Ecological Indicators 61 (2016) 676–682
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Ecological Indicators
jo ur nal ho me page: www.elsevier.com/locate/ ecolind
The use of a functional approach as surrogate of Collembola species
richness in European perennial crops and forests
Filipa Reis
a,∗,1
, Filipe Carvalho
a,1
, Pedro Martins da Silva
a
, Sara Mendes
a
,
Sónia A.P. Santos
b
, José Paulo Sousa
a
a
Centre for Functional Ecology, Department of Life Sciences, University of Coimbra, Calc ¸ ada Martim de Freitas, 3000-456 Coimbra, Portugal
b
Mountain Research Centre (CIMO), School of Agriculture, Polytechnic Institute of Braganc ¸ a, PO Box 1172, 5301-855 Braganc ¸ a, Portugal
a r t i c l e i n f o
Article history:
Received 20 April 2015
Received in revised form
30 September 2015
Accepted 5 October 2015
Available online 7 November 2015
Keywords:
Community traits
Functional diversity
Indicator tools
Biodiversity monitoring programmes
Soil quality
a b s t r a c t
Collembolans are known indicators of soil disturbance, used in several soil biodiversity monitoring pro-
grammes. As for other groups of soil microarthropods, taxonomic determination of Collembola species
requires a huge effort and expert knowledge. In this study, we evaluated whether identification of Collem-
bola species to the morphotype level, using an eco-morphological index which classifies individuals based
on their adaptation to the soil, can be used as a surrogate of species richness in extensive monitoring
schemes. The same evaluation was performed for higher taxa surrogates, using taxonomic categories
at the genus and family levels. Additionally, sampling effort for perennial crops and forest systems was
determined. Species data were collected from 35 sites sampled within different projects with the same
number of samples (16 per site). Results showed that, on average, 8–12 samples are enough to have a
good estimate of species richness for this type of systems, averaging 80–90%, but varying considerably
with site habitat heterogeneity and local Collembola species pool. GLM models (using species richness as
response variable) fitted for family, genus or morphotype levels (explanatory variables) were all signifi-
cant (p < 0.05) but only the latter two had a pseudo R
2
higher than 0.75. This indicates that when a rapid,
cost-effective assessment of Collembola richness in different sites is required, this eco-morphological
trait approach, as well as the determination to the genus level, could be used.
© 2015 Elsevier Ltd. All rights reserved.
1. Introduction
Decline of soil biodiversity has been identified as one of the
main threats to soil functioning and sustainability of natural and
semi-natural ecosystems (Kibblewhite et al., 2008). Currently,
some extensive monitoring schemes have been used in Europe for
assessing soil quality and biodiversity, mainly in agro-ecosystems
(Breure et al., 2005; Gardi et al., 2009). However, because these
monitoring programmes often involve the determination of the
soil organisms to the species level, they are too expensive to be
used over a broad scale, across ecosystems and eco-regions, and at
the desired frequency, necessary to detect deviations from species
richness “normal operational range”.
To overcome this caveat, several alternative approaches have
been suggested to predict species richness and to monitor the spa-
tial and temporal distribution of biodiversity (Cardoso et al., 2004),
from which the use of surrogates to invertebrate fauna has been
∗
Corresponding author. Tel.: +351 967367738.
E-mail address: ferreirareis.filipa@gmail.com (F. Reis).
1
These authors contributed equally to this work.
widely discussed (Andersen, 1995; Biaggini et al., 2007; Brennan
et al., 2006; Cardoso et al., 2004; Derraik et al., 2002; Duelli and
Obrist, 1998; Lovell et al., 2007; Sauberer et al., 2004).
Surrogacy can use different approaches: the higher taxon
approach (Gaston and Williams, 1993) which is addressed in
this study, environmental variables (Braithwaite et al., 1989), and
species richness of indicator groups (Faith and Walker, 1996).
The higher taxonomic level approach (i.e., using genus or
families) is particularly advantageous for large-scale monitoring
schemes, since it delivers information on a large number of taxa,
while not requiring as many time and resources as a species-level
identification would do (Cardoso et al., 2004; Gaston and Williams,
1993), considering that there is a smaller number of higher taxa
and they are more easily identified than species.
Despite the advantages of this approach, there are certain factors
influencing the relationship between species richness and higher
taxa richness that should not be disregarded. Andersen (1995)
noted that this relationship is influenced by sampling intensity,
since when the number of samples increase, more species belong-
ing to higher level taxa already registered can keep being recorded.
Therefore, when doing surrogacy studies, sampling effort is an
important factor to take into account. Despite being essential for
http://dx.doi.org/10.1016/j.ecolind.2015.10.019
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