Copyright # Blackwell Munksgaard 2003
Ecology of Freshwater Fish 2003: 12: 237±240 Printed in Denmark All rights reserved
Lost zooplanktivorous cichlid from Lake Victoria reappears with a new trade Katunzi EFB, Zoutendijk J, Goldschmidt T, Wanink JH, Witte F. Lost zooplanktivorous cichlid from Lake Victoria reappears with a new trade. Ecology of Freshwater Fish 2003: 12: 237±240. # Blackwell Munksgaard, 2003
E. F. B. Katunzi1, J. Zoutendijk2, T. Goldschmidt2, J. H. Wanink2, F. Witte2
Abstract ± The zooplanktivorous cichlid Haplochromis pyrrhocephalus, which was one of the most common haplochromine species in the Mwanza Gulf of Lake Victoria, had almost completely disappeared after the Nile perch upsurge in the 1980s. In the second half of the 1990s, this species suddenly reappeared in the strongly changed ecosystem. Gut content investigation revealed a change in diet. Currently, H. pyrrhocephalus eats large prey more frequently than in the past. These large prey comprise ®sh, shrimps and molluscs. The latter two were never encountered in specimens from the past. Particularly feeding on molluscs was unexpected, as it had been suggested that, because of anatomical constraints, molluscivory and zooplanktivory are incompatible in cichlid ®sh. Our observations provide a new example of the extreme versatility in feeding behaviour in haplochromine cichlids.
1
Tanzania Fisheries Research Institute, PO Box 475, Mwanza, Tanzania, 2Institute of Biology Leiden, University of Leiden, PO Box 9516, 2300 RA Leiden, the Netherlands
Key words: diet shift; ecological changes; Haplochromis pyrrhocephalus; molluscs; Nile perch; prey size F. Witte, Institute of Biology Leiden, University of Leiden, PO Box 9516, 2300 RA, Leiden, the Netherlands; tel.: 31715275027; fax: 31715274900; e-mail:
[email protected] Accepted for publication January 24, 2003
Un resumen en espanÄol se incluye detraÂs del texto principal de este artõÂ culo.
Introduction Lake Victoria, the largest tropical lake in the world, used to be dominated by haplochromine cichlids (Greenwood 1974). During the 1980s, after the upsurge of Nile perch (Lates niloticus L.), an introduced predator, the majority of the haplochromines in the sublittoral and offshore areas disappeared (Ogutu-Ohwayo 1990; Witte et al. 1992). It was estimated that some 200 species became extinct. Concomitantly with the decline of the haplochromines, many other changes were observed in the ecosystem. Most prominent were the increase of the cyprinid Rastrineobola argentea (Pellegrin) and the shrimp Caridina nilotica (Roux), the increase of algal blooms, the decrease in water transparency and oxygen concentrations, and changes in invertebrate composition (Kaufman 1992; Goldschmidt et al. 1993; Mugidde 1993; Hecky et al. 1994; Wanink 1999; Wanink et al. 2001; Katunzi et al. in press). In the second half of the 1990s, after a decline of Nile perch as a result of over®shing, an
unexpected recovery of some haplochromine species was observed (Seehausen et al. 1997; Witte et al. 2000). Of more than 110 species originally found along a research transect across the Mwanza Gulf, some 20 species recovered. Among these are two zooplanktivorous species, Haplochromis (Yssichromis)pyrrhocephalus Witte and Witte Maas and H. (Y.) laparogramma Greenwood and Gee, that currently dominate the haplochromine catches in the northern part of the Mwanza Gulf (Witte et al. 2000; J.H. Wanink, unpublished data). Ecological, morphological and physiological studies are underway to understand how the resurging species cope with their new environment. Here, we report a remarkable change in the feeding habits of H. pyrrhocephalus. Material and methods Haplochromis pyrrhocephalus was collected between 1977 and 2001 in the northern part of the Mwanza Gulf with bottom trawls during the 237
Katunzi et al. Table1. Sampling days, numbers and standard lengths (SL) of fishes used for investigations of stomach and intestine contents. Sampling day
Number
10 October1977 18 November1977 6 January1978 2 June1978 17 August1981 31August1981 29 October1981 10 December1981 22 March1982 5 April1982 3 June1982 18 June1982
2 1 1 5 6 2 3 2 3 2 4 4
Total
35
SL (mm)
Sampling day
67^73 68 67 62^70 56^64 51^63 54^65 62^64 58^71 60^72 55^68 49^69
June1991 10 October1993 19 October1993 21October1993 9 March1999 7 May 2001 29 June 2001 27 September 2001 17 October 2001 20 November 2001 20 December 2001
2 8 1 2 10 3 3 3 3 3 4
Total
42
day. Details on the research stations and catch techniques are given by Goldschmidt et al. (1990) and Witte et al. (1992). Stomachs and intestines of 35 pre-Nile perch specimens, caught in the period 1977±82, were examined (Table 1). For diet analysis of the recovering population, we used 42 specimens collected in the same area between 1991 and 2001. For analysis of the contents of stomachs and intestines, a binocular microscope was used (maximum magni®cation 50). The frequency of occurrence of the major food items in stomachs and intestines was scored for individuals from each of the two periods. To eliminate the effect of unusual collection days and the unequal numbers of ®sh examined per sampling day, we also compared the diets based on sampling days. In this case, gut contents from a single day were pooled. The smallest diameter of the main prey items was measured. Based on these measurements, prey types were classi®ed into four size categories: small (zooplankton 2 mm).
Number
SL (mm) 61^65 54^59 57 55^58 59^69 56^64 54^64 53^59 54^58 50^56 52^61
Results The ranges of standard lengths of the pre- and post-Nile perch specimens investigated were, respectively, 49±73 mm (mean 63 6 mm) and 50±69 mm (mean 58 5 mm) (Table 1). The ®sh of the latter group were slightly smaller (t-test, P 0.000). In 1977±82, the majority (94.3%) of the H. pyrrhocephalus specimens had fed on zooplankton during the day (Table 2). Midge larvae (chaoborids and chironomids) were present in 51.4% of the specimens, insect remains in 20% and ®sh remains in 2.9%. During the period 1991±2001, the frequency of occurrence of zooplankton decreased to 64.3%, whereas that of insects increased to 47.6%. The frequency of shrimps, ®sh and molluscs increased from 0, 2.9 and 0% to 16.7, 16.7 and 21.4%, respectively. Molluscs, ®sh and shrimps were always fragmented; therefore, their maximum size could not be measured, but the smallest diameter of fragments was often larger than 2 mm. Pooling of these large prey types revealed an increase from 2.9% in the ®rst period to 47.6% in the second (Table 2). Most molluscs in the diet were sphaereid bivalves that had been
Table 2. Frequency of occurrence (foo) of the main prey types in the diet of H. pyrrhocephalus during the periods 1977^82 and 1991^2001 in Lake Victoria and P-values of two-tailed Fisher's exact tests (significant values in bold). foo (%) of individual fish Prey zooplankton midge larvae insects shrimps fish molluscs shr fish moll
Size small intermediate intermediate-large large large large large
foo (%) of sampling day
1977^82 (n 35)
1991^2001 (n 42)
P
1977^82 (n 12)
1991^2001 (n 11)
P
94.3 51.4 20.0 0.0 2.9 0.0 2.9
64.3 57.1 47.6 16.7 16.7 21.4 47.6
0.002 0.652 0.016 0.014 0.065 0.003 0.000
100.0 83.3 41.7 0.0 8.3 0.0 8.3
81.8 72.7 81.8 27.3 36.4 18.2 54.5
0.217 0.640 0.089 0.093 0.155 0.217 0.027
Frequencies are given for individual fish and for fish pooled per sampling day. In the last row, large prey are combined (shr shrimps; moll molluscs).
238
Zooplanktivorous cichlid reappears with new trade eaten by 8 out of 10 ®sh collected on 3 March 1999. Bodies without shell remains of two unidenti®ed gastropods were present in two specimens, one from 3 March 1999 and one from 10 October 1991. As far as we could establish, most of the ®sh remains in the guts belonged to the cyprinid Rastrineobola argentea. When using sampling days to test the diet shift, the same trend was present as in individual ®sh. However, except for the pooled large prey items, differences between the two periods were not signi®cant, possibly as a result of the small sample sizes (Table 2). Discussion Comparing the diet of H. pyrrhocephalus before and after the environmental changes by using individual ®sh revealed a dramatic change in food composition. Unusual sampling days may have biased these results. However, when testing sampling days instead of individual ®sh, the increase in frequency of occurrence of the pooled large prey types remained signi®cant in spite of small sample sizes. As both the maximum and the mean size of the ®sh in the post-Nile perch sample were slightly smaller, the increase in large prey cannot be explained by the size of the investigated H. pyrrhocephalus. There are other causes, however, which may explain the increase. In the ®rst place, there was an increase of the cyprinid Rastrineobola argentea and the shrimp Caridina nilotica (Goldschmidt et al. 1993; Wanink 1999) in the lake. Further, the formerly common insectivores, molluscivores and piscivores are currently rare (Seehausen et al. 1997; Witte et al. 2000; J.H. Wanink, unpublished data). The increase of profitable prey types and the absence of ef®cient competitors may have given H. pyrrhocephalus the opportunity to include new prey types in its diet. However, molluscs do not seem to be very pro®table because of a relatively low ratio of energy and handling time, and because of the disadvantage of swallowing large amounts of relatively heavy and indigestible material (Hoogerhoud 1987; Slootweg et al. 1993). Therefore, it is possible that the decrease in water clarity, making it dif®cult to spot small prey, may also have played a role in the dietary shift. Shrimps and molluscs had never been observed before in the diet of H. pyrrhocephalus. Apart from their absence in the 35 specimens of H. pyrrhocephalus of the period 1977±82 that were investigated in this study, these prey were also not found in the 30 specimens that had been collected during nightly catches (Goldschmidt et al. 1990). Likewise, the guts of the closely related species H.
(Y.) heusinkveldi Witte and Witte-Maas and H. (Y.) laparogramma, and several other zooplanktivorous haplochromines studied in the pre-Nile perch period (together more than 300 specimens) never contained molluscs or shrimps (Goldschmidt et al. 1990; Van Oijen & Witte 1996; F. Witte, unpublished data). In the post-Nile perch period, shifts to insects and ®sh were observed in the zooplanktivorous Haplochromis tanaos van Oijen and Witte (van Oijen & Witte 1996), whereas shifts to insects and shrimps were found in the zooplanktivorous cyprinid R. argentea (Wanink 1998). Molluscs, however, were not found in these species after the ecological changes. The intestines of several of the individuals of H. pyrrhocephalus were crammed with sphaereid bivalves. Therefore, it is unlikely that, in the postNile perch period, molluscs have been ingested accidentally by H. pyrrhocephalus while feeding on other bottom-dwelling prey. Molluscivory is remarkable because H. pyrrhocephalus does not seem to have the required anatomy for crushing or shelling that is normally found in molluscivores (Greenwood 1974; Barel 1983). Our observation provides a new example of the versatility in feeding behaviour in haplochromine cichlids. Earlier examples concerned aquarium and ®eld observations in Lake Malawi species that were regarded specialised algae scrapers. In tank experiments, Liem (1980) found an unexpected, wide feeding repertoire for Petrotilapia tridentiger Trewavas. Therefore, he suggested that this species is not only a specialist, but also a jack of all trades. These observations, also referred to as `Liem's paradox', have been criticised as being laboratory artefacts (Van Oijen 1982; Yamaoka 1983). However, the ®eldwork of Mckaye & Marsh (1983) supported Liem. This showed that aufwuchs feeding Mbuna, including P. tridentiger and Pseudotropheus zebra (Boulenger), indeed feed on zooplankton and other items, such as phytoplankton, detritus, ®sh fry and ®sh eggs, when abundant in the ®eld. Barel (1983) did not consider Liem's ®ndings a true paradox. He showed that the repertoires mentioned by Liem (1980) and Mckaye & Marsh (1983) require execution of the two core functions, sucking and biting. According to Barel (1983), these two functions are, to a certain extent, compatible, making every cichlid a jack of a few trades. However, Barel (1983) suggested that combination of molluscivory and zooplankton feeding is unlikely, as a rotational, symmetric, expanded buccal cavity is needed for ef®cient suction, and this is absent in molluscivores. Moreover, zooplankton was virtually never observed in mollusc crushers and shellers (Barel 1983; 239
Katunzi et al. Katunzi 1983). Morphological studies have to reveal how the two feeding trades could be combined in H. pyrrhocephalus. Resumen 1. El cõ clido zooplanctõ voro Haplochromis pyrrhocephalus, que era una de las especies de haplochroÂmidos mas abundantes en el Golfo de Mwanza del Lago Victoria desaparecio practicamente a mediados de los 80 asociado al resurgir de la Perca del Nilo. En la segunda mitad de los 90, esta especie reaparecio repentinamente en este ecosistema substantialmente cambiado. 2. Investigaciones sobre contenidos estomacales revelaron un cambio en la dieta. Ahora, H. pyrrhocephalus se alimenta mas frecuentemente de presas de mayor tamanÄo que en el pasado. Estas presas incluyen peces, gambas y moluscos. Estos dos uÂltimos grupos nunca fueron encontrados en el pasado. Alimentarse de moluscos fue inesperado ya que se ha sugerido que, debido a limitaciones anatoÂmicas, una alimentacioÂn simultanea de moluscos y zooplancton es incompatible en cõ chlidos. Nuestras observaciones aportan un nuevo ejemplo de versatilidad extrema en el comportamiento alimenticio de cõ chlidos haplochroÂmidos.
Acknowledgements We thank our colleagues from TAFIRI (Mwanza Centre) and HEST for their assistance, Aloys Peter, Mhoja Kayeba and Ruben Enoka for help with ®shing. Ole Seehausen is thanked for collecting some of the ®sh, Frank Wesseling for identi®cation of the bivalves and Kees Barel for comments on an earlier draft. Financial support was obtained from WOTRO (grants W 87±189, W 84±488), the section DPO of the Netherlands Ministry of Foreign Affairs, Stichting Leids Universiteits-Fonds, Schure-Beijerinck-Popping Fonds, van Tienhoven Stichting and Yellow Springs Instruments.
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