Download Effects of global climate change on freshwater biota: A review with

Italian Journal of Zoology, December 2010; 77(4): 374–383
REVIEW
TIZO
Effects of global climate change on freshwater biota: A review with
special emphasis on the Italian situation
S. FENOGLIO1*, T. BO1, M. CUCCO1, L. MERCALLI2, & G. MALACARNE1
Impacts of global climate change on freshwater biota
Dipartimento di Scienze dell’Ambiente e della Vita, Università del Piemonte Orientale, Alessandria, Italy, and 2Società
Meteorologica Italiana, Bussoleno, Torino, Italy
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1
(Received 6 February 2009; accepted 8 July 2009)
Abstract
There is much evidence that climate is rapidly changing at a global scale, especially regarding mean annual temperatures,
precipitations and evaporation. The consequences of this rapid environmental change on freshwater biota are still not clear,
but undoubtedly they could be severe. Among the main effects of climate change, we can individuate the enhancement of
water temperatures, particularly important for poikilothermic organisms, with the consequent diminution of dissolved
oxygen, and the reduction of available habitats for most stenothermal organisms. Another consequence of climate change is
the alteration of hydrologic cycles, with increasing intensity and frequency of extreme events such as droughts, especially in
Southern Europe. This scenario could severely affect freshwater biota, especially in mid-latitude regions, such as the Italian
peninsula: shifts in phenology, life cycles and distribution ranges are likely to be expected for many organisms, with the
extinction of many sensitive species. In particular, species adapted to perennial and cold waters are likely to suffer reductions in their distribution range and also local extinctions, while more tolerant organisms may enlarge their distribution ranges.
Global climate change may also promote and enhance invasions of alien species. In this work, concepts and hypotheses about the
presumable impacts of climate change upon freshwater biota are reported, with examples and predictions related to the
Italian situation.
Keywords: Climate change, global warming, freshwaters, biodiversity, Italy
Introduction
Observational records and projections provide an
increasing amount of evidence that at global scale
climate is rapidly changing (IPCC 2007). Although
the climate of our planet varies naturally in response
to differences in solar radiation, volcanic eruptions
and aerosol concentrations, our climate is also subject to forcing from anthropic pressures, such as the
emission of greenhouse gases and the alteration of
land cover (Mann et al. 1998). It is demonstrated
that mean global temperatures have risen during the
last century by about 0.7°C (IPCC 2007; Mann
et al. 2008). Further warming is predicted to continue for the next 100 years: in particular, the
Earth’s mean surface temperature is projected to
increase from 1.8 to 4.0°C by the end of the
twenty-first century (IPCC 2007). This observed
warming is coupled with changes in the hydrological
cycle at a large scale: for example, climate model
simulations predict in the future a precipitation
increase in high latitudes and part of the tropics
and a decrease in sub-tropical and mid-latitude
regions (from 10°S to 30°N). Furthermore, many
areas will be subjected to the increase of drought
and flooding events.
This rapid climate change is projected to affect
the biodiversity of large regions dramatically, with
changes in the presence and distribution of many
species, the decrease of the taxonomic richness, and
*Correspondence: S. Fenoglio, Dipartimento di Scienze dell’Ambiente e della Vita, Università del Piemonte Orientale, Via T. Michel 11, I-15121 Alessandria,
Italy. Tel: +39 0131 360201. Fax: +39 0131 360243. Email: [email protected]
ISSN 1125-0003 print/ISSN 1748-5851 online © 2010 Unione Zoologica Italiana
DOI: 10.1080/11250000903176497
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Impacts of global climate change on freshwater biota
the disappearance of entire ecosystems (Svenning
et al. 2009). There is much evidence that global
warming is already threatening the biological diversity
of our planet (Kühn et al. 2008): for example, recent
studies have found correspondences between temperature increase and changes in the fish community
of the Atlantic Ocean (Quero 1998), Australian and
Caribbean coral reefs senescence and death
(Munday et al. 2008), changes in the life cycles of
some insects (Gomi et al. 2007; Balletto et al.
2008). Extinction risk has grown for many species,
and almost one case of extinction, the disappearance
of the Costa Rican Golden Toad (Bufo periglenes
Savage, 1967) has been associated with climate
change (Pounds et al. 1999).
In this scenario, freshwater ecosystems are particularly vulnerable and freshwater biota could experience
dramatic impacts. Some recent studies underlined
that freshwater biodiversity has declined faster than
either marine or terrestrial ones over the past three
decades (Jenkins 2003). For this reason, there is
increasing attention on the possible influences of climate change upon inland water systems and biota
(Figure 1). The purpose of this review is to provide
information about different aspects of the potential
effects of climate change upon freshwater biota, with
particular reference to the Italian situation.
375
Impacts of global climate change on
freshwater biota
It is well known that inland water conditions are intimately coupled with weather and atmospheric temperature variations, so that climate change may have
strong direct and indirect effects on freshwater biota
(Bates et al. 2008). Among the direct effects we can
consider the raising of inland water temperatures, the
disruption of hydrologic cycles, the alteration of rainfall and snow cover in different regions, and the
increase of extreme precipitation events. In parallel,
the general alteration of climate conditions could lead
to some indirect effects, such as landscape transformation, increase in river morphology alteration, enhancement of agricultural irrigation needs, increase in the
construction of dams with the consequent river fragmentation, worsening water quality, and invasion of
allochthonous species (Figure 2). In this review, we
will focus on some of the main effects of climate
change, such as temperature increase, hydrologic
cycles change and invasions of exotic species, reporting
some of the most important cases of study in Table I.
Temperature increase
Stream temperature is strictly dependent on air temperature, but is also influenced by some other factors,
Figure 1. Number of papers related to Global warming and Biodiversity/Freshwater (©ISI Web of Science).
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376
S. Fenoglio et al.
Figure 2. Direct and indirect effects of climate change on freshwater biota.
such as shading from riparian vegetation, watershed
storage in wetlands, land cover, and groundwater
connections (Mohseni et al. 1999). Water temperature has important effects on freshwater organism
life, both directly and indirectly (for example,
because the solubility of oxygen in water decreases
as temperature increases). Most freshwater animals
are poikilothermic, with an internal temperature that
varies with that of their surroundings: thus, water
temperature influences their main physiological
processes and metabolic activity, and has a strong
effect on the survival, longevity and reproductive
success of freshwater animals (Giller & Malmqvist
1998). In particular, growth of aquatic organisms is
often temperature-dependent, since higher temperatures are known to enhance feeding activity and
digestion rate (Allan 1995). For example, recent
studies in North Italian rivers revealed that populations of the mayflies Oligoneuriella rhenana (Imhoff,
1852) (Ephemeroptera: Oligoneuriidae) and Pothamantus luteus (Linnaeus, 1767) (Ephemeroptera:
Pothamantidae) have a faster development in
warmer environments (Fenoglio et al. 2005, 2008).
Moreover, Erba et al. (2003) recently demonstrated
that thermal characteristics seem to be the major
factor responsible for the observed differences in life
cycle patterns of different species of Baetidae
(Ephemeroptera) in the Italian Alps. We can
hypothesize that, with the projected increase of
water temperatures, the life cycles and phenology of
many aquatic organisms will change, with shifts in
ontogeny and breeding time, decrease of mean body
size, the alteration of sex ratios, and the reduction of
fecundity (Hogg & Williams 1996).
Furthermore, some aquatic organisms in inland
waters are stenothermal, occupying narrow temperature ranges. In lotic environments, the longitudinal
distribution of the species is strictly related to water
temperature, with some groups (such as Salmonidae
among vertebrates and Blephariceridae among
invertebrates) having low lethal thermal thresholds
(about 24–28°C for Brown Trout; Elliott 1994).
Climatic warming has been correlated with poleward and upward distributional shifts of terrestrial
animals (Levinsky et al. 2007), but evidence from
lotic systems is very scarce at the moment. For
example, analysing the Perlid stonefly (Plecoptera)
populations of 35 sites in the Rocky Mountains,
Sheldon (2007) reported that median elevations of
some species, such as Acroneuria abnormis (Newman,
1838) and Eccoptura xanthenes (Newman, 1838),
shifted uphill ∼65 m in the last three decades. It is to
be expected that, with the progressive thermal
increase, the area occupied by many species may
Impacts of global climate change on freshwater biota
377
Table I. Effects of global change on some freshwater organisms.
Taxon
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Mollusca
Dreissena polymorpha (Pallas, 1771)
Pisidium amnicum (Müller, 1774)
Pisidium casertanum (Poli, 1791)
Pisidium henslowanum (Sheppard, 1823)
Pisidium moitessierianum (Paladilhe, 1866)
Pisidium nitidum Jenyns, 1832
Pisidium subtruncatum Malm, 1855
Crustacea
Thermocyclops oithonoide (Sars 1863)
Hesperodiaptomus arcticus (Marsh, 1920)
Eudiaptomus intermedius (Steuer, 1897)
Insecta
Gomphus vulgatissimus (L.)
Chloroperla sp.
Protonemura sp.
Nemoura sp.
Ecdyonurus sp.
Serratella ignita (Poda 1761)
Dinocras cephalotes (Curtis, 1827)
Cloeon dipterum L.
Vertebrata
Salmo trutta fario (Linnaeus 1758)
Cottus gobio Linnaeus, 1758
Lampetra planeri (Bloch 1784)
Gobio gobio (Goc)
Leuciscus cephalus (Lec)
Effect of
global
change
Reference
+
−
−
−
−
−
−
Population increasea
Population collapsea
Population collapsea
Population collapsea
Population collapsea
Population collapsea
Population collapsea
+
Change in phenology and abundance
increaseb
Population reductionc
Modification of life history strategiesd
−
−
−
−
−
−
−
+
−
Change in phenology and emergencee
Habitat reductionf
Habitat reductionf
Habitat reductionf
Habitat reductionf
Habitat expansiong
Habitat reductionf
No direct, immediate effectsi
−
−
−
+
+
Habitat reductionl,m
Habitat reductionl
Habitat reductionl
Habitat expansionl
Habitat expansionl
a, Mouthon & Daufresne 2006; b, Adrian et al. 2006; c, Holzapfel & Vinebrooke 2005; d, Primicerio
et al. 2007; e, Richter et al. 2008; f, Daufresne et al. 2003; g, López−Rodríguez et al. 2009; h,
Fenoglio et al. 2007a; i, McKee & Atkinson 2000; l, Buisson et al. 2008; m, Hari et al. 2006.
restrict or even disappear: in fact, while terrestrial or
marine migratory species can respond rapidly to
yearly climate variation by altering the timing or destination of migration (Parmesan et al. 1999), most
freshwater animals are sedentary and live in confined environments, and are therefore incapable of
rapid responses to environmental variations. In this
context, for example, fish distribution may be dramatically altered by climate warming, because these
organisms have no physiological ability to regulate
their body temperature and their dispersal ability is
constrained by the network structure of drainage
basins (Grant et al. 2007). In a recent study, Buisson et al. (2008) hypothesized that stream fish
assemblages will change in the future throughout
Europe, with warm-water species, such as Barbus
meridionalis Risso, 1826, Gobio gobio (Linnaeus,
1758) and Leuciscus cephalus (Linnaeus, 1758), possibly experiencing an increase in their distribution,
while cold-water ones, such as Salmo trutta fario (Linnaeus, 1758) and Cottus gobio (Linnaeus, 1758), are
expected to lose many previously suitable habitats. It
is likely that, in the future, these impacts could be
enhanced because of the increase of water withdrawal. Furthermore, this situation could be worsened in Italy by the high presence of dams and
barriers that disrupt the longitudinal connectivity of
lotic systems, inhibiting fish migration (Fiorese et al.
2005). In a recent paper, Xenopoulos et al. (2005)
predicted a model of freshwater fish extinction on
the basis of two scenarios (A2 and B2) of climate
change provided by the International Panel of Climate Change (IPCC 2001). Both scenarios predicted an evident reduction in the fish species
richness in two Italian lotic environments. In the Po
River, the most severe scenario (A2) could determine a loss of fish species ranging from 7 to 13%,
while the other (B2) could range from 3 to 6%. In
the Ombrone River, the expected losses would be
more impressive, with the extinction of 10–15%
(A2) or 5% (B2) of the total fish species number in
the future.
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378
S. Fenoglio et al.
Evident changes are also expected in lentic environments, because most mountain lakes, for
example, are characterized by long periods of cold
water and low primary and secondary production.
The thermal increase will result in stronger thermal
stratification, enhanced nutrient resuspension, and
increased lake production (Rouse et al. 1997); consequently, the productivity of the system will move
from benthic to pelagic compartments and the taxonomic composition could be strongly altered
(Primicerio et al. 2007). Finally, water temperature
increases may have unexpected consequences,
because different taxa show different responses to
warming. Winder and Schindler (2004) noticed that
the long-term decline in Daphnia populations in a
large temperate lake was coupled with the disruption
of trophic linkages: because of temperature rise,
phytoplankton bloom advanced by almost a month
in the study period, creating a temporal mismatch
with the presence of zooplankton consumers.
Hydrologic cycle change
One of the most significant consequences resulting
from climate change may be the alteration of
regional hydrologic cycles and subsequent changes
in stream flow regimes (Trenberth 1999; Huntington 2006). It is well known that climate is the most
important element influencing the quantity and timing of river flow which are essential elements for the
biota of river systems (Poff et al. 1997). In recent
years, precipitation and hydrologic regimes have
been changing on a large scale (Mauget 2003);
because of global warming, snowmelt and ice cover
are expected to reduce considerably, while atmospheric water vapour and precipitation are expected
to increase globally. Much of this precipitation
increase may be localized in some regions, such as
high latitudes of the Northern Hemisphere, African
tropics, Southern and Eastern Asia (Nijssen et al.
2001), while other areas, such as the Mediterranean
basin, may become drier (Palmer & Räisänen 2002).
In addition, there is much evidence that future
regimes will be characterized by the enhancement of
frequency and intensity of ‘extreme’ events (Folland
et al. 2001). In particular, climatic scenarios predict
more frequent and extended droughts, especially in
mid latitudes (Boulton & Lake 2008), and so a progressive shift from permanent to temporary water
bodies may occur. In this context, the Deutscher
Verband für Wasserwirtschaft and Kulturbau
(DVWK 1998) provided evidence that droughts
have increased in frequency, duration and severity
over the last few decades throughout Europe, probably in relation to two phenomena: the alteration of
seasonal meteorological conditions and the increase
of artificial influences in catchments (Hisdal et al.
2001). Furthermore, Zanchettin et al. (2008), analysing a 200-year time series of discharges of the Po
River, observed an increase in both peak flow and
low discharge events, with an evident sharpening of
extremes in recent decades (particularly prolonged
drought periods). This hydrologic change is
expected to strongly affect the freshwater biota. The
impact of droughts on aquatic biota can be direct,
due to decreased water level, disruption of the
hydrological connectivity, and habitat reduction
(Stanley et al. 1994), or indirect, due to increase of
competition and predation, and change in the nature
of food resources (Miller & Golladay 1996). Considering flow conditions, we can differentiate between
temporary streams, in which flow occurs either seasonally (intermittent streams) or in response to
irregular rain (episodic streams), and permanent
streams with perennial flow (Hose et al. 2005).
Temporary streams, characterized by a natural dry
period (Williams 1996), can be found in coastal and
Southern regions of Italy with Mediterranean-type
climates, while Apenninic and Northern Italian lotic
environments are considered perennial (Gasith &
Resh 1999). The freshwater biota of intermittent
environments show adaptations and strategies to
survive dry periods (e.g. desiccation-resistant stages
or colonization of hyporheic environment; Boulton
& Lake 1992), but less is known about the biological
impact of droughts in perennial rivers. In a recent
experiment, Fenoglio et al. (2007a) analysed the
impact of the duration of drought periods on macroinvertebrate assemblages in the upper Po River, a
lotic system in which droughts are a recent and
human-induced phenomenon. Macroinvertebrate
samplings were performed in four reaches of the Po
River, characterized by different periods of absence
of surface water, and sub-substratum traps were also
placed to assess hyporheic colonization during dry
periods. The abundance of macroinvertebrates and
taxonomic richness were found to be inversely
related to the length of the dry period, and functional organization of the benthic community was
also affected by the lack of flow permanence. Moreover, areas with a discontinuous presence of water
were mainly colonized by small, fast-growing,
plurivoltine organisms. The sub-substratum traps
showed a low taxa richness, demonstrating that only
few taxa could survive drought periods by colonizing
interstitial and hyporheic habitats (Fenoglio et al.
2006). This study demonstrated that in naturally
perennial prealpine rivers, the recent increase in
droughts will likely cause a general depletion of biological diversity. Finally, we must consider that this
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Impacts of global climate change on freshwater biota
predicted hydrological transformation is not likely to
affect all organisms in the same way. In a recent
study on the life history of Serratella ignita (Poda,
1761) (Ephemeroptera: Ephemerellidae) in two
Mediterranean streams, one permanent and one seasonal, López-Rodríguez et al. (2009) discovered a
great plasticity in the life cycle, secondary production and feeding behaviour of this mayfly. Thanks to
this ecological flexibility, S. ignita shows a high
fitness in both perennial and intermittent habitats;
therefore, this study supports the hypothesis that
such species will cope with the presumable future
global climate change scenario maintaining, or even
increasing, their populations at the expense of more
stenoecic species.
Considering the other hydrological extreme,
floods are usually predictable events, occurring in
the same season year after year, for example following snowmelt in Alpine regions. There is evidence
that these phenomena are also likely to increase in
frequency and strength, because of the increasing
number of precipitation events belonging to the
highest intensity class (Brunetti et al. 2004). Severe
floods can represent ‘pulse disturbances’ (sensu Lake
2000), affecting aquatic organisms by a combination
of increased water velocity, habitat alteration, and
physical scouring (Suren & Jowett 2006). Generally,
river communities react to floods with a reduction in
density and taxonomic richness (e.g. in Piemonte
after the catastrophic 1994 and 2000 floods;
Fenoglio et al. 2003) and evident shifts in community composition, mainly because floods can
affect differently taxa characterized by different morphological and ecological characteristics. For
example, Hendricks et al. (1995) reported that an
important flood event can halve the density of three
Hydropsyche species (Trichoptera: Hydropsychidae),
with no apparent effects on the abundance of
Ephoron leucon Williamson, 1802 (Ephemeroptera:
Polymitarcidae).
Allochthonous species invasion
There is ample evidence that climatic warming influences the distribution of organisms (Southward et
al. 1995; Sagarin et al. 1999; Stachowicz et al.
2002), and many studies assume the existence of a
direct relationship between climate change and biological invasions (Dukes & Mooney 1999; Thomas
& Lennon 1999). Global warming enables some
species to expand their distribution, moving poleward and upward; in particular, climate change
leads to the survival and dispersal of tropical and
sub-tropical species, mainly those able to modify
their seasonal cycles (Turchetto & Vanin 2004).
379
Furthermore, global climate change disrupts community structure and increases native species loss
and extinction. Recent studies evidenced that many
invasive species share traits that allow them to
capitalize on the various elements of global change;
for example, invasive species are more likely to be
generalists than specialists, and thus might be more
able to adapt to new climates (Dukes & Mooney
1999). Biological invasions are among the main
causes of biodiversity loss, and currently represent
the second cause of animal extinctions (Millennium
Ecosystem Assessment 2005). In fact, long-distance
human-mediated dispersal of organisms has, in
recent times, allowed an impressive change in local
faunas throughout the world (Corriero et al. 2007).
There are many examples of successful invasions in
inland waters, mostly because in freshwater environments many human activities, such as sport and
commercial fishing, aquaculture practices, pet trade,
and fur farming, have lead to allochthonous species
import. Furthermore, eradication of aliens can be
very difficult. Recently, Gherardi et al. (2007)
published a list of alien animal species that are nowadays present in Italian inland waters. A total of 112
non-indigenous species (64 invertebrates and 48
vertebrates) was found, contributing about 2% of
the freshwater fauna in Italy. Among vertebrates, the
fish fauna of the Italian peninsula is characterized by
the presence of 29 alien species, which mostly
arrived through direct import, such as the Pumpkinseed Lepomis gibbosus (Linnaeus, 1758) first
introduced in the Varano Lake in 1900, and the
Wels Catfish (Silurus glanis Linnaeus, 1758) which
appeared in 1957 and that in recent years experienced
a noticeable increase in distribution (Zerunian 2002).
Among invertebrates, alien species can be found in
many taxonomic groups, such as Crustacea Copepoda
(Ferrari & Rossetti 2006), Gastropoda Prosobranchia
(Modena & Turin 1991) and Hirudinea (Genoni &
Fazzone 2008). Two impressive examples of successful aquatic invaders in Italian freshwaters are represented by the Zebra mussel and the Red swamp
crayfish. Native of Caspian Sea region, the Zebra
mussel Dreissena polymorpha (Pallas, 1771) has progressively invaded many freshwater ecosystems in
Europe and North America, because of the high
fecundity, high mobility and dispersal rates of its
veligers and postveligers, the adults’ adherence on
boats and other objects, and high adaptability to colonize almost any solid substratum (Lancioni & Gaino
2006; Casagrandi et al. 2007). The crayfish Procambarus clarki Girard, 1859 native of the southeastern
US, nowadays dominates many waterbodies of southern Europe, including Italy (Delmastro 1999; Fea
et al. 2006; Gherardi 2006).
380
S. Fenoglio et al.
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Italian Alpine and Mediterranean areas
There is no doubt that Italy’s climate is changing
rapidly (Figure 3). Recent studies confirmed a temperature increase of about 1°C per century in the
last 150 years, with an increase generally higher for
minimum temperatures than for maximum ones
(Brunetti et al. 2006; Bartolini et al. 2008). Furthermore, analysing 45 daily precipitation series covering quite uniformly the Italian territory for the
period 1880–2002, Brunetti et al. (2004) evidenced
that the number of wet days per year has a clear and
highly significant negative trend all over the peninsula, but, besides this reduction, there is a tendency
toward an increase in the intensity of precipitation.
Unfortunately, evaluations of possible impacts of
recent climate change on Italian inland water fauna
must rely on scarce and indirect evidences. Nevertheless, we can hypothesize that in the future climate
change could affect Italian inland fauna, especially
in some areas such as the Alps, Southern regions,
Sardinia and Sicily.
Alpine aquatic environments are considered especially sensitive to climate change, as warming events
reduce snowpack and ice cover. In this context,
Alpine lakes and ponds could suffer because of
decreased albedo and increased heat absorption
(Strecker et al. 2004), with, as a consequence, the
enhancement of water temperature. Primicerio et al.
(2007) predicted that climate change may represent
a major driver of future biodiversity loss in Alpine
lentic habitats, because these environments are
mostly inhabited by cold stenothermal organisms.
The foreseen global warming may enhance extinction
rates of native species, because of cold water habitat
reduction, dissolved oxygen depletion, changes in the
ecological functioning, and introduction of allochthonous invaders (Holzapfel & Vinebrooke 2005).
Considering that many Alpine organisms are relictual endemisms, and that most of them are zooplanktonic, lacking aerial life stages and with scarce or no
possibilities to migrate, we can predict a severe
biodiversity loss in lentic Alpine fauna in the future.
Also, the fauna of Alpine lotic systems may be
strongly altered by the direct and indirect effects of
global warming: headwaters, and especially glacial
streams, are highly sensitive to climate changes that
may lead to important thermal and hydrological
modifications (McGregor et al. 1995). Alpine stream
faunal communities are mostly composed of coldwater
stenotherm
organisms,
such
as
Plecoptera,
Ephemeroptera, Trichoptera and some specialized
Diptera (Maiolini & Lencioni 2001): some organisms, such as Dyctiogenus fontium (Riss, 1896)
(Plecoptera: Perlodidae), which are orophilous
species endemic to the Alps with a discontinuous
and fragmented distribution (Fenoglio et al. 2007b),
may promptly reduce their distribution or even disappear.
Another subject of great interest is represented by
Mediterranean climate regions (particularly Sardinia,
Sicily and Southern Italy). It is well known that inland
waters in these environments are physically, chemically, and biologically shaped by predictable and
seasonal events of flooding and drying over an
annual cycle (Gasith & Resh 1999). Simulations
predict that the frequency of summers as hot as that
of 2003 will progressively increase to become the
norm in the second half of the twenty-first century
(Schär et al. 2004). In this context, the predicted
increase of warm and dry periods, and the related
water withdrawal for agricultural uses, may lead to
the general alteration of hydrologic regimes, and to
the disappearance of many temporary freshwater
systems and their fauna.
Acknowledgements
We thank R. Bolpagni, M.J. Lopez-Rodriguez,
G. Rossetti, and J.M. Tierno de Figueroa for useful
suggestions.
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