Effects of urban wastewater on crab and mollusc assemblages in equatorial and subtropical mangroves of East Africa

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Abstract

Mangrove forests are known to accomplish crucial ecosystem functions and services. They are nursery areas for fish, prawns and crabs, which provide coastal communities with a variety of food, timber and chemicals, and protect coasts from catastrophic events, such as tsunamis. Recently, a novel ecological service has been proposed for mangrove systems, namely natural wastewater treatment wetlands. This hypothesis was based on experimental data collected mainly in Chinese mangrove systems, which proved that mangrove soils were efficient in absorbing nutrients. Moreover, sewage loading seemed harmless to both plants and benthic communities in these systems. However, before promoting the use of natural mangroves as pollution buffers, or constructed mangrove wetlands as sewage treatment facilities, more data are needed on their overall tolerance to organic loading. Differences in macrobenthos patterns were thus investigated between peri-urban mangroves and sites not affected by sewage disposal in East Africa. We assessed differences in epifaunal assemblages, comprising crabs and molluscs, employing multivariate ACI unbalanced analyses to compare peri-urban mangrove swamps with those characteristic of non-urban mangroves with similar ecological traits. The sampling design was spatially nested, replicates being assessed at equatorial (southern Kenya) and subtropical (southern Mozambique) sites. The results manifested a consistent increase in crab biomass at the peri-urban sites in both Kenya and Mozambique. Moreover, the peri-urban systems were richer than the non-urban mangroves, both in terms of fiddler crabs (Uca spp.) which feed on benthic microalgae and bacteria, and sesarmids, such as Perisesarma guttatum and Neosarmatium meinerti, which feed on both substratum and leaf litter. The abundance of gastropods, in contrast, decreased significantly, especially in Kenya, mainly due to the disappearance of the mud whelk Terebralia palustris. The results thus indicate that, in East African mangrove systems, domestic wastewater has detectable effects on crabs and molluscs, suggesting their usefulness as bioindicators of its effects in mangroves. Transformed benthic patterns at the peri-urban sites indicated the need for further study of the actual potential of natural mangrove forests to absorb pollution in sewage treatment.

Introduction

Mangrove forests accomplish a number of ecosystem functions and services (Duke et al., 2007). Rates of net primary production in mangrove forests are the highest of any ecosystem (> 2 t ha−1 yr−1), and vast amounts of carbon accumulate within their underlying litter (Alongi, 1998, Chmura et al., 2003). As a result, they play a key role in nutrient cycling in coastal ecosystems and global carbon cycling, and have been demonstrated to act both as nutrient sources and sinks (Kristensen et al., 2008). Carbon cycling and other ecosystem processes in mangroves provide crucial ecosystem services to estuarine habitats such as nursery areas for fish, prawns and crabs (Sheridan and Hays, 2003, Crona and Rönnbäck, 2005, Nagelkerken et al., 2008). Coastal human communities which live near mangrove areas also rely on the provision of a variety of food, timber, chemicals and medicines derived from mangrove forests (Ewel et al., 1998, Glaser, 2003, Walters et al., 2008). Their ecological function in coastal protection was demonstrated in the 2004 tsunami when mangroves in good ecological condition proved effective in this regard (Dahdouh-Guebas et al., 2005, Kathiresan and Rajendran, 2005). Last but not least, mangroves host a unique set of associated fauna, such as semi-terrestrial and tree-dwelling brachyuran crabs (Fratini et al., 2005, Cannicci et al., 2008) and insects (Cannicci et al., 2008), and, within soft-sediment habitats, they provide a unique hard-sediment substratum needed for a unique and diverse assemblage of benthos (Farnsworth and Ellison, 1996).

Apart from the above, some researchers have suggested that they have potential as natural wastewater treatment areas, a much-debated subject (Clough et al., 1983, Wong et al., 1995, Wong et al., 1997). Mangrove ecosystems and, in particular, their sediments are very efficient in absorbing nutrients, mainly phosphorous and nitrogen, derived from sewage (Tam and Wong, 1995, Tam and Wong, 1996a, Tam and Wong, 1996b) and shrimp farming effluent (Trott et al., 2004). Moreover, in a field trial of two years in the Funtian Mangrove, P.R.C., Wong et al. (1997) found that sewage disposal had no harmful effect on the higher plant communities. Yu et al. (1997) detected no significant effects of wastewater on benthic biomass, density and community structure at the same experimental site, although they measured a significant decrease in the diversity and biomass of gastropods and interpreted this as a transient phenomenon followed by a recovery phase.

Although these studies of Chinese mangroves may suggest that they are tolerant to a degree of wastewater pollution, much concern still exists about the use of natural mangrove sites for sewage disposal. Kathiresan and Bingham (2001) suggest that the results obtained at Funtial Mangrove may not be applicable to other sites, since Indo-Pacific mangrove forests differ widely and their unique characteristics may lead to differences in tolerance to this perturbation. A second reason for caution relates to the effects of such organic loading on other crucial ecosystem processes and services provided by mangroves, such as the aforementioned functions as nursery grounds and a source of resources for coastal communities (Hogarth, 2007). The recent, extensive research on the use of constructed mangroves as wetlands for domestic wastewater treatment (Yang et al., 2008) could lead to the use of natural mangroves, which are being increasingly threatened by human activities, for this purpose.

The literature on the effects of sewage and peri-urban effluents on the faunal components of other shallow water ecosystems is not encouraging. In fact, although faunal assemblages in mangroves vary considerably spatially, which often confounds the results (Lindegarth and Hoskin, 2001, Chapman and Tolhurst, 2004), the macrofaunal distribution and diversity in peri-urban coastal systems have proven susceptible to a variety of pollutants and impacts, such as metals (Birch, 1996, Bergey and Weiss, 2008), pesticides (Garmouma et al., 1998), hydrocarbons (Siewicki, 1997, Inglis and Kross, 2000) and altered nutrient loads (Carpenter et al., 1998). Although it is often difficult to disentangle the specific effects of these many causes of disturbance, sewage disposal is surely one of the major causes of diversity loss in intertidal (Lercari and Defeo, 2003, Wear and Tanner, 2007) and subtidal coastal ecosystems (Roberts, 1996, Roberts et al., 1998). It appears difficult to hypothesise that wastewater dumping would not result in major changes in mangrove macrofauna.

Based on this background of concerns, the present study was designed to investigate the differences in macrobenthic patterns between peri-urban mangroves, impacted by sewage disposal, and non-urban sites with no evident wastewater disposal, in East Africa. We focused on key macrobenthic species, such as brachyuran crabs and molluscs that are heavily exposed to such perturbation, being strict residents of mangroves throughout their adult life (Skov et al., 2002, Fratini et al., 2004) that ingest sediment and leaf litter (Cannicci et al., 2008).

Section snippets

Study area and sampling design

To assess possible impacts of sewage on crab and mollusc assemblages, a multivariate ACI (After Control/Impact, Underwood, 1992, Underwood, 1994) unbalanced design was followed, comparing the macrofaunal patterns found in a peri-urban mangrove swamp with those characteristic of two non-urban mangroves showing similar ecological traits. The unbalanced ACI sampling design was spatially replicated at equatorial (southern Kenya) and subtropical (southern Mozambique) sites. The mangroves selected

Assemblages

The asymmetrical design of PERMANOVA revealed site differences in both the Avicennia and Rhizophora belts (Table 1), and the epifaunal assemblages differed markedly between locations and sampling periods. In the Avicennia belt, a significant interaction of time and I vs C emerged, testifying to temporal variability in differences between the two control sites.

There was a higher abundance and species diversity within the Avicennia belt at the impacted site than the control sites, where a higher

Discussion

Two major points must be emphasised in discussing the results of this study. The first is the high variability in macrofaunal assemblages, not only at small and large spatial scales, but also on a temporal scale, and the second is that, in spite of this variation, clear and consistent patterns between non-urban and peri-urban mangroves were detected, especially in terms of biomass.

The use of a stratified sampling design, adapted to the natural zonation of East African mangrove forests (Macnae,

Conclusions

The present results show that East African mangrove crab and mollusc populations are significantly affected by domestic wastewater, in contrast to the findings of Yu et al. (1997) in the Futian Mangroves in the P.R.C. There were marked differences in benthic patterns at the peri-urban sites compared to the control sites, the crabs at the former being consistently higher in density and biomass at both the equatorial and subtropical locations. On the other hand, lower densities of gastropods were

Acknowledgements

This study formed part of the PUMPSEA project (peri-urban mangrove forests as filters and potential phytoremediators of domestic sewage in East Africa), contract no. INCO-CT2004-510863, funded by the European Commission within the 6th Framework programme. The authors are indebted to Fundação para a Ciência e Tecnologia (FCT), Portugal, for a scolarship to GPL (SFRH/BD/25277/20005) and to the Fund for Scientific Research (FWO – Vlaanderen) and The Funds for Academic research of the Italian MUR

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