Trophic ecology of the seagrass-inhabiting footballer demoiselle Chrysiptera annulata (Peters, 1855); comparison with three other reef-associated damselfishes
stable isotopes; siber; isotopic niche; pomacentridae; coraf reef; trophic ecology; Toliara; Western Indian ocean; reef fish
Abstract :
[en] Many damselfishes (Pomacentridae) are herbivorous or omnivorous with an important contribution of different kinds of algae in their diet. They display different levels of territoriality and farming behavior, from almost non territorial to monoculture farmers. In addition, few species inhabit seagrass meadows but, presently, none can be considered as seagrass-eating specialists. The footballer demoiselle, Chrysiptera annulata, is found in the seagrass meadows on the reef flat of the Great Reef of Toliara (Madagascar, Mozambique Channel). Regarding this unusual habitat for pomacentrid, this study aimed to answer 3 questions: 1) What is the diet of C. annulata? 2) Do the resources supporting this diet include seagrass? 3) Does its trophic niche overlap those of other sympatric damselfishes (Pomacentrus trilineatus, Chrysiptera unimaculata and Plectroglyphidodon lacrymatus) living in close association with macrophytes or eating algae? Stomach content examination and stable isotope analysis showed that the footballer demoiselle is not a seagrass consumer but is an omnivorous/herbivorous species heavily relying on algal resources and small invertebrates. SIAR, a stable isotope mixing model, indicated it assimilated large amount of turf algae and various benthic or planktonic invertebrates in lower proportions. SIBER metrics pointed out that isotopic niche of the footballer demoiselle partly overlaps the one of its congeneric C. unimaculata, but not those of P. trilineatus and P. lacrymatus. Trophic strategies of C. annulata differed both from farming species such as P. lacrymatus or from less territorial herbivores such as P. trilineatus. Its seagrass meadow habitat on the Great Reef of Toliara allow the conquest of an unusual habitat for damselfishes and could limit competition with C. unimaculata, a species displaying the same territorial behavior and the same isotopic niche but living on the reef itself.
Research Center/Unit :
MARE - Centre Interfacultaire de Recherches en Océanologie - ULiège AFFISH-RC - Applied and Fundamental FISH Research Center - ULiège FOCUS - Freshwater and OCeanic science Unit of reSearch - ULiège
Lepoint, Gilles ; Université de Liège > Département de Biologie, Ecologie et Evolution > Océanographie biologique
Michel, Loïc ; Université de Liège > Département de Biologie, Ecologie et Evolution > Océanographie biologique
Parmentier, Eric ; Université de Liège > Département de Biologie, Ecologie et Evolution > Morphologie fonctionnelle et évolutive
Frederich, Bruno ; Université de Liège > Département de Biologie, Ecologie et Evolution > Morphologie fonctionnelle et évolutive
Language :
English
Title :
Trophic ecology of the seagrass-inhabiting footballer demoiselle Chrysiptera annulata (Peters, 1855); comparison with three other reef-associated damselfishes
Publication date :
2016
Journal title :
Belgian Journal of Zoology
ISSN :
0777-6276
eISSN :
2295-0451
Publisher :
Royal Belgian Zoological Society, Bruxelles, Belgium
Allen GR & Randall JE (1980). A review of the damselfishes (Teleostei: Pomacentridae) of the Red Sea. Israel Journal of Zoology 29(1-3): 1-98
Andréfouët S, Guillaume MMM, Delval A, Rasoamanendrika FMA, Blanchot J & Bruggemann JH (2013). Fifty years of changes in reef flat habitats of the Grand Récif of Toliara (SW Madagascar) and the impact of gleaning. Coral Reefs 32(3): 757-768
Bellwood DR, Goatley CHR, Brandl SJ & Bellwood O (2014). Fifty million yearsof herbivory on coral reefs: Fossils, fish and functional innovations. Proceedings of the Royal Society B: Biological Sciences 281(1781).
Caut S, Angulo E, Courchamp F & Figuerola J (2010). Trophic experiments to estimate isotope discrimination factors. Journal of Applied Ecology 47(4): 948-954
Cebrian J (2002). Variability and control of carbon consumption, export, and accumulation in marine communities. Limnology and Oceanography 47(1): 11-22
Ceccarelli DM, Jones GP & McCook LJ (2005). Effects of territorial damselfish on an algaldominated coastal coral reef. Coral Reefs 24(4): 606-620
Ceccarelli DM, Jones GP & McCook LJ (2011). Interactions between herbivorous fish guilds and their influence on algal succession on a coastal coral reef. Journal of Experimental Marine Biology and Ecology 399(1): 60-67
Choat JH, Robbins WD & Clements KD (2004). The trophic status of herbivorous fishes on coral reefs: II Food processing modes and trophodynamics. Marine Biology 145(3): 445-454
Coplen, T., B, (2011). Guidelines and recommended terms for expression of stable-isotope-ratio and gas-ratio measurements results. Rapid Communications in Mass Spectrometry 25: 2538-2560
Dromard CR, Bouchon-Navaro Y, Cordonnier S, Fontaine MF, Verlaque M, Harmelin- Vivien M & Bouchon C (2013). Resource use of two damselfishes, Stegastes planifrons and Stegastes adustus, on Guadeloupean reefs (Lesser Antilles): Inference from stomach content and stable isotope analysis. Journal of Experimental Marine Biology and Ecology 440: 116-125
Dromard CR, Bouchon-Navaro Y, Harmelin- Vivien M & Bouchon C (2015). Diversity of trophic niches among herbivorous fishes on a Caribbean reef (Guadeloupe, Lesser Antilles), evidenced by stable isotope and stomach content analyses. Journal of Sea Research 95: 124-131
Fishelson L (1998). Behaviour, socio-ecology and sexuality in damselfishes (Pomacentridae). Italian Journal of Zoology 65(SUPPL): 387-398
Flaherty EA & Ben-David M (2010). Overlap and partitioning of the ecological and isotopic niches. Oikos 119(9): 1409-1416
Fox RJ & Bellwood DR (2013). Niche partitioning of feeding microhabitats produces a unique function for herbivorous rabbitfishes (Perciformes, Siganidae) on coral reefs. Coral Reefs 32(1): 13-23
Frédérich B, Fabri G, Lepoint G, Vandewalle P & Parmentier E (2009). Trophic niches of thirteen damselfishes (Pomacentridae) at the Grand Récif of Toliara, Madagascar. Ichthyological Research 56(1): 10-17
Frédérich B, Lehanse O, Vandewalle P & Lepoint G (2010). Trophic Niche Width, Shift, and Specialization of Dascyllus aruanus in Toliara Lagoon, Madagascar. Copeia (2): 218-226
Frédérich B, Sorenson L, Santini F, Slater GJ & Alfaro ME (2013). Iterative ecological radiation and convergence during the evolutionary history of damselfishes (Pomacentridae). American Naturalist 181(1): 94-113
Garpe KC & Öhman MC (2003). Coral and fish distribution patterns in Mafia Island Marine Park, Tanzania: Fish-habitat interactions. Hydrobiologia 498: 191-211
Gillibrand CJ, Harris AR & Mara E (2007). Inventory and spatial assemblage study of reef fish in the area of Andavadoaka, South-West Madagascar (Western Indian Ocean). Western Indian Ocean Journal of Marine Science 6(2): 183-197
Gullström M, Berkström C, Öhman MC, Bodin M & Dahlberg M (2011). Scale-dependent patterns of variability of a grazing parrotfish (Leptoscarus vaigiensis) in a tropical seagrassdominated seascape. Marine Biology 158(7): 1483-1495.
Harmelin-Vivien M (1979). Ichtyofaune des récifs coralliens de Tuléar (Madagascar): écologie et relations trophiques PhD, University of Aix- Marseille II.
Harris A, Manahira G, Sheppard A, Gough C & Sheppard C (2010). Demise of Madagascar’s once great barrier reef-change in coral reef condition over 40 years Atoll Research Bulletin (574): 1-16
Hata H & Kato M (2002). Weeding by the herbivorous damselfish Stegastes nigricans in nearly monocultural algae farms. Marine Ecology Progress Series 237: 227-231
Hata H & Kato M (2004) Monoculture and mixedspecies algal farms on a coral reef are maintained through intensive and extensive management by damselfishes. Journal of Experimental Marine Biology and Ecology 313:285-296
Hata H & Umezawa Y (2011). Food habits of the farmer damselfish Stegastes nigricans inferred by stomach content, stable isotope, and fatty acid composition analyses. Ecological Research 26(4): 809-818
Havelange S, Lepoint G, Dauby P & Bouquegneau JM (1997). Feeding of the sparid fish Sarpa salpa in a seagrass ecosystem: Diet and carbon flux. Marine Ecology-Pubblicazioni Della Stazione Zoologica Di Napoli I 18(4): 289-297
Heck KL & Valentine JF (2006). Plant-herbivore interactions in seagrass meadows. Journal of Experimental Marine Biology and Ecology 330(1): 420-436
Hyslop, E. J. 1980. Stomach contents analysis—a review of methods and their application. Journal of Fish Biology 17:411–429
Jackson AL, Inger R, Parnell AC & Bearhop S (2011). Comparing isotopic niche widths among and within communities: SIBER - Stable Isotope Bayesian Ellipses in R. Journal of Animal Ecology 80(3): 595-602
Jones GP, Santana L, McCook LJ & McCormick MI (2006). Resource use and impact of three herbivorous damselfishes on coral reef communities. Marine Ecology Progress Series 328: 215-224
Khalaf MA (2004). Fish fauna of the Jordanian Coast, Gulf of Aqaba, Red Sea. Journal of King Abdulaziz University: Marine Sciences 15(1): 23-50
Klumpp DW, Salita-Espinosa JT & Fortes MD (1993). Feeding ecology and trophic role of sea urchins in a tropical seagrass community. Aquatic Botany 45(2-3): 205-229
Kramer MJ, Bellwood O & Bellwood DR (2013). The trophic importance of algal turfs for coral reef fishes: The crustacean link. Coral Reefs 32(2): 575-583
Layman CA, Araujo MS, Boucek R, Hammerschlag-Peyer CM, Harrison E, Jud ZR, Matich P, Rosenblatt AE, Vaudo JJ, Yeager LA, Post DM & Bearhop S (2012). Applying stable isotopes to examine foodweb structure: An overview of analytical tools. Biological Reviews 87(3): 545-562
Layman CA, Arrington DA, Montaña CG & Post DM (2007). Can stable isotope ratios provide for commu nity-wide measures of trophic structure? Ecology 88(1): 42-48
Mill AC, Pinnegar J K & Polunin NVC (2007). Explaining isotope trophic-step fractionation: Why herbivorous fish are different. Functional Ecology 21(6): 1137-1145
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. Ichthyological Research 50(1): 15-22
Newsome SD, del Rio CM, Bearhop S & Phillips DL (2007). A niche for isotopic ecology. Frontiers in Ecology and the Environment 5(8): 429-436
Parnell AC, Inger R, Bearhop S & Jackson AL (2010). Source Partitioning Using Stable Isotopes: Coping with Too Much Variation. Plos One 5(3).
Pichon M (1978). Recherches sur les peuplements à dominance d’anthozoaires dans les récifs coralliens de Tulear. Atoll Research Bulletin 222: 490.
Plass-Johnson JG, McQuaid CD & Hill JM (2013). Stable isotope analysis indicates a lack of inter- and intra-specific dietary redundancy among ecologically important coral reef fishes. Coral Reefs 32(2): 429-440
Raubenheimer D, Zemke-White WL, Phillips R J & Clements KD (2005). Algal macronutrients and food selection by the omnivorous marine fish Girella tricuspidata. Ecology 86(10): 2601-2610
Vonk JA, Christianen MJA & Stapel J (2008). Redefining the trophic importance of seagrasses for fauna in tropical Indo-Pacific meadows. Estuarine Coastal and Shelf Science 79(4): 653-660
Wickel J, Jamon A, Pinault M, Durville P & Chabanet P (2014). Composition et structure des peuplements ichtyologiques marins de l’île de Mayotte (sud-oueast de l’océan indien). Cybium 38(3): 179-203
Wilson S & Bellwood DR (1997). Cryptic dietary components of territorial damselfishes (Pomacentridae, Labroidei). Marine Ecology Progress Series 153(1-3): 299-310
Wilson SK, Bellwood DR, Choat JH & Furnas MJ (2003). Detritus in the epilithic algal matrix and its use by coral reef fishes. Oceanography and Marine Biology: an annual review 41: 279-309
