Ecological Indicators 46 (2014) 70–77
Contents lists available at ScienceDirect
Ecological Indicators
jo ur nal ho me page: www.elsevier.com/locate/ ecolind
Assessing the consequences of biological invasions on species with
complex life cycles: Impact of the alien crayfish Procambarus clarkii on
Odonata
Matteo Elio Siesa
a,b,1
, Emilio Padoa-Schioppa
c
, Jürgen Ott
d,e
, Fiorenza De Bernardi
a
,
Gentile Francesco Ficetola
c,f,g,∗
a
Dipartimento di Biologia, Università degli Studi di Milano, Via Celoria 26, 20133 Milan, Italy
b
Via L. settembrini, 14, 20092 Cinisello Balsamo, MI, Italy
c
Dipartimento di Scienze dell’Ambiente e del Territorio, Università degli Studi di Milano-Bicocca, Piazza della Scienza 1, 20126 Milan, Italy
d
L.U.P.O. GmbH, Friedhofstr. 28, 67705 Trippstadt, Germany
e
Department of Environmental Sciences, University of Landau, Germany
f
Laboratoire d’Ecologie Alpine (LECA), Univ. Grenoble Alpes, LECA, F-38000 Grenoble, France
g
CNRS, LECA, F-38000 Grenoble, France
a r t i c l e i n f o
Article history:
Received 19 January 2014
Received in revised form 28 May 2014
Accepted 30 May 2014
Keywords:
Biological impact
Damselfly
Dragonfly, Early assessment,
Environmental features, Freshwater
community, Procambarus clarkii
a b s t r a c t
The temporal dimension is a key parameter when analysing the impact of invasive alien species. Studies
on early invasion stages allow a better understanding of how ongoing processes modify native communi-
ties, helping to plan effective management actions. Procambarus clarkii is an invasive crayfish influencing
multiple features of invaded wetlands, but unravelling its impact on organisms with complex life cycles is
difficult. We monitored 107 wetlands in Northern Italy, and evaluated the relationships between P. clarkii
and the richness of three life history stages of odonates: adults, larvae and exuviae. We measured envi-
ronmental features of each wetland and the natural vegetation in the surrounding landscape. We used an
information-theoretic approach to relate species richness of the three life history stages of odonates to:
wetland features, features of the surrounding landscape; crayfish presence. We used a spatially explicit
technique (Moran Eigenvector Mapping) allowing the integration of spatial autocorrelation into anal-
yses. Wetland and landscape features explained a significant amount of community richness. Wetland
hydroperiod, canopy cover and stream velocity were the variables most strongly related to odonate rich-
ness. Furthermore, we observed significant relationships between P. clarkii and the richness of odonate
communities, but the effect of the crayfish on the three odonate stages was different. Species richness
measured using both larvae and exuviae was negatively related to the crayfish presence, while negative
effects on adults were not evident. Furthermore, negative relationships were observed for Anisoptera
(dragonflies) but not for Zygoptera (damselflies). A significant effect of eigenvectors representing spa-
tial configuration suggests an important role of dispersal-related mechanisms in maintaining species
richness in invaded wetlands, where fitness is likely lower. Larvae and exuviae may be more helpful
for the assessment of the impact of invasive species at early stages of the invasions, while adults may
better describe the long term consequences of the invasion at the landscape scale. Considering multiple
life-history stages improves our understanding of the impact of biological invasions in freshwaters.
© 2014 Elsevier Ltd. All rights reserved.
1. Introduction
Many native ecosystems have been irretrievably modified by
invasive alien species (IAS), which determined the decline and the
∗
Corresponding author at: Laboratoire d’Ecologie Alpine (LECA), Univ. Grenoble
Alpes, LECA, F-38000 Grenoble, France. Tel.: +33 0476514496.
E-mail address: francesco.ficetola@gmail.com (G.F. Ficetola).
1
Permanent address.
extinction of native species, and fresh waters may be particularly
susceptible to the effects of invasions (Drake, 2009; Gherardi, 2007;
Strayer, 2010). IAS can damage native species through multiple
mechanisms, including competition, predation, spread of diseases
and hybridization (Pimentel, 2002). Prevention of new introduc-
tions is the optimal strategy to avoid the negative consequences
of IAS. However, if prevention fails, earlier management actions
have, at the same cost, the greatest effectiveness (Allendorf and
Lundquist, 2003; Leung et al., 2012), and management priority is
given to species showing the strongest negative impact (Jeschke
http://dx.doi.org/10.1016/j.ecolind.2014.05.036
1470-160X/© 2014 Elsevier Ltd. All rights reserved.