African Journal of Aquatic Science 2012, 37(3): 277–288 Printed in South Africa — All rights reserved Copyright © NISC (Pty) Ltd AFRICAN JOURNAL OF AQUATIC SCIENCE ISSN 1608-5914 EISSN 1727-9364 http://dx.doi.org/10.2989/16085914.2012.674009 Macroinvertebrates associated with two submerged macrophytes, Lagarosiphon ilicifolius and Vallisneria aethiopica, in the Sanyati Basin, Lake Kariba, Zimbabwe: effect of plant morphological complexity C Phiri1*, A Chakona2 and JA Day3 1 University of Zimbabwe, Lake Kariba Research Station, PO Box 48, Kariba, Zimbabwe Department of Ichthyology and Fisheries Science, Rhodes University, PO Box 94, Grahamstown 6140, South Africa 3 Freshwater Research Unit, Department of Zoology, University of Cape Town, Rhodes Gift 7707, South Africa * Corresponding author, e-mail: crispenphiri@gmail.com 2 Vallisneria aethiopica and Lagarosiphon ilicifolius are common and abundant submerged macrophytes in Lake Kariba, Zimbabwe. The two species have distinct structural morphologies, with Vallisneria consisting of long ribbonlike leaves, while Lagarosiphon has filiform stems with numerous small alternate leaves. This study investigated the effect of these architectural differences between the two plant species on their epiphytic macroinvertebrate assemblages in the shallow inshore waters of Lake Kariba. Ten sites were sampled on three occasions between May and July 2005. A total of 56 macroinvertebrate taxa was collected, 48 from Lagarosiphon and 45 from Vallisneria. Generally, the two plant species were associated with similar macroinvertebrate communities, but the average abundances of most taxa, and thus the overall macroinvertebrate abundances, were significantly greater on Lagarosiphon. The main macroinvertebrate functional feeding groups found on both plant species were collectorgatherers, grazers and predators, all of which were significantly more abundant on Lagarosiphon. Although the macroinvertebrate assemblages associated with Vallisneria and Lagarosiphon generally consisted of the same taxa, there were distinct and significant differences between them, probably due to the architectural differences between the two submerged macrophytes. Keywords: abundance, aquatic vegetation, community composition, diversity, habitat heterogeneity Introduction Macroinvertebrates are essential elements in the functioning of aquatic ecosystems, playing a vital role in processes such as food web dynamics, productivity, nutrient cycling and decomposition (Diehl and Kornijow 1998, Cheruvelil et al. 2000, Jackson 2003). Macroinvertebrates may reside on or within sediments, or may be associated with aquatic vegetation. Habitat structure plays an important role in structuring ecological communities and maintaining the integrity of ecosystems. In aquatic environments, habitat structure affects the richness, abundance and biomass of invertebrates (Chilton 1990, Blindow et al. 1993, Rennie and Jackson 2005) and fish (Weaver et al. 1996, Johnson et al. 2007). Generally, epiphytic macroinvertebrates are more diverse and abundant than those associated with bare sediments (Orth et al. 1984, Pardue and Webb 1985, Beckett et al. 1992). The abundance and diversity of epiphytic macroinvertebrates is affected by macrophyte abundance, structure and community composition (Cheruvelil et al. 2002). Epiphytic macroinvertebrates tend to be more abundant on plants with complex morphologies than those with simple morphologies (Cheruvelil et al. 2000, 2002), because morphologically complex plants have more attachment and better refuge sites than morphologically simple plants (Thomaz et al. 2008). Thus, plants with finely dissected leaves generally have higher invertebrate abundances per unit biomass than broad-leaved plants (Rooke 1986a, 1986b, Chilton 1990). In contrast, however, some studies (Brown et al. 1988, Cyr and Downing 1988a, Irvine et al. 1990) showed that morphologically complex macrophytes do not support more invertebrates than morphologically simple ones. Lagarosiphon ilicifolius Obermeyer and Vallisneria aethiopica Frenzl are structurally different submerged macrophytes that are common and abundant in shallow marginal areas of Lake Kariba, Zimbabwe. Lagarosiphon Harvey (Hydrocharitaceae) is a genus of perennial submerged freshwater plants consisting of nine species that are naturally distributed in Africa south of the Sahara, including Madagascar (Symoens and Triest 1983). It is usually rooted, but occasionally may detach and be free-floating. Its roots are adventitious and unbranched, and its filiform stems can be up to 5 m long. The stems are circular in transverse section, and branching is axillary. Its leaves are sessile, predominantly alternate but may also be subopposite or subverticillate (Symoens and Triest 1983). The stems of L. ilicifolius in Lake Kariba are normally about 3 mm in diameter, and its leaves, which are mostly alternate, are 2–4 mm broad and 7–12 mm long (CP pers. obs.). The leaves may be closely arranged, giving the stem and leaves together a cylindrical outline. The number of African Journal of Aquatic Science is co-published by NISC (Pty) Ltd and Taylor & Francis 278 leaves per centimetre of stem ranges between 16 and 24 (CP pers. obs.). Vallisneria L. (Hydrocharitaceae Juss.) has a cosmopolitan distribution (Les et al. 2008). Its taxonomic diversity is still in doubt, but it is estimated that there are about 4–10 species worldwide (Les et al. 2008). Vallisneria species are dioecious, annual or perennial plants. The plants have no stem and, in Lake Kariba, they have from 6 to 30 (CP pers. obs.) basally arranged, ribbon-like leaves with entire or minutely serrated margins (Russell 1977). Vallisneria in Lake Kariba normally has leaves with a maximum breadth of about 10 mm and a maximum length (measured from point of intersection with shoot to the apex) of about 40 cm (CP pers. obs.). Thus Lagarosiphon is morphologically more complex than Vallisneria. Both plants are important habitats and sources of food for a number of organisms. Lagarosiphon spp. offer a substrate for a great variety of invertebrates (Symoens and Triest 1983). According to Feldman (2001), the leaves of Vallisneria may support large numbers of invertebrates. Although Lake Kariba, 484 masl, one of the largest manmade lakes in Africa, was created over 50 years ago, and has since then undergone changes in its physical and chemical characteristics, with marked succession in the development of its plant and animal communities (McLachlan and McLachlan 1971, Kenmuir 1984, Machena 1989, Karenge and Kolding 1995), very little is known of the ecology of the macroinvertebrate communities associated with its submerged macrophytes. Therefore, the purpose of the present study was to determine whether epiphytic macroinvertebrate abundance, composition and diversity differed between Lagarosiphon and Vallisneria in Lake Kariba, a large manmade reservoir. The hypothesis tested was that the greater morphological complexity of Lagarosiphon would result in greater macroinvertebrate abundance and diversity, as well as a different macroinvertebrate composition, to that associated with the morphologically less complex Vallisneria. Materials and methods Study area The study was carried out at 10 sites in water 0.5–1 m deep along the shores of the Sanyati Basin, the north-eastern basin of Lake Kariba (Figure 1). Methods Over a period of three months from May to July 2005 samples of epiphytic invertebrates associated with Lagarosiphon and Vallisneria were collected monthly. At each site, for both plant species, 5–7 monospecific patches were randomly chosen at different points along a stretch of 100–200 m of the shoreline, and plants collected for sampling of epiphytic macroinvertebrates. Only those patches that were at least 1 m2 in size and had more than five individual plants randomly scattered within a 1 m2 segment were sampled. The minimum distance between any two patches sampled was about 2 m. A 0.25 m × 0.25 m square, framed hand net of 500 μm mesh with a detachable sample collection bottle was used to sample macroinvertebrates. The net was placed Phiri, Chakona and Day alongside the plants while ensuring minimum disturbance. Using scissors, at least three plants were cut at the base, placed into the net and brought out of the water. The plants were kept within the hand net while they were thoroughly washed in a bucket of water. The macroinvertebrates washed into the detachable bottle were transferred to a sample bottle and preserved in 70% ethanol for taxonomic analysis and enumeration in the laboratory. The washed plant material was placed in labelled plastic bags, stored in cooler boxes and later dried at 105 °C for 24 h to determine dry mass. Macroinvertebrate identification was based on keys by Edmondson (1959), Day et al. (1999, 2001a, 2001b, 2003), Day and de Moor (2002a, 2002b) and de Moor et al. (2003a, 2003b). The macroinvertebrates were identified to genus level, except for taxonomically challenging groups such as Oligochaeta, Hydracarina, Cyclopoida, Ostracoda and most of the Diptera larvae. The macroinvertebrates were also categorised into primary feeding groups according to Merritt and Cummings (1996), so as to assess the feeding dynamics of the invertebrates associated with the two macrophyte species. For Sites 1 and 2, the macroinvertebrate data presented here are for the month of May only, due to spoilage of the samples obtained in June and July. Data analysis Macroinvertebrate abundance was standardised by plant dry weight and abundances expressed as numbers of animals per gram of plant dry mass. For each sample the number of taxa (richness) was recorded and the Shannon-Wiener (H′) diversity and evenness indices were obtained using PRIMER-e version 6.1.5 software (Clarke and Gorley 2006). Evenness is a measure of the proportional distribution of different taxa in a community and the more the variation in the distribution the lower its evenness. Before analysing for any differences in macroinvertebrate assemblage between the two plants, data were tested for normality and homogeneity of variance using Shapiro-Wilks normality test and the variance ratio F-test respectively (Sokal and Rohlf 1981). The data were not normally distributed, variances were non-homogeneous, and transformation using either log n or log (n + 1) could not normalise the dataset. Thus, the statistical differences in macroinvertebrate assemblages between the two macrophyte species were assessed using a non-parametric test, the Wilcoxon signed-rank (paired samples) test. Simfit version 6.0.24 (Bardsley 2009) was used for statistical analysis of the data. Non-parametric multivariate analyses were also used in analysing the data for differences in epiphytic macroinvertebrate community structure of the two submerged plant species using PRIMER-e version 6.1.5 (Clarke and Gorley 2006). Assemblage patterns were visualised in reduced dimensional space using non-metric multidimensional scaling (nMDS). Analysis of similarities (ANOSIM) was used to test for differences in macroinvertebrate community structure. The similarities percentages procedure in SIMPER was used to ascertain the taxa responsible for similarities and dissimilarities between samples. The macroinvertebrate abundances were first square-root transformed and BrayCurtis similarity was used as a measure of resemblance for both ANOSIM and SIMPER. African Journal of Aquatic Science 2012, 37(3): 277–288 279 Vallisneria was present at all 10 sites during the study period. Although Lagarosiphon tended to be the dominant plant at most sites, it was absent from Site 4, which receives effluent from an adjacent crocodile breeding farm. The Lagarosiphon samples from Sites 7 and 9, as well as one Vallisneria sample from Site 4, all obtained in May 2005, are omitted from the analysis, as they did not contain any invertebrates. Sites 7 and 9 were both within harbours, characterised by relatively high levels of boating activities as well as the maintenance and repair of boats (see Phiri et al. 2007). The minimum and maximum numbers of macroinvertebrates collected from Lagarosiphon were 9.9 and 128.2 g–1 plant dry mass, respectively, compared to 0.8 and 25.0 g–1 plant dry mass for Vallisneria. The overall mean macroinvertebrate abundance associated with Lagarosiphon was significantly greater than that on Vallisneria (Wilcoxon signed-rank test, Z = 3.893, p < 0.05) (Table 1). There was no significant difference in the number of taxa obtained from the two macrophytes (Wilcoxon signed-rank test, Z = 0.452, p < 0.05) (Table 1). The Shannon diversity index of the macroinvertebrate assemblage was also not significantly different between the two plant species (Wilcoxon signedrank test, Z = 0.799, p < 0.05) (Table 1). A total of 56 macroinvertebrate taxa were obtained overall, AFRICA ZAMBIA ezi River mb Za of which 16 were dominant on both plants. Forty-eight taxa were collected from Lagarosiphon compared to 45 from Vallisneria. In order of decreasing abundance, the most abundant and frequently occurring taxa on Lagarosiphon were Chironominae, Naididae, Caenis sp., Cloeon sp., Dugesia sp., Orthocladiinae, Bulinus depressus, Lymnaea columella, Physa acuta, Pseudagrion sp., Orthotrichia sp., Melanoides tuberculata, Acari and Ostracoda (Table 2), which together made up 89.0% of the total number of organisms collected from Lagarosiphon. With respect to macroinvertebrate orders, Diptera, Gastropoda, Ephemeroptera and Odonata, with 26.3%, 25.0%, 17.1% and 6.7% relative abundance, respectively, dominated the macroinvertebrate assemblage on Lagarosiphon (Table 2). Twelve taxa, M. tuberculata, B. depressus, Orthocladiinae, Chironominae, Caenis sp., L. columella, Dugesia sp., Orthotrichia sp., Cloeon sp., Naididae, Ostracoda and P. acuta made up 81.8% of the total macroinvertebrate abundance associated with Vallisneria. The gastropods, with a relative percent abundance of 44.7%, dominated the macroinvertebrate assemblage on Vallisneria, followed by Diptera (20.8%), Ephemeroptera (9.1%) and Odonata (6.6%). Thus, the macroinvertebrate assemblages associated with Lagarosiphon and Vallisneria largely comprised the same taxa, although the abundances of the dominant and common taxa were generally greater on Lagarosiphon than on Vallisneria at all sampling sites (Figure 2). ZAMBIA MOZAMBIQUE 18° S Kariba Zimbabwe a rib Ka 0 v Ri ezi b Kariba am 10 50 100 150 km 98 7 6 5 4 5 River r Sha ngani Rive Lake Chivero 10 15 km ZIMBABWE Cha iver rara R 3 16°31′ S er Nyaodza Riv at i La ke Sa ny Livingstone Hwange Z 0 er Results Harare Sanyati Basin ZIMBABWE Gweru eR ve r i 20° S Bulawayo BOTSWANA 1 32° E 2 Sanyati River 28°50′ E d Gachegach 28° E n Su KEY Study site National boundary Basin boundary e River Figure 1: Map of the study area showing locations of 10 sampling stations in the Sanyati Basin, Lake Kariba Table 1: Mean community indices (± SE) of macroinvertebrates associated with Lagarosiphon and Vallisneria in Lake Kariba in 2005. The test statistic (Z) of the Wilcoxon paired-sample signed-rank test and the p-values are shown Index –1 Mean total abundance (no. g dry mass of plant) Richness (no. of taxa g–1 dry mass of plant) Shannon diversity index (H’) Lagarosiphon (n = 21) 40.9 ± 7.3 0.99 ± 0.11 2.03 ± 0.09 Vallisneria (n = 23) 7.8 ± 1.4 0.93 ± 0.07 1.93 ± 0.09 Test statistic (Z) 3.893 0.452 0.799 p-value <0.001 0.658 0.432 Phiri, Chakona and Day 280 Table 2: Macroinvertebrates associated with Lagarosiphon and Vallisneria in Lake Kariba in 2005; n = number of samples, MA = mean abundance (no. g–1 of plant dry mass) ± SE, %MRA = mean percent relative abundance, %Freq = percent frequency of occurrence, √ = present in low numbers and frequency, – = absent Order Family Taxon Rhynchobdellida Oligochaeta1 Nematoda Hirudinae Gastropoda Planariidae Naididae Dugesia sp. Naididae Nematoda Alboglossiphonia sp. Glossiphonidae Isotomidae Poduridae Lobogenes sp. Lymnaea columella Physa acuta Bulinus depressus Bulinus forskalii Biomphalaria pfeiferri Cleopatra nsedwensis Melanoides tuberculata Bellamya capillata Ferrisia sp. Sphaerium sp. Acari Daphnia sp. Cyclopoida Cyclestheria hislopi Ostracoda Isotomidae Poduridae Polymitarcyidae Caenidae Baetidae Povilla sp. Caenis sp. Cloeon sp. Coenagrionidae Pseudagrion sp. Enallagma sp. Ischnura sp. Ictinogomphus sp. Notogomphus sp. Phyllomacromia sp. Hemicordulia sp. Lestes sp. Pantala sp. Bradinopyga sp. Trithemis sp. Zyxomma sp. Appasus sp. Micronecta sp. Plea sp. Dysticus sp. Neochetina sp. Hydrobiidae Lymnaedae Physidae Planorbidae Thiaridae Viviparidae Anyclidae Sphaeridae Hydracarina Cladocera Cyclopoida Conchostraca Ostracoda Collembola Daphniidae Cyclopoida Cyclestheriidae Ephemeroptera Odonata Gomphidae Cordulidae Lestidae Libellulidae Hemiptera Coleoptera Belostomatidae Corixidae Pleidae Dysticidae Curculionidae Trichoptera Hydroptilidae Ecnomidae Leptoceridae Lepidoptera Diptera Philopotamidae Crambidae Ceratopogonidae Chaoboridae Chironomidae Culicidae Sciomyzidae 1 Largely Naididae Orthotrichia sp. Ecnomus sp. Leptocerina sp. Athripsoides sp. Philopotamidae Nymphula sp. Bezzia sp. Chaoborus sp. Chironominae Tanypodinae Orthocladiinae Anopheles sp. Culex sp. Sciomyzidae Lagarosiphon (n = 21) MA %MRA %Freq 2.5 ± 1.4 4.6 ± 2.0 71.4 4.1 ± 0.9 10.4 ± 1.9 90.5 √ √ √ √ √ √ 8.3 ± 2.3 25.0 ± 4.8 95.0 √ √ √ 2.1 ± 0.9 8.3 ± 3.8 76.2 1.7 ± 0.6 4.6 ± 1.5 71.4 2.3 ± 0.8 6.4 ± 2.1 90.5 √ √ √ √ √ √ √ √ √ 1.1 ± 0.7 1.9 ± 1.0 47.6 √ √ √ √ √ √ √ √ √ 1.0 ± 0.5 1.5 ± 0.5 71.4 − − − √ √ √ √ √ √ 1.0 ± 0.5 1.8 ± 0.7 61.9 √ √ √ √ √ √ 7.3 ± 1.9 17.1 ± 3.4 100.0 − − − 3.9 ± 1.2 9.6 ± 3.2 76.2 3.3 ± 1.0 7.4 ± 1.7 95.2 2.5 ± 1.1 6.7 ± 1.8 100.0 1.5 ± 0.8 3.4 ± 0.9 100.0 √ √ √ 0.7 ± 0.3 2.2 ± 0.7 81.0 √ √ √ √ √ √ √ √ √ √ √ √ √ √ √ − − − √ √ √ √ √ √ − − − − − − √ √ √ √ √ √ √ √ √ √ √ √ 1.9 ± 0.6 4.7 ± 1.3 90.5 1.1 ± 0.4 2.8 ± 1.0 71.4 0.8 ± 0.3 1.8 ± 0.5 81.0 − − − − − − √ √ √ √ √ √ 11.4 ± 3.6 26.3 ± 4.6 100 − − − √ √ √ 8.2 ± 2.6 18.9 ± 3.3 100.0 √ √ √ 81.0 2.4 ± 0.7 5.9 ± 1.1 √ √ √ √ √ √ √ √ √ Vallisneria (n = 25) MA %MRA %Freq √ √ √ 0.3 ± 0.1 4.4 ± 1.5 68.0 − − − √ √ √ 3.4 ± 0.8 44.7 ± 5.5 100.0 √ √ √ 0.7 ± 0.2 12.6 ± 3.4 84.0 0.2 ± 0.1 5.0 ± 1.6 52.0 0.9 ± 0.3 11.6 ± 2.8 76.0 √ √ √ √ √ √ √ √ √ 1.1 ± 0.5 8.9 ± 3.7 48.0 √ √ √ √ √ √ √ √ √ √ √ √ √ √ √ √ √ √ √ √ √ 0.3 ± 0.2 2.2 ± 1.3 32.0 √ √ √ − − − 1.1 ± 0.5 9.1 ± 2.6 68.0 √ √ √ 0.8 ± 0.5 5.5 ± 2.3 36.0 0.3 ± 0.1 3.5 ± 1.1 52.0 0.3 ± 0.1 6.6 ± 1.6 80.0 √ √ √ √ √ √ √ √ √ √ √ √ − − − − − − √ √ √ − − − √ √ √ √ √ √ √ √ √ √ √ √ √ √ √ √ √ √ − − − − − − − − − 0.4 ± 0.2 4.9 ± 1.5 68.0 0.3 ± 0.1 3.8 ± 1.4 40.0 √ √ √ √ √ √ √ √ √ − − − √ √ √ 1.9 ± 0.5 20.8 ± 3.6 92.0 √ √ √ − − − 0.8 ± 0.2 11.1 ± 2.1 88.0 √ √ √ 0.9 ± 0.4 7.1 ± 2.5 64.0 − − − − − − √ √ √ African Journal of Aquatic Science 2012, 37(3): 277–288 281 Dugesia sp. 1.2 Naididae L. columella P. acuta B. depressus M. tuberculata Caenis sp. Cloeon sp. Coenagrionidae Trichoptera Chironominae Orthocladiinae Grazers Predators Lagarosiphon Vallisneria 1.0 0.8 0.6 0.4 0.2 1.2 1.0 0.8 0.6 0.4 ABUNDANCE (Log x + 1) 0.2 1.2 1.0 0.8 0.6 0.4 0.2 1.4 1.2 1.0 0.8 0.6 0.4 0.2 1.8 1.6 1.4 1.2 1.0 0.8 0.6 0.4 0.2 Collector-gatherers 1 2 3 4 5 6 7 8 9 10 1 2 3 4 5 6 SITE 7 8 9 10 1 2 3 4 5 6 7 8 9 10 Figure 2: Mean abundances (no. per gram of plant dry mass) of the most abundant and frequently occurring macroinvertebrate taxa and functional feeding groups associated with Lagarosiphon and Vallisneria in Lake Kariba in 2005. Error bars denote SE Phiri, Chakona and Day 282 The mean abundances of Dugesia sp., Naididae, P. acuta, Caenis sp., Cloeon sp., Coenagrionidae (Ischnura sp., Enallagma sp. and Pseudagrion sp.), Trichoptera (Ecnomus sp., Orthotrichia sp., Athripsoides sp., Leptocerina sp. and Philopotamidae), Chironominae and Orthocladiinae were significantly greater on Lagarosiphon than on Vallisneria (Wilcoxon signed-rank tests, p < 0.05) (Table 3). The mean abundances of L. columella, B. depressus and M. tuberculata were not significantly different between the two plant species (Wilcoxon signed-rank tests, p > 0.05) (Table 3). The dipteran subfamily Chironominae dominated the epiphytic macroinvertebrate community on Lagarosiphon, with a mean abundance (8.2 ± 2.6), which was significantly greater than that of most other taxa (Wilcoxon signed-rank tests, p < 0.05), except for Naididae with which there was no significant difference (Wilcoxon signed-rank test, Z = 1.590, p > 0.05). On Vallisneria, the mean abundance of Chironominae was significantly greater than that of Dugesia, Naididae, P. acuta, M. tubercuta, Cloeon, Coenagrionidae and Trichoptera (Wilcoxon signed-rank test, p < 0.05), but did not differ significantly from L. columella, B. depressus and Caenis (Wilcoxon signed-rank test, p > 0.05). The abundances of Naididae, Dugesia, Chironominae, P. acuta, Cloeon and Coenagrionidae were more than 500% greater on Lagarosiphon than on Vallisneria (Table 3). The main macroinvertebrate functional feeding groups associated with the two macrophyte species were collectorgatherers, grazers and predators, with filterers occurring in low numbers on both plants (Table 3). Collector-gatherers, grazers and predators were significantly more abundant on Lagarosiphon than on Vallisneria (Wilcoxon signed-rank tests, p < 0.05), while the abundance of collector-filterers did not differ between the two plant species (Wilcoxon signedrank test, p > 0.05) (Table 3). Collector-gatherers made up nearly 60% of the total number of organisms associated with Lagarosiphon, and their abundance was significantly greater than those of the other functional feeding groups (Wilcoxon signed-rank tests, p < 0.05). There was no significant difference in the abundances of grazers and predators on Lagarosiphon (Wilcoxon signed-rank test, Z = 0.278, p > 0.05). Filterers were significantly less abundant than the other three functional feeding groups on both Lagarosiphon and Vallisneria (Wilcoxon signed-rank tests, p < 0.05). The mean abundances of collector-gatherers and grazers on Vallisneria were not significantly different (Wilcoxon signedrank test, Z = 1.077, p > 0.05), but both were significantly greater than predators (Wilcoxon signed-rank test, p < 0.05). The comparison of percent differences in abundance of each functional feeding group on the two macrophyte species showed that the mean abundances of collector-gatherers and predators were more than 500%, while those of filterers and grazers were about 200% greater on Lagarosiphon than on Vallisneria (Table 3). Analysis of the epiphytic macroinvertebrate assemblages on the two plant species, using non-metric multidimensional scaling (MDS), showed a clear separation of these communities (Figure 3). The distribution of macroinvertebrate samples from Lagarosiphon was clumped, while that from Vallisneria was more broadly scattered (Figure 3), due to the greater abundance of a few taxa such as Chinorominae and Naididae on Lagarosiphon than on Vallisneria (Figure 3). ANOSIM showed that there were significant differences in macroinvertebrate community structure associated with the Lagarosiphon and Vallisneria (Global R = 0.356, p < 0.001), with high average dissimilarity of 72.03%. Fourteen taxa were identified by SIMPER as significantly contributing to differences in macroinvertebrate community structure on the two plant species (Table 4). All 14 taxa occurred on both plant species, and SIMPER also showed that, with the exception of M. tuberculata, which was slightly more abundant on Vallisneria, most taxa were much more abundant on Lagarosiphon (Table 4). Table 3: Comparisons of difference using the Wilcoxon signed-rank test in mean abundances (no. per gram plant dry mass) of major taxa and functional feeding groups associated with Lagarosiphon and Vallisneria in Lake Kariba in 2005. Significant p-values in bold type. Percent difference indicates how much higher the abundance of each taxon and functional feeding group on Lagarosiphon was compared to that on Vallisneria Taxon/functional feeding group Taxon Dugesia sp. Naididae L. columella P. acuta B. depressus M. tuberculata Caenis sp. Cloeon sp. Coenagrionidae Trichoptera Chironominae Orthocladiinae Functional feeding group Collector-gatherers Filterers Grazers Predators Lagarosiphon (n = 21) Vallisneria (n = 23) Test statistic (Z) p-value 2.5 ± 1.4 4.1 ± 0.9 2.1 ± 0.9 1.7 ± 0.6 2.3 ± 0.8 1.2 ± 0.7 3.9 ± 1.2 3.3 ± 1.0 2.3 ± 1.1 1.9 ± 0.6 8.2 ± 2.6 2.4 ± 0.7 0.2 ± 0.1 0.2 ± 0.1 0.5 ± 0.1 0.2 ± 0.1 1.0 ± 0.4 0.7 ± 0.5 0.9 ± 0.6 0.4 ± 0.1 0.3 ± 0.1 0.4 ± 0.2 0.8 ± 0.2 0.9 ± 0.5 2.874 3.789 1.027 2.698 1.529 0.588 2.556 3.823 2.556 2.676 3.406 2.155 0.001 <0.001 0.312 0.002 0.128 0.569 0.004 <0.001 0.004 0.003 <0.001 0.015 1 150 1 950 320 750 130 71 333 725 667 375 925 167 23.1 ± 5.4 0.3 ± 0.2 8.3 ± 2.3 8.0 ± 2.4 3.6 ± 1.1 0.1 ± 0.1 2.7 ± 0.7 1.0 ± 0.2 3.719 1.540 3.059 3.406 <0.001 0.129 <0.001 <0.001 542 200 207 700 % Difference African Journal of Aquatic Science 2012, 37(3): 277–288 283 Discussion This study shows that the two plant species were characterised by similar epiphytic macroinvertebrate assemblages, although most taxa occurred in much greater abundance on Lagarosiphon than on Vallisneria. The differences in macroinvertebrate community can be attributed to differences in the physical morphology of the two plants. The small but numerous leaves on the stems of Lagarosiphon create a more complex habitat, harbouring larger quantities of particulate organic matter as well as providing more attachment surfaces for invertebrates than the long ribbonlike leaves of Vallisneria. The surfaces of macrophytes with complex morphologies have been shown not only to trap greater amounts of fine and coarse particulate organic matter (Rooke 1986a), but also have greater amounts of periphyton (Warfe and Barmuta 2006), which is an important food source for many epiphytic invertebrates. Complex morphology also provides better refuge for invertebrates from fish predation (Irvine et al. 1990, Cheruvelil et al. 2002) 2D Stress: 0.2 Vegetation Lagarosiphon Vallisneria Figure 3: nMDS plot of epiphytic macroinvertebrate communities associated with Lagarosiphon and Vallisneria in Lake Kariba in 2005 and fish predators are generally less effective in structurally complex habitats (Crowder and Cooper 1982, Swisher et al. 1998, Rennie and Jackson 2005). Thus, the greater morphological complexity of Lagarosiphon possibly increased food availability and protection from predation for macroinvertebrates and so resulted in much greater abundances of macroinvertebrates, especially collector-gatherers. A number of studies have found similar results when comparing differences in epiphytic macroinvertebrate abundances between macrophytes of differing morphological complexity (e.g. Cattaneo et al. 1998, Bogut et al. 2007). Cheruvelil et al. (2000) also found that, for macrophyte species with similar morphological structure, there were no differences in the abundance of macroinvertebrates. However, the effect of structural differences among aquatic macrophyte species on epiphytic invertebrates is debated because other studies (Cyr and Downing 1988a, Brown et al. 1988, Irvine et al. 1990) found no difference in invertebrate abundances among structurally different macrophyte species. On both plants the Chironomidae were largely represented by the subfamilies of Chironominae and Orthacladiinae, with small numbers of Tanypodinae. The abundances of all three subfamilies were much greater on Lagarosiphon than on Vallisneria. The Naididae also made up a significant portion of the macroinvertebrate community on Lagarosiphon. Chironomids are among the most successful aquatic macroinvertebrate taxa (Mackie 2001). The dominance of Chironomidae in epiphytic macroinvertebrate assemblages on various aquatic plants has been observed in a number of studies (e.g. Tessier et al. 2004, Albertoni et al. 2007, Bogut et al. 2007). This has been attributed to their wide range of feeding behaviour and food preference (Lindegaard 1997). Oligochaetes also tend to be among the dominant macroinvertebrates associated with vegetation in freshwater environments (Botts and Cowell 1993). Eleven gastropod taxa occurred on both Lagarosiphon and Vallisneria, and four of these, L. columella, P. acuta, B. depressus and M. tuberculata, made up a significant proportion of macroinvertebrate community on both macrophyte species. On Vallisneria, L. columella (12.6%) and Table 4: Taxa identified by SIMPER as making significant contributions to the dissimilarity in macroinvertebrate assemblages associated with Lagarosiphon and Vallisneria in Lake Kariba in 2005 Taxon Chironominae Naididae Caenis sp. Cloeon sp. Orthocladiinae L. columella B. depressus P. acuta Dugesia sp. M. tuberculata Orthotrichia sp. Pseudagrion sp. Ostracoda Ischnura sp. Average dissimilarity Average abundance Lagarosiphon (n = 21) Vallisneria (n = 25) 0.76 0.21 0.58 0.09 0.43 0.12 0.44 0.09 0.39 0.15 0.29 0.19 0.36 0.20 0.28 0.07 0.31 0.06 0.15 0.16 0.22 0.08 0.27 0.06 0.18 0.07 0.17 0.03 72.03 Average dissimilarity 8.53 7.51 6.06 5.43 5.33 5.01 4.81 4.02 3.83 3.43 3.29 3.10 2.55 2.52 Contribution (%) 11.85 10.43 8.41 7.54 7.39 6.95 6.68 5.58 5.32 4.77 4.57 4.30 3.54 3.50 Cumulative (%) 11.85 22.28 30.69 38.23 45.62 52.57 59.25 64.83 70.15 74.91 79.48 83.79 87.32 90.83 284 B. depressus (11.6%) were the most abundant of all the taxa. Gastropods were the most abundant order on Vallisneria and were the second most abundant order after Diptera on Lagarosipon. Freshwater snails have been shown to feed directly on living aquatic macrophytes (Sheldon 1987, Li et al. 2009), and on periphyton on the surface of plants (Brönmark 1989, 1990) as well as to use plant surfaces to deposit eggs (Lodge 1985). Thus, food was generally available for snails on both plant species, but greater food concentration and refuge from fish predation probably resulted in overall greater snail numbers on Lagarosiphon compared to Vallisneria. An increased proportion of snails on Vallisneria (44.7%) compared to Lagarosiphon (25%) suggests that the level of predation by fish on snails on Vallisneria was less than that on other macroinvertebrate taxa. Lake Kariba has only one fish species which predominantly preys on snails, the cichlid Sargochromis codringtonii. In a recent lake-wide survey, Zengeya and Marshall (2008) found that this species formed only 1.4% of the total number of fish collected from shallow bays, which suggests low predation by fish on snails. Differences in periphyton density among plants of varying architecture have been reported for several macrophyte taxa (e.g. Cattaneo and Kalff 1980). The simpler and large, ribbon-like leaf morphology of Vallisneria may reduce self-shading, thus enabling light to reach greater proportions of the plant surface, thereby facilitating increased periphyton abundance. The simpler structure may also enable easier access to and utilisation of the periphyton associated with the plant by snails. Thus, Vallisneria would have been expected to have higher periphyton abundances for snails to feed on compared to Lagarosiphon, but the much lower abundances of snails on Vallisneria than Lagarosiphon suggest low periphyton abundances on Vallisneria, implying the possible inhibition of high algal growth levels on Vallisneria leaves. A number of authors have suggested that low phytoplankton and epiphyte densities in shallow vegetated lakes may be due to allelopathic inhibition by submerged macrophytes (Blindow et al. 2002, Gross 2003, Gross et al. 2003, 2007). Thus, the possibility that Vallisneria exhibits allelopathy requires further research. Ephemeropteran nymphs contributed greater numbers (17%) to macroinvertebrate fauna on Lagarosiphon than on Vallisneria (9%). Caenis and Cloeon were the two most common and abundant mayfly taxa associated with both plants. The abundance of Caenis was not significantly different from that of Cloeon on both plants. The abundances of both Caenis and Cloeon were significantly greater on Lagarosiphon than on Vallisneria. Mayflies primarily feed on algal or detrital material from submerged surfaces (Salas and Dudgeon 2003) and are a food source for invertebrate and vertebrate predators (Brittain and Sartori 2003). Warfe and Barmuta (2006), using three differentshaped macrophyte analogues under different fish predator treatments, found that the greatest periphyton biomass as well as macroinvertebrate abundance and diversity were associated with the most structurally complex analogue. In aquatic environments, complex habitats generally provide a higher available surface for the growth of periphyton (Bowen et al. 1998), as well as greater sedimentation of particulate organic matter (Taniguchi and Tokeshi 2004). Warfe and Barmuta (2004) also showed that, in experimental systems Phiri, Chakona and Day comprising a predatory damselfly, Ischnura heterosticta tasmanica, and a fish predator, Nannoperca australis, the prey capture success of both predators was significantly reduced in the structurally complex plant analogue compared to that in structurally simpler analogues. Thus, in our study, the greater abundances of algal and detrital feeders such as Caenis and Cloeon on Lagarosiphon compared to Vallisneria may have been due to the availability of more food resources and better protection from both invertebrate and fish predators on Lagarosiphon than on Vallisneria. Five trichopteran taxa were recorded, but only two, a hydroptilid, Orthotrichia, and an ecnomid, Ecnomus, occurred in comparatively high numbers on the two macrophytes, and Orthotrichia tended to be more abundant than Ecnomus on both plants. The larvae of Orthotrichia primarily feed on algae (Wiggins 1977), while those of Ecnomus largely prey on other smaller invertebrates (Chessman 1986). Thus, the greater numbers of Orthotrichia on both Lagarosiphon and Vallisneria was probably a reflection of the greater amount of attached algal food on the plants for Orthotrichia than the invertebrate prey for Ecnomus. Periphyton biomass tends to be greater in complex, structured habitats than in simpler habitats of aquatic environments (see Bowen et al. 1998, Warfe and Barmuta 2006) and, in our study, Lagarosiphon was probably associated with a greater periphyton biomass food source for algal feeders than Vallisneria. The current study also showed that the abundance of small invertebrates such as oligochaetes and chironomids that are preyed on by Ecnomus (see Chessman 1986) were greater on Lagarosiphon than on Vallisneria. Thus, the greater abundances of Orthotrichia and Ecnomus that occurred on Lagarosiphon than on Vallisneria, suggest not only better protection from predators for the caddisfly larvae but also the availability of more food items on Lagarosiphon. The most abundant odonate nymphs associated with Lagarosiphon and Vallisneria were coenagrionids. Coenagrionid nymphs are typical inhabitants of aquatic vegetation (Bergey et al. 1992). They are generalist predators, feeding on the most common species of suitable size and their diet includes insects, oligochaetes, small crustaceans and molluscs (Hilsenhoff 1991). Consequently they may play an important role at the top levels of invertebrate food webs (Hilsenhoff 1991). According to Corbet (1999), anisopteran nymphs are generally the top insect predators in freshwater systems and usually occur in high abundance. Although the taxon richness of Anisoptera was considerably higher than that of Zygoptera on both Lagarosiphon and Vallisneria, anisopteran nymphs were much less abundant than zygopteran nymphs on both plants. Three coenagrionid genera, Pseudagrion, Enallagma and Ischnura, were the most common and abundant large insect predators on both plants. Predation by fish plays an important role in structuring invertebrate assemblages in aquatic habitats (Diehl 1992, Hornung and Lee Foote 2006) and, according to Sih (1987) and McPeek (1990), fish predation is one the main factors that structures odonate nymph communities in freshwater ecosystems. Damselfly nymphs usually hide among vegetation to escape fish predation (Dionne et al. 1990). According to Dionne and Folt (1991), the impact of fish predation on African Journal of Aquatic Science 2012, 37(3): 277–288 odonate nymphs depends on substrate complexity, with fish predation success usually being higher in structurally simpler habitats than in complex habitats (see also Gilinsky 1984). A number of studies (e.g. Chilton 1990, Lombardo 1995) have shown that, in the presence of fish predators, damselfly nymph abundances are usually greater on architecturally complex macrophytes than on simpler ones. Chilton (1990) and Lombardo (1997) also showed that macrophyte type has no effect on the predation activities and success of damselfly nymphs. They therefore suggested that the greater numbers of damselfly nymphs on structurally complex macrophytes may be due to greater abundances of a broad spectrum of prey, which results in higher predation success than on structurally simple macrophytes. In the current study, Pseudagrion, Enallagma and Ischnura were much more abundant on Lagarosiphon than on Vallisneria, probably due to better refuge from fish predators and the availability of more food resources on Lagarosiphon. There were also differences in macroinvertebrate assemblages associated with the two submerged macrophytes with respect to functional feeding groups. Collector-gatherers dominated the functional macroinvertebrate assemblages of both macrophyte species, but with a much greater proportion on Lagarosiphon. The abundance of collectorgatherers was more than 500% greater on Lagarosiphon than on Vallisneria. This can be attributed to the greater morphological complexity of Lagarosiphon compared to Vallisneria, which provides more protection from predators, as well as enhancing the accumulation of particulate matter on the plant surfaces and therefore greater concentrations of food for collector-gatherers. Grazers, largely dominated by gastropods, were more abundant on Lagarosiphon than on Vallisneria, but the relative abundances of L. columella, B. depressus and M. tuberculata compared to other taxa were much greater on Vallisneria, resulting in the Gastropoda being the dominant macroinvertebrate order on Vallisneria. Thus, unlike Lagarosiphon, on which collector-gatherers were the dominant functional feeding group, collector-gatherers and grazers were equally abundant on Vallisneria. Fisher (2005), using complex Hydrilla-like and simple Vallisneria-like artificial plants, found that plant morphology had no significant effect on macroinvertebrate abundances, except for the densities of gastropod grazers, whose abundance was much greater on the simple-structured plants. Sargochromis codringtonii, the only fish species in Lake Kariba that feeds primarily on snails, occurs in comparatively low numbers in shallow inshore waters of the lake (Zengeya and Marshall 2008). Thus, fish predation on molluscs in Lake Kariba may be low, which may account for the greater proportions of gastropods found on Vallisneria. The use of aquatic macrophytes by invertebrate grazers as a food source is debated (Sheldon 1990, Lodge 1991, Newman 1991) and it has conventionally been thought that herbivory on living macrophytes is low due to their poor nutritive value and to the presence of secondary chemicals that retard grazing (Lamberti and Moore 1984, Brönmark 1990). But it has been shown that the number of grazers is positively associated with the biomass of periphyton on submerged aquatic macrophytes (Cattaneo 1983, Kairesalo and Koskimies 1987). Hence, the much lower abundance of grazers found 285 on Vallisneria may have been due to low periphyton biomass on Vallisneria compared to Lagarosiphon. Both Lagarosiphon and Vallisneria were associated with low abundances of filter-feeder macroinvertebrates. Other studies have shown that the proportion of filterers in epiphytic macroinvertebrate communities tends to decrease with an increase in microhabitat complexity (Cyr and Downing 1988b, Rennie and Jackson 2005). According to Carpenter and Lodge (1986), low abundances of filterers associated with macrophytes are a result of the decrease in suspended algal concentrations in macrophyte beds, which promote sedimentation of algae rather than its suspension in the water column, due to shading and reduction of water velocity or current. There were differences in the functional assemblage of macroinvertebrate communities associated with the two macrophytes. The greater morphological complexity of Lagarosiphon was associated with a community skewed towards collector-gatherers, while on Vallisneria, collectorgatherers and grazers were equally important. This study also shows that the greater abundances of collectorgatherers, filterers and grazers on Lagarosiphon, all of which are used as a food source by higher trophic levels, resulted in the abundance of predatory invertebrates on Lagarosiphon being 700% greater than on Vallisneria. Diversity is positively associated with habitat complexity (Washington 1984). Habitat complexity has also been shown to affect species abundance and richness aquatic invertebrate assemblages (Beisel et al. 2000). However, the present study showed that habitat complexity may not necessarily result in greater assemblage diversity and taxon richness. Although macroinvertebrate abundances tended to be greater on Lagarosiphon than on Vallisneria, the average number of taxa and diversity were not different, while evenness was significantly greater on Vallisneria. The slight but significantly lower evenness of the macroinvertebrate community associated with Lagarosiphon compared to Vallisneria was generally due to the greater dominance of taxa such as Chironominae and Oligochaeta on Lagarosiphon. Conclusions This study showed that the same invertebrate taxa occurred on Lagarosiphon and Vallisneria, but with much lower numbers of virtually all taxa occurring on Vallisneria. These findings lend support to the theory that macrophyte morphological complexity does have an impact on epiphytic macroinvertebrate community structure (e.g. Cheruvelil et al. 2000, 2002). Although similar macroinvertebrate communities were associated with the two plant species, the greater morphological complexity of Lagarosiphon resulted in greater abundances of most taxa on it, because of the availability of better refuge from predation and high quantities of trapped particulate organic matter that are used as food by many invertebrates. Thus the study supports to some extent the ‘habitat heterogeneity hypothesis’, which postulates that highly complex habitats provide more niches, greater feeding opportunities and increased refugia from predation, and are therefore associated with greater abundances and diversity of organism than simple habitats (Tews et al. 2004). 286 Lagarosiphon is the most widespread and dominant submerged macrophyte in Lake Kariba (Machena and Kautsky 1988) and the greater epiphytic macroinvertebrate abundances on Lagarosiphon than on Vallisneria possibly make it a more valuable habitat and invertebrate food source for fish species. Nevertheless, more research is required to validate this assumption. Therefore changes, especially those favouring the dominance of Vallisneria, may have a negative effect on fish species diversity and abundance in Lake Kariba. A more comprehensive understanding of the ecology of epiphytic macroinvertebrates in Lake Kariba, and of their effects on ecosystem dynamics, requires further research. There is a need for studies on the effects of physicochemical aspects such as temperature and lake level fluctuations on invertebrate assemblages. Research is also needed on the relationship between primary production, especially epiphytic algal production, and invertebrate production, as well as on the effects of biotic interactions such as predation and competition on invertebrate community structure. 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