Copepod has an important ecological role as a main food of several fishes on which commercial fisheries are based in Lake Tanganyika. However, very little multi-annual monitoring programs have been conducted for this group of crustacean zooplankton. This study was conducted in the northern part of Lake Tanganyika by weekly sampling at both pelagic and littoral sites over three consecutive years (2012–2014). The analyzed samples showed that Lake Tanganyika copepod was essentially composed of three suborders including Calanoida (30% by number) with a single endemic species, Cyclopoida (69%) with four dominant species and Harpacticoida (1%). These taxa showed variations in their abundance respectively at pelagic and littoral sampling sites. The average densities of copepods did slightly vary during the sampling period in both areas although higher peaks were observed in 2013. For the post-nauplii stage, Tropocyclops tenellus predominated while the nauplii of T. simplex predominated at both sampling sites. Seasonal fluctuations of copepod densities showed higher peaks in September/October and April/May, respectively, for the three most common species. T. simplex and M. aequatorialis ovigerous females showed higher peaks in the rainy season in 2013. These results can benefit pelagic fisheries research and lake environmental management efforts as the copepod abundance seems to be closely correlated to that of sardines in Lake Tanganyika.

Introduction

Lake Tanganyika is remarkable in its large biodiversity and high fish production (Mannini, 1999; Phiri and Shirakihara, 1999). Commercial fisheries mainly target two pelagic clupeids, Stolothrissa tanganicae (Regan) and Limnothrissa miodon (Boulenger), and four latids, especially Lates stappersii (Boulenger) (Roest, 1992; Sarvala et al., 1999). Clupeids feed mainly on copepods which occupy a key position in both food chain and energy transfer between primary producers (phytoplankton) and superior taxa (Langenberg et al., 2003). In Lake Tanganyika, copepod spatial distribution is mainly due to the increase in phytoplankton biomass closely driven by hydrodynamics and water mixing (Plisnier et al., 1999, 2009). Nevertheless, copepod populations have been the subject of few environmental studies in Lake Tanganyika. Earlier studies on their ecology (e.g. seasonal variations in abundance) were also limited by difficulties linked to the determination of many endemic species still requiring revision (Dussart et al., 1984). The description of Lake Tanganyika copepod species was previously conducted by Sars (1909), Gurney (1928) and Lindberg (1951). The Copepoda group is more diversified than other zooplankton groups and only harpacticoids, cyclopoids and calanoids are well represented in Lake Tanganyika (Lindberg, 1951; Dussart et al., 1984). Thirty nine cyclopoid species are present in Lake Tanganyika with three dominant species in the open waters: Mesocyclops aequatorialis aequatorialis (Kiefer), Tropocyclops tenellus (Sars) and Microcyclops cunningtoni (Sars) (Coulter, 1991). The cyclopoids are the most diverse group with a high endemicity while Tropodiaptomus simplex (Sars) is the unique endemic calanoid species known, widely distributed in Lake Tanganyika open waters (Lindberg, 1951; Mgana et al., 2014). The harpacticoid are reported but poorly known in Lake Tanganyika. Most species of this group seem to be parasites and benthic (Coulter, 1991). Previous researches on zooplankton have highlighted the vertical distribution of copepods in relation to planktivorous fish in the lake (Mulimbwa, 1988; Kurki et al., 1999; Vuorinen et al., 1999). Not much attention was paid to species diversity. Calanoids were noted to be more abundant in the south whereas cyclopoids were observed to dominate in the north (Kurki et al., 1999). Fluctuations in copepod abundance between both pelagic and littoral zones and the different life cycle stages (nauplii and post-nauplii) were not well investigated in Lake Tanganyika previously, despite their high biomass and relation with fish distribution. Densities and biomass of copepod taxa observed previously were preliminary and did not permit conducting comprehensive analyses due to the diversity of sampling methods used in the lake (Sarvala et al., 1999). Although zooplankton is sensitive to climate change (Richardson, 2008), it has not been used for this type of analyses in Lake Tanganyika. To overcome this knowledge gap, the present study performed regular monitoring to evaluate copepod populations in both pelagic and littoral waters and analyzed their inter-annual, seasonal and spatial variations in the northern part of Lake Tanganyika.

Materials and methods

Study site

Lake Tanganyika is located in Eastern Africa and is bordered by Burundi, Tanzania, Zambia and the Democratic Republic of Congo. The Democratic Republic of Congo covers over 14,800 km2 (45%) of the surface of the lake and 795 km (43%) of its perimeter. Monitoring of copepods was carried out in the open waters off Uvira at the extreme northwest of Lake Tanganyika. Two sites and two different sampling approaches were chosen: in pelagic site (03°24′56.7, 29°10′38.1″E) at 5 km from the shore and at an estimated depth of over 60 m; and in littoral site (03°25′01.2″S, 29°02′56.9″E) nearly 10 m from the shores with a variable depth estimated from 1 to 2.5 m. These sites were accessible from the Centre of Research on Hydrobiology (CRH, Uvira) and the pelagic site was very close to that of the LTR/FAO/FINNIDA project (Plisnier et al., 1999). In littoral areas we sampled at a site characterized by mixed substrates (rock-sand) with strong influence of human activities.

Data collection and sampling design

Sampling was conducted following two levels: spatial (pelagic and littoral) and temporal (weekly) from January 2012 to August 2014. At each site, a double and regular sample was taken weekly (every Tuesday) between 8–10 a.m. using a plankton net (100 µm aperture mesh, 25 cm diameter). Each sample was collected in a plastic pot and adjusted to a volume of 50 ml and immediately preserved in 4% formalin (Haney, 1988). The net was ballasted with a lead seal and raised slowly (0.5 m/s) on a vertical haul from 60–0 m in the pelagic zone or attached on floaters and pulled horizontally over a distance of 20 m slightly below the lake surface in the littoral site. The identification of copepod groups and species was conducted mainly in the laboratory of Biology at the CRH, Uvira (DR Congo) and complemented in laboratories at the Royal Museum for Central Africa and Royal Institute of Natural Science of Belgium. For this, each sample was transferred into 70% ethanol and isolated specimens were dissected into 10% glycerin solution onto slides using fine forceps (Type brucelle Dumont clockmaker). To perform copepod preparations, we followed patterns given in Kiefer (1956) and revised by Dussart (1980). For copepod species identification, a sound knowledge of their morphology was required and for this we used both light-microscopic observations and scanning electron microscopy (SEM) methods according to the scheme proposed by Dussart and Defaye (2001), Harnandez-Chavarria and Schaper (2000) and Fiers (Unpublished data). These procedures permitted broader view of specimen appendices of copepod taxa. Microscopic counting (OLYMPUS CH30RF200 and DIALUX 20) was carried out by sub-samples of 1 ml from the entire adjusting sample using a pipette (4 mm opening) (Isumbisho et al., 2006a,b). Counting taxa according to their development stages (nauplii and post-nauplii) was conducted following the methods described in Kurki (1993, 1997) and Vuorinen (1993). Copepods were determined to species level except for harpacticoids (group level).

Data analysis (descriptive statistics, One-way ANOVA and t-test) was performed using Excel 2007, StatView and SPSS 16.0 software to test for differences in temporal and spatial abundance. Differences between means were considered significant at p < 0.1.

Results

Composition and relative abundance of taxa

The three identified copepod suborders (Calanoida, Cyclopoida and Harpacticoida) show unequal proportions in their abundance (F = 80.3, p < 0.001) in Lake Tanganyika (Figure 1). Total densities indicate that cyclopoids with four common species predominate with ascending percentages of T. tenellus (52%) > M. aequatorialis (14%) > Thermocyclops oblongatus (2%) > M. cunningtoni (1%), respectively, followed by calanoid T. simplex (30%) and harpacticoids (1%) throughout the sampling period (Figure 1). Copepods are more abundant in the pelagic (n = 142, mean of 2069 ind.m−3, 66%) than in the littoral (n = 142, mean of 1060 ind.m−3, 34%) sites sampled here (F = 61.5, p < 0.001). Harpacticoids, although observed in both sites, were rare in the pelagic site. Average densities of copepods has varied slightly during the study period (r = 0.086, F = 7.4, p = 0.001).

Figure 1.

Total densities (individuals m−3) of copepod according to their suborders (a) and species (b) in both pelagic and littoral sampling sites and study period in the northern Lake Tanganyika. n = number of samples.

Figure 1.

Total densities (individuals m−3) of copepod according to their suborders (a) and species (b) in both pelagic and littoral sampling sites and study period in the northern Lake Tanganyika. n = number of samples.

Distribution and abundance of Copepod populations

The variations in total abundance of copepods by stages show that copepodids and nauplii are more dominant respectively for T. tenellus and T. simplex (Table 1). The male individuals of post-nauplii (mean number = 545 ind.m3, 23%) are slightly dominant over females (mean number = 503 ind.m−3, 21%) (t = 3.9, r = 0.924, p < 0.001). The ovigerous females are less abundant (mean number = 38 ind.m−3, 1.6%) and increasingly rare in the littoral site for all taxa. Differences in abundance of copepod taxa indicate that T. tenellus prevails at all stages except for nauplii for which T. simplex dominates in both habitats.

Table 1.

Average densities (Individuals number m−3± Standard Deviation) followed by the number of samples and percentages (in brackets) of copepod taxa in pelagic and littoral sampling sites according to stages in life cycle. N = nauplii, C = copepodid, F = female, M = male, OV. F = ovigerous female and T. COP. = total copepod.

PELAGIC (n = 142) LITTORAL (n = 142) 
Copepod taxa OV. F T. COP. OV. F T. COP. 
Tropodiaptomus simplex 1784 ± 130
(47) 
1321 ± 909
(26) 
1117 ± 109
(25) 
1162 ± 114
(24) 
149 ± 303
(34) 
5535 ± 386
(30) 
1700 ± 272
(57) 
598 ± 973
(20) 
257 ± 475
(17) 
255 ± 474
(15) 
4 ± 22
(14) 
2890 ± 366
(30) 
Tropocyclops tenellus 1512 ± 1499
(38) 
2608 ± 1400
(52) 
2471 ± 1821
(55) 
2664 ± 1678
(55) 
0 ± 0
(0) 
9155 ± 4288
(49) 
1053 ± 167
(36) 
1904 ± 199
(64) 
1066 ± 147
(70) 
1199 ± 149
(70) 
0 ± 0
(0) 
5424 ± 493
(57) 
Mesocyclops aequatorialis 586 ± 900
(15) 
902 ± 1013
(18) 
752 ± 1082
(17) 
812 ± 1132
(17) 
142 ± 328
(33) 
3193 ± 3716
(17) 
169 ± 436
(6) 
373 ± 814
(12) 
98 ± 269
(6) 
130 ± 367
(8) 
5 ± 47
(21) 
788 ± 1570
(8) 
Thermocyclops oblongatus 0 ± 0
(0) 
133 ± 271
(3) 
126 ± 232
(3) 
151 ± 260
(3) 
142 ± 211
(33) 
470 ± 767
(3) 
0 ± 0
(0) 
28 ± 79
(1) 
24 ± 72
(2) 
17 ± 47
(1) 
17 ± 111
(65) 
75 ± 164
(1) 
Microcyclops cunningtoni 0 ± 0
(0) 
33 ± 114
(1) 
57 ± 169
(1) 
47 ± 125
(1) 
0 ± 0
(0) 
148 ± 432
(1) 
0 ± 0
(0) 
3 ± 27
(0) 
16 ± 84
(1) 
2 ± 19
(0) 
0 ± 0
(0) 
39 ± 228
(0) 
Harpacticoida 1 ± 10
(0) 
1 ± 11
(0) 
0 ± 0
(0) 
1 ± 9
(0) 
0 ± 0
(0) 
3 ± 21
(0) 
51 ± 139
(2) 
91 ± 250
(3) 
57 ± 167
(4) 
97 ± 248
(6) 
0 ± 0
(0) 
309 ± 605
(3) 
PELAGIC (n = 142) LITTORAL (n = 142) 
Copepod taxa OV. F T. COP. OV. F T. COP. 
Tropodiaptomus simplex 1784 ± 130
(47) 
1321 ± 909
(26) 
1117 ± 109
(25) 
1162 ± 114
(24) 
149 ± 303
(34) 
5535 ± 386
(30) 
1700 ± 272
(57) 
598 ± 973
(20) 
257 ± 475
(17) 
255 ± 474
(15) 
4 ± 22
(14) 
2890 ± 366
(30) 
Tropocyclops tenellus 1512 ± 1499
(38) 
2608 ± 1400
(52) 
2471 ± 1821
(55) 
2664 ± 1678
(55) 
0 ± 0
(0) 
9155 ± 4288
(49) 
1053 ± 167
(36) 
1904 ± 199
(64) 
1066 ± 147
(70) 
1199 ± 149
(70) 
0 ± 0
(0) 
5424 ± 493
(57) 
Mesocyclops aequatorialis 586 ± 900
(15) 
902 ± 1013
(18) 
752 ± 1082
(17) 
812 ± 1132
(17) 
142 ± 328
(33) 
3193 ± 3716
(17) 
169 ± 436
(6) 
373 ± 814
(12) 
98 ± 269
(6) 
130 ± 367
(8) 
5 ± 47
(21) 
788 ± 1570
(8) 
Thermocyclops oblongatus 0 ± 0
(0) 
133 ± 271
(3) 
126 ± 232
(3) 
151 ± 260
(3) 
142 ± 211
(33) 
470 ± 767
(3) 
0 ± 0
(0) 
28 ± 79
(1) 
24 ± 72
(2) 
17 ± 47
(1) 
17 ± 111
(65) 
75 ± 164
(1) 
Microcyclops cunningtoni 0 ± 0
(0) 
33 ± 114
(1) 
57 ± 169
(1) 
47 ± 125
(1) 
0 ± 0
(0) 
148 ± 432
(1) 
0 ± 0
(0) 
3 ± 27
(0) 
16 ± 84
(1) 
2 ± 19
(0) 
0 ± 0
(0) 
39 ± 228
(0) 
Harpacticoida 1 ± 10
(0) 
1 ± 11
(0) 
0 ± 0
(0) 
1 ± 9
(0) 
0 ± 0
(0) 
3 ± 21
(0) 
51 ± 139
(2) 
91 ± 250
(3) 
57 ± 167
(4) 
97 ± 248
(6) 
0 ± 0
(0) 
309 ± 605
(3) 

Seasonal variations of copepods

Seasonal variations in total copepod abundance by developmental stages indicate higher peaks in September/October 2013 at the beginning of the rainy season respectively for copepodids > males > females > nauplii > ovigerous females in both sampling sites (Figure 2). These peaks are followed by that of post-nauplii (male and female adults) in April throughout the sampling period (Figure 2).

Figure 2.

Total copepod number (individuals m−3) according to the stages of development in the northern Lake Tanganyika (pelagic and littoral sampling waters) during the study period.

Figure 2.

Total copepod number (individuals m−3) according to the stages of development in the northern Lake Tanganyika (pelagic and littoral sampling waters) during the study period.

The changes in total seasonal abundance of copepod taxa are most noteworthy in 2013 compared to other periods with higher peaks respectively for the three most dominant species (T. tenellus, T. simplex and M. aequatorialis) in October 2013 (start of the rainy season) and second peaks in April/May (end of the rainy season) in both sites (Figure 3a). Ovigerous females in pelagic waters have increasing longer duration peaks from October 2013 for T. simplex and M. aequatorialis (Figure 3b).

Figure 3.

Number (individuals m−3) of total copepod (a), ovigerous female (b), nauplii (c), copepodid (d), female (e) and male (f) in pelagic and littoral sites and by species in the northern Lake Tanganyika during the study period. Wet and dry seasons are indicated.

Figure 3.

Number (individuals m−3) of total copepod (a), ovigerous female (b), nauplii (c), copepodid (d), female (e) and male (f) in pelagic and littoral sites and by species in the northern Lake Tanganyika during the study period. Wet and dry seasons are indicated.

Variations in seasonal and monthly abundance of total nauplii by copepod taxa indicate increasing peaks in the dry season (August/September) and the end of the rainy season (April/May). These peaks are more pronounced with longer duration in the littoral site in 2013 throughout the dry season (Figure 3c). T. simplex nauplii are predominant with higher and prolonged peaks throughout the dry season and the beginning of the rainy season in 2013 in the littoral site. In the pelagic one, these peaks are observed towards the end of the rainy season. Copepodids are abundant in 2013 with higher peaks in October and secondary ones in April/May and September/October in both sites. Unlike nauplii, copepodid peaks are headed by T. tenellus in both study sites (Figure 3d).

The copepod male and female individuals show almost similar seasonal fluctuation profiles and are predominant in 2013 with ascending peaks in April and September/October, i.e. towards the end and beginning of the rainy season in both pelagic and littoral zones (Figures 3e and f).

Discussion

Copepods are extremely abundant in freshwater (from five orders) and comprise a major component of most planktonic, benthic and groundwater communities. This diversity is reflected in the enormous range of life styles adopted, and in sub-Saharan Africa, the major contributors are the Cyclopidae, especially Eucyclops and Thermocyclops, and the Diaptomidae, especially Tropodiaptomus, followed by the Lernaeidae (Boxshall and Halsey, 2004; Boxshall and Defaye, 2008). Cyclopoids are the most diversified copepod group in both Lake Tanganyika (Coulter, 1991) and Victoria (Gophen et al., 1993; Mwebaza-Ndawula, 1994). Our results are compared to some earlier works on Tanganyikan copepods, broadly related to limnology and pelagic fisheries management, for the five common species identified includind T. simplex, T. tenellus, M. aequatorialis, T. oblongatus and M. cunningtoni, respectively (Narita et al., 1986; Kondo and Hori, 1986; Coulter, 1991; Kurki, 1993; Kurki et al. 1999; Vuorinen, 1993; Vuorinen et al., 1999; Dumont, 2006; Langenberg et al., 2008; Mgana et al., 2014). As Lake Baikal, around 49% of copepod species are endemic in Lake Tanganyika (Coulter, 1991; Boxshall and Defaye, 2008). Globally, the abundance of zooplankton follows a cycle closely related to the seasonal cycle of rainfall and phytoplankton populations in Lakes Tanganyika (Plisnier et al., 1999; Mulimbwa et al., 2014a) and Victoria (Cocquyt et al., 1994). Recently, a tight positive correlation between monthly rainfall and copepod biomass was reported in the north of Lake Tanganyika (Mulimbwa et al., 2014b). This could be linked to river discharges into the lake and higher nutrients in coastal areas particularly during the rainy season due to surface runoff and increased groundwater flow from the lake basin (Coulter, 1991). Similarly, peaks in total abundance of copepod zooplankton appeared to follow this pattern in the rainy season (September/October and April, respectively) through our results. The success of clupeids, therefore, appeared to be linked to rainfall and abundance of copepods in the lake (Mulimbwa et al., 2014b). This seasonality is correlated to phytoplankton biomass as in other Great Lakes such as lakes Malawi and Kivu. In Lake Tanganyika zooplankton biomass appears to be generally lower in contrast to Lake Malawi possibly because of the presence of specialized clupeids in Lake Tanganyika while in Lake Malawi, Chaoborus are present and there seems to be little efficient zooplankton utilization by e.g. Engraulicypris sardella (Hecky, 1984; Bootsma and Hecky, 1993).

T. simplex is the only calanoid species known and widely distributed in Lake Tanganyika with differences in densities along the north and south axis of the lake. Unlike in the north, T. simplex is distributed over a larger water column in the south of Lake Tanganyika and becomes increasingly rare in upper layers (Vuorinen et al., 1999). The copepod species globally have shown variations in their littoral-pelagic abundances according to their developmental stages. In the littoral area, variations of taxa were remarkable for T. simplex, in ascending order of nauplii > copepodids > post-nauplii (male and female) > ovigerous females, respectively, and almost the opposite in the pelagic zone. This means that the proportion of post-nauplii globally decreased in the littoral site for this species. T. simplex nauplii have dominated in both study sites compared to other taxa. This could be due to both the sampled water column (60–0 m) and the vertical migration profiles of T. simplex in the pelagic zone where post-nauplii inhabit deeper layers during daytime and ascend into the upper layers at night (Vuorinen et al., 1999). Perhaps also in order to escape predation by S. tanganicae and to graze on phytoplankton increasingly abundant in the upper layers during the daytime and known as seasonally regulated by the hydrodynamic cycles of the lake (Plisnier et al., 1999). Larval and juvenile clupeids in Lake Tanganyika feed essentially on copepod with preference for larger organisms (e.g. T. simplex, M. aequatorialis or T. oblongatus) when available (Mannini et al., 1996; Sarvala et al., 2002). So, the monthly catches of clupeids are known to fluctuate with cohort peaks shortly originated after those of copepods, mainly determined by the catches of S. tanganicae and L. miodon towards July and October and April–May in the north parts of Lake Tanganyika (Mulimbwa et al., 2014a). We must also take into account the significant differences in body size between T. simplex and cyclopoids such as a T. simplex nauplius whose size is comparable to a T. tenellus adult (Kurki et al., 1999). Coulter (1991) stated that in the pelagic zone, T. simplex is the most affected species by predation of clupeids and Chéné (1975) found that S. tanganicae fed largely on this species (72.9%) in the north of the lake. Kurki et al. (1999) suggested that T. simplex is the most vulnerable species preyed upon because of its larger size. Kondo and Hori (1986) collected zooplankton vertically and horizontally near the coasts (between 0–5 m in depth) in a rocky area off Luhanga, South of Uvira (DRC) during both day- and nighttime. Their results indicated that the nauplii and cyclopoid copepodids predominated; this confirmed partially our results at the littoral site off Uvira but the planktivory by littoral cichlid diversity of Lake Tanganyika has not yet demonstrated in details. A positive correlation between phytoplankton chlorophyll in Kigoma area (Kimirei and Mgaya, 2007) or spatio-temporal phytoplankton blooms (Plisnier et al., 2009) and the abundance of S. tanganicae (catches) have been already mentioned in Lake Tanganyika. However, clear abundance links of both copepods and clupeids remain unproven for fisheries management although data from experimental trawl catches of pelagic fish were positively correlated with post-naupliar copepod abundance in the south basin of Lake Tanganyika (Kurki, 1998); but sometimes strong fish cohorts could arise even under poor food conditions in the north basin (Mulimbwa et al., 2014a) and the timing of reproductive activities in clupeids species is likely to be subject to strong year-to-year variation.

T. tenellus is a small species (female: 0.32–0.36 mm; male: 0.30–0.33 mm of total length, TL). Since the original description by Sars (1909), various revisions of this species took place (Kiefer, 1956; Dumont, 2006). T. tenellus predominated in our samples and was well distributed throughout the water column although there were differences between littoral (54%) and pelagic (49%) areas. This species was much more abundant compared to T. simplex and other cyclopoid taxa with dominance males. The slight dominance of males against their respective females may be due to a better capability in the feeding competition (e.g. grazing mode, selection and size of phytoplankton cell available) or the predation by fish. Tanganyikan clupeids are known as visual predators and their feeding mode are related with the prey sizes. In our observations, the males were relatively smaller than females and might be less visible by sardines. This was more noticeable in the most common T. tenellus due to its small size and maybe its grazing/feeding habit in the study area unlike other copepod species. The high abundance of cyclopoids could be explained by the fact that most of them live in the littoral zone (Kondo and Hori, 1986). T. tenellus has shown also high densities of post-nauplii, followed by relevant copepodids in littoral and pelagic waters. However, the average density of individuals was generally higher in pelagic, almost twice the values for post-nauplii of this species. This larger proportion of T. tenellus could be due to the vertical distribution of copepod populations during the daytime in the lake. Our sampling was focused in the first 60 meters where T. tenellus is supposed to be more abundant, unlike other species (Sarvala and Salonen, 1995). The cyclopoids confined in upper layers (Vuorinen et al., 1999; Kurki et al., 1999) were mainly T. tenellus (Dumont, 2006). The hypothesis was that T. tenellus rarely occurs deeper than 40 m where species like M. aequatorialis and Thermocyclops spp. are abundant to avoid competition and maybe also predation (Dumont 2006). Otherwise, Mulimbwa et al. (2014b) sampled zooplankton in closely similar pelagic site (0–100 m) off Uvira as in this study in 2007–2008 and found T. simplex and M. aequatorialis to predominate while smaller cyclopoids (probably T. tenellus) were very low in density. This was different from Kurki et al. (1999), Vuorinen et al. (1999), Dumont (2006) and our own observations study. Sampling at different moments might explain variability in observations.

M. aequatorialis (male: 0.6–0.7 mm and female: 0.8–1 mm) occurs in both Lakes Tanganyika and Kivu though the genus Mesocyclops Sars, 1914 is well distributed in many aquatic systems of Africa (for revision see Dahms and Fernando [1992]; Ueda and Reid [2003]; Isumbisho et al. [2006b]). This species was found in both littoral (8% of total density) and pelagic (17%) sites with lower densities than T. tenellus and T. simplex. This could be also attributed to the water column sampled during the study period. Like T. simplex and their predators (Clupeidae), M aequatorialis is more abundant in the lower layers (40–80 m) during the daytime (Dumont, 2006). Nauplii and copepodids of this species were more prevalent in littoral site compared to post-nauplii individuals. It is known that M. aequatorialis and Thermocyclops spp. adult individuals may predate T. tenellus individuals which, in turn, are in competition with their nauplii and copepodids in Lake Tanganyika (Chèné, 1975; Dumont, 2006). M. aequatorialis nauplii were very rare at the beginning of rainy season (September/October) and reappeared during December/January. Mulimbwa et al. (2014) found this species to be most abundant around November/October and April in pelagic waters in Uvira in agreement with our own results. Kurki et al. (1999) have investigated the seasonal changes in three localities off Bujumbura, Kigoma and Mpulungu and they also obtained comparable results in Kigoma.

The genus Thermocyclops Kiefer, 1927 is represented by four species in Lake Tanganyika (Lindberg, 1951; Kiefer, 1956) (see Babwingure et al. (2001); Ueda and Reid (2003); Dussart and Dufaye (2006) for revisions). Only T. oblongatus was observed (respectively, 1 and 3% of total copepods in the littoral and pelagic waters) during this study in Lake Tanganyika. By cons the genus is rather represented by T. consimilis (Kiefer) in Lake Kivu where it is dominant in the pelagic waters with M. aequatorialis (Kiefer) and T. confinis (Kiefer) (Isumbisho et al., 2006a). Although T. oblongatus was not more detailed in previous studies in Lake Tanganyika, Dumont (2006) reported that it lives in deeper open waters during the daytime like M. aequatorialis. In our results, T. oblongatus was observed more frequently in March and July throughout the study period except in 2014. The genus Microcyclops Claus, 1893, is represented by five taxa in Lake Tanganyika among which M. cunningtoni lives in open waters (Lindberg, 1951). This species was less abundant in our results (1% of total copepod in pelagic and almost absent in littoral). M. cunningtoni was often observed in the April/May rainy season in 2012 and 2013 but absent at the same period in 2014.

The Harpacticoida are poorly known in Lake Tanganyika basin. Five genera and 16 species and subspecies of this group are reported (Lindberg, 1951). We have sporadically observed them in littoral waters at the start of rainy season but rarely in pelagic waters. This could be explained by the fact that this copepod group is essentially associated with the littoral and benthic environment in Lake Tanganyika.

Conclusions

Monitoring of Copepods was carried out in the north of Lake Tanganyika during three years in pelagic and littoral waters. Copepods were more abundant in pelagic than littoral with disparities for different taxa identified. These changes in copepod abundance have fluctuated depending on development stages of each taxon. T. simplex nauplii were most abundant in the littoral site compared with those of other taxa. T. tenellus was dominant in both sampling sites and throughout the study period for post-nauplii. Seasonally, copepods were dominant at the beginning (higher peaks) and the end (slightly lower peaks) of rainy season in the north of Lake Tanganyika. Diversity and ecology of copepod species, especially cyclopoids are still largely understudied in littoral waters characterized by cichlid fish diversity. The accurate identification of zooplankton species is a domain where further studies are highly desired to allow additional progress in environmental and fisheries research on Lake Tanganyika.

Acknowledgements

We express our thanks to all field and laboratory staff at the Centre of Research on Hydrobiology (CRH, Uvira) involved in the CHOLTIC project for their assistance in data acquisition and compilation. We also thank sincerely Dr. Didier Van den Spiegel (Royal Museum for Central Africa) and Dr. Frank Fiers (Royal Institute of Natural Sciences of Belgium) for support and access in their laboratories. Thanks also to IdeaWild for field equipment and to Global Taxonomy Initiative, Belgium for the training in taxonomy to D. M. C.

Funding

The CHOLTIC project (“Cholera outbreaks in Lake Tanganyika induced by climate change?”) was funded by BELSPO (Federal Belgian Science Policy).

References

Babwingure, D., Thirion, C., Dumont, H.J.,
2001
.
The integumental pore signature of Thermocyclops oblongatus (Sars, 1927), with the description of Thermocyclops africae new species, and comparison with Thermocyclops emini (Mrazek, 1895)
.
Hydrobiologia
458
,
201
220
.
Bootsma, A. H., Hecky, R. E.,
1993
.
Conservation of the African Great Lakes; A limnological Perspective
.
Conservation Biology
7
(
3
),
644
656
.
Boxshall, G. A. and Defaye, D.,
2008
.
Global diversity of copepods (Crustacea: Copepoda) in freshwater
.
Hydrobiologia (2008)
595
,
195
207
. DOI
Boxshall, G. A. and Halsey, S. H.,
2004
. An Introduction to Copepod Diversity .
The Ray Society
,
London
.
Chèné, G.,
1975
. Etude des problèmes relatifs aux fluctuations piscicoles du lac Tanganyika (Study of problems relating to fluctuations in fish from Lake Tanganyika. In French.).
Bachelor thesis
,
Université de Liège
,
Belgium
.
Cocquyt C. and Vyverman W.,
1994
.
Composition and diversity of the algal flora in the East African Great Lakes: a comparative survey of Lakes Tanganyika, Malawi (Nyasa) and Victoria
.
Archiv für Hydrobiologie, Ergebnisse der Limnologie
44
,
161
172
.
Coulter, G. W.
(Ed.)
,
1991
.
Lake Tanganyika and its Life
.
Oxford University Press
.
London
.
Dahms, H.-U. and Fernando, C. H.,
1992
.
Naupliar development of Mesocyclops aequatorialis similis and Thermocyclops consimilis (Copepoda: Cyclopoida) from Lake Awasa, a tropical rift valley lake in Ethiopia
.
Can. J. Zool.
70
,
2283
2297
.
Dumont, H. J.,
2006
.
Morphology and ecology of a group of small, pelagic, tropical Tropocyclops (Crustacea, Copepoda, Cyclopoida), with the description of a new species from South China
.
Ann. Limnol. - Int. J. Lim.
2006
,
42
(
4
),
261
275
.
Dussart, B. H.,
1980
.
Les Crustacés Copépodes d'Afrique, catalogue et biogéographie
.
Hydrobiologia
72
,
165
170
.
Dussart, B. H. and Defaye, D.,
2001
. Introduction to the Copepoda. (2nd
Edition
) In: H. Dumont (
Ed.
),
Guide to the Identitification of the Microinvertebrates of the Continental Waters of the World
.
Backhuys Publishers
,
Leiden
.
Dussart, B. H. and Defaye, D.,
2006
. World Directory of Custacea Copepoda of Inland Waters .
II- Cyclopiformes
.
Backhuys Publishers
,
Leiden
.
Dussart, B. H., Fernando, C. H., Matsumura-Tundisi, T., and Shiel, R. J.,
1984
.
A review of systematics, distribution and ecology of tropical freshwater zooplankton
.
Hydrobiologia
113
,
77
91
(1984)
.
Gophen, M., Pollingher, E., Ochumba, P.,
1993
. Feeding habits of Tilapia and the limnology of Lake Victoria.
Final Report (1989-1991), T6/93
.
Kinneret Limnological Laboratory
,
Tiberias
.
Gurney, R.,
1928
.
Some copepoda from Tanganyika collected by Mr. S. R. B. Pask
.
Proc. Zool. Soc., London
,
22
,
317
332
.
Haney, J. F.,
1988
.
Diel patterns of zooplankton behavior
.
Bulletin of Marine Science
,
43
,
583
603
.
Harnandez-Chavarria, F. and Schaper, S.,
2000
.
Mesocyclops thermocyclopoides (Copépoda: Cyclopoida): A Scanning Electron Microscopy Study
.
Ravista Latinoamericana de Microbiologia
(2000)
45
,
53
56
.
Hecky, R. E.,
1984
. African Lakes and their efficiencies, A temporal perspective. In: D. G. Meyers and J. R. Strickler (Eds.),
Trophic interaction within aquatic ecosystems
, pp.
405
448
.
American Association for the Advancement of Science
,
Rome
.
Isumbisho, M., Sarmento H., Kaningini B., Micha J.-C. and Descy J.-P.,
2006a
.
Zooplankton of Lake Kivu, East Africa, half a century after the Tanganyika sardine introduction
.
Journal of Plankton Research
28
,
971
989
.
Isumbisho, M., Sarmento H. and Descy J.-P.,
2006b
. Qualitative composition of the pelagic mesozooplankton in Lake Kivu, eastern Africa: impact of Limnothrissa miodon introduction.
In:
M. Isumbisho
(Ed.)
,
Zooplankton Ecology of Lake Kivu (Eastern Africa). PhD thesis
,
Presses Universitaire de Namur
,
Belgium
.
Kiefer, F.,
1956
.
Ruderfusskrebse aus dem Tanganjika See (Copepods of the Tanganyika Sea. In German)
.
Rev. Zool. Bot. Afr.
54
(
3–4
),
241
266
.
Kimirei, I. A., Mgaya, Y. D.,
2007
.
Influence of environmental factors on seasonal changes in clupeid catches in the Kigoma area of Lake Tanganyika
.
African Journal of Aquatic Science
32
,
291
298
.
Kondo, T. and Hori M.,
1986
.
Abundance of zooplankters on a rocky shore of Lake Tanganyika: A preliminary report
.
African Study Monographs
,
6
,
17
23
.
Kurki, H.,
1993
.
Field notes on zooplankton
.
FAO/FINNIDA Research for the Management of the Fisheries on Lake Tanganyika. GCP/RAF/271/FIN-FM/09 (En)
.
Kurki, H.,
1997
.
Résultats de l'échantillonnage de zooplancton sur trois localités du lac Tanganyika : juillet 1993 - décembre 1995
.
FAO/FINNIDA Recherche pour l'Aménagement des Pêches au Lac Tanganyika. GCP/RAF/271/FIN-TD/51 (Fr)
.
Kurki, H.,
1998
.
Results of plankton net and torpedo sampling during cruises on board R/V Tanganyika Explorer
.
FAO/FINNIDA Research for the Management of the Fisheries on Lake Tanganyika GCP/RAF/271/FIN-TD/85(En)
.
Kurki, H., Vuorinen, I., Bosma, E. and Bebwa, D.,
1999
.
Spatial and temporal changes in copepod zooplankton communities of Lake Tanganyika
.
Hydrobiologia
407
,
105
114
.
Langenberg, V. T., Sarvala, J. and Roijackers, R.,
2003
.
Effect of wind induced water movements on nutrients, chlorophyll-a, and primary production in Lake Tanganyika
.
Aquatic Ecosystem Health and Management
,
6
(
3
),
279
288
.
Langenberg, V. T., Tumba, J.-M., Tshibangu, K., Lukwesa, C., Chitamwebwa, D., Bwebwa, D., Makasa, L., Roijackers, R.,
2008
.
Heterogeneity in physical, chemical and planktoncommunity structures in Lake Tanganyika
.
Aquat. Ecosyst. Health Mgmt.
11
(
1
),
16
28
.
Lindberg, K.,
1951
.
Cyclopoides (Crustacés Copépodes)
.
Explor. Hydrobiol. Lac Tanganyika
(1946–1947), III
.
2
,
47
91
.
Mannini, P.,
1999
.
Monitoring programme for Lake Tanganyika
.
Lake Tanganyika Research (LTR) Newsletter
28
,
11
15
.
Mannini, P., Aro, E., Katonda, I., Kissaka, B., Mambona, C., Milindi, E., Paffen, P., Verburg, P.,
1996
.
Pelagic fish stocks of Lake Tanganyika: biology and exploitation
.
FAO/FINNIDA Research for the Management of the Fisheries on Lake Tanganyika. GCP/RAF/271/FIN - TD/53 FAO ROME (En)
.
Mgana, H. F., Herzig, A. and Mgaya, Y. D.,
2014
.
Diel vertical distribution and life history characteristics of Tropodiaptomus simplex and its importance in the diet of Stolothrissa tanganicae
,
Kigoma, Tanzania. Aquat. Ecosyst. Health Mgmt
.
17
(
1
),
14
24
.
Mulimbwa, N.,
1988
. Seasonal changes in the abundance of zooplankters in the northwestern end on Lake Tanganyika during 1987. In: H. Kawanabe and M. K. Kwetuenda
(Eds)
,
Ecological and Limnological Study on Lake Tanganyika and its Adjacent Regions
,
V.
57
59
.
Department of Zoology, Faculty of Science, Kyoto University
,
Kyoto
606
,
Japan
.
Mulimbwa, N., Raeymaekers, J. A. M. and Sarvala, J.,
2014a
.
Seasonal changes in the pelagic catch of two clupeid zooplanktivores in relation to the abundance of copepod zooplankton in the northern end of Lake Tanganyika
,
Aquat. Ecosyst. Health Mgmt.
,
17
(1),
25
33
.
Mulimbwa, N., Sarvala, J., and Raeymaekers, J. A. M.,
2014b
.
Reproductive activities of two zooplanktivorous clupeid fish in relation to the seasonal abundance of copepod prey in the northern end of Lake Tanganyika
.
Belg. J. Zool.
,
144
(
2
),
77
92
July 2014
.
Mwebaza-Ndawula, L.,
1994
.
Changes in relative abundance of zooplankton in northern Lake Victoria, East Africa
.
Hydrobiologia
272
,
259
264
.
Narita, T., Mulimbwa N. and Mizuno T.,
1986
.
Vertical distribution and seasonal abundance of zooplankters in Lake Tanganyika
.
Afr. Study Monogr.
6
,
1
16
.
Phiri, H., Shirakihara, K.,
1999
.
Distribution and seasonal movement of pelagic fish in southern Lake Tanganyika
.
Fisheries Research
41
(1999)
,
63
71
.
Plisnier, P.-D., Langenberg V., Mwape L., Chitamwebwa D., Tshibangu K. and Coenen E.,
1999
.
Limnological annual cycle inferred from physical-chemical fluctuations at three stations of Lake Tanganyika
.
Hydrobiologia
407
,
45
58
.
Plisnier, P.-D., Mgana H., Kimerei I., Chande A., Makasa L., Chimanga J., Zulu F., Cocquyt C., Horion S., Bergamino N., Naithani J., Deleersnijder E., André L., Descy J.-P. and Cornet Y.,
2009
.
Limnological variability and pelagic fish abundance (Stolothrissa tanganicae and Lates stappersii) in Lake Tanganyika
.
Hydrobiologia
(2009)
625
,
117
134
.
Richardson, A. J.,
2008
.
In hot water: zooplankton and climate change
.
ICES Journal of Marine Science: Journal du Conseil
,
65
(
3
),
279
295
.
Roest, F. C.,
1992
.
The pelagic fisheries resources of Lake Tanganyika
.
Mitt.Internat. Verein. Limnol.
23
,
11
15
.
Sars, G. O.,
1909
.
Report on the Copepoda. Zoological Results of the Third Tanganyika Expedition (1904–1905)
.
Proceedings of the Zoological Society of London
,
1
,
31
77
.
Sarvala, J. and Salonen, K.,
1995
.
Preliminary experiments on phytoplankton production ecology in Lake Tanganyika
.
FAO/FINNIDA Research for the Management of the Fisheries in Lake Tanganyika. GCP/RAF/271/FIN-TD/36 (En)
.
Sarvala, J., Salonen, K., Jarvinen, M., Aro, E., Huttula, T., Kotilainen, P., Kurki, H., Langenberg, V., Mannini, P., Peltonen, A., Plisnier, P.-D., Vuorinen, I., Mölsä, H., and Lindqvist, V. O.,
1999
.
Trophic structure of Lake Tanganyika: carbon flows in the pelagic food web
.
Hydrobiologia
407
,
149
173
.
Sarvala, J., Tarvainen, M., Salonen, K., Mölsä, H.,
2002
.
Pelagic foodweb as the basis of fisheries in Lake Tanganyika: A bioenergetics modeling analysis
.
Aquat. Ecosyst. Health Mgmt.
5
(
3
),
283
292
.
Ueda, H., and Reid, J. W.
(Eds.)
,
2003
. Copepoda: Cyclopoida: Genera Mesocyclops and Thermocyclops ,
In:
H. J. Dumont
(Ed.)
,
Guide to the Identification of the Microinvertebrates of the Continental Waters of the World
.
Backhuys Publishers
,
Leiden
.
Vuorinen, I.,
1993
.
Sampling and counting zooplankton of Lake Tanganyika
.
FAO/FINNIDA Research for the Management of the Fisheries in Lake Tanganyika. GCP/RAF/271/FIN-FM/06
.
Vuorinen, I., Kurki, H., Bosma, E., Kalangali, A., Mölsä, H. and Lindqvist, O.,
1999
.
Vertical distribution and migration of pelagic Copepoda in Lake Tanganyika
.
Hydrobiologia
407
,
115
121
.