Advertisement

Marine Biology

, Volume 158, Issue 7, pp 1483–1495 | Cite as

Scale-dependent patterns of variability of a grazing parrotfish (Leptoscarus vaigiensis) in a tropical seagrass-dominated seascape

  • Martin Gullström
  • Charlotte Berkström
  • Marcus C. Öhman
  • Maria Bodin
  • Mattis Dahlberg
Original Paper

Abstract

Although herbivorous fish form critical linkages between primary producers and higher trophic levels, the major factors regulating their spatial structure in seagrass systems remain poorly understood. The present study examined the parrotfish Leptoscarus vaigiensis in seagrass meadows of a tropical embayment in the western Indian Ocean. Stomach content analysis and direct field observations showed that L. vaigiensis is an efficient grazer, feeding almost exclusively on seagrass leaves. Seagrass shoot density was highly correlated to all density variables (total, juvenile and subadult) and juvenile biomass of L. vaigiensis, while subadult biomass was predicted by distance to neighbouring coral habitat. Moreover, density and biomass of predatory fish (piscivores) were predicted by seagrass canopy height and the distribution patterns of predators followed those of L. vaigiensis. Hence, factors at local (seagrass structural complexity and feeding mode) and landscape scale levels (seascape context and distribution of piscivores) likely mutually structure herbivorous fish communities. The findings underscore the importance of incorporating multiple scale-dependent factors when managing coastal seagrass ecosystems and their associated key species.

Keywords

Canopy Height Potential Predator Seagrass Meadow Herbivorous Fish Shoot Density 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

We wish to thank Mcha Manzi for assistance throughout all field periods, and Mohammed Nur Mohammed, Saleh Yahya, Lisa Adelsköld, Maria Asplund, Maricela de la Torre Castro and Johan Eklöf for assistance during part of the field work. We are also grateful to Kristina Halling, Nils Kautsky, Jerker Lokrantz, and Per Nilsson for useful comments on earlier versions of the manuscript. Furthermore, thanks to Mats Lindegarth for statistical advice as well as Mats Björk for helping with identification of epiphytes. The Institute of Marine Sciences (University of Dar es Salaam) at Zanzibar provided research facilities and we appreciate the support given by Narriman Jiddawi. The study was supported by the Swedish International Development cooperation Agency (Sida) through the Sida/SAREC Bilateral Marine Science Programme between Sweden and Tanzania as well as the Sida/SAREC-funded project ‘Changes in tropical seagrass beds induced by eutrophication’.

References

  1. Alcoverro T, Mariani S (2004) Patterns of fish and sea urchin grazing on tropical Indo-Pacific seagrass beds. Ecography 27:361–365CrossRefGoogle Scholar
  2. Almeida AJ, Marques A, Saldanha L (1999) Some aspects of the biology of three fish species from the seagrass beds at Inhaca Island, Mozambique. Cybium 23:369–376Google Scholar
  3. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance in ecology. Aust Ecol 26:32–46Google Scholar
  4. Anderson MJ (2005) PERMANOVA: a FORTRAN computer program for permutational multivariate analysis of variance. Department of Statistics, University of Auckland, New ZealandGoogle Scholar
  5. Bardgett RD, Wardle DA (2003) Herbivore-mediated linkages between aboveground and belowground communities. Ecology 84:2258–2268CrossRefGoogle Scholar
  6. Bartholomew A, Diaz RJ, Cicchetti G (2000) New dimensionless indices of structural habitat complexity: predicted and actual effects on a predator’s foraging success. Mar Ecol Prog Ser 206:45–58CrossRefGoogle Scholar
  7. Beck MW, Heck KL, Able KW, Childers DL, Eggleston DB, Gillanders BM, Halpern B, Hays CG, Hoshino K, Minello TJ, Orth RJ, Sheridan PF, Weinstein MR (2001) The identification, conservation, and management of estuarine and marine nurseries for fish and invertebrates. Bioscience 51:633–641CrossRefGoogle Scholar
  8. Bell JD, Pollard DA (1989) Ecology of fish assemblages and fisheries associated with seagrasses. In: Shepherd SA (ed) Biology of seagrasses–a treatise on the biology of seagrasses with special reference to the Australian region. Elsevier, Amsterdam, pp 565–609Google Scholar
  9. Bell JD, Westoby M (1986a) Abundance of macrofauna in dense seagrass is due to habitat preference, not predation. Oecologia 68:205–209CrossRefGoogle Scholar
  10. Bell JD, Westoby M (1986b) Importance of local changes in leaf height and density to fish and decapods associated with seagrasses. J Exp Mar Biol Ecol 104:249–274CrossRefGoogle Scholar
  11. Björndal KA (1980) Nutrition and grazing behaviour of the green turtle Chelonia mydas. Mar Biol 56:147–154CrossRefGoogle Scholar
  12. Blaber SJM, Brewer DT, Salini JP, Kerr JD, Conacher C (1992) Species composition and biomass of fishes in tropical seagrasses at Groote Eylandt, Northern Australia. Estuar Coast Shelf Sci 35:605–620CrossRefGoogle Scholar
  13. Bohnsack JA, Harper DE, McClellan DB, Hulsbeck M (1994) Effects of reef size on colonization and assemblage structure of fishes at artificial reefs off southeastern Florida, USA. Bull Mar Sci 55:796–823Google Scholar
  14. Bologna PAX, Heck KL (1999) Differential predation and growth rates of bay scallops within a seagrass habitat. J Exp Mar Biol Ecol 239:299–314CrossRefGoogle Scholar
  15. Burkepile DE, Hay ME (2008) Herbivore species richness and feeding complementarity affect community structure and function on a coral reef. Proc Natl Acad Sci USA 105:16201–16206CrossRefGoogle Scholar
  16. Cederlöf U, Rydberg L, Mgendi M, Mwaipopo O (1995) Tidal exchange in a warm tropical lagoon: Chwaka Bay, Zanzibar. Ambio 24:458–464Google Scholar
  17. Connolly RM (1994a) Removal of seagrass canopy: effects on small fish and their prey. J Exp Mar Biol Ecol 184:99–110CrossRefGoogle Scholar
  18. Connolly RM (1994b) The role of seagrass as preferred habitat for juvenile Sillaginodes punctata (Cuv. & Val.) (Sillaginidae, Pisces): habitat selection or feeding? J Exp Mar Biol Ecol 180:39–47CrossRefGoogle Scholar
  19. Connolly RM, Hindell JS (2006) Review of nekton patterns and ecological processes in seagrass landscapes. Estuar Coast Shelf Sci 68:433–444CrossRefGoogle Scholar
  20. Crawley MJ (1997) Plant–herbivore dynamics. In: Crawley MJ (ed) Plant ecology. Blackwell Science, Oxford, pp 401–474Google Scholar
  21. Dahlgren A (2006) Consumption of seagrass by herbivore parrotfish in major fishing grounds of Chwaka Bay, Zanzibar. Master’s Thesis, University of Gothenburg, SwedenGoogle Scholar
  22. Davies TE, Beanjara N, Tregenza T (2009) A socio-economic perspective on gear-based management in an artisanal fishery in south-west Madagascar. Fish Manage Ecol 16:279–289CrossRefGoogle Scholar
  23. Dorenbosch M, Verberk WCEP, Nagelkerken I, van der Velde G (2007) Influence of habitat configuration on connectivity between fish assemblages of Caribbean seagrass beds, mangroves and coral reefs. Mar Ecol Prog Ser 334:103–116CrossRefGoogle Scholar
  24. Duarte CM (1990) Seagrass nutrient content. Mar Ecol Prog Ser 67:201–207CrossRefGoogle Scholar
  25. Duarte CM, Kirkman H (2001) Methods for the measurement of seagrass abundance and depth distribution. In: Coles RG (ed) Global seagrass research methods. Elsevier, Amsterdam, pp 141–153CrossRefGoogle Scholar
  26. Duffy JE (2006) Biodiversity and the functioning of seagrass ecosystems. Mar Ecol Prog Ser 311:233–250CrossRefGoogle Scholar
  27. Edgar GJ, Shaw C (1995) The production and trophic ecology of shallow-water fish assemblages in southern Australia 1. Species richness, size-structure and production of fishes in Western Port, Victoria. J Exp Mar Biol Ecol 194:53–81CrossRefGoogle Scholar
  28. Eklöf JS, Gullström M, e Castro M, Muthiga N, Uku J, Muthiga N, Lyimo T, Bandeira SO (2008) Sea urchin overgrazing of seagrasses: a review of causes, consequences and management. Estuar Coast Shelf Sci 79:569–580CrossRefGoogle Scholar
  29. Froese R, Pauly D (eds) (2009) FishBase. http://www.fishbase.org
  30. Gell FR, Whittington MW (2002) Diversity of fishes in seagrass beds in the Quirimba Archipelago, northern Mozambique. Mar Freshw Res 53:115–121CrossRefGoogle Scholar
  31. Goecker ME, Heck KL, Valentine JF (2005) Effects of nitrogen concentrations in turtlegrass Thalassia testudinum on consumption by the bucktooth parrotfish Sparisoma radians. Mar Ecol Prog Ser 286:239–248CrossRefGoogle Scholar
  32. Gotceitas V (1990) Plant stem density as a cue in patch choice by foraging juvenile bluegill sunfish. Environ Biol Fish 29:227–232CrossRefGoogle Scholar
  33. Grober-Dunsmore R, Frazer TK, Lindberg WJ, Beets J (2007) Reef fish and habitat relationships in a Caribbean seascape: the importance of reef context. Coral Reefs 26:201–216CrossRefGoogle Scholar
  34. Gullström M, de la Torre-Castro M, Bandeira SO, Björk M, Dahlberg M, Kautsky N, Rönnbäck P, Öhman MC (2002) Seagrass ecosystems in the Western Indian Ocean. Ambio 31:588–596CrossRefGoogle Scholar
  35. Gullström M, Lundén B, Bodin M, Kangwe J, Öhman MC, Mtolera SP, Björk M (2006) Assessment of changes in the seagrass-dominated submerged vegetation of tropical Chwaka Bay (Zanzibar) using satellite remote sensing. Estuar Coast Shelf Sci 67:399–408CrossRefGoogle Scholar
  36. Gullström M, Bodin M, Nilsson PG, Öhman MC (2008) Structural complexity and landscape configuration as determinants of tropical fish assemblage composition. Mar Ecol Prog Ser 363:241–255CrossRefGoogle Scholar
  37. Heck KL Jr, Orth RJ (1980) Seagrass habitats: the roles of habitat complexity, competition and predation in structuring associated fish and motile macroinvertebrate assemblages. In: Kennedy VS (ed) Estuarine perspectives. Academic Press, New York, pp 449–464CrossRefGoogle Scholar
  38. Heck KL Jr, Orth RJ (2006) Predation in seagrass beds. In: Larkum AWD, Orth RJ, Duarte CM (eds) Seagrasses: biology, ecology and conservation. Springer, Netherlands, pp 537–550CrossRefGoogle Scholar
  39. Heck KL Jr, Hays G, Orth RJ (2003) Critical evaluation of the nursery role hypothesis for seagrass meadows. Mar Ecol Prog Ser 253:123–136CrossRefGoogle Scholar
  40. Hughes TP, Rodrigues MJ, Bellwood DR, Ceccarelli D, Hoegh-Guldberg O, McCook L, Moltschaniwskyj N, Pratchett MS, Steneck RS, Willis B (2007) Phase shifts, herbivory, and the resilience of coral reefs to climate change. Curr Biol 17:360–365CrossRefGoogle Scholar
  41. Huntly N (1991) Herbivores and the dynamics of communities and ecosystems. Annu Rev Ecol Syst 22:477–503CrossRefGoogle Scholar
  42. Hyndes GA, Kendrick AJ, MacArthur LD, Stewart E (2003) Differences in the species- and size-composition of fish assemblages in three distinct seagrass habitats with differing plant and meadow structure. Mar Biol 142:1195–1206CrossRefGoogle Scholar
  43. Jackson EL, Rowden AA, Attrill MJ, Bossey SJ, Jones MB (2001) The importance of seagrass beds as a habitat for fishery species. Oceanogr Mar Biol Annu Rev 39:269–303Google Scholar
  44. Jormalainen V, Honkanen T, Heikkilä N (2001) Feeding preference and performance of a marine isopod on seaweed hosts: cost of habitat specialization. Mar Ecol Prog Ser 220:219–230CrossRefGoogle Scholar
  45. Kirsch KD, Valentine JF, Heck KL Jr (2002) Parrotfish grazing on turtlegrass Thalassia testudinum: evidence for the importance of seagrass consumption in food web dynamics of the Florida Keys National Marine Sanctuary. Mar Ecol Prog Ser 227:71–85CrossRefGoogle Scholar
  46. Larkum AWD, Orth RJ, Duarte CM (eds) (2006) Seagrasses: biology, ecology and conservation. Springer, NetherlandsGoogle Scholar
  47. Lawrence J (1975) On the relationship between marine plants and sea urchins. Oceanogr Mar Biol Annu Rev 13:213–286Google Scholar
  48. Levin SA (1992) The problem of pattern and scale in ecology. Ecology 73:1943–1967CrossRefGoogle Scholar
  49. Lobel PS, Ogden JC (1981) Foraging by the herbivorous parrotfish Sparisoma radians. Mar Biol 64:173–183CrossRefGoogle Scholar
  50. Lugendo BR, Pronker A, Cornelissen I, de Groene A, Nagelkerken I, Dorenbosch M, van der Velde G, Mgaya YD (2005) Habitat utilisation by juveniles of commercially important fish species in a marine embayment of Zanzibar, Tanzania. Aquat Living Resour 18:149–158CrossRefGoogle Scholar
  51. Lugendo BR, Nagelkerken I, van der Velde G, Mgaya YD (2006) The importance of mangroves, mud and sand flats, and seagrass beds as feeding areas for juvenile fishes in Chwaka Bay, Zanzibar: gut content and stable isotope analyses. J Fish Biol 69:1639–1661CrossRefGoogle Scholar
  52. McClanahan TR, Nugues M, Mwachireya S (1994) Fish and sea urchin herbivory and competition in Kenyan coral reef lagoons: the role of reef management. J Exp Mar Biol Ecol 184:237–254CrossRefGoogle Scholar
  53. Middleton MJ, Bell JD, Burchmore DA, Pollard DA, Pease BC (1984) Structural differences in the fish communities of Zostera capricorni and Posidonia australis seagrass meadows in Botany Bay, New South Wales. Aquat Bot 18:89–109CrossRefGoogle Scholar
  54. Moksnes P-O, Gullström M, Tryman K, Baden S (2008) Trophic cascades in a temperate seagrass community. Oikos 117:763–777CrossRefGoogle Scholar
  55. Mumby PJ, Dahlgren CP, Harborne AR, Kappel CV, Micheli F, Brumbaugh DR, Holmes KE, Mendes JM, Broad K, Sanchirico JN, Buch K, Box S, Stoffle RW, Gill AB (2006) Fishing, trophic cascades, and the process of grazing on coral reefs. Science 311:98–101CrossRefGoogle Scholar
  56. Nagelkerken I (2009) Evaluation of nursery function of mangroves and seagrass beds for tropical decapods and reef fishes: patterns and underlying mechanisms. In: Nagelkerken I (ed) Ecological connectivity among tropical coastal ecosystems. Springer, London, pp 357–399CrossRefGoogle Scholar
  57. Nagelkerken I, van der Velde G (2002) Do non-estuarine mangroves harbour higher densities of juvenile fish than adjacent shallow-water and coral reef habitats in Curacao (Netherlands Antilles)? Mar Ecol Prog Ser 245:191–204CrossRefGoogle Scholar
  58. Nagelkerken I, Kleijnen S, Klop T, van den Brand RACJ, Cocheret de la Morinière E, van der Velde G (2001) Dependence of Caribbean reef fishes on mangroves and seagrass beds as nursery habitats: a comparison of fish faunas between bays with and without mangroves/seagrass beds. Mar Ecol Prog Ser 214:225–235CrossRefGoogle Scholar
  59. Nagelkerken I, Roberts CM, van der Velde G, Dorenbosch M, van Riel MC, Cocheret de la Morinière E, Nienhuis PH (2002) How important are mangroves and seagrass beds for coral-reef fish? The nursery hypothesis tested on an island scale. Mar Ecol Prog Ser 244:299–305CrossRefGoogle Scholar
  60. Nakamura Y, Sano M (2004) Comparison between community structures of fishes in Enhalus acoroides- and Thalassia hemprichii-dominated seagrass beds on fringing coral reefs in the Ryukyu Islands, Japan. Ichthyol Res 51:38–45CrossRefGoogle Scholar
  61. Nakamura Y, Horinouchi M, Nakai T, Sano M (2003) Food habits of fishes in a seagrass bed on a fringing coral reef at Iriomote Island, southern Japan. Ichthyol Res 50:15–22CrossRefGoogle Scholar
  62. Ogden JC (1988) The influence of adjacent systems on the structure and function of coral reefs. Proc 6th Int Coral Reef Symp, Australia, 1:123–129Google Scholar
  63. Ohta I, Tachihara K (2004) Larval development and food habits of the marbled parrotfish, Leptoscarus vaigiensis, associated with drifting algae. Ichthyol Res 51:63–69CrossRefGoogle Scholar
  64. Orth RJ, Heck KL Jr, Van Montfrans J (1984) Faunal communities in seagrass beds: a review of the influence of plant structure and prey characteristics on predator-prey relationships. Estuaries 7:339–350CrossRefGoogle Scholar
  65. Pittman SJ, McAlpine CA, Pittman KM (2004) Linking fish and prawns to their environment: a hierarchical landscape approach. Mar Ecol Prog Ser 283:233–254CrossRefGoogle Scholar
  66. Pittman SJ, Caldow C, Hile SD, Monaco ME (2007) Using seascape types to explain the spatial patterns of fish in the mangroves of SW Puerto Rico. Mar Ecol Prog Ser 348:273–284CrossRefGoogle Scholar
  67. Pollard DA (1984) A review of ecological studies on seagrass-fish communities, with particular reference to recent studies in Australia. Aquat Bot 18:3–42CrossRefGoogle Scholar
  68. Pronker A (2002) Utilization of seagrass, mangrove and other bay habitats by commercially important fish species in Chwaka Bay, Zanzibar, Tanzania. Master’s Thesis, University of Nijmegen, NetherlandsGoogle Scholar
  69. Randall JE, Allen GR, Steene RC (1997) The complete divers′ and fishermen′s guide to fishes of the great barrier reef and coral sea. Crawford House Publishing Pty Ltd, BathurstGoogle Scholar
  70. Robertson DR, Reinboth R, Bruce RW (1982) Gonochorism, protogynous sex-change and spawning in three sparisonmatinine parrotfishes from the western Indian Ocean. Bull Mar Sci 32:868–879Google Scholar
  71. Salita JT, Ekau W, Saint-Paul U (2003) Field evidence on the influence of seagrass landscapes on fish abundance in Bolinao, northern Philippines. Mar Ecol Prog Ser 247:183–195CrossRefGoogle Scholar
  72. Smith MM, Heemstra PC (1991) Smith′s sea fishes. Southern Book Publishers, JohannesburgGoogle Scholar
  73. Tobisson E, Andersson J, Ngazi Z, Rydberg L, Cederlöf U (1998) Tides, monsoons and seabed: local knowledge and practice in Chwaka Bay, Zanzibar. Ambio 27:677–685Google Scholar
  74. Tomas F, Turon X, Romero J (2005) Effects of herbivores on a Posidonia oceanic seagrass meadow: importance of epiphytes. Mar Ecol Prog Ser 287:115–125CrossRefGoogle Scholar
  75. Unsworth RKF, Wylie E, Smith DJ, Bell JJ (2007a) Diel trophic structuring of seagrass bed fish assemblages in the Wakatobi Marine National Park, Indonesia. Estuar Coast Shelf Sci 72:81–88CrossRefGoogle Scholar
  76. Unsworth RKF, Taylor JD, Powell A, Bell JJ, Smith DJ (2007b) The contribution of scarid herbivory to seagrass ecosystem dynamics in the Indo-Pacific. Estuar Coast Shelf Sci 74:53–62CrossRefGoogle Scholar
  77. Valentine JF, Duffy JE (2006) The central role of grazing in seagrass ecology. In: Larkum AWD, Orth RJ, Duarte CM (eds) Seagrasses: biology, ecology and conservation. Springer, Netherlands, pp 463–501Google Scholar
  78. Valentine JF, Heck KL Jr (1999) Seagrass herbivory: evidence for the continued grazing of marine grasses. Mar Ecol Prog Ser 176:291–302CrossRefGoogle Scholar
  79. Warfe DM, Barmuta LA (2004) Habitat structural complexity mediates the foraging success of multiple predator species. Behav Ecol 141:171–178Google Scholar
  80. Werner EE, Hall DJ (1988) Ontogenetic habitat shifts in bluegill: the foraging rate-predation risk trade-off. Ecology 69:1352–1366CrossRefGoogle Scholar
  81. Werner EE, Gilliam JF, Hall DJ, Mittelbach GG (1983) An experimental test of the effects of predation risk on habitat use in fish. Ecology 64:1540–1548CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Martin Gullström
    • 1
    • 2
    • 3
  • Charlotte Berkström
    • 1
  • Marcus C. Öhman
    • 2
  • Maria Bodin
    • 4
  • Mattis Dahlberg
    • 2
  1. 1.Department of Systems EcologyStockholm UniversityStockholmSweden
  2. 2.Department of ZoologyStockholm UniversityStockholmSweden
  3. 3.Department of Marine Ecology - KristinebergUniversity of GothenburgFiskebäckskilSweden
  4. 4.Department of Marine Ecology - TjärnöUniversity of GothenburgStrömstadSweden

Personalised recommendations