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Résumé:

L’article qui suit analyse l'impact d'eaux usées domestiques sur le fonctionnement et la dynamique de la végétation de la mangrove de Malamani, après 12 et 18 mois de rejets. Une vue aérienne du site d’étude, complétée par des observations sur le terrain de la dynamique de croissance des rameaux et feuilles de palétuviers révèle un effet évident des eaux usées sur la végétation. Sur photographies prises par vol ULM, les parcelles impactées se démarquent du reste de la végétation de mangrove par une coloration verte plus intense. Sur le terrain, la comparaison de feuilles prélevées sur les parcelles impactées et sur les parcelles témoins équivalentes confirme ce changement de coloration.

Pour analyser ces changements en lien avec les rejets d'eaux usées, la structure de la végétation, l’efficacité photosynthétique, la concentration en pigments foliaires, et la croissance des palétuviers ont été suivies dans les parcelles impactées et témoins de deux faciès de mangrove respectivement dominés par Ceriops tagal et Rhizophora mucronata..

La structure de la végétation a été analysée avant les premiers rejets d'eaux usées (novembre 2006,) puis 6 mois et 18 mois après le début des rejets. Aucune différence significative n'a été observée dans la période et la structure de la végétation n'a pas été modifiée en termes de densité ou de taux de mortalité.

En revanche, l’apport d'eaux usées domestiques prétraitées sur deux faciès de végétation engendre une augmentation significative de l’efficacité photosynthétique, de la concentration en pigments, et de la croissance des palétuviers. Pour C. tagal, la concentration en chlorophylle a double entre la parcelle témoin et la parcelle impactée (1,47 à 2,88 mg.g-1

MS (janvier 2009) et 1,23 à 3,28 mg.g-1MS (avril 2009)). La concentration moyenne en caroténoïdes augmente de 0,39 (témoin) à 0,83 mg.g-1

MS (impactés), et en xanthophylles de 0,07 (témoin) et 0,14 mg.g-1

MS (impactés). Pour R. mucronata, la concentration en chlorophylle a augmente aussi significativement de 2,08 à 2,87 mg.g-1

MS (janvier 2009) et de 3,01 à 4,01 mg.g-1

MS (avril 2009). La concentration moyenne en caroténoïdes augmente de 0,70 (témoin) à 0,9 mg.g-1MS (impactés), et en xanthophylles de 0,12 (témoin) et 0,17 mg.g-1MS (impactés).

Le taux photosynthétique moyen augmente significativement de 5,98 (témoin) à 9,69 (impacté) µmol.m-2

.s-1

pour les C. tagal ainsi que pour les R. mucronata : 8.68 (témoin) contre 10,66 (impacté) µmol.m-2

.s-1

. Enfin, les effluents ont aussi engendré une augmentation significative de la croissance des palétuviers, en particulier de la longueur et largeur des feuilles, de la taille des rameaux et de la longueur des propagules.

Composées essentiellement de N, P et véritable apport en eau douce, les eaux usées ont le même effet qu’un fertilisant, d’autant plus dans un milieu aussi pauvre en nutriments et aussi salé que les sédiments de mangrove. Ces résultats mettent en avant la capacité de cet écosystème à absorber l’apport de composants organiques comme l'azote sans provoquer de rupture dans l’équilibre fonctionnel observable à court terme et sans effets secondaires apparents sur la végétation. Cependant, de récents articles ont mis en avant des conséquences négatives face à l'enrichissement excessif en éléments nutritifs dans la mangrove (Martin et al., 2010), pouvant même conduire à la mort des palétuviers dans des condition de salinité élevée (Lovelock et al.., 2009).

Si nos résultats semblent démontrer que des eaux usées domestiques ont des effets positifs sur le fonctionnement de la mangrove après 18 mois de rejets, certains auteurs montrent néanmoins que l’excès de N et P pourrait, dans certains cas, entrainer une rupture fonctionnelle pour la végétation de mangrove (Lovelock et al., 2009 ; Martin et al., 2010). Tandis que nos résultats préliminaires montrent que les eaux usées sont absorbées par les palétuviers et stimulent le fonctionnement de la végétation, des expérimentations doivent être poursuivies et des bilans de N total et P doivent être établis afin d’évaluer l'efficacité bioremédiatrice de la mangrove et de connaitre les effets cumulés de l’apport des eaux usées à plus long terme.

Effects of pretreated domestic wastewater supplies on leaf pigment content, photosynthetic efficiency and growth of mangrove trees: a field study from

Mayotte Island, SW Indian Ocean. M. Hertemana,

*, F. Fromarda

, L. Lambsa

,

a

ECOLAB - Laboratoire d'écologie fonctionnelle, UMR 5245 (CNRS-UPS-INPT), 29 rue Jeanne Marvig - 31055 Toulouse- France

* Corresponding author,

Tel: 00 33 5 62 26 99 86 Fax: 00 33 5 62 26 99 99

E-mail adresses : herteman@cict.fr, lambs@cict.fr

Submitted for publication to Environmental Pollution Abstract

After 12 and 18 months of daily wastewater discharge onto mangrove plots in Mayotte Island, SW Indian Ocean, leaf pigment content, photosynthetic efficiency and growth of Rhizophora

mucronata and Ceriops tagal mangrove trees were evaluated and compared with similar

individuals from control plots. Chlorophyll and carotenoid contents, measured using an HPLC analyser, were significantly higher in leaves of mangrove trees receiving wastewater discharges. Photosynthetic efficiency and transpiration rate, analysed using an LCi portable system, increased significantly for mangrove trees in impacted plots. Measurements of leaf areas, young branch length and propagule length showed significant increases in plots receiving wastewater. These results suggest a beneficial effect of domestic wastewater on R.

mucronata and C. tagal mangrove tree functioning. Analyses and observations on mangrove

ecosystems as a whole – taking into account water and sediment compartments, crab populations and nitrogen and phosphorus cycles – are nevertheless necessary for evaluation of bioremediation capacities of mangrove ecosystems.

Keywords: Wastewater, Mangrove plants, Photosynthesis, Chlorophyll, Growth

1. Introduction

1.1. Mangroves and bioremediation

The utilisation of mangrove swamps as natural systems for wastewater treatment has been proposed as an efficient and low-cost solution for tropical coastal areas. Characterised by a high primary production and biomass and established as often as not on nutrient-poor sediments, mangrove ecosystems are considered able to absorb nutrients in excess contained in sewage, without any major structural or functional disturbance (Saenger, 2002).

Nedwell (1975) showed that the discharge of pretreated wastewater into a mangrove swamp in Fiji could be a means of reducing eutrophication in coastal waters, and therefore suggested that mangroves might be used as the final stage in sewage treatment. Clough et al. (1983) published one of the first review articles dealing with the impact of sewage on mangrove ecosystems. These authors established that the capacity of mangroves to remove nutrients from sewage was largely determined by hydrodynamic factors in the short term and that the efficiency of the processes was largely dependent on the sediment properties and biological characteristics of the ecosystem in the longer term. Corredor and Morell (1994) demonstrated that the excess nitrogen coming from a sewage treatment plant in Puerto Rico could be absorbed by the mangrove ecosystem through natural denitrification processes, without any damage.

In an exploration of the different aspects of the role of mangrove swamps as sinks for wastewater-borne pollutants through numerous experiments conducted in the Hong Kong and Shenzen area (South China), Tam and Wong (1995, 1996) successively showed that mangrove soils are good traps to fix phosphorus and certain heavy metals from wastewater; that no significant change was observed in the plant community structure or in leaf nutrient content of a mangrove site receiving wastewater discharges for one year (Wong et al., 1995, 1997); and that litter production and decomposition were not perturbed (Tam et al., 1998). The addition of wastewater to mangrove soils also seems to stimulate the growth of microbial populations, probably through nutrients and carbon components present in wastewater (Tam, 1998). More recently, these authors showed that a mangrove plant community growing in a constructed microcosm receiving wastewater was effective in removing organic matter, nitrogen and phosphorus (Wu et al., 2008), but also indicated from greenhouse experiments that strong wastewater discharge could induce disturbances in the functioning of the mangrove tree rhizosphere (Pi et al., 2010).

1.2. Mangrove tree growth and nutrient enrichment

While the use of mangrove ecosystems for removing pollutants from sewage discharges is becoming rather well documented, the response of mangrove plants themselves in terms of growth should be analysed and controlled, and results in this domain are still contradictory. Henley (1978) reported that mangrove tree growth in Darwin area,Australia, was not affected when they received sewage discharges, and Clough et al. (1983) concluded that nutrient enrichment of a mangrove ecosystem through wastewater supply did not appear harmful and in some cases might have a beneficial effect on growth and productivity. Kelly (1995),

investigating the impact of sewage effluents on mangroves dominated by Avicennia marina in Australia, found that the N and P leaf concentrations were higher at impacted sites, but no clear growth-enhancing effects were noted at these same sites. From similar experiments concerning the two mangrove species Kandelia candel and Aegiceras corniculatum, Wong et al. (1995) did not find any significant differences in plant growth after one year of sewage discharges, but noted that effects – positive or adverse – on vegetation functioning could become apparent only over a longer term. Mandura (1997) studied A. marina stands in Saudi Arabia that had received sewage discharges for at least 15 years, and showed that growth, distribution and structure of pneumatophores had been greatly perturbed, leading to retarded growth of the mangrove trees.

More recently, Lovelock et al. (2009) established that nutrient enrichment (N and P) could increase the mortality of mangroves in sites characterised by low annual rainfall and high sediment salinity. These authors added that mortality rates were significant in landward scrub forests and no tree deaths occurred in fringe forests. Lovelock et al. (2004) and Martin et al. (2010) specified that N and P enrichment significantly increased mangrove tree growth, but in certain salinity conditions might alter the structure of mangrove forests.

1.3. Mangrove tree functioning and environmental stresses

Relationships between nutrient enrichment and metabolic processes in mangroves are still little documented. Peculiarly, data on photosynthesis activity in mangrove trees as a functional marker of their health state are rare; such data are generally linked to hydrological and salinity parameters and take into account propagule populations in greenhouse conditions (Ball and Farquhar, 1984; Youssef and Saenger, 1998; Kao and Tsai, 1999; Kao et al,. 2001; Krauss and Allen, 2003). Some studies considered the links between mangrove structure (scrub vs. fringe mangrove), mangrove tree height and photosynthesis characteristics (Lin and Sternberg, 1992; Lovelock et al., 2004), and Naidoo and Chirkoot (2004) established in a specific context that photosynthetic performance of A. marina was reduced when coal dust was deposited on the leaf surface of the mangrove trees.

In other studies, pigment content of mangrove leaves has been analysed in relation to the light environment of the mangrove forest canopy (Lovelock and Clough, 1992; Moorthy and Kathiresan, 1997). Rajesh et al. (1998) established correlations between growth rate, photosynthetic and pigment characteristics, and salinity levels for Ceriops populations. MacFarlane and Burchett (2001) showed that photosynthetic pigment concentration decreased in A. marina populations impacted by heavy metals, and MacFarlane (2002) suggested that