Biology of the marbled lungfish, Protopterus aethiopicus Heckel, in Lake Baringo, Kenya

In this paper we provide life history characteristics for an introduced marbled lungfish (Protopterus aethiopicus) population in Lake Baringo, Kenya, including their length–weight relationship, body condition, fecundity, sex ratio, reproduction and food. These data are compared with those of other populations. Samples were obtained from the commercial fishery between January and October 2001. The lungfish exhibited positive allometric growth, with the length–weight relationship described by the equation: logW = ?6.41 + 3.52 logTL. The mean relative condition factor was close to unity, did not vary much between months and was not significantly different between sexes. The overall sex ratio was skewed in favour of females. The size of fish at first maturity was 70–76 cm total length (TL) for females and 82–88 cm TL for males. Fish in maturity stages III–IV occurred in all monthly samples suggesting year round spawning. The marbled lungfish in Lake Baringo is largely piscivorous and its impact on other fishes certainly warrants further research.     

Genetic variation in the marbled lungfish Protopterus aethiopicus in Lake Victoria and introduction to Lake Baringo, Kenya

Marbled lungfish Protopterus aethiopicus in Lake Victoria and two nearby smaller lakes were found to have high levels of DNA sequence variation in their mitochondrial control regions (35 haplotypes in 61 fish) but no population genetic structure (Φ_ST= 0·00). In contrast, marbled lungfish in Lake Baringo, Kenya, appeared to be fixed for a single control region haplotype, which occurred at low frequency in the other lakes. Using FLUCTUATE software, the female effective population size in Lake Victoria during the late Pleistocene was estimated to be c. 500 000, similar to the value estimated for the present-day population. These observations suggest that, during the late Pleistocene dry period, a large marbled lungfish population survived either in wet refugial areas within the lake basin or in surrounding areas. Marbled lungfish were reported to have been introduced into Lake Baringo 30 years ago with a founding population of only three individuals. The lack of control region variation in the Lake Baringo population is consistent with that situation.     

Movement and habitat use by the marbled lungfish Protopterus aethiopicus Heckel 1851 in Lake Baringo, Kenya

The marbled lungfish, Protopterus aethiopicus, a recent introduction into Lake Baringo, Kenya is now an important commercial species there. Because little is known about its behaviour, we used ultrasonic telemetry to investigate its movements and use of habitat as part of a broader biological study. Twelve marbled lungfish were implanted with ultrasonic tags and tracked for variable periods between September 2001 and 2002. Two individuals were tracked for most of the study period. Daily movement ranged from little or none to 5.2 km. Mean hourly rates of movement for three fish located twice a day (morning and late afternoon) over several days suggested that individuals were active throughout the diel period. Maximum lake depth was about 3 m and fish utilized all depths greater than 1 m. Six home ranges described for four lungfish varied in size from 5.8 to 19.8 km ² and were occupied for between 2 and 4.5 months. Use of habitat and the movement of marbled lungfish in Lake Baringo appeared to be influenced more by biotic than abiotic factors.     

Decline of the African lungfish (Protopterus aethiopicus) in Lake Victoria (East Africa)

Catch and effort data for the period 1973–1990 demonstrate a dramatic decline of lungfish in the Tanzanian waters of Lake Victoria. Bottom trawl catches in the Mwanza Gulf showed a decline in catch rates from 67.5 kg h⁻¹ in 1973 to 5.5 kg h⁻¹ in 1986. Trawling of commercial vessels in the Speke Gulf revealed a decline in lungfish catches from 1.3 kg h⁻¹ in 1986 to 0.07 kg h⁻¹ in 1990. The development of anoxia in the deeper waters of Lake Victoria, the algal blooms, and the decline of water transparency, all associated with eutrophication, are not likely to have contributed to the decreased catch rate. However, the lungfish decline may reflect the interaction of overexploitation by the fishery and a low level of Nile perch predation that restricts lungfish to wetland refugia. We suggest that this may have been reinforced over the past few decades by large-scale conversion of wetlands to agricultural land and harvesting of nest-guarding male lungfish leading to decreased recruitment of young.     

Reproductive biology of the East African lungfish (Protopterus aethiopicus) in Mwanza Gulf, Lake Victoria

The population of lungfish (Protopterus aethiopicus (Heckel)) was sampled by bottom trawling for 12 months from June 1984 to May 1985. A total of 576 lungfish were investigated. The sex ratio in the population was 1 male : 1 -98 females. Average size at maturity was found to be 960cm total length (TL) but the smallest matured male measured 72-9 cm and the female 840 cm TL. It was not possible to establish spawning times and reproductive activity trends either from the variation in relative condition factor ‘kn’ or from gonadosomatic index (GSI). Whereas male lungfish seem to show no further increase in GSI after gonadal maturity stage III, females exhibit GSI values that vary directly with oocyte maturation and ovarian weights. Fat deposited along the gonads was found to be a better basis for assessing maturation and spawning in lungfish. The potential spawning period was found to be from September to May. Absence of lungfish with spent gonads over the 12-month period and the presence of different egg sizes in ovaries, suggest that the fish is a multiple spawner. Fecundity was found to range from 705 eggs (in 84-cm TL fish) to 14,922 eggs (in 130-cm TL Fish).     

The morphology of the lung of the African lungfish,Protopterus aethiopicus

Summary The lung of the African lungfish (Protopterus aethiopicus) is paired, long and cylindrical. It is situated on the dorsal aspect of the coelomic cavity ventral to the ribs. Much of the gas exchange tissue is found in the proximal aspect of the lung with the caudal part largely taken up by a centrally situated air-duct with a few large peripherally located alveoli. Interalveolar septa, arranged at differing hierarchical levels from the air-duct, subdivide the lung into alveoli, the gas exchange compartments. The alveolar surface is covered by some cells characterized by microvilli on their free surface, while others are devoid of such structures. The general organization of the lung of Protopterus aethiopicus is similar to that of the other genera of Dipnoi, Neoceratodus and Lepidosiren, with the interalveolar septa increasing the surface area for gas exchange through pulmonary compartmentation. The abundant septal smooth muscle fibres and elastic tissue may contribute to the physiomechanical compliance of the lung. The undifferentiated alveolar pneumocytes and the double capillary system, observed in Protopterus, in general appear to characterize the very primitive lungs of the lower air-breathing vertebrates.     

Respiratory allocation and standard rate of metabolism in the African lungfish, Protopterus aethiopicus

This paper quantifies the relationship between respiratory allocation (air vs. water) and the standard rate of metabolism (SMR) in the primitive air-breathing lungfish, Protopterus aethiopicus. Simultaneous measurements of oxygen consumed from both air and water were made to determine the SMR at ecologically relevant aquatic oxygen levels for juveniles 2 to 221 g. Total metabolic rate was positively correlated with body mass with a scaling exponent of 0.78. Aerial oxygen consumption averaged 98% (range=94% to 100%) of total respiratory allocation under low aquatic oxygen levels. Measurements of oxygen consumption made across a gradient of dissolved oxygen from normoxia to anoxia showed that P. aethiopicus maintains its SMR despite a change in respiratory allocation between water and air.     

Ultrastructural study on nuclear-cytoplasmic relationships in oocytes of the African lungfish,Protopterus aethiopicus

Summary Growing oocytes of Protopterus, like those of some amphibians and teleosts, show an impressive development of the nucleolar apparatus. Numerous nucleolus-like bodies establish close spatial relationships with the nuclear envelope by extending pedicels and streams of finely dispersed material towards the inner membrane.At such contact points, gaps in the perinuclear cistern are more frequent than elsewhere along the nuclear boundary. Expansion of the outer nuclear membrane gives rise to blebs, with or without visible content, and these become pinched off to form small vesicles in the perinuclear cytoplasm.Small, electron dense aggregates, indistinguishable from nucleolar material occur on both sides of the nuclear envelope opposite to each other, some being connected by a slender portion of the same material within a nuclear pore. Such accumulations are interpreted as detached parts of nucleolar bodies in transit to cytoplasmic sites where they presumably participate in the biogenesis of ribosomes. At the height of nucleolar emission, nucleoplasm and perinuclear cytoplasm are so rich in small electron dense particles that they are almost indistinguishable from each other.At this stage of massive transport, the route provided by the nuclear pores seems to be insufficient and another, more spacious, gateway may be in operation. The latter involves direct passage of material across the nuclear membranes preferentially where these form blebs.This view is supported not only by the overt spatial relationships between nucleolar pedicels and blebs, but by the occurrence within perinuclear lacunae and blebs of particles that seem to be derived from nucleolar bodies. Furthermore, frequent interruptions in the nuclear membranes preferentially located where they expand into outpocketings suggest that at these sites temporary gateways may exist in the living cell that permit easy access of intranuclear components to the cytoplasm.Supported by grants AM-3984, NB-00840, and NB-05219 from the U.S.P.H.S.     

Assessing the true status of the fish species Labeo cylindricus (Peters 1868) (Teleostei: Cyprinidae) in Lake Baringo,Kenya

Eutrophication contributes to the proliferation of alien invasive weed species such as water hyacinth Eichhornia crassipes. Although the South American moth Niphograpta albiguttalis was released in South Africa in 1990 as a biological control agent against water hyacinth, no post-release evaluations have yet been conducted here. The impact of N. albiguttalis on water hyacinth growth was quantified under low-, medium- and high-nutrient concentrations in a greenhouse experiment. Niphograpta albiguttalis was damaging to water hyacinth in all three nutrient treatments, but significant damage in most plant parameters was found only under high-nutrient treatments. However, E. crassipes plants grown in high-nutrient water were healthier, and presumably had higher fitness, than plants not exposed to herbivory at lower-nutrient levels. Niphograpta albiguttalis is likely to be most damaging to water hyacinth in eutrophic water systems, but the damage will not result in acceptable levels of control because of the plant's high productivity under these conditions. Niphograpta albiguttalis is a suitable agent for controlling water hyacinth infestations in eutrophic water systems, but should be used in combination with other biological control agents and included in an integrated management plan also involving herbicidal control and water quality management.     

X-ray analysis coupled with scanning and transmission electron microscopic observations of spermatozoa of the African lungfish, Protopterus aethiopicus

Spermatozoa from the reproductive tubules and epididymis of the African lungfish, Protopterus aethiopicus , were examined by scanning, transmission and scanning-transmission electron microscopy. The biflagellate nature of lungfish spermatozoa was confirmed as a general rule by examining large numbers of specimens in the scanning mode. All have two flagella with attached undulating membranes, a short middle piece and a large sperm head without condensation of the nucleus. The various portions of the sperm have been subjected to analysis of the X-rays emitted upon electron bombardment, and the relative concentrations of several elements have been determined.     

Marbled lungfish growth rates in Lake Baringo, Kenya, estimated by mark‐recapture

Mark‐recapture was used to quantify the relationship between body mass ( M _T) and individual growth rates of sub‐adult marbled lungfish Protopterus aethiopicus in Lake Baringo, Kenya. Specific growth rate (in mass) was found to be a well defined and decreasing function of M _T over the size range of recaptured fish. Growth trajectories based on this function indicated that Lake Baringo African lungfish reached maturity at an age of c . 3 years and had a low reproductive effort.     

On the limnology of Lake Baringo (Kenya): II. Pelagic primary production and algal composition of Lake Baringo,Kenya

Sicilian reservoirs, a vital resource for this densely populated island, are undergoing increased eutrophication processes, due to the lack of urban waste treatment plants and to intense agriculture. Massive blooms of toxic cyanobacteria represent one of the most obvious consequences, and can be dangerous for population health. The possibility of a fast, even if only short term, recovery of water quality through application of lime, was tested through analysis of ion dynamics in two reservoirs, to develop an `emergency plan', to counteract cyanobacterial blooms and to decrease the risk for human health. The results indicate that these water bodies are suitable for lime treatments, even though the high content of sulphate and their managed hydrological cycles, have to be considered.     

Mitochondria-rich cells in gills and skin of an African lungfish, Protopterus annectens

We used scanning electron microscopy, the vital dye DASPEI and an antibody to the inner mitochondrial membrane to study the presence and localisation of mitochondria-rich cells in the gills and skin (opercular, dorsal and ventral) of the lungfish Protopterus annectens in its free-swimming conditions and at the beginning of aestivation. In the free-swimming period, the gills were short and thick and the pavement cells were extremely large (30-40 microns). The mitochondria-rich cells, which were distributed in the secondary and primary epithelium, occurred as two morphologically different types, i.e. elongated and oval, similar to the alpha and beta chloride cells of fresh water teleosts. In the skin, only one type of mitochondria-rich cells was found, resembling the alpha chloride cells. All the mitochondria-rich cells distributed in the gills and skin were labelled with anti Ca(2+)-ATPase serum indicating the possible uptake of Ca2+ at freshwater chloride cell level. At the start of aestivation, the skin and gills were covered by a thick layer of mucus and the epithelium of the gills was reduced. The mitochondria-rich cells were almost completely covered by the pavement cells.     

Trophic state and nutrient limitation in Lake Baringo,Kenya

The trophic state of Lake Baringo and factors that could be limiting the development of algal biomass in it were investigated during one wet/dry hydrological cycle in 2014–2015. Water samples were analysed for dissolved inorganic nutrients, including , and , total phosphorus and Chlorophyll a. Light attenuation was estimated using Secchi depth. The trophic state was determined using Carlson trophic state indices (CTSI). Deviations in CTSI, nutrient ratios and ambient nutrient concentrations were used to identify factors limiting phytoplankton growth. The mean values measured for Secchi depth, nitrate, total phosphorus and Chlorophyll a showed significant seasonal variation (p < 0.05). Based on the Carlson trophic state index, the results show that Lake Baringo is eutrophic. However, the lake is also experiencing phosphorus limitation and poor light penetration, because of high turbidity, which is more pronounced during the wet season.     

The African lungfish (Protopterus dolloi): ionoregulation and osmoregulation in a fish out of water

Although urea production and metabolism in lungfish have been thoroughly studied, we have little knowledge of how internal osmotic and electrolyte balance are controlled during estivation or in water. We tested the hypothesis that, compared with the body surface of teleosts, the slender African lungfish (Protopterus dolloi) body surface was relatively impermeable to water, Na(+), and Cl(-) due to its greatly reduced gills. Accordingly, we measured the tritiated water ((3)H-H(2)O) flux in P. dolloi in water and during air exposure. In water, (3)H-H(2)O efflux was comparable with the lowest measurements reported in freshwater teleosts, with a rate constant (K) of 17.6% body water h(-1). Unidirectional ion fluxes, measured using (22)Na(+) and (36)Cl(-), indicated that Na(+) and Cl(-) influx was more than 90% lower than values reported in most freshwater teleosts. During air exposure, a cocoon formed within 1 wk that completely covered the dorsolateral body surface. However, there were no disturbances to blood osmotic or ion (Na(+), Cl(-)) balance, despite seven- to eightfold increases in plasma urea after 20 wk. Up to 13-fold increases in muscle urea (on a dry-weight basis) were the likely explanation for the 56% increase in muscle water content observed after 20 wk of air exposure. The possibility that muscle acted as a "water reservoir" during air exposure was supported by the 20% decline in body mass observed during subsequent reimmersion in water. This decline in body mass was equivalent to 28 mL water in a 100-g animal and was very close to the calculated net water gain (approximately 32 mL) observed during the 20-wk period of air exposure. Tritiated water and unidirectional ion fluxes on air-exposed lungfish revealed that the majority of water and ion exchange was via the ventral body surface at rates that were initially similar to aquatic rates. The (3)H-H(2)O flux declined over time but increased upon reimmersion. We conclude that the slender lungfish body surface, including the gills, has relatively low permeability to water and ions but that the ventral surface is an important site of osmoregulation and ionoregulation. We further propose that an amphibian-like combination of ventral skin water and ion permeability, plus internal urea accumulation during air exposure, allows P. dolloi to extract water from its surroundings and to store water in the muscle when the water supply becomes limited.     

The interplay of increased urea synthesis and reduced ammonia production in the African lungfish Protopterus aethiopicus during 46 days of aestivation in a mucus cocoon

This study was undertaken to test the hypothesis that the rate of urea synthesis in Protopterus aethiopicus was up-regulated to detoxify ammonia during the initial phase of aestivation in air (day 1-day 12), and that a profound suppression of ammonia production occurred at a later phase of aestivation (day 35-day 46) which eliminated the need to sustain the increased rate of urea synthesis. Fasting apparently led to a greater rate of nitrogenous waste excretion in P. aethiopicus in water, which is an indication of increases in production of endogenous ammonia and urea probably as a result of increased proteolysis and amino acid catabolism for energy production. However, 46 days of fasting had no significant effects on the ammonia or urea contents in the muscle, liver, plasma and brain. In contrast, there were significant decreases in the muscle ammonia content in fish after 12, 34 or 46 days of aestivation in air when compared with fish fasting in water. Ammonia was apparently detoxified to urea because urea contents in the muscle, liver, plasma and brain of P. aethiopicus aestivated for 12, 34 or 46 days were significantly greater than the corresponding fasting control; the greatest increases in urea contents occurred during the initial 12 days. There were also significant increases in activities of some of the hepatic ornithine-urea cycle enzymes from fish aestivated for 12 or 46 days. Therefore, contrary to a previous report on P. aethiopicus, our results demonstrated an increase in the estimated rate of urea synthesis (2.8-fold greater than the day 0 fish) in this lungfish during the initial 12 days of aestivation. However, the estimated rate of urea synthesis decreased significantly during the next 34 days. Between day 35 and day 46 (12 days), urea synthesis apparently decreased to 42% of the day 0 control value, and this is the first report of such a phenomenon in African lungfish undergoing aestivation. On the other hand, the estimated rate of ammonia production in P. aethiopicus increased slightly (14.7%) during the initial 12 days of aestivation as compared with that in the day 0 fish. By contrast, the estimated rate of ammonia production decreased by 84% during the final 12 days of aestivation (day 35-day 46) compared with the day 0 value. Therefore, it can be concluded that P. aethiopicus depended mainly on increased urea synthesis to ameliorate ammonia toxicity during the initial phase of aestivation, but during prolonged aestivation, it suppressed ammonia production profoundly, eliminating the need to increase urea synthesis which is energy-intensive.     

Intranuclear bundles of microfilaments and microtubules in chromaffin cells of the auricle of the heart of a lungfish, Protopterus aethiopicus

Intranuclear microtubular-microfilamentous rod-like inclusions were investigated in chromaffin cells of the auricle of the heart of lungfishes. In conventional electron microscopy, these inclusions reveal a wide variety in appearance, depending on their orientation to the plane of sectioning. Whereas originally they were merely interpreted as a bundle of microfilaments, application of a goniometer stage showed the rod- or spindle-shaped intranuclear inclusions to have a basic substructure of parallel arranged microtubules among microfilaments, which are clearly connected to chromatin granules, occasionally penetrating dense areas of chromatin. The chemical nature and biological significance of these structures, which so far remain enigmatic, are discussed.     

Multilocus isozyme systems in African lungfish,Protopterus annectens: distribution,differential expression and variation in dipnoans

Distribution of ADH, ALP, FBALD, GAPDH, G3PDH, G6PDH, GPI, LDH, MDH, PGM, and SOD was identified in retina, heart, muscle, liver, kidney, gills, brain, gut, lung and ovary of the African lungfish. Data are compared with patterns previously described in dipnoans and other vertebrates. The number of loci expressed for all enzymes was found to be similar to those of diploid Actinopterygii. Differences in the number of loci expressed in Amphibia were found for ALP, sG3PDH, GPI, LDH, MDH and SOD. Differences in tissue distribution were noted in ALP due to the absence of an intestinal-specific form typical of teleostean fish, amphibians, reptiles and birds, and in GPI and MDH, due to the tissue expression, as in primitive fish. There were also differences in LDH, where a third locus (LDH-C*) was expressed in the gills of Protopterus annectens and not in the retina or liver tissues, as in teleosts. LDH-A₄ was most common in all the tissues. Major differences were noted in the tissue patterns of protein expression in the three dipnoans compared. As expected, the least divergence was found between the two species belonging to the same family (Lepidosirenidae). The highest index of divergence was observed between Neoceratodus forsteri and Lepidosiren paradoxa, belonging to the families Ceratontidae and Lepidosirenidae, respectively. The divergence is revealed by changes at the enzyme and morphological levels. These results suggest that P. annectens occupies an interesting systematic position, its biochemical characteristics distinguishing it from N. forsteri, L. paradoxa, the advanced fish and amphibians.