Fisheries and cichlid evolution in the African Great Lakes: progress

Transcription

131
Article
Fisheries and cichlid evolution in the African Great
Lakes: progress and problems
Rosemary Lowe-McConnell
St George’s Park, Burgess Hill, Sussex RH15 0SG, UK. Email: [email protected]
Received 22 May 2009; accepted 25 September 2009; published 16 November 2009
Abstract
This paper updates Recent Advances in the African Great Lakes: Fisheries, Biodiversity and Cichlid
Evolution published by the Freshwater Biological Association in Freshwater Forum (LoweMcConnell, 2003).
Since 2003 many international teams have continued research on lakes
Malawi, Victoria and Tanganyika. This review discusses the decline of the important commercial
fisheries in all three lakes, together with changes in ecological and limnological conditions
which the fishes now face.
It also describes advances in our understanding of how the
spectacular flocks of endemic cichlid species have evolved in each lake and continue to coexist.
Keywords: African lakes; cichlid evolution; cichlid ecology; fisheries; Lake Victoria; Lake Malawi; Lake
Tanganyika.
Introduction
obtain funds for projects on lakes Malawi, Tanganyika
and Victoria. These lakes were all facing serious threats
The East African Great Lakes have long been renowned for
caused by the rapid rise in human populations, with
fisheries of vital importance for the rapidly rising riparian
associated over-fishing, sedimentation, and pollution from
human populations and as biodiversity hotspots with
changes in land use in the lake basins. Since the early 1990s
spectacular endemic faunas. The flocks of cichlid fishes
research involving over a hundred scientists, financed
unique to each of the three largest lakes, Victoria (69 000
by many international bodies, has produced numerous
km ) and the long deep rift-valley lakes, Tanganyika and
publications in widely-scattered journals. In 2003, the
Malawi (previously Nyasa) (Fig. 1), have offered unique
Freshwater Biological Association published a Special
opportunities to investigate how new species evolve and
Issue of Freshwater Forum on Recent Advances in the African
coexist (as discussed by Lowe-McConnell, 1993, 1996).
Great Lakes: Fisheries, Biodiversity and Cichlid Evolution
In 1989, an International Symposium on ‘Resource Use
(Lowe-McConnell, 2003). This synopsis summarised the
and Conservation of the African Great Lakes’ was held at
status of the fisheries and the then current ideas on how
Bujumbura on Lake Tanganyika, followed by numerous
the rich endemic fish faunas had evolved. It also described
workshops at other venues. Further international interest
the biodiversity surveys made in each lake based on
in biodiversity, generated at the Rio Earth Summit in 1992,
underwater (SCUBA) observations of fish ecology and
then enabled the United Nations and other agencies to
behaviour, followed by cichlid breeding experiments in
2
DOI: 10.1608/FRJ-2.2.2
Freshwater Reviews (2009) 2, pp. 131-151
© Freshwater Biological Association 2009
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Lowe-McConnell, R.
Fig. 1. The East African Great Lakes: Lake Victoria drains via Lake Kyoga and Lake Albert to the Nile, Lake Tanganyika to the Congo
system (Zaire) and Lake Malawi to the Zambezi River. Figure originally from Lowe-McConnell, R. 1996. Fish communities in the African
Great Lakes. Environmental Biology of Fishes, 45: 219-235. Reproduced with kind permission of Springer Science and Business Media.
aquaria and DNA techniques in many laboratories to test
ideas on the evolution, origins and relationships of the
Fisheries
cichlid species. New publications since 2003 have further
advanced our understanding of how the spectacular
Lake Malawi fisheries
flocks of cichlid species have evolved and coexist in lakes
Victoria and Malawi, but the main commercial fisheries
Sixty years ago the first fishery survey of Lake Nyasa (now
of these lakes, so needed to feed the rapidly rising human
L. Malawi) showed that the main commercial fisheries
populations, have declined. The present review describes
were supported by cichlid tilapia caught in shore seines
the most outstanding contributions on both these topics
and open water ring nets (Bertram et al., 1942). Since
published from 2003 to 2009.
then, however, tilapia abundances have declined and the
DOI: 10.1608/FRJ-2.2.2
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Fisheries and cichlid evolution in the African Great Lakes
species of endemic tilapia are now so scarce that the main
could adversely affect Malawi’s endemic fishes, as it did
commercial fishery (Maldeco, which works in association
when introduced into Madagascar (Reinthal et al., 2003).
with the Malawi Fishery Department) has resorted to
Research into environmental conditions affecting fish
breeding tilapia in fish-farm ponds to stock large enclosures
production in Lake Malawi has included, for example,
fixed in open waters in the south east arm of the lake.
the work by Duponchelle et al. (2005) on food partitioning
Here they rear endemic tilapia (Oreochromis shiranus and
within the species-rich benthic fish community. Using a
‘chambo’ O. karongae) but the endemic, more open-water-
combination of stable isotopes and stomach analyses, they
dwelling O. lidole, once so abundant in ring net catches, has
found that, although benthic algal production contributed
been over fished to such an extent that it has now vanished
to the energy requirements of offshore fishes living in
and is ‘probably extinct’ (Turner, personal communication).
water 10 m to 30 m deep, the larvae of the abundant lake
Maldeco, which produces 70 % of Malawi’s total fish catch,
fly Chaoborus edulis were the most important food source
no longer targets tilapia (the most popular fish) which was
for demersal fishes, thus supporting the hypothesis
reported in 2005 to be at the ‘lowest point ever’. Artisanal
that demersal fish production in L. Malawi is sustained
fisheries for cichlids and other fishes continue elsewhere on
mainly through the pelagic food chain, rather than from
this 600 km long lake, from which total catches are reported
benthic detritus.
by the Malawi Fisheries Department to fluctuate between
with apparently similar diets, feeding behaviour and
26 000 and 47 000 tonnes annually. To augment the fish
depth preferences, suggested that important resource
supplies Maldeco uses three bottom trawlers which catch
partitioning does exist among L. Malawi’s benthic
mainly very numerous small haplochromine cichlid species,
haplochromine cichlids. A Special Issue of the Journal of
including ndunduma Diplotaxodon of several species,
Great Lakes Research on The African Great Lakes (eds Bootsma
discovered during the UK/SADC Pelagic Zone survey in
et al., 2003), has an introductory paper by Bootsma &
1995. Small cichlid species now contribute between 60 %
Hecky (2003) comparing the biology and limnology of
and 70 % of Maldeco’s annual catch, of which 90 % is sold
the African Great Lakes. Twelve of the other very diverse
fresh (frozen); Maldeco also has a fish processing plant and
papers were based on data from L. Malawi. These, in
smoke kiln for fillets of any large fish they catch, especially
addition to discussing seasonal and spatial patterns of
catfish Bagrus meridionalis. To help meet the country’s large
experimental trawl catches (Deponchelle et al., 2003)
demand for fish, they have acquired another landing site at
and the return to local fisheries management (Dobson &
Salima on the main lake, for which a fourth fishing vessel is
Lynch, 2003), included other observations by numerous
on order (Press Corporation Ltd, 2009).
authors on meteorology, nutrient upwelling, sources
Isotopic differences among species
Fish from smaller lakes in Malawi, and from pond
and fluxes of organic carbon, silica cycling, community
culture, also contribute to the country’s total catch. The
composition, distribution and nutrient status of epilithic
WorldFish Centre, based in the Philippines, has assisted
periphyton in the rocky littoral, environmental factors
Malawian farmers to grow tilapia in rain-fed ponds for
controlling the distributions of benthic invertebrates on
which new varieties of tilapia are being selected for fast
rocky shores, and nitrogen and phosphorus regeneration
growth. Commendably, Malawi does not stock exotic fish,
by cichlids in the littoral zone. In a paper on the impact
which can so easily escape to the detriment of indigenous
of land use on sediments and nutrients, Hecky et al.
The very vigorous Nile tilapia (O. niloticus),
(2003) showed that changes in land use in the L. Malawi
cultivated in many ponds worldwide, when introduced into
basin, with its rapidly increasing human population and
Lake Victoria ousted the endemic tilapia (as described later).
associated agricultural development and forest clearance,
This aggressive species has now spread in southern Africa,
probably increased nutrient loading to the lake by 50 %.
species.
including Lake Kariba from where it has replaced Zambezi
tilapias (Tweddle, 2007). This very dominant tilapia species
DOI: 10.1608/FRJ-2.2.2
Responses
to
nutrient-enrichment
experiments
(with P, N and Fe) demonstrated that, in adequate light,
134
Lowe-McConnell, R.
nutrient-deficient.
O. niloticus thrived despite the presence of this predatory
Enrichment experiments with and without zooplankton
centropomid (now Latidae) that was introduced into the
(> 50 µm) by Guildford et al. (2003) in Lake Malawi
Ugandan waters of the lake in the mid 1950s as a ‘sport’ fish
(during three seasons – stratified rainy, deep mixing and
and to crop the numerous small haplochromine species.
phytoplankton
quickly
become
stratified dry) demonstrated that, when light is adequate,
phytoplankton in containers quickly become nutrient-
The rise and fall of Nile perch populations
deficient. When Fe was added with N and P, the response
The HEST (Haplochromis Ecology Survey Team)
measured as chlorophyll was four times the response
team from Leiden University, which has reviewed the
without Fe. Light was a factor controlling phytoplankton
chronology and causes of the Nile perch invasion in Lake
growth in situ during the deep mixing season. Grazer
Victoria (Goudswaard et al., 2008) record how Nile perch
experiments demonstrated that zooplankton (> 50 µm)
were unofficially introduced into Ugandan waters of Lake
are important in modifying the response of algae to
Victoria in August 1954 by the Game & Fisheries Department
light and nutrients. In Lake Victoria, experiments had
(Amaras, 1986). This followed the Department’s pre-1960
demonstrated
primarily
introduction of Nile perch into Lake Kyoga, into which
limited during the early stratified season; increased
L. Victoria flows (Kinlock, 1972; Jackson, 2000; Pringle,
light levels resulted in N deficiency. The addition of Fe
2005). In May 1960, fishermen reported the first Nile perch
stimulated N uptake in both lakes Victoria and Malawi.
from gillnet catches near Jinja; seven others caught near
that
phytoplankton
were
there in the same year were subadults of 28 cm to 43 cm in
Lake Victoria: the present state of the
length. Several years later Nile perch were caught in Kenya,
fisheries
then in low densities lake-wide in 1969–1970. In Tanzanian
waters large numbers of sub-adults and adults appeared in
1983, while juveniles were first seen there in 1985.
Tilapia in Lake Victoria
In Lake Victoria the endemic tilapia (O. esculentus and
Catches of haplochromines in trawl nets had started
O. variabilis), here caught mainly by gillnets, were also the
to decline shortly after the onset of the commercial trawl
basis for the first commercial fisheries. Tilapia catches
fishery, reputedly due to intensive fishing, but their
declined as fishing effort intensified in the three riparian
final disappearance occurred after the Nile perch boom
countries (Kenya, Uganda and Tanzania) as the human
and despite the abandonment of the commercial trawl
population increased. In the mid-1950s, in an attempt to
fishery in 1986. HEST also suggested that this decline of
boost catches, Tilapia zillii, a macrophyte-feeding species,
the haplochromines (which included loss of the large,
was introduced from Lake Albert in western Uganda. As
predatory species) had, by decreasing predation on, and
an inshore dweller it was thought that this species would
competition with, juvenile Nile perch, paved the way for
not interfere with the endemic tilapias and would help to
the successful reproduction of those Nile perch that had
clear swamps. However, with it came O. leucostictus and
immigrated. Perhaps over-exploitation of haplochromine
Nile tilapia O. niloticus (Lowe-McConnell, 1990, 2006). The
cichlids in the 1970s in the Nyanza Gulf in Kenya might
latter, introduced from other Ugandan lakes, has now
have played a similar role. Once their densities were high,
replaced (possibly with some hybridisation) the endemic
pioneering sub-adult Nile perch might have effected a
O. esculentus; O. variabilis is now rare in catches from the
change in the species composition by the eradication
lake (probably affected by the introduction of T. zillii).
of haplochromines in favour of juvenile Nile perch.
The smaller O. leucostictus, found in swampy places, are
commercially unimportant.
Nile perch had also been introduced earlier into
Goudswaard et al. (2002)
Lake Kyoga, into which Lake Victoria drains before it
reviewed the status of the tilapiine fish stock before and after the
continues over the barrier of the Murchison Falls into
upsurge of Nile perch (Lates niloticus) in Lake Victoria, where
Lake Albert. Lake Kyoga had a Nile perch boom about
DOI: 10.1608/FRJ-2.2.2
135
a decade earlier than L. Victoria, when the total fish
countries. Catch statistics indicate that fish landings of
yield increased from 18 000 tonnes in 1964 to 167 000 t
ca. 100 000 t per year rose to ca. 500 000 t annually in the
in 1978, largely due to a rise in Nile perch catches from
early 1990s, just after the Nile perch boom when this species
700 to 71 000 t. This was followed by a fall in Nile perch
formed more than 70 % of the catch. During the 1990s the
catches to 15 000 t in 1989. By 2006, L. Kyoga’s estimated
establishment of so many processing plants around the
total catch of 34 700 t consisted of 15 % Nile perch, 44 %
lake led to a depletion of Nile perch catches through over
Rastrineobola argentea, 28 % the introduced O. niloticus,
fishing. The factories now have a total capacity of 420 t per
together with native lungfish Protopterus aethiopicus, some
day, but many operate well below capacity. In 2003 the
haplochromines, and catfishes Clarias gariepinus and
estimated catch was worth at least US$ 540 million at the
Bagrus docmac. The haplochromine species that had almost
fish landings, plus a large sum earned by fish exports from
disappeared showed signs of recovery (Witte et al., 2009).
each of the three countries, and over a million people were
Lakes George and Edward, in western Uganda, once
directly or indirectly dependent on the lake fishery.
had one of the most productive fisheries for indigenous
To gather information on the fish stocks, the ecology
O. niloticus, the main commercial fishery for Nile tilapia
of the commercial species, and social and economic
supporting the TUFMAC fish factory on L. George, with
aspects of management – all necessary for the fisheries to
catches fluctuating around 2700 t a year. This had to close
be sustainable – a Lake Victoria Fisheries Research Project
in the late 1970s due to the decline in size of tilapia caught,
(LVFRP) was set up. This worked in close association
together with political difficulties affecting transport and
with Uganda’s Freshwater Resources Research Institute
increased poaching, which all exacerbated the decline
(formerly EAFFRO (East African Freshwater Fisheries
of this once very profitable fishery (Lowe-McConnell,
Research Organisation); Lowe-McConnell, 2003), based
2006). Nile perch are absent from the L. George fish
in Jinja. The LVFRP – a consortium of the Hull (UK)
fauna so were not responsible for the decline in catches
International Fisheries Institute in collaboration with the
there. In the 1990s lakes George and Edward produced
Fishery Research Institutes of Uganda, Kenya and Tanzania
over 11 000 t of fish a year for Uganda, but catches now
and a renewed Lake Victoria Fisheries Organisation – was
have a much smaller proportion of O. niloticus together
also based in Jinja. The stock assessment from 1997–2001
with catfishes and lungfish (Protopterus).
These lakes
for Tanzanian waters, with comparative references for
ultimately flow into Lake Albert, via the Semliki River,
Ugandan and Kenyan waters (Mkumbo et al., 2007), linked
whose indigenous Nile perch are part of its nilotic fish
both fisheries-independent data from bottom trawl surveys,
fauna and where very few haplochromine species have
and fisheries-dependent data to growth, mortality and
evolved (see Lowe-McConnell, 1987). Commercial catches
reproductive characteristics of the stock. The 2000 frame
from L. Albert are mainly of large characins and catfishes.
survey had revealed an intensive fishing effort and the Nile
perch fishery was found to depend largely on juvenile fish;
The Lake Victoria Fisheries Research Project
(LVFRP)
male Nile perch first matured at 54 cm total length (TL) (1.6
HEST’s routine trawl samples had shown that as the Nile
80 % of the commercial catch was below the maturation
perch population erupted ca. 200 endemic haplochromine
size for males and 99 % below that for females. Bottom
species vanished from the Tanzanian waters of Lake Victoria
trawl data (88 % juveniles) suggested good recruitment
(as discussed later), a loss of biodiversity that horrified
to the stock, but modelling of yield per recruit indicated
biologists internationally. But, in time and with factories
unsustainable tendencies. From LVFRP studies the annual
set up to purchase and freeze fillets, the originally despised
yield was estimated to be 138 324 t, well above the estimated
Nile perch became the most important commercial fish,
sustainable level of 109 000 t. They therefore recommended
supporting a valuable export trade from all three riparian
that the exploitation rate should be reduced by 50 %, and
DOI: 10.1608/FRJ-2.2.2
years old) and the females at 76 cm TL (2.5 years old). Over
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Lowe-McConnell, R.
for Nile perch the size at first capture should be increased.
in algal biomass. After re-examining the LVFRP stock-
Co-management was considered to be the most effective
assessments (all based on classical steady-state models)
option to implement monitoring, control and surveillance.
this team concluded that claims of over fishing of the
A management plan was set up to harmonise fishery
lake are not valid, as fish biomass, catch rates and size
policies in the three riparian countries. This adopted
structures have remained stable over the last 30 years.
lake-wide regulations and a co-management approach,
The resilience of the lake’s fish stocks as a whole could
with 160 Beach Management Units (BMUs) arranged on
only be explained by intensified biological productivity
fish landing sites around the lake. The harmonised rules
due to eutrophication. Algal production in the lake has
included banning beach seines and bottom trawls, cast
been shown to be light-limited and an upper level of
nets, gill nets of mesh less than 130 mm (5 inches), and a
production has been reached, so there is a danger that the
slot size of 50 cm to 85 cm TL for Nile perch. Sadly (and
eutrophication process will reverse into an accelerated
perhaps understandably) some violence was reported
process of decay. The immediate threat to L. Victoria
from a few Ugandan beaches between the locally elected
is, in their view, not over fishing but eutrophication,
BMU officials and the fishermen whose gear they
and management should, therefore, be more concerned
confiscated (Cowx, personal communication).
Other
with controlling eutrophication than focusing on ‘illegal
LVFRP studies included a sociological investigation of
fishing practices that have no significant effect on fish
why hunger and malnutrition still exist among some of the
stocks’. As Turner (1996) had pointed out, the decision
lakeshore peoples despite income from the valuable Nile
on whether to manage lakes in a way which maximises
perch fishery. Geheb et al. (2007) found that the fishermen
yields (for local food) or profits is essentially political;
who receive the earnings from the Nile perch processing
fisheries based on large predators (such as Nile perch)
factories fail to pass them on to the women who are
may be more profitable in the short term, but those based
responsible for feeding their families, hence the increasing
on the smaller, short-lived species can give greater yields.
level of malnutrition observed in lakeside villages.
The small endemic pelagic cyprinid, dagaa (Rastrineobola
argentea) has become the second most important commercial
Limnological conditions affecting fisheries in
Lakes Victoria and Malawi
species in Lake Victoria since the decline of Nile perch,
The Special Issue on The African Great Lakes (eds Bootsma
so its biology and distribution in the lake was examined
et al., 2003) has, in addition to the papers on Lake Malawi
to formulate a rational exploitation and management plan
already discussed, several papers on Lake Victoria.
for this species. From five acoustic surveys made between
Stable isotope analyses of nitrogen and carbon values in
1999 and 2001, combined with bottom and pelagic frame
biota have proved a powerful tool with which to study
trawl surveys, the mean total biomass of R. argentea in the
trophic position and dietary sources of the L. Victoria
lake was estimated as 476 902 t, the majority of which was
fishes (Campbell et al., 2003a). Data on stable isotope
distributed in waters more than 40 m deep. The biomass
analyses of food web structure in fish diets, comparing
increased progressively over the survey period as Nile
those from Winam Gulf (Kenya) and Napolean Gulf
perch predation decreased (Tumwebaze et al., 2007).
(Uganda), illustrated a short food web with the top
But how reliable were the catch statistics? Another
predator, Nile perch, feeding on a restricted set of fish,
team (Kolding et al., 2008), in an attempt to understand
macroinvertebrates and their own juveniles. There was
feedbacks in the whole ecosystem, re-analysed fish catch
an increase in both N and C values with fish size, showing
records from Lake Victoria in relation to limnological
how piscivory increases and reliance on invertebrates
changes in the lake where the tripling of the human
decreases as Nile perch mature. Nile tilapia, in contrast,
populations had led to a doubling of nutrient input and
feed at lower trophic levels in littoral water. The small,
primary productivity, resulting in a 6- to 10-fold surge
pelagic cyprinid, Rastrineobola, and the haplochromine,
DOI: 10.1608/FRJ-2.2.2
137
Haplochromis laparograma had surprisingly high N values,
than in benthic species, and highest in the largest fish
not consistent with isotopic values of their assumed prey,
within each species. The Hg–nitrogen isotope relationship
probably reflecting other planktivore invertebrates in their
in L. Malawi food webs was comparable to those found
diets, such as lake flies (chironomids and chaoborids). The
in temperate and arctic lakes, suggesting that the Hg
basal stable isotope values were found to be different in the
accumulation in freshwater food webs is independent of
two gulfs, reflecting the different hydrological conditions
climate change and species composition. In L. Victoria,
– Winam (Nyanza) Gulf is a shallow, mesotrophic to
Campbell et al. (2003b) found total water mercury (THg)
eutrophic gulf nearly closed off from the main lake, while
concentrations ranged from 1.75 ng L-1 to 5.8 ng L-1, while
the Napolean Gulf is in the vicinity of the Buvuma Channel
methylmercury (MeHg) concentrations ranged from
leading from the main lake to the source of the Nile near
0.2-1 ng L-1. Concentrations of mercury in the water
Jinja. Despite the differences in overall values for N and C
were higher here than in temperate great lakes, but the
at the base of the food web, food web structures were very
top fish predator, Nile perch, had relatively low THg
similar in these two widely separated gulfs of L. Victoria
concentrations compared with temperate piscivorous fish.
which had different water qualities and anthropogenic
The water Hg concentrations were similar in Napoleon
impacts, demonstrating that food web studies in one gulf
(Uganda) and Winam (Kenya) Gulfs, but the THg
may be extrapolated to another. The freshwater shrimp
concentrations in their biota were significantly different,
Caridina nilotica, now present in nearly all habitats and
which may have been due to biogeochemical differences
eaten by most fish species, had a wide range of C values
in the two gulfs. Concentrations of THg in Nile perch
but low N values.
and Nile tilapia increased with total length of the fish in
Studies of pelagic biological nitrogen fixation in
both gulfs at the same rate of increase. The rates of THg
inshore and offshore waters of northern Lake Victoria
bioaccumulation for each food web were within the
showed that it was high (often more than 0.5 μg N per
range of those observed in temperate and tropical lakes
litre per hour), greatly exceeding estimates of atmospheric
elsewhere, suggesting that (as in L. Malawi) Hg
nitrogen and river input (Mugidde et al., 2003).
accumulates at a similar rate in diverse food webs
N-fixation increased with light availability and maximal
regardless of latitude and species composition. In the
rates occurred when the lake was thermally stratified and
Jinja area of L. Victoria, Ramlal et al. (2003) found mercury
mixing limited to a shallow layer at the surface. Algal
in muscle tissue of 2+ and 3+ year old Nile perch to be
biomass and N-fixation rates were lowest in July when
90–250 ng/g wet weight. Here the average total mercury
the lake was mixing more deeply. Nitrogen enrichment
in the water column was 7.5 ng Hg L-1, and the average
experiments demonstrated that phytoplankton was
concentration in the solid top 10 cm of sediments was
primarily limited during the early-stratification season;
220 ng Hg g-1 (close to that found in the Laurentian
increased light levels resulted in N-deficiency but Fe
Great Lakes). Methylmercury in surface water near a
additions stimulated N uptake (Guildford et al., 2003).
variety of wetland vegetation was low, with the possible
Little is known about the concentrations of mercury
exception of water collected near roots of water hyacinth
(Hg) and factors affecting this contaminant in tropical
(Eichhornia crassipes).
waters. Bootsma et al. (2003) includes three studies of
fish are within the accepted guidelines of the FAO (Food
mercury pollution and its transfer through the food
and Agriculture Organization of the United Nations)
webs: one from Lake Malawi, followed by two from Lake
and the World Health Organization, they advised that
Victoria. In L. Malawi in 1996 and 1997, Kidd et al. (2003)
monitoring of fish mercury levels should be continued
found that concentrations of Hg in fish and invertebrates
as the diet of the riparian peoples contains so much fish.
Although mercury levels in the
were generally low (2 to 200 ng/g wet weight). The
concentrations were considerably higher in pelagic fish
DOI: 10.1608/FRJ-2.2.2
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Lowe-McConnell, R.
pelagic fish catches, but concluded that, although surface
Lake Tanganyika fisheries
temperatures do indeed show warming trends, evidence
The deepest lake in the Rift Valley, Lake Tanganyika,
for decreased productivity is ambiguous and no overall
has a remarkably rich cichlid fauna at the generic level,
decline in fish catches has been documented. Total lake-
attributable to the steep rocky shores which shelter the
wide catches increased up to 1995 as regional declines
cichlid communities from four endemic species of Lates
in the industrial fishery have been compensated for by
and many other predators. The main commercial fishery
lake-wide increases in artisanal catches. Since the present
was an open water ring-net fishery for pelagic clupeids.
evidence is not sufficient to demonstrate the effects of
Burundi has provided one of the longest records of
climate change on fish stocks, this suggests intensification
catch statistics (1956–1992) for any tropical fishery, and
of the fishery has been the major factor in these changes.
these were analysed by van Zweiten et al. (2002). More
Plisnier et al. (2009) have examined fluctuations in
recently, data on wind patterns, evaporation and physical
abundance of the clupeid Stolothrissa tanganicae and of
variables affecting the L. Tanganyika fisheries have been
the pelagic Lates stappersii and found that these species
collected from several automatic sampling stations and
now fluctuate on considerably different time scales, with
meterological buoys on the lake. These have shown that
an inverse correlation between their abundances, which
nocturnal mixing in the south is more dependent on wind
had previously been attributed to the consequence of
forcing and evaporation, while heat loss from the surface
predator–prey relationships. Currently, however, the two
plays a more important role at the north end of the lake
species appear spatially segregated in the lake, S. tanganicae
(Verberg & Hecky, 2003). External nutrient sources for the
dominating in the north while L. stappersii is generally more
lake, assessed from the physico-chemical characteristics
abundant in the south, where it feeds mostly on shrimps,
of the three largest inflowing rivers (Rusizi, Malagarasi
not clupeids. The limnological factors associated with
and Lufubu), showed that the Rusizi provided the most
variability of these fish catches indicated that abundance
and Lufubu the least of total riverine nutrient inputs. Wet
of S. tanganicae was positively correlated with plankton
atmospheric deposition (rainfall) provided approximately
biomass, while for L. stappersii water transparency, depth
83 % of dissolved inorganic nitrogen, 37 % of total
of mixed layer and oxygenated water appeared to be the
phosphorus, 63 % of total dissolved phosphorus and 64 %
important drivers of its abundance. Alternating mixing
of soluble reactive phosphorus, but only 1 % of soluble
and stable states of the epilimnion, related to seasonal and
reactive silicate, the remaining load being derived from
internal wave variability, probably determine the short-term
riverine sources. External loading forms the main pathway
variability in abundance of both species. There was a close
for nutrients to enter the productive layers of the lake
relationship between phytoplankton blooms at the time of
during stratified periods (February to May) (Langenberg
trade wind changes and increased catches of S. tanganicae in
et al., 2003).
the south. The ‘anti-correlated’, alternating abundances of
Langenberg (2008), in a series of papers with full
S. tanganicae and L. stappersii probably reflect the underlying
bibliographies written for his PhD on the limnology of
fluctuations of the limnological environment, clearly
Lake Tanganyika, gives data on the limnological annual
showing that fisheries studies need to integrate limnological
cycle
fluctuations,
and planktonic monitoring in order to understand large
wind induced changes in the plankton community,
and complex ecosystems such as Lake Tanganyika.
carbon flows and trophic structure in the pelagic food
McIntyre et al. (2006), who studied the effects of nutrient
web, and whether climate change has had an impact
availability and grazers in the littoral zone of L. Tanganyika
on productivity.
He questioned whether increases in
near Kigoma during the dry seasons of 2001 and 2002,
regional temperatures, related to global climate change,
found that fish and other large grazers had much stronger
had resulted in a substantial decline in L. Tanganyika’s
effects on periphyton than did the nutrients, concluding
inferred
from
physico-chemical
DOI: 10.1608/FRJ-2.2.2
139
that littoral nutrient availability did influence periphyton
The clear warm waters of lakes Malawi and Tanganyika
productivity
predominated.
also attract aquarists, which has led to many colourful
but
top-down
control
Deep-drilled cores from Lake Tanganyika have been
publications (for example Brichard, 1978; Konings, 1995;
used by Tierney et al. (2008) to reconstruct precipitation
and other Tropical Fish Hobbyist publications). In the
and temperature variations during the last 60 000 years.
more turbid (and with a risk of bilharzia infection) waters
These cores showed that temperatures in L. Tanganyika
of L. Victoria, SCUBA was only used later, in clear water
follow Northern Hemisphere insolation. They indicated
around rocky islands at the south end of the lake, by HEST
that warming in SE Africa during the Last Glacial
teams from Leiden University.
Termination began to increase ca. 3000 years before
a whole new community of cichlids (locally known as
atmospheric carbon dioxide concentrations started to
mbipi), comparable with the mbuna rock cichlids of L.
increase. Hydrogen isotope data from two deep sediment
Malawi (Seehausen, 1996).
Here they discovered
cores also showed that this region experienced changes in
hydrology at the same time as orbital and millennial events
Lake Malawi cichlids
in the Northern Hemisphere monsoonal climate records.
This implies that precipitation in tropical SE Africa is more
Historically, sediments in deep cores and seismic records
strongly controlled by changes in Indian Ocean surface
have shown that extremely arid conditions existed in
temperatures than by the migration of the Intertropical
tropical Africa in several discrete episodes, resulting in
Convergence Zone. These influences from outside the
very low lake levels between 135 000 and 90 000 years
lake system on rainfall in the Tanganyika basin help to
ago. From well-dated paleoecological records Cohen et al.
explain the variance in pelagic fish catches found when
(2007) found that Lake Malawi (currently 706 m deep), was
the very long series of catch records from L. Tanganika
reduced to a ca.125 m deep, saline, alkaline, well mixed
pelagic fisheries was analysed by van Zweiten et al. (2002).
lake until aridity diminished after 95 000 years ago. Lake
levels then rose erratically and salinity/alkalinity declined,
Cichlid evolution
reaching near modern conditions after 60 000 years, i.e.
approximately 30 000 years ago. This record of lake levels
The classic taxonomic investigations of cichlid species flocks
and changing limnological conditions has provided a
in the African Great Lakes were based on collections at the
framework for interpreting the evolution of L. Malawi’s
British Museum Natural History (now the Natural History
fish and invertebrate species flocks. More than 500 species
Museum) (see Bertram et al., 1942 and Trewavas, 1983 for
of cichlid fish have evolved in L. Malawi within the last
Lake Malawi; Greenwood, 1974 for Lake Victoria), and at
million years, from only a few common ancestors. Their
Tervuren in Belgium (see Poll, 1956 for Lake Tanganyika
rapid diversification has been attributed to morphological
cichlids). When stationed at Nkata Bay on L. Malawi,
adaptation to use very diverse food sources, and to sexual
Fryer (1959) described the cichlid communities adapted
selection.
for life either on rocky or sandy shores, before the advent
Establishing relationships among these taxa using
of SCUBA permitted underwater observations of these
molecular methods had been frustrated by the persistence
communities by Ribbink and teams from the JLB Smith
of ancestral polymorphism within species. Albertson et
Institute, Grahamstown, South Africa (Ribbink et al., 1983;
al. (1999), however, averaged the evolutionary history
Lowe-McConnell, 1987). In L. Tanganyika, the ecology and
of thousands of genes among closely related Mbuna
behaviour of cichlids inhabiting rocky shores were studied
cichlids, to produce a dendrogram indicating that
over 20 years by teams of Japanese and African scientists
adaptive divergence in trophic morphology played an
organised by Prof. H. Kawanabe, of Kyoto University,
important role during the early history of the lake, but
Japan (see Kawanabe et al., 1997; Lowe-McConnell, 2003).
subsequent species diversity has arisen with little change
DOI: 10.1608/FRJ-2.2.2
140
Lowe-McConnell, R.
in trophic morphology. This suggested that other forces
to reduced predation pressure by Nile perch but also to
are responsible for the continued speciation of these fishes.
increasing eutrophication, leading to reduced oxygen in
Later, Albertson (2008) studied jaw morphology as a
the water (hypoxia) and loss of water clarity, which is so
predictor of feeding performance and habitat partitioning
important for breeding success in cichlids whose sexual
in six species of the rock-dwelling Tropheops species
behaviour is visually-orientated.
complex in L. Malawi. The conclusion was that, for these
In addition to studying ecological changes in the lake,
species, depth was a major axis of trophic niche partitioning
morphological and genetic changes in the species that
within this complex, and competition for trophic resources
recovered have been made by comparisons with material
(epilithic organisms) had led to habitat partitioning and the
from HEST’s earlier collections, housed at Naturalis
establishment and maintenance of the Tropheops species.
(National Museum of Natural History) in Leiden, where
George Turner and his team, now based at Bangor
more than 120 000 specimens of over 400 species from
University, UK, have continued studying sexual selection in
Lake Victoria are stored and information is now available
Lake Malawi cichlids. Their numerous recent publications
on a computerised catalogue.
include, for example, Genner et al. (1999) and Genner &
revealed changes in habitat, an increase in fecundity and,
Turner (2005) in which the mbuna cichlids of L. Malawi
most strikingly, changes in diet. Both zooplanktivores and
are used as a model for rapid speciation and adaptive
detritivores had switched to macro-invertebrates (as had
radiation. Barson et al. (2007) reported on the genetic
some non-cichlid species). Least affected have been the
architecture of colour differences between L. Malawi
rocky shore species living where they are protected from
cichlid species, while Genner et al. (2007a) have found
Nile perch predation. There has been a differential impact
reproductive isolation among deep water cichlid fishes of
on different trophic groups: large species like piscivores,
L. Malawi differing in monochromatic male breeding dress.
molluscivores and insectivores declined faster than
The recovering species
zooplanktivores and detritivores, and the latter now had
Cichlid speciation in Lake Victoria
many suspected hybrids. Was this because detritivores
spawn in more turbid areas? By 2001, the zooplanktivores
The haplochromine species flocks in Lake Victoria are
had reached their previous level of abundance but their
among the most striking examples of rapid evolution
diversity had declined from more than 12 species to only
known; ecologically they are as diverse as those that
three. Although four detritivorous species reappeared,
have evolved in the older lakes Malawi and Tanganyika.
they made up only 15 % of the number of individuals,
Trophic specialisation is the basis of their radiations in
while zooplanktivores made up more than 80 %. Currently,
L. Victoria and they have evolved into at least 16 trophic
zooplanktivore densities are higher than before the ecological
groups, with body form and teeth specialised for life such
changes, whereas those of detritivores are much lower.
as detritivores, zooplanktivores, insectivores, prawn-eaters,
When reconsidering these changes in cichlid diversity
molluscivores or piscivores (of which there are more than
and the reputedly ‘1ost’ species, the HEST team found that
100 species). The HEST team from Leiden University has
haplochromine abundance has increased since the decline
been monitoring these cichlids from their field station near
of the Nile perch in the late 1990s but the number of species
Mwanza for nearly thirty years. As populations of the
is lower and the trophic composition has changed. A few
introduced, predatory Nile perch have diminished, the
of the ‘lost’ species have been rediscovered in different
main excitement has been the reappearance of about 20 of
areas, but the sampling of many habitats during the
the 200 ‘lost’ haplochromine species, previously thought
past 18 years has yielded only a few of the 200 or more
to be possibly extinct. The Leiden team had a unique
species they estimated as being lost. The group’s work
opportunity to investigate how the resurgent species have
on these haplochromines has been summarised by Witte
adapted to the changed ecological conditions, not only
et al. (2007a, b), each paper having a good bibliography.
DOI: 10.1608/FRJ-2.2.2
141
Ecological adaptations in the recovering zooplanktivores
cones and increased size of the red/green sensitive double
have included increased fecundity, habitat extension and
cones. How have Lake Victoria’s haplochromine species
shifts to a more generalised diet, including larger and less
flocks evolved faster than any other known vertebrates?
evasive prey that can be obtained without good visibility.
Witte and colleagues, who looked at morphological
Trophic groups like prawn-eaters and parasite eaters were
changes in H. pyrrhocephalus, described how gill surface
absent, piscivores were rare and only a few large mollusc-
had increased by 64 % enhancing oxygen uptake. Head
crushing specimens were seen. The new data suggest
length and head volume had decreased in size, which may
that although Nile perch predation strongly reduced
enhance their ability to accelerate in sudden bursts to escape
haplochromine densities in general, eutrophication,
Nile perch (Chapman et al., 2008). Eye length also decreased
rather than Nile perch predation, has reduced the
which may have created a space for larger gills. Small eyes
species diversity, possibly by hybridisation and selective
generally reduce resolution. So this could be responsible
eradication of species that need clear, oxygen-rich water.
for the larger prey types in their diet. A marked increase
To find out how closely related species had responded
in the depth of muscle responsible for the biting force of
to environmental changes, the HEST team chose a pair of
the pharyngeal jaws is probably a response to the changed
species (Haplochromis heusinkveldi and H. pyrrhocephalus)
diet. These striking morphological changes had been made
which formerly had almost identical distribution and
over a time span of only two decades. Is it the combined
migration patterns and were equally abundant before the
results of phenotypic plasticity and genetic changes which
Nile perch boom. Why then had H. heusinkveldi vanished
have helped the recovery of this species (Witte et al., 2008)?
while H. pyrrhocephalus became the commonest species in
Chapman et al. (2008) tabulated studies providing
Mwanza Gulf? The team found differences in: a) the retinal
evidence for phenotypic, morphological and diet
structure of their eyes – H. pyrrhocephalus had eyes better
changes coincident with the Nile perch introduction
adapted to low-light conditions allowing it to breed under
in these haplochromines and other species in Lake
lower light conditions than H. heusinkveldi; b) ecological
Victoria.
differences in their diets – H. heusinkveldi used to include
Gnathonemus
phytoplankton in its diet; and c) in their spawning times
changes in gills, body shape and diet in Rastrineobola
– H. heusinkveldi had a spawning period limited to months
argentea, and diet in Oreochromis niloticus, Lates niloticus
with high water transparency whereas H. pyrrhocephalus
and the catfishes Bagrus docmak and Schilbe intermedius.
is less restricted. In another recovering zooplanktivore
The investigations of diet shifts, made by comparing
(H. tanaos), formerly restricted to shallow sandy bottoms
stomach contents of small benthivorous cichlids caught
but now found over mud, the eyes had adapted to the
before and after the ecological changes, showed that the
lower water clarity by a shift in retinal structure allowing
diet of these species had shifted from one dominated by
better usage of ambient light of longer wave lengths
detritus and phytoplankton (supplemented by small
(Witte et al., 2005). Analysis of Nile perch stomachs
quantities of midge larvae and zooplankton) to a diet of
since 2005 showed that small Nile perch were once again
larger-sized invertebrate prey. These species now had
feeding mainly on small haplochromines, whereas at the
a more carnivorous diet, and concomitantly the ratio of
beginning of the1990s they were eating mainly shrimps,
intestine length to fish length had decreased by 30 %. The
Rastrineobola and juvenile Nile perch (Katunzi et al., 2006).
stomach contents of the former detritivores, which now
When compared with HEST’s earlier material, some
have a diet very similar to that of the zooplanktivores,
species revealed morphological changes which seemed
contained midge larvae, shrimps, molluscs and a very
adaptive to the new environmental conditions, including
small amount of detritus and phytoplankton (Kishe-
increased gill area, changes in the feeding apparatus and
Machumu et al., 2008). Wanink had also found changes
changes to the eye retina, with a loss of blue-sensitive single
in gill structure and diet in the zooplantivorous pelagic
DOI: 10.1608/FRJ-2.2.2
These include gill size in the mormyrids
victoriae
and
Petrocephalus
catastoma,
142
Lowe-McConnell, R.
cyprinid Rastrineobola in these same waters. The multiple
mate choice which could exert diversifying (disruptive)
strategies used by Lake Victoria cichlids to cope with life-
sexual selection causing rapid speciation in these cichlids.
long hypoxia have been examined by Rutjes et al. (2007)
Seehausen (now at University of Bern and Eawag
who concluded that lifelong adaptation is mainly due to
(Swiss Federal Institute for Aquatic Science)) and 12 co-
improved oxygen transport within the blood system.
authors, in ground-breaking work combining many
Eutrophication has also led to much reduced
techniques (Seehausen et al., 2008), have now demonstrated
penetration of light into Lake Victoria.
This has
sensory-driven speciation within island populations of
influenced the strategies of the cichlids for foraging and
cichlid fish by identifying the ecological and molecular
for communication, including the visual signals used for
basis of divergent evolution in the cichlid visual system.
mate choice, as shown by HEST in an earlier study by
They have also demonstrated associated divergence in
Seehausen et al. (1997). The wave length of downward
male colouration and female preferences, and shown
transmission of light into water depends on the content
subsequent differentiation at neutral loci indicating
of dissolved and dispersed organic materials. In clear
reproductive isolation.
lakes (and oceans) light becomes bluer as path length
in several pairs of sympatric populations and species.
increases while, in water carrying green organic matter,
Variations in the slopes of the environmental gradients
light becomes greener and, with undecomposed products
explained variation in progress towards speciation, which
of plant and animal decay, light shifts to longer (red) wave
occurred on all but the steepest gradients. Thus they
lengths. Seehausen et al. (2003a) discussed the theoretical
have provided the most complete demonstration so far
effects of visual range on foraging, niche partitioning, and
of speciation through sensory drive without geographical
coexistence with predators; and the effects of colour vision
isolation.
on cichlid foraging, communication and coexistence. They
explanation for the collapse of cichlid fish species diversity
concluded that increased turbidity caused by increased
during the anthropogenic eutrophication of L. Victoria.
eutrophication (possibly in combination with the effect of
A masterly summary in graphical form puts together
visual range on selectivity of mate choice) might explain
data on ecological, phenotypic, genetic and behavioural
the rapid erosion of cichlid species richness in L. Victoria
differentiation between blue and red Pundamilia nuptial
in recent years. Using a transect of littoral research stations
phenotypes at five islands. This shows how adaptation of a
in the clear water off small rocky islands in southern
haplochromine’s eyes and colours to its visual environment
L. Victoria, they found that the number of coexisting
has biased cichlid females to mate with different males
cichlid species was positively correlated with the width
according to their colouration, a preference which can
of the light band. Furthermore, along this transect the
contribute to the formation of new species sympatrically.
The evidence was replicated
Their results also provide a mechanistic
proportion of putative hybrids between two sympatric
They have shown this by working with two species
species (Pundamilia pundamilia and P. nyererei) was inversely
(‘blue male’ Pundamilia pundamilia and ‘red male’ P.
correlated with light band width; and off very turbid or
nyererei) which typically have blue or red male spawning
very steep shores, which had a very narrow light spectrum,
colours respectively. These males were found to have a
each haplochromine genus was represented by just one
genetic variation for visual sensitivity to these colours; in
species, whereas there were up to six species per genus at
some populations females with blue-biased vision seem
locations with broad light spectra (Seehausen et al., 1997).
to mate only with blue males, red-biased females only
Associated breeding experiments in aquaria showed
with red males. The authors therefore suggested that
that with haplochromines exhibiting different coloured
barriers could arise within a population, so it does not, as
breeding males, females vary in their preferences for mates
some had previously thought, require a phase in which
of different colour variants, demonstrating a potential for
red and blue populations have evolved allopatrically.
Lake Victoria has diverse visual environments; in turbid
DOI: 10.1608/FRJ-2.2.2
143
water and on steep sites this spectral shift is rapid, on
therefore, may be an important agent of diversification
gently sloping beaches more gradual. Starting from the
previously neglected among studies of cichlid fishes.
shore and descending along the bottom, red becomes
The females of all these haplochromines are mouth
increasingly dominant in the visual spectrum. To find
brooders in which the female broods eggs in her
out what the fish see, the team identified genetic variables
mouth then guards the young after they hatch. Using
(alleles) in one of the opsin genes in eye tissue responsible
P. pundamilia and P. nyererei (caught from Mkobe Island)
for tuning the fish’s sensitivity to different colours. Then,
in cross-fostering experiments, Verzijden & ten Cate
by cultivating eye tissue genes in vitro, and measuring the
(2007) obtained evidence that learning in the form of
absorption properties of the resultant proteins, they found
sexual imprinting helps to maintain reproductive isolation
some variants red biased in their sensitivities, others blue
among closely related cichlid species. By swapping eggs
biased. In the lake the numbers of males with red, blue or
between the mouths of red and blue morph mothers
intermediate nuptial colours varied between populations.
they found that female fish raised by foster mothers
At Mkobe Island, where the spectral shift was neither
belonging to a different species from their genetic mothers,
very rapid nor very gradual, blue males were confined
preferred males of that different species. This suggests
to the shallows, red males to greater depths; at this site
that learning at a young age contributes to reproductive
the blue males carried the blue-biased opsin variant,
isolation in these cichlids, in addition to other mechanisms.
whereas most red males carried the red-biased variant.
Maan et al. (2008), from field observations of the
Colour morphs also showed differences in other genetic
colour polymorphic Neochromis omnicaeruleus in Lake
markers suggesting they are nascent species. At sites
Victoria, found that blotched fish incurred more predator
where the spectral shift was rapid, intermediate colour
attacks from wild birds.
forms were found and genetic differentiation was absent.
revealed behaviour differences between the sexes which
Red and blue colour morphs occur in other cichlids
Underwater observations
entailed an additional predator risk for males.
This
(Seehausen & Schluter, 2004) suggesting that colour
differential predation with regard to colour pattern
polymorphism may be very ancient and the red and
and sex may be another important selective force in the
blue-biased opsin alleles much older than in the species
evolution and maintenance of colour polymorphism.
studied here. This led Seehausen et al. (2008) to suggest
that one key to the spectacular species radiation of African
The origins and evolution of the cichlid
lake cichlids may be that they have inherited from distant
species flocks
ancestors a trove of genetic variation for sensory systems
and male signals, possibly contributed during an inferred
Where did these cichlid species flocks originate? In an
episode of interbreeding 20 000 years ago, and this
important paper, nine authors collated information on the
variation may be entrained again and again in speciation
origins of the Lake Victoria and Lake Malawi species flocks
events. Using a large dataset of the distributions and
from riverine haplochromines, using information based
nuptial colours of 52 cichlid species on 47 habitat islands
on phylogenetic analyses of polymorphism in nuclear
in Lake Victoria, Seehausen & Schluter (2004) tested
DNA (Seehausen et al., 2003b) which they contrasted with
their hypothesis that competition between males for
mitochondrial DNA data published previously (Meyer et
breeding sites promotes such colour diversification and,
al., 1996). The later analyses suggested that the species flock
thereby, speciation. The distribution of closely related
of the L. Victoria region is derived from a single ancestral
species over the habitat islands was determined by
species found in the rivers of East Africa and closely related
nuptial colouration and implied that selection of nuptial
to the ancestor of the L. Malawi flock. The L. Victoria flock
colouration is a sufficiently strong force to override other
contains ten times less mt DNA variation than the L. Malawi
effects of species distributions. Male to male competition,
flock. This is consistent with the current ages of the lakes,
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Lowe-McConnell, R.
for which molecular and geological evidence agrees that
The nuclear genetic data did not confirm strict
colonisation in L. Malawi occurred between 500 000 and
monophyly of either the Victoria or Malawi species flocks
2 million years ago, whereas geological and palaeolimno-
but raised the possibility that these flocks have arisen from
logical evidence has indicated that the L. Victoria basin is
hybrid swarms (Seehausen, 2004). The species flocks in lakes
ca. 400 000 years old, although the lake was dry for several
Victoria and Malawi have, it seems, evolved independently
thousand years and only refilled about 15 000 years ago.
and hence the extensive parallelisms in morphology
In a review of geophysical and paleoecological evidence
and evolution in some of their cichlid species probably
Stager & Johnson (2008) state that L. Victoria was at its
reflect true parallelism, similar to that shown between
lowest level between 14 000 and 18 000 years ago and
cichlid species endemic to lakes Tanganyika and Malawi.
dried out at least once during that time. They found no
How old are the cichlid radiations in the African
evidence of remnant ponds or marshes and concluded
Great Lakes? New dates for the lake radiations are given
that L. Victoria’s diverse biota must be reconciled with the
by Genner et al. (2007b) who report that phylogenetic
incontrovertible geophysical and paleoecological evidence
reconstructions are consistent with cichlid origins prior
of the ca.15 000 year age of this lake.
to Gondwana landmass fragmentation 121–165 million
Low genetic variation in the Lake Victoria flock had
years ago, considerably earlier than the first known cichlid
made it hard to understand how selection could have
fossils (Eocene). They found that accumulations of genetic
produced the large functional diversity observed in a time
diversity within the radiating lineages of lakes Malawi,
that translated into between 30 000 cichlid generations
Victoria, Barombi Mbo, and the Palaeolake Makgadikgadi,
for L. Victoria and 400 000 for the entire Victoria–Edward
began around, or after the time of, basin formation.
region. The nuclear markers used in the study by Seehausen
Calibrations suggest Lake Tanganyika was colonised
et al. (2003b), however, now showed unexpected genetic
independently by the major radiating cichlid tribes that
variation and a Congolese–Nilotic origin of the L. Victoria
thereafter began to accumulate genetic diversity (contrasting
cichlid species flock; it demonstrated that the Victoria–
with the widely accepted theory that diversification
Edward flock is derived from the morphologically and
into major lineages took place within the L. Tanganyika
ecologically diverse cichlid genus Thoracochromis from the
basin). Their evidence suggests that ancient lake habitats
Congo and the Nile, rather than from the phenotypically
have played a key role in generating and maintaining
conservative East African Astatotilapia (as formerly
diversity within radiating lineages, also that the lakes
believed). This result is not entirely surprising as rivers
have captured pre-existing cichlid diversity from multiple
feeding L. Victoria were tributaries of the Congo until the
sources from which adaptive radiations have evolved.
region west of the lake became elevated ca. 400 000 years ago
Lake Tanganyika contains the highest diversity of
and they subsequently became tributaries of the Nile. This
ancient cichlid lineages. Its basin is believed to have started
finding also implied that the ability to express much of the
to form around 20 million years ago, initially as extensive
morphological diversity found in the flock may far predate
swampland, attaining deep-lake conditions some 6–12
the origin of the lake. As the new data indicate, the nuclear
million years ago. Dates indicate ancestors of every major
diversity of the Victoria–Edward species flock is similar to
tribe entered the lake independently and that molecular
that of the Lake Malawi flock. This also indicates that its
diversity within some tribes began to accumulate around
genetic diversity is considerably older than the 15 000 years
the time of colonisation, or in two cases (Trematocarini and
since L. Victoria began to refill and, in the L. Victoria cichlid
Ectodini) possibly before colonisation. The Haplochromini
species, most of the variation was manifested in trans-
may have split into several lineages prior to the formation
species polymorphisms which also suggests very recent
of deep-water conditions. At least two haplochromine
cladogenesis from a genetically very diverse founder stock.
lineages colonised the basin independently prior to
rifting.
The first lineage, Pseudocrenilabrus, has one
DOI: 10.1608/FRJ-2.2.2
145
species in the catchment, the second contains Tropheini,
rates of speciation, whereas ca. 0.5 million years into a
a group endemic to the lake basin that has radiated into
radiation speciation becomes much less frequent. The
a large number of species/geographical races. The genus
numbers of species in a radiation increases with lake size,
Astatotilapia includes A. burtoni from an East African
supporting the prediction that species diversity increases
haplochromine mt DNA lineage and A. stappersii of the
with habitat heterogeneity, also with the opportunity for
Lake Victoria-region lineage, and may also be related
isolation by distance. Finally, the propensity to radiate
to some Lake Malawi species (Seehausen et al., 2003b).
within lakes is a derived property that evolved during
Within the Lake Malawi haplochromine radiation,
the evolutionary history of some African cichlids and
comprising 450–600 species in around 50 genera, the onset
does not coincide with the appearance of proposed
of accumulation of genetic diversity was dated to 4.63
key innovations in cichlid morphology and life history.
and 2.44 million years ago, estimates which support the
The cichlid fish of Lake Tanganyika also present a
hypothesis that the flock radiated within the timescale of
celebrated example of species diversification with a rich
the basin’s history. The rifting that formed L. Malawi is
literature. As population subdivision is likely to play an
now estimated to have begun 8.6 million years ago, with
important role, Wagner & McCune (2009) contrasted
deep-water conditions attained by 4.4 million years ago.
patterns of spatial structure in sympatric cichlid species
The age of the Lake Victoria region cichlid fishes is
living in a mosaic of rocky and sandy habitats north of
more controversial. Over 600 closely related cichlid species
Kigoma, to find out how habitat features interact with
comprise the East African ‘superflock’ inhabiting lakes
demographic, behavioural and ecological attributes to
Victoria, Kyoga, Rukwa, Kivu, Albert, George–Edward and
influence gene flow and population divergence. Using
surrounding water bodies. Within this superflock region,
multilocus microsatellite genotypes they contrasted
L. Victoria forms a phylogenetic zone largely distinct in
population differentiation in two species of Petrochromis
mt DNA from the western rift lakes Albert, George–Edward
and a Simochromis species and found that, despite their
and Kivu. Divergence within the L. Victoria catchment
close phylogenetic relationship and shared habitat affinity,
has been dated to between 120 000 and 89 000 years ago,
they showed striking differences in their patterns of
estimates that suggest diversity arose after the formation of
genetic subdivision within the same geographical region,
the L. Victoria catchment approximately 400 000 years ago.
indicating different patterns of gene flow. In particular, the
Seehausen (2006) reviewed the literature and identified
two trophically specialised Petrochromis species exhibited a
33 intralacustrine radiations and 76 failed radiations
much more restricted gene flow over sandy habitat than
which he then related to lake size, age, and phylogenetic
did the trophically opportunistic Simochromis species. This
relationships of the cichlids. In doing this, he addressed
shows how ecological and behaviour traits have a strong
two questions: (i) whether the rate of speciation and
influence on the scale and degree of population subdivision.
resulting species richness are related to temporal and
The ecological causes of evolutionary diversification
spatial variation in ecological opportunity (a key prediction
are a major focus of biology but little has been said about
of ecological theory but untested for cichlid radiations),
the effects of evolutionary diversity on ecosystems.
and (ii) whether the likelihood of undergoing adaptive
Studying the three-spined stickleback (Gasterosteus
radiations is similar for different African cichlid lineages
aculeatus), Harmon et al. (2009) have shown that adaptive
(as suggested in a former hypothesis that the propensity of
radiations, even over short timescales, can have profound
cichlids to radiate is due to a key evolutionary innovation
effects on ecosystems. This stickleback has, within the
shared by all African cichlids).
He found evidence
past 10 000 years, undergone parallel diversification in
suggesting that speciation rate declines as niches get
several lakes in coastal British Columbia, resulting in the
filled during adaptive radiations: young radiations and
formation of two specialised species (benthic and limnetic)
early stages of old radiations are characterised by high
from a generalised ancestor. Using mesocosm experiments
DOI: 10.1608/FRJ-2.2.2
146
Lowe-McConnell, R.
Harmon et al. have demonstrated that this diversification
unintentional experiment on a vast scale), whereas many
has strong effects on ecosystems, affecting prey community
cichlid species living on open sandy/muddy bottoms,
structure, total primary production and the nature of
where they lacked cover, vanished during the Nile perch
dissolved organic materials that regulate the spectral
boom.
properties of light transmission in the system. These
Forty years ago studies on the sympatric tilapia
effects all reflect the complex and indirect consequences of
species in Lake Nyasa (Malawi) where they are most
ecosystem engineering by sticklebacks. When commenting
readily distinguished by male nuptial colours, strongly
on this paper, Seehausen (2009) has stressed how their
suggested some form of sympatric speciation must be
evidence that speciation and adaptive radiation can change
involved. The idea of sympatric (as opposed to allopatric)
the properties of an ecosystem is a reminder of the pressing
speciation was then hotly contested (as discussed by
need to integrate ecosystem science and evolutionary
Lowe-McConnell, 1987, chapter 5) as no mechanism for
biology. He adds a warning that, with the rapid human-
this had then been determined. So recent demonstrations
induced collapse of species diversity in ecosystems
of speciation without geographical isolation for Lake
dominated by recent adaptive radiations, we should expect
Victoria’s haplochromine cichlids, together with news of
to see the collapse of nascent species diversity, leading to
further studies on other spectacular cichlid species flocks
severe perturbations in ecosystem functioning – a process
in both lakes Malawi and Tanganyika, is very gratifying.
that may already be underway in the African Great Lakes.
Research on these African Great Lakes has demonstrated
clearly how knowledge of their very complex fish
Concluding Remarks
communities (especially of cichlid fishes) has depended
on knowing what species of fish are present, the ecology
Seehausen (2007) discussed how chance, contingency and
and behaviour of individual species, and the limnological
historical determinism jointly determine the rate of adaptive
conditions governing their life cycles. Lake Victoria, the
radiation, pointing out that the two major phylogenetic
largest tropical lake in the world is now suffering from severe
lineages responsible for most of the adaptive radiations of
eutrophication and the probable loss of up to half of its 500+
cichlid fishes in African lakes – the three genera of tilapiines
species of endemic cichlid fishes. Eutrophication-induced
(Tilapia, Oreochromis, Sarotherodon) and the Astatotilapia-
loss of deep-water oxygen, which started in the early 1960s,
related haplochromines, widely distributed across African
may have contributed to the 1980s collapse of indigenous
lakes – often occur together but rarely radiate in the same
fish stocks by eliminating suitable habitats. The prime
lake.
This may imply possible suppression between
cause of this change has been the rapid and accelerating
unrelated cichlid lineages. In this paper he also referred to
rise in human populations of all three lake basins. In the
the 1960s dispute on the impact of predators on adaptive
L. Victoria basin this has grown from 4.6 million people
radiation in these cichlids, citing Lowe-McConnell (1993)
in 1932 to 27.7 million in 1995, and is predicted to double
who summarised this debate. Lowe-McConnell noted
to 53 million by the year 2020 (United Nations, 1995: see
that in Lake Tanganyika, the four endemic predatory
Verschuren et al., 2002). This rapid population growth,
Lates species quite probably inhibited speciation among
with immigration and improved health conditions, started
the openwater-living fishes, but could have promoted it
the pattern of large-scale deforestation and conversion to
among the rock-dwelling species for whom cover was
agriculture. Palaeolimnological data have now established
available, by increasing isolation between the various
a strong historical connection between land use and algal
populations. The discovery by Seehausen (1996) of a flock
production in L. Victoria, which indicates that landscape
of cichlids inhabiting the rocky shores in Lake Victoria has
disturbance, rather than (or combined with) food web
supported this idea as these species survived the impact of
alteration from introduced species or climate change,
the introduced Nile perch Lates (which had provided an
is the dominant cause of the ongoing eutrophication
DOI: 10.1608/FRJ-2.2.2
147
(Verschuren et al., 2002).
Further degradation of the
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Author Profile
The author prepared for African studies at the
Freshwater Biological Association, then directed by
Barton Worthington a pioneer in African lake fishery
surveys, and with Ethelwynn Trewavas at the British
Museum (Natural History) before undertaking a
fisheries survey of Lake Nyasa in 1945–47. She was
then based in Uganda from 1948–54 on the staff of the
East African Fisheries Research Organisation and from
1987 onwards visited these African lakes repeatedly
when she was Convenor of the African Lakes Group
of the International Limnological Society (SIL).
DOI: 10.1608/FRJ-2.2.2

Fisheries and cichlid evolution in the African Great Lakes: progress

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