Diversity and distribution of seagrasses around Inhaca Island, southern Mozambique
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1 South African Journal of Botany 2002, 68: Printed in South Africa All rights reserved Copyright NISC Pty Ltd SOUTH AFRICAN JOURNAL OF BOTANY ISSN Diversity and distribution of seagrasses around Inhaca Island, southern Mozambique SO Bandeira Department of Marine Botany, Göteborg University, PO Box 461, SE Göteborg, Sweden Present address: Department of Biological Sciences, Universidade Eduardo Mondlane, PO Box 257, Maputo, Mozambique Received 21 September 2000, accepted in revised form 15 August 2001 Nine seagrass species were identified around Inhaca as well as a more narrow form of Thalassodendron ciliatum (Forsk.) den Hartog occurring in rocky pools at the north east coast. Seagrasses were mapped and grouped in seven distinct community types (in order of areas covered): Thalassia hemprichii/halodule wrightii, Zostera capensis, Thalassodendron ciliatum/cymodocea serrulata, Thalassodendron ciliatum/seaweeds, Cymodocea rotundata/halodule wrightii, Cymodocea serrulata and Halophila ovalis /Halodule wrightii; with the ninth species Syringodium isoetifolium occurring in three of these communities. A dichotomous identification key is presented. Seagrasses covered half of the whole intertidal area around Inhaca Island and diversity was also high at community level. Transects at macro and micro scales showed zonation of species which may be due to tidal gradients or topographic variation. Cluster analysis indicated ecological dissimilarities between co-dominant species. A decline of Zostera capensis has recently been seen outside the local village. Baseline studies like this are important for coastal zone management in developing countries, where large future changes in seagrass cover can be expected. Introduction Although diversity and occurrence of seagrasses are generally known on a global scale (Den Hartog 1970, Phillips and Menez 1988, Kuo and McComb 1989), very few studies have been published from the east African region and Mozambique. In coastal areas of developing countries, one can expect large future changes as tourism, modern fishing techniques, aquaculture, shipping and industrialisation increase. Thus, baseline studies such as the present one are needed to document the original pristine and natural distribution of dominant species and communities before anthropogenic impact and changes in water quality have grown too large. Results of such studies should then be taken into consideration for coastal zone management and the protection of biodiversity. In Mozambique, the first publications of seagrasses were by Moss (1937) and Cohen (1939); they were followed later by a number of studies performed by scientists based in South Africa (Kalk 1959, Macnae and Kalk 1962, Macnae 1969, Munday and Forbes 1979) dealing mostly with seagrasses of Inhaca Island but including also other areas of the country. Later, marine botanical work covering southern Mozambique and a taxonomical compilation on seagrasses in the western Indian Ocean was published (Bandeira 1995, 1997). Martins (1997) produced a first account on Zostera capensis of Inhaca Island and the Maputo area covering both distribution and other ecological performances. Recently, De Boer (2000) emphasised the importance of seagrasses as a nutrient source in the southern bay at Inhaca. Distribution and factors influencing their zonation patterns in other areas of the western Indian Ocean were mostly carried out in Kenya and Tanzania (Isaac 1968, Uku et al. 1996, Björk et al. 1997, 1999). Despite all this, and the importance those communities have as nursery and foraging areas for the fauna, including many commercial fishes (Larkum et al. 1989), there is still little research focussed on the distribution of seagrass communities and their zonation in the region. This paper updates and revises earlier research, emphasising the distribution and zonation of the seagrass communities around Inhaca Island. Methods Inhaca island is situated north east of Maputo Bay between latitudes S and S and longitudes and E. The intertidal zones around this island have two contrasting features. The east side is exposed to the open sea, to the dominant south east wind (Kalk 1995), and to an abrupt depth increase at the beach line. The west side, facing Maputo bay, is relatively protected having a gentle topographic slope reaching in some areas a distance of 1km
2 192 Bandeira between the coast and the low spring tide level. The tidal amplitude vary between 0.1m and 3.9m. Inshore water temperature around Inhaca island varies within the extremes of C, and the salinity within 30 39ppt (mean 35ppt) while being constant at 35ppt at the northern end of Inhaca Island (Bandeira unpublished data). Specimens of seagrasses were collected and identified using literature (Macnae and Kalk 1969, Den Hartog 1970, Larkum et al. 1989, Simpson 1989). Identification was checked with herbarium material at Eduardo Mondlane University Herbarium (LMU). A dichotomous identification key was made based on characters from both fresh and dried material as well as from literature (Isaac 1968, Macnae and Kalk 1969, Den Hartog 1970, Phillips and Menez 1988, Larkum et al. 1989). To map the seagrass communities around Inhaca two main steps were followed. Firstly, the species composition was determined semi-quantitatively by applying a nominal scale of frequency of species occurrence: highly frequent, frequent and present. The communities were then characterised by the number of highly frequent species. Secondly, ground truthing (walking and snorkelling during spring low tide) all over the island with a map 1: was made in order to delineate the contours of the seagrass communities; a reference point on the island, for precision of mapping, was used (Kirkman 1996). Black and white aerial photographs were also used to visualise inner and outer contours of the seagrass beds. The community types were named after the most dominant species. For this, visual estimates of percentage cover based on density classes (Tomasko et al. 1993) were also used. The area of each community type was calculated by weighing paper with the traced area. Some of the seagrass communities show macro-scale and micro-scale variation in species composition, which may be derived from the tidal gradient and small scale topographic variation. Therefore, macrotransects and microtransects were performed to study the zonation patterns. Six macrotransects, 1m wide, running from the coastline to the low water spring tide level were marked and a sample collected in a 1m 2 quadrat at each 10m of the transect. These macrotransects were outlined in three community types (with higher species diversity): Thalassia hemprichii/halodule wrightii, Thalassodendron ciliatum/ Cymodocea serrulata and Zostera capensis. Two microtransects showing species diversity on a small-scale depth gradient were analysed during low tide in the T. hemprichii/h. wrightii community type located at the south bay of the island. At 1m long microtransects, presence/absence of species were recorded at each cm. The reason for choosing only the T. hemprichii/h. wrightii community for closer analysis was that this community shows a high species diversity at a small scale. Also, most of its topography has small depressions and elevations intermingled with smooth surfaces. Data on macrotransects were subjected to cluster analyses using the computer programme STATISTICA 5.5, to ascertain possible ecological affinities between seagrass species (Shepherd and Womersley 1981). Results Species diversity and taxonomical key Nine seagrass species distributed in three families were identified for Inhaca: Cymodocea rotundata Ehrenb. et Hempr. ex Aschers., C. serrulata (R. Br.) Aschers. et Magnus, Halodule uninervis (Forsk.) Aschers. in Bossier, H. wrightii Aschers., Syringodium isoetifolium (Aschers.) Dandy, Thalassodendron ciliatum (Forsk.) den Hartog (Cymodoceaceae), Halophila ovalis (R.Br.) Hook. f., Thalassia hemprichii (Ehrenb.) Aschers. in Petermann (Hydrocharitaceae) and Zostera capensis Setchell (Zosteraceae). An identification key for these species is given (Appendix 1). T. ciliatum occurs in two forms: in sandy substrate with broad/wide leaves and in rock pools with narrow, shorter leaves. Different size-forms of leaf width were observed in Halophila ovalis varying from mm in width. Size forms and leaf tip variants were also observed in Halodule wrightii. Such morphological variations also occur in Brazilian H. wrightii. (Creed 1997). Mapping Seven seagrass community types were identified around Inhaca (listed in order of areas covers): Thalassia hemprichii/halodule wrightii, Zostera capensis, Thalassodendron ciliatum/cymodocea serrulata, Thalassodendron ciliatum/seaweeds, Cymodocea rotundata/halodule wrightii, Cymodocea serrulata and Halophila ovalis /Halodule wrightii (Table 1). The boundaries of each community type were drawn and the seagrass map was then established (Figure 1). Overall, seagrasses covered around 50% of the entire intertidal area around Inhaca. The three largest community types: T. hemprichii/h. wrightii, Z. capensis and T. ciliatum/c. serrulata covers 88% of the seagrass beds around the island (Table 2). T. hemprichii/h. wrightii is the most species-rich community type, where all nine seagrass Table 1: Species composition in each seagrass community type Community type Species Th Tc Cs Cr Hw Hu Si Zc Ho Th/Hw *** * * ** *** ** * ** ** Tc/Cs * *** *** * ** ** ** ** Cs *** * * * Cr/Hw *** *** * Ho/Hw *** * *** Zc * * *** Tc/seaweeds *** Cr Cymodocea rotundata Cs Cymodocea serrulata Hu Halodule uninervis Hw Halodule wrightii Si Syringodium isoetifolium Tc Thalassodendron ciliatum Th Thalassia hemprichii Zc Zostera capensis Ho Halophila ovalis *** highly frequent ** frequent * present
3 South African Journal of Botany 2002, 68: Figure 1: Map of Inhaca Island showing the seagrass communities
4 194 Bandeira Table 2: Area occupied per each community type Community Type Area(km 2 ) Percentage of total Thalassia hemprichii/halodule wrightii Zostera capensis Thalassodendron ciliatum/ Cymodocea serrulata Thalassodendron ciliatum/seaweeds Cymbocea rotundata/halodule wrightii Cymodocea serrulata Halophila ovalis/halodule wrightii species listed for Inhaca are represented, closely followed by the T. ciliatum/c. serrulata community with eight species (Table 1). Z. capensis (the second largest community type, located at the south bay and at Portinho) dominates in areas with high content of organic matter and, apparently, with high quantity of ooze and mud compared with the other community types (cf. Martins 1997). This community is mostly located in an area surrounded by mangroves both at Inhaca Island and the mainland peninsula in the south. Recently, a decline of Z. capensis was observed at the Harbour area (Portinho, Figure 1, personal observation). This decline might be due to increasing density of boats, shallow water fishing, and in addition, increasing trampling of the area at low tide. The T. ciliatum/c. serrulata community occurs in an extensive area with gentle topographic slope. The real area cover of this community type is higher than what was calculated since a rather extensive area of T. ciliatum is constantly subtidal, and could not be mapped, thus increasing the total cover of seagrass beds around the island. At the northernmost point of the island (Ponta Mazónduè), a community of T. ciliatum and seaweeds has established in rocky pools and creeks. This is an area of high hydrodynamics with huge surf waves and strong currents. Here, T. ciliatum and seaweeds are strongly attached to the substrate, and grow directly on rocks. The most common seaweed species observed here were: Anadyomene wrightii Harvey ex J.E. Gray, Colpomenia sinuosa (Martens ex Roth) Derbès et Solier, Chamaedoris delphinii (Hariot) Feldmann et Boergesen, Dictyota spp. Digenea simplex (Wulf.) C. Ag., Gracilaria spp., Halimeda cuneata Hering in Krauss, Hormophysa cuneiformis (J.F. Gmelin) P.C. Silva, Hypnea rosea Papenfuss, Neomeris vanbosseae M. Howe, Pseudocodium de-vriesii Weber van Bosse, Padina boryana Thivy, Sargassum spp., Valoniopsis pachynema (G. Martens) Boergesen and Valonia macrophysa Kützing. An extensive list of seaweeds occurring at Inhaca island mostly at Ponta Mazónduè is provided by Critchley et al. (1997). Zonation The species Thalassia hemprichii (Figure 2a) and Thalassodendron ciliatum (Figure 3a) tends to occupy deeper areas far from the coastline whereas, Halodule wrightii (Figure 2a) and Cymodocea serrulata (Figure 3a) tends to occupy shallow areas closer to the coastline. T. ciliatum, in the subtidal fringe, occurs in homogenic stands except in some areas where it is also accompanied by a band of Syringodium isoetifolium parallel to the coastline. The rela- (a) Th Tc Cs Cr Hw Zc Ho (b) Th Tc Ho Cs Cr Zc Hw DISTANCE (m) Figure 2: (a) Macrotransect of the Thalassia hemprichii/halodule wrightii community type from northern bay (0m corresponds to the level of low water spring tide); (b) cluster analysis of the same transect. For species symbols see Table 1
5 South African Journal of Botany 2002, 68: (a) Th Tc Cs Hw Hu Si Zc DISTANCE (m) (b) Th Si Hw Hu Zc Cs Tc Figure 3: Macrotransect of the Thalassodendron ciliatum/cymodocea serrulata and Zostera capensis community types at Portinho area (0m corresponds to the level of low water spring tide); (b) cluster analysis of the same transect. For species symbols see Table 1 tionship between T. hemprichii and H. wrightii in the T. hemprichii/h. wrightii community type is repeated at small scale variation in the microtransect where most T. hemprichii occups depression areas and most H. wrightii was found in elevated areas (Figure 4) all observed at spring low tide, when this seagrass meadow was only covered by residual water. This microtransect also showed that Halodule uninervis has a tendency to occur in submerged areas, while Cymodocea rotundata occurs in both immersed and emersed areas (Figure 4). Those two species have broader leaves, especially if compared to H. wrightii and Zostera capensis. Cluster analysis revealed a high dissimilarity index between the co-dominant species in each community type, as the two co-dominants seem to explore different zonation patterns (Figures 2b, 3b). Discussion Nine seagrass species occur around Inhaca, making up 75% of the total number of seagrass species occurring in Mozambique and 16% of the 58 world seagrass species (Den Hartog 1970, Kuo and McComb 1989). This diversity is high for such a small area as Inhaca Island. Furthermore, all nine species could be found within only a small area of Thalassia hemprichii/halodule wrightii community type. One of the highest species diversity observed in the world was reported by Walker et al. (1988) for Shark Bay, Western Australia, with 12 species in an area 84 times bigger than that of Inhaca island. Twelve seagrass species occur along the whole eastern African coast and 26 along western Australian waters (Isaac 1968, Kuo and McComb 1989, Bandeira 1997). Extensive areas with seagrasses were also observed in northern Mozambique and Tanzania (Bandeira and António 1996 and personal observation). The taxonomic key presented is based on distinctive and practical features to differentiate the species. The key can be used for either fresh or dried specimens. Halophila ovalis showed large leaf variability, with broad, narrow and intermediate leaf forms; the shape of the leaf blade being obovate-ovate, oblong-elliptic up to linear. Very narrow forms were described as H. ovalis (R. Br.) Hook. f. ssp. linearis (Den Hartog) Den Hartog (Den Hartog 1970, Kuo and McComb 1989). Plasticity of H. ovalis has also been observed elsewhere (McMillan 1983) and some variability seems related to different salinities (Benjamin et al. 1999). The seagrass community types observed in this study are similar to those observed along other parts of the Mozambican coast such as the north beach of Maputo city, where Zostera capensis is the dominant species and coexists with Halodule wrightii (Martins 1997); at Bazaruto Island (21 34 S, E) where Thalassodendron ciliatum was observed as dominant to the west coast; at Inhassoro (21 32 S, E) where Thalassia hemprichii, coodominant with H. wrightii and T. ciliatum, occurs in subtidal areas (personal observation). At Mecúfi (northern Mozambique (13 17 S, E), a coral limestone area), the seagrasses often occur together with seaweeds (Bandeira and António 1996). Coppejans et al. (1992) reported the existence of beds dominated by T. hemprichii, T. ciliatum and Enhalus acoroides L. (Royle) in Kenya. Hemminga et al. (1995) found that T. ciliatum was the dominant species in subtidal areas in Kenya. Stands of E. acoroides were observed by the author at Quissanga Bay and Quirimbas Archipelago (northern Mozambique, around S, E); Z. capen-
6 196 Bandeira Figure 4: Changes in species composition with depth along a one metre microtransect of the Thalassia hemprichii/halodule wrightii community type sis which forms rather pure stands in the Maputo Bay area and at Inhaca, was only observed in a mangrove area of Mecúfi (Bandeira and António 1996). In the Indo-Pacific region the seagrasses T. hemprichii, T. ciliatum and E. acoroides dominate in many areas (Brouns 1985a, b, Brouns and Heijs 1986, Miller and Sluka 1999). Cluster analysis tended to reflect ecological affinities (Shepherd and Womersley 1981, Bandeira and António 1996). Different zonation patterns between T. hemprichii and H. wrightii and between T. ciliatum and C. serrulata have also been observed elsewhere (Coppejans et al. 1992). Thalassodendron ciliatum in rocky pools, at Ponta Mazónduè, have adapted to strong waves and water-swept habitat similar to other rocky areas in southern Mozambique and eastern South African coast (Barnabas 1982, 1991, Bandeira 1995). A closer inspection of this community showed that T. ciliatum accumulates shell debris and sometimes large grained sand amongst roots and rhizomes. This may help anchorage of the plants. It also seems that in rainy seasons (October March), when winds are stronger, some rocky pools accumulate some sand. T. ciliatum in rocky habitat seems to have adapted similarly to Phyllospadix spp., a genus occurring only on rocks on water-swept Pacific shores (Den Hartog 1970, Turner 1985, Cooper and McRoy 1988, Ramírez-García et al. 1998). North of Inhaca island, east of the small Portuguese island and between these two islands at the silted channel, new sand is often brought in (Hatton and Couto 1992) and these new areas are colonised by Cymodocea serrulata which acts as a pioneer species. C. serrulata is reported to be highly tolerant to siltation (Bach et al. 1998). Halophila ovalis ssp. linearis and Halodule wrightii have also been found as pioneers at the bare areas close to the coastline, at the west coast of Inhaca. These findings agree with those reported by Coppejans et al. (1992) who stated that H. ovalis and H. wrightii are pioneer species in Gazi Bay, Kenya. These species have been observed as pioneers also elsewhere (Gallegos et al. 1994, Bach et al. 1998). Recently, in 2000, it was observed that part of the sand bank, in the northern bay of the island, never became submerged giving rise to Sangala Island some 1 500m in length and 40m in width (Figure 2, personal observation). Flowering of seagrasses at Inhaca has been seen frequently only in Thalassodendron ciliatum (but not in the rock pools), Thalassia hemprichii and Halophila ovalis. At Mecúfi, frequent flowering of Syringodium isoetifolium has also been observed. In Kenya, apart from the above species, flowering was seen once or a few times, or only flower fragments were collected, in Cymodocea serrulata, Enhalus acoroides, Halodule uninervis, Halophila minor and Halophila stipulacea (Isaac 1968, McMillan 1980). C. serrulata, H. stipulacea, S. isoetifolium and Zostera capensis from Kenya did, however, flower under experimental environmental manipulations in Texas (USA) in controlled conditions of temperature, salinity, day/night period, nutrients with synthetic seawater (McMillan 1980). The technique for mapping seagrasses could be improved for more accuracy and possibly for better comparison with other studies carried out elsewhere. Remote sensing techniques such as photo-interpretation using digitised colour aerial photographs or videos could be used (Long et al. 1994, Chauvaud et al. 1998, Ramage and Schiel 1999). Landsat images could also be used (Kirkman 1996, Ward et al. 1997). The information collected can be loaded in a Geographical Information System (GIS) (Kirkman 1996). Such data gathered in GIS, including maps, could be useful for the study of losses and increase of seagrass beds (Lee Long et al. 1996, Garrabou 1998). A combination of different methods, involving both simple and high-tech methods, combining e.g. digitised aerial photographs, GIS and ground-truthing, would be ideal to get a better picture of seagrass mapping, diversity, zonation, as well as for understanding possible dynamics in plant distribution (Kirkman 1990, 1996, Chauvaud et al. 1998). The ecological demands of the seagrass species making up the different communities at Inhaca could not be analysed. Tidal gradient associated with species tolerance to desiccation might be among the main factors inducing zonation. Björk et al. (1999) did not find any apparent relation between zonation and desiccation in tropical seagrasses from Zanzibar, as the shallow intertidal species were, in general, more sensitive to desiccation than the deeper species. The species growing highest in the intertidal zone, e.g. Halophila ovalis and Halodule wrightii, did not seem to desiccate much in situ during low tide because their leaves lie flat on the moist sand (Björk et al. 1999). Björk et al. (1997) showed that intertidal species growing mostly at shallow depths, e.g. H. wrightii, had a higher affinity for the form of carbon (HCO 3 ) commonly available in desiccating environments contrarily to species occurring more in subtidal regions/waters, e.g. T. ciliatum, which showed low affinity to this inorganic carbon species. At saturating irradiances the seagrass Cymodocea serrulata, which grew in the intertidal areas of Inhaca island, showed almost twice as high net photosynthetic rate as that of T. ciliatum (Johnson et al. 1993). Nutrient competition between species as well as growth pattern may also affect the species composition and successions in seagrass beds as was shown to occur between H. wrightii and Thalassia testudinum in Florida, USA (Fourqurean et al. 1992). Acknowledgements I thank Prof Inger Wallentinus (Department of Marine Botany, Göteborg University, Sweden) and Dr John Hatton (Department of Biological Sciences, Universidade Eduardo
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In: Polhill RC, Simpson D (eds) Flora of Tropical East Africa. Royal Botanic Gardens, Kew, UK, pp ISBN Tomasko DA, Dawes CJ, Fortes MD, Largo DB, Alava MNR (1993) Observations on a multi-species seagrass meadow offshore of Negros Oriental, Republic of the Philippines. Botanica Marina 36: Turner T (1985) Stability of rocky intertidal surfgrass beds: persistence, pre-emption and recovery. Ecology 66: Uku JN, Martens EE, Mavuti KM (1996) An ecological assessment of littoral seagrass communities in Diani and Galu coastal beaches, Kenya. In: Björk, Semesi AK, Pedersén M, Bergman B (eds) Current Trends in Marine Botanical Research in the East African Region. SIDA, Uppsala, pp ISBN Walker DI, Kendrich GA, Mccomb AJ (1988) The distribution of seagrass species in Shark Bay, Western Australia, with notes on their ecology. Aquatic Botany 30: Ward DH, Markon CJ, Douglas DC (1997) Distribution and stability of eelgrass beds at Izembek Lagoon, Alaska. Aquatic Botany 58: Appendix 1: Identification key for the nine seagrass species occurring at Inhaca Island 1a. Leaves petiolate Halophila ovalis 1b. Leaves never petiolate, always with a leaf blade and leaf sheath 2 2a. Leaf blade cylindric or circular in transverse section Syringodium isoetifolium 2b. Leaf blade flattened, strap-shaped or rectangular in transverse section, not cylindrical or circular as above 3 3a. Leaves narrow, in general less than two mm wide; leaf apex concave, convex or obtuse 4 3b. Leaves broad, in general more than two mm (mostly more than four mm) wide; leaf apex round, often serrulate 6 4a. Leaf apex obtuse or rounded; parallel and translucent transverse veins present, parallel veins more than five; shoot and rhizome yellowish Zostera capensis 4b. Leaf apex not obtuse, always concave-bidentate or convex-tridentate; transverse veins absent, parallel veins three; shoot and rhizome not yellowish 5 5a. Leaf blade usually less than 1 mm wide; apex concave or bidentate Halodule wrightii 5b. Leaf blade usually more than 1 mm wide; apex convex or tridentate Halodule uninervis 6a. Roots and shoots arising at each rhizome node 7 6b. Roots and shoots usually arising at each fourth or more rhizome nodes 8 7a. Older leaf sheaths attached on stem, leaving a shaggy mass surrounding the lower shoot; leaf pale-green, with apex entire or minutely serrulate; one root per each rhizome node Cymodocea rotundata 7b. Older leaf sheaths becoming detached leaving a naked lower stem; leaf not pale-green, apex serrulate; two roots per each rhizome node Cymodocea serrulata 8a. Roots and shoots usually arising in more than each fourth rhizome node; older leaf sheaths persistent, leaving a shaggy mass surrounding the shoot; apex not serrulate; stem, rhizome and roots herbaceous Thalassia hemprichii 8b. Roots and shoots arising in each fourth rhizome node; older leaves becoming detached leaving a naked stem; apex strongly serrulate; stem, rhizome and roots semi-ligneous or ligneous (occurring in sandy and rocky habitats, the latter with narrow leaves, thinner stem and condensed rhizome) Thalassodendron ciliatum Edited by RN Pienaar
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