Ecological Indicators 37 (2014) 105–118
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Ecological Indicators
jou rn al hom epage: www.elsevier.com/locate/ecolind
Can different biological indicators detect similar trends of marine
ecosystem degradation?
Sofia Henriques
a,∗
, Miguel Pessanha Pais
a
, Marisa Isabel Batista
a
, Célia M. Teixeira
a
,
Maria José Costa
a,b
, Henrique Cabral
a,b
a
Centro de Oceanografia, Faculdade de Ciências, Universidade de Lisboa, 1749-016 Lisboa, Portugal
b
Departamento de Biologia Animal, Faculdade de Ciências, Universidade de Lisboa, 1749-016 Lisboa, Portugal
a r t i c l e i n f o
Article history:
Received 12 April 2013
Received in revised form 8 October 2013
Accepted 13 October 2013
Keywords:
Benthic macroinvertebrate assemblages
Fish assemblages
Marine soft-substrates
Structural and functional approach
Anthropogenic pressures
Human pressure index
a b s t r a c t
Marine ecosystems are typically under the influence of multiple Human activities, which hinders the
assessment of the effects of a specific activity upon their biological assemblages. In this context, distance-
based linear models were used to analyse the relationships of several structural and functional metrics
of both macroinvertebrates and fish assemblages with the specific types of pressure (i.e. fishing, organic,
physical and non-point-source) as well as the global pattern of cumulative pressures. Both indicators
detected similarly the effects of the global degradation and the analyses of the metrics’ sensitivity (given
the expected response trends) suggested that the non-point-source had the strongest contribution to this
pattern, followed by organic pollution. The difficulties of assessing single pressure effects in a multiple
pressures context are discussed. An approach based on the previous identification of pressure sources, a
sampling strategy directed to those sources, together with indicator response is highly recommended, as
it could be the only way to accurately predict human-induced changes on broad range ecosystems, with
likely implications in the success of marine management plans.
© 2013 Elsevier Ltd. All rights reserved.
1. Introduction
Awareness of the harmful effects of human pressures on the
marine environment has resulted in an increasing attention to
monitoring using biological indicators, in order to identify which
human pressures are driving changes on the ecosystem structure
and function, as well as design management plans to minimize
impacts (Niemi et al., 2004; Rogers and Greenaway, 2005; Smale
et al., 2010). In this context, recent policies have been developed
with the purpose of promoting sustainable use of marine resources
and protect marine ecosystems (e.g. Marine Strategy Framework
Directive, MSFD; Directive 2008/56/CE). To implement the MSFD,
an integrated ecosystem-based approach should be applied, giving
priority to the attainment of a “good environmental status” through
the assessment of physical and chemical elements, together with
several biological indicators, among which are fish and macroin-
vertebrates (see Annex III in Directive 2008/56/CE).
Due to the difficulty of analysing patterns of change in com-
plex, spatially and temporally diverse multi-species assemblages,
the need to assess environmental status comes with new challenges
concerning the use of biological indicators in marine waters (Mee
∗
Corresponding author. Tel.: +351 217500826; fax: +351 750 02 07.
E-mail addresses: snpires@fc.ul.pt, henriques.sofia@gmail.com (S. Henriques).
et al., 2008; Niemi et al., 2004; Niemi and McDonald, 2004). Addi-
tionally, stress in marine ecosystems is usually characterized by
the effects of multiple human pressure sources, and as physical
boundaries between marine habitats are difficult to define, thus
the identification of pressures that are affecting an area consti-
tutes a complex task (Ban et al., 2010; Niemi et al., 2004). This
way, coupling human pressure and biological response analyses
is essential to link the causes of stress to the response of indicators.
Otherwise, it would be extremely difficult to identify sources of dis-
turbance, unless specific metrics for each pressure exist and detect
such changes (Niemi et al., 2004; Niemi and McDonald, 2004).
Earlier attempts at comparing the response of fish-based and
macroinvertebrate-based metrics have been focused on freshwater
ecosystems (e.g. Hering et al., 2006; Johnson et al., 2006; Marzin
et al., 2012). In general, these studies showed that macroinver-
tebrates and fish have different sensitivities depending on the
human pressure analysed, with fish responding more to hydrolog-
ical changes, while macroinvertebrates show a higher sensitivity
to water quality and/or geomorphological changes (Hering et al.,
2006; Marzin et al., 2012). However, these assemblages differ
deeply from those of marine waters. For example, fish assemblages
are known to be species-poor in streams (Hering et al., 2006). To
the best of our knowledge, only few studies have compared the
response of multiple indicators in coastal waters (marine and estu-
arine ecosystems), but through multimetric indices (e.g. Azevedo
1470-160X/$ – see front matter © 2013 Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.ecolind.2013.10.017