Variabilichromis moorii
A species of populations being phenotypically uniform but genotypically distinct
Introduction
Variabilichromis moorii (Boulenger, 1898) is a large unit of numerous populations that occur in the shallow, rocky biotope along the shore of the southern half of Lake Tanganyika. It is a member of the tribe Lamprologini (Poll 1986: 46). V. moorii was discovered and collected for formal description by J. E. S. Moore at Mbity Rocks and Kinyamkolo, in the “extreme south” of the lake, in the late nineteenth century (Boulenger 1898a; 1898b: 8; 1901: 138). The first specimens from that collection were described as being dark brown with blackish fins and measuring 93 mm in total length. A subsequent study indicated a maximum length of 103 mm (Poll 1956: 483). An interesting feature of the fish is the colouration of the juveniles. These are not dark brown, but usually yellow or beige. The colourational change from yellow to brown usually starts when juveniles are around 3–4 cm, and “on reaching a length of five centimetres the fish has turned brownish” (Staeck and Linke 1994: 107), or occasionally yellow and even up to 6 cm (Herrmann 1987: 95). There seems to be some variation in the ontological change among populations. A few populations have juveniles changing colour early in life, and others much later. Konings (1998: 91) reports on the Congolese populations being dark already from the beginning, while those juveniles in populations from around Kipili are among the deepest bright yellow; moreover, the juveniles in the population in Cameron Bay are dark from the beginning (Konings 1988: 138). Büscher (1998b) reports on the presence of V. moorii at Tembwe (southeast of Moba) in the Congo, but nothing in particular on the colouration of the juveniles. However, a photo by Büscher of a breeding pair with juveniles at Tembwe appears in Elster (1998: 108, Fig. bottom); the juveniles are beige yellow. Kohda et al. (1996: 238ff, Figs. 1–3) report on black juveniles (1 cm in size) in all populations of V. moorii between Cape Chaitika and Katoto in Zambia. At Cape Chipimbi, Zambia, V. moorii is said to be very common (Brichard 1978). Based on personal experiences of the Congolese populations, some have beige juveniles (especially in the south) and a few others have a very dark brown already at a size of about 20 mm, e.g. the juveniles in the population at Cape Tembwe (north of Moba), a variant which was exported by us in the late nineties and indicated in our stocklists of that time as: Neolamprologus moorii "Black - Cape Tembwe, Zaire". In 1998 we found and collected a single adult V. moorii with a striking bright orange colouration (see picture in Smith 2014: 52). The collecting site was along Longola Hill in the Congo, which is about 10 km south of Zongwe, and 24 km north of Kapampa. This individual likely had a chromatic mutation, and was the only one of its kind; the rest of the population was an ordinary black. Recently, an unknown population of V. moorii was discovered in southern Tanzania. Here the juveniles maintain their beautiful bright yellow colouration until they reach 8–9 cm, and then they change colour relatively quickly {see a video sequence of the juveniles here}. No significant populational variation seems to occur regarding the adults; they have a uniform dark brown (Fig. 1) or black (Fig. 2) colouration with a bright blue or white caudal-fin margin. Populations of V. moorii have been found at Cape Tembwe in the Congo (Poll 1956: 484) and at Cape Mpimbwe (Fig. 17) {see a map here} in Tanzania (Lundblad and Karlsson 1992); these two locations seem to be the outermost boundaries of the geographical distribution of the species. Alternatively, Kalemie (north of Cape Tembwe) harbours the northernmost population on the west coast (Konings 1998; Duftner et al. 2006).
 |
Fig. 1. Adult individual of Variabilichromis moorii at Kashia Island. This population has a dark brown body colouration with a beige dorsal fin.
|
 |
Fig. 2. Variabilichromis moorii, adult individual at Izinga Island, 5 metres depth. This population demonstrates a black body colouration.
|
General ecology: Diet, reproduction and territory
In its natural habitat, V. moorii is very often observed together with its offspring, tenaciously protecting the fry. Spawns can reach 500 eggs (Herrmann 1987: 95; Konings 1998: 91); the ovaries of an examined female contained about 250 eggs, with a size of 1 mm (Poll 1956: 484). In aquaria the number of fry reaches around 100 (Jach 1982; Rundström 1982; Nilsson 1983), or 60-70 (Schlake 1988); for further details on spawning in aquaria see Thompson (1980), Kombächer (1986), Elster (2002), and Moor (2002). Examination of stomach content of wild specimens showed crustaceans and microorganisms, as well as filamentous algae (Poll 1956: 483f); Yamaoka (1997) also reports on filamentous algae likely being part of its diet. Sturmbauer et al. (2008b: 50) report that V. moorii “feeds on small invertebrates and aufwuchs, i.e. epilithic algae and organisms therein”; elsewhere the species is stated to feed primarily or exclusively on small invertebrates (AFC 1993; Sturmbauer et al. 2008a: 58). Lake observations from southern Tanzania (documented in the underwater video Lake Tanganyika Cichlids in the Wild: Tropheus moorii “Murago Tanzania”; Karlsson and Karlsson 2014) showed the herbivore species Tropheus moorii entering the territories of V. moorii but without being firmly chased away, while subsequently, T. moorii was briskly attacked if intruding on the territories of the herbivore Ophthalmotilapia boops, which may suggest that the two herbivore species are competing for the same or a similar source of food, while V. moorii is not {see a video sequence here}. Staeck and Linke (1994: 108) believe the food source is lying in the lawn of algae. Commonly, V. moorii is observed at rocks covered with a thick layer of long algae (Fig. 6), as reported in the inventorial diving log by Karlsson (1998). In this lawn of algae live the crustaceans and other small edible animals, which are the primary diet; the filamentous algae are not unlikely a secondary diet which inevitably come along when feeding on the crustaceans and more. Alternatively, it may be a trophically less specialised omnivore species. The buccal dentition of V. moorii (Fig. 15), having “9 or 10 equal, moderately large conical teeth in front of each jaw” (Boulenger 1898b: 8), was speculated as being the dentition of a predator (Elster 1998), but Büscher (1998a) concluded, apart from the general trophic aspect, that such a dentition is likely also to concern the “weapons used, e.g. in brood defence”. V. moorii does not behave like a typical herbivore, i.e. spending most of its time feeding; it behaves like a carnivore, i.e. feeding only occasionally, even though foraging may be continuous, as concluded from observations. V. moorii juveniles are frequently seen waiting for something edible (crustaceans and microorganisms) to be stirred up from the algal growth when herbivore species, such as Tropheus moorii, are foraging {see a video sequence here}. On the other hand, a lamprologin species in the same habitat which is frequently seen feeding on the algae is Telmatochromis brachygnathus, which has a similar pattern of geographical distribution to V. moorii (Hanssens and Snoeks 2003), i.e. it occurs in the southern part of the lake, and in addition in the central part. Among scientific researchers, V. moorii is, nevertheless, widely regarded as being a herbivore (Karino 1998; Ota et al. 2012b), a herbivore browser (Hata et al. 2014), and an algivore (Rossiter 1991; Ochi and Awata 2009; Ochi et al. 2012). Variabilichromis moorii is a biparental substrate-breeder, which breeds among rocks in relatively shallow water. At Maleza Island (Figs. 3–4) in southern Tanzania, V. moorii is very common, and it seems to outnumber any other cichlid fish species in the shallow habitat {see a video sequence here}. Individuals at this location are seen down to about 10 metres. At many other sites in the very south of the lake the highest density among all cichlid species has been found to be V. moorii (Fig. 5) (Konings 1988: 138), and representing, for example, almost one third of the entire cichlid population at Kalambo, Zambia, and almost two thirds of all cichlids at Kasakalawe, Zambia (Sturmbauer et al. 2008a: 61, 62, Table 1). A 20-year-long census of fish at Kasenga Point, a rocky habitat near Mpulungu, Zambia, resulted in V. moorii representing 13.6% of the whole littoral fish community, whereby being the second most common species after T. vittatus (Takeuchi et al. 2010: 242). Studies in the wild have shown that V. moorii can have very complex territories, in which both parents defend separate sub-territories, which may be shifted slightly depending on the movements of the fry (Figs. 6, 18). The total size of a territory varied between 1 and 4 m2, depending on depths (Sturmbauer et al. 2008b: 49), but normally one of the parents is hovering close to the fry, and the other patrolling the periphery of the territory (Rossiter 1991: 182). Territory size and territorial defence have been studied and compared involving sites at different depths. Territories in shallow sites were intruded by other fish more often, and territories in deeper sites were larger, presumably as a result of lower cost of defence due to fewer competitors (Karino 1998). Other studies have also shown that the territory size in general increases with increasing depth (summary in Sturmbauer et al. 2008a: 66). V. moorii may occur down to around 13 metres (Ota et al. 2012b). “Aside of resource defence, motivation for territoriality relates to reproduction and brood care” (Sturmbauer et al. 2008b). Several studies in the lake concerning the defensive behaviour of parents of V. moorii having different brood sizes and offspring sizes have also been conducted. The attack and defence rate by guarding parents was positively and strongly correlated with brood size and somehow negatively correlated with fry size, suggesting that the parental decision for brood defence seemed to be primarily determined by brood size; members of a smaller group, independent of their individual size, have a much lower chance of survival when predators are present (Karino 1997).
 |
Fig. 3. Maleza Island with Nausingili Island in the background.
|
 |
Fig. 4. Nakasenga Point with Maleza and Nausingili Islands in the distance. Also Singa Island is discernable on the left, behind Nakasenga Point and in front of Chopa Hill.
|
Alternative Reproductive Tactics (ARTs)
Alternative Reproductive Tactics (ARTs) (Taborsky et al. 2008: 1; Fleming and Huntingford 2012: 290), also known as “alternative reproductive phenotypes” (Sefc et al. 2008: 2531), or Alternative Mating Tactics (Taborsky 1994: 9), have been studied extensively on zoological species in general (see summaries in Oliveira et al. 2012 and Ota et al. 2012c), and in fish species in particular (e.g. Taborsky 1994: 11, Table 1; Taborsky 2008). In Lake Tanganyika there are several species practising some kind of ART, with the best known among Lamprologini perhaps being Lamprologus callipterus (Sato 1994), Neolamprologus brevis (Ota et al. 2012c), Telmatochromis temporalis (Katoh et al. 2005), and T. vittatus (Ota and Kohda 2006; Ota et al. 2012a). More species in the lake are likely to be added to this group as more details become known on their possibly ART-like behaviour, e.g. Telmatochromis dhonti, Altolamprologus compressiceps; on possibly ART-like behaviour in Lepidiolamprologus, see Karlsson and Karlsson (2012: 16). Recently, an alternative mating tactic was discovered regarding Variabilichromis moorii (Sefc et al. 2008). As stated above, V. moorii is a biparental species with rather fierce defence behaviour, especially when defending the brood. V. moorii would seem a very solid monogamous species. Yet, a lake-based genetic study of 10 broods of V. moorii (Sefc et al. 2008) revealed multiple paternity (several different fathers), suggesting that solitary wandering males of V. moorii are likely to perform reproductive parasitism as sneakers. The sneaker is an alternative category of reproductive males (of which there are among fishes not only two types but at least four, normally genetically correlated, i.e. phenotypes: sneaker males, satellite males, territorial males and piracy males), which are typically smaller in size, that may dart into pair-spawning territories and ejaculate sperm in order to fertilise the spawn (Ota and Kohda 2006); a sneaker male may in mouthbrooding fish taxa also be a mimicry of a female, e.g. Mchenga eucinostomus (McKaye 1983) and Ophthalmotilapia ventralis (Haesler et al. 2009). The study (Sefc et al. 2008) suggests that there are at least two different reproductive types of V. moorii males: small solitary sneakers and large monogamous territory holders.
 |
Fig. 5. Neolamprologus pulcher and Variabilichromis moorii are dominating the rocky habitat at 6 metres depth at Mikongolo Island, Kala Bay.
|
 |
Fig. 6. Breeding pair of Variabilichromis moorii with fry at Izinga Island.
|
Special ecology: Lunar influenced but not moonstruck
Seemingly, Lake Tanganyika cichlids possess an interesting appearance and behaviour. But there is more than meets the eye. Apart from the intriguing different mating tactics, there is also the “lunar spawning”. Lunar-influenced spawning is known from a marine environment, where it has been related mainly to tidal fluctuations (Rossiter 1991). In lakes, however, significant lunar tidal effects are limited or absent. Yet, the analyses of V. moorii broods of four different sizes revealed each to have originated on or near a first quarter moon (Rossiter 1991). The study rejected the synchronisation possibly being socially triggered, or produced by a possible fluctuating food supply, and instead focused on the moonshine as an explanatory factor. Guarding parents of V. moorii (Figs. 7–8) are capable of successfully defending their offspring during the day, with available daylight, but are rather unsuccessful in doing so during dark nights. Nocturnal predators, e.g. bagrid catfish and mastacembelid eels, are thought to be the main predators in Lake Tanganyika (Fryer and Iles 1972). A breeding pair of V. moorii places its spawn in a concealed position on the vertical face of a crevice, at the centre of the territory. The eggs take at least 3 days to hatch. Spawning with lunar synchronisation increases the survival rate of the offspring, especially at the larval stage, because with the aid of the moonlight the guarding parents can actually see the attacking predators. During the first quarter to full moon period, moonlight over Lake Tanganyika appears as soon as the sun sets (Fig. 9). Timing of spawning therefore ensures the brood at its most vulnerable stages, i.e. eggs or larvae, to occur when lunar illumination has its maximum duration and intensity. “Exact spawning synchronization on the days when the greatest amount of moonlight is available could be expected to evolve in fishes with exposed eggs. This may be one possible reason why two other typical lunar spawning species, Lepidiolamprologus elongatus and L. profundicola, showed more exactly synchronized spawning than did the other species” (Nakai et al. 1990: 597) {more info on Lepidiolamprologus here}. The moonlight helps the parents in the visual detection of predators, but also, during a full moon, hunting activity of the true nocturnal predators is strongly reduced, as they are normally not active when there is moonlight (McKaye 1983). This is a fact well recognised by local fishermen, who do not fish at night during this period. After the full moon towards the second quarter moon, the period of darkness following a sunset gets progressively longer again; this provides new opportunities for nighttime predators (Rossiter 1991). However, lunar spawning synchronisation is far from being a completely secure strategy for broods to survive. Several other predatory species are specialised to exploit this strategy. The nocturnal predator Mastacembelus zebratus (similar to, and grouped with, M. ellipsifer Matthes 1962: 69) seems to exhibit highly specialised feeding on eggs from lamprologin substrate spawners, as reported from the study (Ochi et al. 1999: 450). “This spiny eel ate many eggs in the first and second quarters of the lunar cycle when the spawning of substratum-brooding cichlids was active, while it nearly ceased eating in the latter half of the cycle”. Another lamprologin species which spawns under the influence of the moon is Neolamprologus mondabu, which starts its breeding activity during the first half moon (Takemon and Nakanishi 1998: 263); a fifth lamprologin lunar spawning species is Telmatochromis temporalis, studied by Takahashi (2010: 139). He reports the lunar spawning synchronisation to be a “widely observed phenomenon” in marine environments; however, it is rare in freshwater fish (Nakai et al. 1990). Paleolamprologus toae (Figs. 13–14), possibly closely related to V. moorii (see Sturmbauer et al. 2010), is another potential lunar spawner (Nagoshi 1987). But studies on the reproductive biology of P. toae have shown only weak or no evidence of a lunar spawning synchronisation (Nakai et al. 1990: 591, 592, Fig. 2; Rossiter 1991: 183). Apart from the lamprologin Tanganyikan species, the biparental female-to-male shift mouthbrooder Eretmodus cyanostictus is also known to display lunar synchronised spawning, and “seems to mate around full moon” (Neat and Balshine-Earn 1999: 336). Regardless of being potentially predatory or lunar spawning, nighttime-active lamprologin species are reported or assumed to include Neolamprologus furcifer (Yanagisawa 1987; Brichard 1989) and N. timidus (Kullander et al. 2014a). In summary, Takahashi (2010) concludes that “spawning prior to the full moon probably decreases the incidence of approaching brood predators and increases the guarding efficiency of parents”.
 |
Fig. 7. Male individual of Variabilichromis moorii with juveniles at Molwe.
|
 |
| Fig. 8. Adult individual with juveniles at Kalubale near Kambwimba in southern Tanzania. |
 |
Fig. 9. Full moon over Lake Tanganyika (left). The moonlight may trigger lunar influenced spawning among several fish species. In the opposite direction the sun is just setting (right). Cape Mpimbwe in the background with the Congo in the far distance. Pictures captured simultaneously, at the waterfront, African Diving camp.
|
Special ecology: Juvenile colourational mimicry
Several cichlid species in Lake Tanganyika display distinct colourational differences between adults and juveniles. The change from juvenile to adult colouration seems to be correlated to the reproductive stage in the life history of the species. Individuals with a juvenile colouration may not be looked upon by conspecific adults as reproductive rivals, and thus not chased away as determinedly from reproductive grounds, possibly containing edibles as well as shelter. This kind of colourational difference can be seen in many types of Tropheus, e.g. Tropheus moorii “Murago Tanzania” {see a video sequence here}. In populations of Variabilichromis moorii in Tanzania, juveniles are bright yellow, contrasting to black adults, and do in some cases not change the yellow colouration to black until approaching adulthood. Kohda et al. (1996) report on the differences between southern populations regarding this colourational change. Brood care in V. moorii has been found to last for around 100 days (Rossiter 1991: 182); by comparison, in Lepidiolamprologus profundicola and Altolamprologus compressiceps the whole brooding period is less than 20 days (Nakai et al. 1990: 595). The juveniles of V. moorii may be almost fully grown, but as long as they keep their yellow colouration they may reside within parents’ or conspecific adults’ territories (Figs. 10, 19). Interestingly, other lamprologin species with a similar colouration to the juvenile V. moorii seem to be allowed within these territories as well. Field observations suggest Neolamprologus mustax (Fig. 12) to be such a species (Ochi et al. 2007; Ochi and Awata 2009); see also Büscher and Wirtz (2009). Its yellow colouration, which resembles that of V. moorii juveniles (Figs. 19–21), facilitates access to the territories of V. moorii adults; by displaying the host’s juvenile colouration, the guest species may reduce aggression of the highly territorial host (Maan and Sefc 2013). N. mustax, being a zoobenthivore, exploits these territories as feeding grounds (Ochi et al. 2007: 400; Ochi and Awata 2009: 741). In addition, all individuals of N. mustax are not yellow. Within and between populations, individuals may also be dark brown (Konings 1998: 78). The field observations by Ochi and Awata (2009) clearly demonstrated that adult V. moorii were less aggressive towards yellow intruders than they were towards black ones. Therefore, it seems that dark-coloured N. mustax may not forage in the territories of V. moorii without being attacked. Furthermore, in another study (Ochi et al. 2012) it was found that N. mustax spends 60% of daylight hours foraging in the territories of V. moorii, from which most other fish are chased out. The study showed that each N. mustax individual seems to correlate with a certain V. moorii territory, where it was given access to the foraging ground without being chased away; but when the same N. mustax individual entered another V. moorii territory (as it was set up to do in the experimental study; Ochi et al. 2012), it would be attacked and chased out. The study did not mention the type of N. mustax colouration, but we may assume it was yellow, and if so, then we may conclude that having a yellow colouration may not give individuals of N. mustax a priori access to V. moorii territories. They must also be individually accepted.
 |
Fig. 10. Adult and sub-adults of Variabilichromis moorii at Katondo Point, Cape Mpimbwe.
|
 |
Fig. 11. At the camp of African Diving there are no Variabilichromis moorii, but just 8 km across Utinta Bay, at Cape Mpimbwe (visible in both photos), the northernmost (at this side of the lake) population of the species is encountered {see a map here}.
|
 |
Fig. 12. Neolamprologus mustax, NRM 61025. Due to its similarity to Variabilichromis moorii, this species may enjoy protection from breeding pairs of the same.
|
Morphology: Osteocranial study
In the middle of the eighties, Colombé and Allgayer made a revision of the genus Lamprologus, describing three new genera — Variabilichromis, Paleolamprologus, and Neolamprologus — and redescribing Lamprologus and Lepidiolamprologus; the revision focused on the presence of the infraorbital bones (a series of mostly small bones located below and around the eye) (1985: 9). Separating V. moorii and P. toae from Neolamprologus was a necessity in order to preserve the homogeneity of the latter genus, since the two species exhibit a different structure of the infraorbitals, the character with which the genus Neolamprologus was initially diagnosed from Lamprologus (Colombé and Allgayer 1985: 24; Poll 1986: 47; Kullander et al. 2014a: 324). Several authors followed the new taxonomy (Herrmann 1987; Ufermann et al. 1987; Zurlo 1987a–b), while others did not, recognising only one lamprologin genus, Lamprologus (Loiselle 1994); still, others objectively reported on the available names (Hesse 1987: 10ff, Tables 1–2; Staeck 1999). Poll (1986: 47, 57, 62) rejected the infraorbital structure as diagnostic for lamprologin genera, considered it to be too variable*, and therefore suspended Variabilichromis and Paleolamprologus, instead diagnosing Neolamprologus from Lamprologus based on the pelvic-fin rays, and from Lepidiolamprologus based on the scales in a longitudinal row (Kullander et al. 2014a: 324). But Stiassny (1997: 518) resurrected Variabilichromis partly in virtue of the same skeletal character. Moreover, she also pointed out the even stronger infraorbital dissimilarity of Paleolamprologus and Neolamprologus than that of Variabilichromis and Neolamprologus (1997: 517), but did not suggest a resurrection of Paleolamprologus by that time due to the fact that P. toae and N. cylindricus, a species which she did not examine in that study, ended up as pairs in the mtDNA analysis of Sturmbauer et al. (1994). Takahashi (2003: 14) found that all examined lamprologin species had one to five infraorbitals, except for P. toae and V. moorii (which had more; in P. toae up to nine) (2003: 15, Fig. 8D). Kullander et al. (2014a: 324) suggested recognition of Paleolamprologus as a distinct taxon based on its infraorbital state (Colombé and Allgayer 1985; Stiassny 1997; Takahashi 2003) and on the most recent molecular phylogenies (Day et al. 2007; Sturmbauer et al. 2010) with P. toae and V. moorii in succession each representing basal clades in one group of Lamprologini. Under three different methods (Bayesian inference, maximum likelihood and maximum parsimony) of phylogenetic inference from mtDNA analysis, Paleolamprologus toae is the more basal taxon within Lamprologini (Day et al. 2007: 638). In addition to being the basal clades, or lineages, the monotypic taxa Variabilichromis and Paleolamprologus were already separated from the remaining Lamprologini at the very base of the radiation (Sturmbauer et al. 1994; Duftner et al. 2006; Day et al. 2007; Sturmbauer et al. 2010).
* Poll considered the structure of the post-lachrymal infraorbital bones to be too variable in order to generically diagnose the lamprologin members based on this character, which is especially true in V. moorii, hence its name; etymologically, Paleolamprologus derives from the taxon’s infraorbital state believed by the authors to be the most ancestral (Colombé and Allgayer 1985). “Most species of this tribe [Lamprologini] exhibit intraspecific variation in the numbers of infraorbitals” (Takahashi 2003: 14).
 |
Fig. 13. Pair of Paleolamprologus toae at Kansombo. Etymologically, Paleolamprologus derives from the taxon's infraorbital state believed to be the most ancestral.
|
 |
Fig. 14. Paleolamprologus toae from Kansombo, NRM 51589 with dental close-up.
|
 |
Fig. 15. Variabilichromis moorii from Katondo, Cape Mpimbwe, NRM 59611 with dental close-up.
|
Genetics: Population structure study
Variabilichromis moorii, which occurs over a distance of roughly 600 km (Fig. 11), is a highly stenotopic* rock-dwelling cichlid, but is found to display no, or very little, phenotypic variation {see a video sequence of Cape Mpimbwe, the northernmost locality on the east coast, here}. As stated above, the juvenile colouration may vary between black, dark brown, beige, yellow and orange (Figs. 20–21), and there is also a variation between populations regarding the size when juveniles change colouration (Fig. 16). The adults may be viewed as largely phenotypically uniform, even though there is some slight variation. In most populations they are black, and in a few others they may be dark brown, or slightly yellowish dark brown (Figs. 1–2, 7–8). On a side note, comparing species status of morphologically similar allopatric populations, such as the populations of V. moorii, with the species status of populations in e.g. Lake Malawi, may reveal considerable differences. Stated in Genner et al. (2004: 93): “Among African lakes, levels of assignment to species status of allopatric populations were found to be distinctly different” and “For equivalent geographical areas, substantially higher proportions of recognized species were totally allopatric within the studied Lake Malawi and Lake Victoria complexes, than those of Lake Tanganyika”. Seemingly, allopatric populations in Lake Tanganyika are among taxonomists more frequently looked upon as a single species, than those equivalent populations in Lake Malawi, which are more often considered to belong to different species.
Several studies of the genetic structure among cichlid fishes have focused on populations which are confined to shore sections of rocky substrate and are isolated by geographical barriers (habitat barriers due to environmental discontinuity); in stenotopic rock-dwelling species, gene flow has been documented to be interrupted by habitat barriers such as short stretches of sand, river estuaries or deep waters; gene flow has been shown to be rather unrestricted within continuous rocky shores; and cichlids that are less confined to any specific habitat type display higher rates of gene flow (Duftner et al. 2006). But geographical barriers do not always prevent gene flow. Barriers of whatever type are rarely, if ever, a solid obstacle; ultimately, they are passable. On the other hand, distinct genetic structures can develop in subsets of populations along a continuous habitat, without geographical barriers, and evidently genetic differentiation does not necessarily correlate to morphological diversification.
 |
Fig. 16. Variabilichromis moorii, sub-adult at Molwe. This individual is in a transition state between juvenile and adult colouration. Note the yellow dorsal fin. Size about 7 cm.
|
 |
Fig. 17. Katondo Point, Cape Mpimbwe. At the promontory lives Tanzania’s northernmost population of Variabilichromis moorii.
|
In Lake Tanganyika, lake level fluctuations have very likely affected the patterns of gene flow, diversification and distribution of the stenotopic rock-dwelling cichlids (Sturmbauer and Meyer 1992; Cohen et al. 1997; Duftner et al. 2006). In Lamprologini, colouration as a character of species distinction is only moderately present, and instead eco- and tropho-morphological characters diversify the unit. Nevertheless, V. moorii being a species confined to a rocky habitat should perhaps be expected to show some kind of morphological variation. Lamprologini is estimated to be about 5 million years old, and V. moorii is the older of its members (Sturmbauer et al. 2010); any lack of diversification is unlikely due to time limitation. But as already stated, V. moorii is largely phenotypically uniform. This may suggest that there is a steady gene flow between populations, i.e. a flow of potentially reproductive V. moorii individuals crossing habitat barriers, entering neighbouring allopatric populations. However, the genetic study by Duftner et al. (2006) has shown quite the opposite: not only are the allopatric populations genetically distinct, but also there are subsets of genetically distinct structures within populations that are occurring along a continuous rocky shoreline, which suggests that V. moorii is a philopatric and less disperse species, with individuals not moving far away from their birthplace. The rather wide geographical distribution that V. moorii possesses, covering almost half of the lake, in spite of the species’ weak dispersal ability, may suggest a species of old age. Nevertheless, there is evidently morphological stasis in this highly stenotopic cichlid (Duftner et al. 2006). Similar patterns of genetic structures with high levels of differentiation within populations along continuous shorelines have been found in Eretmodus cyanostictus (Taylor et al. 2001) and in Tropheus species (Baric et al. 2003), which are living sympatrically with V. moorii. Despite the potentially limited propensity for dispersal, closely DNA-related V. moorii populations have been found on either side of the lakeshore, which is remarkable for a highly stenotopic philopatric species such as V. moorii (Duftner et al. 2006: 2387). The explanation of such an unexpected dispersal pattern is the ability of a lake crossing via underwater ridges in periods of a low water level, plus the possibly fluctuating water level that may have forced individuals and populations to disperse. Similar patterns of lake crossing dispersal have been found in Eretmodini (Verheyen et al. 1996; Duftner et al. 2006: 2388) and Tropheus (Baric et al. 2003; Sturmbauer and Meyer 1992) {see a video sequence of the lake crossing dispersal animated here}.
 |
Fig. 18. Breeding pair Variabilichromis moorii at Kapere. Numerous fry are present in the crevice.
|
 |
Fig. 19. Adult and sub-adults at Kapere in the extreme south of Tanzania.
|
The Lake Tanganyika cichlids are much older than those of, for example, Lake Malawi, which is reflected not only by the greater morphological and genetic differentiation between Lake Tanganyikan species, but also by the greater genetic structures within populations and species of Lake Tanganyika cichlids, e.g. as seen in the study of V. moorii (Duftner et al. 2006). The Lamprologini exhibit perhaps the greatest ecological diversity in their trophic morphology and habitat of all tribes of cichlid fishes. However, all cichlid species in Lake Tanganyika are concluded to have diversified very slowly, and the assemblage seems to be derived from a prolonged accumulation of species, rather than rapid, recent radiation (Day et al. 2008: 5). But evidence on rapid phenotypic diversification in fish, due to alternative environments during biological invasions, is commonly reported, e.g. by Lucek et al. (2012). Not unlikely, the diversification and radiation events in Lake Tanganyika took place at an early stage, and then slowed down to the present morphological stasis. Of course, exceptions exist. Isolated species with a limited range of geographical distribution may represent a relatively recent diversification and speciation event, such as the newly discovered Lepidiolamprologus kamambae (Kullander et al. 2012; Karlsson and Karlsson 2013).
* stenotopic, the opposite of eurytopic, i.e. being able to tolerate only a narrow range of environmental changes, e.g. staying within the surge-stricken rocky surroundings, as opposed to tolerating both rocky and sandy surroundings in both shallow and deep waters.
Morphological stasis and stepwise diversification
The morphological stasis in V. moorii is concluded to correlate to an ecologically adaptive top, and prevails in the effect of stabilising selection favouring a certain ideal of morphology. The population structure and pattern of differentiation in V. moorii are similar to those of the sympatric Tropheus and Eretmodus, and the three taxa also share the absence of eco-morphological diversification among populations, with colouration excluded (Duftner et al. 2006: 2388; Sefc et al. 2007). The apparent absence in morphological diversification is further seen in another dark-coloured, multi-populational, highly stenotopic, rock-dwelling lamprologin species, Chalinochromis cyanophleps (Kullander et al. 2014b; Karlsson and Karlsson 2012); see also Staeck (2014).
Regarding morphological stasis in other types of fishes, the lungfish clade, the Dipnoi, traces back in fossil records to about 400 million years, with little morphological diversification; and the West African lungfish, Protopterus annectens, a living fossil (a species being morphologically similar to its fossil ancestor), is thought to be the same species today as it was 100 million years ago, with no significant morphological alteration. Another extant lobe-finned fish and living fossil is the amazing coelacanth species Latimeria chalumnae, which has been morphologically unchanged for 70 million years; there is no doubt that morphological stasis really exists (Skelton 2001; King et al. 2011; Amemiya et al. 2013; Russell et al. 2014: 721, Fig. 32.19).
 |
Fig. 20. Sub-adult Variabilichromis moorii at Kampemba Point {see a map here}, just south of Cape Mpimbwe; size about 5 cm.
|
 |
Fig 21. Beautiful yellow sub-adult at Kapere village, Tanzania, 3.5 km north of Kalambo River, border with Zambia.
|
The results of the studies of V. moorii (Duftner et al. 2006) and Eretmodus and Tropheus partially (Sefc et al. 2007), that isolated allopatric intraspecific populations with distinctly different genotypes may have more or less identical phenotypes, show not only that morphological diversification does not necessarily accompany genetic diversification, but also that morphological stasis may prevail in the presence of genetic diversification, which in turn may suggest that evolution does not necessarily always proceed at a constant and gradual pace, but rather in an erratic and stepwise manner. It is often assumed that Charles Darwin believed evolution to be smooth and gradual. Of course, for Darwin it was important to dissociate himself from the prevailing ideas of catastrophism and progressive creationism (species being supernaturally created at intervals), and possibly as a necessary consequence thereof, a perfectly gradual pace of evolution became associated with his work. However, Darwin did not believe in a perfectly smooth and gradual type of evolution, but rather in prolonged stasis and stepwise diversification, as seen in the following passage from his The Origin of Species, 5th edition: “Many species when once formed never undergo any further change but become extinct without leaving modified descendants; and the periods, during which species have undergone modification, though long as measured by years, have probably been short in comparison with the periods during which they have retained the same form” (Darwin 1869: 551).
Species may exist for millions of years without altering important specific characteristics; widespread, less specialised species may give rise to more advanced forms without becoming extinct themselves; and diversification and speciation may proceed in stepwise manners. These and many more ideas were parts of the Punctuated Equilibria (Eldredge and Gould 1972), the widely criticised macro-evolutionary theory that received increasing recognition in the nineties and onwards (Mayr 1992). Being a theory about the change in the natural world, it generally also agrees with Darwin’s theory of evolution by natural selection (Eldredge 2006). The phenomena of morphological stasis and interrupted stability, as seen in the history of African lake faunas, are further studied in Fryer et al. (1983). On morphological stasis in Lepidiolamprologus, see Karlsson and Karlsson (2013: 16f); on stepwise diversification in Ophthalmotilapia, see Konings (1992).
Suggestion on how to cite this blog article;
Karlsson, M. and Karlsson, M. (2014) Variabilichromis moorii - A species of populations being phenotypically uniform but genotypically distinct. African Diving Blog. Available from: http://blog.africandivingltd.com/2014/11/variabilichromis-moorii-species-of.html (accessed [day] [month] [year])
Reference;
AFC, Association France Cichlid (1993) Atlas des cichlides No. 5/93 - Les Neolamprologus. Revue française des Cichlidophiles, supplément au no. 133. Pp 16.
Amemiya, C. T et al. (2013) The African coelacanth genome provides insights into tetrapod evolution. Nature, 496 (7445): 311-316; doi:10.1038/nature12027 PDF: http://goo.gl/xR9JYO
Baric, S., Salzburger, W. and Sturmbauer, C. (2003) Phylogeography and Evolution of the Tanganyikan Cichlid Genus Tropheus Based upon Mitochondrial DNA Sequences. Journal of Molecular Evolution, 56 (1): 54–68; doi:10.1007/s00239-002-2380-7
Boulenger, G. A. (1898a) Report on the fishes recently obtained by Mr. J. E. S. Moore in Lake Tanganyika. Proceedings of the Zoological Society of London, 1898 (3): 494-497.
Boulenger, G. A. (1898b) Report on the collection of fishes made by Mr. J. E. S. Moore in Lake Tanganyika during his expedition, 1895-96. Transactions of the Zoological Society of London, 15 (1, 1): 1-30.
Boulenger, G. A. (1901) Third contribution to the ichthyology of Lake Tanganyika. Report on the collection of fishes made by Mr. J. E. S. Moore in lakes Tanganyika and Kivu during his second expedition, 1899-1900. Transactions of the Zoological Society of London, 16 (1, 4): 137-178.
Brichard, P. (1978) Un inventaire des poissons du Cap Chipimbi Lac Tanganyka (Zambie). Revue Zoologique Africaine, 92 (1): 201-207.
Brichard, P. (1989) Pierre Brichard's book of cichlids and all the other fishes of Lake Tanganyika. T.F.H. Publications, Neptune City, NJ, 544 pp.
Büscher, H. H. (1998a) Anmerkung der Redaktion. P. 110 in: Elster, U. Neolamprologus moorii: Ein seltener Aquarienbewohner aus dem Tanganjikasee. DCG-Informationen, 29 (6): 106-110. Deutsche Cichliden-Gesellschaft e. V.
Büscher, H. H. (1998b) Artenvielfalt im Tanganjikasee - Die Cichlidengemeinschaft von Tembwe (Kongo). DATZ, 51 (12): 785-793. Eugen Ulmer-Verlag, Stuttgart.
Büscher, H. H. and Wirtz, P. (2009) Variabilichromis moorii und Neolamprologus mustax. Im Jugendkleid ins fremde Territorium DATZ, 62 (11): 8. Eugen Ulmer-Verlag, Stuttgart.
Cohen, A. S., Lezzar, K.-E., Tiercelin, J.-J. and Soreghan, M. (1997) New palaeogeographic and lake-level reconstructions of Lake Tanganyika: implications for tectonic, climatic and biological evolution in a rift lake. Basin Research, 9 (2): 107-132.
Colombé, J. and Allgayer, R. (1985) Description de Variabilichromis, Neolamprologus et Paleolamprologus genres nouveaux du Lac Tanganyika, avec redescription des genres Lamprologus Schilthuis, 1891 et Lepidiolamprologus Pellegrin, 1904. Revue française des Cichlidophiles (49): 9-16, 21-28.
Darwin, C. (1869) On the origin of species by means of natural slection, or the preservation of favoured races in the struggle for life. 5th edition. John Murray, London, 596 pp. Website: http://goo.gl/ys20i
Day, J. J., Cotton, J. A. and Barraclough, T. G. (2008) Tempo and mode of diversification of Lake Tanganyika cichlid fishes. PLOS One, 3 (3): e1730: 10 pp; doi:10.1371/journal.pone.0001730 Public Library of Science (PLOS). http://goo.gl/lONs8v
Day, J. J., Santini, S. and Garcia-Moreno, J. (2007) Phylogenetic relationships of the Lake Tanganyika cichlid tribe Lamprologini: The story from mitochondrial DNA. Molecular Phylogenetics and Evolution, 45 (2): 629-642.
Duftner, N., Sefc, K. M., Koblmüller, S., Nevado, B., Verheyen, E., Phiris, H. and Sturmbauer, C. (2006) Distinct populations structure in a phenotypically homogenous rock-dwelling fish from Lake Tanganyika. Molecular Ecology, 15 (9): 2381-2395.
Eldredge, N. (2006) Confessions of a Darwinist. The Virginia Quarterly Review, 82 (2): 32-53. http://goo.gl/eUyF1N
Eldredge, N. and Gould, S. J. (1972) Punctuated equilibria: An alternative to phyletic gradualism. Pp. 82-115 in: Freeman, T. J. M. (ed.) Models in paleobiology. Freeman, Cooper & Co., San Francisco, CA, 250 pp.
Elster, U. (1998) Neolamprologus moorii: Ein seltener Aquarienbewohner aus dem Tanganjikasee. DCG-Informationen, 29 (6): 106-110. Deutsche Cichliden-Gesellschaft e. V.
Elster, U. (2002) Zum Verhalten von Variabilichromis moorii. DCG-Informationen, 33 (11): 253-255. Deutsche Cichliden-Gesellschaft e. V.
Fleming, I. A. and Huntingford, F. (2012) Reproductive behaviour. Pp. 286-321 in: Huntingford, F., Jobling, M. and Kadri, S. (eds.) Aquaculture and behavior. Wiley-Blackwell, Oxford, UK, 358 pp.
Fryer, G. and Iles, T. D. (1972) The Cichlid Fishes of the Great Lakes of Africa. Their Biology and Evolution. T. F. H. Publications, Neptune City, NJ & Oliver & Boyd, Edinburgh, UK, 641 pp.
Fryer, G., Greenwood. P. H. and Peake, J. F. (1983) Punctuated equilibria, morphological stasis and the palaeontological documentation of speciation: a biological appraisal of a case history in an African lake. Biological Journal of the Linnean Society, 20 (2): 195-205.
Genner, M. J., Seehausen, O., Cleary, D. F. R., Knight, M. E., Michel, E. and Turner, G. F. (2004) How does the taxonomic status of allopatric populations influence species richness within African cichlid fish assemblages? Journal of Biogeography, 31 (1): 93-102.
Gould, S. J. and Eldredge, N. (1977) Punctuated equilibria: the tempo and mode of evolution reconsidered. Paleobiology, 3 (2):115–151.
Haesler, M. P., Lindeyer, C. M., and Taborsky, M. (2009) Reproductive parasitism: male and female responses to conspecific and heterospecific intrusions at spawning in a mouth-brooding cichlid Ophthalmotilapia ventralis. Journal of Fish Biology, 75 (7): 1845–1856.
Hanssens, M. and Snoeks, J. (2003) A new species and geographical variation in the Telmatochromis temporalis complex (Teleostei, Cichlidae) from Lake Tanganyika. Journal of Fish Biology, 63 (3): 593-616.
Hata, H., Tanabe, A. S., Yamamoto, S., Toju, H., Kohda, M. and Hori, M. (2014) Diet disparity among sympatric herbivorous cichlids in the same ecomorphs in Lake Tanganyika: amplicon pyrosequences on algal farms and stomach contents. BMC Biology, 12 (90): 14 pp; doi:10.1186/s12915-014-0090-4 http://goo.gl/v1iZx4
Herrmann, H.-J. (1987) Die Buntbarsche der Alten Welt - Tanganjikasee. Reimar Hobbing, Essen, West Germany, 239 pp.
Hesse, B. (1987) Neue Namen der Tanganjikasee-Buntbarsche - Die systematische Neuordnung. TI, 20 (6): 10-12; nr. 84. Tetra-Verlag, Melle.
Jach, H.-D. (1982) Ein Geduldsspiel - die Zucht von Lamprologus moorii. DCG-Informationen, 13 (1): 10-13. Deutsche Cichliden-Gesellschaft e. V.
Karino, K. (1997) Influence of brood size and offspring size on parental investment in a biparental cichlid fish, Neolamprologus moorii. Journal of Ethology, 15 (1): 39–43.
Karino, K. (1998) Depth-related differences in territory size and defense in the herbivorous cichlid, Neolamprologus moorii, in Lake Tanganyika. Ichthyological Research, 45 (1): 89-94.
Karlsson, M. (1998) Det förflutnas djup. Ciklidbladet, 31 (5): 26-40. Nordiska Ciklidsällskapet.
Karlsson, M. and Karlsson, M. (2012) Chalinochromis sp. “blue vein”. Ciklidbladet, 45 (2): 16-22. Nordiska Ciklidsällskapet. [See http://goo.gl/dMO0qX]
Karlsson, M. and Karlsson, M. (2013) Lepidiolamprologus kamambae - A new predatory cichlid from Lake Tanganyika. African Diving Lakesite articles, 1 (1): 1-24; no. 1. First edition; printed. MMK, Sweden. http://goo.gl/3jZLdy
Karlsson, M. and Karlsson, M. (2014) Lake Tanganyika Cichlids in the Wild: Tropheus moorii ”Murago Tanzania” [video]. Production MMK, Sweden. https://www.youtube.com/watch?v=DA4MCypRH4Y (accessed 22 Nov. 2014)
Katoh, R., Munehara, H. and Kohda, M. (2005) Alternative male mating tactics of the substrate brooding cichlid Telmatochromis temporal is in Lake Tanganyika. Zoological Science, 22 (5): 555–561.
King, H. M., Shubin, N. H., Coates, M. I. and Melina E. Hale, M. E. (2011) Behavioral evidence for the evolution of walking and bounding before terrestriality in sarcopterygian fishes. Proceedings of the National Academy of Sciences of the United States of America (PNAS), 108 (52): 21146-21151; doi: 10.1073/pnas.1118669109 http://goo.gl/Fm3CM2
Kohda, M., Yanagisawa, Y., Sato, T., Nakaya, K., Niimura, Y., Matsumoto, K and Ochi, H. (1996) Geographical colour variation in cichlid fishes at the southern end of Lake Tanganyika. Environmental Biology of Fishes, 45 (3): 237-248.
Kombächer, W. (1986) Erfahrungen mit Lamprologus moorii. DCG-Informationen, 17 (10): 183-187. Deutsche Cichliden-Gesellschaft e. V.
Konings, A. (1988) Tanganyika cichlids. Verduijn Cichlids and Lake Fish Movies, Zevenhuizen and Herten, 272 pp.
Konings, A. (1992) Ledtrådar till en etappvis artbildning. Pp. 6-9 in: Konings, A. (ed.) Ciklidårsboken, 2 (The Cichlids Yearbook, 2, Swedish edition). Cichlid Press, St. Leon-Rot, Germany / Forhman Aquaristik, Partille, Sweden.
Konings, A. (1998) Tanganyika cichlids in their natural habitat. Cichlid Press, El Paso, TX, 272 pp.
Kullander, S. O., Karlsson, M. and Karlsson, M. (2012) Lepidiolamprologus kamambae, a new species of cichlid fish (Teleostei: Cichlidae) from Lake Tanganyika. Zootaxa, 3492: 30-48. http://www.mapress.com/zootaxa/2012/f/zt03492p048.pdf
Kullander, S. O., Karlsson, M., Karlsson, M. and Norén, M. (2014b) Chalinochromis cyanophleps, a new species of cichlid fish (Teleostei: Cichlidae) from Lake Tanganyika. Zootaxa, 3790 (3): 425–438. http://mapress.com/zootaxa/2014/f/zt03790p438.pdf
Kullander, S. O., Norén, M., Karlsson, M. and Karlsson, M. (2014a) Description of Neolamprologus timidus, new species, and review of N. furcifer from Lake Tanganyika (Teleostei: Cichlidae). Ichthyological Explorations of Freshwaters, 24 (4): 301-328. http://www.pfeil-verlag.de/04biol/pdf/ief24_4_03.pdf
Loiselle, P. V. (1994) The Cichlid Aquarium. Revised & expanded edition. Tetra-Press, Melle, Germany, 447 pp.
Lucek, K., Sivasunder, A. and Seehausen, O. (2012) Evidence of adaptive evolutionary divergence during biological invasion. PLOS ONE, 7 (11): e49377, 6 pp; doi:10.1371/journal.pone.0049377
Lundblad, J. and Karlsson, M. (1992) Ett besök i den tysta världen - I vattnet vid Cape Mpimbwe. Akvariet, 66 (9): 268-272. Sveriges Akvarieföreningars Riksförbund (SARF), Gothenburg, Sweden.
Maan, M. E. and Sefc, K. M. (2013) Colour variation in cichlid fish: Developmental mechanisms, selective pressures and evolutionary consequences. Seminars in Cell & Developmental Biology; doi:10.1016/j.semcdb.2013.05.003
Matthes, H. (1962) Poissons nouveaux ou intéressants du lac Tanganika et du Ruanda. Annales, Musée Royal de l’Afrique Centrale, Tervuren, Sér. in-8°, Sciences Zoologiques (111): 27-88.
Mayr, E. (1992) Speciational evolution or Punctuated equilibria. Pp. 21-48 in: Somit, A. and Peterson, S. (eds.) The Dynamics of evolution - The punctuated equilibrium debate in the natural and social sciences. Cornell University Press, New York, NY, 325 pp.
McKaye, K. R. (1983) Ecology and breeding behaviour of a cichlid fish, Cyrtocara eucinostomus, on a large lek in Lake Malawi, Africa. Environmental Biology of Fishes, 8 (2): 81-96.
Moor, J. (2002) Ein Souvenir aus Sambia: Variabilichromis moorii. DCG-Informationen, 33 (6): 129-133. Deutsche Cichliden-Gesellschaft e. V.
Nagoshi, M. (1987) Survival of broods under parental care and parental roles of the cichlid fish, Lamprologus toae, in Lake Tanganyika. Japanese Journal of Ichthyology, 34 (1): 71-75. PDF: http://goo.gl/LtF20j
Nakai, K., Yanagisawa, Y., Sato, T., Niimura, Y. and Gashagaza, M. M. (1990) Lunar synchronization of spawning in cichlid fishes of the tribe Lamprologini in Lake Tanganyika. Journal of Fish Biology, 37 (4): 589–598.
Neat, F. C. and Balshine-Earn, S. (1999) A field survey of the breeding habits of Eretmodus cyanostictus, a biparental mouthbrooding cichlid in Lake Tanganyika. Environmental Biology of Fishes, 55 (3): 333–338. PDF: http://goo.gl/3b27n0
Nilsson, R. (1983) Lamprologus moorii. Ciklidbladet, 16 (7): 6-7. Nordiska Ciklidsällskapet.
Ochi, H. and Awata, S. (2009) Resembling the juvenile colour of host cichlid facilitates access of the guest cichlid to host territory. Behaviour, 146 (6): 741–56; doi:10.1163/156853909X446181
Ochi, H., Awata, S. and Kohda, M. (2012) Differential attack by a cichlid fish on resident and non-resident fish of another cichlid species. Behaviour, 149 (1): 99–109; doi:10.1163/156853912X629139
Ochi, H., Hata, H. and Hori, M. (2007) Advantage of harmlessness in gaining preferential access to a heterospecific territory. Journal of Fish Biology, 71 (2): 399-410.
Ochi, H. Sato, Y. and Yanagisawa, Y. (1999) Obligate feeding of cichlid eggs by Caecomastacembelus zebratus in Lake Tanganyika. Journal of Fish Biology, 54 (2): 450-459.
Oliveira, R. F., Taborsky, M. and Brockmann, H. J. (2008) (eds.) Alternative Reproductive Tactics. Cambridge University Press, Cambridge, UK, 518 pp.
Ota, K. and Kohda, M. (2006) Description of alternative male reproductive tactics in a shell-brooding cichlid, Telmatochromis vittatus, in Lake Tanganyika. Journal of Ethology, 24 (1): 9–15.
Ota, K., Aibara, M., Morita, M., Awata, S., Hori, M. and Kohda, M. (2012c) Alternative reproductive tactics in the shell-brooding Lake Tanganyika cichlid Neolamprologus brevis. International Journal of Evolutionary Biology, 2012 (915265): 10 pp. http://goo.gl/Iz4eZM
Ota, K., Hori, M. and Kohda, M. (2012a) Changes in reproductive life-history strategies in response to nest density in a shell-brooding cichlid, Telmatochromis vittatus. Naturwissenschaften, 99 (1): 23-31.
Ota, K., Hori, M, and Kohda, M. (2012b) Testes investment along a vertical depth gradient in an herbivorous fish. Ethology, 118 (7): 683-693.
Poll, M. (1956) Poissons Cichlidae. Exploration Hydrobiologique du Lac Tanganika (1946-1947). Résultats scientifiques, 3 (5B): 1-619.
Poll, M. (1986) Classification des Cichlidae du lac Tanganika. Tribus, genres et espèces. Académie Royale de Belgique, Mémoires de la Classe des Sciences, Collection in-8° (2), 45 (2): 1-163.
Rossiter, A. (1991) Lunar spawning synchroneity in a freshwater fish. Naturwissenschaften, 78 (4): 182–184; doi:10.1007/BF01136210
Rundström, B. (1982) Mina erfarenheter av Lamprologus moorii. Ciklidbladet, 15 (5): 15-18. Nordiska Ciklidsällskapet.
Russell, P. J., Hertz, P. E. and McMillan, B. (eds.) (2014) Biology - The dynamic science. Third edition. Brooks/Cole, Cengage Learning, Belmont, CA, 1456 pp. [Google Books: http://goo.gl/H6kkFk]
Sato, T. (1994) Active accumulation of spawning substrate: a determinant of extreme polygyny in a shell-brooding cichlid fish. Animal Behaviour, 48 (3): 669–678. PDF: http://goo.gl/r9gyrd
Schlake, F. (1988) Variabilichromis moorii, (Boulenger, 1898) - Der neue alte “Lamprologus” moorii - Seine Pflege und Zucht. TI, 21 (5): 15-16; nr. 89. Tetra-Verlag, Melle.
Sefc, K. M., Baric, S., Salzburger, W. and Sturmbauer, C. (2007) Species-specific population structure in rock-specialized sympatric cichlid species in Lake Tanganyika, East Africa. Journal of Molecular Evolution, 64 (1): 33-49. (Epub 09 Dec 2006)
Sefc, K. M., Mattersdorfer, K., Sturmbauer, C. and Koblmüller, S. (2008) High frequency of multiple paternity in broods of a socially monogamous cichlid fish with biparental nest defence. Molecular Ecology, 17 (10): 2531–2543.
Skelton, P. H. (2001) A complete guide to the freshwater fishes of southern Africa. First published by Southern Book Publishers in 1993. Struik Publishers, Cape Town, South Africa, xiv + 395 pp.
Smith, M. (2014) Trematochromis benthicola (Matthes, 1962). Tanganika Magazyn, 8 (1); nr. 15. “Tropheus” Robert Mierzeński, Kraków, Poland. [In Press]
Staeck, W. (1999) Neue Ergebnisse der Evolutionsforschung. DATZ, 52 (8): 6. Eugen Ulmer-Verlag, Stuttgart.
Staeck, W. (2014) Zwei neue Tanganjikasee-Cichliden beschrieben: Neolamprologus timidus und Chalinochromis cyanophleps. Aquaristik Fachmagazin, 46 (5): 54-56; nr. 239. Tetra-Verlag, Berlin-Velten, Germany. Preview: http://goo.gl/FYqE6k
Staeck, W. and Linke, H. (1994) African Cichlids II: Cichlids from eastern Africa. 1st completely revised edition. Tetra-Press, Melle, Germany, 199 pp.
Stiassny, M. L. J. (1997) A phylogenetic overview of the lamprologine cichlids of Africa (Teleostei, Cichlidae): A morphological perspective. South African Journal of Science, 93 (11-12): 513-523.
Sturmbauer, C. and Meyer, A. (1992) Genetic divergence, speciation and morphological stasis in a lineage of African cichlid fishes. Nature, 358 (6387): 578-581. PDF: http://goo.gl/6bmkrM
Sturmbauer, C., Fuchs, C., Harb, G., Damm, E., Duftner, N., Maderbacher, M., Koch, M. and Koblmüller, S. (2008a) Abundance, distribution, and territory areas of rock-dwelling Lake Tanganyika cichlid fish species. Hydrobiologia, 615 (1): 57-68.
Sturmbauer, C., Hahn, C., Koblmüller, S., Postl, L., Sinyinza, D. and Sefc K.M. (2008b) Variation of territory size and defense behavior in breeding pairs of the endemic Lake Tanganyika cichlid fish Variabilichromis moorii. Hydrobiologia, 615 (1): 49–56.
Sturmbauer, C., Salzburger, W., Duftner, N., Schelly, R. and Koblmüller, S. (2010) Evolutionary history of the Lake Tanganyika cichlid tribe Lamprologini (Teleostei: Perciformes) derived from mitochondrial and nuclear DNA data. Molecular Phylogenetics and Evolution, 57 (1): 266-284; doi: 10.1016/j.ympev.2010.06.018 http://goo.gl/PQBbzX
Sturmbauer, C., Verheyen, E. and Meyer, A. (1994) Mitochondrial phylogeny of the Lamprologini, the major substrate spawning lineage of cichlid fishes from Lake Tanganyika in Eastern Africa. Molecular Biology and Evolution, 11 (4): 691–703. http://goo.gl/UDCzWS
Taborsky, M. (1994) Sneakers, satellites, and helpers: parasitic and cooperative behavior in fish reproduction. Advances in the Study of Behavior, 23: 1–100. Academic Press, San Diego, CA, 284 pp.
Taborsky, M. (2008) Alternative reproductive tactics in fish. Pp. 251-299 in: Oliveira, R. F., Taborsky, M. and Brockmann, H. J. (eds.) Alternative Reproductive Tactics. Cambridge University Press, Cambridge, UK, 518 pp.
Taborsky, M., Oliviera, R. F. and Brockman, H. J. (2008) The evolution of alternative reproductive tactics: concepts and questions. In: Oliveira, R. F., Taborsky, M. and Brockmann, H. J. (eds.) Alternative Reproductive Tactics. Cambridge University Press, Cambridge, UK, 518 pp.
Takahashi, T. (2003) Comparative osteology of the infraorbitals in cichlid fishes (Osteichthyes: Teleostei: Perciformes) from Lake Tanganyika. Species Diversity, 8 (1): 1–26. Japanese Society of Systematic Zoology.
Takahashi, T. (2010) Different degrees of lunar synchronization of ovary development between two morphs of a Tanganyikan cichlid fish. Hydrobiologia, 644 (1): 139-143.
Takemon, Y. and Nakanishi, K. (1998) Reproductive success in female Neolamprologus mondabu (Cichlidae): influence of substrate types. Environmental Biology of Fishes, 52 (1-3): 261-269.
Takeuchi, Y., Ochi, H., Kohda, M., Sinyinza, D. and Hori, M. (2010) A 20-year census of a rocky littoral fish community in Lake Tanganyika. Ecology of Freshwater Fish, 19 (2): 239–248.
Taylor, M. I., Rüber, L. and Verheyen, E. (2001) Microsatellites reveal high levels of population substructuring in the species-poor Eretmodine cichlid lineage from Lake Tanganyika. Proceedings of the Royal Society of London, Series B, Biological Sciences, 268 (1469): 803–808. http://goo.gl/lDWIX0
Thompson, R. R. (1980) Spawning Lamprologus moorii. Buntbarsche Bulletin, (77): 18-20. The American Cichlid Association.
Ufermann, A., Allgayer, R. and Geerts, M. (1987) Cichlid-Catalogue (Pisces, Perciformes, Cichlidae Bonaparte, 1840). Volume 1. Alphabetical catalogue of the cichlid fishes. xv + 439.
Verheyen, E., Rüber, L., Snoeks, J. and Meyer, A. (1996) Mitochondrial phylogeography of rock-dwelling cichlid fishes reveals evolutionary influence of historical lake level fluctuations of Lake Tanganyika, Africa. Philosophical Transactions of the Royal Society of London, Series B, Biological Sciences, 351 (1341): 797-805.
Yamaoka, K. (1997) Trophic ecomorphology of Tanganyikan cichlids. Pp 25-56 in: Kawanabe, H., Hori, M. and Nagoshi, M. (eds.) Fish Communities in Lake Tanganyika. Kyoto University Press, Kyoto, Japan, 298 pp.
Yanagisawa, Y. (1987) Social organization of a polygynous cichlid Lamprologus furcifer in Lake Tanganyika. Japanese Journal of Ichthyology, 34 (1): 82–90.
Zurlo, G. (1987a) Man nannte sie Lamprologus - Erster Akt - ”Es war einmal”. Das Aquarium, 21 (9): 444-448; no. 219. Albrecht Philler-Verlag, Minden.
