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. —Ss«éBULLETIN OF

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BRITISH MUSEUM (NATURAL HISTORY)
IG ee ae oo Supplement 6
e. = LONDON: 10974 |

_ THE CICHLID FISHES OF LAKE VICTORIA,
EAST AFRICA : THE BIOLOGY AND
_ EVOLUTION OF A SPECIES FLOCK

BY

PETER HUMPHRY GREENWOOD

Pp 1-134; 1 Plate, 77 Text-figures

— ee BULLETIN OF

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9

{

SE CICHLID FISHES: OF LAKE VICTORIA,
EAST AFRICA : THE BIOLOGY AND
EVOLUTION. OF. A’ SPECIES’ FLOCK

By PETER HUMPHRY GREENWOOD

CONTENTS

Page
INTRODUCTION . P : : ‘ ‘ : : 3
LAKE VICTORIA, ITS PHYSIOGRAPHY AND HISTORY. : ; : 7,
THE FISHES OF LAKE VICTORIA . ‘ : : : : : : II
The non-cichlid fishes. : : : : : ; : : II
The cichlid fishes . : . : ; ; ‘ , 13
THE HAPLOCHROMIS SPECIES FLOCK : : i : 2 oes 19
Introduction. : : ; ‘ Z ; ; : : ; 19
Basic morphology . : 5 : : ; Ze
Feeding habits of the H Diag eine species ‘ ‘ ; : 30
Intralacustrine distribution of the Haplochromis species : : , 44
Breeding biology of the Haplochromis species . 50
INTERRELATIONSHIPS OF THE LAKE VICTORIA HAPLOCHROMIS SPECIES 56
The insectivorous species : : . ‘ ; : : : 58
Phytophagous species . ; : : ; ‘ , 63
Species feeding on benthic One eee : : é : ‘ 67
Scale eating species : , : : : : ; ; : 69
Mollusc eating species. . , : : : 69
Predators on larval and Sao dichia Aches : : : : : 75
Piscivorous predators. ‘ ‘ : : : : 80
Conclusion . . ; . : : : : 93
THE RELATIONSHIPS OF THE MONOTYPIC GENERA . ; , ; 99
THE ANATOMICAL BASIS FOR THE ADAPTIVE RADIATION . : : 103
SPECIATION ; : , ; ; d ; : : TII
CONCLUSION . 3 : ‘ : 119
ACKNOWLEDGEMENTS : : : : : : : . : 124
REFERENCES . : ‘ ‘ : : ‘ : . : : T25

INDEX >. : : : ; : : : 3 : : : 12

INTRODUCTION

Tue freshwater fishes of the Great Lakes of Africa have long fascinated and perplexed
students of evolution. As far back as 1913, Plate suggested that the cichlid fishes in
Lake Tanganyika might show a mode of speciation different from that of the usual
kind. This view, broadened to include fishes from other lakes, was supported by
many subsequent workers, with Rensch (1933) a notable exception, and is still
_ echoed today (Trewavas, Green & Corbet, 1972).

The problem has, if anything, increased in its complexity (and interest) since
_Plate’s time, despite our greatly increased knowledge of these fishes. The publica-
tion recently of a book some 500 pages long (Fryer & Iles, 1972) summarizing re-
searches into the biology and evolution of but one family of African fishes (the
Cichlidae) is a good indicator of the problem’s size.

PH. GREENWOOD

Attention has always centred on species of the family Cichlidae, perch-like fishes
widely distributed in tropical America and Africa, but also occurring in India, Shri
Lanka (Ceylon) and Malagasi. This focus on African cichlids has, to a certain extent,
distracted attention from other African freshwater fishes, and even from the cichlids
of South America (see Lowe-McConnell, 1969), a sad but understandable state of
affairs.

Each of the larger African lakes is characterized by a strongly endemic cichlid
species complex (Table I). In most lakes these species dominate the fish fauna,
both in an ecological and a taxonomic sense. Ecologically, the lake cichlids generally
show a wider spectrum of adaptive radiation than do all the other families combined.

The bare figures of Table I show clearly the high degree of endemism, the extensive
speciation undergone by these fishes and also the preponderance of cichlid taxa over
those of all other families. Some measure of the morphological differentiation within
the various species flocks may be taken from the number of endemic genera recog-
nized in each lake. |

Much of the literature dealing with African lake fishes has been concerned with
these various phenomena, but in particular with the mode or modes of speciation
involved, and the reasons for the disparate levels of taxonomic diversity found in
different lakes (see Fryer & Iles, 1972). Far less attention has been given to the
question of why the Cichlidae more than any other family display this evolutionary
potential, a point to which I shall return later (p. 103).

One peculiarity of the African Cichlidae which Table I does not bring out is the
contrast in diversity and numbers between lake and river dwelling species. The
situation in most rivers is quite the reverse of that in the lakes, with species from
other families providing the dominant faunal elements. A comparison between Lake
Malawi and the Congo river illustrates this point very clearly, especially since both
ecosystems have the most speciose fish faunas known from Africa.

In Lake Malawi there are ca 200 cichlid species comprising some 78 per cent of the
entire fish fauna (ca 242 species), but in the Congo only 7 per cent of the 410 known
species are cichlids (Lowe-McConnell, 1969, where comparisons between other
African lake and river faunas are clearly demonstrated in text-fig. 2, and comparisons
are also made between the African and South American faunas).

The contrast between cichlid and non-cichlid species is even greater if one compares
Lake Victoria (with ca 170 species of Cichlidae) to any of its affluent rivers. In
these, only three cichlid species have been recorded at any distance from the lake
itself.

Obviously this peculiarity is closely connected with the question of what factors
influence and stimulate speciation within the lakes. It is also, of course, associated
with the greater number of ecological niches provided by a lacustrine environment.
(Niche used here, and elsewhere, in the sense of Elton [1928] rather than that of
Weatherley [1963].) These questions will not be considered further and are only
mentioned because of their relevance to that of the ancestral species which must
have populated the embryo lakes from the preexisting river systems.

To return to the lake cichlids. When the evolutionary radiation summarized in
Table 11 is seen against a time scale for lake histories, its speed is outstanding. Ee

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4

EVOLUTION OF A CICHLID SPECIES FLOCK

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of the lake basins is still far from settled, but current estimates suggest that the oldest
(Lake Tanganyika) is not more than 10 million years old, that Lake Malawi is about
2 million years, and that Lake Victoria originated during the mid-Pleistocene, about
750 000 years B.P. (see summaries in Fryer & Iles, 1972 ; and Temple, 1969, for Lake
Victoria). Lake age must undoubtedly be one of the factors affecting the degree of
differentiation within a flock, as must the time and completeness of a lake’s isolation
from other major water bodies, be they lake or river systems. Thus the specifically
depauperate and ecologically impoverished species flocks of Lakes Rudolf and Albert
are a measure of age and lack of isolation. Both lakes are moderately young (early
Pleistocene) and both have, or have had until recently, free contact with the
Nile.

Lake Victoria, the lacustrine background to this essay, is younger, but it has been
a closed drainage basin for most of its existence (Doornkamp & Temple, 1966 ;

Temple, 1969 ; Greenwood, 1973a). Its cichlid flock is adaptively multiradiate, is

highly speciose, but 1s composed of species which, with seven exceptions (two species
of Tilapia, and five monotypic genera) are all members of a single genus, Haflo-
chromis (but see p. 99). The five monotypic genera are all derived from and closely
related to the genus Haplochromis (Greenwood, 1956a, 1959a; alsop.gg below). In
this respect its species flock can be considered a relatively simple one when compared
with those of Lakes Tanganyika and Malawi (see Table I), as it can also be from the
viewpoint of morphological divergence among its Haplochromis species.

The situation in Lake Victoria can probably be taken as a real model of a stage
through which the flocks of Tanganyika and Malawi have already passed. Its
importance in this context is enhanced by the fact that the components of the flock
are already well-advanced along different paths of ecological specialization.

The comparison with Lake Tanganyika is perhaps less complete because there the
species seem to be derived from two major phyletic components of the African
Cichlidae (the so-called ‘Tilapia’ and ‘Haplochromis’ lineages; see Regan, 1920 ;
also Fryer & Iles, 1972). In Lakes Malawi and Victoria by contrast, the flocks,
except for a small group of Tilapia species, are members of the “Haplochromis’
lineage.

As was noted earlier, most attention has been paid to the problems of speciation
within the lakes, and to purely taxonomic and ecological studies of the fishes. Little
has been written about the phylogeny of a particular flock (Fryer’s [1959] analysis of
the ‘Mbuna’ generic complex in Lake Malawi excepted), and virtually nothing has
been said about the evolution of adaptive characters within a flock. By the latter
I mean particularly the anatomical basis for the adaptive trends observed within a
phylogenetic framework.

I believe that the Haplochromis species flock of Lake Victoria provides very suit-

able material for such an analysis, the more especially since it can be linked with a
fairly certain physiographical background to speciation within the developing lake
basin. I also believe that from such an analysis, it is possible to throw light on one
aspect of the question of why cichlids are able to undergo rapid and ecologically
successful adaptive radiations when other families remain, by comparison, evolu-
tionarily inert.

EVOLUTION.OF -A. CICHLID: SPECIES ‘FLOCK i

PEAKE VIi€TORIA, ITS-PHYSIOGRAPHY. AND HISTORY

Lake Victoria is a large, and by comparison with other African lakes, shallow water
body lying across the equator (0°21’N — 3°0’S, 31°39’ — 34°53’E). Its surface area
is approximately 69 000 km?, its greatest length and breadth ca 400 and 320 km
respectively. The coastline is extremely irregular, and totals some 3300 km in
length. Especially in the northern half there are a number of large islands (Text-fig
1) whose shorelines are as varied as those of the mainland.

Broadly speaking, the habitat types provided by the shore comprise deeply in-
dented, shallow and protected bays, sandy exposed beaches and, occasionally, rocky
cliffs or broken rock exposures. [ringing papyrus swamps are common around much
of the shore, and many of the bays terminate in broad swamps extending over several
square kilometres. |

Much of the lake is less than 20 m deep ; the deepest zone (60-90 m) lies somewhat
eccentrically towards the eastern shore and occupies a kidney-shaped area (see
Graham, 1929). The bottom profile in the deeper waters is not entirely flat, oc-
casional ‘hills’ rise well above the general level of the lake floor. Much of the bottom
in these deep areas is covered by a thick deposit of organic mud with, here and there,
isolated patches of hard substrate (sand, shingle or rock). Organic mud substrata
occur inshore as well, especially in sheltered bays, but also along the open coastline
in protected regions. In most places where there is a sandy beach, the sand sub-
strate grades imperceptibly into mud some few hundred metres from the shore ;
rather rarely does the sand extend for more than two or three kilometres offshore and
into water over 30m deep. Substrate type appears to be an important factor in
limiting the distribution of many species (see p. 46).

There is little annual variation in water temperature, the mean surface tempera-
ture being ca 24°C (that of deeper water about a degree lower). An annual cycle of
thermal stratification (Fish, 1957; Talling, 1963) leads to a marked reduction of
dissolved oxygen in deeper parts of the lake. The effects of this relative deoxygena-
tion on the biology of fishes living in affected areas has not been satisfactorily in-
vestigated. At one time (Greenwood, 1965a) it was thought that no cichlids, and
few other species, inhabited depths below about 30m. However, later researches
showed that many species of Haplochromis live in water at this depth and deeper.
Indeed, there is probably no offshore area of the lake without its populations of
_Haplochromis species. What we have yet to discover are the reactions of these
fishes during periods of deoxygenation, whether they can temporarily adapt their
respiratory requirements to the new environment or whether there is some migration
into shallower and better oxygenated zones.

In this respect Lake Victoria contrasts strongly with Lakes Malawi and Tangan-
yika. In these deep (704 and 1470 m) and trough-like lakes the lower water layers
are permanently stratified (Beauchamp, 1964) and no fishes live there (Text-fig. 2).
The greatest depth at which fishes have been recorded in Lake Tanganyika, for
example, is about 200 m, and in Lake Malawi ca1toom. But these deep-living species
are exceptional, and most species (particularly Cichlidae) are restricted to the upper
30 or 40 m),.

Pp... GREENWOOD

NAPOLEON GULF

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Kisumu |

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SPEKE GULF

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Fic. 1. Sketch map of Lake Victoria. The approximate positions of the 20, 40 and
50 m isobaths are indicated by dotted lines. |

|

EVOLUTION -OF A CICHLID SPECIES FLOCK 9

Detailed analyses of the chemical composition of the water are given by Tailing
& Talling (1965). Lake Victoria is categorized by these authors as a lake with a low
total ionic concentration (conductivity between 90 and 145 pmho). There is virtually
no short term change in major ionic composition.

LAKE TANGANYIKA LAKE MALAW!
DEPTH IN
METRES N. BASIN (LAT. 5°S ) S. BASIN(7°S) (LAT. 11°S)
=a
23-6-26:5°C
93-5-27:5 C
500
1000 PERPETUALLY
DEOXYGENATED
LAKE VICTORIA
(LAT. I°S)
)
q 23-8 -26:0°C
100

Fic. 2. Schematic cross-sections through Lakes Tanganyika (north and south basins),
Malawi and Victoria to show differences in the shape and depth of their basins, and the
extent of permanently deoxygenated water.

The horizontal scale is proportional for lake width at the latitudes indicated.
The annual temperature range of surface waters in the epilimnion is shown, as is the
mean annual temperature of the hypolimnion (modified after Beauchamp, 1964).

Probably the major climatic factor affecting overall lake ecology is the biannual
rainy season (most marked in the northern half of the lake), in November and
December, and from March to May. Apart from any direct effect by rainfall on the
water mass itself, the rainy seasons effect the inflow of water through not only the
_ larger affluent rivers (Kagera and Nzoia) but also the numerous and often seasonal
streams draining the surrounding countryside.

10 Ps er. GRE IN W.@ OD

Lake Victoria is, and seemingly always has been, an internal drainage basin
(Temple, 1969; Bishop, 1969; Kendall, 1969) fed principally by the four larger
rivers (Kagera, Katonga, Nzoia and Mara). Its only outflow, formed late in the
lake’s history (Bishop, 1969), established contact with another, much smaller basin,
that now occupied by the swampy Lake Kioga. Lake Kioga in turn has a river con-
nection with the Nile at the northern end of Lake Albert. Faunistically, Lake
Victoria is, however, isolated from the Victoria Nile and Lake Kioga by the now
artificially submerged Ripon Falls. (The Owen Falls dam, built downstream of the
Ripon Falls is probably an even more effective barrier to faunal interchange than were
the falls.) Lake Kioga is cut off from the Nile by the utterly impassable Murchison
Falls, some 40 m high. |

Since the fishes of Lake Kioga, and especially the Cichlidae, are mostly conspecific
with those of Lake Victoria (Greenwood, 1966a) it is very likely that the latter lake
was the chief source of fish stocks for Kioga. Regrettably, the cichlids of Kioga have
not been investigated at all thoroughly, but at least two endemic Haplochromis
species occur there (Greenwood, 1967), and my own studies suggest that more await
description.

Lake Victoria originated during the mid-Pleistocene, about 750 000 years B.P.
(see Bishop, 1969; Doornkamp & Temple, 1966, for summaries of geological and
other evidence). At that time the future lake basin was crossed by several westward
flowing rivers, of which the Kagera, Katonga, Nzoia and Mara are present-day relicts.
These rivers drained the eastern highlands of Kenya, and emptied into what is now the
Congo system. A gradual but large-scale warping of the plateau surface between
the two arms of the rift valley led to a reversal of river flow and a back-ponding of
the western reaches of these rivers. It should be noted that, for some of the rivers,
the western upwarp that interrupted and reversed their flows back towards the east
was relatively slight, probably in the region of 30-50 m.

As a result of upwarping a two-way drainage was established, eastward into the
developing Victoria basin, and westward into the proto-Lakes Albert and Edward.
This drainage pattern still persists (Doornkamp & Temple, 1966; Greenwood,
1973a).

Temple (1969) is of the opinion that backponding of the reversed rivers began
earliest in the southern region of the Victoria basin, and progressed northwards along
the slowly sinking plateau. As a river valley gradually filled it became a shallow,
dendritic lake. Lake Kioga, lying near the head of the now interrupted and re-

versed Kafu river valley, may well be a surviving example of such a lake (see especi-

ally text-fig. 4 in Bishop, 1969).
Eventually, each of the several lakes formed in this way overtopped the inter-

vening and low watersheds and joined its neighbour. Developed and developing ~

lakes were gradually linked together to form a single, expansive water body that
occupied an area considerably greater than that of the present lake. Raised
beaches also indicate that at one time the Pleistocene lake was considerably deeper
than it is now.

Even after the single water body came into existence the lake basin was subject
to periods of tectonic instability. These caused a tilting of the basin and correlated

EVOLUTION OR. A CICHLiID-SsPECIES* FLOCK II

changes in water level at the raised and lowered areas of its margins. One im-
portant consequence of a major tilt to the northeast was the formation of an outlet
(at Jinja) to the Kioga basin. Once the outlet was cut (possibly about 20-25 000
years B.P.; see Bishop & Trendall, 1967 ; Bishop, 1969) there was a gradual fall in
lake level to that of the present day.

It has been thought that during one period of the middle Pleistocene Lake
Victoria was in contact, through rivers, with the proto-Lake Edward—George
(Trewavas, 1933; Greenwood, 1959d, 1965a; Fryer & Iles, 1972). Evidence for
this connection stemmed mainly from overall similarities in the Haplochromis fauna
of the two lake systems, and the supposed sharing between them of certain otherwise
endemic species (Trewavas, 1933). Recent research on the Haplochromis of Lakes
Edward and George (Greenwood, 1973a) suggests, however, that these resemblances
are more likely the result of parallel evolution. The supposedly shared endemics
are, in fact, specifically distinct and thus endemic each to its own basin.

Throughout the early history of Lake Victoria, and particularly during the later
stages of tectonic stability, local and more widely spread climatic changes may well
have produced fluctuations in lake levels if only by a few metres (Bishop, 1969 : III ;
Kendall, 1969). Such changes would undoubtedly lead, first, to the formation of
peripheral water bodies, and later to their reunion with the parent lake. A sequence
of events like this would have a profound influence on the evolution, particularly the
speciation pattern, of the fishes (see Greenwood, 1965a). I shall return to this point
later.

But, even more important in interpreting the phyletic and evolutionary picture of
the Haplochromis species flock, especially its adaptive radiation, were the stages of
independent lakes through which the basin passed early inits history. In effect, the
present lake must be considered an amalgam of several lakes (Greenwood, 1965a ;
and p. 114 below).

FER PIshns OF LAKE VICTORIA

The non-cichlid fishes

Before going on to treat in detail the various elements of the Haplochromis species
flock, some attention must be given to the other fishes with which the cichlids share
their environment, and with which they may compete for food and living space.

Unfortunately it is not possible to discuss the intriguing and fundamental question
of competition in any detail because too little precise information is available on the
ecology of Lake Victoria fishes, both cichlid and non-cichlid. Likewise, little is
known about the invertebrate animals on which so many of the fishes feed.

‘With a few partial exceptions, the 38 species of fishes belonging to families other
than the Cichlidae share habitats with the cichlids (Greenwood, 1966a ; and p. 45
below). The partial exceptions are those species whose habitat ranges include
zones of the lake where cichlids are absent. For example, certain airbreathing
species like the lungfish Protopierus aethiopicus, the anabantoid Ctenopoma muret
and at least two species of the catfish Clarias penetrate fairly deeply into papyrus
swamps. Only one cichlid (Hemihaplochromis multicolor) is found in this habitat

12 PH. GREENWOOD

and even then it is confined to the peripheral and better oxygenated area. The
small cyprinid Engraulicypris argenteus is the only truly pelagic fish in the lake.
Inshore, where a distinction between pelagic and benthic zones is unrealistic,
Engraulicypris does occur with several Haplochromis species, but it alone occupies
the surface waters of the open lake.

Most non-cichlid species enter rivers and the larger permanent streams at all times
of the year, but apparently few cichlids doso. Those that do (Haplochromts nubilus,
Hemthaplochroms multicolor and A statoreochromis alluaudt) are all species with a wide
distribution in Uganda (Greenwood, 1959a, 1965b, 19732).

The greatest intermingling of cichlid and non-cichlid species occurs in the littoral
and sublittoral zones of the lake. Beyond a depth of ca 20m cichlid (1.e. Hapilo-
chronus species) dominance is clear-cut, and few non-cichlids occur in deeper waters.
Only one non-cichlid (the clariid catfish Xenoclarias) is confined to deeper water
(10-90 m), a sharp contrast with the forty or more Haplochromis species known only

from similar habitats. It is perhaps significant that, excepting Xenoclarias, non-—

cichlid fishes inhabiting deepwater areas are all from species whose adults reach a
length of over 250 mm, usually over 500 mm.

Most non-cichlids do not breed in the lake, but migrate up streams and rivers to
spawn during the rainy seasons (Whitehead, 1959 ; Greenwood, 1966a), again con-
trasting sharply with the cichlid species. There is, however, some evidence that a
few non-cichlids are able to breed in particular lacustrine habitats (Corbet, 1960,
1961; the deepwater clariid Xenoclarias [Greenwood, 1958a] only recognized after
Corbet’s studies were completed, should also be included in this category). In-
terestingly, the majority of deepwater inhabiting non-cichlids (Bagrus docmac,
Mormyrus kannume, Synodontis victoriae and Xenoclarias eupogon) are also those
species thought capable of breeding within the lake. These species would, therefore,
not have to undertake the extensive vertical and horizontal migrations necessary to
reach suitable breeding sites in rivers. It would be interesting to know if the deep-
water populations of these species still follow the seasonal breeding patterns of their
shallow-water congeners. Of the deepwater non-cichlids not suspected of lacustrine
spawning (Protopterus aethiopicus and Claritas mossambicus), one (Clarias) is already
known to make long migrations from offshore regions to reach suitable spawning
sites (personal observations). The breeding habits of Protopterus (nest construc-
tion, parental care etc., see Greenwood, 1958b) and aspects of its larval behaviour
(Greenwood, op. cit.) certainly imply that this species is an obligatory inshore
breeder. :

Feeding habits of non-cichlid species have been studied in some detail (Corbet,
1961). The majority can be classified as insectivores, with chironomid larvae as their
principal food organisms. Four species are essentially molluscivorous (feeding on
both gastropods and bivalves) and three are predominantly piscivorous (with Haplo-
chromis species as the main prey). The small pelagic cyprinid Engraulicypris
argenteus mentioned before is the only species that can be considered a zooplankton
feeder. Only two species, the characids Alestes sadleri and A. jacksoni are primarily
herbivorous, feeding on rooted plants of the littoral region ; both species, however,

also eat insects.

EVOLULION OF WAY CICHLID SPECIES FLOCK 13

This résumé is perforce oversimplified ; as Corbet (1961) cautions, the feeding
habits of all the non-cichlid fishes are to a certain extent facultative (at least within
and sometimes beyond the major food categories used here) and vary with the size of
the fish. Despite the broadly overlapping food requirements of these fishes, Corbet’s
(op. cit.) elegant and detailed analysis led him to believe that there was little inter-
specific competition for food ; to quote: ‘The few species with specialized feeding
habits appear to enjoy a superabundance of food, whereas the others achieve the
same object by remaining mobile and facultative.’

Regrettably, there are no comparably detailed studies on the food of the Lake
Victoria cichlids (see Greenwood, 1956-69). However, sufficient is known about
these species to indicate the existence of a considerable and broad interspecific
trophic overlap, as well as the existence among these fishes of trophic specializations
not encountered in the non-cichlids (see pp. 30-44 below).

Corbet’s work also shows that non-cichlid feeding habits in lacustrine and fluviatile
environments are essentially similar. This fact could be of importance in the ulti-
mate evolution of trophic diversity within the Haflochromts species flock (see p. I15).
In rivers, the non-cichlid species are the dominant fishes (see p. 4 above). Thus
the early colonizers of the embryo Lake Victoria (itself probably a series of river-like
lakes) would be mainly non-cichlid species. In the present-day rivers of Uganda,
for example, there are only one or two Haplochromis species (and two or three other
cichlids) as compared to twenty or more non-cichlids. The restricted environment
of a developing lake would probably favour fishes that could exploit unoccupied
feeding niches. That the ancestral Haplochromis were able to respond to this selec-
tion is manifest in the trophic diversity of their descendant species. Some of the
reasons for this cichlid potentiality are discussed in detail below (p. 103 ef seq.).

The cichlid fishes

The exact number of cichlid species in Lake Victoria is still undetermined ; every
new collection yields undescribed species, especially now that fishery research vessels
are operating in the deeper waters of the lake (Greenwood & Gee, 1969). It should
also be noted, parenthetically, that cichlid species are being added to the fauna as
the result of introductions from other lakes. In the following discussion these
exotic species will not be considered ; most belong to the genus Tv/apza but inevitably
species of other genera have been added unintentionally.

There are two endemic Tilapia species (T. esculenta and T. variabilis) and between
150 and 170 species of the genus Haplochromis of which all but one, H. nubilus, are
endemic (see Greenwood, 1973a where the presumed occurrence of Victoria species in
Lakes Edward and George is discussed fully, and the idea discounted).

Not all the Haplochromis species have been formally described, and the taxonomic
revision of certain nominal taxa is stillincomplete. The estimated number of Haflo-
chromts species is based on collections still unworked, on personal observations in the
field, and on information from fishery biologists now engaged on deep- and midwater
trawling surveys.

In addition to the Haplochromis species sensu stricto there are four endemic
monotypic genera (Macropleurodus bicolor, Hoplotilapia retrodens [Text-fig 72],

z4 P, H. GREENWOOD

Platytaentodus degeni | Text-fig 71] and Paralabidochromts victoriae ; see Greenwood,
1956a). All are derivatives of Hapflochromis species. A fifth monotypic genus,
Astatoreochromis alluaud1, again a Haplochromis derivative (Greenwood, 1959,
1965c) is not restricted to Lake Victoria.

A sixth species, also of wide distribution outside the lake, is Hemshaplochromis
multicolor. This species is probably the only cichlid in the lake that should more
properly be considered a fluviatile than a lacustrine one. Until recently Hemi-
haplochromis multicolor was classified with Haplochromis. It is now separated from
that genus because of its distinctive breeding habits (Wickler, 1963).

I have certain reservations about the phyletic soundness of recognizing, as genera
distinct from related Haplochromis species, some of the endemic monotypic genera
(see Greenwood, 1973a; also p. 99 below).

At this point it is interesting to compare the cichlid species flocks of Lakes Vic-
toria and Malawi. Lake Tanganyika is not brought into the comparison because its

cichlid species flock (or more correctly, species flocks) is not dominated by Haplo- —

chroms and Haplochromis derivatives (see Regan, 1920; and Fryer & Iles, 1972

where Regan’s views on the diphyletic origin of these fishes is questioned, I think |

justifiably on the evidence now available).

There are more Haplochromis species in Lake Victoria than in Lake Malawi
(ca 150, cf 105) but far fewer endemic Haplochromis-group genera (four cf about 20
in Lake Malawi). Furthermore, these latter taxa in Lake Victoria are monotypic
whereas those in Lake Malawi are mostly polyspecific (Trewavas, 1935; Fryer &
Iles, 1972). What interpretation can be derived from these figures?

First, and most importantly, it should be stressed that the figures do truly repre-
- sent differences between the degree of morphological differentiation existing in the
species flocks of the two Jakes. The phyletic conclusions to be drawn are less ob-
vious (see p. 99). Possibly the greater age of Malawi and the history of its lake
basin (a deep rift valley lake) are or were important factors, as are the different types
of habitat provided by a ‘graben’ as opposed to a saucer-shaped ultimate basin. All
in all it seems likely that the Lake Victoria Haplochromis flock (including all but one
monotypic genus) can be looked upon, at this point in time, as an arrested early
stage in the more complex and morphologically more differentiated type of flock
seen in Lake Malawi. I believe that the multiple-lake origin of Victoria (see p. 114)
combined with its youth (and perhaps the relative rapidity with which it passed
through the multiple-lake stage) are reasons why there has been greater speciation
and less opportunity for more profound morphological differentiation among the
flock. |

In certain respects this question of different degrees of morphological divergence
between the two flocks is more apparent than real. Considering both flocks from a

phyletic viewpoint (i.e. one where propinquity of descent is a more realistic yardstick

for measuring taxonomic relationships than are morphological gaps per se), I can find
few grounds for elevating some of the Lake Malawi taxa to generic rank. Neverthe-
less, there are still some Malawian taxa showing greater anatomical specialization
than is seen in Lake Victoria. The Lake Victoria flock is undoubtedly a simpler
one with a lower overall level of morphological divergence from the basic fluviatile

|

|
'

EVOLUTION: OF A’ CICHLID<«SPECIES..FLOCK is

v

Haplochromis type (as represented today in East Africa by Haplochromis bloyeté
(Greenwood, 1971)).

The two endemic Tzlapia species of Lake Victoria (7. esculenta and T. variabilis)
also provide a simpler picture, taxonomically and ecologically, than do the five
endemic species of Lake Malawi (Lowe, 1952, 1953). There are good grounds
for thinking that the Lake Victoria species were each derived from different ancestral
lineages. Thus, strictly speaking, they do not constitute a species flock like the
Tilapia of Lake Malawi (Fryer & Iles, 1972).

Both Victoria species are specialized phytoplankton feeders (Greenwood, 1953).
Tilapia esculenta obtains its food principally from phytoplankton in suspension, but
T. variabtlis feeds mainly on the moribund phytoplankton of the bottom deposits.
At least partly correlated with the trophic differences are marked interspecific
differences in habitat preference (and in breeding biology). Both species are essen-
tially from inshore regions, with T. esculenta penetrating into deeper water (Gee, 1968),
but rarely to depths greater than 30m. Although the speciescan occupy similar habi-
tats, T. esculenta is commoner in sheltered gulfs and bays, and T°. vaviabilis on exposed
shores. (The principal references to the biology of Tilapia species in Lake Victoria
are Lowe-McConnell, 1956; Fish, 1951, 1955; Garrod, 1957; and Fryer, 1961.)

As specialized phytoplankton feeders the two Tilapia species probably occupy a
virtually unique trophic niche in the lake. The records of Clarias mossambicus
having ingested large quantities of phytoplankton (Graham, 1929; Greenwood,
1966a) only reflect the omnivoracity of this species (Corbet, 1961) if, that is, the
ingestion of phytoplankton is not just accidental.

Among the Haflochromis species, at least four combine the characteristic gut
morphology of a vegetarian with known records of feeding on phytoplankton (see
p. 39 below). None, however, shows the specialized pharyngeal dentition of the
Tilapia species, nor such relative elongation of the gut. It seems likely that all four
Haplochromis species get their food mainly from bottom deposits (i.e. are like T.
variabilts in their feeding habits, but not in habitat as none has been captured in an
exposed locality).

Only these four Haplochromis can be considered in any way trophically competitive
with the endemic Tilapia species. The whole question of interspecific relationships
between the Tilapia and other species of Lake Victoria is, however, insufficiently
studied for there to be any clear-cut indication of their pattern or consequences.
About all that can be said is that Tilapia and Haplochromis species occur together
in most habitats, and at all sizes, and that some Haplochromis tap the same food
sources as does Tilapia variabilis.

My recognition of Tilapia esculenta and T. variabilis (and by implication other
members of the genus) as specialized species contradicts somewhat the views of
Fryer & Iles (1969, 1972). These authors (1972) believe that species of Talapia

. are in many respects more generalized than most fishes with which we are con-
Bed (other lacustrine cichlids), and even their specialized feeding habits are little
removed from those of “‘bottom grubbers”’’.

That Tilapia are highly adaptable to a variety of habitats and environmental
conditions (a phenomenon well established by field and experimental observations)

16 P. H. GREENWOOD

might, I agree, be considered an indication of generalization. Stenotopic species
usually evolve from a more generalized ancestor to exploit a particular niche. But,
the pharyngeal apparatus of Tapia (especially in the phytoplankton feeders), its
musculature and dentition, and the alimentary tract modifications (see Greenwood,
1953) also constitute a specialized condition within the Cichlidae. Attention may
be drawn to the differences between these characters in the phytoplankton-feeding
Haplochromis species and those in the various Tilapia species. The former only
show marked departure from the generalized, omnivorous Haplochromts in the some-
what lengthened gut ; the pharyngeal apparatus is nowhere near as specialized as it
is in Tilapia. 1 would agree that, anatomically, H. erythrocephalus and other
phytoplankton eating Haplochromis in Lake Victoria do not depart greatly from
generalized ‘bottom grubbers’, but 77/afza I must consider specialized in its feeding
habits.

Unfortunately, few comparative data are available for any intergeneric differences
in digestive physiology. Recent work by Moriarty and Moriarty:(1973) does not,
however, indicate any differences in the ability to digest and assimilate blue-green
algae between Tilapia milotica and the phytoplankton-feeding Hapflochroms mgn-
pinnts of Lake George. (Haplochromis mgripinnis shows about the same departure
from a generalized Haplochromis as does its trophic counterpart, H. erythrocephalus,
in Lake Victoria.)

If it be accepted that the pharyngeal apparatus, and as a correlate the feeding
habits, of Tilapia are specialized it is not surprising that this genus has failed to
produce any great radiation in trophic adaptations comparable with that seen in the
Haplochromis species flocks. The anatomically generalized fluviatile Haplochromis
species (like other generalized animals) have a greater evolutionary potential, as will
be discussed later (p. 103 ef seq).

What is surprising, is the relatively low level of speciation in Tilapia. That there
are about 70 species of Tilapia in Africa compared to nearly 300 Haplochromis species
in Lakes Malawi and Victoria alone underlines this point. In Lake Victoria there
are only two Tilapia species (each derived from a different ancestral lineage), and in

Lake Malawi merely five species (but nevertheless the largest single naturalassemblage —

of Tilapia species in any lake). Furthermore, among the fluviatile Tilapia species
there are many with a considerably greater geographical range than any fluviatile
species of Haplochromis.

The question of why Tziplapia did not speciate to the same degree as did the
Haplochromis in Lake Victoria (whose developmental history [see pp. 10 & 114] would

seem to provide an ideal background for allopatric speciation) is particularly diffi- —
cult to answer. There are, among the Haplochromis of this lake, several instances |
of species multiplication within any one trophic group. That is, evolutionary change |

not involving any change in the particular trophic specializations possessed by the
group. .

The endemic Haplochromts species of Lake Nabugabo (a but recently isolated bay
of Lake Victoria ; see Greenwood 1965b) are another example of speciation without |
noticeable adaptive change in feeding habits. The Tilapia isolated in this lake did |
not speciate.

EVOLUTION OF A CICHLID SPECIES FLOCK 17

It is possible that conditions in the various water bodies which have contributed
to, and have been part of, Lake Victoria did not provide sufficient food for isolated
Tilapia populations to survive long enough for speciation to take place. This,
however, seems a most unlikely explanation. Tilapia, of several species, kept in
aquaria and dams are able to survive and breed on the most atypical diets
(including carnivorous ones), and their adaptability to adverse environments is well
known.

About the only conclusion to be drawn at present is that some inexplicable
genetical stability, and thus evolutionary conservatism, is an inherent characteristic
of Tilapia. By contrast, Haplochromis appears to possess an extreme degree of
genetical instability that manifests itself in the repeated explosive speciation of this
taxon.

The theoretical resolution of this problem is not, unfortunately, quite so simple
when it is extended beyond the genus 77/apza to include other parts of the tilapiine*
lineage.

The supposedly tilapiine derivatives that feature so prominently in the species
flocks of Lake Tanganyika (Regan 1920; Poll 1956) seem to show an evolutionary
potential at least equal to that of the haplochromines in Lakes Victoria and Malawi
and, indeed, in Lake Tanganyika. Doubt has recently been cast on the phyletic
integrity of this lineage in Lake Tanganyika (Fryer & Iles, 1972). If the revised and
admittedly tentative phylogeny of Tanganyika Cichlidae proposed by Fryer & [les
(op. cit. : 502-508) is a better approximation to reality than that implicit in Regan’s
(1920) classification, then the evolutionary potentiality of haplochromines is even
more outstanding.

There is, however, one outstanding example of what seems to be a truly tilapiine
radiation, the fishes of Lake Barombi-Mbo (Trewavas, 1972). The 11 endemic
cichlid species of this isolated crater lake in northwest Cameroons have been carefully
investigated by Trewavas (op. cit.). Four of the five genera present are endemic.
Despite their peculiar oral and pharyngeal dentitions, and their unusual body form,
the tilapiine affinities of the group are more obvious than are those of most Tanganyika
genera. The endemic species of the single non-endemic genus (Saroherodon) depart
quite considerably from the ‘typical’ species of that genus.

For the moment I would consider that the Barombi-Mbo cichlids provide the most
serious challenge to the arguments against tilapiine affinities for the Tanganyika
genera mentioned above.

The deviation, from their nearest relatives, shown by the Barombi-Mbo fishes is
certainly greater than that seen in the four endemic monotypic genera of Lake
Victoria. All four are undoubtedly haplochromine derivatives (Greenwood, 1956a)
as is the fifth and more widely distributed taxon, Astatoreochromis alluaudt (Green-
wood, 1956a, 1959a, 1965b 197384). |

That none of these Lake Victoria taxa is polyspecific like so many of their morpho-
equivalents in Lake Malawi (e.g. the nine genera and 28 species of the ‘Mbuna’
complex, Trewavas, 1935; Fryer, 1959) may be attributable in part to the greater
-* The terms ‘tilapiine’ and ‘haplochromine’ are used here without any formal taxonomic (i.e. sub-

familial) connotation, and merely as convenient handles for the supposed two major cichlid lineages.
2

18 P. H. GREENWOOD

age of Malawi, and in part to the fact that the Victoria species have not exploited a
habitat which was unexploitable by less specialized Haplochromts species.

The five monotypic genera have been distinguished from Haplochromis purely on
the basis of the morphological gap separating each from any Haplochromis in the
lake (Greenwood, 1956a). One genus, Macropleurodus bicolor, is, however, very
closely similar to an extant Haplochromis species, H. prodromus (Greenwood, 1957 ;
and p. 71 below) ; had more been known about the morphology of Victoria Haplo-
chromis at the time of its description (and its later redescription), Macropleurodus
might well have been included in that genus. The same reasoning applies to the
classification of Paralabidochromis victoriae. This species (Greenwood, 1956a) is
known only from a single specimen, whose dentition closely resembles that of the
genus Labidochroms from Lake Malawi (Trewavas, 1935), a fact that certainly
influenced my decision to place it in a separate genus.

The other two genera, Platytaeniodus degeni and Hoplotilapia retrodens, do have
very distinctive dental characters (Text-figs 73 and 74 respectively ; also Greenwood,
1956a). Even now, neither can be related to any particular Haplochromis species within
or without the lake. They provide, in fact, the only recorded instance of specialized
dental or other characters not linked by intermediates to the generalized condition.

Astatoreochromts alluaudi is the only monotypic genus differentiated from Haplo-
chromis by non-dental characters; its differential characteristics are the higher
number of dorsal and anal fin spines, especially the latter (four to six spines cf three
in Haplochromis). It also differs from the other genera in having a distribution that
extends beyond Lake Victoria to include Lakes Nabugabo, Edward and George,
and several small lakes in western Uganda (Greenwood, 1959a, 1965b, 197384).
Unlike most Lake Victoria cichlids, A. alluaudi freely enters streams and swamps.
Within the lake the species shows a wider habitat tolerance than do the other mono-
typic genera and, indeed, many endemic Haplochromts species of the inshore lake
regions. But, like these various species it does not penetrate into water more than
about 20 m deep.

The specialized crushing pharyngeal apparatus of A. alluaudz is identical with that
found in two endemic Haplochromis species, H. tshmaeli and H. pharyngomylus
(Text-fig. 5). The diet of all three species is identical, viz. gastropod molluscs,
especially Melanotdes tuberculata. Despite this shared pharyngeal specialization I
do not think that A. alluaudt is closely related to either of the Haplochromis species.
Indeed, there are good reasons for considering it to be derived from a different stem
to that of the other monotypic genera and the rest of the Haplochromts species flock

(Greenwood, 1954, 1959; also p. 100 below).
Trophically, all the monotypic genera (except Paralabidochromis whose feeding

habits are unknown) can be classed as mollusc eaters. Macropleurodus bicolor

feeds on gastropods, its feeding methods are like those of Haplochromis species that
remove the snail from its shell before ingesting the soft parts (Greenwood, 1957, and
p. 37 below). Hoplotilapia eats, principally, bivalves, crushing the shells between
its broad bands of jaw teeth; Text-fig. 74 (also Greenwood, op. cit.). Astatoreo-
chromis alluaudi feeds on gastropods which are crushed in the hypertrophied
pharyngeal mill (Greenwood, 1959a, 1965c). The feeding habits of Platytaeniodus

ere eres

EVOLUTION OF A CICHLID SPECIES. FLOCK 19

degent (Text-fig. 73) are largely unknown, but bivalves have been recorded from its
gut contents, as have bottom detritus and insect remains (Greenwood, 1956a).

It is clear that despite the outstanding dental characters (Text-figs 73-75) of
these genera, there is little to indicate that any one has entered an adaptive grade,
or a particular habitat, which is not occupied by at least one Haplochromis species
(see below). Perhaps the only point of interest in this context is to note that whereas
Haplochromis species feeding on bivalves crush the shells by means of variously
hypertrophied pharyngeal teeth, the monotypic genera achieve the same ends by
using an hypertrophied oral dentition.

Four of the monotypic genera are female mouth brooders (as are all Lake Victoria
Haplochromis species whose brood care is known) ; nothing is known about breeding
in Paralabidochromts victoriae.

The monotypic genera of Lake Victoria can be equated with the ‘Mbuna’ generic
complex of Lake Malawi (Trewavas, 1935 ; Fryer, 1959) on the basis of their having
distinctive dental and oral characteristics. There, however, the comparison ends
because the ‘Mbuna’ genera have occupied a habitat (rocky surfaces) to the virtual
exclusion of Haflochromis species. In Lake Victoria the monotypic genera are,
from the ecological viewpoint, indistinguishable from Haplochromts species.

Pie Ae LOCH ROMIS SPECIES FVOCK

Introduction

Having reviewed what might almost be considered the ‘minor characters’ amongst
the fishes of Lake Victoria, attention can now be given to that ecologically and
morphologically diverse, closely related and dominant assemblage, the Haplochromis
species flock.

The estimated total of 150-170 Haplochromis species in Lake Victoria is based
partly on the number of species already described (Greenwood, 1956-67 ; Greenwood
& Gee, 1969) but also on the undescribed taxa from collections still under study and
from information given to me by workers who have sampled areas of the lake in
which I have not worked (particularly deep benthic and midwater habitats).

In the accounts that follow, data are drawn mainly from the 95 species that have
been described or redescribed and which I have studied in the field. It must be
emphasized that nothing learned from the still undescribed species in my possession
seriously modifies this picture.

The term ‘species flock’ ( = species swarm of Mayr, 1963) should, strictly speaking,
be applied to a species assemblage of monophyletic origin. A monophyletic origin
cannot definitely be established for the Lake Victoria species, although the evidence
points in that direction. If the origin was not monophyletic then it was extremely
oligophyletic (see below). The existing species are certainly more closely related
to one another than to any species outside the lake, and it seems justifiable to refer
to the assemblage as a species flock.

The Haplochromis of Lake Nabugabo (Greenwood, 1965b), of course, contradict
these last remarks. But Nabugabo cannot, in this context, be considered ‘another’

lake ; were it not for a narrow sandbar it would be part of Lake Victoria.

20 P. H. GREENWOOD

A close relationship between the species of Lake Victoria and those of Lakes
Edward and George (but not Rudolf and Albert) cannot be denied. In fact, if
Haplochromis from either of these lakes were put into Lake Victoria, they would not
seem at all ‘out of place’ toataxonomist. The same cannot be said for the majority
of Haplochromis species from Lake Malawi. For example, in all but one or two
species the Malawi Haflochromis have the caudal fin covered by small scales ; only
the basal third, rarely the proximal half of this fin is scaled in Victoria species. And
again, there are male breeding colours and colour patterns among Malawi Haplo-
chromis and related genera that do not occur in the Victoria flock (Regan, 1921 ;
Fryer & Iles, 1972 ; personal observations). :

The problem of a mono- or polyphyletic origin for the Lake Victoria flock is not a
simple one to solve (Astatoreochromis alluaudi excepted since it is manifestly more
closely related to species outside the flock, see p. 100). |

Tt has long been thought, on morphological evidence, that the flock could have

stemmed from a single species (Regan, 1922; Trewavas, 1949). Finding evidence

to refute this hypothesis is difficult, and is bound to be so if the mid-Pleistocene rivers
of eastern Africa carried a similar Hapflochromis species complement to that of the
present-day rivers — one or at most two very closely related species.

There seem to be no grounds for assuming that the situation might be any dif-
ferent in mid-Pleistocene times. Even if different species did occur in neighbouring
rivers, the chances are that they would be closely related. Thus it is not surprising
to find that many elements from the species flocks of Lakes Victoria, Edward, George,
Albert and Rudolf have a close overall resemblance to one another. The rivers
that first drained into these lakes were all part of the east African highland drainage,
and presumably carried the same or genetically similar Haplochromis species.

The relicts of this drainage system are now populated by a single Haplochromis
species. Previously this fish was thought to be H. wingatu (see Trewavas, 1933) but
recent work indicates that it is either H. bloyett or a closely related species (Green-
wood, 1971). Haplochromis wingatu is restricted to the Nile and Lake Albert, and
appears to represent a lineage quite distinct from that of most east African lake
Haplochromis species (see Greenwood, 1971, 19738).

Lake Malawi is geographically far removed from the rivers of the old east African
drainage and it is likely that its ancestral Haplochroms populations would differ from
those of Lakes Victoria, Edward and Albert (see p. 99). The modern representative
of the basal Haplochromis stock in Lake Malawi is thought to be H. calipterus
(Trewavas, 1949). Structurally, this species too is not far removed from H. bloyet.

Lake Tanganyika poses a problem. Geographically and hydrographically it lies
within the range of present-day H. bloyeti (unpublished observations) yet its cichlid
flocks are very different from those of Lake Victoria (Regan, 1920; Poll, 1956;
Fryer & Iles, 1972). For one thing, the genus Haplochromis is barely represented
in the lake by two species. One of these (H. burtoni) is a generalized species of
restricted intralacustrine distribution (Poll, of. cit.; personal observations). The
other (H. horet) is a moderately specialized predator also of relatively restricted
intralacustrine distribution. Furthermore, nearly half the species flock is composed

of genera apparently belonging to the tilapiine lineage (Regan, 1920; but see p. 17

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EVOLUTION (\OFUVA CICHLID::SPECIES FLOCK 21

above). Those genera belonging to the haplochromine lineage are as distinct from
the general Haplochromis morphotype as are the monotypic genera of Lake Victoria,
or even more So.

Here then we have the anomaly of two geographically distinct lakes, Victoria and
Malawi, with basically similar species flocks neither of which resembles superficially
or phylogenetically that of the geographically interposed Lake Tanganyika. No
immediate explanation is available.

Of course the flock in Lake Tanganyika (even restricting comparisons to supposedly
haplochromine derivatives) is much further differentiated than that of Victoria —
probably a reflection of the lake’s greater age — thereby making an inter-lake assess-
ment of relationships very difficult. But, even allowing for differences in lake age,
topography and history, there does seem to be a prima facie case for thinking that the
ancestral species in Lake Tanganyika were quite different from the progenitor or
progenitors of the Lake Victoria flock.

Basic morphology

Viewed in their entirety the Lake Victoria Haplochromis species show remarkably
little diversity in body form, particularly when compared to the species flocks in
other lakes (compare Text-fig. 3 with figs. 5-23 in Fryer & Hes, 1972).

The piscivorous predators, as a whole, are generally recognizable by their rather
elongate form and large mouth (see Text-figs 3, 11-15, 52-56 and 58-64). But, in
this trophic group there are several species (the ‘sevranus’ group in particular,
Greenwood, 1967) that, apart from their larger size, closely resemble the trophically
unspecialized species (cf Text-fig. 9 with Text-fig. 48). Even some of the most
specialized predators, the paedophagous species (Greenwood, 1959b ; and pp. 31-37
below), are not particularly outstanding in their superficial appearance (see Text-figs
16-18). There are, of course, exceptions and again most of these are found amongst
the piscivores. In these species the outstanding morphological features are as-
sociated with the head, like a strongly prognathous lower jaw, an upwardly directed
mouth, or the deeply concave dorsal head profile often associated with this mouth
form (see Text-figs 14, 56, and 64).

The generalized Haplochromis body and head shape (found in more than half of
the known species) cloaks a wide variety of trophic specializations, from algal
grazing to mollusc eating and even predation on other Haplochromis.

These remarks apply to first impressions coming from a superficial examination
of the fishes. Closer inspection in many cases shows differences in jaw and tooth
morphology among otherwise similar species. Indeed, it is in the head and dentition
that the real diversity of these species becomes apparent, and in which lies the
evolutionary success of the Haplochromis species flock. Nevertheless, even the most
extreme forms (except for two of the monotypic genera ; p. 103) are linked with the
generalized type by species showing between them all intermediate stages in the
development of a particular characteristic.

From the last few remarks it must not be concluded that every species is 1m-
mediately distinguishable by its cranial characters. Rather, these should be taken as
‘species group’ characters, shared in many instances by more than half a dozen

22 Pp, H. GREENWOOD

H. pallidus

Hse ee MUN?
i a

EA
<=<=S . ee =
H. chilotes ~~

Macropleurodus bicolor

nae MM ify

i “Za seamen i
(@) = @) . fos
Rog SS oe

eE SS SS
H. saxicola & H. empodisma WS Ss

Outline drawings (not to scale) of various Lake Victoria Haplochromis species
(and one monotypic genus, Macropleurodus bicolor) to show range of body form in this
species flock.

Fic. 3.

EVOLUTION:-OF A CICHLID SPECIES. FPLOCK 23

H. ishmaeli

De oy VG p74
Mh foefff B=
{7 {ff ff fi, Yf AY y P oo
Z Yi V4 or
LF >
LEE

H. dentex

H. obesus

SS SS H. longirostris

H. parvidens Mtl Wipes

H. guiarti.

H. macrognathus

24 P. H. GREENWOOD

species. The two mollusc-eating species groups (Greenwood, 1957, 1960), the
‘tvidens’ group of species feeding on benthic Crustacea in deep water (Greenwood &
Gee, 1969) and the several morphogroups of piscivorous predators (Greenwood, 1962,
1967) typifying this situation. Within a group the morphological characters
separating species are mainly slight proportional differences, squamation patterns,
differences in the number or disposition of teeth (and less commonly tooth shape)
and, most clearly, differences in male breeding coloration (see p. 52 below and Plate
I). In most of what may be termed ‘specific characters’, except male coloration,
there is a high level of individual variability.

To exemplify this last point, and at the same time to emphasize the relative in-
variability of some morphological features, one may consider the meristic characters
of the flock. The range of fin ray numbers, lateral line and most other scale counts,
and the number of vertebrae is such that the range for the entire flock can be en-
countered in one species. There are a few exceptions to this generalization ; all are

species with an elongate body form. In the exceptional species, the modal number ~

and upper limits for the range of vertebral and lateral line scale counts may lie beyond
the general range, but the lower limits lie within that range.

Few species show any external evidence of modifications associated with a par-
ticular habitat. Exceptional in this regard are some, but not all, species from deeper
water (i.e. > 50m). These fishes have relatively larger eyes, and the cephalic
laterosensory canals and openings are slightly enlarged, presumably as adaptations
to a dimly lit environment (Greenwood & Gee, 1969 ; Greenwood, 1973a).

Adult individuals of most species are small fishes, between 70 and 110 mm long,
but with some of the piscivorous predators growing to lengths of 180-220 mm.

In all the morphological features discussed so far, the Lake Victoria Haplochromis
flock (including the monotypic genera) shows less diversity than does the flock in
Lake Malawi (even if the derivative genera are excluded). Because few morpho-
metric data are available for individual species of Malawi Haplochromis, it is im-
possible to compare the levels of intraspecific variability in the two flocks.

Contrasting with the relative uniformity of body shape, the jaw teeth and dental
patterns in Lake Victoria Haplochromis show a much wider range of diversity (see
Text-figs 4, 36, 39 and 41). It is this particular diversity, more than any other
factor, that has contributed to the success of these fishes in the lake (and in other
lakes). There are, of course, correlated changes in syncranial architecture, especially
neurocranial shape, and many of these are probably to be considered the primary
changes involved inanadaptiveradiation. Certainly, takenin concert, skull form and

dentition are basic to the trophic radiation so characteristic of all cichlid species flocks.

The well-developed pharyngeal apparatus of the cichlids (i.e. the toothed and
separate upper pharyngeal bones and the toothed but suturally united lower ele-

ments, together with the associated musculature) are effectively a second pair of

jaws. In many species these ‘jaws’ are of greater importance than the true jaws, or
at least have given the species an enhanced potential for exploiting a wider variety
of food sources.

Examples of this potential realized are found in the phytoplankton feeders (Green-
wood, 1953), the mollusc eaters (Greenwood, 1959a, 1960) and in the piscivorous

EVOLUTION OF A CICHLID SPECIES FLOCK 25

Fic. 4. Jaw teeth of various Haplochromis species.

A: H. macrops (an omnivore) ; bicuspid outer and tricuspid inner tooth from the
dentary. These teeth may be considered as representative of the typical generalized
tooth form.

B: Unicuspid, caniniform outer teeth from the premaxilla of H. dentew (a piscivore),
showing different degrees of curvature.

C: Stout, strongly recurved, bicuspid outer row tooth from the dentary of H. welcommei
(a scale scraper) in buccal (left) and lateral (right) views.

D-G: Teeth of four vegetarian species showing morphological stages in the evolution of
specialized, obliquely cuspidate cuter teeth in the periphyton grazer, H. obliquidens (G).
The species represented are: (D) H. evythrocephalus (phytoplankton eater), (E) H. nuchi-
squamulatus, (F) H. lividus and (G) H. obliquidens, all periphyton grazers (see p. 39).

predators (Greenwood, 1962). Phytoplankton feeders have the pharyngeal teeth
fine and hooked, thus enabling the fish to comb aggregates of mucus and phyto-
plankton into the oesophagus. In mollusc eaters the molariform pharyngeal teeth
(Text-fig. 5), strong pharyngeal bones and powerful upper branchial musculature
enable the fish to crush gastropod shells. In piscivores (Greenwood, 1962 : 211)
there is a macerating action of the strong but fine upper and lower pharyngeal teeth
moving against the prey caught between them. This allows the predator to ingest
much larger prey than would be possible if the food was bolted whole (as is the usual
-way in most non-cichlids).

Such examples are, in some respects, extreme cases. Most species have what can
be described as a ‘general purpose’ pharyngeal apparatus. Consequently there is,

26 P. H. GREENWOOD

on the whole, rather less diversity in bone form and tooth shape than is seen in the
morphology and dentition of the jaws.

In the jaws (premaxillary and dentary bones) there is always an outer row of large
teeth, followed by from one to five (sometimes more, but usually two or three) rows
of much smaller teeth (Text-fig. 41A). Teeth in the outer row show greater vals
in shape and size (Text-fig. 4) than do those of the inner series.

Fic. 5. Lower pharyngeal bones (in occlusal view) of four species to show increasing
molarization of the teeth associated with an increasingly molluscivorous diet. Haplo-
chromis empodisma (extreme right) has a mixed diet of insects and bottom detritus while
H. pharyngomylus (extreme left) is exclusively molluscivorous when adult. Drawings
not to scale. B: H. obtusidens. C: H. humilior.

Inner teeth are generally tricuspid or unicuspid ; their main contribution to dental
diversity is in the number and pattern of the rows present. For example, there are
the broad bands of fine, tricuspid inner teeth in those species that scrape epiphytic
and epilithic algae (e.g. H. obliquidens, H. lividus, H. mgricans and H. nuchisqua-
mulatus ; Greenwood, 1956b) or, ike H. welcomme1, which scrapes scales from the
caudal fins of other cichlids (Text-fig. 39 ; and Greenwood, 1966b). Broad bands,
this time of stouter teeth (Text-fig. 41), are found in certain of the species feeding on
molluscs, either by wrenching the snail from its shell or by crushing the shell between
the jaws as in H. prodromus, H. granti and H. xenognathus ; see Greenwood, 1957.
The ultimate development of this trend is seen in the broad and posteriorly expanded
inner tooth rows of Hoplotilapia retrodens and Platytaeniodus degen (Text-figs 73
and 74).

Teeth from the outer row in the premaxilla and dentary are, despite their diversity
in form, variants of two basic types (Text-fig. 4). In one, the crown is compressed
and unequally bicuspid, in the other the crown is conical and protracted into a single
sharp point (i.e. it is unicuspid). Occasionally, tricuspid teeth are found in the
outer rows, but with few exceptions (e.g. H. tvidens and related species ; Greenwood
& Gee, 1969) are never common anteriorly in the jaws.

Teeth morphologically intermediate between the fully bicuspid and the unicuspid |
type are known, but never seem to occur in the same species or in the same individual
(except as the result of wear on a bicuspid).

The bicuspid tooth is, by analogy with teeth in generalized and fluviatile species
like H. bloyeti, taken to be the basic and generalized tooth form (Text-fig 30B). It
also seems to be the juvenile tooth form irrespective of the definitive tooth shape for a

EVOLULION-OF A CICHLID SPECIES. FLOCK 27

particular species. This temporal succession is seen, albeit in muted form, among
species whose definitive dentition is that of unequally bicuspid teeth ; in some large
antividuals of these species there is often an admixture of bi- and unicuspids in the
inderior and lateral parts of the dental arcade.

One or two relatively enlarged unicuspids are generally developed at the posterior
end of the outer tooth row in the premaxilla, irrespective of tooth shape elsewhere in
this jaw ; exceptional are the few species like H. obliquidens (Text-fig 4G) where
crown form is very greatly modified from the usual condition.

Tooth succession is vertical, the replacement teeth developing in alveoli beneath
the erupted and functional teeth. As far as can be determined, the replacement of
outer teeth is more regular than that of inner ones (personal observations).

The basic bicuspid tooth has one cusp (the major cusp) noticeably larger than the
other (Text-fig. 4A and D). Both major and minor cusps are triangular in outline,
and lie in the same plane. Variations on this pattern involve changes in the size of the
apical angle of the cusps, changes in the relative sizes of the two cusps or the inclina-
tion of one cusp away from the plane of the other. The minor can be as large as the
major (Text-fig. 36) or the latter can be drawn out obliquely into a scraping blade
many times larger than the minor cusp (Text-fig. 4G).

Another but rarer type of variation involves a coarsening of the whole tooth with
a consequent increase in the breadth of the crown ; sometimes this trend is combined
with one of those noted earlier, and results in the powerful teeth of Macropleurodus
bicolor, an admittedly extreme example of this trend (Text-fig. 75).

The length of a tooth’s neck also varies interspecifically, as does its circumference.
In consequence, teeth can be short and stout, long and slender, or of a intermediate
type, but all with a similar cusp shape.

Unicuspid teeth differ in relative size, degree of curvature (usually in the neck of
the tooth, but sometimes in the angle between the crown and neck, as in HZ. obesus,
H. maxillaris and H. melanopterus ; see Greenwood, 1959b), or in the angle at which
the whole tooth is implanted on the jaw bone. These differences are well exemplified
by the more specialized piscivorous species, and by some of the specialized insectivores
and certain mollusc eaters. In the former group (Greenwood, 1962, 1967), the teeth
are large and strongly recurved, thereby providing a means for gripping the prey
while the pharyngeal teeth macerate it preparatory to swallowing. In certain
specialized insectivores and mollusc eaters the teeth are also relatively enlarged, and
although the tips are recurved, the teeth are implanted so as to project forward
(Greenwood, 1957, and 1959b : 207-211). The procumbent teeth in the insectivores
(especially H. chilotes, Text-fig. 33) create an effective ‘forceps’ used to remove
burrowing insects from their holes. In the molluscivores, the teeth are used either
to hold a snail while it is eased from its shell, or actually to crush the shell away from
the body.

Lake Malawi Haplochromis (and especially the derivative genera) show an even
greater range of dental morphology and arrangement. The difference is clearly
seen by comparing Text-figs 4, 36 and 73-75 here with those for Malawi species
published by Fryer (1959) and Fryer & Iles (1972) ; similarly for the haplochromine
species of Lake Tanganyika (Poll, 1956 ; Fryer & Iles, op. cit.).

28 P. H. GREENWOOD

The whole subject of cranial and dental morphology in the Lake Victoria Haplo-
chromts flock is dealt with in greater detail below (pp. 56-99). For the moment it
must suffice to note that although species showing specialized dental, pharyngeal and
syncranial characters are very distinctive (and readily advertise their feeding habits)
the majority are linked, through species with these characters at an intermediate
stage, to the generalized type (see Text-figs 4, 5 and 65-60). :

Many of these morpho-lineages appear also to be truly phyletic ones because the
component taxa can be related, primarily, though shared specializations, and secon-
darily by degrees of specialization in the same characters. There are a few instances
where intraspecific variability in a complex of specialized characters is such that,
were only the extreme individuals known, they would probably be classified as a
separate genus (for example, H. xenognathus, Greenwood, 1957; and H. welcommei,
Greenwood, 1966b).

Surprisingly, amongst species with such diverse feeding habits, there is little
diversity in the shape, length or number of gill rakers; the modal numbers of rakers
aregorio. The plankton-feeding species (e.g. H. erythrocephalus ; Text-fig. 6) have

A

Why,

~.
“.,

vorous—piscivorous species) and B: H. erythrocephalus (a phytoplankton feeder).

rakers that are but marginally longer than those of an insectivore, are only a little
more closely spaced, and are more numerous by one or two rakers. No explanation —
can be offered, except that the feeding mechanism of phytoplankton feeders may not
require the evolution of close-set and fine rakers. These species entangle the plank-
ton in mucus boli that are too large to pass through even the relatively wide spaces
between rakers of the first row ; subsequent rows of rakers interdigitate and have

even smaller interspaces (Greenwood, 1953 ; and unpublished observations on several
Haplochromis species).

EVOLUTION OF A CICHLID SPECIES FLOCK “2g

The theory of character displacement (Brown & Wilson, 1956) may be discussed
here because it has been largely established on morphological characters, and because
it would seem to be of particular relevance to a species flock situation. Its ecological
counterpart, the concept of competitive exclusion (Gause’s Law), will be considered
later (p. 48) when discussing species’ interrelationships in the lake.

In essence, the theory of character displacement postulates that closely related
sympatric species will generally show more differences than similarly related allopatric
ones. In other words, selection will sharpen differences between sympatric species
if these differences lead to reduced interspecific competition. A species flock should,
therefore, provide good material against which to check the first premise of the
theory, although the second premise cannot be tested because none of the species
ever occurs allopatrically with a close relative.

The general effect of character displacement seems to be discernible within the
flock for many morphological features (and, by implication, even more clearly for
ethological characters, see p. 51). A most striking example is provided by the dif-
ferences in male breeding coloration (see p. 52). This example is particularly
interesting because interspecific colour differences are most marked among species
that occur syntopically and are less obvious between allotopic species.

The picture for other morphological features, especially anatomical ones, is far
less obvious, and at first glance might even seem to contradict the idea of enhanced
differentiation between sympatric species.

To illustrate this difficulty one can take the several anatomically and morphometri-
cally stmilar species clustered around any one adaptive peak in a phyletic lineage.
This is especially well demonstrated among such disparate groups as the generalized
insectivores (Greenwood, 1960), in the specialized mollusc crushers (Greenwood, of.
cit.), and particularly in the piscivores (Greenwood, 1962, 1967). However, traces
of character displacement are evident, not so much at the level of individual species
but at the level of species groups (i.e. phyletic lineages.) The characteristic features
of these groups are, almost without exception, trenchantly defined.

Proximately, of course, what are now recognizable as phyletic groups must have
originated as species. It was presumably at that level and at that time that selec-
tion pressure, and hence character displacement, was most intense.

The mosaic of interspecific similarities and dissimilarities in the Hapflochromis of
Lake Victoria could well mirror the way in which the flock evolved. Character
displacement (and the origin of phyletic lines) would be most marked during early
phases of lake development when a high premium might be placed on trophic speciali-
zation. Character replication, through simple speciation without obvious adaptive
change, is likely to be a feature of later lake development, with the isolation and re-
incorporation of peripheral, Nabugabo-like lakes (see p. 112).

_ That intragroup character replication should exist on the scale it does among these
fishes is certainly unusual (see the numerous contrary examples cited by Brown &
Wilson, 1956). It seems to suggest two possible explanations, either a lowered level
_ of competition and selection during certain phases of lake evolution, or the involve-
ment of adaptive characters other than those reflected in morphological features. A
temporal factor may also be involved. Ona purely subjective assessment there seems

30 Po oe GREENWOOD

to be greater interspecific differentiation among the Haplochromis species of Lake
Malawi than those of Lake Victoria. The Malawi flock is older (see p. 6), and
during its longer life perhaps some of the less distinctive taxa (1.e. less particularly
specialized species) have been eliminated at times of more rigorous selection.

Feeding habits of the Haplochromts species

The importance of trophic specializations in the adaptive radiation of Lake Vic-
toria Haplochromis species has long been recognized (see Regan, 1921, in the pre-
factory remarks to the first systematic revision of these fishes). The full magnitude
of this radiation only became apparent, however, when field studies were made
(Graham, 1929; Greenwood, 1959c, 1905a, 1973b, and in taxonomic papers dealing
with these species, 1956-69).

Lake Victoria Haplochromis species are by no means unique in this respect, and
the phenomenon can be considered a characteristic of cichlid fishes in many African
lakes (and elsewhere in the world). Outlines of these different radiations were
published, for Lake George by Greenwood, 1973a ; for Lake Malawi by Fryer, 1959
and especially by Fryer & Iles, 1972; for Lake Tanganyika by Poll, 1956 (also in
Fryer & Iles, op. cit.), and for Lake Albert by Trewavas, 1938.

When discussing Haplochromis feeding habits in Lake Victoria certain points must
be borne in mind. First, the food of small fishes (i.e. < 20 mm long) is unknown for
the majority of species, partly because small individuals were rarely caught, but
mainly because it is impossible to identify fishes of this size. Second, fishes caught
by trawling in deep water usually have everted guts when brought to the surface,
and much of the food is lost in this way. Finally, there has been little detailed
research (like that of Corbet’s [1961] on non-cichlids) into the food of Haplochromis ;
what data there are, derive chiefly as an offshoot from my own taxonomic studies.

Within these limitations it is possible, however, to say that every major food
source in the lake, except for zooplankton, has been exploited by one or several
Haplochromis species (Text-fig. 7).

Insects, especially larval and pupal chironomids and Ephemeroptera, are prob-
ably the most important food organisms. Besides the 11 species* feeding principally
on insects many others include some insect material in the diet, either regularly or
opportunistically.

Most insectivores are morphologically (Text-figs 3, 8-g and 42) and dentally
generalized fishes, with bicuspid jaw teeth, generalized jaw structure (Text-figs 31

* Only the 95 species so far dealt with in my revision are used in these analyses.

Fic. 7. Diagrammatic representation of feeding habits in the Lake Victoria Haplochromis
species studied to date (see p. 19). For details of species in the H. macrops, H. serranus,
H. prognathus and H. tridens species complexes see text, pp. 58; 81; 85; and 67.

Where more than one food is represented, the lengths of the bars are not strictly pro-
portional ; they should be considered merely as indicative of the relative importance of
the particular foods in the diet of that species. Only the principal types of food organisms
are shown. ‘The species are arranged in phylogenetic groups (see Text-fig. 70).

TZ FO

H. brownae

H. cinereus TILL LL

H. pharyngomylus

=n” An

sei 8

snuajdourjew) ‘H

H. bloyeti — like
ancestor

mH

salineds ¢
one

Hadios Sd

@
H. Rrogna
(eo)
s e
Farban,
e@
cr,
14
e Ploda,
LY, iy
N NO) “roy
N NA i
V N Q %
mm ‘A.
\ IS on
\ *
Vo @
; %
V \ 4 “yg
z %,
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@ %
eS :
a 6.
Je % N Insects ig Mollusca
(w
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—<

Bg Phytoplankton ij Fish

-

H, serranus complex
(IN species)

H. parorthostoma

thy.
* (20 speqi ote,

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Detritus

<

1! eee

un
8
e Periphyton Macrophytes Crustacea

Fish eggs &
larvae

Rie

Br
sano

ye
+
‘

EVOLUTION OF A CICHLID SPECIES FLOCK 31

and 33) and a pharyngeal apparatus as unspecialized as the primary jaws (Text-figs
5D and 30). The indications are that these species feed by sucking or picking their
prey from the bottom or other substrata (plants, rocks, etc.).

The most specialized insectivore, H. chilotes (Text-fig. 10), is also, by virtue.of its
hypertrophied lips, the most easily recognized species in the whole flock. Anatomi-
cally, H. chilotes has a forceps dentition of procumbent, unicuspid and slightly
curved teeth (Text-fig. 33 also see p. 27 and p. 61 below). With these teeth H.
chilotes is able to extract the larvae of a boring mayfly (Povilla adusta) from their
burrows ; prawns are also probably removed in the same way from cracks and holes
in rocks. The hypertrophied lips (which are highly variable in their degree of
development) seem to serve merely as shock absorbers when the fish forces its mouth
against the rock or wood face ; histological examination of lip tissue does not show
any particular increase in the number of sensory cells as compared to lip tissue from
other species. Free-living insect larvae are also eaten by H. chilotes, and presumably
taken, like the food of less specialized species, from the lake bottom.

Another species, H. chromogynos, has teeth and jaws closely similar to those of H.
chilotes (see Text-fig. 33), but there is no suggestion from its known food (larval
Diptera) of specialized feeding habits.

Next to insects, fishes are probably the most important source of food for Haplo-
chromis (Greenwood, 1962, 1905a, 1967). I have estimated (Greenwood, 1959¢,
1967) that about 40 per cent of Haplochromis species in Lake Victoria are piscivorous
predators. With more knowledge of deep water species (Greenwood & Gee, 1969 ;
unpublished observations) I would now reduce that figure to one of about 30 per cent,
still a high proportion.

Most of the fishes eaten by the piscivores are other Haplochromis, although small
cyprinids (especially Engraulicypris argenteus) constitute part of the diet in the larger
predators. ‘The fish remains recovered from a predator’s guts are so macerated that
it is generally impossible to identify the species of the Haplochromis prey consumed.
Generic identification, however, is certain. No Tilapia remains have ever been iden-
tified with certainty ; probably this is because the young TiJapza (of both species)
are ‘protected’ in their nursery zones (where Haplochromts species do not penetrate)
until they reach a size where they are too large to be eaten by a predatory Haplo-
chromis.

The clearly recognizable ‘predatory’ facies of fish-eating Haplochromis (see Text-
figs 3, 12-15 and 52-63) was noted before. There are, however, a few species which
superficially and even in their dentition and mouth size could well be mistaken for
generalized insectivores (see Text-figs 48 and 50). The principal components of the
‘predatory facies’ are a large, moderately distensible mouth, strong unicuspid jaw
_-teeth (Text-fig. 4B), and pharyngeal teeth, also strong, with the crowns so orientated
and shaped as to form a macerating mill. Some piscivorous Haplochromis are
-among the largest in the lake, reaching, when adult, lengths of between 200 and
300 mm.

__ Also to be included in the piscivore category is a group of eight species that feed
exclusively (or principally) on the embryos and yolk-sac larvae of other cichlids
(Greenwood, 1959b, 1967). The feeding habits are definitely established for six of

P. H. GREENWOOD

OS aes
he

Fic. 9. Haplochromis pallidus, an insectivore. (Natural size.)

Fic. 10. Haplochromis chilotes, a specialized insectivore ; see p. 31. (Natural size.)

EVOLUTION. OF A CICHLID SPECIES FLOCK 33

these species, strongly indicated for the seventh and assumed on anatomical grounds,
for the eighth species.

Apparently none of these paedophagous species preys on the embryos or larvae of
non-cichlid fishes. This is not surprising when one recalls that most non-cichlids
breed outside the lake (Greenwood, 1966 ; Corbet, 1960) and then only biannually.
Cichlids, on the other hand, spawn throughout the year (see p. 51). However, all
the Lake Victoria Haplochromis (and other cichlids) for which data are available
brood the embryos and larvae in the female parent’s mouth ; there are no indications
whatsoever that any cichlid in the lake does not practise mouth-brooding. One
might reasonably conclude, therefore, that the paedophages have evolved some
method of obtaining their food from the mouth of a brooding female (but see
below).

Two lineages are involved in this trophic specialization (see p. 75), with both
showing a certain degree of convergence (pace Fryer & Iles, 1972: 101). For in-
stance, there is a marked trend towards increased distensibility and protrusibility of
the mouth, and a tendency for the teeth to be buried in a thickened oral mucosa (so
much so that superficially the more specialized species in each lineage appear to be
edentulous). The least specialized species in each lineage, H. cronus (Text-fig. 16)
and H. barbarae (Text-fig. 29), differ little from the trophically generalized species
at their particular level of overall specialization (see Greenwood, 1959b and 1967 for
the species respectively). That is, H. cronus resembles certain species in the benthic
omnivore-insectivore grade, and H. barbarae species in the near basal piscivore grade.

Precisely how the paedophagous predators obtain their food has not been estab-
lished. The turbid water of Lake Victoria effectively prevents underwater observa-
tions, and aquarium studies have yielded equivocal results. In an aquarium #H.
parvidens (Text-fig. 18) did show behavioural patterns suggesting that it might engulf
the snout of a brooding female, and in this way force it to disgorge its brood. Cer-
tainly the very distensible mouth characterizing all but the two most generalized
paedophages lends support to the idea of snout-engulfing. The deeply embedded
teeth also give support to this idea, since hidden in this way there would be less
chance of the attacker becoming too firmly attached to the brooding female. If the
predator has to struggle to free itself there is a danger of it losing its meal in the
process.

On the other hand, a greatly distensible mouth could be an adaptation for sucking
in the small, dispersing prey should the mother be induced by some other means to
jettison her brood. In either eventuality it must be emphasized that brooding
female H aplochromis are extremely tenacious of their broods, even when under great
stress, like capture in a seine-net, handling after CONC or being chased around an
aquarium (personal observations).

Fryer & Iles (1972) do not think it likely that paedophagous species get their food
by directly attacking or threatening the parent fish. Instead, they believe that the
predators rely on brooding females jettisoning a brood without direct interference
from external sources. That females should voluntarily abandon their broods is
thought by Fryer & Iles to be one of several homeostatic population density control
mechanisms operating within the flock.

3

34

Fic. 11. Haplochromis serranus, a piscivore.

hiGs 12

HIG: 13;

P. He GREENWOOD

Haplochromis spekii, a piscivore.

Haplochromis prognathus, a piscivore.

(Half natural size.)

(Half natural size.)

—

EVOLUTION OF A CICHLITD SPECIES FLOCK 35

Fic. 14. Haplochvomis estoy, a piscivore. (Half natural size.)

Fig. 15. Haplochromis mento, a piscivore. (Half natural size.)

Fic. 16. Haplochvomis cronus, a paedophage ; see p. 33.

P. H. GREENWOOD

Fic. 18. Haplochromis parvidens, a paedophage. (Half natural size.)

CSE
Z Xela 1
EONS aie i

SS

Fic. 19. Haplochromis sauvagei, a mollusc eater (oral sheller, see p. 69). (Natural size.)

EVOLUTION OF: A CICHLID SPECIES FLOCK 377

With no direct evidence to support either suggested mode of food gathering,
further speculation is pointless. However, I cannot agree with some of the evidence
(or interpretation of observations) that Fryer & Iles (op. cit. : 101) use in support of
their thesis for homeostatically induced jettisoning of the brood. As this evidence
is concerned mainly with anatomical features and questions of physiology, discussion
is deferred to a later page (p. 75 ef seq.).

As to the origin of paedophagy, I would agree with Fryer & Iles (op. cit.) that it,
like other trophic specializations, stemmed from an originally facultative habit later
selected for, and further developed by, the evolution of more specific anatomical
specializations. Certainly the existing ‘basic’ paedophages, H. cronus and 4H.
barbarae, could not be excluded from other trophic groups on anatomical grounds alone.

Haplochromis species feeding on Mollusca form a fairly well-defined group which
does, however, intergrade with the insectivorous one ; some species have a mixed
insect and mollusc diet. .

Ten species can be classed as predominantly molluscivorous. In this group there
is a clear-cut dichotomy into species that crush the prey in the pharyngeal mill (six
species) and those either wrenching the snail from its shell or crushing the shell be-
tween the jaws before swallowing the soft parts (four species). It will be recalled
that at least two monotypic genera (Hoplotilapia and Macropleurodus) belong to the
second group, a third (Platytaeniodus) may do so, and that a fourth (A statoreochromis)
belongs to the first category.

Those species crushing or dismembering molluscs orally form a distinct phyletic
assemblage (Greenwood, 1957; and p. 69 et seg. below) which includes one of the
monotypic genera, Macropleurodus bicolor. Snails are the chief food organisms of
this group.

The species that crush molluscs (both bivalves and gastropods) intrapharyngeally
are of diverse relationships (see p. 72). A common feature in all, however, is some
degree of hypertrophy in the pharyngeal bones, particularly the lower one, and some
molarization of the dentition on these bones (again, particularly the lower one, see
Text-fig. 5). In the virtually exclusive mollusc eaters (H. ishmaeli and H. pharyn-
gomylus, Text figs 3 and 23), these bones and their dentition reach the peak of
development seen in this trophic group (see Text-fig. 5 and Greenwood, 1960).
Other members of the group (e.g. H. theliodon, H. humilior [Text-fig. 22], H. riponianus
[Text-fig. 42] and H. obtusidens) have the lower pharyngeal bone but slightly stouter
than that in generalized species ; usually only the median tooth rows show any
molarization. It is these species which, to a certain extent, are the mixed mollusc-
insect eaters, and in which bivalves predominate over gastropods in the diet (Green-
wood, 1960).

In terms of a restricted diet, and in associated anatomical specializations, the
mollusc-eating Haplochromis (particularly the pharyngeal crushers) clearly show
species at every major stage in the development of the trend (Text-fig. 5A, B,C). It
seems likely that the anatomical ability to crush mollusc shells has evolved, indepen-
dently, on a number of occasions. But at least one phyletic line can be detected, with
representatives of its insect—-mollusc eating species, bivalve-gastropod eating species
and almost exclusively gastropod eating species, still extant (see pp. 69-75 below).

38

FIG. 20.

P. H. GREENWOOD

Haplochromis granti, a mollusc eater (oral sheller). (About natural size.)

ea
any ryt
a ae Ss ™ >,
SAE

(Natural size.)

FIGs 22°

Haplochromis humilioy, a mixed mollusc—insect eater, the molluscs are crushed
in the pharynx. (Natural size.)

EVOLUTION :OF .A{ CICHLID SPECIES FLOCK 39

Small Crustacea, especially ostracods and, to a lesser extent, prawns of the genus
Caridina, contribute to the diet of several Haflochromis species in the insectivore
and the mollusc-insectivorous trophic groups.

There is, however, a small group of five species that appear to feed equally on
insects and Caridina (Greenwood & Gee, 1969; Greenwood, 1967 for H. tridens).
All are bottom feeders and most occur in water 20-35 m deep (with one species
extending into shallow water). Almost certainly more species will be added to this
group when undescribed material from the deep waters of the lake is analysed. No
obviously adaptive anatomical features are associated with the insect—crustacean
diet ; all the species in this group, with one possible exception, appear to be closely
related (Greenwood & Gee, I969 ; and p. 67 below; Text-figs 24 and 25).

Plant material (especially algae) is frequently found in the guts of bottom feeders
whose food is otherwise of animal origin. The nutritive value of the plant material
in the diet of such species is unknown ; usually the quantity ingested is small and
rarely does it appear to be digested completely.

Eight species, however, show the characteristically long, much coiled intestine
and the highly distensible stomach, associated with a truly vegetarian diet. The
gut contents of all eight species confirm their placement in this trophic category.
Once again, there are indications from the unstudied material at my disposal that
the number of phytophagous species will be increased eventually.

The plant eating species can be split into three subgroups: those feeding on epi-
phytic and epilithic algae, those feeding on phytoplankton and those eating macro-
phytic plants.

Since only one species (H. phytophagus ; Greenwood, 1966b) is known from the
latter subgroup it can be discussed briefly. Haplochromis phytophagus has the overall
structural and dental characters of a generalized species, except that the teeth (both
oral and pharyngeal) seem adapted for biting off and then macerating the relatively
tough tissues of higher plants. Analyses of gut contents suggest, however, that the
principal source of food is not this tissue itself, but the associated flora of attached
diatoms. Only the ruptured leaf and stem cells appear to be digested.

The four species feeding directly on epilithic and epiphytic algae (Greenwood,
1950b) obtain their food in a different way from that of H. phyiophagus. They
graze the algae from the substrate and little higher plant tissue is ingested (and, as in
H. phytophagus, this is poorly digested). One of the four species (H. nigricans ;
Greenwood, op. cit.) is predominantly a grazer on epilithic algae and is rarely caught
away from rocks and rocky shore lines.

The other three species (H. obliquidens, H. lividus and H. nuchisquamulatus) some-
times extend into the habitat range of H. nigricans and also graze off rocks. Usually,
however, these species are found in or near stands of rooted plants.

All four species feeding on periphyton show some dental modifications (Text-figs
AD-G and 36), with H. obliqguidens the most obviously specialized in this respect
(Text-fig. 4G). The phyletic-structural story here is interesting because, despite
the different degrees of specialization in tooth shape (from near generalized in H.
nuchisquamulatus, through H. lividus to highly specialized in H. obliquidens), there
is apparently little difference in their effectiveness as scrapers. The teeth of H.

P. H. GREENWOOD

40

(Natural size.)

(pharyngeal crusher).

a mollusc eater

Haplochromis ishmaelt,

ZZ

Fic.

(|

\

\

\

\

\

il

{

\

WNIT

————

—S
_——=
SS
SS = SS
SSS
=
SSS, ————

Haplochromis dolichorhynchus, a benthic crustacean eater.

1G.24:

F

is tyrianthinus, a benthic crustacean eater.

Haplochrom

Fic. 25.

EVOLUTION OF A CICHLID SPECIES FLOCK 41

nigricans (Text-fig. 36) are quite different, and probably are associated with its diet
of epilithic periphyton.

The three phytoplankton feeders (H. erythrocephalus [Text-fig. 26], H. paropius
and Hf. cinctus | Text-fig. 27]) are in all respects, except the long gut, typical members
of the structurally generalized species groups. None shows any obvious superficial
characters correlated with feeding on finely particulate matter. The gill rakers, for
example, are neither longer nor more closely arranged than in an insectivore (Text-
fig. 6), although in HZ. erythrocephalus there is a slight increase in number (12 or 13 cf
8-10 for the other phytoplankton feeders and most insectivores).

Judging from the nature of the algal and other material found in the stomachs of
these fishes, food is taken from the bottom and not while it is in suspension (Green-
wood & Gee, 1969).

Finally, there is the enigmatic H. acidens (Text-fig. 28), an apparent phytophage
with a distinctly predatory facies. The gut contents of the 16 fishes examined
(from different localities) consist mainly of finely macerated phanerogam tissue, but
also a few insect remains, some bones of small fishes and in one specimen the soft
parts of a mollusc. The intestine of H. acidens is proportionately somewhat longer
than that in omnivores, but is shorter than in other vegetarian species. To confuse
the issue further, the jaws, skull and teeth of this species are typically those of a
piscivorous predator (see Text-fig. 37; and Greenwood, 1967; also p. 67 below).
It was with a piscivorous lineage that I originally suggested H. acidens be related
(Greenwood, op. cit.).

Fryer & Iles (1972) call H. acidens an ‘. . . adventurous species, formerly pisci-
vorous, which made experimental sorties into plant eating . . . an almost vacant
niche in Lake Victoria’. They go on to note that such a trophic shift would be one
from a way of life in which specialization was at a premium to one in which the reverse
is true, thus explaining what might be considered ‘imperfections’ for phytophagous
habits in the jaws and teeth of H. acidens. This idea is intriguing but it must be
remembered that there are trophically generalized species not far removed anatomi-
cally from the basal species in the piscivore radiation with which H. acidens was first
associated (but see p. 67 below). Recent studies on this species, however, indicate
that it could as well be related to a generalized and omnivorous species in a lineage
that produced no predators but which did produce another herbivore (H. erythro-
cephalus). The ‘predatory facies’ of H. acidens is thus all the more difficult to
explain. |

The last trophic group to be considered comprises a single species, H. welcommet
(Text-figs 3 and 39), the only known lepidophagous species in the lake. The guts of
all specimens examined, contained numerous small fish scales (like those covering the
caudal fin base of Haplochromis), together with a few fragmentary fin rays and bits
of skin. (The number of guts checked is now considerably greater than when the
species was first described [Greenwood, 1966b], but is still too small for satisfactory
generalizations to be drawn.)

Scale eating is practised by many cichlid species in Lakes Malawi and Tanganyika
(reviews in Greenwood, 1966b and Fryer & Iles, 1972). Some of these species, like
H. welcommei, scrape the caudal fin squamation from other cichlids ; others nip

42

= OO WAAR
ie ue
DES SOOT

Nei
\':

' > of) 4
y Ai \o,
1 Dice 3
Sas
YY asi)
IRA Cc) 4 f

“5 4 Bp

Fie. 28." i aplochromis acidens, probably a feeder on macrophytes, see p. 41.

EVOLUTION OF A CICHLID SPECIES FLOCK 43

scales from the body of a variety of fishes. The diet of H. welcommez is, however,
not entirely one of scales and fin rays ; most guts also contain a quantity of the dia-
tom Melosiva, and in some there are fragments of macerated plant epidermis. This
plant material suggests that H. welcommei may also feed by grazing on the epiphytic
flora of rooted plants, for which habit its dentition would seem well adapted (Text-
fig. 39 ; also p. 69 below). If this is so, then the species shares a trophic niche with
H. obliquidens and the other grazers (see above, p. 39).

Interestingly, one of the Lake Malawi lepidophages, Genyochromis mento, also
feeds on periphyton (Fryer, 1959) which it browses rather than grazes from rock
surfaces. Fryer (op. cit.) suggests that G. mento could have evolved from the same
specialized stem as some of the epilithic algal grazers in that lake. Haplochromis
welcommet, on the other hand, does not seem to be at all closely related to the
grazing species of Lake Victoria. Its relationships are apparently with the benthic,
crustacean-eating species discussed on p. 67 (see also Greenwood, 1966b).

There are still several of the described Haplochromis species whose feeding habits
are unknown, or for which so few and contradictory data are available that the species
cannot be put in any particular trophic category. Furthermore, there are at least
thirty undescribed species collected recently from several deepwater habitats in the
centre lake region. Preliminary studies indicate that most belong to the insectivore
and crustacean-eating groups, with two or three other species referable to the
piscivores.

The absence of a pelagic zooplankton eating Haplochromis species has already been
commented upon. No reason for this obvious gap in the trophic radiation is im-
mediately apparent. There is, of course, a non-cichlid Engraulicypris argenteus
occupying this niche, but then there are non-cichlid species in all the other trophic
niches occupied by Haplochromis species living in the same habitat. Possibly there
isa heavy predation of zooplankton by young fishes (and other animals) in the littoral
and sublittoral lake regions, so that the niche is, in fact, fully exploited. This purely
speculative suggestion would not seem to apply to the offshore, open-water areas of
the lake (except for at least their partial occupancy by shoals of E. argenteus ; see
Graham, 1929). Here again one is hampered by a lack of information on zooplank-
ton density and distribution, and by a complete ignorance of what trophic categories
of cichlids there are in the pelagic and midwater zones of the lake.

Before moving on to consider other aspects of Haplochromis biology one should
recall that the adaptive radiation described above has taken place in a single genus.
To put this phenomenon in perspective one should also remember that in any major
tropical marine biotope (say a coral reef) there might be as much trophic diversity
among its fishes, but several phyletically distinct families would be involved (Green-
wood, 1965a).

Particularly instructive in this respect, since it involves a lacustrine community
(albeit a cold temperate one), is the work by Keast & Webb (1966) on the feeding
habits of fishes in Lake Opinicon, Ontario. These authors analysed the mouth and
body forms, and the feeding habits of 14 species belonging to seven families (represent-
ing, incidentally, five orders). In terms of their overall function and gross mor-
phology (except fin position) the characteristics of these different taxa are all

44 P. H. GREENWOOD

apparent in various Lake Victoria Haplochromis species. - What is more, the Haplo-
chromts have exploited more trophic niches than have the fishes of Lake Opinicon.

Keast & Webb (of. cit.) conclude that mouth and body structure combine with food
specializations and habitat preferences to reduce greatly interspecific competition.
By contrast, in Lake Victoria it is usual for more than one Haplochromis species to
occupy the same trophic niche in the same habitat. There is, however, a similarity
in the two lake situations, for the Hapflochromis species, like the fishes of Lake
Opinicon, retain a measure of flexibility in their feeding habits (see data in papers by
Greenwood, 1956-69). Keast & Webb (op. cit. : 1871) consider such flexibility an
important feature for survival in cold temperature lakes ; it may well be equally
important in warm tropical lakes, and have played a part in the evolution of the
Haplochromis species flock (see p. 115 below).

The Lake Victoria Haplochromis are, of course, not unique in these respects.
The Lake Malawi species are even more adaptively multiradiate, and occupy some

niches not even represented among the Victoria flock (although paedophagy seems -

to be a unique feature of that flock). For a detailed account of the situation in Lake
Malawi the reader is referred to the excellent account given by Fryer & Iles (1972).

Intralacustrine distribution of the Haplochromis species

When considering the distribution, habitats and vertical range (i.e. depth distribu-
tion) of the Lake Victoria Haplochromis species the same restrictions must be applied
as were applied to data on feeding habits (see p. 30 above). Furthermore, the murky
waters of the lake (transparency 1:3-8-2 m, depending on habitat, lowest in sheltered
bays) have greatly impeded field observations on the fishes. Thus, information on
the distribution of a species within a major habitat has to be got indirectly, and its
precision is largely dependent on the type of collecting gear used. For example, a
trawl or seine net could pass through clumps of plants, could traverse several types
of bottom and could take fishes at a variety of depths. Lack of rigorously quanti-
fiable data on the number of individuals in any one habitat is also a hindrance in
assessing species’ distributions and in determining habitat preferences.

Major habitat types within the lake tend to intergrade with one another, but are
recognizable as:

(i) Exposed beaches dit some wave action. The substrate here is generally
sandy, with small rocks and rocky outcrops ; some rooted plants occur, and there
are often marginal stands of emergent vegetation. The sandy substrate extends
offshore for variable distances, grading gently into the organic mud substrate charac-
teristic of sheltered bays and the deeper parts of the lake.

(ii) Sheltered bays, usually fringed with papyrus swamps ; often the inshore end

of a bay is an extensive papyrus swamp. In most sheltered bays the bottom is

composed of organic mud extending right up to the marginal papyrus ; sometimes,
however, there are narrow sand beaches, particularly if the papyrus margin is in-
terrupted.

(111) and (iv) Sub-littoral regions (water depth 6-20 m), and deepwater regions
(more than 20m deep). These are rather more artificial than natural categories,
and are used in order to divide the offshore zones into ‘shallower’ and ‘deeper’

es

EVOLUTION::OF A CICHLID SPECIES FLOCK 45

waters. The sublittoral substrate is either organic mud, shingle, or mud with low
outcrops of lateritic rock that extend for several metres as flat sheets rising one or
two metres above the prevailing substrate. This zone grades imperceptibly into the
‘deepwater’-one where the substrata are also similar.

Islands of various sizes (from Buvuma island, about the size of the Isle of Wight,
to mere rock pinnacles, ca 10-20 m across) are common in the sublittoral zone.

Depending on the island’s size, its shoreline can be as varied as that of the main-
land. Larger islands also provide the chief areas of truly rocky habitats.

(v) Coastal littoral other than sandy beaches. Apart from a few regions of the
lake where there is a rocky coastline, much of this littoral region is adjacent to
fringing papyrus and often includes a water-lily swamp zone. The bottom can be
hard (sand or shingle) or soft (organic mud). The papyrus swamps (even narrow
fringing ones) rarely harbour cichlids, except at the perimeter where, unlike water
further into the swamp, the dissolved oxygen level is adequate for these fishes.
Otherwise the chief occupants of such swamps are air-breathing non-cichlids (see
. LI).

The large gulfs and sounds (e.g. Kavirondo Gulf, Napoleon Gulf, Smith Sound)
are not in themselves particular habitats ; each contains most of the habitats detailed
above.

An indication of the number of Haplochromis species occupying a particular habitat
can be derived from an exposed beach near Jinja (Nasu Point beach) and a sheltered,
papyrus fringed bay about 8 km south of Jinja. In both places I was able to carry
out regular sampling over a period of six years.

The beach habitat is occupied by 35 Haplochromis species, the bay by 21 species.
In the former habitat few non-cichlids (Barbus spp. and Clarias mossambicus)
appear to be regular inhabitants, and then only in very small numbers. Occasion-
ally, however, the beach was invaded by large shoals of the characin Alestes sadlert,
or by shoals of juvenile Tilapia variabilis (otherwise not a regular component of the
cichlid faunas in that habitat).

Ekunu Bay, by contrast, carries a varied non-cichlid fauna including Protopterus
aethiopicus, Synodontis victoriae, Clarias mossambicus, Bagrus docmac, Mormyrus
kannume, Gnathonemus spp., Labeo victortanus and, occasionally, the large Barbus
altianalis. Both Tilapia esculenta and T. variabilis are resident inhabitants.

The two habitats differ quite markedly in the species of Haplochromis present ;
probably not more than two species are shared, apart from the ubiquitous A statoreo-
chromis alluaud1. There are differences too in the trophic specializations shown by
the Haplochromis of the two habitats. In this respect Nasu Point beach is somewhat
more varied, but there is a higher proportion of piscivorous predators in Ekunu Bay
(13 of 21 Haplochromis species, cf 13 of 35 at Nasu Point).

Surveys made in other beach and bay habitats seem to confirm the impression of
greater diversity of Haplochromis species from beaches, and the virtual exclusion of
non-cichlids from this habitat.

Some idea of population density in the Haplochromis species occupying a beach
and its sandy sublittoral region can be gained from the commercial catches made in
these areas. Over the period 1951-58 the average annual catch from seine nets

40 P. H. GREENWOOD

operated at a beach near Majita (Tanzania) was 2-5 million individuals ; the highest
annual seine net catch ever recorded, also from a beach in Tanzanian waters (at
Nyamwikumulu in 1957), was 7 589 599 individuals in a total of 317 hauls (figures
from the Lake Victoria Fisheries Service Annual Reports). Both these figures in-
clude the monotypic genera (which were not distinguished from Haplochromts by the
counters), but these species contribute only a small fraction of the whole (personal
observations on these beaches). For comparison, the catch of non-cichlid fishes in
the same number of seine net hauls at the same beach, Nyamwikumulu, in 1957 was
10 974. 3

As far as I can detect, the nature of the substrate is the major factor influencing
the distribution of many Haplochromis species, at least within the depth limits of
the various species (see below). Some species are virtually confined to habitats (or
parts of a habitat) where the bottom is muddy. Others are restricted to places where
the substrate is hard and composed of sand, rock or shingle. Unfortunately, the
data available are not sufficiently refined to be able to tell if the exact nature of the

substrate, that is its constitution, or its associated flora and fauna, has the more

particular influence on species distribution.

Of the 69 species apparently restricted to water less than 20 m deep (i.e. inshore
Species), 27 are found only over hard substrates, and five only over organic mud or
other soft substrates. The remaining 37 species have been caught over both hard
and soft bottoms, but it must be stressed that of these species, nine rarely occur over
soft substrates and seven are rare over hard bottoms. In other words, 32 of the 69
species have a restricted substrate preference, and 21 occur over either substrate
type with sufficient frequency for one to consider them as being free from substrate
restraint (data from Greenwood, 1956-69).

Correlating specific substrate preferences with the trophic groups to which the
species belong is difficult, and because of insufficient data also rather subjective and
imprecise. Some species in all trophic groups, except the algal grazers, show no
marked substrate preferences. Molluscivorous species of the group crushing gas-
tropods orally (or wrenching them from the shell) are virtually confined to hard
substrata, as are the paedophagous species (see pp. 31-37 above). All other trophic
types are found over every type of substrate.

Likewise it seems that representatives of all trophic categories are found in each
of the major habitats. However, the algal grazers and the species feeding on higher
plants (p. 39 above) are restricted to habitats or parts of a habitat where there are
rooted plants or, in the case of the grazers, suitable substrata for algal growth.
Haplochroms nigricans of this group seems to have the most restricted distribution,
rarely being found far from rock surfaces. The paedophages as a group are relatively
restricted to littoral habitats, probably because it is mainly in these regions that

brooding female Haflochromis are concentrated. Particular interest attaches to

six specimens of H. obesus (or a taxon anatomically very like that species) caught
over a mud bottom at a depth of 27-30 m (Greenwood & Gee, 1969). Collections of
Haplochromis from this and similar habitats rarely produce brooding females (or
individuals showing the characteristic buccal distortion that goes with brooding and
which persists for a short while after the young have been jettisoned). Thus it is

Se

EVOLUTION. OF A CICHLID SPECIES FLOCK 47

especially noteworthy that these deep-living H. obesus had all fed exclusively on
cladocerans and copepods.

It is clear from field observations that more than one Haplochromis species of a
particular trophic group can be found in any one habitat. The extent of such inter-
specific overlap, and hence possible trophic competition, may be less than is implied
by the mere record of several species seeming to feed on the same food source.

Two algal grazers, H. lividus and H. obligudens, occur together in the sandy beach
habitat ; but the former species extends its range into deeper water than does H.
obliquidens. Haplochromis mgricans, with similar food requirements, also occurs in
this habitat but it feeds principally from submerged rocks and stones.

A similar situation exists with two mollusc eaters in this habitat, H. sauvage and
H. prodromus, where H. prodromus extends into the sublittoral beach zone. Further-
more, the two species have different feeding methods, H. sauvagez levering the snail
from its shell, and H. prodvomus crushing the shell between its jaws. These dif-
ferences may influence the selection of prey species by the predators. The monotypic
genus Macropleurodus bicolor also enters the picture since its habitat range overlaps
in part those of H. sauvage: and H. prodromus, being very like that of the latter
species (Greenwood, 1956a, 1957). Its feeding habits, too, are more like those
of H. prodromus, although it is known to feed on insects as well as snails (Green-
wood, op. cit.), and probably to a greater extent than H. sauvager, also a mixed
feeder.

The whole situation is further complicated by the presence of two other mollusc
eaters of the same trophic complex, H. granti and H. xenognathus (see p. 69 et seq.).
Both these species occur in the habitat under discussion, and both share the same
food sources and intrahabitat preferences as the species already considered. Nor are
these the only mollusc eaters present. Haplochromis humilior and H. pharyngomylus
also live in beach habitats (Greenwood, 1960). These two species, unlike the others,
crush their prey in the pharyngeal mill; the food of H. pharyngomylus (chiefly the
snail Melanoides tuberculata) is virtually identical with that of H. prodromus, H.
xenognathus, H. granti and M. bicolor. The food of H. humilior, a smaller fish,
overlaps that of these species but does include a greater proportion of other organisms,
especially insects (Greenwood, 1960). Other partly molluscivorous species could be
mentioned but I think the problem is sufficiently obvious without introducing
additional complexities.

An equally complicated picture can be compiled for the insectivorous species in a
habitat, and to a lesser extent for the phytoplankton eating species as well.

The piscivorous predators provide perhaps the strongest prima facie case for
interspecific trophic congruence ; yet even here interspecific competition cannot
definitely be established from the data available. In the habitats I have studied
there seems always to be a group of piscivorous species with completely overlapping
ranges, as well as a few species showing a restricted distribution. All these fishes
feed on other Haflochromis species. Since it is impossible to identify prey recovered
from the guts to more than the generic level, it is equally impossible to tell what
degree of competition (if any) there is for prey species. On a subjective impression
there would seem to be a sufficiency of prey species for competition between the

48 P. H. GREENWOOD

predator species not to develop, and the situation is further ameliorated by some of
these having a limited intrahabitat distribution.

The extent to which some species may move between habitats, or from one type
of substrate to another, has not been established. Thus I would be chary of sug-
gesting, as have Fryer & Iles (1972 : 308), albeit tentatively, that in Lake Victoria
‘.. . It seems probable that some species will at times utilize this ability, (to shift
habitat), at least as a temporary expedient for avoiding adverse conditions’.

I would, however, agree with the general conclusion reached by these authors,
that in Lake Victoria there is, as compared to Lake Malawi, less obvious stenotopy
amongst members of the cichlid species flock (always bearing in mind that far less
is known about the generality of Haplochromis species in Lake Malawi than about
the ‘Mbuna’ generic complex and the few rock-haunting Haplochromis species that
coexist with them, a point not explicitly made by Fryer & Iles).

None of the Lake Victoria Hapflochromis or related species shows any geographical
restriction within the lake, nor have any morphologically distinguishable populations
been discovered. In both these respects the Victoria species differ from those of
Lake Malawi, and especially Lake Tanganyika (see summary in Fryer & Iles, 1972).

The question of interspecific overlap in feeding habits and habitat requirements
among Lake Victoria Haplochromis species has direct bearing on the principle of
“competitive exclusion’ (the so-called Gause’s principle, but see Mayr, 1963). This
postulated that no two species can exist at the same locality if they have identical
ecological requirements. As Wynne-Edwards (1962) has demonstrated, the principle
is logically and ecologically unsound. If two species have truly identical require-
ments they will be, in effect, ecologically one species. Competition will then be on
an intraspecific rather than an interspecific level ; that is, between individuals.

From what is known about the inshore Haplochromis species considered so far,
there are relatively few, if any, aggregates with absolutely identical ecological re-
quirements (i.e. a condominium, sensu Wynne-Edwards). Instead there are many
species with a certain degree of overlap. Following the spirit of Professor Wynne-
Edward’s terminology, perhaps such groups should be thought of as a ‘common-
weal’?

The vertical movement of inshore Haplochromis species is very poorly known,
and their apparent restriction to water less than 20 m deep may prove illusionary.
Taking the latter point first, most available depth records were obtained before the
deeper, offshore areas of the lake were studied intensively. In recent years there
has been a great deal of exploratory trawling in these areas. To a certain extent
this research has confirmed the earlier depth distribution records, but it has also
provided some surprises. The extended range of H. obesus has already been noted
(p. 46 above). During a recent trawl survey a haul made over sand at a depth of
ca 50 m in midlake (opposite Entebbe) contained, in addition to deepwater species,
several other species that were previously known only from inshore beach habitats
(personal observations). |

Little can be said about the movement of inshore species through the water —
column. The indications are that species in this zone remain near the bottom, at |
least during daylight (personal observations). In water less than 2 or 3m deep, |

EVOLUTION: OF A CICHLID SPECIES FLOCK 49

many species may range from surface to bottom, but in progressively deeper water
their behaviour pattern becomes increasingly benthonic. Judging from the presence
of bottom debris associated with food in the guts, most species feed on or near the
bottom. For the piscivorous species, such indirect evidence is not available; the
occasional field observation in clear water suggest that piscivores range rather freely
through the water column, at least in shallow parts of the lake.

As yet the taxonomy of deepwater species is very incompletely known, and the
ecology of even the described species is still imperfectly documented (Greenwood &
Gee, 1969). Apart from a few inshore species whose range extends beyond ca 20 m,
17 described species are known from deeper waters (Greenwood & Gee, op. cit. ;
Greenwood, 1967). I estimate that at least 30 more species will be described from
collections already obtained. Only two species, H. dolichorhynchus and H. ery-
throcephalus, have been recorded from depths less than 15m; these species have
depth ranges of 10-30 and 10-35 m respectively. Depth ranges for the remaining
species are between 17 and 70m. Most have a wide range within the limits of 25-
35 m, but there are indications of some species being restricted to depths near the
upper and lower limits of the total range. None extends into the truly littoral zone,
but several species may live at depths greater than those recorded here (personal
observations).

Deepwater species are necessarily confined to the strictly offshore regions of the
lake, but at least three species (fH. erythrocephalus, H. dolichorynchus and H. crypto-
gramma) have been caught in the deeper areas of large bays (Greenwood & Gee,
1969).

It is impossible to define habitats in the deeper water, and the collecting gear
employed there (trawl nets) means that several habitats may be sampled in one
trawling period (half an hour at a speed of about 2 knots). That all but two of the
known species were caught over a soft bottom is probably not a true reflection of the
species’ substrate preferences ; more trawling has been done over mud than over hard
substrata. Nor, because of limits imposed by the collecting methods, is it possible
to determine the species structure of any particular area. All one can say is that
several species are caught in a trawl, that these species will be from several trophic
groups, and that any particular trophic group is usually represented by more than
one species. In other words, a replication of the situation in shallower waters of the
littoral and sublittoral.

The structute of deepwater communities may, however, be simpler because certain
trophic groups are not represented there. So far, insectivores, bottom detritus
feeders, predators on small Crustacea and piscivorous predators have been identified
(Greenwood & Gee, 1969). No mollusc eaters have been found, and the sole paedo-
phage (or presumed paedophage, H. obesus, see p. 46 above) had fed on Crustacea.
These remarks must, however, be qualified by reference to the ‘inshore’ species
complex caught in midlake (see p. 48); at least two mollusc eaters (including
Hoplotilapia retrodens) were amongst the species then caught.

The apparent paradox of that deep-living ‘shallow water’ community shows clearly
the difficulty of generalizing about the ecology of deepwater regions in the lake. If
sandy bottom, inshore species can adapt to deep water, why is it that none of the

4

50 P. -H. GREENWOOD

soft bottom inshore species has done likewise, especially since the nature of the soft
substrata in both regions is apparently identical? Much more will have to be learned
about deepwater fishes, and particularly if there are species confined to sand at those
depths, before an attempt can be made to answer this question.

It is assumed from the evidence available (par ticularly the nature and composition
of gut contents) that all deepwater species are benthic in habit (Greenwood & Gee,
1969). One species, H. laparogramma, is suspected, however, of feeding away from
the bottom (Greenwood & Gee, op. cit.), and other members of the insect—crustacean
eating trophic group may have similar habits, or at least be facultative in this respect
because their prey are not necessarily confined to the benthos.

Echo-sounding has demonstrated the presence of fish in midwater at a variety of
depths (Gee, 1968). So far it has been impossible to identify these fishes ; that they
may be species of Haplochromts is indicated by some rather inconclusive midwater
experimental trawling. (Personal communication from staff members of the
E-ALE.E-R:-O., 1071.)

No counts are available for the number of individual fish caught per trawl in

deep waters. An estimate by eye suggests that the density of Haplochromis in
these waters is not significantly less than from inshore habitats (see p. 46 above).

Brief mention may be made here to the habit of shoaling. In Lake Malawi
several of the offshore, zooplankton-eating Haplochromis species (the ‘Utaka’
group) exhibit shoaling behaviour, as does the rock frequenting H. kiwimgi during
the zooplankton-eating phase of its life cycle (see Fryer & Iles, 1972).

The Lake Victoria Haplochromis species do not appear to furnish a single example
of shoaling, at least during adult life. Since adult shoaling is associated with feeding
on suspended, particulate food (zooplankton or phytoplankton) the absence of this
behavioural trait is not altogether surprising. However, it should be remembered
that direct observation on fishes in Lake Victoria is well nigh impossible, and the
recognition of a shoal would be from the extreme abundance of a particular species
inacatch. Thus, with trawling, when several thousand individuals are caught from
over a large area, a small shoal could pass undetected in the catch.

Species of the shoaling ‘Utaka’ Haplochromis group in Lake Malawi have charac-
teristic ‘shoaling marks’, in the form of spots, or a well-defined stripe, on the flanks.
Few Lake Victoria species show such coloration, at least as fixed patterns (see p. 52).
Of the species that do, H. martini and H. michael: (lateral stripe) provide no evidence
for shoaling, and neither species is a plankton eater. The possibility remains open
for two deepwater species with marked patterns (H. laparogramma [a lateral stripe]
and H. cryptogramma [an interrupted lateral stripe]). Both species are caught only
in trawls, thus making an estimate of their relative abundance in a catch particularly
difficult. Since H. cryptogramma feeds on the pupae of chironomid flies (which
occur in dense aggregates), and seems to feed away from the bottom, it is the most
likely suspect for shoaling behaviour.

Breeding biology of the Haplochromis species

To conclude this review of Haplochromis bionomics the rather scattered informa-
tion on their breeding biology will be brought together and reviewed.

|

;

EVOLUTION-.OF A. CICHLID SPECIES FLOCK 51

Many species are known to be female mouth brooders. There is no indication,
either direct or by implication, that any species does not practise this form of parental
care. For the several species where females actually carrying young have not been
caught there is indirect evidence of mouth brooding ; namely, spent females with
the characteristic deformation of the buccal cavity (a deeply depressed hyoid arch)
associated with mouth brooding, and the presence of few but large ova in the mature
ovary. These ova also fail to show the modifications to the zona radiata which are
invariably associated with substrate spawning habits in the Cichlidae (see Fryer &
Iles, 1972 for review).

No records are available for the breeding activity in any particular species.
However, repeated observations made at a beach near Jinja, and from other localities
in northern waters of the lake, strongly suggest that at least part of a population is
breeding at any one time. That is to say, for the majority of known inshore species
breeding is continuous. (Unpublished personal observations.) Nothing (except
indirect evidence for mouth brooding) is known about the reproductive behaviour of
species from deeper waters.

Regrettably the opaque water of Lake Victoria does not often permit direct
observation of the fishes, and even when this is possible it is not easy to identify the
species seen. Thus the exact spawning sites for inshore species, or the mode of their
spawning, is not known. On occasion I have seen males guarding simple pit nests
in the clear sand bottom near stands of emergent swamp grass. If nest building (or
at least the preparation of a substrate for oviposition) is a common feature for all
species, the question is raised of where do species living over soft substrate spawn.
The flocculent organic mud covering so much of the lake floor would seem to be a
most unsuitable substrate for this purpose.

This leads one to consider the possibility of species which live over soft mud
during non-breeding phases moving to areas more suitable for spawning. Brooding
females of some of these species are, however, found in the same areas as non-
breeding fishes.

The same question is raised with regard to the deepwater species. None has
been found inshore so presumably breeding takes place offshore, possibly over those
areas where the bottom is hard. There are numerous other unanswered problems
associated with the breeding habits of these species. For instance, if there is a
migration to hard substrata, is there competition for breeding space with species
normally resident in such places, or at least conflict between breeding immigrants
and feeding residents?

Then there is the question of light and vision in deep water. Visual signals and
stimuli play an important part in cichlid courtship and reproductive behaviour (see
extensive summary of researches in this field given by Fryer & es [1972], and papers
by Baerends & Baerends van Roon [1950], Wickler [1966] and Neil [1964]). Light
penetration in Lake Victoria is low even in water less than 10 m deep ; it must be
even less at greater depths. For the moment we are nowhere near supplying an
answer to these problems, and their resolution will be difficult.

All known Haflochromis species and the monotypic genera show clearly defined
sexually dimorphic coloration. With two exceptions, it is the male fish that has the

52 P. H. GREENWOOD

brighter and more colourful livery, even in non-breeding periods. The exceptions
are provided by H. dichrourus (Greenwood, 1967) and H. chromogynos (Greenwood,
1959b). In H. dichrourus, although the sexes are differently coloured, the female is
more polychromatic than the male (see Greenwood, 1967 ; these observations have
since been confirmed and extended by additional specimens). In H. chromogynos,
too, there is dimorphic coloration. Males have what may be termed ‘typical male
coloration’ but the females are distinctly marked by a black-and-white piebald
coloration that is otherwise found as a sex-limited polymorph in females of certain
species (where its frequency is never in excess of ca 30 per cent [Greenwood, 1956a
and b, and p. 53 below; also discussion in Fryer & Iles, 1972]).

The importance of male coloration in species recognition amongst many cichlid
genera is now well established (see Baerends & Baerends van Roon, 1950). Thus itis
not surprising to find male breeding coloration is, at least to the human eye, species
specific. (Personal observations ; see also descriptions in Greenwood, 1956-69.)

With the relatively limited chromatophore pigments and interference colours

available it is also not surprising to find these differences not always sharply marked.

That is, there is not always a gross interspecific difference in coloration or colour
pattern. Instead, apart from differences in ground coloration, the specific differ-
entiae involve differently coloured suffusions (red, orange, coppery) over various
parts of the flanks, belly, chest or head, and differently patterned colour flushes
(especially red or pink) on the median fins (particularly the anal and caudal fins). In
addition there may be coloured lappets (predominantly red or orange) on the dorsal
fin, or these may be colourless (Plate 1).

It is difficult to create a word picture for the ground colour of the body. Reduced
to basic colours, four principal types are found, viz: blue-grey (the commonest),
shades of green and blue (from turquoise to malachite), yellow to yellow brown (with
beige as an extreme) and, least common, uniformly black.

Ground coloration is most intense on the dorsal half of the body, shading to silver,
grey or yellow ventrally ; in other words the fishes are basically countershaded.
Most species show patterns of dark vertical bars and horizontal stripes on the body,
and various bars and stripes on the head and opercular region (see Text-fig. 8).
These patterns are, with few exceptions, under emotional control and seem to play
an important part in the fishes’ repertoire of signals (see Wickler, 1964). The
exceptional species (e.g. H. percoides [Text-fig. 52A], H. flavipinnis [Text-fig. 52B],
H. martim [Text-fig. 50] and H. squamulatus [Text-fig. 49] and some others) have
fixed, but individually variable, patterns which are present in both sexes.

Species from deepwater habitats also show bright male coloration (Greenwood &
Gee, 1969). Indeed, several species have colours not seen among inshore species,

PLAGE «1

Above. Haplochromis riponianus. Sexually active male. Note the prominent ‘egg dummies’
on the anal fin.

Below. Haplochromis brownae. Adult male, showing almost complete development of
breeding coloration.

Photographs by André Roth.

Bull. Br. nat. 5) BEAL Bain

EVOLUTION OF A CICHLID SPECIES FLOCK 53

for example bright purple and pastel green. Although various shades of purple
seem to predominate in the species so far described, this colour does not appear to
be at all common in the species still awaiting description.

Females from all habitats, in sharp contrast to males, are drably coloured, with
greyish silver or sandy ground colours predominating (H. chromogynos and H.
dichrourus, excepted ; see p. 52 above). Unlike males there are few marked inter-
specific differences in female coloration, but slight differences do exist between some
species. Cephalic and somatic bars and stripes are developed as in males, and also
seem to be under emotional control.

A very prominent and characteristic feature in the males of all Haplochromis
species (and related genera) are the ocelli or ‘egg dummies’ on the anal fin. From
one to several “egg dummies’ are located on the posterior quarter of this fin. Each
is a roughly ovoid colour patch, usually yellow or orange-yellow, surrounded by a
completely colourless ring of fin membrane. In life this clear zone gives the spot a
three dimensionality such that it closely resembles a Haplochromis egg. The func-
tional importance (and indeed the name) of these ‘egg dummies’ was discovered by
Wickler (1962a and b, 1968). He was able to demonstrate that, after the female
has oviposited and taken the ova into her mouth, the male displays his anal fin in
such a way as to bring these spots into prominence. The female then attempts to
pick up the spots, presumably identifying them as newly deposited ova. Whilst
she is in the close proximity of the male’s anal fin, and thus near his genital papilla,
he ejaculates (Wickler, of. cit.). Clouds of sperm are then drawn into the female’s
mouth, and the ova are fertilized. In other words, these fishes have evolved a kind
of secondary internal fertilization.

“Egg dummies’ have not been found in any female, but there are often colour
spots on the anal fin of females in the same position as the ‘egg dummies’ in males.
However, there is never a clear zone around the spots and they certainly do not have
the appearance of a true ‘egg dummy ’, neither are they so large nor so clearly defined.

Sex-limited female polychromatism occurs in at least eight species of the Lake
Victoria Haplochromts, and in two of the endemic monotypic genera (Macropleurodus
bicolor and Hoplotilapia retrodens). In none of these species does the occurrence of
polymorph individuals exceed ca 30 per cent of females in a population. The
commoner polymorph coloration found in all species showing the phenomenon is an
irregular black piebald-on a silver or yellow background (Text-fig. 29) ; no inter-
grades between the piebald and normal female coloration have been found. This
piebald pattern does not vary with the emotional state of the fish, nor with the type
of habitat in which the fish is living. A second morph is also known from Hoplo-
tilapia retrodens, and in at least one undescribed Haplochromts species ; it comprises
a blotched yellow and orange ground coloration on which is superimposed small black
blotches or merely a fine but distinct peppering of melanophores (Greenwood,
1956a).

The eight Haplochromis species showing piebald coloration belong to at least four
different phyletic groups, none of which shows especially close interrelationships
within this admittedly closely related species flock. Algal grazing species (H.
nigricans), paedophages (H. cronus, H. obesus and H. barbarae), mollusc eaters (H.

54 P. H. GREENWOOD

sauvaget), specialized insectivores (H. chilotes) and a piscivore (H. altigents) all exhibit
the phenomenon.

Selective advantages associated with the maintenance of this balanced poly-
morphism are unknown (Greenwood, 1956a; see also discussion in Fryer & Iles,
1972), but must be fairly substantial considering both the frequency of polymorph
individuals in a population, and the fact that 1t occurs in so many species.

LS

Boats Ear) u
SSE

SEE

Fic. 29. Haplochromis barbarae female, showing piebald coloration (see p. 53).

The usually complete linkage of piebald coloration to the female sex is disturbed
in Macropleurodus bicolor, where two piebald males have been found (Greenwood,
1950a). In one of these fishes the pattern is identical with that of females, but in
the other it is less intense and the background coloration is darker. As far as I can
determine, the gonads of these atypical males contained only testicular tissue, and
provided no evidence to suggest possible protandry in the species (as is suspected for
a Malawian genus Labeotropheus fuelleborm [report by Professor H. Peters, quoted
in Fryer & Iles, 1972: 172]). A male showing partial female-type piebald colours
is also recorded for Hoplotilapia retrodens (Greenwood, 1956a), and I have seen a live
Haplochromis chilotes with piebald coloration and well-defined ‘egg dummies’ on the
anal fin. Unfortunately it was not possible to dissect the latter specimen, an
aquarium fish.

The genetic basis for this almost completely sex-limited polychromatism, and its
occasional breakdown, has not been determined. Fryer & Iles (1972) argue cogently
in favour of its being the manifestation of a potency balance between the expression
of alleles on autosomes and ‘suppressor’ alleles on the sex chromosomes. On the

assumption that female cichlids are the heterogametic sex (which is also assumed in

my explanation of the phenomenon ; Greenwood, 1956a), this interpretation seems
at least to provide a working hypothesis. I am less sanguine about their view that
the occurrence of atypically coloured (i.e. piebald) males violates the sanctity of male
coloration as an important factor in species recognition. That the proportion of
piebald males is very much lower than that of polymorph females suggests that alleles
with a potency sufficient to overcome the ‘suppressor’ alleles are extremely rare.

EVOLUTION:-OF A CICHLID SPECIES FLOCK 55

Could not this rarity be attributable to adverse selection pressure on those in-
dividuals possessing them? That is, the chances of such males being ‘recognized’
and ‘chosen’ by a female (an obligatory prelude to spawning) are greatly reduced ;
this in turn would lead to a great reduction in the number of these ‘ powerful’ alleles
in the population. Is it not even possible that piebald males do not mate at all, and
that the alleles in question are maintained purely by mutation?

To me, a far more telling point against the importance of male coloration as the
prime means of species recognition in courtship derives from the Haplochromis
species flock in Lake George. In this lake the euphotic zone extends only to a depth
of 50-60 cm (Greenwood, 1973a). Most Haplochromis species live and apparently
spawn below this depth, or at least in places with extremely low light intensities. To
the human observer underwater in these lighter areas, a fish’s shape, but not its
colour, is just apparent. Thus in these species there seems to be a prima facie case
against the overriding importance of male coloration. Yet, males are brightly
coloured, and their coloration (with one exception, see Greenwood, 19734) is species
specific, and does not show any greater degree of intraspecific variability than do the
colours of the Lake Victoria species.

Finally, in dealing with colour aberrancies in Lake Victoria species, mention must
be made of apparently melanic Haplochromis obesus. Atypically dark individuals
of both sexes are known, but melanic males are commoner. The degree of darkening
shown by these fishes is somewhat variable ; extreme individuals are uniformly
black, but others are much brighter ventrally and do in fact intergrade with the
normal male coloration. No correlation has been observed between locality or
environment and the presence of melanic individuals, nor with the degree of melanism
displayed.

In a large and complex species flock like that of Lake Victoria, with many species
occupying the same habitats, one might well expect a number of interspecific hybrids.
Detecting hybrid individuals on purely morphological grounds would be difficult
because of the close similarity between putative parent species. Nevertheless,
despite constant awareness of this possibility, I have found only one specimen that
might bea hybrid. Whatever the barriers to interspecific mating may be, they seem
to be very effective.

Comparisons between the coloration of Haplochromis species from Lakes Victoria
and Malawi are difficult to make, partly because of difficulties in verbalizing colours,
and partly because colour descriptions are not available for many Lake Malawi
species. Nevertheless, the views of those who know both faunas strongly indicate
a fundamental difference in colour patterns and dominant colours (see remarks in
Fryer & Iles [1972]; also personal comments by Drs Fryer, Lowe-McConnell and
Trewavas). :

The reasons for these differences are probably manifold (for example, the greater
number of pelagic species in Lake Malawi, the existence of shoaling species in that
lake etc.), and must be, in part, of phylogenetic origin. In this context it is important
to emphasize the basic similarity in coloration between species of the Lake Victoria
and Lake Edward—George fishes, where phyletic integrity is ascertainable on other
grounds (Greenwood, 1973a).

56 P. H. GREENWOOD

INTERRELATIONSHIPS OF THE LAKE VICTORIA HAPLOCHROMIS SPECIES

Having outlined the main morphological and biological features of this Haplo-
chroms species flock, attention can now be turned to four major evolutionary ques-
tions. These are, the origin of the flock, its internal phylogeny, the factors under-
lying its explosive speciation and adaptive radiation and, finally, why it is that,
under such conditions the Cichlidae, more than any other family, react in this fashion
(see p. 4 above and pp. 103-111 below).

The phylogenetic problem can be considered first (Text-fig. 70). Any attempt to
analyse this flock is fraught with difficulties. The very basis for a phyletic study,
the flock’s monophyletic origin, cannot be established unequivocally. Reasons for
assuming a mono- or oligophyletic origin for the endemic species have already been
discussed (p. 20 above). To these may be added one other, namely, that a careful
survey of most known species indicates a basic morphological homogeneity that
would be unlikely if several unrelated species were implicated as ancestors. In other

words, if the flock is not strictly monophyletic in origin, its stem species were likely —

to have been no more distantly related than sister species (sensu Hennig, 1966).
Be that as it may, it is certainly possible to establish monophyletic groups within the
flock (Text-fig. 70).

At a gradal level, the Victoria Haplochromis species present an interesting and, for
extant animals, an unusual picture of virtually complete morphological intergradation
between the generalized and the specialized in any one adaptive radiation. Two
trenchant examples are found in the mollusc-eating species and a third in the pis-
civorous predators (see pp. 31 and 37 above).

Graded anatomical stages, involving changes in dentition and dental pattern
among species that shell molluscs orally are all represented in the lineage H. sauvagen,
H. prodromus and H. xenognathus, with H. grant a slight deviant from the Z.
prodromus stem (see Text-fig. 41 ; and Greenwood, 1957). The genus Macropleuro-
dus 1s an extreme modification of the same morphotype (see Text-figs 75A and B;
also Greenwood, 1957). Stages in the hyperdevelopment of a pharyngeal crushing
mill amongst mollusc eaters are well represented by seven species, H. pallidus, H.
riponianus, H. saxicola, H. humilior, H. theliodon, H. obtusidens and H. ishmael1, the
species listed in approximate order of increasingly molarized lower pharyngeal teeth
(see Text-fig. 5 and Greenwood, 1960 ; also p. 37 above). The piscivorous predators
present an even more complex and just as complete picture of bridged gaps between
specializations (see Greenwood, 1962, 1967, 1973b). The other trophic groups all
show similar, but often shorter, trends in specialization.

The question now to be asked is whether all the constituent species of each gradal -

complex represent truly monophyletic lineages within the flock, or whether we are
confronted by a web of parallelisms. Detailed studies of the species comprising the

different radiations suggest that the latter explanation is the more likely one. The —

task then is to untangle the gradal groups by seeking out combinations of specialized
characters (apomorph characters of Hennig, 1966) that will link together phyletic
lineages within each grade.

The student of the Lake Victoria flock is in the position of a palaeontologist who
has a nearly complete phyletic record for several branches of a monophyletic lineage,

EVOLUTION. OF A CICHLID SPECIES FLOCK 57

the extant end-products of which are clearly defined taxa, but some of whose an-
cestors tried out, as it were, specializations now characterizing living taxa in a sister
lineage. Unlike the palaeontologist, the student of the Lake Victoria Haflochromis
has no temporal sequence to help him sort out branching points.

Historically, some of these difficulties could spring from the flock’s relative youth.
In an older assemblage a number of species now seen as representing an intermediate
stage of specialization could well have been eliminated as unsuccessful competitors
with more specialized species of their own or related lineages.

Whether or not an older cichlid species flock would be an easier subject for phyletic
analysis, and whether the results would be more precise, are moot points. Un-
fortunately no such test has been made on the flocks of either Lake Tanganyika or
Lake Malawi in their entirety. Fryer (1959; also repeated in Fryer & Iles, 1972)
has, however, attempted to work out the interrelationships of the ‘Mbuna’ generic
complex in Lake Malawi. His criteria of relationship are not explicitly defined and
the resulting ‘tree’ seems more an indicator of parallel radiation than of phylogenesis.

A feature shared by Haplochromis in both the older flock of Lake Malawi and the
younger one of Lake Victoria is the existence of two or more very similar species
clustered around any one level of adaptation. It is these species in particular that
have given the Cichlidae a reputation among taxonomists of being a difficult group.
Examples of species knots from Lake Victoria would include five species in the
insectivore lineage (H. macrops, H. megalops, H. pallidus, H. lacrimosus and H.
piceatus ; see Text-figs 3, 8 and g and p. 30 above), the five species of the crustacean
eating, deepwater, H. tvidens group (see p. 39 above ; also Greenwood & Gee, 1969),
H. sauvage: and H. prodromus in the mollusc eating grade (Text-figs 3 and 19-21 ;
see also p. 37 above ; and Greenwood, 1957), H. wshmaelt and H. pharyngomylus in
the other molluscivore grade (see p. 37 above ; and Greenwood, 1960), H. riponianus,
and H. saxicola (Text-figs 3 and 42) also mollusc crushers (Greenwood, op. cit.), H.
obesus, H. maxillaris and H. melanopterus among the paedophages (Text-figs 3 and
17; see also p. 33 above; and Greenwood, 1959b), and many other examples of
twin, triplet and even quintuplet species among the piscivorous predators (Green-
wood, 1962, 1967).

These species groups (if they are truly phyletic, and some certainly seem to be that)
may reflect the physiographical background to speciation in the lake, and be the

products of simultaneous multiple speciation each from the same common ancestor
isolated in different water bodies (see p. 10 above and p. 114 below).

Relatively few characters can be used to construct phylogenies. It will be recalled

that meristic characters are almost uniform throughout all species. Thus, interest
centres on cranial and dental features which, on the whole, clearly show levels of
specialization or generalization. .
_ As the base line for this study I have identified as generalized those characters
shared by Victoria species and a fluviatile species widespread in the rivers of Uganda
(i.e. a taxon anatomically identical with, if not actually H. bloyeti ; see Greenwood,
1g7I).

Skull shape, jaw form and tooth morphology in this species are illustrated in
Text-figs 30 and 31. Characteristic features of this skull type are the relatively

58 P. H. GREENWOOD

decurved dorsal profile to the preorbital face of the neurocranium (giving the orbital
margin a near-rounded circumference), the high cranial vault and the relatively
short ethmovomerine region. The premaxillary ascending process is shorter than
the dentigerous arm of the bone, and the lower jaw (dentary plus articular) is neither
foreshortened nor elongate.

The lower pharyngeal bone is not noticeably thickened, and its equilateral denti-
gerous surface is covered by fairly well-spaced rows of cuspidate and laterally com-
pressed teeth. Teeth in the median rows are usually a little coarser than those
situated laterally (Text-fig. 30A).

3mm

Fic. 30. Haplochromis bloyeti. A: Lower pharyngeal bone in occlusal view. B: Outer
row teeth from the premaxilla; viewed anterolaterally. Scale = Imm.)

The outer jaw teeth in H. bloyeti are unequally bicuspid, the cusps triangular in
outline (Text-fig. 30B) ; the inner teeth are small and tricuspid, and are arranged in
not more than three rows in either jaw. Usually a few unicuspid teeth occur pos-
teriorly in the outer row of the premaxilla, and in larger fishes (> 80 mm long) a
few unicuspids are intercalated with the bicuspids anteriorly and anterolaterally in
both jaws.

Among extant Lake Victoria endemic species, H. pallidus has a syncranium and
dentition virtually identical with that of H. bloyets (see Text-figs 31-33), and there
are several other similarly generalized species known.

Having established the anatomical nature of a generalized species, each trophic

group (see pp. 58-80) will be considered in turn, probable phyletic lineages (based ©

on shared specialized characters, i.e. synapomorphy) will be delimited and, where
possible, interrelated.

The insectivorous species

Typically generalized skull, jaws and dentition are found in five species (#.
pallidus [Text-figs 32 and 33], H. macrops [Text-figs 32 and 33], H. lacrimosus, H.
megalops and H. piceatus ; see Greenwood, 1960 and Greenwood & Gee, 1969). In
all except H. pallidus the lower pharyngeal dentition is also generalized; in H.

EVOLUTION OF A CICHLIID SPECIES FLOCK 59

Fic. 31. Haplochromis bloyeti. Neurocranium and lower jaw, in left lateral view.
(Scale := 3 mm.)

pallidus some median teeth are slightly enlarged. A sixth species, H. cinereus, is
osteologically one of this group, but differs in having a predominance of unicuspid
over bicuspid outer jaw teeth, even in fishes at a size where bicuspids predominate
in other species (Greenwood, 1960).

Because of their generalized cranial anatomy it is impossible to determine the
interrelationships of these six species ; all could be cognate. However, except for
H. pallidus all species have the preorbital skull face slightly more decurved than in
the presumed ancestral type, with which H. pallidus is virtually identical.

Anatomically, it is interesting to see amongst these fishes a representation, in
embryo as it were, of many characters that are developed in various characteristic
ways among more specialized trophic groups. For instance, there are the unicuspid
teeth of H. cinereus (but see below), the incipient development of enlarged pharyngeal
teeth in H. pallidus, and a basic syncranial ‘bauplan’ that, through differential
growth of certain elements (or regions in the case of the neurocranium), provides the
starting point for the different types found in other trophic groups.

None of the species considered so far has adults exceeding a length of more than
105 mm.

Haplochromis saxicola is, superficially, like the foregoing species (cf Text-figs 3
with 8 and 9). However, its neurocranial morphology departs from the basic type
towards that of some piscivorous species (Text-figs 34 and 68). That is, the pre-
orbital region is more elongate (as is the entire skull anterior to the brain case), its
dorsal profile is not noticeably decurved and it slopes downwards less steeply, and
there is a reduction in the depth of the brain-case region. The jaw dentition too
differs somewhat from the generalized type because unicuspid teeth predominate ;
since the smallest H. saxicola known is larger than the largest members of the general-
ized group, this observation may be of doubtful significance (see p. 106). Thus, H.
saxicola, although still an insectivore, does depart from the presumed basal members
of that trophic group in several important anatomical features, and in reaching a
larger adult size, vzz 125 mm.

The nearest living relative of H. saxicola is H. riponianus (Text-figs 34 and 42),
here classified as a mollusc eater (see below). Nevertheless, as the representative of
a specialized structural level, the H. saxicola condition could be ancestral to the pisci-
vorous predator radiation (see p. 82).

60 P.. Ho. GREENWOOD =

H. macrops
H. pallidus

H. empodisma

H. chilotes

Fig. 32. Neurocranial form in insectivorous Haplochromis species (see also Text-fig. 33).
(Scale+— 93 ams)

EVOLUTION OF A’ CICHLID SPECIES FLOCK 61

Also related to H. saxicola, at least on the basis of jaw and neurocranial morphology
(Text-fig. 34), is H. aelocephalus, a predominantly insectivorous species that also
feeds on other invertebrates, including molluscs. Externally, H. aelocephalus is
readily distinguished by its protracted snout which, in extreme individuals, is almost
tubular (see Greenwood, 1959b). The outer jaw teeth in H. aelocephalus are simple
unicuspids like those in H. saxicola, but the inner teeth are arranged in broad bands,
more like those in the H. sauvagei—H. chilotes lineage (see p. 72 below). There is,
however, no reason to suppose that H. aelocephalus is at all closely related to that
lineage, from which it differs in neurocranial morphology, the shape of the outer jaw
teeth, and in having an elongate and slender lower jaw.

H. macrops H. pallidus

H. chilotes

H. chromogynos

Fic. 33. Lower jaw form in insectivorous Haplochromis species (see also Text-fig. 32).
(Scale = 3 mm.)

Even superficially, H. chilotes, with its hypertrophied and lobate lips (Text-fig. 10),
would qualify as a specialized species, a rating confirmed by its feeding habits (see
p. 31). The oral dentition of H. chilotes departs markedly from that in all the
species so far considered (Text-fig. 33). The outer teeth are stout unicuspids with
the crown strongly incurved ; such teeth occur in only one other group of species
(see p. 72 below). The lower jaw is short and stout, but the ascending process of
the premaxilla is relatively longer than in the generalized type of bone. The
neurocranium of H. chilotes could be classified as a derivative of the generalized type
in which the preorbital region has become strongly decurved. Adult H. chilotes
reach a length of ca 150 mm.

62 P. H. GREENWOOD

H. saxicola

H. aelocephalus

H. aelocephalus H. saxicola

Fic. 34. Neurocranial and lower jaw form in insectivorous Haplochromis species.
(Scale = 3 mm.)

Virtually identical syncranial morphology and dentition are found in H. chromo-

gynos (Text-figs 32 and 33), but the lips are not hypertrophied in this species ; adult -

fishes are apparently smaller (maximum length 110 mm) than in H. chilotes.
I would consider H. chilotes and H. chromogynos to be sister species, with H.

chilotes the derived (apomorph) member of the pair. Similarly specialized skull and ©

jaw forms and outer tooth morphology are seen in one lineage of mollusc eaters, and
it is thought that H. chilotes and H. chromogynos are members of the same lineage
(see p. 72, and Text-fig. 66).

Finally in the insectivorcus group there is Haplochromis empodisma, a species which
could be described as a deep-bodied and larger form of the five species described first

EVOLUTION. OF A -GICHLID SPECIES FLOCK 63

in this section (Greenwood, 1960) ; adults of H. empodisma reach a length of 120 mm,
compared to 100 mm in the other species.

The oral and pharyngeal dentition of H. emposdisma are of a basic type, but the
neurocranium departs quite noticeably both from the generalized type (Text-fig. 32)
and, especially, from that of H. chilotes and H. chromogynos. The preorbital profile
is straighter and slopes less steeply because the brain-case depth is somewhat
shallower, giving the whole skull a more linear and less rounded appearance. In
fact, the skull of H. empodisma is almost intermediate between the H. saxicola type
and that of the more generalized species (e.g. H. pallidus and H. macrops).

Admittedly the H. empodisma neurocranial form differs less markedly from the
basic form (e.g. H. pallidus) than does the skull in H. saxicola or, more especially, H.
chilotes. But it does seem to represent a distinct type and one which appears
elsewhere within the flock. One near relative of H. empodisma is the mixed
mollusc—insect eating H. obtusidens (see p. 73 below ; and Greenwood, 1960).

To summarize. Among the insectivorous species there are four distinct lineages
(Text-figs 65, 66,68 and 70). One, the most generalized, departs little from the pre-
sumed ancestral and fluviatile species represented by H. bloyeti. The second (H.
saxicola) shows an elongation of the skull and jaws approaching that found in certain
piscivorous and paedophagous species. The third lineage (H. chilotes and H.
chromogynos) exhibits strong decurvature of the skull anteriorly, strengthening of
the jaws (especially the lower) and a distinctive dentition, all features shared with a
specialized branch of the mollusc-eating trophic group. The fourth lineage (H.
empodisma) represents a slight departure from the generalized H. pallidus-like condi-
tion towards a type seen in certain piscivorous predators and other trophic groups.

Apart from their dentition, the differentiation of these lineages is manifest in a
changed shape to the anterior moiety of the neurocranium and, to a lesser extent, in
the relative length of the lower jaw. In other words, a change in relative growth
patterns. It is probably significant in this connection that there are marked dif-
ferences in the maximum adult size attained by members of the various lineages,
with those of the more specialized lines growing to a larger size.

Phytophagous species

In most respects the morphologically least differentiated member of this trophic
group is H. phytophagus (see Greenwood, 1966b), one of the two species known to
feed directly on macrophytes ; see pp. 39 & 41. Syncranial organization in H. phyto-
phagus is like that in any generalized insectivore. Specialization is seen in the coarser
jaw teeth, the coarser, less numerous teeth on the pharyngeal bones, and in the
lengthened intestine. The dental modifications, however, are but slight variants of
the basic bicuspid oral dentition, and even slighter changes in the pharyngeal denti-
tion ; both are adaptations for biting and then macerating the plant tissues eaten
(particularly leaves).
_ Three of the four algal grazing species (H. nuchisquamulatus, H. lividus and H.

obliqguidens) also have a generalized syncranium. All four species (i.e. including H.
nigricans, see p. 39) have a greatly elongate intestine (Greenwood, 1956b) and rather

64

PY oH. vGREEN WOOD

BIG. 35.

H. erythrocephalus

H. paropius

LS
TRESS

H. obliquidens

Neurocranial and lower jaw form in phytophagous Haplochromis species.
(Seale = 3 muz:)

EVOLUTION JOE A-*CICHELD SRECIES FLOCK 65

fine and numerous pharyngeal teeth, but H. nigricans does show certain syncranial
pecularities not shared by the others.

As far as tooth shape 1s concerned, H. nuchisquamulatus has the least specialized
dentition (Text-fig. 4) since it is of the basic bicuspid type with acutely pointed
cusps ; compared with the generalized insectivore, however, H. nuchisquamulatus
does show an increase in the number of inner tooth rows, a wider area of implantation
for these teeth, and all the teeth are moveably implanted. Hapflochromts lividus, in
comparison, has many outer jaw teeth in which the major cusp is relatively broader
and obliquely truncate (not acute), see Text-fig. 4F ; a few teeth retain a generalized
shape. Inner jaw teeth and the pharyngeal dentition in H. lividus do not differ
from those of H. nuchisquamulatus.

The morphological trend apparent in the teeth of H. lividus is accentuated in H.
obliquidens. Here the minor cusp is suppressed, and the major cusp is drawn out and
obliquely truncate (Text-fig. 4G) ; occasionally some teeth have a vestigial minor
cusp, and a few teeth of the H. lividus-type may be present posteriorly in the pre-
maxilla. Generally the inner teeth are typical tricuspids, but there is often an ad-
mixture of these and teeth differing from those of the outer row only in their smaller
size. (It may be noted that larval H. obliquidens have the fine, setiform teeth that
probably occur in all Haplochromis species irrespective of their definitive adult dental
morphology ; Greenwood, 1956b, and further, unpublished observations.)

It seems reasonable to consider H. obliquidens, H. lividus and H. nuchisquamulatus
as members of a phyletic lineage ; certainly H. obliquidens and H. lividus are sister
species. Although it is difficult to be certain of the relationship between these
species and H. nuchisquamulatus, a relationship seems to be indicated by the slight
departure of tooth form in the latter towards the H. lividus type (i.e. moveable
implantation, expansion of the crown and its less acutely pointed tip). The base of
this lineage lies undetectably within the generalized insectivore species group.

The relationships of H. nigricans, the fourth species feeding on phytoplankton,
provide something of a puzzle. Its oral dentition is of a modified bicuspid type
(Text-fig. 36), but does not show the obliquely cuspidate major cusp typifying the

Saree

Fic. 36. Outer row teeth from the dentary of H. nigricans (seen in lateral view).
(Scale = 1 mm.)

other species. Indeed, many teeth are subequally cuspidate, the cusps rather bluntly
pointed, although the whole crown, as in the grazers, is expanded relative to the
neck of the tooth (Text-fig. 36). The inner teeth are tricuspids and are arranged in
numerous rows with a reduced space between them and the outer tooth row (again,

5

66 P. H. GREENWOOD

like the other species). Haplochromis migricans differs in the shape of its neuro-
cranium, in which the preorbital face is somewhat decurved (Text-fig. 35), and in
having a stouter lower jaw. In both these characteristics, H. nigricans shows some
approach to the H. chilotes-H. chromogynos condition.

The question raised by these contrasting features is whether the neurocranial and
jaw characters indicate relationship to the H. chilotes lineages, or whether they are to
be interpreted as parallelisms.

I incline towards the latter interpretation mainly because of the very different
morphology of the teeth in H. chilotes and other members of its lineage. Haplo-
chromis mgricans, unlike the other periphyton grazers, feeds principally from rocks
and not plants, and it has a rather different feeding method. The epiphytic feeders
scrape algae mainly from leaves which are taken and held between the jaws. Haplo-
chromis mgricans, on the other hand, nibbles algae from a rigid substrate, for which
the stout jaws, downward protrusion of the upper jaw (because of the decurved
surface on which the premaxillae slide) and the subequally bicuspid outer teeth would
appear to be adaptations. ,

The three remaining phytophages (H. dps [Text-fig. 27], H. pavopius and H.
erythrocephalus {Text-fig. 26] ; Greenwood & Gee, 1969) all feed on phytoplankton
apparently gathered from the bottom and not while in suspension ; all have rela-
tively long intestines.

Unfortunately, lack of material precludes a detailed knowledge of cranial anatomy
in H. cinctus ; however, its dentition, both oral and pharyngeal, is of the generalized
bicuspid type (Greenwood & Gee, 1969). Haplochromis paropius has the syncranial
architecture and oral dentition of a generalized insectivore like H. macrops (see
Text-figs 32, 33 and 35), but its pharyngeal dentition is of the finer type found in the
periphyton feeders (Greenwood & Gee, op. cit.).

The neurocranium in H. erythrocephalus differs from this generalized type in
exactly the same way as does the neurocranium of H. empodisma (see p. 63 above ;
also Greenwood & Gee, op. cit.). The pharyngeal and oral dentition of these two
species is also similar. No immediately obvious adaptive features are apparent in
this type of syncranial architecture. Possibly the larger mouth and deeper oro-
pharyngeal cavity (relative to those of the generalized type) are of advantage to a
species which, when feeding, must pass a considerable volume of water and par-
ticulate material through this cavity in order to obtain its food.

Because of their generalized cranial characters and dentition, H. cinctus and H.
paropius cannot be related to any particular species. But because of their specialized
alimentary characters the species must be considered as apomorph derivatives of the |
generalized insectivore stock, and are probably related to one another (i.e. sister
species). Haplochromis erythrocephalus, on the other hand, can be related to H.
empodisma also as a derived species (Text-figs 65 and 70).

To summarize: Three phyletic lines are represented among the phytophages so
far considered. The periphyton grazers comprise a single lineage in which most of
the adaptational stages of the radiation are still extant, together with a differently
specialized offshoot, H. nigricans. The phytoplankton feeders comprise two line-
ages; one (H. cinctus and H. paropius) is little different from the basal insectivore

EVOLUTION OF A CICHLID SPECIES FLOCK 67

stem, the other (H. erythrocephalus) is part of a lineage whose living basal representa-
tive is probably H. empodisma. Haplochromis phytophagus, a browser on macro-
phytes, could belong to the same lineage as H. cincius ; like those species its dentition
shows little departure from the generalized type, but it does have the same alimentary
canal specializations. Possibly the three species are an offshoot of the lineage cul-
minating in the periphyton grazers (Text-figs 65 and 70).

There remains one other species, H. acidens (Greenwood, 1967), which, like H.
phytophagus, feeds directly on macrophytes. The skull, jaws and unicuspid dentition
(Text-fig. 37) of this species conform with the type found among a group of specialized
piscivorous predators (Greenwood, op. cit.), as does the pharyngeal dentition.
Furthermore, despite the vegetarian habitats of H. acidens, its intestine is relatively
shorter than in other plant-eating species, although it is longer than in a piscivore.

Fic. 37. Neurocranium and lower jaw of the enigmatic H. acidens (see p. 41).
(Scale = 3 mm.)

I have suggested elsewhere (Greenwood, 1967) that, anatomically, H. acidens
could be a member of a particular piscivore lineage (the ‘sevranus’ group, see Green-
wood, 1962). It could also be a derivative from an H. empodisma-like species ;
the principal change involved would be an increase in the relative number of uni-
cuspid teeth so that these teeth predominate over bicuspids in both jaws (there is an
admixture of bi- and unicuspids in large H. empodisma [i.e. > 95 mm long] and in
H. acidens < 90 mminlength). In both species the teeth, irrespective of cusp form,
are slender in comparison with those of the generalized type. Considering the rather
indefinite feeding habits of H. empodisma (a benthic insectivore also ingesting quanti-
ties of plant debris) and the interspecific similarities in syncranial architecture, I
would now consider H. acidens to be a derivative of the H. empodisma lineage, rather
than of the ‘seyvanus’ piscivore group (see also p. 41).

Species feeding on benthic Crustacea

This small and trophically rather ill-defined assemblage of five species, the ‘trzdens’
_ group (H. dolichorynchus, H. tyrianthinus, H. chlorochrous, H. cryptogramma and H.
trvidens [Text-figs 24 and 25 ; Greenwood & Gee, 1969 ; Greenwood, 1967] is, how-
ever, well-defined morphologically. Group syncranial architecture (Text-fig. 38) is

68 Ps... GREENWOOD

essentially of the H. saxicola type (Text-fig. 34; see also p. 59 above), but the oral
definition is peculiar. There is a high proportion of tricuspid teeth in the outer_
tooth rows of both jaws, but especially in the lower one. The other teeth in these
series are either slender bicuspids or unicuspids ; that is, like the teeth of H. saxicola.
Unlike H. saxicola, none of the ‘tvidens’ group shows any enlargement of the median
teeth on the lower pharyngeal bone (and never, as in some H. saxicola individuals,
an enlargement of the bone itself ; see Greenwood, 1960).

Fic. 38. Typical neurocranial form in a member of the H. tvidens lineage (ex H. iridens).
(Scale = 3 mm.)

Neither the ‘tvidens’ group nor H. saxicola exhibits any specialized characters
obviously associated with their feeding habits (unless the slightly enlarged
median pharyngeal teeth of H. saxicola are considered thus; but the known
diet for this species does not indicate any increase in the number of molluscs eaten
as compared with generalized insectivores). It is, therefore, impossible to consider
either the ‘tvidens’ species or H. saxicola as the apomorph (1.e. derived) sister group
of the other. That both should be considered part of the same phyletic lineage
seems likely from their shared syncranial specializations.

At least one other species, H. melichrous, might be included in this trophic group
(Greenwood & Gee, 1969). It has a rather generalized dentition of mixed bi- and
unicuspid teeth, but the occasional tricuspid does occur in the posterior part of the
lower jaw. Haplochromis melichrous differs from members of the ‘tvidens’ group in
its neurocranial morphology, and in these characters resembles members of the
‘serranus’ group piscivores (Greenwood, 1967). The dentition of H. melichrous 1s
sufficiently generalized (despite the occasional tricuspid teeth) for it to be of little -
value as a phyletic indicator. Skull and jaw characters are also not particularly
clear-cut in this context, although they do seem to exclude the possibility of relation-
ship with species in the ‘tvidens’—‘ saxicola’ lineage. For the moment, H. melichrous —
can only be associated with the ‘sevvanus’ group, to be discussed on p. 81 ef seq.

In summary, the benthic crustacean-eating group seems to comprise two lineages.
The larger one is a derivative of the H. saxicola line, the smaller (H. melichrous only)
is of uncertain affinity but could possibly be related to the ‘servvanus’ piscivore
lineage (Text-fig. 70).

EVOLUTION: OF A CICHLID SPECIES FLOCK 69

Scale eating species

Comparatively little is known about the anatomy of H. welcomme: (Greenwood,
1966b) the unique lepidophage in Lake Victoria. The slender, moderately elongate
body (Text-fig. 3), and the superficial head shape of this species are not unlike those
of species in the ‘ividens’ group discussed above. The broad bands of inner teeth
in H. welcomme: (Text-fig. 39) are a specialization not found in that group, and are
in fact not approached by the dental pattern in any other species (except, perhaps,

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below. Only one half of each jaw is shown.

the monotypic Platytaeniodus degent, see p. 103 and Text-fig. 73). Judging from
radiographs of the head (no skeletons are available), H. welcomme: does have a
neurocranium like that of a ‘tvidens’ group species, although it also resembles H.
paraguiarii, one of the piscivorous predators (see p. 89 below). Until good osteo-
logical material is available the relationships of H. welcomme: must remain enig-
matic, although the indications are of affinity with the ‘tvzdens’ lineage (Text-fig. 70).

Mollusc eating species

_ The clear-cut dichotomy in feeding methods among species in this trophic grade
has been discussed in detail on p. 37. |

Those species that wrench snails from their shells (or crush the shell orally) con-
stitute one of the best defined phyletic lineages within the whole flock. Specializa-
tions shared by all four species (H. sauvagei [Text-fig. 19], H. prodromus, H. grants
[Text-fig. 20] and H. xenognathus [Text-fig. 21]) are the strongly decurved, in some
species almost vertical, preorbital skull, a stout lower jaw, the stout unicuspid teeth

70 P. H. GREENWOOD

H. prodromus H. xenognathus

H. prodromus

Fic. 40. Neurocranial and jaw form in two species of mollusc-eating Haplochromis,
both oral-shellers. (Scale = 3 mm.)

with strongly incurved crowns, and the broadly arranged rows of unicuspid inner
teeth (see Text-figs 40, 41 and 66; also Greenwood, 1957). Smaller members of
these species (that is fishes between 80 and 100 mm long, depending on the maximum
size reached in the species) do have bicuspid outer teeth, or a mixture of bi- and
unicuspids. The bicuspids, like the unicuspids, are strongly recurved, thus contrast-
ing with the barely recurved generalized type of bicuspid. The lower jaw is shorter
than the upper in all species but H. granti, where it is sometimes a little longer.
Haplochroms grant: also differs from other members of the group in having the
mouth inclined upwards at a small angle ; it is horizontal in the others.

Anatomically, H. xenognathus is the most specialized species, H. sauvage: and H.

prodromus the least specialized (cf Text-figs 40 and 41); but these degrees of dif-
ference are not apparent in feeding habits, which are identical (Greenwood, 1957).
Haplochromis xenognathus differs chiefly in having some lower jaw teeth implanted
horizontally, the inner tooth rows in much broader bands, with those of the
dentary presenting a convex occlusal surface (see Text-fig. 41C). Haplochromis
sauvager and H. prodromus are virtually identical in their oral, dental and neuro-
cranial morphology, but individuals of the latter species reach a larger size (130,
cf 105 mm).

EVOLUTION OF A CICHLID SPECIES FLOCK 71

The monotypic genus Macropleurodus bicolor is, on the basis of its syncranial
architecture, a member of the same species group. The jaw teeth of M. bicolor
(Text-fig. 75) differ from those of other species in being coarser, more strongly in-
curved and in generally retaining traces of a minor cusp (Text-fig. 75B). This cusp
persists as a slight, vertical hump on the near-horizontal occlusal surface presented
by the major cusp. The dentigerous arms of the premaxillae are bowed (usually
more so on one side than the other) ; consequently one side of the mouth is slightly

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both oral shellers. A: H. prodvomus, occlusal view, premaxilla uppermost. Band C:
H. xenognathus, occlusal view of both jaws, and lateral view of lower jaw respectively.

open even when the jaws are closed. This peculiar arrangement could be of adaptive
significance in a species whose feeding involves grasping a snail so that it cannot
withdraw into its shell. In other words, because of its arched upper border the gape
is increased without an increase in the extent to which the dentary would otherwise
_ have to be lowered.

The near vertical ethmoid region (over which the ascending processes of the pre-
maxillae run) in all H. sauvagei-group species (see Text-figs 40 and 66) produces an

72 P. H. GREENWOOD

unusual jaw opening movement, namely downward and slightly forward rather than
mostiy forward ; the short and deep adductor mandibulae muscles ensure a powerful
and rapid closing action for the dentary. The strong jaws and teeth, coupled with
these jaw movements, all indicate a high level of adaptation for the unusual feeding
methods practised by members of the lineage. It is interesting to see that the ethmo-
vomerine bloc in the skull of these fishes is slightly longer than the near-horizontal
ethmo-vomer of a generalized skull. (In fact, it is relatively as long as in many
piscivorous species groups; see pp. 80-93.) Presumably the lengthened ethmo-
vomer gives added support and backing to the premaxillary processes when the
upper jaw is protruded downwards and the fish is wrenching a snail from its shell.

A possible phyletic relationship between the H. sauvagei group and the insecti-
vorous species H. chilotes and H. chromogynos has already been suggested (p. 61).
The skull in these latter species is rather less strongly decurved (see Text-figs 32,
40 and 66), and this coupled with their relatively unspecialized feeding habits

(except, on occasion, in H. chilotes, see p. 31), leads me to rank the H. sauvager —

lineage as the apomorph sister group of the H. chilotes-H. chromogynos pair. Phylo-
genetically it may be significant that black-and-white piebald female polymorphs
(see p. 53) are recorded in four of the six species in this lineage (H. sauvager, Macro-
pleurodus bicolor, H. chilotes and H. chromogynos [where it is, indeed, the ‘normal’
female coloration]). Similar polychromatism occurs in several other species (none
closely related to the “sauvagez’ lineage) but never elsewhere is it known from so
many species in a presumed lineage (see pp. 53-54 above).

When more is known about certain Lake Victoria species, for example H. crassila-
bris (see Regan, 1922), the H. sauvagei lineage may have to be expanded. Hopefully
it will then prove possible to find the group’s plesiomorph relatives.

The second mollusc eating group is made up from those species in which the prey is
crushed between the upper and lower pharyngeal teeth and bones.

Two species, H. tshmaelt and H. pharyngomylus (Greenwood, 1960; also p. 37
above), have the most highly developed pharyngeal mills (see Text-fig. 5A). The lower
bone is greatly enlarged and most of its teeth are molariform ; the upper bones are
correspondingly modified. The skull is essentially like that of the generalized type,
except for the better-developed ventral apophysis on which the upper pharyngeal
bones articulate, see Text-figs 43 and 44. This apophysis is formed, as in all Haplo-
chromis species, mainly from the parasphenoid and basioccipital bones, but there is
also a small contribution from the prootics as well (Text-fig. 44D). The jaws and
oral dentition are essentially those of a generalized species like H. pallidus (see Text-

figs 33 and 43). What differences there are lie within the limits of variation resulting ©

from allometric growth; individuals of H. ishmaelt and H. pharyngomylus reach a

much larger size (125-135 mm) than do those of the ‘pallidus’ insectivore group

(ca 100-105 mm).

Superficially, H. obtusidens closely resembles H. ishmaeli and H. pharyngomylus
(see Greenwood, 1960), but its pharyngeal mill is at an intermediate level of hyper-
trophy, the lower bone moderately stout and its dentition partly molarized ; see
Text-fig. 44B. The paryngeal apophysis on the skull is also at an intermediate level
of specialization.

EVOLUTION OF A CICHLID SPECIES FLOCK 73

Fic. 42. Haplochromis riponianus. (Natural size.)

The skull of H. obtusidens taken as an entity is, however, more like that of H.
empodisma (cf Text-figs 32 and 43), an insectivorous, bottom-detritus eating species
(see p. 63 above). Thus, although I have previously indicated a close relationship
between HZ. obtusidens and the H. tshmaeli pair (Greenwood, 1960) and therefore a
possible phyletic lineage of increasing specialization, I now suspect that this was an
error. Recent analysis of various character complexes suggests that although H.
empodisma and H. obtusidens are related (and are members of the ‘empodisma’
lineage, see p. 63) and although H. ishmaeli and H. pharyngomylus are also inter-
related, the latter species pair belong to a distinct lineage (Text-fig. 70).

The most likely plesiomorph sister species for H. tshmaelt and H. pharyngomylus
is H. humilior (Text-figs 5C and 43; see also Greenwood, 1960). In H. humulior the
pharyngeal mill is moderately developed (and shows a high degree of intraspecific
variability, see Greenwood, op. cit.) and the pharyngeal apophysis shows some depar-
ture towards the ‘zshmaelt’ condition (an increased area of basioccipital in the facet ;
see Text-fig. 44C). But the overall form of the neurocranium in H. humilior is of the
basic insectivore type, with a short and decurved preorbital face (see Text-fig. 43).
Apart from the larger pharyngeal apophysis, the neurocranium in H. zshmaeli is
identical with that of H. humilior (Text-fig. 43).

Haplochromis humlior could well be derived from a species like H. pallidus, a
taxon in which there is already some slight hypertrophy of the lower pharyngeal
teeth (see p. 59). The close correlation that can exist between the relative massive-
ness of the pharyngeal bones (and their teeth) and the degree to which the neuro-
cranial apophysis is developed has been clearly demonstrated in both natural and
experimental populations of the mollusc-crushing Astatoreochromis alluaudi (Green-
wood, 1959a, 1965c). It is also apparent in ontogenetic series of H. tshmaeli and
H. pharyngomylus (personal observations). Thus the interspecific differences seen
in that region of the skull in H. pallidus and H. humilior on the one hand and H.
ishmaeli and H. pharyngomylus on the other would seem to be associated with in-
creasing hypertrophy of the pharyngeal mill.

74 P. H. GREENWOOD

Zane if
H. humilior peo ( \
d \

|

H. ishmaeli

H. obtusidens

H. obtusidens

Fic. 43. Neurocranial and jaw form in some mollusc-eating species (all pharyngeal
crushers). Arrow indicates the apophysis (formed from the parasphenoid and _ basi-
occipital bones) on which the upper pharyngeal bones articulate (see Text-fig. 44). (Scale
=3 mm.)

All the species considered so far are those in which Mollusca (especially gastropods)
are the chief food source. Two other species, H. riponianus and H. theliodon
(Greenwood, 1960), are mixed insect—mollusc eaters.

Haplochromts riponianus shares the syncranial (Text-fig. 34) and dental charac-
teristics of H. saxicola but with a more consistent hypertrophy of the median tooth

EVOLUTION: OF A CICHLID SPECIES FLOCK 75

rows on the lower pharyngeal bone, and generally some enlargement of the bone as
well. As in all other species with similar characteristics of the pharyngeal mill, the
degree of bone and tooth hypertrophy is size correlated. Phylogenetically, H.
viponianus is clearly the apomorph sister species of H. saxicola.

Lack of sufficient material for anatomical studies makes it impossible to suggest
the relationships of H. theliodon (see discussion in Greenwood, 1960).

In brief, at least four distinct lineages are involved in the mollusc-eating adaptive
radiation ; each can be traced back to an essentially insectivorous level still repre-
sented by different species in the flock (Text-figs 65 (3), 66, 68 (2) and 70).

Predators on larval and embryo cichlid fishes

This, the paedophage radiation, was described at length on pp. 31-37. There
is a clear-cut diphyletism in the group, the branches comprising H. obesus, H.

Fic. 44. Ventral view of the neurocranial apophysis for the upper pharyngeal bones,
showing the relative increase in the size of the basioccipital facets correlated with
increasing stoutness of the pharyngeal bones and teeth (see Text-fig. 5). (Scale = 3 mm.)

A: H. empodisma (typical of condition found in most species).

B: H. obtusidens (a species with slightly enlarged pharyngeal bones and teeth).
C: H. humilior (with moderately enlarged pharyngeal bones and teeth).

D: H. ishmaeli (massive pharyngeal bones and teeth).

76 P. H. GREENWOOD

maxillaris and H. melanopterus (Text-figs 3 and 17), and H. cryftodon, H. microdon
and H. parvidens (Text-figs 3 and 18) respectively (Greenwood, 1959b). There are
two other paedophagous species, H. cronus (Greenwood, op. cit.) and H. barbarae
(Greenwood, 1967) whose lack of anatomical specializations relative to the main
lineages make their relationships difficult to determine (Text-figs 16 and 29).

In both lineages the anatomical specializations involve, particularly, development
of a large mouth that is both protrusible and laterally distensible, a reduction in the
number of jaw teeth, together with their restriction to the anterolateral parts of the

H. obesus

H. barbarae

SES

H. microdon

Fic. 45. Neurocranial form in paedophagous species (see text p. 75; also Text-fig. 46).
(Seale)—=) 3mm.)

EVOLUTION OF A-.CICHLID SPECIES FLOCK 77

jaw bones, and their almost complete burial in the thickened oral mucosa. (In one
species, H. maxillaris the teeth are further covered by an inward curvature of the
upper lip tissue.)

The functional anatomy of the jaws in these species has not been adequately
analysed. Dissection does not reveal any marked departure from a typical arrange-
ment and interrelationship of the jaw bones, ligaments and muscles. However, in
all species the ascending premaxillary processes are long, the maxilla is rather bullate
distally, and in all except H. obesus and H. maxillaris, the lower jaw shows a marked
narrowing at about the middle of its length. As a result of this latter peculiarity,
the lower jaw closes within the upper jaw. Gauged from the effects of manipulation
on freshly dead fishes, the mouth is more protrusible, and there is greater lateral
displacement of the upper jaw in members of the H. cryptodon lineage than in those
of the H. obesus line.

Haplochromis obesus, H. maxillaris and H. melanopterus are characterized by all or
most of the outer dentary teeth having the cusp inclined outwards (Text-fig. 460A).
This tooth shape is found in no other Lake Victoria Haplochromis species. Haplo-
chromts obesus has a neurocranium rather like the generalized type (Text-fig. 45).
That of H. maxillaris (Text-fig. 45) has a slightly straighter preorbital face, in this
respect approaching the H. empodisma skull type (see Text-fig. 32). Despite this
difference in neurocranial shape, the shared peculiarity in lower jaw tooth shape
seems to exclude the possibility of there being closer relationships between H.
empodisma and H. maxillaris than between the latter species and H. obesus or H.
melanopterus. Judging from the relative extent of jaw protrusibility in H. maxillaris
(possibly correlated with the flatter skull profile) this species is more specialized than
H. obesus. Regrettably no skeletal material of H. melanopterus is available, and the
species is included in the H. obesus lineage mainly on the characteristic shape of its
lower jaw teeth (see Greenwood, 1959b).

Neurocranial shape in the H. cryptodon and H. parvidens lineage (Text-figs 45 and
68) is essentially of the type found in the less extreme members of the ‘prognathus’
group of piscivorous predators (see Greenwood, 1967, and pp. 85-89 below). Haplo-
chromis parvidens (Text-fig. 45) has the most ‘prognathus’-like skull, H. microdon
and H. cryptodon the least modified in that direction (Text-fig. 45). Dentary shape
is correlated with neurocranial shape, H. parvidens having the most extreme degree
of anterior narrowing (Text-fig. 46C). It is this unusual and unique shape of the
dentary, combined with overall neurocranial morphology, that provide the principal
evidence for the presumed monophyly of the group. Morphologically, the oral
teeth in these fishes are like those of typical piscivorous predators in the ‘serranus’
and ‘prognathus’ groups (see Greenwood, 1960, 1967 ; and pp. 82-89 below).

The maximum adult size reached by members of both paedophage lineages is in
the range of 130-170 mm ; that is, these are among some of the larger Haplochromis
species in Lake Victoria.

Haplochromis barbarae (Greenwood, 1967) and H. cronus (Greenwood, 1959b) are
included as members of the paedophage group solely on the basis of their feeding
habits. Neither species shows any of the dental or oral specializations of either the
H. obesus or H. cryptodon lineages.

78 P. H. GREENWOOD

Fic. 46. Lower jaw in two paedophagous species. A: H.obesus. BandC: H. parvidens.
A and B in lateral view, C in ventral view to show characteristic outline of the dentary in
H. parvidens-group paedophages. (Scale = 3 mm.)

In H. cronus the outer jaw teeth are moderately stout unicuspids, not noticeably
reduced in number or size, nor restricted in their distribution nor deeply embedded
in the mucosa. Little is known about the syncranial architecture of the species,
except from partial dissection of one fish. Judging from information gleaned in
this way, H. cronus does not have the syncranial characteristics of any piscivorous ©
group. Like H. tshmaeli, which it resembles in many ways, H. cronus seems to
share the syncranial morphology of a generalized insectivore, but it is larger than
any of these fishes (adult sizes range to at least 135 mm). Unlike the majority of
Lake Victoria species, irrespective of their trophic associations, H. cronus has almost
the entire surface of the caudal fin densely covered with small scales (Greenwood,
1959b).

As H. cronus seems to have the syncranial architecture and dentition of a general-
ized Haplochromis, it could be ranked as the plesiomorph sister group to the H.

EVOLUTION OF A CICHLID SPECIES FLOCK 79

obesus lineage. These fishes, more than those of the H. cryptodon lineage, have
retained a near-generalized skull and jaw morphology (despite the slight but obvious
specializations of the latter). For these reasons, the relationships of the H. obesus
lineage cannot be defined readily. It could be considered either an independent off-
shoot from the basal complex of insectivorous species (p. 63 above) or as a derivative
of the A. cinereus—H. squamulatus line.

Haplochromts barbarae, on the other hand, has the syncranial architecture (Text-
fig. 45) of the ‘altigenis’ predator group (see p. 82), and the type of oral dentition
found in small individuals of that species assemblage (adult H. barbarae are
85-106 mm long). Basically, skull morphology in members of the ‘altigenis’ group
is not greatly different from that in less specialized species of the ‘prognathus’
group (Greenwood, 1962, 1967 ; also pp. 82 & 85 below). It will be recalled that the
neurocranial form in the H. crypiodon lineage is also like that among basal members
of the “prognathus’ group (see above, p. 77). Thus, in view of its feeding habits
and of its anatomical specializations, H. barbavae could be included in the H.
cryptodon lineage as the plesiomorph sister group of the other species combined.

Fryer & Iles (1972) believe that there is ‘. . . lack of striking diagnostic indications
of feeding habits among these species .. .’ and that this ‘. . . is not really surprising’.
They go on to argue that the collection of such ‘soft morsels’ as fish embryos and
larvae does not require the evolution of a specialized anatomy in the predator.
Furthermore, Fryer & Iles believe the morphological variation found in paedophage
species suggests ‘. . . dissociation of structure and function ...’. I fail to find any
evidence supporting a single one of these ideas.

In both paedophage lineages there is ample evidence for anatomical differentiation
in jaw morphology, especially in the H. cryptodon lineage (see above), and in the
buried dention of all species (a specialization that Fryer & Iles themselves acknow-
ledge). Finally, the manifestation of these various anatomical traits is very obvious
to anyone who has handled fresh specimens and compared the extent of their jaw
protrusion with that in most other Lake Victoria Haplochromis species. (Some
predator species are excluded from this generalization, but these belong to lineages
whose basic cranial specializations are greater than those of the paedophages.) As
for the postulated dissociation of structure and function, surely the anatomical
evidence negates any such idea in its entirety?

I find it surprising that Fryer & Iles should think that there are no diagnostic
indications of feeding habits among the paedophages. Once one has associated
the morphology of any paedophage species with its diet, it is remarkably easy to
recognize any other paedophage at sight, or so has been my experience and that of
others working in the field, even when dealing with the species of another lake.

The intraspecific variability seen in paedophagous species (Greenwood, 1959b) is
high, but no higher than that in many other species. It is perhaps the generally
bizarre cranial morphology of these fishes that accentuates this variability. I can
find nothing to suggest, as Fryer & Iles imply, that paedophage anatomy is not
directly correlated with feeding habits (i.e. is non-adaptive) and that there has been
a consequent relaxation of selection pressure leading to greater deviation from the
mode in these characters. Fryer & Iles’ views, I suspect are coloured by their

80 Pon GREENWOOD

belief in the idea that paedophages do not actively obtain their prey from a parent
fish, but snap up voluntarily jettisoned young and embryos (see p. 33 above).

I find myself more in agreement with Fryer & Iles (op. czt.) when it comes to the
question of how paedophagous habits originated. The habit probably stems from a
facultative response to the appearance of young liberated by the parent during the
normal course of brood care. That many Hapflochromis species, irrespective of their
usual feeding habits, respond to the sudden appearance of small objects in the water
is often demonstrated in Lake Victoria. On several occasions at Nasu Point beach
near Jinja, every species present was found to be gorged on termites after a heavy
hatch of these insects had been carried into the lake. On other occasions all species
(including specialized piscivores) had ingested large quantities of colonial blue-green
algae that were floating in the water after a period of rough weather (unpublished
personal observations).

Whatever the origins of paedophagy, there are now two phyletic lines of paedo-

phagous species in Lake Victoria (the only lake, apart from Lakes Edward and —

George, in which the habit has evolved [Greenwood, 1973a]). One lineage (H. obesus
and related species) evolved from a basic piscivore stem, the other (H. cryptodon
and allies) from a derived, piscivore line (Text-figs 67, 68 and 70).

Piscivorous predators

The 35 or more species in this trophic group present the most complicated phyletic
puzzle in the whole flock. In part this is attributable to the larger number of species
involved, but mainly it is because of the few characters that can be used to determine
relationships. Whereas in other groups oral and pharyngeal dentition provide
indications of relationship, among predators the dentition is essentially a uniform
one of strong, somewhat recurved, unicuspids (Text-figs 4B and 57). Even small
individuals have this type of dentition, although in juveniles the teeth are bicuspid
and of the generalized type. Body form, too, is of little value. The only character
complex seemingly of phyletic value is the syncranium, especially the shape of the
neurocranium (Greenwood, 1962, 1967).

Difficulties are also encountered when interpreting these neurocranial features,
and it seems unlikely that a satisfactory scheme of phyletic interrelationships can
be achieved. To start with, it is impossible to tell whether the main groups of
predators are of monophyletic origin, even if the concept of monophylogeny is
broadened to include origin from more than one species provided the species are
themselves sister taxa.

The chief diagnostic features of the piscivorous predator grade concern adaptations.

for feeding on larger and faster moving objects than are utilized as prey by the other
trophic groups. This has involved elongation of the preotic part of the skull,

elongation of the jaws (often associated with a marked upward inclination of the

gape), and the development of a strong, unicuspid dentition adapted for holding a
struggling prey fish. In short, the production of a large-mouthed, streamlined fish
of a somewhat greater size than the members of species in other trophic groups.

In previous papers (Greenwood, 1962, 1967) three principal groups of piscivorous
predators were defined, chiefly on the grounds of neurocranial shape and proportions.

EVOLUTION: OF: A CICHEID SPECIES FLOCK 81

H. guiarti H. squamulatus

H. martini

H. serranus

Fic. 47. Neurocranial form in piscivorous predators. The species represented are from
the H. guiarti-H. squamulatus and the H. serranus lineages. (Scale = 3 mm.)

The first or “servranus’ group (comprising eight species) has a neurocranial form
nearest that of the generalized type, but one already showing some elongation of the
preotic skull and a marked flattening of the dorsal outline to the preorbital face
(Text-figs 47 and 57). The second or ‘altigenis’ group (also of eight species) has a
more elongate neurocranial outline, with the preotic face slightly longer and sloping
less steeply than in the ‘sevvanus’ type (Text-figs 51 and 57). The third or ‘frogna-
thus’ group (11 species, Text-figs 51, 57 and 62) shows further accentuation of the
‘altigenis’ trend, together with an overall narrowing of the skull. A number of

6

82 P. H. GREENWOOD

smaller and probably polyphyletic groups, all of uncertain affinities with the major
ones, were also recognized (Greenwood, op. cit.).

Originally I thought the three major groups were each of monophyletic origin,
but with a strong possibility of the ‘altigenis’ and ‘prognathus’ groups stemming
from an ancestor not shared with the ‘sevrvanus’ group. However, species discovered
recently (Greenwood & Gee, 1969) and further study of the known species have
caused me to modify somewhat the views expressed before.

To begin with, it seems that the ancestral skull type 1s not of the kind found in
H. guiarti and H. brownae (pace Greenwood, 1962). These species have a skull form
very like the generalized insectivore type (see pp. 57-59), whereas the basic predator
skull type (‘serranus’ group) is, in fact, more specialized and akin to that found
in H. saxicola (see p. 59). Haplochromis saxicola is, of course, an insectivore but
its whole level of syncranial organization departs from the generalized H. pallidus
type toward that of the piscivorous predators (including preotic elongation of the
neurocranium, marked flattening of the dorsal preorbital profile and a preponderance
of uni- over bicuspid teeth). Individuals of. H. saxicola also reach a larger adult
size than do those of the H. macrops-like species ; but adult size may be of secondary
importance because H. brownae, an insectivore—piscivore is no larger than H.
macrops. The possible relationships of H. brownae and H. guzartt will be discussed
later (p. 85).

Since H. saxicola (despite its insectivorous habits) has a neurocranial form already
specialized towards that of the piscivorous predators, it seems more reasonable to
consider some HZ. saxicola-like species as the ancestor of almost the entire piscivorous
predator radiation.

Of the three predator groups originally defined, I would now consider the ‘alt-
gems’ and ‘prognathus’ lines to represent a single phyletic assemblage (henceforth
called the prognathus group). In other words, species of the ‘frognathus’ group
could be derived both from species at an ‘altigenis’ level of specialization and from
species that had already reached the ‘prognathus’ level. This conclusion was
reached after reexamination of the two ‘lineages’ had shown not only their great
similarity, but also the impossibility of demonstrating, unequivocally, that a species
in the more specialized lineage could only be derived from an equally specialized
taxon rather than as a somewhat more apomorphic derivative of a species at the
‘altigents’ level.

The phyletic integrity of the ‘serranus’ group, on the other hand, remains un-
changed, although its membership has to be increased (see p. 84 below). There is
no evidence to suggest that any member of the ‘prognathus’ lineage might have been
derived from a ‘serranus’-like species. The specialized neurocranial form in the
‘pbrognathus’ lineage is more readily derived from that of the presumed H. saxtcola-
like common ancestor of the two lineages than through a ‘sevranus’-like form.
Neurocranial shape in the ‘servranus’ lineage is less variable interspecifically than it
is in its apomorph sister group (‘prognathus’), and the general facies of its con-
stituent species is also more uniform (cf Text-fig. 68 (3) with Text-figs 68(4) and 69).

Determining the intrarelationships of species within the two lineages is very
difficult, and the results presented here must be considered extremely tentative.

EVOLUTION OF A CICHLID SPECIES FLOCK 83

Peat

Fic. 48. Haplochromis guiarti. (About % natural size.)

Fic. 49. Haplochromis squamulatus. (About half natural size.)

Fic. 50. Haplochromis martini. (About natural size.)

84 P. H. GREENWOOD

H. paraguiarti

H. flavipinnis

H. xenostoma

Fic. 51. Neurocranial form in piscivorous predators. (Scale = 3 mm.)

To the eight species originally placed in the ‘sevvanus’ group (H. serranus [Text-fig.
11], H. victorianus, H. nyanzae, H. speki [Text-fig. 12], H. maculipinna |Text-fig. 47],
H. boops, H. thuragnathus and H. pachycephalus ; see Greenwood, 1967), three others
should be added, viz H. cavifrons [Text-fig. 3], H. plagiostoma [Text-fig. 47] and H.
decticostoma (see Greenwood, 1967; Greenwood & Gee, 1969). Neurocranial
morphology in all three species (Text-figs 47 and 57) is typically that of the ‘serranus’
lineage, despite the rather atypical general facies of H. cavifrons and H. plagiostoma
(Text-fig. 3). Indeed, apart from these two species the ‘sevvanus’ lineage has a

EVOLUTION OF -A-CIGHLID SPECIES FLOCK 85

remarkably uniform facies. Haplochromis cavifrons and H. plagiostoma not only
differ in their gross appearance (from one another as well as from other species) but
also have coloration that is outstandingly different.

Because of the few noticeably specialized features shown by its members, intra-
lineage relationships are not at all distinct. Once again A. cavifrons and H. plagio-
stoma are outstanding (because of their oblique jaws), but there is little else to indi-
cate a particularly close relationship between them. Certainly their coloration
would belie any such suggestion (see Greenwood, 1962).

As mentioned earlier, Haplochromis guiartt (Text-fig. 48), formerly considered a
member of the ‘altigenis’ group (see Greenwood, 1967), has a neurocranial shape
little different from that of the generalized H. pallidus type (see Text-fig. 47 ; and
pp. 58-59 above). What specialization there is, is manifest in the somewhat more
elongate preotic skull, and the slightly less curved preorbital skull roof. The denti-
tion in H. guzarti is, however, predominantly unicuspid in fishes of a size that in H.
pallidus-like species would have bicuspid teeth only. In this respect H. guzarti is
a more specialized (and larger) form of H. brownae (Greenwood, 1962), a species little
removed in neurocranial form and in dentition from H. pallidus. Thus, H. gwiarti
and H. brownae could be sister species, apomorph derivates from the H. pallidus—H.
macrops species complex.

Three other piscivorous (or predominantly piscivorous) species, H. michaeli, H.
squamulatus (Text-fig. 49) and H. martini (Text-fig. 50), have a neurocranial shape
close to that of H. gwiarii (see Text-figs 47 and 67 ; also Greenwood, 1962, 1967, 1960
for the species respectively). In H. martini (maximum length 104 mm) the outer
series of jaw teeth are mostly bicuspids, with a few unicuspids intercalated ; in H.
squamulatus (a larger fish, maximum size 198 mm) a similar admixture of teeth is
found in fishes less than 115 mm long, but unicuspids predominate in larger fishes,
while in H. michael1 (maximum size 145 mm, smallest known specimen 117 m) all
the outer teeth are unicuspid.

All three species have very small scales on the pectoral region (a character rarely
encountered in the Lake Victoria species), and a well-developed, apparently in-
variable, midlateral stripe from the opercular margin to the caudal fin origin or
slightly beyond (another unusual feature for this species flock). Furthermore, both
H. martim and H. squamulatus have a distinctly yellow ground coloration, also an
uncommon feature. (The live colours of H. michaels are not known.)

Although neurocranial shape (Text-fig. 47) in these species (and in H. guzarti) 1s
more like the generalized than the ‘serranus’ type, it is nevertheless a derived form
(see above). Thus H. guzarts and the species discussed above may represent a true
phyletic lineage, with H. squamulatus, H. martint and, H. michaeli more closely
related to one another than any one is to H. guiarti (Text-figs 67 and 70). The
origin of this presumed lineage, unlike that of the ‘serranus’ and ‘prognathus’
lineages, is probably from an H. macrops- or H. pallidus-like species, for example a
species akin to H. brownae which is part insectivore and part piscivore (Greenwood,
1962). ,

_ The 20 species comprising the ‘ prognathus’ lineage (i.e. the combined ‘ prognathus—
alugents’ groups of Greenwood, 1962 and 1967; see p. 82 above) all have a more

GREENWOOD

Peon

86

(About half

: HA. flavipinnis.

B

(About natural size.)

: H. percoides.

A

Fic. 52.

)

1Ze

natural s

Haplochromis paraguiarti.

53°

FIG

EVOLUTION OF A CICHLID SPECIES FLOCK

ae ei Tire

Fic. 54. Haplochromis pseudopellegrini.

Fic. 55. Haplochromis gilberti.

Fic. 56. Haplochromis xenostoma ; a juvenile fish. (About half natural size.)

87

P. H. GREENWOOD

H. gowersi

H. mento

Fic. 57. Neurocranial and lower jaw form in piscivorous predators. The neurocrania are
from members of the H. prognathus lineage, the lower jaws from members of the H.
sevvanus (left) and H. prognathus (right) lineages. (Scale = 3 mm.)

Fic. 58. Haplochromis pellegrint. (About natural size.)

EVOLUTION OF A CICHLID SPECIES FLOCK 89

specialized skull form than that occurring in the other two predator lineages (see
Text-figs 51, 57, 68(4) and 69). The preotic length of the neurocranium is further
elongate (65-68 per cent of neurocranial length, cf 60-65 per cent for the other
lineages), the brain-case is shallower (28-32 per cent neurocranial length, cf 34-40
per cent), and the preorbital profile slopes at a much smaller angle (cf Text-figs
68(3) and 68(4) ; also Text-figs 47 and 51). Within the lineage a gradual intensifica-
tion in this trend can be detected.

Two species (H. bayont and H. dentex [Text-fig. 63]; see p. 92 below) in the
‘prognathus’ lineage can be grouped together on the basis of their having a skull in
which the ethmo-vomerine region is noticeably decurved, although the rest of the
skull retains the form typical for this lineage (Text-fig. 62).

Apart from these two species, all the others can, on the basis of increasingly
specialized skull form, be collected into four subgroups. The phyletic interrelation-
ships of the subgroups are but vaguely discernible. Indeed these categories show in
cameo the difficulties involved in studying the phylogeny of the whole flock. Essen-
tially, the problem is whether these intralineage groups are true, hierarchically
evolved, sister groups (showing increasing apomorphy), or whether they represent
gradal assemblages of polyphyletic ancestry (the ancestral species of each having, of
course, reached the ‘prognathus’ level of apomorphy). For the moment, this prob-
lem seems insoluble.

Species in each subgroup show some variation in gross morphology, although
most are elongate, relatively slender fishes (the adult size range 140-200 mm),
with a large mouth in which the inner and outer teeth are strong and unicuspid
(even in small fishes, although some bicuspid outer and tricuspid inner teeth are
found in the smallest fishes where these are known).

The first subgroup (‘pavaguiartt’) has a neurocranial shape nearest that charac-
terizing the ‘servranus’ lineage (Text-figs 51 and 68(4); see p. 84). Of its seven
constituent species, four, H. paraguiarti (Text-fig. 53), H. gilberti (Text-fig. 55), H.
pseudopellegrimt (Text-fig. 54) and H. altigenis are fairly similar in appearance, having
a slightly oblique mouth and moderately slender body (Greenwood, 1967 ; Green-
wood & Gee, 1969). Other species depart from this morphotype. Haplochromis
artaxerxes has greatly elongate pectoral fins and a near horizontal mouth (Greenwood,
1962), H. xenostoma (Text-fig. 56) has a markedly oblique mouth (40-45 degrees
with the horizontal) and a rather deeper body (Greenwood, 1967), while H. favipinnis
(Text-fig. 52B) also has an oblique mouth but with a deeply concave dorsal head
profile (convex or straight in the other species ; Greenwood, 1962).

Neurocranial form in members of the ‘faraguzarti’ subgroup is shown in Text-fig.
68(4). ;

- Morphologically, species of the second subgroup (‘prognathus’, containing five
species) are somewhat less uniform than those of the ‘faragwiarti’ subgroup.
Haplochroms prognathus (Text-fig. 13 ; Greenwood, 1967) and H. barton (Greenwood,
1962) are closely similar species, but H. mandibularis (Greenwood, 1962) has a nar-
rower head, deeper cheek and more prognathous lower jaw, giving it a distinctive
appearance seen again in a species of the following subgroup. Hapflochronus
pellegrint (Text-fig. 58 ; Greenwood, 1962) is of interest because of its small adult

P. H. GREENWOOD

Fic. 59. Haplochromis macrognathus. (About half natural size.)

Fic. 60. Haplochromis longivostris. (About half natural size.)

GL
ee & =

Fic. 61. Haplochromis argenteus.

EVOLUTION OF A CICHLID SPECIES FLOCK gl

size (7I-105 mm). Inits gross morphology H. fellegrinz is rather like H. paraguiarti
(of that nominal subgroup) but its neurocranial shape is virtually identical with that
of H. prognathus ; in other words, of a more specialized kind. The fifth member,
H. percoides (Text-fig. 52A ; Greenwood, 1962) also has small adults (7o-95 mm),
but its body shape and head form are quite unlike those of H. pellegrini ; in these
characters H. percoides closely approaches H. flavipinnis (of the ‘paragumiarti’
subgroup), a species with which I previously considered it to be closely related
(Greenwood, 1967). Like H. flavipinnis, H. percoides has a distinctive and unique
colour pattern (cf Text-figs 52A and B).

Neurocranial form in members of the ‘prognathus’ subgroup is shown in Text-figs
51 and 60(1).

The five species comprising the ‘estoy’ subgroup are perhaps the most striking and
obviously predatory Haplochromis in the ‘prognathus’ lineage. All have what may
be considered a ‘full’ development of the skull type characterizing the lineage
(Text-figs 57 and 69(2)), and all except H. longirostvis (maximum adult size 145 mm)
are among the larger piscivorous Haplochromis species in Lake Victoria.

Three species, H. gowersi, H. mento (Text-fig. 15) and #. estor (Text-fig. 14) are
rather similar in appearance (Greenwood, 1962). <A fourth, H. longirosiris (Text-fig.
60 ; Greenwood, 1962), does not depart greatly from these species except for its
rather terete habitus ; skull shape in H. longirostris is, however, less extreme than in
other members of the subgroup. Haplochromis macrognathus (Text-figs 57 and 59 ;
Greenwood, 1962) is an extreme development of the subgroup morphotype (and
superficially resembles H. mandibularis of the ‘prognathus’ subgroup [see p. 89
above] but the head is narrower and the lower jaw is longer and more prognathous).

Neurocranial shape for the ‘estor’ subgroup is seen in Text-figs 57 and 69(2).

The fourth subgroup of the ‘prognathus’ lineage comprises a single species, H.
avgenteus (Text-fig. 61 ; Greenwood, 1967). This species, superficially, resembles H.
longirostris (see above), but has a neurocranial form that is more anteriorly protracted
than in any species of the ‘estor’ subgroup (Text-figs 62 and 69(3)).. This elongation,
unlike that in the ‘estor’ subgroup skull, involves relative protraction of the ethmo-
vomerine region as well as the region of the skull between the prefrontals and the
prootic.

_ Fic. 62. Neurocranial form in H. dentex (left) and H. argenteus, two piscivorous predators
of the H. prognathus lineage. (Scale = 3 mm.)

92 P. H. GREENWOOD

The relationship of H. argenteus to the ‘estor’ species is undoubted, and its place-
ment as a separate subgroup is only justified because of the unusual involvement of
the ethmo-vomerine region in skull elongation.

Finally in this lineage there is the bispecific subgroup of H. dentex and H. bayonm
(see p. 89 above), characterized by the fairly sharp decurvature of the ethmo-
vomerine skull region (Text-figs 62 and 69(3)). This deviation from the typical
skull form of the ‘prognathus’ lineage is reflected in the almost horizontal alignment
of the mouth in both species compared with the variously oblique jaws in other
members (cf Text-figs 63 and 59-61). Besides this shared similarity in jaw align-
ment, both species are unusual in having relatively few (modal number 36-40) and
larger outer jaw teeth. Judging from their overall neurocranial morphology, H.
dentex and H. bayom appear to be linked with the ‘estor’ subgroup (see p. 91 above).

Fic. 63. Haplochromis dentex. (About half natural size.)

Four species, H. dichrourous, H. apogonoides, H. orthostoma and H. parorthostoma
(Greenwood, 1967), have not so far been mentioned in this analysis, mainly because
there is little information available on their cranial anatomy.

Haplochromis dichrourous is known to be piscivorous, but nothing is known about
the diet of the three other species. The strong unicuspid teeth and large gape of
H. apogonoides suggest that it may be a piscivore, as do the near vertical orientation
of the jaws and the large gape in H. orthostoma and H. parorthostoma (Text-fig. 64).

Skull and jaw morphology in H. apogonordes is typically that of a generalized H.
macrops-like species, although the stout, strongly recurved and unicuspid teeth
resemble those of H. sauvagei (see pp. 69-70 ; also Greenwood, 1967). Since the skull
form of H. apogonoides is not like that of the ‘sauvager’ group species (p. 70), and
because its teeth could be interpreted as stouter versions of the kind found in ZH.

squamulatus, the relationships of the species are probably with the latter group (see —

p. 85 above) and not, as I suggested previously, with the ‘sauvage’ group (Green-
wood, 1967).

From the little evidence available (radiographs, partial dissection and overall
morphology) Haplochromis dichrourous could well be a member of the ‘prognathus’
lineage, probably of the ‘pavaguiarts’ subgroup (p. 89 above).

Radiographs of H. orthostoma and H. parorthostoma indicate a neurocranium of
the H. serranus-type. Tentatively the species can be considered a derived offshoot
of the ‘serranus’ lineage (see p. 84 above). Certainly each is more closely related

EVOLUTION OF A CICHLID SPECIES FLOCK 93

Fic. 64. Haplochromis parorthostoma.

to the other than to any other extant species. Haplochromis parorthostoma is known
only from Lake Victoria, while its sister species, H. orthostoma, is confined to the
Lake Kioga system.

To summarize this attempted phylogenetical survey of the piscivorous predators
(Text-figs 65-70) we may note that, like other trophic groups, it is composed of
more than one lineage. However, unlike the other groups, there seems to have been
a greater phyletic evolution within the main piscivore lineage. One lineage (the
H. guiarti-H. squamulatus line) may stem directly from a generalized insectivore of
the ‘pallidus’ type (see pp. 58-59). The other main lineage comprises two sister
groups (the ‘sevranus’ and ‘prognathus’ lineages) and seems to stem from an H.
saxicola-like ancestor. The ‘prognathus’ lineage is divisible into a number of sub-
groups probably of phyletic origin. No piscivorous lineage can be traced with
certainty to an ancestor with H. empodisma-like affinities (see p. 63 above), although
the possibility of the ‘serrvanus’ group having such affinities cannot be ruled out
(Text-fig. 70).

Conclusion

To close this discussion on the possible phyletic history of the Lake Victoria
species flock, I would return briefly to the question of its mono- or oligophyletic
origin, and also touch on the question of evolution above the species level in this and
other species flocks.

In most trophic radiations (the paedophages [p. 75], lepidophages [p. 69], and
possibly the piscivores [p. 80], excepted) the various member species seem referable
to one of three lineages. The basic morphotypes of these lineages are represented
today by the species H. pallidus (or H. macrops), H. empodisma and H. saxicola. All
are insectivores, and the two latter species (with their close relatives) each represent
a stage in the evolution of syncranial architecture from that of the presumed basic

H. bloyets type (see pp. 58-59).

94

P. H. GREENWOOD

H. empodisma H. obtusidens H. erythrocephalus

Fics. 65-69. Neurocranial form in representative members of the principal lineages shown
in the phyletic diagram (Text-fig. 70). (In all, scale = 3 mm.)
In this figure: 1. H. bloyeti and a member of the H. macrops line.
2. The H. phytophagus—H. obliquidens lineage.
3. The H. pallidus—H. pharyngomylus lineage.
4. The H. erythrocephalus—H. obtusidens lineage.

EVOLUTION OF A CICHLID SPECIES FLOCK 95

Species with syncrania of the H. empodisma and H. saxicola types are not found
in the present-day east African river systems, whereas the H. pallidus type is well
represented. In the absence of early Pleistocene Haplochromis fossils it is impossible
to tell whether this situation also obtained in the rivers of that period, or whether
the ‘empodisma’ and ‘saxicola’ skull types were then represented among fluviatile
species.

Syncranial differences between A. bloyeti, H. pallidus and H. empodisma are, in
fact, very slight (see Text-figs 31, 32 and 65). Conceivably, one of the earliest

H. chilotes

H. prodromus H. xenognathus

M. bicolor
Fic. 66. The H. chilotes-Macropleurodus bicolor lineage.

96 P. H. GREENWOOD

dichotomies from an H. bloyeti-like stem species within the developing lake could
have given rise to the H. pallidus and H. empodisma-like types. From this point a
very slight differentiation of the H. pallidus skull type would give rise to the H.
macrops type (see p. 59 and cf Text-figs 65(1) and (3)), and a somewhat greater
change (but still only one of differential growth ; see p. 63) would produce, from the
H. empodisma-like stem, a syncranium of the H. saxicola type (cf Text-figs 65(4) and
68(2)).

H. guiarti H. squamulatus H. martini

H. maxillaris
H. obesus

Fig. 67. 1. The H. cinereus—H. squamulatus lineage.
2. The H. cronus—H. melanopterus lineage.

Although a complete phyletic analysis of the flock cannot yet be made, it seems

unlikely that additional material will alter substantially the scheme given in Text-

fig. 70. Species still to be described will increase the number of terminal points ©

categorized as a ‘species complex’ (or increase the number of species in those already
recognized). They are unlikely to provide new lineages.

Even this partial phyletic analysis of the flock shows that, despite the superficial
impression of virtually complete morphological and adaptational intergradation
amongst its species, a number of distinct groups are discernible. For example there

EVOLUTION OF A CICHLID SPECIES FLOCK 97

H. paraguiarti

Fic. 68.

BwWN H

H. flavipinnis H. altigenis

The H. barbarae—H. parvidens lineage.

The H. riponianus—H. welcommei lineage.

The H. serranus lineage.

The H. prognathus lineage ; the H. paraguiarti subgroup.

98 P. H. GREENWOOD

H. dentex H. argenteus

Fig. 69. The H. prognathus lineage continued.
1. The H. prognathus subgroup.
2. The H. estoy subgroup.
3. The H. dentex subgroup (left) and the H. argenteus sub-
group (right).

are the H. pallidus—H. pharyngomylus, H. nuchisquamulatus—H. lividus, H. cinereus—
H. squamulatus, H. sauvagei—H. chromogynos, H. cronus-H. melanopterus and H.
barbarae-H. parvidens groups, and the H. serranus and H. prognathus species com-
plexes.

Each lineage is definable on the basis of certain shared morphological specializations
and, on the whole, each is recognizable from its trophic peculiarities (see Text-fig.
7). The distinguishing characters would be sharpened if the least specialized mem- |
bers of the groups had been eliminated in the past (as may have happened in the
history of Hoplotilapia and Platytaemodus). In other words, we seem to have
species aggregates which might be accorded higher rank.

That the origin and evolution of higher categories involve processes no different
from those involved in speciation is now generally accepted. The real problem in
this particular situation is to find some satisfactory definition of the genus, a definition
that is not purely a pragmatic one like that which Mayr (1969) proposes. The size
of the morphological gap (Mayr’s criterion) separating two taxa does not necessarily

EVOLUTION“OF A. CICHLID. SPECIES: FLOCK 99

indicate the degree of their phyletic divergence (for example, take Macropleurodus
bicolor ; see p. 71 and Text-fig. 75).

That a genus must be monophyletic is self-evident, but the points where ‘generic’
lines are to be drawn are by no means evident in the case of a species flock. For
example, when discussing this problem with my colleagues, one suggested that a
genus should comprise, at most, the two apomorph and the two plesiomorph sister
species arising from three dichotomies. This definition could not be applied to a
situation where there was multiple synchronous speciation from a common ancestral
species isolated in several places (as may well have happened in the evolution of the
Victoria species flocks ; see pp. 108-114). In other words, at an early stage in the
evolution of this flock each of several populations from the same ancestral species
could have given rise to very differently specialized lineages. Polychotomous
rather than dichotomous branching could be basic to the evolutionary history of this
and other lacustrine cichlid species flocks. Similar branching patterns could also
have occurred within a lineage, thereby giving rise to the clusters of very similar
species at any one level of apomorphy or plesiomorphy.

Because for the moment I see no solution to this ‘generic problem’, the various
lineages indicated in Text-fig. 70 are left within a single but almost certainly artificial
genus.

A large question mark also hangs over the phyletic relationship of the Lake
Victoria Haplochromis species with those of Lake Malawi. The generalized species
in both lakes are alike in all anatomical features, and of greater import, both flocks
have species with identical specializations. Although this would seem strongly to
indicate close similarity in the genotypes of their ancestral species, it cannot be
established if these taxa were conspecific. Further arguments against the ancestors
being conspecific are the greater age of Lake Malawi (see p. 6), and the occurrence
in Lake Malawi Haplochromis of certain colour patterns and types of squamation
not seen.in any Lake Victoria species (p. 20). On a truly phyletic basis, thereiore,
it is problably wrong to place any of the Lake Malawi species in the same genus (or
genera) as those from Lake Victoria.

Both these ‘generic’ problems are under investigation, as are the inter- and intra-
relationships of the Lake Tanganyika Cichlidae.

THE RELATIONSHIPS OF THE MONOTYPIC GENERA

The five monotypic genera, Astatoreochromis alluaudi (Greenwood, 1959a), Hoplo-
tilapia retrodens, Platytaeniodus degent, Macropleurodus bicolor and Paralabidochromis
victoriae (see Greenwood, 1956a) are all clearly derived from Haplochromis ancestors.
Except for Macropleurodus bicolor and Astatoreochromis alluaudt, however, it has so
far proved impossible to suggest with which extant Haplochromis species these
genera show the closest affinities.

The relationship of Macropleurodus bicolor (Text-fig. 3) with the H. sauvager group
of mollusc eaters is discussed on p. 71.

Arguments are presented elsewhere (Greenwood, 1954, 1959a; also see p. 18
above) that Astatoreochromis alluaudi originated from a stem distinct from that of
all other Lake Victoria haplochromine species. Apparently the nearest living

100 P. H. GREENWOOD

Fic. 70. A tentative phylogenetic arrangement of the Lake Victoria Haplochromis species
flock based on the assumed synapomorphy of various character states (particularly
those of the neurocranium and the dentition) ; see text pp. 57-99. Although each
lineage (except the H. macrops complex) is recognized on the basis of specialized characters
shared by its constituent species, no shared specializations have yet been found that will
enable one to link, dichotomously, the different lineages to a common ancestral species.
That is to say, the basal members of a particular lineage show only specializations inter- |
relating them with members of that particular lineage ; in other respects they are at a
generalized (plesiomorph) level of organization. Each could have been derived (and
derived synchronously) from an H. bloyeti-like ancestor (see text, pp. 57-58).

It has also proved impossible to interrelate constituent species of the H. macrops, H.
sevvanus, H. tridens and H. prognathus complexes. In the three latter groups all species
show an equally derived level of organization, while in the H. macrops complex the species
are so generalized that synapomorphies are not detectable (and thus the association
may not constitute a truly phyletic assemblage).

Fic. 71. Platytaeniodus degen.

relative of A. alluaudi is a small, mollusc-crushing species Haplochromis vanderhorstt
from the Malagarasi river system of Tanzania (Greenwood, 1954) ; it differs from
A statoreochromis alluaudi mainly in having the typical Haplochromis number of anal
fin spines (3), rather than the elevated number found in Astatoreochromis, viz 4-6.

As there is but one specimen of Paralabidochromts victoriae available for study |

(Greenwood, 1956a) only superficial characters can be used to assess its relationships.
The peculiar, procumbent, elongate and unicuspid teeth of this species, coupled

with its narrow dental arcade, seem to imply relationship with Haplochromis

chilotes, a specialized and insectivorous member of the H. sauvagei lineage (see p. 61
above). This conclusion cannot, however, be tested until osteological material
becomes available for comparison.

For Hoplotilapia retrodens and Platytaeniodus degeni (Text-figs 71 and 72), despite
adequate study material, it is impossible to suggest any living species or species

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EVOLUTION OF A CICHLID SPECIES FLOCK

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Fic. 72. Hopblotilapia retrodens.

Fic. 73. Platytaeniodus degeni. A: Lower jaw in occlusal view. B: Dental pattern
of the premaxilla ; in larger individuals the posterior part of tooth band on each side is
expanded medially. (Scale = 3 mm.)

302 P. H. GREENWOOD

lige j

Adana

Fic. 74. Hoplotilapia vetvodens. Lower jaw in lateral (A) and occlusal (B) views.
(Scale = 3 mum-)

Fic. 75. Macropleurodus bicolor. Left premaxilla, occlusal view seen from above and
medially. A: From a large fish (a male, 115 mm standard length), in which the minor
cusp is absent from all teeth. B: A smaller individual (a female, 88 mm S.L.) showing
the prominent minor cusp. (Scale = I mm.)

EVOLUTION OF A CICHLID SPECIES FLOCK 103

group as the nearest relative. An earlier view (Greenwood, 1956a) that both taxa
are related to the H. crassilabris species complex of Lake Victoria can no longer be
substantiated on either dental or neurocranial similarities. Hoplotilapia and Platy-
taeniodus have, as their diagnostic features, a great widening of the tooth bands in
both the dentary and the premaxilla (Text-figs 73 and 74), combined with a tendency
for teeth of the inner rows to be as large as those in the outer row. Although
premaxillary shape and tooth arrangement is basically similar in both genera
(particularly in small individuals ; see Greenwood, 1956a) the shape of the dentary
and its tooth bands are markedly different (cf Text-figs 73 and 74). In H. retrodens
the dentary is flattened and the broad bands of teeth extend posteriorly onto the
ascending coronoid process (a feature not encountered in any other Lake Victoria
haplochromine). In P. degenz the bone is deep and stout anteriorly, and the multi-
seriate teeth are virtually confined to its anterior third. Tooth shape also differs
intergenerically ; in P. degen the crowns of the unicuspid teeth are flattened and
resemble those of a typical bicuspid, whereas in H. rvetrodens the teeth, also unicuspid
in adults, are conical and recurved.

Neurocranial form is identical in Hoplotilapia and Platyiaeniodus (Text-fig. 76) and
approaches the generalized H. macrops type. But no member of the macrops—
pallidus lineage (see p. 58) shows even an incipient development of the dental
features characterizing either genus. This absence of anatomically annectent species
is, as will be recalled, an outstanding feature in this species flock where all other
structural grades are completely bridged by intermediate forms.

Now that more is known about the anatomy and ecology of the whole flock, my
original interpretation (Greenwood, 1956a) of the monotypic genera as being the
results of quantum evolution (sensu Simpson, 1953) hardly seems tenable. There
are numerous examples within the flock of species that, trophically and morphologi-
cally, occupy intermediate positions with respect to different adaptive (i.e. trophic)
zones, and there are several species in the mollusc-eating grade to which Hoplotilapia
and Platytaeniodus belong. In other words, these genera do not occupy a niche or
adaptive grade unoccupied by a close relative, one of the features characterizing
quantum evolution. Nor, with respect to the absence of morphological inter-
mediates, is it clear why those linking Platytaemiodus and Hoplotilapia should have
been any more ill-adapted (and therefore rapidly exterminated) than those annectent
forms still surviving in other lineages.

The morphological isolation of at least these two monotypic genera remains a
mystery (with undertones, almost, of Goldschmidtian ‘macromutations’ and ‘hope-
ful monsters’). The generic status of Macropleurodus and Paralabidochromis is, |
now think, questionable.

THE ANATOMICAL BASIS FOR THE ADAPTIVE RADIATION
It is chiefly in their cranial anatomy that one sees the results of the adaptive
radiation undergone by the Lake Victoria Haplochromis species during the last
three-quarter million years.
Some of the interspecific differences seem profound. Yet, on careful examination
the different characteristics are found to be relatively simple variants of a basic

104 P. H. GREENWOOD

Hoplotilapia retrodens

Platytaeniodus degeni

Macropleurodus bicolor

Fic. 76. Neurocranial shape in three endemic monotypic genera. (Scale = 3 mm.)

bauplan. The relative simplicity of these morphological changes, coupled with the
basic anatomical level already reached by the ancestral lake cichlids, has, I believe,
given the haplochromine fishes a great ‘morpho-potential’ with which to meet the
environmental opportunities provided in a developing lake (Greenwood, 1973b).

Alexander (1967) first drew attention to certain peculiarities in the jaw mechanism
of a South American cichlid, Pterophyllum. Subsequently I have been able to show
that this specialized type of jaw mechanism occurs in all the Lake Victoria Haplo-
chromis species I have dissected (i.e. the majority of species, including most mono-
typic genera).

These specializations concern functional interrelationships of the premaxillae and
maxillae, the effect of which is to allow greater protrusion of the upper jaw, and firmer
fixing of that jaw in the protruded position (see Text-fig. 77). As aresult, the lower
jaw can be closed firmly against the upper jaw whilst the latter is still protruded.
The advantages of this system are discussed in detail by Alexander (1967). They
are further exemplified by the exploitation of this system in some groups of mollusc

EVOLUTION OF A CICHLID SPECIES FLOCK 105

eaters (the shell-wrenchers, p. 69), a type of feeding habit that could hardly evolve
without the cichlid-type of protrusion mechanism. Its advantages are also seen
variously exploited in other benthic feeders, and again in the great piscivorous
predator radiation (including, particularly, the paedophagous species ;_ p. 75 ef seq.).
Indeed, the functional flexibility of the cichlid type of jaw mechanism is probably
one of the prime factors leading to the evolutionary success of these fishes.

With few exceptions (e.g. the monotypic genera [Text-figs 73-75] and some of
the paedophages [Text-fig. 46, and p. 77]) there is relatively little variation in the
shape of the jaw bones. In the molluscivores that crush snail shells orally, or wrench
the body from its shell, the dentary (Text-figs 40 and 41) is noticeably shorter and

ROS CART ROS CART

ART MAX 22

ASP PMX
ART MAX

iL __ asp pmx

A

PAL

3mm

Fic. 77. View, from a dorsolateral position, of the right upper jaw in: Perca fluviatilis
(Right) and : Haplochromis brownae (Left). The associated ligaments and other connec-
tive tissues, and the cartilaginous menisci between the various elements are omitted.
The rostral cartilage, however, is shown in situ.

In Perca, the articular process of the maxilla (ART MAX) is in direct contact with the
dorsal and dorsomedial aspect of the premaxillary articular process (ART PMX) through
a cartilaginous meniscus, and also partly overlaps the posterolateral face of the same
process. Additional contact between the articular process of the maxilla and the pre-
maxilla is brought about through its contacting the rostral cartilage (ROS CART) under-
lying the ascending process of the premaxilla (ASP PMX). As a result of these
contacts, protrusion of the premaxilla is at least partly effected through the rotation
of the maxilla (see Alexander, 1967, and also Liem, 1970). In Haplochromis (all species
examined, see p. 104) the articular process of the maxilla only contacts the premaxilla
at one point, through a cartilaginous meniscus with the ventrolateral face of the pre-
maxillary ascending process (i.e. anterior to the rostral cartilage). Unlike Perca there
is neither contact with the articular process of the premaxilla (ART PMX) nor with the
rostral cartilage.

Protrusion of the premaxilla thus seems to be effected mainly through the sinking of the
lower jaw, to which the premaxilla is linked by the connective tissue of the lips. When the
premaxilla is fully protruded, the articular process of the maxilla (ART MAX) does,
however, contact the upper part of the premaxillary articular process. In this way it
helps in holding the upper jaw in the protruded position even when the lower jaw is
raised (see text p. 107).

106 P. H. GREENWOOD

the premaxillae somewhat stouter than in other species. - In certain lineages
(especially those adapted for preying on other fishes) the jaws may be relatively
longer, as may the ascending processes of the premaxillae, but the overall ae
of these bones shows little change (cf Text-figs 31 and 57).

Liem (1970) has demonstrated the importance of a high ‘coronoid’ process on the
dentary for increasing the speed at which both the j jaws can be closed. In all the |
Lake Victoria Haplochromis species examined (and in the generalized Z. bloyett)
the coronoid process could be classed as ‘high’. It is relatively a little higher in
certain species, particularly among the advanced piscivores and in both lineages of
paedophages. In many of these species (and particularly among the piscivorous
predators) the lower jaw is relatively longer and the upper jaw markedly protrusile,
a combination of characters enhancing the grasping range and rate of the jaws, and
increasing the volume of the buccopharyngeal cavity (Liem, of. cit.).

In general, however, it could be said that jaw form is relatively constant through-
out the flock; what interspecific differences there are can, in most instances, be
attributed to the results of allometric growth changes.

The high coronoid process of all Haplochromis species can be considered as one of
the basic features contributing to the success of the Haflochromis-bauplan as raw
material for an adaptive trophic radiation.

Basically, only two types of outer jaw teeth occur throughout the Lake Victoria
species flock (see Text-fig. 4), namely, teeth with bi- or unicuspid crowns. The
great variety of bicuspid crowns, including the extremes in shape and development
of one cusp found in algal grazing species (Text-figs 4D-—G), are simply the products
of relative growth, as is the degree to which the tooth neck is curved inwards or
even outwards (Text-figs 4, 33 and 46).

Except in their degree of curvature, unicuspid teeth show little variation in shape.
Unicuspid teeth are usually taken as the mark of a piscivorous predator, and their
adaptive significance in this group is self-evident. However, an analysis of tooth
form in all species shows, with few exceptions, that the presence and relative
abundance of unicuspid teeth is generally a correlate of the fish’s size. In other
words, individuals in all species have bicuspid teeth until a length of ca 80-90 mm
is reached; above that length there is a size range (80-110 mm) in which the
dentition is a mixture of bi- and unicuspids. This is followed by a wholely uni-
cuspid dentition in larger individuals. Since the maximum size attained by fishes
in the majority of non-piscivorous species is rarely greater than 100 mm, it follows
that the dentition in these species is generally a bicuspid one.

The only exceptions I can find to this generalization are the algal grazing species
(see pp. 63-66) where, as might be expected, the specialized bicuspid tooth (Text-figs
4D-G and 36) is retained even in the largest fishes (although individuals larger than
95mm are rare). Also exceptional are the very few piscivorous species where
unicuspid teeth predominate in fishes less than 80 mm long, irrespective of the maxi-
mum adult size attained (be it more or less than 100 mm).

Thus, generally speaking, in the evolution of piscivorous fishes an increase in adult
size would have the double adaptational value of providing a unicuspid dentition
and an increase in speed (since larger fishes swim faster than smaller ones). Clearly,

EVOLUTION: OF A: CICHLID SPECIES. FLOCK 107

some piscivores have succeeded in breaking away from this size-correlated change in
dental form, as witnessed by the few exceptional species mentioned above, but this
is unusual.

Inner row jaw teeth show less variation in shape than do those of the outer row.
The main differentiation here is in the disposition of the teeth ; that is, a relative
increase or decrease in the number of tooth rows and the area over which the widen-
ing of a tooth band is manifest. Obvious functional correlation with increased width
of inner tooth bands is seen in the algal grazers (p. 65), some mollusc eaters (p. 71 ;
Text-fig. 41) and in the scale-eating H. welcommez (p. 69 ; Text-fig. 39).

The pharyngeal bones and dentition show considerable variation in form (see
Text-figs 5 and 30). Here again the changes involved are simple ones concerning,
chiefly, an increase in the stoutness and robustness of the lower pharyngeal bone
and a differentiation of its dentition. The upper pharyngeal bones show a cor-
related change, but usually the changes are less marked.

The principal pharyngeal dental changes involve either the replacement of com-
pressed, bicuspid teeth by flat-crowned, stout teeth, or a coarsening or refining of the
teeth without a change in their basic bicuspid form. The change from a laterally
compressed pharyngeal tooth to a molariform one would seem to be greater than any
seen in the oral dentition (see above). Furthermore it is not simply correlated with
the fish’s size, as is the change from bi- to unicuspid jaw teeth (although the degree
of molarization in a pharyngeal dentition is often positively correlated with the
fish’s length). Strengthening of the pharyngeal bones is, in general, correlated with
the change from a basic bicuspid dentition to one in which molariform teeth are
present. Other variants in the pharyngeal mill pattern involve the shape of the
dentigerous area on the lower bone (always basically triangular, however), and the
spacing of the pharyngeal teeth on it.

Changes in neurocranial form have been described and figured in the preceding
chapter. (pp. 93-99; Text-figs 65-69). Their importance in trophic adaptation
is seen especially in the ethmo-vomerine region, the base on which the upper jaw
moves and is supported. Thus it is not surprising that changes in the shape and
relative proportions in this region of the skull are so obvious in this Haplochromis
flock. Through alteration to the angle at which the ethmo-vomerine region slopes,
changes are effected in the striking angle of the upper jaw during protrusion ; relative
changes in ethmo-vomerine length influence the degree to which the premaxilla
can be protruded whilst still retaining a firm foundation, and it is this region of the
skull that plays an important role in allowing the lower jaw to bite hard against a
still protruded upper jaw (see p. 105 above). The involvement of all these different
factors can be seen, individually or in combination, in the skull forms of various
Haplochromts species. .

In the ‘sauvagei’ radiation of mollusc eaters (pp. 69-72) we clearly see all three
factors involved. The steep ethmo-vomerine slope (Text-figs 40 and 66) induces a
downward as well as the usual forward protrusion of the upper jaw. This region
of the skull is relatively elongate so that the ascending processes of the premaxillae
are strongly supported at all stages of protrusion. Finally, the lower jaw can shut
quickly and firmly against the upper jaw whilst it is still protruded, thus allowing the

108 P. H. GREENWOOD

fish to hold the snail shell firmly whilst it either wrenches the shell away from the
body oi crushes it between the upper and lower jaws.

The morphological changes that have allowed the development of this particular
feeding habit represent simple alterations in the growth pattern of a generalized
(i.e. H. macrops-like) syncranial type, and are especially obvious in the neurocranium
(cf Text-fig. 65(1) with Text-fig. 66). 3

Relative growth changes in parts of the neurocranium are particularly well illus-
trated in the ‘frognathus’ lineage of the piscivore radiation (see pp. 85-92). Here
the changes involve a relative lengthening of the entire preotic skull region,* a
decrease in the height of the neurocranium and, as a consequence, a marked decrease
in the angle at which the preorbital face of the skull slopes downwards (cf Text-fig.
68(4) with Text-fig. 69(1-3)). In turn, this gentler slope of the path over which the
premaxillary processes slide results in a different orientation of the toothed pre-
maxillary arms as compared to the situation in a generalized skull. The ascending
processes and the toothed arms of the premaxillae meet at almost a right angle in all
species ; consequently in fishes with the skull shape under consideration, the denti-
gerous arms, relative to those in a generalized syncranium, lie at a steeper angle to
the horizontal (because the ascending processes lie more nearly horizontally on the
flatter ethmo-vomerine region). Correlated changes in the relative length of the
lower jaw (inevitable if the system is to remain functionally integrated) result in a
larger gape than is possible in fishes with a generalized neurocranial shape. Further-
more, the gape is directed forward and horizontally (advantageous in a hunter) and
not obliquely downwards as in a generalized syncranium (a condition, nevertheless,
suited to benthic feeding habits). Possibly the chief gain of the former mouth type
to a predator is in being able to take prey at the same level as the fish’s line of forward
progress, rather than by having to align its body away from the horizontal in order
to bring the gape into that plane.

The cichlid type of premaxillary—maxillary relationships (see Text-fig. 77 ; also
Alexander, 1967), enabling the fish to brace the protruded premaxillae and to raise
its lower jaw with the upper jaw fully protruded, seems to be of particular significance
in the piscivore radiation. First, it allows a slightly greater protrusion of the
upper jaw than does the basic percoid arrangement (Alexander, 1967) and thus an
increase in the volume of the orobranchial cavity. Second, it allows the prey to be
firmly gripped between the jaws without a marked decrease in the orobranchial
volume (as would happen if the upper jaw has to be retracted before the lower jaw
closed on it). This latter characteristic is of particular importance because cichlids
do not swallow their prey whole. Instead, the body of the prey is gradually rasped
away by the pharyngeal mill posteriorly while the rest is held by the jaws and oro-
branchial cavity.

Theoretically, this combination of pharyngeal mastication, firm jaw grip and in-
creased expansion of the orobranchial cavity would permit the capture and ingestion
of larger prey than would be possible if ingestion was simply by swallowing the prey

* i.e. The skull from the anterior tip of the vomer to the anterior margin of the prootic, and thus
including the frontals and the parasphenoid.

' EVOLUTION OF A CICHLID SPECIES FLOCK 109

whole. Unfortunately this idea cannot be tested because no figures are available
for the relative differences in prey sizes of cichlids and species bolting their prey
without pharyngeal mastication. However, subjective appraisal certainly suggests
that the cichlids do eat relatively much larger prey than does, say, the catfish
Clarias mossambicus, although the latter will probably consume more individuals
per unit feeding time (personal observations).

To return to the modifications in neurocranial form seen in piscivorous Hapflo-
chromis. As was the case in the molluscivorous ‘sawvagei’ radiation (see above), the
alterations in relative skull proportions are a reflection of differential growth changes.
Correlated modifications in jaw size and in proportions of the suspensorium are also
due to changes in relative growth. Growth related changes are also seen in the
increased streamlining of body form and head shape (Text-fig. 3) and, more directly,
the increased body size. Many changes are, of course, allometrically correlated
with this increased overall size and so too is the shift from a bicuspid to a unicuspid
oral dentition (see p. 106 above). |

Apparently without exception then, the underlying morphological principal
involved in the evolution of this trophically complex and morphologically varied
species flock is one of differential growth in various elements of the syncranium.
Included in this generalization are, of course, the muscular as well as the bony
components. Less work has been done on the cranial musculature than on the
skeleton of these fishes. The observations I have made suggest that throughout the
flock the chief myological differences are also proportional ones, coupled with slight
differences in the insertion points of certain muscles, especially the adductor mandi-
bulae series.

As far as I can tell from published accounts (and from limited personal experience)
the same generalizations can be made about the osteology and myology of the Cichli-
dae from Lakes Malawi and Tanganyika. Certainly they apply to those of Lakes
Edward, George and Albert. In Lakes Malawi and Tanganyika some species
(generally referred to genera other than Haplochromis) do exhibit a more profound
change in the form of the outer, less frequently the inner, jaw teeth (compare Text-
fig. 4 with text-figs 28 and 29 in Fryer & Iles, 1972). Nevertheless, the derivation
of these teeth from a basic bi-, tri- or unicuspid type is evident and of the same nature
as that seen in the Lake Victoria species.

The importance of changed habits and behaviour in the origin of new adaptive
trends is rightly emphasized by Fryer & Iles (1972 : 207 and 486). But their state-

ments that these ‘produce . . . changes in function which themselves lead to changes
in structure ...’, and again ‘. . . differences in habits and behaviour can precede and
initiate morphological differences . . .’ are, to say the least, equivocal. Possibly

they had in mind the example provided by A statoreochromis alluaudt where differences
in diet have pronounced effects on the degree to which certain specialized characters
are developed (Greenwood, 1959a, 1965c). Fishes deprived of their usual diet of
gastropods, or those feeding on snails with thin shells, have less well-developed
pharyngeal bones, fewer molariform pharyngeal teeth, and a much reduced apophy-
sis for the upper pharyngeal bones on the skull base. Yet, despite their reduced
state, all three specialized characters are present and are recognizable as such.

110 PP? oH: GREENWOOD

Many Haplochromis species in Lake Victoria are facultative and opportunistic
feeders (personal observations). During the early stages of the flock’s evolution
this ability could have had important survival value in isolated populations. Such
behaviour might include incipient trophic specialization in an otherwise generalized
feeder and thereby lay the foundation for the selection of specialized anatomical
features. But apart from Astatoreochromis alluaudt nowhere amongst the Lake.
Victoria Haflochromis have I found evidence of unequivocal phenotypic modifi-
cation in response to an environmental influence.

The evidence from Astatoreochromts alluaud1, however, strongly suggests that the
supposedly ‘reduced’ condition found in ‘atypical’ populations may represent the
full extent of genetical control over the development of these specialized characters.
The condition in other populations (the ‘typical’ ones) would then be an environ-
mentally influenced hypertrophy of the genetically controlled condition. The
reason for reaching this conclusion is the appearance, in a few generations, of the
‘reduced’ characters in an aquarium population descended from parents showing
full hypertrophy of these features (Greenwood, 1965c).

A contradictory situation is found in H. ishmaeli of Lake Victoria and a very
closely related species, H. mylodon, of Lakes Edward and George (Greenwood,
1973a). In Lake Victoria H. ishmaels feeds mainly on the hard-shelled gastropod
Melanoides tuberculata (also the food of Astatoreochromis alluaudi). In Lakes
Edward and George, H. mylodon feeds on both insects and molluscs, the latter thin
shelled and usually of genera other than Melanoides (Greenwood, 1973a). Yet, the
pharyngeal bones and skull apophysis in the two species show the same degree of
hypertrophy. Here it would seem that the major factor controlling development of
the specialized characters is a genetical one.

Even though we are far from an understanding of the epigenetical mechanisms
influencing ontogeny, the results of these processes, as argued above, are interpretable
in terms of changes in relative growth. Taken in conjunction with the basic syn-
cranial and dental characters of a generalized haplochromine cichlid, this relatively
simple mechanism could explain, in large part, the evolutionary success of these
fishes in the African lakes (see also p. 111). It could also explain the rapidity with
which the Cichlidae have been able to produce the adaptive modifications underlying
their ecological dominance in the fish faunas of these lakes.

Another factor that may have contributed to rapid adaptive radiation in the
changing environments of a developing lake is the nature of the dental modifications,
both oral and pharyngeal.

Judging from the ‘intermediate’ morphology still preserved in species of some
lineages (especially the mollusc crushers, the periphyton grazers and the mollusc
shellers) the change from a generalized tooth form could have immediate or almost
immediate selective value. It would not, therefore, have to undergo any (or much)
modification before reaching a preadaptive stage with respect to its new function.
In other words, selection forces acting on it would be essentially postadaptive
rather than the usual succession of pre- and postadaptive ones (see Bock, 1959).

The outstanding explosive radiations of cichlid fishes (particularly haplochromine
species) in developing lakes may well be consequent upon there being an abundance

EVOLEUIIONCOE. A “CICHETD SPECIES FLOCK 111

of selection forces for new structures (as compared with the pre-existing and stabilized
river situation) and the likelihood that slight morphological changes (in, of course,
the right synanatomical context) are sufficiently preadaptive for these forces to
become immediately effective.

In essence, the success of the haplochromine cichlids seems attributable to their
fluviatile ancestors having reached a level of general specialization which could be
further developed and differentiated by simple ontogenetic reorganization. Ana-
tomically the other fishes were either too specialized (e.g. the catfishes, the Cyprini-
dae, Mormyridae, Characidae and Cyprinodontidae) or not sufficiently specialized
(e.g. Centropomidae) for this sort of anatomical change to be effective or even
possible.

None will deny that, anatomically, these other families have undergone con-
siderable evolution, in some cases more profound than that seen in the Cichlidae as a
whole (the characids and mormyrids are spectacular examples). But this differentia-
tion is of longer standing than that of the lake Cichlidae (witness the wide geo-
graphical distribution of these other species over much of Africa). Also this past
differentiation has resulted in specializations that are inhibiting in terms of multiple
adaptive radiation. The specialized dentition and jaws of the characids, the jaws
of mormyrids, the edentulous but kinetically specialized jaws of the cyprinids and
the specialized jaws of the cyprinodonts are all examples of a restriction in adaptive
potential. Other inhibiting factors (especially breeding habits, see p. 12) were certain-
ly operative in further restricting the evolution of these fishes in a lake environment.

In contrast, the syncranial characteristics of the Centropomidae (e.g. Lates and
Luctiolates species), although of a percoid grade, are in general far less specialized
than those of a generalized Haplochromis species ; the jaw mechanism (see Alexander,
1967) is a particular case in point. Further, the syncranial organization in centro-
pomids is a less suitable basis for the type of relative growth changes that have been
so successful in the Haplochromis morphotype. Neither is the multiserial, microdont
type of oral dentition in centropomids such an effective starting point for dental
evolution as are the larger and fewer teeth of a haplochromine fish, and nor are the
smaller, medially separated lower pharyngeal bones of a Lates such a suitable basis
for the elaboration of a pharyngeal mill.

SPECIATION
All that has been discussed so far is proximately the product of one natural pro-
cess, speciation. A great deal has been written about the background to, and
mechanism of, speciation in African cichlid fishes. The subject is well reviewed by
Fryer & Iles (1972), to whom reference should be made, especially for their detailed
consideration of speciation in the cichlids of Lake Malawi.

Speciation involves two major but closely interrelated processes, genotype
reorganization and the development of inherent barriers to reproduction with the
mother species and related taxa. Genotypic reorganization requires that the popu-
lation undergoing speciation should be isolated from genetic interchange with the
stem species. It is this aspect of the problem that has received most attention in
African cichlids (see below).

112 P. H. GREENWOOD

Little direct information is available on the evolution and nature of the barriers
to interspecific crossing in these fishes. Whatever these barriers are, their effective-
ness in the Lake Victoria Haplochromis species flock is very obvious. Despite the
lack of definite and specific breeding seasons, and despite the close physical proximity
of breeding sites occupied simultaneously by several species, there is virtually no
evidence of interspecific hybridization (see p. 55). The effectiveness of these bar-_
riers is all the more remarkable when it is recalled that this flock of over 150 species
has evolved, within little more than three-quarters of a million years, from one or at
most afew closely related species. Clearly some, in genetical terms, simple mechanism
is involved.

The breeding behaviour of several cichlids (including a few Haplochromis species,
but unfortunately none from Lake Victoria) is now well known (Baerends & Baerends
van Roon, 1950; Wickler, 1962a and b, 1963, 1966). Compared to that in many
fishes it is complex, and in this complexity may lie a pointer to the ‘ease’ with which
barriers to interspecific crosses are evolved. In other words, a slight deviation from
an established pattern could provide an effective barrier to successful courtship and
mating. The deviation might involve either behavioural patterns in courtship, or a
specific recognition signal like male coloration (see p. 52). That there is no repeti-
tion of male coloration among the Haplochromis species of Lake Victoria points to
the probable importance of this character as a specific recognition signal. Un-
fortunately we have no information on the genetical basis of coloration in these
fishes nor on the mechanism whereby a female recognizes the male breeding colours
of her species. Since young fishes of both sexes have a similar female-type coloration,
and certainly are non-shoaling at an age when male breeding colours develop, it is
unlikely that any element of imprinting is involved. Presumably the ability to
recognize male conspecificity is inherent in females.

That differences in male breeding colours can evolve rapidly is well demonstrated
by the endemic Haplochromis species of Lake Nabugabo (Greenwood, 1965b). This
small lake was isolated from Lake Victoria by a sand spit formed some 3500 years
B.P. Of the six Haplochromis species now occurring in the lake, five are endemic,
but obviously related each to a species still living in Lake Victoria. Anatomically,
the Nabugabo species are little different from their Victoria sister species (Greenwood,
op. cit.). But, the differences in male coloration are very trenchant.

Since the Nabugabo species were derived from already fully differentiated Lake
Victoria taxa isolated in the newly formed lake, there can be no grounds for thinking
that the colour differences evolved in response to strong selection favouring charac-
ters that would prevent interspecific hybridization. In this respect the colour
differences would seem merely to be one product of the genic reorganization under-
gone by the isolates. The significant feature, however, is the appearance of this
character change in all but one of the isolated taxa, thus suggesting that, whatever
its genetic basis, it is likely to occur whenever a genotype is reorganized.

If the situation in Lake Nabugabo is a typical consequence of isolating segments of
a Haplochromis species, and if male coloration is of prime importance as a recognition
signal (and there is little evidence to negate these suppositions) then we have a clear-
cut example of the rapidity with which a Haplochromis species can originate.

EVOLUTION OF A-CICHEID, SPECIES FLOCK LES

Indeed, it seems that in these fishes speciation is an almost inevitable consequence of
isolation, at least in a lacustrine environment.

This correlation of speciation and a lacustrine environment may have a dual
basis. A lacustrine environment undoubtedly provides a greater number of spatially
distinct, often repeated, niches than does a fluviatile one. Habitat preference could
then lead to the isolation of populations, a situation which Fryer (1959 ; also Fryer
& Iles, 1972) considers of first importance in the speciation of Lake Malawi cichlids.
Secondly, a lake in its genesis is liable, through climatic or tectonic changes, to be
broken up into smaller water bodies, or to give rise to peripheral isolates (like Lake
Nabugabo). It is this type of background that I consider to have been involved in
the speciation of the Lake Victoria flock (Greenwood, 1965a).

Much of the literature on evolution and speciation in Lake Victoria Haplochromis
is concerned with the nature and origin of these primary isolating factors (see Regan,
1922; Worthington, 1937, 1954; Mayr, 1942, 1947; Brooks, 1950; Greenwood,
1951, 1959C, 1905a; Hubbs, 1961; Kendall, 1969 ; Temple, 1969 ; and review in
Bryer Iles, 1972).

Apart from Mayr (1947), who then argued for the flock’s origin by multiple coloni-
zation, the principal contention has been whether primary isolation was through
habitudinal factors or by physical isolation in distinct water bodies. Mayr (1963)
later acknowledged the unlikelihood of multiple colonization from rivers as a major
factor in the evolution of these lake faunas (not specifically mentioning Lake Vic-
toria amongst the examples he cites; Grant [1963] still cites the earlier Mayr
reference when dealing with the evolution of species swarms). Instead, Mayr (op.
cit.) favoured extrinsic barriers within the lake as the most important factor in the
isolation of populations within the lakes.

With the exception of Mayr (1963), Hubbs (1961) and Regan (1922), all other
authors have agreed that some sort of gross physical isolation was the principal
factor leading to speciation in these fishes. Hubbs (of. cit.) argues for ecological
and temporal segregation, and Regan (op. czt.) for speciation and adaptive radiation
through habitudinal segregation (sensu Gulick, 1905). It must be remembered
that in Regan’s time little was known of the lake’s history, and that Regan’s remarks
on the evolution of Lake Victoria cichlids were also a reflection of his dissatisfaction
with ‘. .. the modern view of evolution by accidental mutation’.

The role of habitudinal segregation in the speciation of Lake Victoria Haflochromis
is difficult to establish. Few of the contemporary species show such close associa-
tion with a particular habitat as do several of the Lake Malawi cichlids (Fryer &
Iles, 1972), and none appears to be specialized for utilizing a food source that is itself
restricted to a narrow habitat. It is, therefore, difficult to envisage any ecological
barrier that might be sufficiently absolute to prevent some genic exchange between
populations. In the present-day lake the major habitats themselves are not so
clearly delimited as seems to be the case in Lakes Malawi and Tanganyika. Finally,
and again unlike the two other lakes (see Fryer & Iles, 1972), there is no indication
of any intralacustrine differentiation of populations ; thus, the implication is of
genetical continuity of species’ populations throughout the lake. Until fairly
recently (see summaries in Kendall, 1969 ; also Doornkamp & Temple, 1966) thinking

8

114 P. H. GREENWOOD

on the physiographical background to Haplochromis evolution in Lake Victoria was
dominated by Wayland’s (1934) Pluvial hypothesis. That is, the developing lake
expanded and contracted (or was dried out completely) as a result of differing rainfall
régimes during the Pleistocene. This theory of lake fractioning was first used by
Brooks (1950) in his arguments to show that the Lake Victoria species flock could
have evolved by means of the usually accepted process of allopatric speciation, —
rather than through sympatric (i.e. intralacustrine) means.

Wayland’s theories were also basic to my first interpretation of speciation and
adaptive radiation in the flock (Greenwood, 1951). In that paper I attempted to
correlate what seemed to be the three structurally and ecologically definable major
groups of endemic species with the three major Pluvial and Interpluvial periods
influencing the lake’s development. With increasing knowledge of the species’
ecology and their phyletic relationships, and with new information on the lake’s
history, the conclusions I reached in that paper are no longer tenable. The inter-
relationships of the fishes are far more complex, both ecologically and phyletically
than I realized then, so that such a direct and simple correlation between lake
development, adaptive radiation and phylogenesis cannot be achieved. Indeed, it
seems that the three adaptive groups (Greenwood, op. cit.) are not only polyphyletic
(i.e. are grades sensu Huxley, 1958) but that each evolved simultaneously. That is
to say, there was concurrent speciation and differentiation of the trends occurring
within the different phyletic lineages contributing to a grade.

The spatial isolation needed to separate the developing taxa now appears to be a
correlate of both the way in which Lake Victoria originated and of later, tectonically
induced, changes in the lake basin and its outflows (see p. 10 above ; also Greenwood,
1965a). Climatic changes, it seems, had little effect on the lake’s early history and
thus on the primary evolution of the Haplochromis species flock (Doornkamp &
Temple, 1966; Temple, 1969; Kendall, 1969). Later, however, climatic effects
could have played some part, especially in the isolation of small Nabugabo-like
peripheral lakes (see Kendall, op. cut.).

A brief outline of Lake Victoria’s origin (essentially from the results of river rever-
sals and backponding) has already been given (see p. 10; also Greenwood, 1965a).
On this basis Fryer & Iles (1972) constructed a detailed model of the way in which
topographical events during the early period could have provided a variety of smaller
and larger lakes, at times partially or wholly interconnected, at other times partially
or wholly isolated from one another. The culmination of this history would, of
course, be the union of separate lakes to form a single lake. But, even at this period
there were lake-level changes leading to the isolation and reuporporangm of small
peripheral water-bodies (Kendall, 1909).

Initial differentiation of the main phyletic lines, and the development of trophic
radiations within these lines must have taken place among the Haplochromis species
inhabiting the shallow lakes first formed as the rivers were reversed and ponded back.
Potentially, each isolate could be the cradle of a species, provided that sufficient
time elapsed before the isolation was broken. That this time period might be a
short one is demonstrated by the evolution of five species in Lake Nabugabo during
a maximum time lapse of ca 3500 years (Greenwood, 1965a ; also p. 112 above).

EVOLUTION OF A CICHLID SPECIES FLOCK 115

At first the Haplochromis species would be in competition only with various non-
cichlid species. By analogy with the non-cichlids of present-day rivers (Greenwood,
1966), these would include a number of specialized feeders (e.g. insectivorous Mormy-
ridae and epilithic grazing cyprinids like Labeo) as well as more generalized feeders
like the Barbus species, and the piscivorous catfishes (Claritas and Bagrus species).
One can only presume from the trophically multiradiate Haplochromis species of the
present lake that strong selective forces were operating in favour of specialized
feeding habits. It 1s not possible to tell at what stage in the development of the
flock these forces were most intense. Possibly this happened, not at first (when a
generalized feeder might fare better against specialized competitors), but later when
the number of Haplochromis species had increased. That is, after at least some of
the original water-bodies with their contained Haplochromts species were inter-
connected. Thus, the competition would be between species of Haplochromis,
a situation rendered more likely if the species tended to occupy habitats not especially
favoured by the non-cichlid species (as is the situation in the present lake). It is
even possible that the Haplochromits species occupied the more lacustrine areas of the
developing lake, the non-cichlids occupying those regions which were environmentally
more nearly fluviatile.

Once a few Haplochromis species had evolved, further fractioning of the growing
lake would lead to an accelerated output of species. (Five species isolated in each
of seven cut-off portions of the lake could give rise to 35 new species.)

As the number of species increased so it is reasonable to assume that
selection pressures would rise in the competition for food and other niches,
and with this a concomitant development of anatomical and physiological special-
izations.

The continuous spawning in Haplochromis populations (see p. 51) could be an
important contributory factor in the development of such adaptations because it
would expose to selective action a greater genetical turnover than would be the case
in seasonally breeding species; advantageous gene combinations would also be
spread more rapidly through a population. No data are available on the generation
time for any Lake Victoria species, but for closely related species in Lake George,
bred in aquaria, the figure is probably about two generations per year (Dr C. D. N.
Barel, Leiden ; personal communication).

The evolutionary literature is replete with references to the genetical effects of
isolating small populations (for reviews see Mayr, 1963 and Grant, 1963). Although
there are adverse effects, in terms of genic loss and also from genetically ill-adapted
founder populations, the overall results of such population fractioning would seem
to accord well with the situation found in present-day Lake Victoria. Possibly
some of the adverse effects associated with small isolates’ might be mitigated by the
speed with which Haplochromis can speciate, and the relatively short developmental
period for Lake Victoria.

A noticeable feature of any adaptive trend within a Haplochromis lineage from
this lake is the persistence of species showing intermediate stages in the evolution of
a particular specialization (see pp. 57-93). This peculiarity would seem to suggest
that during the evolution of a trend, selection pressure acting on sister derivatives

I16 PP. H. GREENWOOD

was not at the same intensity. The size of the different water-bodies, the various
combinations of species isolated together, and the probability of there being, at
least for part of the lake’s history, a large main body of water in which environmental
conditions were more stable and selection less intense, are all possible factors allowing
the persistence of graded specializations.

The existence in any one lineage (and at any adaptive grade in that lineage) of |
several closely related species distinguished by male coloration and slight mor-
phometric differences is probably a reflection of their origin from populations of the
same mother species isolated in different water-bodies. This mode of speciation
would contradict Hennig’s (1966) postulate that at a given point in time a stem species
gives rise, dichotomously, to no more than two daughter species (one of which is the
original stem species less that part of its genome incorporated in the new species).
However, Brundin (1972) allows that an ancestral species may evolve into *. . . two
or several daughter species’, a view with which I would agree from my experience
with the Lake Victoria Haplochromis. Later in the same paper Brundin expresses
the view that simultaneous multiple splitting is a situation that cannot be con-
clusively demonstrated. Within the limits imposed by techniques available for
identifying species and their relationships, this is undoubtedly true. But the Lake
Victoria Haplochromis species do appear to be as good a prima facie case as can be
found for simultaneous multiple splitting.

The development of the Lake Victoria Haplochromis flock cannot be construed as
strictly intralacustrine for the majority of species and ecologically defined species
groups. In this respect it differs from the cichlid flock of Lake Malawi, at least as
far as the evolution of that flock is understood. Fryer & Iles (1972) argue cogently
in favour of true intralacustrine speciation by habitat restriction and thus micro-
geographic isolation in Lake Malawi. However, I do not find all their arguments
equally convincing, particularly since they are based essentially on a detailed study
of only certain elements in the cichlid fauna ; the strength of habitat restriction is
unknown for most of the Haplochromis species in Lake Malawi.

To me the weakest point in Fryer & Iles’ argument lies in their failure to explain
how the early invaders of the lake, species relatively unspecialized ecologically, were
confined to and isolated in particular habitats. Isolated, that is, with sufficient
effectiveness to prevent interpopulation gene flow. Even assuming that this did
happen or that some type of stasipatric evolution (Key, 1968) occurred, and that
the newly derived species became more closely tied to their habitats (as Fryer &
Iles postulate) how, ultimately, did these stenotopic taxa manage to achieve lake-
wide distribution? Undoubtedly some of the means suggested by Fryer & Les
(fluctuating lake levels in particular, of. cit. : 524) were operative. But there stiil
seems to be a fundamental contradiction in an argument which invokes greater
stenotopy in relatively unspecialized ancestors than in their observably stenotopic
and highly specialized descendants (for example the several species that show inter-
populational differences [Fryer & Iles, of. cit.] within Lake Malawi). Finally, I do
not think that sufficient consideration has been given to conditions prevailing when
Lake Malawi was first forming. Admittedly its present topography is very different
from that of Lake Victoria, but was it necessarily a deep trench from its very

EVOLUTION OF A CICHLID SPECIES FLOCK 117

inception? Could it not have passed through a period of shallow, isolated lakes like
those at the start of Lake Victoria?

Despite these reservations, however, there is sufficient evidence both historical
and contemporary (see Fryer & Iles, 1972) indicating that the cichlid flocks of Lakes
Malawi and Victoria did have somewhat different evolutionary histories.

Mention was made above of the virtual absence of evidence for truly intralacustrine
speciation in Lake Victoria. A possible exception may be provided by the several
species confined to deeper waters (p. 49). Considering the physiographical history
of the Lake, deepwater habitats were unlikely to have become available until the
basin settled into more or less its present form. If that is so, then geographical
barriers cannot be invoked to account for isolation of the evolving deepwater
species. The alternative explanation would be an invasion of deep waters by in-
dividuals or populations of species occupying inshore habitats. Speciation initiated
in this way would require that the migrant populations be able to establish breeding
sites in their new habitats, and that no gene flow occurred between the in- and off-
shore communities. There is little evidence from contemporary species to support
this hypothesis, and neither does it gain much support from what is known of the
interrelationships of the deepwater species (see pp. 67-68). The presumed
phylogeny of the ‘ividens’ group of crustacean-eating species suggests an evolutionary
history similar to that of any inshore lineage. That is, multiple simultaneous (or
near simultaneous) speciation from a common stem. One can therefore only assume
that the now deep living species evolved along with species from other habitats but,
unlike the latter species, were able to colonize deep habitats when these became
available. This question, like many others, should be left open and reconsidered
when more is known about the deepwater species, particularly their range of depth
tolerance in shallower regions of the offshore lake.

There has been a long-standing argument on the effects predatory species have had
on the processes of speciation in African lakes. The debate was sparked off by
Worthington (1937) who suggested that the presence of the large, piscivorous
predators Hydrocynus (Characidae) and Lates (Centropomidae) in a lake inhibited
speciation among the cichlids. His ideas derive from the fact that, excepting the
Lake Tanganyika cichlid complex, cichlid species flocks only occur in lakes where
Lates and Hydrocynus are absent. Lake Victoria in Worthington’s view is a prime
example of speciation unhampered by predators. Worthington, however, over-
looked (or more correctly was unaware of) the predatory effects exerted by the
numerous piscivorous Haplochromis species in the lake (see above p. 31) and those
of the several non-cichlid predators also present (Greenwood, 1959C).

Palaeontological evidence (Greenwood, 1959d) shows that the Haplochromis
species flocks of Lakes Edward and George (another key lake system in Worthington’s
hypothesis) evolved in the presence of Lates and Hydrocynus.

The physiographical history of Lakes Albert and Rudolf (lakes with rudimentary
Haplochromis flocks, but with Lates and Hydrocynus) could just as well be responsible
for the lack of speciation (see summary of the evidence in Fryer & Hes, 1972).

Indeed, the whole issue of predator—speciation interaction is ably and critically
summarized by Fryer & Iles (of. cif.) and need not be discussed further here. In

118 P. H. GREENWOOD

brief, there is no evidence supporting Worthington’s original hypothesis (Worthing-
ton, 1937, 1954). On the contrary, the bulk of evidence suggests that predators are
to be considered, if anything, factors promoting rather than inhibiting speciation
(Greenwood, 1959C). |

Connell & Orias (1964) have proposed an interesting ecological model to account
for species diversity, especially in a tropical environment. The authors discount |
various commonly accepted ideas to explain this diversity, such as the number of
available niches, rigorousness of the environment and the concept of ‘biological
immaturity’ in temperature regions versus an equilibrium state in the tropics.

Instead they propose a model based essentially on the distribution of energy flow
in physically stable environments contrasted with unstable environments. The
tropics (stable) allow a greater proportion of energy to be used for net productivity
(i.e. growth and reproduction) rather than for regulatory activities to counter
environmental changes. From this, they argue, there will be larger populations,
hence more genetic variation within populations, and thus better opportunities for
successful speciation. Increased numbers of species will in turn provide a positive
feedback by increasing environmental stability through, among other factors,
increased recycling rates for nutrients. This feedback, Connell & Orias suggest,
would be most marked in the early stages of evolution and would of course further
the process of speciation. Ultimately, it is hypothesized, there would develop
‘overspecialization’ amongst the species produced, resulting in smaller populations
and hence a negative feedback into the system.

The Connell—Orias model is based, implicitly, on homeothermic and terrestrial
animals. Yet, there are interesting parallels with the situation, both historically
and contemporaneously, in the Lake Victoria species flock. On the whole these
fishes would seem to conform closely with the model. If increasing species diversity
and number encourages further speciation and environmental stability, the rapidity
with which Haplochromis speciates may contribute to the ecological success of these
fishes and also account in part for their dominance in the lacustrine environment.
Possibly in some taxa (e.g. the monotypic genera and other anatomically specialized
species) we are seeing the ‘overspecialization’ that Connell & Orias consider as
contributing to the negative feedback of the system.

The evolution of the Haplochromis species flock in Lakes Edward and George 1s
usually linked with that of Lake Victoria (Trewavas, 1933 ; Greenwood, 1951, 1950d ;
Fryer & Iles, 1972). There are two reasons for this. First, there is the great
similarity existing between the species of the two lake systems (Lakes Edward and
George are interconnected and can be considered one lake for the purpose of this
discussion) ; this includes the sharing of certain Haplochromis and related species
(Greenwood, 1973a). Second, the existence of river systems connecting the two
lakes, and along which some transfer of fishes might have occurred in the past ;
indeed, some geological evidence even suggests almost interlacustrine connections
(Temple, 1969). These rivers now flow in two directions, eastward into Victoria and
westward into Lake Edward—George. The watershed is a low swamp divide (Doorn-
kamp & Temple, 1966). Today these swamps are impenetrable to all but air-
breathing species, but they could have been less effective species filters in the past.

EVOLUTION OF A CICHLID SPECIES FLOCK 119

A recent revision of Lake George fishes (Greenwood, 1973a) shows that, although
the Haplochromis species are closely related to those of Lake Victoria, there are
fewer shared species than was once thought (Trewavas, 1933). The shared species
are non-endemic taxa (i.e. Haplochromis nubilus, Astatoreochromis alluaudi and
Hemthaplochromis multicolor). Recent geological studies (especially those of
Doornkamp & Temple, 1966) show that although Lake Edward-George was filled
from the same river systems as Lake Victoria, the Edward basin was established
before that of Lake Victoria. Also, the Edward basin has been effectively isolated
from that of Victoria for all of its existence.

The common fluviatile ancestry of the two lakes means, of course, that their
species flocks also had, in large part, a common ancestory. The implications of this
are manifold and include the possibility that Lates and Hydrocynus (known as fossils
from Lake Edward, but no longer extant there ; Greenwood, 959d) might also have
been components of the early Lake Victoria biota (see p. 10 above). Unfortunately
the Quaternary fossil record for Lake Victoria is virtually non-existent (Bishop,
1969) so this possibility cannot be checked.

A common ancestry for the Victoria and Edward Haplochromis species does allow
one to make a meaningful comparison of the two species flocks (see Greenwood,
1973a). The pattern of adaptive radiation is extremely similar, with species
showing all the trophic specializations found in the Lake Victoria flock (and, in addi-
tion, the evolution of a pelagic zooplankton eater). There are fewer species in Lake
Edward—George (see Table I). The situation in Lake Edward, like that in Lake
Nabugabo (see p. 112), could be looked upon as a live model of a phase in the evolu-
tion of the Lake Victoria flock. Lake Edward would then represent one of the
larger preamalgam water-bodies (in which both speciation and adaptive radiation
had taken place) and Lake Nabugabo a much smaller peripheral water-body in which
differentiation had proceeded only to the level of speciation. That is, representative
of the earlier and the later phases in the development of Lake Victoria.

No precise speciation rate can be determined for the Haplochromis of Lake Vic-
toria. Dating of the lake’s inception cannot be fixed more accurately than the mid-
Pleistocene (Doornkamp & Temple, 1966; Temple, 1969), 1.e. about 750 000 years
B.P. Thus all one can say is that between 150 and 170 species have evolved in
about three-quarter million years. Obviously the actual rate of transformation from
one species to another must have been much faster. The figure derived from Lake
Nabugabo (see Greenwood, 1965b) would indicate that a species can evolve in less
than 3500 years, but even here we are still far from knowing the time taken to effect
genetical isolation between mother and daughter species. If this figure is taken
simply as an order of magnitude, and if due allowance is made for a tropical environ-
ment and the relatively short generation time in Hapflochromis, speciation rate is
about one and a half times to twice that in the few other genera of fishes (all non-
cichlids) for which comparable data are available (Myers, 1960 ; Hubbs & Raney,
1946).

CONCLUSION

There has been a tendency to consider the African cichlid species flocks as a

somewhat unique evolutionary phenomenon (see p. 3). What justification is

120 P. H. GREENWOOD

there for this attitude, and what contribution do these flocks make to understanding
the broader picture of speciation and evolution among freshwater fishes, and in
general?

It is usual to compare the cichlids to the Galapagos Island Finches (Darwin’s
Finches) and to the Hawaiian Honeycreepers. There are indeed many broad
similarities between these bird and fish, island and lake, species flocks. In both.
situations the main evolutionary trends have been towards trophic specialization
(with concomitant anatomical specializations ; see Lack, 1947; Amadon, 1950).
The comparison between the lakes and islands as vacant, geographically isolated,
multi-niche environments is also a valid one. This latter point is particularly
evident when it is recalled that, during its early history, Lake Victoria was a group
of lakes and thus geographically akin to the background of evolution in the two bird
groups, more so than would be a single lake. Fryer & Iles (1972) argue, however,
that marked habitat differentiation in such lakes as Malawi and Tanganyika makes
them in effect multiple and not single water-bodies. Be that as it may, the end
point of speciation in these lakes is basically little different from that in Lake Victoria.

The range of anatomical and ecological diversity found amongst the cichlid fishes
far surpasses that of the Finches and Honeycreepers. This I believe is explicable
on an anatomical basis alone. The fish syncranium is a better starting point for
trophically orientated morphological modification than is a bird skull. Especially
is this so for a cichlid fish where the jaws, teeth and pharyngeal apparatus have
reached a level of differentiation that gives the system a high degree of morpho-
potential (see pp. 103-111 above). Other factors, both inherent and environmental,
can be adduced to explain the greater differentiation and speciation of the Great
Lake cichlid fishes (See p. III).

It is believed that one factor encouraging adaptive radiation in island invading
birds was the lack of competition in their new habitat, especially when compared
to conditions on the mainland. Conditions for fluviatile cichlid species invading a
developing lake might be different. Unlike the lone bird species colonizing an island,
the ancestral river Haplochromis species would enter the new environment in the
company of several different kinds of fishes. These would include, particularly,
members of various non-cichlid families such as the Cyprinidae, Mormyridae and the
catfishes.

In this assemblage, so it is argued (Fryer & Iles, 1972), there is potential competi-
tion for the one or two founder cichlid species. However, since the colonizers had
already established some kind of equilibrium in the river environment, and since the
developing lake would differ little from a river, there might, in fact, be little competi-
tion at first. That is to say, there would be pre-emption of certain habitats from the
outset by the differently adapted invaders. Only after the cichlids had speciated
would competition become a major factor in their evolution. In this respect I
believe that there is really little difference between the island birds and the lake
fishes. However, I would agree with Fryer & Iles when they point out that one major
difference lies in the fact that the cichlids, unlike the birds, evolved in the presence
of predators ; but the consequences of that interaction are debatable ; see above,

pali7.

EVOLUTION. OF “A. CICHLID:. SPECIES FLOCK E27

All in all, the cichlid species flocks, despite the similarities in evolutionary back-
ground, are more complex and probably more successful than are the species flocks
of Galapagos Geospizidae and Hawaiian Drepaniidae.

A similar conclusion is reached when the cichlid flocks are compared with the few
other examples of lacustrine species swarms among fishes (including those of the
non-cichlids occurring sympatrically with the cichlids). The best studied of these
are the cyprinid flock of Lake Lanao in the Philippines (18 endemic species ; see
Myers, 1960), the 14 endemic species of the cyprinodont subfamily Orestiinae in
Lake Titicaca (Ichernavin, 1944 ; Brooks, 1950) and the 18 endemic cottoid species
of Lake Baikal (Berg, 1925, 1928; Brooks, 1950; Kozhov, 1963). Lesser flocks
are discussed by Myers (1960) and Mayr (1963) ; all are completely overshadowed
by the cichlid flocks, as indeed are all other vertebrate and most invertebrate species
swarms. Exceptional among the latter are the gammarid Crustacea of Lake Baikal
(Brooks, 1950; Kozhov, 1963) and, particularly, the drosophilid flies of Hawaii.
The similarities between the flies and the African cichlids are remarkably close,
involving localized species swarms of up to 160, mostly endemic, species, and much
morphological diversity associated with trophic specialization (see discussion in
Piven oc Liles, 1972).

Thus, an answer to the first question posed at the beginning of this section seems
to be largely in the negative. The cichlid species flocks are not a unique evolutionary
phenomenon, nor has their evolution involved organic or physical processes unique
to these animals or the environment in which they occur. But, the cichlids are
outstanding examples of this particularly concentrated and tachytelic type of evolu-
tion, be they compared with vertebrate or invertebrate animals. The reasons for
this singularity seem to lie in the fortuitous combination of environmental circum-
stances, the great morpho-potential of most cichlid taxa, and the biology (especially
the reproductive biology) of these taxa.

Turning now to the question of what light the species flocks throw on evolutionary
processes in general, there is one concept that in part reflects back onto the presumed
peculiarities of lacustrine species flocks, and in part has broader application.

Myers (1960) drew attention to a peculiar feature of many endemic lake fish faunas,
of which the cichlid flocks (especially those of Lakes Malawi and Tanganyika)
provide outstanding examples. This feature, which Myers called ‘supralimital
specialization’, involves the evolution of characters in taxa, of circumscribed distri-
bution, that transcend the morphological limits of a related taxon’s systematic
category elsewhere in its range. Myers is particularly concerned with what might
be termed ‘suprafamilial’ character transgression, but it is clear that he applies the
term to situations transcending generic limits as well.

-Philosophically, one may jib at the circularity of this coricept, but its observational
basis is undeniable. In Lake Victoria the monotypic genera Platytaeniodus and
Hoplotilapia (and even Macropleurodus) would qualify as supralimital taxa, and there
are even better examples among the species of Lakes Tanganyika and Malawi (Poll,
to50:: ‘Fryer & Tes, 1972).

According to Myers (of. cit. : 332) supralimitally specialized species are ‘. . . often
capable of becoming the founders of new genera, families or perhaps even higher

9

122 Pi. GREENWOOD

categories, at new adaptive levels. They have unquestionably done so in the older
lake fish faunas... .’ The importance of this statement would seem to lie in the
implication that the development of supralimital specializations lead to evolutionary
success because their possessors are able to enter new adaptive levels. It is this
aspect of Myer’s concept that requires careful consideration.

In Lake Victoria there are several examples of supralimital specialization. At the -
species level there are Haflochromis xenognathus (see p. 70), H. welcommet (p. 69)
and H. aelocephalus (p. 61; also Greenwood, 1959b) ; at the generic level, Macro-
pleurodus bicolor, Platytaeniodus degent and Hoplotilapia retrodens (see pp. 99-103).
As might be expected (and as is implied in Myer’s formulation of the supralimital
phenomenon), these morphologically distinctive taxa also show definite ecological
specializations as well, namely in these examples, trophic specialization. Each
example represents an evolutionary break-through into a new adaptational level.
But equally distinctive breaks have been made by many other Victoria Haplochromis
species which do not exhibit morphological changes that could be termed supra-
limital. It would, for example, be difficult to consider the mollusc-crushing species
(p. 72), the algal grazers (p. 63) or the piscivores (p. 80) as transcending generic
limits unless one took a narrowly typological view of the flock’s taxonomy. _(Ironi-
cally, the type species for the genus Haplochroms is H. obliqumdens, a species with
highly specialized teeth ; see p. 65).

In other words, the Lake Victoria Haplochromis species have succeeded in occupy-
ing several adaptational levels (levels that are new relative to that of the ancestral
fluviatile species) without producing supralimital specializations. Expressed in
another way, supralimital specialization is not a necessary prerequisite for evolu-
tionary success nor is it necessarily a common way of achieving it.

Myers (op. cit. : 331) also implies that the full success of supralimital specializations
can only be exploited outside their place of origin: ‘If they (the specialized species)
could get out of their lakes and use their supralimital specializations in other lakes
or streams, ... many existing lake fishes could easily become the founders of large
and flourishing new groups at new adaptational levels’. I submit that the lake
cichlids have done this, and 77 sztu ; also, that it is unnecessary to link such success
with altered taxonomic status (i.e. marked morphological change) for the animal
achieving it. What strikes me as more important than extreme morphological
change per se is the evolutionary opportunity offered by lakes (or a similar type of
evolutionary background) in the development of ecological specialization. In this
sense I would endorse Myer’s ideas on the probable importance of lakes (or near
lacustrine conditions) in the evolution of fish faunas now no longer lacustrine but,
as it were, secondarily fluviatile. For example, the characid fishes of tropicai
America (cited by Myers, 1960) and probably several of the endemic species groups
in the Congo river (see Roberts, 1972 : 128).

The reasons for the existence of “supralimital’ morphotypes in species flocks
remains to be explained, especially since, as in Lake Victoria, apparent adaptational
success can be achieved without extreme anatomical modification. With only the
information currently available it is, of course, impossible to really evaluate this
success, and each example of a ‘successful’ species can only be considered in the

EVOLUTION OF A CICHLID SPECIES FLOCK 123

context of its particular environment. Thus it is possible that during the evolution
of various biotopes in Lakes Tanganyika and Malawi more intense selection has
resulted in the greater morphological differences seen in the species of those lakes
than in those of Lake Victoria. In other words, a specialization has to be more
specialized if it is to succeed in the former lakes. Once again, a dearth of ecological
information for species of Lakes Malawi and Tanganyika hampers speculation.

Myer’s views (1960) on the importance of tachytelic supralimital specialization is
in direct conflict with an hypothesis put forward by Briggs (1966). According to
Briggs there are two, simultaneously occurring kinds of evolutionary change. One
(the so-called successful type) is slow and likely to produce species with a potential
phyletic future, the other (so-called unsuccessful) is rapid and unproductive of species
with phyletic potential.

Briggs (op. cit.) associates the centres of unsuccessful evolution with peripheral
areas of a species’ distribution, and with evolutionary traps (sensu Simpson, 1953),
like lakes and islands. It cannot be denied that a lake is potentially a trap (both in
the physical and evolutionary senses of that word). Equally, it cannot be overruled
as a source of phyletically potential taxa if its fauna is later dispersed (see above ;
also Myers, 1960, and Roberts, 1972, for possible examples of this having happened).
Again one faces the difficulty of assessing evolutionary success. At the present
moment lake cichlids are a successful group in that environment, and I can find no
a priovt reason why some of these species could not be successful if they were to
invade a major new system. That the fluviatile fishes are not generally outstanding
in their diversity (but recall the Congo and Amazon ; p. 4) is probably attributable
to the absence, historically, cf these physio-geographic circumstances that charac-
terize lake formation and development.

Briggs (following Bates [1960]) cites, as a general evolutionary principle, the
greater stability of communities composed of diverse types and numerous species
(see also the ideas of Connell & Orias [1964] discussed on p. 118). From this,
Briggs argued that stable ecosystems are the most important centres for successful
evolution. The unstable beginnings of Lake Victoria seem to have had important
evolutionary results, and it is very probable that the early environments (ecologically
and physiographically) of Lakes Malawi and Tanganyika were also unstable. The
end product in all three lakes, however, was a diverse multi-specific ecosystem of
apparent stability. Furthermore, this has been achieved, even in the older lakes,
at a rate which can only be described as tachytelic.

Thus, one might postulate, from the viewpoint of evolutionary potential, that
situations akin to those of the African lakes are important because their faunas are
able to reach a level of diversity, and therefore ultimate stability, in a short time.

Like the concept of supralimital specialization, that of Briggs’ ‘successful’ and
‘unsuccessful’ evolutionary change seems as much semantic as biological, with the
added difficulty of distinguishing between evolutionary success and phyletic longe-
vity. Can one really compare, in terms of evolutionary success, the coelacanths and
teleosts?

Without doubt factors used by Myers and Briggs to support their opposing argu-
- ments have played a part in the ebb and flow of phylogenesis. Perhaps the most

124 P. H. GREENWOOD

realistic conclusion is that of Romer (1960), who agreed that explosive evolution
(i.e. rapid diversification) is often followed by extinction, but that it is not an excep-
tional process nor, for most groups, an unusual one.

In this, as in so many other respects, the cichlid species flocks are evolutionary
microcosms repeating on a small and appreciable scale the patterns and mechanisms
of vertebrate evolution. It is interesting, in this context, to quote the last para- |
graph of the summary from Grant’s book The origin of adaptations (1963): ‘It
follows that long continued evolutionary trends in some phyletic lines which undergo
rapid and continual formation of new adaptive allelle combinations may be expected
to follow a course of repeated speciational branchings. The phyletic line in such
cases progresses through a steplike succession of divergences, in which each daughter
species with its particular new adaptive allelle combination, branches off from a
genetically different and more conservative ancestral population, and later gives
rise in its turn to another new daughter species which diverges again in the same
general direction.’

The aim of Grant’s book was‘... to set forth the causal theory of evolution as
applied to diploid sexual organisms’. Yet, the paragraph quoted above could well
describe the three-quarter million year old Haflochroms species flock in Lake
Victoria.

ACKNOWLEDGEMENTS

Very many people have contributed in one way or another to this study. It is
with pleasure that I offer them my thanks and deep appreciation for their help,
intellectual or physical (and in the case of my colleagues in east Africa, often of both
kinds).

I am particularly indebted to two people. First, to my former teacher Professor
D. J. Nolte of the Witwatersrand University, South Africa, who started it all by
stimulating my interest in problems of speciation and evolution. Next, Dr
Ethelwynn Trewavas (then Curator of Fishes in this Museum), whose pioneering and
wide-ranging researches into African cichlids were one of my early stimuli and have
remained as a constant inspiration. Her kindness and knowledge were unstintingly
given to me, first as a student and then over many years of close association as
colleagues. I shall always be grateful to her for suggesting that I study the Haflo-
chroms of Lake Victoria, and for the time and patience she expended on my introduc-
tion to these fishes (and to ichthyology in general).

My work in the field, as a member of the East African Fisheries Research Organiza-
tion (1951-58), was strongly supported by its director Mr R. S. A. Beauchamp; I
take this opportunity to thank him not only for this, but for his appreciation of the
need to carry out basic taxonomic work on the freshwater fishes of east Africa. My
best thanks go also to Dr R. H. Lowe-McConnell and Dr Philip S. Corbet, former
colleagues at E.A.F.R.O., with whom I collaborated on many ecological aspects of
Haplochromts biology.

More recently I have received a great deal of assistance from the current director
of E.A.F.R.O. (now the East African Freshwater Fisheries Research Organization),
Dr John Okedi, his staff (in particular Dr Michael Gee), and the director of the

EVOLUTION OF A CICHLID SPECIES FEOCK 125

F.A.0./U.N.D.P. team, Mr Peter Jackson and his staff, working with E.A.F.F.R.O:
on the fisheries of Lake Victoria.

In the British Museum (Natural History) I am particularly indebted to Mr Gordon
Howes on whose willing shoulders and into whose capable hands have fallen much of
the drudgery in preparing this paper. Most of the osteological and anatomical
figures are his work, and for this alone I am especially grateful.

To the many people not mentioned by name I can only repeat my thanks for their
considerable help in so many different ways.

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P. H. GREENWOOD, D.Sc.

Depariment of Zoology

British MusEuM (NATURAL HISTORY)
CROMWELL ROAD

LONDON SW7 5BD

129

INDEX

N.B. Page numbers in ztalics refer to illustrations.

Albert, Lake,“5, 6(age of), 10, 20, 109, 117
Alestes
A. jacksoni, 12
A. sadleri, 12, 45
A statoreochromis alluaudti, 14, 17
anatomy, 73, 109
breeding, 19
dentition, 73
distribution, 12, 18, 45, 119
ecophenotypic variation, Iog-II0
food; 18; 37; 73, 109
relationships, 18, 20, 99 et seq.

Bagrus, 115

B. docmac, 12, 45
Baikal, Lake, 121
Barbus, 45, 115

B. altianalis, 45
Barombi-Mbo, Lake, 17

catfishes (see also Bagrus, Clarias and
Syndontis), 111
Centropomidae, 111 (see also Lates)
Characidae, III, 117
character displacement, 29
Clarias, 11, 115
C. mossambicus, 12, 15, 45, 109
coloration, 51-55
Congo, River; 4,5, 122
Ctenopoma muret, 11
Cyprinodontidae, 111

Darwin’s Finches (Geospizidae) compared
with Lake Victoria Haplochromis spp.,
120-121

dentition of Haplochromis :
changes with age, 106
pharyngeal, 107

drosophilid flies of Hawaii, compared with
Cichlidae, 121

ecophenotypes, absence of in Lake Victoria,
110

Edward, Lake, 5, Io, 11, 18, 20, 55, 109, 110,
117-119

egg dummies, 53

Engraulicypris argenteus, 12, 31, 43

‘estoy’ subgroup, 91, 9S

Gause's law, .20, 48
_ generic subdivisions of Lake Victoria flock, 99

Genyochromis mento, compared with dH.
welcommet, 43

George, Lake, 5, 11; 16,18, 20;-55; 100; Lio,
117-119

Gnathonemus, 45

gradal versus phyletic classification, 56-57,

114

haplochromine lineage, 17, 21, IIo
success in lakes, IIO-III
Haplochromis
breeding, 19
catches of, 46
evolutionary success of, III
generation time, I15
habitat preferences, 45~46
rate of speciation, 112, I19
Haplochromis acidens, 42
anatomy, 41, 67
dentition, 67
food, 30, 41, 67
relationships, 67, T0o
H. aelocephalus
anatomy, 61, 62, 97
dentition, 62
food, 30, 61
relationships, 61, 97, I0o
supralimital specialization in, 122
Hi. altigenis
anatomy, 84, 89, 97
coloration, 54
food, 3o (see H. prognathus complex), 80
relationships, 89, 97, roo (see H. progna-
thus complex)
H. apogonoides
anatomy, 92
dentition, 92
food, 30
relationships, 92, 100
H. argenteus, 90
anatomy, 9I, 92
food, 30 (see H. prognathus complex), 80
relationships, 91, 92, roo (see H. progna-
thus complex)
H. avtaxerxes
anatomy, 89
food, 80
relationships, 89, roo (see H. prognathus
complex)
H. barbarae, 54
anatomy, 76, 77, 79, 97

130 P. H. GREENWOOD

coloration, 53, 54
food, 30, 33, 37, 76
relationships, 79, 97, 100
H. bartoni
anatomy, 89
food, 30 (see H. prognathus complex)
relationships, 89, roo (see H. prognathus
complex)
H. bayont
anatomy, 89, 92
dentition, 92
food, 80
relationships, 89, roo (see H. prognathus
complex)
FH. bloyeti, 22
anatomy, 57-56, 59, 94, 95
dentition, 26, 58, 59
distribution, 57
relationships, 20, 58, 63, 95, 100
H. boops
anatomy, 84
food, 30 (see H. servanus complex), 80
relationships, 84, roo (see H. servanus
complex)
H. brownae, 52
anatomy, 28, 85, 105
dentition, 85
food, 30
relationships, 85, roo
H. burtont, 20
H. callipterus, 20
FH. cavifrons, 23
anatomy, 84
coloration, 85
food, 30, 80
relationships, 84, roo (see H. servanus
complex)
ie chelotes,:22., 32
anatomy, 60, 61, 95
coloration, 54
dentition, 27, 31, 60, 61
fO0d) ZO, 3E
relationships, 62, 63, 72, roo
H. chlorochrous
anatomy, 68
dentition, 68
food, 67
relationships, 68, roo (see tvidens complex)
A. chromogynos
anatomy, 60, 61, 62, 95
coloration, 52
dentition, 31
food, 30, 31
relationships, 62, 63, 72, roo

1. cinctus
anatomy, 41, 66
dentition, 66
distribution, 66
food, 30, 41, 66
relationships, 66, 100
1. cinereus
anatomy, 59
dentition, 59
food, 30
relationships, 100
FAA. cronus, 35
anatomy, 76, 77, 78
coloration, 53
dentition, 78
food, 305377170
relationships, 76, 78, 100
H. cryptodon
anatomy, 76, 77
dentition: 76; 77
food, 30, 75
relationships, 76, 100
H. cryptogramma
anatomy, 68
coloration, 50
dentition, 68
distribution, 49
food, 50, 67
relationships, 67, roo (see H. tridens
complex)
H. decticostoma
anatomy, 84
food, 30 (see H. servranus complex), 80
relationships, 84, roo (see H. servranus
complex)
FT. dentex,, 23, 92
anatomy, 89, 9I
dentition, 25, 92
food, 30 (see H. prognathus complex),
80
relationships, 89, 92, roo (see H. prognathus
complex)
HH, dichrourus
anatomy, 92
coloration, 52
food, 92
relationships, 92
H. dolichorynchus, 40
anatomy, 68
dentition, 68
distribution, 49
food, 67
relationships, 68, zoo (see H. trvidens
complex)

INDEX

H. mepodisma, 22, 93
anatomy, 26, 62, 63, 75, 94, 95, 96
dentition, 26, 63, 67
food; 30; 62; 73
relationships, 63, 67, 93, 95, 96, Too
H. erythrocephalus, 42
anatomy, 16, 28, 41, 64, 66, 94
dentition, 25, 66
distribution, 49
food, 16, 28, 30, 41
relationships, 66, 67, T0o
A, estor, 35
anatomy, 9I
food, 30 (see H. prognathus complex), 80
relationships, 91, roo (see H. prognathus
complex)
H. flavipinnis, 86
anatomy, 84, 97
coloration, 52
food 3o (see H. prognathus complex), 80
relationships, 89, 97, roo (see H. prognathus
complex)
A, gilberti, 87
anatomy, 89
food, 30 (see H. prognathus complex)
relationships, 89, roo (see H. prognathus
complex)
H. gowerst
anatomy, 88, 91
food, 30 (see H. prognathus complex), 80
relationships, 91, z00 (see H. prognathus
complex)
H. grantt, 22, 38
anatomy, 69, 70, 71
dentition, 26, 69, 70
distribution, 47
food, 26, 30, 69, 72
relationships, 72, 100
H. guiarti, 23, §3
anatomy, 81, 85, 96
dentition, 85 :
food, 30, 80
relationships, 85, 96, roo
H. humilhior, 38
anatomy, 73, 74, 75, 94
dentition, 26, 73
distribution, 47
food, 30, 37
relationships, 73, 100
H. 1tshmaeli, 18, 23, 40, 110
anatomy, 71, 74, 75, 94
dentition, 71, 74
food, 18, 30, 37, 72
relationships, 73, 100

131

H. lacrimosus
anatomy, 58
dentition, 58
food, 58
relationships, 59
H. laparogramma
coloration, 50
distribution, 50
food, 50
A. lividus
anatomy, 63, 65
dentition, 25, 26, 39, 65
distribution, 47
food, 26, 30, 39, 63
relationships, 65, roo
FH. longirostris, 90
anatomy, 9I
food, 30 (see H. prognathus complex), 80
relationships, 91, roo (see H. prognathus
complex)
H. macrognathus, 23, 90
anatomy, 88, OI
food, 30 (see H. prognathus complex), 80
relationships, 91, roo (see H. prognathus
complex)
H. macrops, 32, 93
anatomy, 60, 61, 94, 96
dentition, 25, 6r
food, 30, 58
relationships, 59, 73, 100
H. maculipinna
anatomy, 81, 84, 97
food, 30 (see H. serranus complex), 80
relationships, 84, 97, roo (see H. servanus
complex)
H. mandibularis
anatomy, 84, 89, 98
food, 30 (see H. prognathus complex), 80
relationships, 89, roo (see H. prognathus
complex)
H. martini, 83
anatomy, 81, 85, 96
coloration, 50, 52, 85
dentition, 85
food, 30, 85
relationships, 85, 96, roo
H. maxillaris, 36
anatomy, 76, 77, 96
dentition, 27, 76, 77
food, 30, 75
relationships, 77, 80, 96, roo
H. megalops
anatomy, 58
dentition, 58

132 P. H:- (GREENWOOD

food, 58
relationships, 59
H. melanopterus
anatomy, 76, 77
dentition, 27, 76, 77
food, 30, 75
relationships, 77, 80, roo
H. melichrous
anatomy, 68
dentition, 68
food, 30, 68
relationships, 68, 100
H. mento, 35
anatomy, 88, 91
dentition, 88
food, 30 (see H. prognathus complex), 80
relationships, 91, roo (see H. prognathus
complex)
H. michaelt
anatomy, 85
coloration, 50
dentition, 85
food, 30, 85
relationships, 85, 100
H. microdon
anatomy, 76, 77, 97
dentition, 76, 77
food, 30, 75
relationships, 76, 97, 100
H. mylodon, 110
H. nigricans
anatomy, 64, 66, 94
coloration, 53
dentition, 26, 41, 65
distribution, 46, 47
food, 26, 30, 39, 47, 63, 66
relationships, 65, 66, roo
H. nubilus, 12, 119
H. nuchisquamulatus
anatomy, 63, 65
dentition, 25, 26, 39, 05
food, 26, 30, 39, 63
relationships, 65, 100
H. nyanzae
anatomy, 84
food, 30 (see H. sevranus complex), 80
relationships, 84, roo (see H. servanus
complex)
Hi. obesus, 23
anatomy, 76, 77, 78, 96
coloration, 53, 55
dentition, 27, 77, 78
distribution, 46
food, 30, 75

relationships, 77, 80, 96, roo
H. obliquidens, 122
anatomy, 63, 64, 65, 94
dentition, 25, 26, 27, 39, 64, 65
distribution, 43, 47
food, 26, 30, 37, 63
relationships, 65, 100
H. obtusidens
anatomy, 72, 73, 74, 75, 94
dentition, 26, 72, 74
food,, 30, 37; 72
relationships, 73, 100
H.. orthostoma
anatomy, 92
relationships, 92
H. pachycephalus
anatomy, 84
food, 30 (see H. sevvanus complex), 80
relationships, 84, roo (see H. sevvanus
complex)
H. pallidus, 22, 32, 93
anatomy, 58-60, 73, 94, 85, 96
dentition, 61, 73
food, 30, 58
relationships, 58-59, 93, 95, 96, I00
H. pavaguiarti, $6
anatomy, 84, 89, 97
food, 30 (see H. prognathus complex), 80
relationships, 89, 97, roo (see H. prognathus
complex)
H. paropius
anatomy, 41, 64, 66, 94
dentition, 66
distribution, 66
food, 30, 41, 66
relationships, 66, roo
H. parorthostoma, 93
anatomy, 92
distribution, 93
food, 30
relationships, 92, 93, 100
H. parvidens, 23, 36
anatomy, 76, 77, 78, 97
dentition, 76, 77, 78
food, 30, 33, 75
relationships, 76, 97, 100
H. pellegrini, 88
anatomy, 90, 9I
food, 30 (see H. prognathus complex), 80 -
relationships, 90, roo (see H. prognathus
complex)
H. percoides, 86
anatomy, 91
coloration, 52, 91

relationships, 90, 91, roo (see H. prognathus
complex)
H. pharyngomylus, 18
anatomy, 72
dention, 26, 72
distribution, 47
foods 18, 30,:37;°72
relationships, 73, 100
HA. phytophagus
anatomy, 63
dentition, 63
food, 30, 39, 63, 67
relationships, 67, 100
H. piceatus
anatomy, 58
dentition, 58
food, 58
relationships, 59
H. plagiostoma
anatomy, 81, 84, 97
coloration, 85
food, 30 (see H. serranus complex), 80
relationships, 84, 97, roo (see H. serranus
complex)
H. prodromus
anatomy, 69, 70, 95
dentition, 26, 69, 70, 7I
distribution, 47
food: 20,3047, 60, 72
relationships, 18, 72, T00
H. prognathus, 34
anatomy, 84, 89
food, 30 (see H. prognathus complex), 80
relationships, 89, roo (see H. prognathus
complex)
H. pseudopellegrini, 87
anatomy, 89
food, 30 (see H. prognathus complex), 80
relationships, 89, roo (see H. prognathus
complex)
H. vriponianus, 52,73 .
anatomy, 59, 62, 74, 75, 97
dentition, 75
toed, 30, 373.74
relationships, 59, 75, 97, I00
H. sauvaget, 37
anatomy, 69-71, 107
coloration, 54
dentition, 70
distribution, 47
L005. 30) 47,09, 72
relationships, 72, 100
H. saxicola, 22, 93
anatomy, 59, 62, 82, 96, 97

dentition, 59, 61, 62
food, 30, 59
relationships, 59, 63, 82, 93, 96, 97, 00
H. sevrvanus, 34
anatomy, SI, 97
food, 30 (see H. servranus complex), 80
relationships, 84, 97, roo (see H. sevvanus
complex)
I. spekit, 23, 34
anatomy, 84
food, 3o (see H. serrvanus complex), 80
relationships, 84, roo (see H. servanus
complex)
H. squamulatus, 83
anatomy, S71, 85, 96
coloration, 52, 85
dentition, 85
food, 85
relationships, 85, 96, roo
H. theliodon
anatomy, 75
food, 37, 74
relationships, 75
AH. thuragnathus
anatomy, 84
food, 30 (see H. seyranus complex), 80
relationships, 84, roo (see H. sevvanus
complex)
AH. tridens
anatomy, 68
dentition, 26, 68
distribution, 117
food, 30, 39, 67
relationships, 68, roo (see H. tridens
complex)
H. tyrianthinus, 40
anatomy, 67, 68
dentition, 68
food, 67
relationships, 68, roo (see H. tridens
complex)
H. vanderhorstt
relationship with A statoreochromis alluaudi,
100
H. victorianus
anatomy, 84
food, 30 (see H. seyranus complex)
relationships, 84, roo (see H. sevvanus
complex)
H. welcommei, 22, 28
anatomy, 69
dentition, 25, 26, 69
distribution, 43
food, 30, 41, 43

134 P. H. GREENWOOD

relationships, 69, 100
supralimital specialization, 122

H. wingatii, 20

H. xenognathus, 28, 38
anatomy, 69, 70, 71, 95
dentition, 26, 69, 70, 7I
distribution, 47
food, 26) 30; 09). 72
relationships, 72, 100
supralimital specialization, 122

H. xenostoma, 87
anatomy, 84
food, 30 (see H. prognathus complex), 80
relationships, 89, roo (see H. prognathus

complex)

Hawaiian honeycreepers (Drepaniidae) com-
pared with Lake Victoria Haplochromis
spp., 120-121

Hemthaplochromis multicolor, 11, 14, 119

Hoplotilapia vetrodens, 13, 99, IOI, 121, 122
anatomy, I02, 103, 104
breeding, 19
coloration, 53, 54
dentition, 26, 102, 103
distribution, 49
food, 18, 37
relationships, 18, 99 et seq.

Hydrocynus, 117, 119

jaw mechanism in Haplochromis, 104-106
Kioga, Lake, 5, 10

Labeo, 115

L. victovianus, 45
Lanao, Lake, 121
TALES, ULL geL 7 LO

Macropleurodus bicolor, 13, 22, 99, 121, 122
anatomy, 71, 95, 104
breeding, 19
coloration, 53, 54
dentition, 26, 71, 102
distribution, 47
food, 18, 37; 71
relationships, 18, 71, 99 et seq.

Malawi, Lake, 4, 6 (age of), 7, 9, 14, 16-21,
24, 27, 30, 41, 43, 44, 48, 50, 55, 57, 99,
109, 113, 116 (speciation compared with
Lake Victoria), 120-123

Mbuna, 6
Mormyridae, I1I, I15
Mormyrus kannume, 12, 45

Nabugabo, Lake; 5, 16, 18, 10, 1123 Ata
Opinicon, Lake, 43, 44

‘pavaguiavw’ subgroup, 89, 97
Paralabidochromis victoriae, 14
anatomy, 100
breeding, 19
dentition, 100
food, 18
relationships, 18, 100
Perca fluviatilis ; jaws compared with Haplo-
chromis, T05
Platytaeniodus degeni, 14, 99, I00, 121, 122
anatomy, 103, 104
breeding, 19
dentition, 26, TOT, 103
food), 19) 37
relationships, 18, 99 et seq.
polychromatism, sex limited, 52, 53-55
‘brognathus’ lineage ; complex, 85 ef seq. ; 93,
97, 98
‘brognathus’ subgroup, 89, 98
Protopterus aethiopicus, 11, 12, 45

relative growth, in evolution, 106-I09
Rudolf, Lake, 5, © (age of), 117

speciation, rates of, 112, 114, 119
species group, 50-57

supralimital specialization, 121-123
Synodontis victoriae, 12, 45

Tanganyika, Lake, 3, 5, 6 (age of), 7, 9, 14,
17; 21, 41,-57, 99, 100, E13, 117, 220 ee
Tilapia, 6, 15-17, 31
T. esculenta, 13, 15, 45
T. nilotica, 16
I. variabilis, 13, 15, 45
tilapiine lineage, 17, 20
Miticaca awakes a27

Utaka, 50

Xenoclarias, 12

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A LIST OF SUPPLEMENTS _
TO THE ZOOLOGICAL SERIES
OF THE BULLETIN OF
THE BRITISH MUSEUM (NATURAL HISTORY)

Kay, E. Arison. Marine Molluscs in the Cuming Collection British Museum
(Natural History) described by William Harper Pease. Pp. 96; 14 Plates.
1905. (Out of Pant.) .{375-

WHITEHEAD, P. J. P. The Clupeoid Fishes described by Lacepéde, Cuvier and
Valenciennes. Pp. 180; 11 Plates, 15 Text-figures. 1967. £4.

TAYLOR, J. D., Peete oe W. J. & Hatt, A. The Shell Structure and Mineralogy
of the Bivalvia. Introduction. Nuculacea-Trigonacea. Pp.125; 29 Plates
77 Text-figures. 1969. £4.50. 7

Haynes, J. R. Cardigan Bay Recent Foraminifera (Cruises of the R.V. Antur)
1962-1964. Pp. 245; 33 Plates, 47 Text-figures. 1973. {10.80.
WHITEHEAD, P. P:; J. The Clupeoid Fishes of the Guianas, 22p; 227;
72 Text-figures. 1973. £9.70.

Printed in Great Britain by John Wright and Sons Ltd. at The Stonebridge Press, Bristol BS4 s5NU

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