Ecological Indicators 11 (2011) 395–406
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Ecological Indicators
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Original article
Determinants of wintering waterbird changes in a Mediterranean coastal lagoon
affected by eutrophication
F. Robledano
∗
, M.A. Esteve, J. Martínez-Fernández, P. Farinós
Departamento de Ecología e Hidrología, Facultad de Biología, E-30100 Espinardo (Murcia), Spain
article info
Article history:
Received 2 October 2009
Received in revised form 7 June 2010
Accepted 17 June 2010
Keywords:
Coot
Grebes
Indicators
Jellyfish
Monitoring
Nutrients
abstract
Southern Mediterranean lagoons are among the more vulnerable systems regarding human activities
(e.g. agriculture, tourism, urbanization) leading to eutrophication. We analyse the relationship of water-
birds with locally measured or modelled environmental variables (nutrient load, fish production, jellyfish
blooms) related with this process, in the Mar Menor lagoon (Murcia, SE Spain), and discuss the potential
value of birds as indicators of the trophic status of the wetland. We use GLMs to relate the biomass of the
five most abundant and representative waterbird species to these variables, accounting for the poten-
tial influence of external factors affecting their population at higher biogeographical scales. A significant
effect of such factors was only found for Great Cormorant, which biased the positive response of the
piscivore guild to nutrient load (NLD). Red-breasted Merganser appeared relatively insensitive to nutri-
ent enrichment, although declined in the long term. The remaining species responded positively, NLD
being a significant predictor of their biomass when a 2-year lag was allowed, although this variable alone
had a low explanatory power except for the Coot. When homogeneous temporal phases were defined,
grebes could be identified as early warners of eutrophication, and Coot as late-stage ones. The increase
of piscivores along a period of declining fish catches could reflect a shift in fish community composition
or structure that favours their feeding preferences. The interactive role of jellyfish, buffering temporally
the loading of nutrients, may also be related to these changes.
© 2010 Published by Elsevier Ltd.
1. Introduction
Wetlands and coastal waters experience strong pressures on
their biodiversity and water quality (e.g. Maltby, 1986; Gibbs,
2000), due to the strong human demands on their surrounding
land, shoreline and littoral waters (Gopal, 2003). Southern Mediter-
ranean lagoons are among the most vulnerable systems to such
pressures (De Stefano, 2004; Viaroli et al., 2005). They are influ-
enced by intensively farmed and densely populated watersheds,
particularly during summer when the Mediterranean becomes the
major world’s tourism hotspot (Vogiatzakis et al., 2006). Eutroph-
ication is one of the main consequences (Caddy and Bakun, 1995),
and despite a number of studies have focused on this process (e.g.
Delbaere and Nieto-Serradilla, 2004; García Pintado et al., 2007),
there is still little information about the response of biodiversity
to the biotic changes that it brings. The lack of adequate datasets
on nutrient inputs into the lagoons is an important obstacle for
such research, although environmental modelling has partially off-
set this gap (Rodríguez et al., 2005). Unfortunately there are not
∗
Corresponding author. Tel.: +34 868 88 43 24; fax: +34 868 88 39 63.
E-mail address: frobleda@um.es (F. Robledano).
comparable datasets on “response” biological variables for the same
time span, with the exception of wintering waterbirds, regularly
counted for decades in many Mediterranean wetlands (Hoffmann
et al., 1996).
Waterbirds are considered useful indicators of changes in wet-
lands, responding in an integrative manner to stressors (Kushlan,
1993; Adamus, 1996; Amat and Green, 2009). Although the use of
indicators based on bird numbers has been critiziced (Morrison,
1986; Landres et al., 1988), they often associate with changes in
the structure and functioning of wetland ecosystems (Kerekes and
Pollard, 1994; Noordhuis et al., 2002; Hebert et al., 2009). Besides,
birds are well studied and monitored (many non-professional
ornithologists are willing to help create data sets for large-scale
studies). A growing number of papers are including waterbirds,
coupled with other environmental data, in studies of water quality
and ecological restoration of wetlands and coastal waters (Ysebaert
et al., 2000; Stapanian et al., 2004; Holm and Clausen, 2006;
Philippart et al., 2007).
In the framework of an EU-funded research project (DITTY),
aimed at the development of decision-support tools for the
management of Mediterranean lagoons and their watersheds,
we started to consider waterbirds as indicators of environ-
mental change. Wintering waterbird censuses in one of these
1470-160X/$ – see front matter © 2010 Published by Elsevier Ltd.
doi:10.1016/j.ecolind.2010.06.010