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Effects of Sea Urchin Grazing on Seagrass (Thalassodendron Ciliatum) Beds of a Kenyan Lagoon

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Effects of Sea Urchin Grazing on Seagrass (Thalassodendron Ciliatum) Beds of a Kenyan Lagoon MARINE ECOLOGY PROGRESS SERIES Vol. 226: 255–263, 2002 Published January 31 Mar Ecol Prog Ser Effects of sea urchin grazing on seagrass (Thalassodendron ciliatum) beds of a Kenyan lagoon Teresa Alcoverro*, Simone Mariani Centre d’Estudis Avançats de Blanes (CSIC), Carretera Sta. Bàrbara s/n, 17300 Blanes, Spain ABSTRACT: We present the results of experimental and descriptive field studies on the effects of dense sea urchin aggregations on seagrass beds in the Mombasa lagoon (Kenya). The study area was dominated by the slow-growing seagrass Thalassodendron ciliatum (49.6% cover), and supported an average sea urchin density of 1.6 m–2, mostly Tripneustes gratilla (90%). In the T. ciliatum meadows, 39% of the cover was heavily grazed by the sea urchins (more than 75% dead shoots), 23.4% was moderately grazed (more than 50% dead shoots) and 38.5% was slightly grazed (19.8% dead shoots). We observed 5 aggregations (fronts) of T. gratilla in the study area (5000 m2), 4 of these within the T. ciliatum meadows. These aggregations were linear in structure, with mean densities of 10.4 m–2, and left in their wake a ‘trailing edge’ area of defoliated seagrass rhizomes (85% dead shoots). Graz- ing rates were measured in 2 ways: marked permanent quadrats along the fronts, and sea urchin addition experiments. The first method produced grazing rates of 1.8 ± 0.43 shoots m–2 d–1, and the second produced slightly higher values of 5 ± 0.86 shoots m–2 d–1. New shoot recruitment was esti- mated from the marked permanent quadrats in the fronts as 0.32 shoots m–2 d–1. Simple models indi- cated that the return interval (i.e. the average frequency of the passage of sea urchin fronts through a seagrass patch) for the ‘sea urchin grazing fronts’ was 99 or 34 mo, depending on the method used, and that T. ciliatum recovery time was 44 mo. We conclude that the sea urchin aggregations observed in the Mombasa lagoon control T. ciliatum density by grazing its exposed apical tips. KEY WORDS: Seagrass · Sea urchins · Herbivory · Grazing · Thalassodendron ciliatum · Tripneustes gratilla Resale or republication not permitted without written consent of the publisher INTRODUCTION In general, large-scale seagrass overgrazing by sea urchins in temperate seagrass communities does not The effects of sea urchin grazing on benthic macro- appear to occur with either the frequency or magni- phyte communities have been widely studied. Heavy tude reported for kelp forests and algae-dominated grazing by sea urchins is important in determining the communities. Nevertheless, in the tropical western structure and abundance of both macrophyte and sea- Atlantic, studies have reported sea urchin overgrazing grass assemblages in many marine littoral ecosystems. of large meadows of Thalassia testudinum (Camp et al. Massive urchin aggregations of the genus Strongylo- 1973) and Syringodium filiforme (Maciá & Lirman centrotus have been widely reported to overgraze 1999, Rose et al. 1999). Whether these patterns of over- giant kelp forests (e.g. Bernstein et al. 1981, Hart & grazing represent a general trend along tropical Scheibling 1988, Tegner et al. 1995, Scheibling et al. ecosystems outside of the western Atlantic is 1999). Heavy grazing by the sea urchin Paracentrotus unknown, as most of the tropical seagrass systems lividus can mediate the transition of assemblages from remain still unexplored (see review by Duarte 1999). erect algae to coralline barrens in the Mediterranean Kenyan reefs are ideal sites to study the impact of Sea (Sala et al. 1998). herbivores on seagrass communities. Seagrass species richness is very high (Wakibya 1995) and the lagoons *E-mail: [email protected] have a diverse array of sea urchins and fishes as poten- © Inter-Research 2002 · www.int-res.com 256 Mar Ecol Prog Ser 226: 255–263, 2002 tial seagrass herbivores (McClanahan et al. 1994, Ma- 10 m2 quadrats (n = 10) randomly placed over an area riani & Alcoverro 1999). In October 1997, while moni- of ~0.5 km2. To obtain the size-distribution of the sea toring seagrass meadows in the Mombasa Marine urchins (Tripneustes gratilla), we measured the hori- National Park (MNP) lagoon we repeatedly observed zontal diameter of 90 tests (to the nearest mm) in Octo- the presence of several grazing aggregations of the sea ber and February. urchin Tripneustes gratilla (localised densities of 137 Sea urchin aggregations in Mombasa lagoon. The sea urchins per 10 m2) within seagrass beds dominated sea urchin (Tripneustes gratilla) aggregations were by the species Thalassodendron ciliatum. The aggre- quantified in 50 × 10 m belt transects (n = 10) over an gations were in highly defoliated seagrass patches and area of ~0.5 km2. Additionally, for each sea urchin seemed to be moving through vegetated areas of the aggregation observed, we recorded the size of the meadows as small fronts. front in metres (front length and width). In the light of these observations, we decided to Percentage of dead shoots in Thalassodendron monitor the grazing aggregations in the Mombasa ciliatum meadows. Many dead shoots of T. ciliatum lagoon more closely. We carried out a series of descrip- (i.e. grazed shoots lacking leaves and apical meris- tive studies and experiments to: (1) characterise and tems: Fig. 1) were observed in the Mombasa lagoon. quantify the principal sea urchin and seagrass species These dead shoots were very irregularly distributed within the Mombasa MNP lagoon, (2) estimate num- within the meadows, and we found patches with 0 to bers of sea urchin aggregations in the beds, (3) quan- 100% dead shoots. The presence of dead shoots was tify the percentage of dead Thalassodendron ciliatum evaluated using a 4-rank visual scale (I: 0 to 25% areas, (4) describe the sea urchin aggregations and dead shoots; II: 25 to 50%; III: 50 to 75%; IV: 75 to evaluate their effects on the T. ciliatum beds, (5) quan- 100%). Estimates of each rank were based on six 50 tify experimentally the feeding rates of the sea urchin m linear transects within T. ciliatum beds. Along the Tripneustes gratilla within the grazing aggregations transect axis, the position of each transition of rank and the capacity of T. ciliatum to re-grow after being (as I to IV) or sand was recorded as the distance (to grazed, and finally (6) link small-scale grazing experi- the nearest cm) to the transect origin. Percentage ments with large-scale meadow dynamics through the cover of each rank (I to IV) or sand corresponded return interval for grazing disturbance and the recov- to their proportion on the line transects. To correct ery time of the plant. the possible bias of our visual rank estimates, along some of the transects, 3 replicate 50 × 50 cm MATERIALS AND METHODS Study site. The study was carried out in the Mombasa MNP lagoon between October 1997 and February 1998. The lagoon is characterised by shallow depths (0.3 to 2 m) during low tides, is protected from waves and currents, and the seagrass beds are dominated by Thalassodendron ciliatum (Ochieng & Erftemeijer 1999). Characterisation of Mombasa lagoon. To charac- terise the seagrass beds in the lagoon we measured seagrass (all species) abundance (as %cover), coral and sand abundance (%cover) and sea urchin (all spe- cies) density (ind. m–2). Estimates of seagrass, coral and sand %cover were based on 50 m line-transects (n = 10) randomly placed over a ~0.5 km2 area within the sea- grass beds. Along the transect axis, the position of each transition of sand, coral or seagrass species was recorded as the distance (to the nearest cm) to the transect origin. Gaps of <10 cm were not considered (see Manzanera & Romero 2000 for details). Percent- age cover of each substrate class (seagrass, coral, and sand) corresponded to their proportion on the line transects. Fig. 1. Thalassodendron ciliatum plant. Dead shoots (lacking Sea urchin abundance in the seagrass beds was leaves and apical meristems), living shoots and new branch- recorded twice (in October 1997 and February 1998) in ing rhizomes (new-shoot recruits) are shown Alcoverro & Mariani: Sea urchin grazing on seagrass beds 257 quadrats were placed in areas visually assigned to Table 1. Summary of total area of Thalassodendron ciliatum each of the 4 visual classes. Living and dead shoots plots and number of sea urchins (Tripneustes gratilla) added were counted in each quadrat. Average values from to each plot during the sea urchin addition (SA) experiment. C: control treatment this standardisation were used to correct the visual estimates and to obtain the proper proportion of dead shoots. Treatment Area No. of sea Sea urchin (m2)urchins density Characterisation of sea urchin aggregations within Thalassodendron ciliatum meadows. Three randomly SA 1.5 15 10.0 chosen sea urchin aggregations, approximately 500 m SA 2.2 22 10.0 apart, were selected, and the impacts of the grazing SA 1.8 17 9.4 C 2.5 0 0.0 front were estimated by comparing the T. ciliatum C 1.5 0 0.0 dead shoots in front of and behind the urchins. Three C 1.3 0 0.0 belt-transects (10 m long × 5 m wide) on an imaginary axis perpendicular to the front were chosen: a ‘trailing edge’ grazed area, a ‘middle’ area, and ‘leading edge’ mately the same size (Table 1) lying apart from the area (see Rose et al. 1999), which corresponded to sea- main seagrass beds. These patches were initially sea grass patches with high densities of dead shoots (dis- urchin free, possibly because the surrounding sand tance from middle area = –10 m), a high density of sea acted as a natural barrier to their immigration. We urchins (distance from middle = 0 m) and a moderate added sea urchins (Tripneustes gratilla) at a density density of sea urchins advancing across living seagrass of 10 m–2 (the average density of the middle area of shoots (distance from middle = +10 m), respectively.
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