Ferraro & Cole 1992, Engle et al. 1994). ...... Ferraro SP, Cole FA (1992) Taxonomic level sufficient for ... Editorial responsibility: John Gray (Contributing Editor),.
MARINE ECOLOGY PROGRESS SERIES Mar Ecol Prog Ser
l
Published March 17
Effects of anthropogenic disturbances of tropical soft-bottom benthic communities Patrick Frouin* Laboratoire d'ecologie marine, UniversitB de la Reunion. BP 7151,97715 Saint Denis Messag Cedex 9. France
ABSTRACT: The benthic ecosystem of the lagoon surrounding Tahiti, the most populated island of French Polynesia, was investigated to assess the impacts of terrestrial runoff on these benthlc cornmunities. Five lagoonal zones based on population densities around the coast of T a h t i were identified, and within each zone a transect from the fringing reef to the barrier reef was sampled, a total of 18 stations. Only large macrofauna collected on a 2 mm sieve were considered in this study. Multivariate analysis uslng total biomass and environmental factors showed that the stations formed 3 main groups which were related to sediment characteristics, including percentage of silt, organic matter and phaeop~gment levels. The distribution of the major feeding groups was related to the amounts of terrestrial inputs and distance from the shore. The stations on the barrier reef and those in zones adjacent to low population areas were not impacted by these terrestrial inputs. Deposit-feeding communities of capitellid polychaetes were dominant in the channel parts of the lagoon, which acted as decanting ponds. Chaetopterid polychaetes played a n important role in recycling sediments of terrigenous origin in the fringing ecosystem. The patterns of diversity, density and biomass of the benthos around the lagoon revealed that some areas were impacted by moderate terrigenous inputs. It appears that the intermediate disturbance hypothesis explains the functioning of the parts of the benthic lagoonal ecosystem which are subjected to human impact. The organic enrichment by terrestrial inputs contrasts with food limitation that appears to occur in the non-dsturbed areas. Despite high organic loads, the benthic communities present a t the harbour station were not depauperate, as bioturbation by burrowing alpheids and callianassids prevented anoxic conditions from developing.
KEY WORDS: Lagoon . Macrobenthic communities . Polychaetes . Deposit-feeders . Terrestrial inputs . Tropical
INTRODUCTION
The effects of anthropogenic inputs on coastal marine ecosystems can be quantified by studying benthic communities subjected to varying levels of input (Pearson & Rosenberg 1978). Soft-bottom macrobenthic communities have also been used to investigate levels of disturbance and human-mediated perturbations (Pearson & Rosenberg 1978,Keough & Quinn 1991, Ferraro & Cole 1992, Engle et al. 1994). Such studies are generally undertaken as part of environmental impact studies before major development is undertaken. Polychaetes, a dominant component of such communities, especially capitellids, have often been
O Inter-Research 2000 Resale of full article not permitted
used to assess the effects of organic enrichment (e.g. Hily 1985, Plantecuny et al. 1993, Forbes et al. 1994, Heip 1995, Ellis & Schneider 1997). In the Pacific, numerous studies have been undertaken in atoll lagoons of the Tuamotu Archipelago as well as in Moorea, French Polynesia (see Hutchings et al. 1994).Even though most of French Polynesia's population lives on Tahiti, especially in or around Papeete, which is also the location of most of the industry within the territory, its lagoonal environment is poorly known (Frouin 1996). With increasing development in the coastal zone of the island, where the majority of the population lives, impacts are certainly occurring on lagoonal communities, but the existing data were inadequate to quantify them prior to t h s study. It is known that in the tropics, increased rates of sedimentation and eutrophication related to terrestrially derived or-
40
Mar Ecol Prog Ser 194: 39-53, 2000
Zone l INDUSTRIAL ZONE
Zone 2 HARBOUR ZONE
Zone 5 REFERENCE ZONE
P
AP*~TAHITI
Fig. 1. Location of the 18 statlons in the lagoon of Tahiti. The scale on the side of each zone shows approximate depth (m).The first digit of the station number relates to the zone, the second digit to reef morphology: 1 is for fringing reef (FR), 2 for fringing reef-channel transition (TR), 3 for channel (CH) and 4 for inner flat of the barrier reef (BR). Example: 53 is channel station in Zone 5. Characteristics of zones and stations are shown in Table 1 and described in 'Material and methods'
ganic enrichment are the most significant sources of anthropogenic impacts on coral reefs (Hatcher et al. 1989, Grigg & Dollar 1990). The objective of this study was to investigate the soft-bottom macrobenthic communities of Tahiti lagoon and to assess the response of these communities to anthropogenic disturbances. It was assumed that these anthropogenic inputs were from the coastal zone and related to the densities of human populations around the island and associated industrial and tourist activities. As polychaetes dominated these benthic communities (Frouin & Hutchings in press), both in terms of number of species and individuals, they were primarily used to investigate the effects of increased rates of sedimentation and organic enrichment from terrestrial inputs on these communities.
MATERIAL AND METHODS
Study area. Tahiti ( I F S , 149"W) is the main high basaltic island in French Polynesia, south-eastern Pacific Ocean, with a population of about 200 000 inhabitants, most of whom live in and around Papeete, the capital. The majority of the wastewater is returned
to the lagoon via rivers and creeks without any treatment (Hutchings et al. 1994). Stream flow is related to rainfall, which is about 2 m annually on the coast and more than 10 m in the mountains, with the highest rainfall occurring during the wet season (December to March). About 30 floods occur annually, 2/3 of these occurring during the wet season (Lafforgue 1984). Five zones (industrial, harbour, hotels, residential and reference) identified by the type of adjacent coastal development and population densities ran from the shore to the barrier reef. Four stations were sampled in each zone, fringing reef (FR), fringing reefchannel transition (TR),channel (CH) and in the inner flat of the barrier reef (BR). However, in Zone 2 (Papeete harbour) only 1 station of the CH type could be defined (Stn 20) and in Zone 1, 2 stations were sampled in the TR (Stns 12 and 15) because of the complex reef morphology, so that a total of 18 stations were sampled (Fig. 1, Table 1). The location and physical characteristics of each station are given in Table 2 , together with a synopsis of the adjacent coastal development to each zone. Sampling procedure. Macrofauna of soft-bottom sediment5 were sampled with large PVC corers (30 cm height, 11.5 cm wide) using SCUBA and sorted on a
Frouin: Anthropogenic disturbances of tropical benthic communities
Table 1. General features of the stations (FR, fringing reef; TR, fringing reef-channel transltlon; CH, channel; BR, inner flat of the barrier reef). Values in parentheses for organic lodd are standard error (n = 8; except Stn 15 with n = 6 and Stn 43 with n = 7) Zone
1
Zone type (population)
Stn
Station type
Depth Mean sediment Organic (m) grain size (mm) load (%)
Industrial Zone 11 (20-40 inhab. ha-') 15 12 13 14
FR TR TR CH BR
6 6 18 2.5
0.464 0.074 0.043 0.048 0.682
4.76 (0.37) 13.40 (0.70) 5.23 (0.18) 13.31 (0.32) 4.09 (0.11)
2
Harbour Zone 20 (80-220 inhab. ha-')
CH
13
0.032
12.65 (0.26)
3
Hotel Zone 31 (40-80 inhab. ha-') 32 33 34
FR TR CH BR
200 mV; Fenchel 1969) down to depths of 20 cm, the length of the cores. It is suggested that this is because of bioturbation of sediments and irrigation of burrows by Callianassa spp, and Alpheus spp. Burrow densities of these decapods were up to 436 + 21 burrow openings per square metre (Stn 20; n = 12), and these species are known to have complex burrows, which may be 1 to 2 m in depth (Vaugelas de 1985, Nickell & Atkinson 1995). Such complex burrows and the high mobility of these organisms were probably responsible for them being poorly represented in benthic samples (Ansell et al. 1972, Chardy et al. 1988, Frouin et al. 1998). Water flux in burrows generated by ventilation associated with interstitial water circulation due to sediment-reworking greatly contributes to the oxygenation of sediments (Forster & Graf 1992, Ziebis et al. 1996) and favours the persistence or the settlement of other macrobenthic populations. Moreover, their activity is also important in incorporating organic matter into deeper layers of the sediment and recycling in relation to the bacterial loop (Driscoll 1975, Anderson & Meadows 1978, Daumas 1990, Ebenhoh et al. 1995). In the highly impacted Harbour Zone, it is suggested that decapod activity is the key element in maintaining the di-
52
Mar Ecol Prog Ser
verse macrofaunal community. It appears that no equivalent ecological process has been recorded from temperate systems. It is strongly recommended that additional studies are carried out to confirm this important role, and the possible risks if decapod populations are not maintained. Reductions of the decapod population, or even loss of them, could lead to anoxic conditions developing and under such conditions, loss of the macrobenthic communities. This could have major impacts on the marine ecosystem of this region. In conclusion, this study has shown that the lagoon of Tahiti is ideally suited for studying disturbance, with enhanced effects on a small spatial scale (the lagoon never exceeds 2 km in width). Inputs from terrestrial sources into the lagoon were composed of fine terrigenous elements (silt and clay) and organic matter, and the amount of these inputs was related to coastal population densities. Lagoonal hydrodynamic patterns also played a n important role in the functioning of the ecosystem. Particulate organic and inorganic enrichment leads to a simplified trophic structure dominated by non-selective deposit-feeders, Dasybranchus sp. 1. In areas of high sedimentation bioturbation by decapods ensures that the sediments remain aerated and that diverse benthic communities a r e maintained. Acknowledgements. I would like to thank J . Orempiiller, N. Maihota. J. Paoaafaite and J. Teuri for their assistance in field and laboratory. I am also grateful to I. Karakassis for useful comments. Pat Hutchings corrected the initial drafts of this manuscript. This research was funded by ORSTOM (now IRD), the French Ministry for Education and Research, the French University of the Pacific, and the Research and Environment Delegations of French Polynesia. LITERATURE CITED Agard JBR, Gobin J , Warwick RM (1993) Analysis on marine macrobenthlc community structure in relation to pollution, natural oil seepage and seasonal disturbance in a tropical environment (Trinidad, West Indies). Mar Ecol Prog Ser 92:233-243 Alongi DM (1986) Population structure and trophic composition of the free-living nematodes inhabiting carbonate sands of Davies Reef, Great Barrier Reef, Australia. Aust J Mar Freshw Res 37:609-619 Alongi DM (1989) The role of soft-bottom benthic communities in tropical mangroves and coral reef ecosystems. CRC Crit Rev Aquat Sci 1:243-280 Alongi DM (1990)The ecology of tropical soft-bottom benthic ecosystems. Oceanogr Mar Biol Annu Rev 28:381-496 Alongi DM, Chnstoffersen P (1992) Benthic infauna and organism-sediment relations in a shallow, tropical coastal area: influence of outwelled mangrove d ~ l r i l u sand phyqical disturbance. Mar Ecol Prog Ser 81:229-245 .+2nderson JG, Meadows PS (1978) Microenv~ronmentsin marine scdiments. Proc R Soc Edinb Sect R Biol Sci 76:l-l6 Ansell AD, Sivadas P, Narayanan B, Sankaranrlrayanan VN,
Trevallion A (1972) The ecology of two sandy beaches in South West I n b a . I. Seasonal changes in physical and chemical factors, and in the macrofauna. Mar Biol 17:38-62 Bailey-Brock JH (1979) Sediment trapping by chaetopterid polychaetes on a Hawaiian fringing reef. J Mar Res 37543-655 Chardy P, Clavier J (1988) Biomass and trophic structure of the macrobenthos in the south-west lagoon of New Caledonia. Mar Biol 99:195-202 Chardy P, Chevillon C, Clavier J (1988) Major benthic commumties of the south-west lagoon of New-Caledonia. Coral Reefs 7:69-75 Clarke KR, Ainsworth M (1993) A method of linking multivariate community structure to environmental variables. Mar Ecol Prog Ser 92:205-219 Clarke KR, Green RH (1988) Statistical design and analysis for a 'biological effect' study. Mar Ecol Prog s e r 46: 213-226 Connell J H (1978) Diversity in tropical rain forests and coral reefs Science 199.1302-1310 Curras A, Sanchez-Mata A, Mora J (1994) Estudio comparativo d e la macrofauna bentonica d e un fondo d e Zostera marina y un fondo arenoso libre d e cubierta vegetal. Cah Biol Mar 35:91-112 Daumas R (1990) Contribution of the water-sediment interface to the transformation of biogenic substances: application to nitrogen compounds. Hydrobiologia 207:15-29 Dollar SJ, Tribble GW (1993) Recurrent storm disturbance and recovery - a long-term study of coral communities in Hawaii. Coral Reefs 12:223-233 Driscoll EG (1975) Sediment-animal-water interaction, Buzzards Bay, Massachusetts. J Mar Res 33:275-302 Ebenhoh W, Kohlmeier C , Radford PJ (1995) The benthic biological submodel in the European Reglonal Seas Ecosystem Model. Neth J Sea Res 33:423-452 Edgar GJ (1993) Estimates of the carrying capacity of benthic habitats using a metabolic-rate based index. Oecologia 95-115-121 Ellis JI, Schneider DC (1997) Evaluation of a gradient sampling design for environmental impact assessment. Environ Monit Assess 48:15?-172 Engle VD, Summers JK, Gaston GR (1994) A benthic index of environmental condition of Gulf of Mexico estuanes. Estuaries 17:372-384 Everett RA (1994) h4acroalgde in marine soft-sediment communities: effects on benthic fauna1 assemblages. J Exp Mar Biol Ecol 175:253-274 Fauchald K, Jumars P (1979) The diet of worms: a study of polychaete feeding guilds. Oceanogr Mar Biol Annu Rev 17:193-284 Fenchel TM (1969) The ecology of nlanne microbenthos. IV. Structure and function of the benthic ecosystem, its chemical and physical factors and the microfauna communities with special reference to the ciliated protozoa. Ophelia 61-182 Ferraro SP, Cole FA (1992) Taxonomic level sufficient for assessing a moderate impact on macrobenthic communities in Puget Sound, Washington, USA. Can J Fish Aquat Sci 49:1184-1188 Field J G , Clarkr! KR, Warwick Rh,l (1982) A practical strategy for analysing multispecies distribution patterns. >Tar Ecol Prog Ser 8:37-52 Folk RI., Ward NC (1957) Brazos River Rar: a study of the significdnce of grain size p a r a m e t ~ r s J. Sedrmpnt Petrol 27: 3-26 Forbes TL, Forbcts VE, Depledge X1H (1994) Individl~dlphysiological responses to environmental hypoxia and organic
Frouin: Anthropogenic disturbance!S of tropical benthic communities
53
enrichment: implications for early soft-bottom community succession. J Mar Res 52:1081- 1100 Forster S, Graf G (1992) Continuously measured changes in redox potential influenced by oxygen penetrating from burrows of Cahanassa subterranea. Hydrobiologia 235/236: 527-532 Frouin P (1996) Structure et fonctionnement des ecosystemes benthiques des lagons soumis aux perturbations anthropiques: le lagon de Tahiti (Polynesie f r a n ~ a i s e )PhD . thesis, French University of the Paciflc, Papeete Frouin P, Hutchings P (in press) Xfacrobenthic communities in a tropical lagoon (Tahiti, French Polynesia, Central Pacific Ocean). Coral Reefs Frouin P, Hily C, Hutch~ngsP (1998) Ecology of spionid polychaetes in the swash zone of exposed beaches in Tahiti (French Polynesia). C R Acad Sci Ser I11 Life Sci 321~47-54 Gallagher ED. Jumars PA, Trueblood DD (1983)Facilitation of soft-bottom benthic succession by tube-builders. Ecology 64:1200-1216 Grigg RW, Dollar SJ (1990) Natural and anthropogenic disturbance on coral reefs. In: Dubinsky Z (ed) Ecosystems of the world. coral reefs, Vol 25. Elsevier Science, Amsterdam, p 439-452 Grigg RW, Polovina JJ, Atkinson IMJ (1984) Model of a coral reef ecosystem. 111. Resource limitation, community regulatlon, fisheries yleld and resource management. Coral Reefs 3:23-27 Hansen JA, Alongi DM, Moriarty DJW, Pollard PC (1987) The dynamics of benthic microbial communities at Davies Reef, central Great Barrier Reef. Coral Reefs 6:63-70 Harris P (19981 Modification des caracteristiques chimiques du laqon d e Papeete 1.ieesa I'activlte humalne: inter& des trace& sedimentaires g6ochimques et biogkochimiques dans la reconstitution d e l'evolution d e l'environnement au cours des 150 dernieres annees. PhD thesis, French University of the Pacific. Papeete Harvey M, Gauthiet D, Munro J (1998) Temporal changes in the composition and abundance of the macro-benthic mvertebrate communities at dredged material dlsposal sites in the Anse a Beaufils, Baie des Chaleurs, Eastern Canada. Mar PoIlut Bull 36:41-55 Hatcher BG, Johannes RE, Robertson AI (1989) Review of research relevant to the conservation of shallow tropical marine ecosystems. Oceanogr Mar Biol Annu Rev 27:337-414 Help C (1995) Eutrophication and zoobenthos dynamics. Ophelia 41:113-136 Hily C (1985) kcologie d e la macrofaune benthique dans les sediments du port de Brest pollues par la matiere organique. Oceanis 11:263-276 Hily C, Frouin P (1998) Short term bioturbation activity in the lagoonal sediments of Tikehau atoll (Tuamotu Archipelago, French Polynesia). Int Rev Hydrobiol 83:335-347 Holm-Hansen 0 , Lsrenzen CJ, Holrnes RW, Strickland JDH (1965) Fluorometric determination of chlorophyll. J Cons Int Explor Mer 30:3-15 Hutchings P, Payri C, Gabrie C (1994) The current status of coral reef managment in French Polynesia. Mar Pollut Bull 29:26-33 Karakassis I, Eleftheriou A (1997) The continental shelf of Crete. structure of macrobenthic communities. Mar Ecol Prog Ser 160:185-196 Keough MJ. Quinn GP (1991) Causality a n d the choice of measurements for detecting human impacts in marine environments. Aust J Mar Freshw Res 42:539-554 Krumbein WC (1936) Application of logarithmic moments to size freauencv distribution of sediments. J Sediment Petrol 6:;5-47
Kruskal JB, Wish M (1978) Multidimensional scaling. Sage University Paper series on Quantitative Applications in the Social Sciences, 07-011. Sage Publications, Newbury Park, CA Lafforgue A (1984) Hydrologle de l'ile de Tahiti (aide-memoire succinct). Archives d'hydrologie Centre ORSTOM d e Tahiti 84-13:l-13 Lafforgue A (1994) ~ t u d ehydrologique pour l'amenagement d e la riviere Nymphea. Rapport d e campagne et elements de calcul pour Ies ouvrages d'assainissement des zones urbanisees du secteur Faaa-Punnauia. Hydro Consult International-GIE ORSTOM EDF, Papeete Long BG, Poiner IR (1994) Infaunal benthic community structure and function in the Gulf of Carpentdrid, Northern Australia. Aust J Mar Freshw Res 45293-316 Lsrenzen CJ (1967) Determination of chlorophyll and phaeopigments: spectrophotometric equations Limnol Oceanogr 12:343-346 Nickell LA, Atkinson RJA (1995) Functional morphology of burrows and trophic modes of three thalassinidean shrimp species, and a new approach to the classification of thalassinidean burrow morphology. Mar Ecol Prog Ser 128: 181-197 Nilsson HC. Rosenberg R (1994) Hypoxic response of two marine benthic communities. Mar Ecol Prog Ser 115: 209-211 Pastorok RA, Bilyard GR (1985)Effects of sewage pollution on coral reefs communities. mar Ecol Prog Ser 21:175-189 Pearson TH, Rosenberg R (1978) Macrobenth~csuccession in relation to organic enrichment and pollut~onof the marine environment. Oceanogr Mar Biol Annu Rev 16:229-311 Plantecuny MR, Salen-Picard C, Grenz C, Plante R, Alliot E, Barranguet C (1993) Experimental field study of the effects of crude oil, drill cuttings and natural biodeposits on microphytozoobenthic and macrozoobenthic communities in a Med~terraneanArea. Mar Biol 117:355-366 Riddle MJ (1988) Patterns in the distribution of macrofaunal communities in coral reef sediment on the central Great Barrier Reef. Mar Ecol Prog Ser 47:281-292 Riddle IMJ, Alongi DM, Dayton PK. Hansen JA, Klumpp DW (1990) Detrital pathways in a coral reef lagoon. Mar Biol 104:109-118 Torreton JP, Fouquet 0,Frouin P (1997) Bacteriobenthos biomass and productivity in relation to organic matter in the lagoon of Tahiti, Vol 2. In: Lessios HA, MacIntyre IG (eds) Proc 8th Int Coral Reef Symp. Smithsonian Troplcal Research Institute, Balboa, Panama, p 1857-1862 Vaugelas de J (1985)On the presence of the mud-shrimp Callichirus armatusin the sediments of Mataiva lagoon. Vol6. In: Gabrie et al. (eds) Proc 5th Int Coral Reef Cong Antenne Museum - EPHE, Moorea, French Polynesia, p 314-317 Warwick RM, Ruswahyuni (1987) Comparative study of the structure of some tropical and temperate marine soft-bottom macrobenthic communities. Mar Biol 95:641-649 Wolanski E, Delesalle B, Dufour V, Aubanel (1993) Modeling the fate of pollutants in the Tiahura lagoon, Moorea, French Polynesia. In: Proc 11th Aust Conf Coastal Ocean Engineering. Institution of Engineers. Townsville, p 583-587 Ziebis W, Forster S, Huettel M, Jsrgensen BB (1996) Complex burrows of the mud shrimp Callianassa truncata and their geochemical impact in the sea bed. Nature 382:619-622 Zmarzly DL, Stebbins TD, Pasko D, Duggan RM, Barwick KL (1994) Spatial patterns and temporal succession in softbottom macroinvertebrate assemblages surrounding a n ocean outfall on the southern San Diego Shelf: relation to anthropogenlc and natural events. Mar Biol 118:293-307
Editorial responsibility: John Gray (Contributing Editor), Oslo, Norway
Subnlitted: September 9, 1998; Accepted: July 13, 1999 Proofs received from author(s): March 2, 2000
