparently (Haq & Van Eysinga, 1987) show that the currents of cichlids were distributed throughout the continent, the South Atlantic in the Late Cretaceous and Early probably limited only by low temperatures or lack Tertiary are essentially the same as today. The South of water. Such a shared hydrography explains the Equatorial Current sweeps along the west coast of relationship between the Eocene East African Mah- Africa, from the southern tip of the continent to the enge ichthyofauna, and that of modern West Africa Gulf of Guinea, then crosses the Atlantic in the tropical noted by Greenwood (1968a) and Greenwood & Pat­ zone (with a warm water temperature) to the north­ terson (1967). eastern coast of Brazil (Brown et al., 1989). The speed In the Miocene, roughly 20 Mya, rifting caused of an ocean current is variable, dependent upon factors waters in the eastern part of Africa to drain to the including wind and temperature; however, a reason­ Indian Ocean, severing most hydrographic connections able average speed for the current is 0.5 knots (based between east and west Africa. The creation of the on Couper, 1983). At this speed, fishes could be carried Great Lakes, where the majority of cichlid species are 500 km in as little as 23 days. Even with a larger gap now found, opened up new habitats, which probably between continents, deflection of the current, or winds lead to the great diversity of more advanced cichlid deflecting progress, it is possible that fishes could lineages now found there. The more basal African have been swept across the Atlantic well within their lineages are found predominantly in West Africa or lifetimes, so a lack of breeding sites would not prevent have a pan-African distribution (Fig. 2). cichlids from reaching South America. A trans-Atlantic trip also may have been facilitated by areas of shal­ lower waters in the ocean, caused by the Mid-Atlantic DISPERSAL TO SOUTH AMERICA FROM AFRICA Ridge and the Ceara and Sierra Leone rises (Fig. 3), The Neotropical cichlids are considered to comprise a which may have been close to the surface or even monophyletic group, whereas the African cichlids may subarial during regressions in the Early Tertiary, pro­ not (Stiassny, 1991; but see Farias et al., 1999 for a viding shallow water areas en route to Brazil. possible monophyletic African cichlid group), therefore, After reaching the waters of South America, cichlids it is more parsimonious to assume that a single lineage could easily have spread from there to Central America migrated to South America from Africa, rather than and as far north as Texas, perhaps with several lin­ that multiple lineages migrated the other way. Even if eages independently colonizing those areas. Myers the South American and African cichlids are eventually (1966) suggested that cichlids from South America confirmed to be reciprocal monophyletic sister groups, invaded Central America sometime in the Late Ter­ it still would be more likely that a lineage from Africa tiary (Neogene) by crossing open seas or following coast crossed to South America, rather than vice versa, lines, although a continental connection may have because if cichlids arose in Madagascar they would existed in the Early Tertiary (Gayet et al., 1993). The likely pass through Africa to reach the Neotropics. A Miocene or Pliocene fossil cichlid from Haiti sets a latest date for cichlid dispersal across the South At­ minimum date for cichlids to have reached the West lantic is determined by the Miocene fossil cichlids Indies. known from the Neotropics (Table 1). Palaeoreconstructions of the continents, such as those by Smith et al. (1994), show the last connection DISPERSAL TO IRAN AND THE LEVANT between western Africa and Brazil at the end of the The extant endemic cichlid Iranocichla hormuzensis Early Cretaceous (Albian, 105 Mya). By the Cam­ is considered to be a member of the predominantly panian, the South Atlantic separated the two con­ African tilapiine lineage, possibly the sister-group to tinents by about 500 km (Tarling, 1982; map in Smith Tristramella, found in the Jordan Valley (Coad, 1982) et al., 1994) and from the Maastrichtian through Early or Danakilia, endemic to Lake Afrera in Ethiopia Tertiary, the separation was between 500 and 800 km (Trewavas, 1983). Coad (1982) regarded the current (Fig. 3). This gap might be considered a long migration distribution of Iranocichla to be a result of for a swimming cichlid, however, a ‘deliberate’ range throughout a larger area that included the Tigris- extension across the ocean is not being suggested. Euphrates basin, with only a relict population left However, over a period of millions of years, it is plaus­ extant in Iran. However, Iranocichla inhabits saline ible that a few individuals might be swept by flooding streams between 40-400 m above sea level (Kiabi & CICHLID BIOGEOGRAPHY 527

Figure 3. Geographical relationship of South America and Africa in the Early Tertiary (about 55 Mya). Based on maps in Smith et al. (1994). Shaded areas are land mass above sea level and thinner lines indicate outline of present day continents. Solid arrows mark the South Equatorial current. Dotted lines indicate submarine ridges: C, Ceara Rise; RG, Rio Grande Rise; SL, Sierra Leone Rise; W, Walvis Rise.

Abdoli, 2000) of a small coastal plain blocked land­ freshwater deposits in Jordan (Weiler, 1970), and in­ wards by mountains which quickly rise to over 1000 m. determinate cichlids are known from the Pliocene of If it is a relict population, it likely must have arrived the Jordan Valley (Avinimelech & Steinitz, 1951). More in the coastal plain before the mountains attained than one cichlid lineage probably colonized the Levant, their current height. Alternatively, the ancestor of as the extant cichlids found there do not form a mono- Iranocichla hormuzensis may have reached Iran from phyletic group. the sea, either by travelling through brackish waters of river mouths along the coast of the Arabian plate (the possible objections to this have been noted above for the Indian lineage) or through the waters of the EUROPEAN CICHLIDS Tethys Sea/Indian Ocean. The earliest date of col­ The Miocene remains of Europtilapia have all come onization for Iranocichla in the area it presently in­ from brackish or mixed brackish and freshwater en­ habits is Middle Miocene, when it rose above sea level vironments (Gaemers, 1989). Similarly, the Italian (map in Smith et al., 1994). Messinian (terminal Miocene) specimens are from Tristramella and Sarotherodon galilaeus, the cich- coastal lagoons that had an environment that would lids in the Jordan Valley and Syria, may have dispersed have been close to the salinity of sea water. Landini via fresh waters to the Levant from Africa via a land & Sorbini (1989) and Gaemers (1989) suggested that bridge (Leveque, 1997), which would result in the time a regression or an evaporitic event allowed cichlids to of arrival in this area being limited to prior to the cross a land bridge into Europe, possibly through the Middle Miocene or after the end of the Miocene, when a Arabian Peninsula, then later transgressions isolated direct land connection between Africa and the Arabian the European cichlids which eventually became extinct plate existed (maps in Smith et al., 1994). Alternately, because of the cooling of the European climate. In these cichlids may have travelled along the coastline contrast to this, the non-cichlid fishes from the Italian of the Mediterranean Sea or across the isthmus of deposits were considered to be relicts from the Tethys Suez (Roberts, 1975), or travelled up the Red Sea, after Sea (Landini & Sorbini, 1989). It seems unnecessary its opening in the Middle Miocene, to attain their to postulate land bridges for cichlids that were living current range. Fossil cichlids of unknown affinities in brackish or salt environments. It is more likely that have been recovered from Late Oligocene or Miocene all these Miocene cichlids crossed the Tethys Sea or 528 A. M. MURRAY

Figure 4. A composite tree of the family of Cichlidae (based on Fig. 2 with the addition of the Eocene Mahengechromis) superimposed on the geological time scale. Note that the time scale is not drawn to be proportionally representative. Black circles indicate known cichlid occurrences. Representative references for fossil occurrences are: (1) Lippitsch & Micklick (1998); (2) Casciotta & Arratia (1993); (3) Greenwood (1957, 1959, 1968b); (4) Murray & Stewart (1999); (5) Van Couvering (1982).

circumnavigated the coastal waters, to reach Europe age, must have that same minimum age. Therefore, directly via saline waters. although many lineages of cichlids do not have a fossil record, minimum ages for some individual lineages still can be determined (Fig. 4). THE AGE OF ORIGIN OF LINEAGES If Mahengechromis, the Eocene fossil genus, forms Identifiable fossils from accurately dated localities give the sistergroup to the hemichromine cichlids (Murray, an absolute minimum time of origin for particular 2000c), then the latter lineage must have a minimum lineages. Based on phylogenetic relationships, the sis- middle Eocene age. A minimum Oligocene age can be tergroup of a lineage with an established minimum assigned for the tilapiine lineage based on fossils. A CICHLID BIOGEOGRAPHY 529 third age can be assigned, that of the cichlids of lakes (3) It is consistent with the fossil evidence. Malawi and Victoria. These lakes are considered to Furthermore, the proposed scenario is potentially more hold species flocks which arose in the lakes; however easily falsefiable with new information on cichlid in­ the lakes did not form until rifting in the Miocene. A terrelationships and new fossil cichlid finds. For ex­ maximum Miocene age can therefore be assigned to ample, if we find both Neotropical and African groups these lineages. Fossils from Saudi Arabia were tent­ to be polyphyletic with more than one lineage shared atively identified as belonging to three lineages, Astato- between the two continents, or if fossils of Neotropical tilapia (a riverine haplochromine), Heterochromis, and lineages are found in Africa, the most parsimonious the tilapiine lineage (Lippitsch & Micklich, 1998). If explanation would be that cichlids were widely dis­ the identifications are correct, these fossils give a tributed within Gondwana prior to the split of the minimum Oligocene date for these groups, and there­ continents. Although the scenario proposed above may fore the haplochromine lineage must have existed in eventually fail the test, it serves to emphasize that an the Oligocene before invading the Miocene African Rift Early Cretaceous Gondwanan origin for cichlids should Lakes. not be accepted without question. Only if such an Although also formed during Mio­ early origin is demonstrated can the distribution and cene rifting, giving a maximum age for the cichlids to phylogeny of these fishes be used to indicate past have invaded the lake, these lineages cannot be given continental connections, or past connections be used a minimum age of origin. The lineages of Lake Tan­ to infer evolutionary and biogeographical information ganyika do not form a single monophyletic group, and about cichlids. therefore the ancestors of these lineages may have invaded the lake separately. The Neotropical lineage can be given a minimum ACKNOWLEDGEMENTS age of Miocene, based on fossil remains in South and Central America. However, based on the phylogenetic I am grateful to N. Alfonso, R. L. Carroll, B. W. Coad, relationships (Fig. 2), the Neotropical lineage, as well and R. B. Holmes for many helpful discussions and as Tylochromis, Heterochromis and the Madagascan comments on the manuscript. Thanks also to M. Gayet and Indian cichlids must have arisen before the mini­ and an anonymous reviewer for additional suggestions mum Eocene origin of more derived lineages, provided for improving the ms. by the fossil cichlids from Mahenge.

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