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Changes in the range of dragon ies in the Netherlands and the possible role... 155
Changes in the range of dragonflies in the Netherlands
and the possible role of temperature change
Tim Termaat1, Vincent J. Kalkman2, Jaap H. Bouwman3
1 Dutch Butter y Conservation, De Vlinderstichting, P.O. Box 506, 6700 AM Wageningen, e Netherlands
2 European Invertebrate Survey – e Netherlands, National Museum of Natural History Naturalis, P.O. Box
9517, 2300 RA Leiden, e Netherlands 3 Groene Weide 62, 6833 BE Arnhem, e Netherlands
Corresponding author: Tim Termaat (tim.termaat@vlinderstichting.nl)
Academic editor: Jürgen Ott|Received5 August 2010|Accepted 15 September 2010|Published 30 December2010
Citation: Termaat T, Kalkman VJ, Bouwman JH (2010) Changes in the range of dragon ies in the Netherlands and the
possible role of temperature change. In: Ott J (Ed) (2010) Monitoring Climatic Change With Dragon ies. BioRisk 5:
155–173. doi: 10.3897/biorisk.5.847
Abstract
e trends of 60 Dutch dragon y species were calculated for three di erent periods (1980–1993, 1994–
1998 and 1999–2003). Comparing period 1 and period 3 shows that 39 of these species have increased,
16 have remained stable and 5 have decreased. ese results show a revival of the Dutch dragon y fauna,
after decades of ongoing decline. e species were categorized in di erent species groups: species with a
southern distribution range, species with a northern distribution range, species of running waters, species
of fenlands and species of mesotrophic lakes and bogs. e trends of these di erent species groups were
compared with the all-species control group. As expected, a signi cantly higher proportion of the south-
ern species show a positive trend than the all-species group. In the northern species group on the contrary,
a signi cantly higher proportion of the species show a negative trend than the all-species group. Di erent
explanations for these results are discussed, such as climate change, improved quality of certain habitats
and degradation of other habitats. It is likely that the observed increase of southern species is at least partly
caused by the increasing temperatures. e less positive picture of the northern species group is probably
more in uenced by other environmental factor than directly by climate change.
ree out of six southern species which have become established since 1990 have done so during the
aftermath of large invasions. It is concluded that dragon ies are well capable of using changing climate
circumstances to colonise new habitats.
Keywords
dragon ies, Odonata, climate change, invasion, trends, conservation, Netherlands
BioRisk 5: 155–173 (2010)
doi: 10.3897/biorisk.847
http://biorisk-journal.com/
Copyright T. Termaat, V.J. Kalkman, J.H. Bouwman. This is an open access article distributed under the terms of the Creative Commons Attribution
License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
RESEARCH ARTICLE
BioRisk
A peer-reviewed open-access journal
Tim Termaat, Vincent J. Kalkman & Jaap H. Bouwman / BioRisk 5: 155–173 (2010)
156
Introduction
During the last century, the Dutch dragon y fauna has shown large changes. De-
struction of habitats, canalisation of streams and rivers, desiccation, eutrophication,
acidi cation and pollution led to an often strong decline of many species. is started
in the rst half of the 20th century, but was especially severe in the sixties and seventies
of that century (Kalkman et al. 2002). Most a ected were species of running waters
and species of mesotrophic lakes and bogs (Wasscher 1994, 1999), some of which
even disappeared from the Netherlands (Coenagrion mercuriale, Nehalennia speciosa,
Gomphus avipes, Ophiogomphus cecilia, Oxygastra curtisii, Leucorrhinia caudalis). e
degradation of the Dutch dragon y fauna reached a maximum in the 1980’s. Since
the start of the 1990’s, many species have increased. is is very obvious for some
species of running water and ubiquistic species for which the Netherlands lie on the
northern limit of their distribution range. ese species seem to have pro ted from
the improving water quality (RIVM 2003) and the recent warm summer seasons
(KNMI 2006). However, a number of species of other habitats, such as mesotrophic
lakes and bogs, have also increased during last decade.
In this article we describe the revival of the Dutch dragon y fauna, which seems to
be happening. Special attention is given to the role of temperature change.
Methods
Database
e database used for this article is build and maintained by the Dutch Society for
Dragon ies, Butter y Conservation and the European Invertebrate Survey – the
Netherlands. It contains over 307,000 records of 71 dragon y species up to and in-
cluding 2003, mainly submitted by volunteers. Each record constitutes a species on
a date on a locality. e records are checked for mistakes by a committee of experts,
based on the known distribution and ight period of the species. For records of rare
species further documentation like a picture or a description is required.
More than 279,000 records are available from the period 1980–2003. By far the
largest number of these records was collected from 1994 onwards, but the number of
records prior to this period is large enough to give a good impression of the distribu-
tion of the species in that period.
e database gives good information on the distribution of species. However it is
subject to in uences of the di erences between eldwork done by the volunteers and
large-scale professional projects. erefore, results based on the database can only be
interpreted correctly with a good knowledge of the database itself.
Changes in the range of dragon ies in the Netherlands and the possible role... 157
Calculation of trends
e data set was divided in three periods: 1980–1993 (period 1), 1994–1998 (period
2) and 1999–2003 (period 3). Relatively few records are available from each year in
period 1. erefore, this period includes fourteen years while periods 2 and 3 only
include ve years. e 5×5 kilometre squares which had been visited at least in three
di erent months in the period May till August were selected for each year (table 1).
Only records from these squares were used for the analysis. For eleven of the 71 Dutch
species this resulted in usable records for only one or none of the three periods. ere-
fore these species, all extinct or very rare, were not included in the trend calculation.
Presence or absence of dragon y species in the selected 5×5 kilometre squares was
used, instead of the recorded number of individuals, as the latter is more prone to di er-
ences in recording behaviour. e consequence of this method is that a decrease or increase
in observed numbers or in localities within a 5×5 kilometre square will go unnoticed.
For each species and period the relative abundance (RA) was calculated as follows:
RA= (Number of squares in which a species is recorded)/(number of investi-
gated squares) × 100%.
e RA’s for each year were summed for each period and divided by the number of
years. e relative change of a species was calculated as follows:
Trend= (RA in recent period – RA in historical period)/(RA historical period
× 100%
e trends were divided in ve trend categories (table 2).
Southern and northern species group
e Dutch dragon y species were categorized as southern species, northern species or
species without a typical southern or northern distribution pattern. is categorization
was based on distribution maps of Northwest Europe (NVL, 2002). A southern spe-
cies was de ned as a species of which the northern limit of its range runs through the
southern tip of Sweden or more southwards. A northern species was de ned as a species
of which the southern border of its range runs through the Netherlands or Belgium and
which is further south only found at higher elevations or in small, scattered populations.
Habitat groups
Next to the southern and northern species groups, three ecological species groups were se-
lected: species of running water habitats (rheophilic species), species of mesotrophic lakes
Tim Termaat, Vincent J. Kalkman & Jaap H. Bouwman / BioRisk 5: 155–173 (2010)
158
and bogs and species of fenlands. For this categorization the habitat preference of Dutch
dragon ies was used, as given in NVL (2002). Table 3 lists the species of the four selected
species groups. Note that some species are appointed to more than one species group.
Statistics
χ2-tests were conducted to test the di erences between the all-species group and the se-
lected distribution and habitat species groups. is was done by using Microsoft Excel
2000 software. Species with increasing (>20 %) and strong increasing trends (>100 %)
were lumped together and tested as increasing species.
Results
e relative abundance for each period and the trend between the periods is given for
each species in table 4. Table 2 gives the number of species showing a certain trend
between the di erent periods.
Period 1 Period 2 Period 3
Year Well investigated
squares Year Well investigated
squares Year Well investigated
squares
1980 5 1994 151 1999 235
1981 9 1995 260 2000 235
1982 16 1996 242 2001 241
1983 12 1997 205 2002 260
1984 11 1998 180 2003 372
1985 14 Total 1038 Total 1343
1986 19
1987 20
1988 14
1989 20
1990 28
1991 23
1992 45
1993 68
1994 151
1995 260
1996 242
1997 205
1998 180
Total 1342
Table 1. e number of well investigated 5×5 kilometre squares
Changes in the range of dragon ies in the Netherlands and the possible role... 159
Trend In table 4 as period 1 to 2 period 2 to 3 period 1 to 3
Strong increase >100% ++ 19 (32%) 6 (10%) 13 (25%)
Increase >20% and <100% + 9 (15%) 19 (32%) 14 (25%)
Stable -20% to 20% 0 19 (32%) 28 (47%) 16 (31%)
Decrease <-20% - 13 (22%) 7 (12%) 9 (17%)
Table 2. Categories of trend and the number of species showing this trend between periods
Trends between the rst and the third period could be calculated for 60 species. 39
species (65%) show a positive trend, 16 species (27%) remained stable and 5 species
(8%) show a negative trend. Most increasing species show the strongest positive trend
between the rst and second period (see gure 1).
e results of the χ2-tests are given in table 5.
Species with a southern distribution pattern
Within the southern species group, signi cantly more species show a positive trend
than the all-species group, when period 1 is compared to period 2 and when period 1
is compared to period 3. Furthermore, a signi cantly lower proportion of the southern
species remained stable, when period 1 is compared to period 3 ( gure 2).
Species with a northern distribution
Within the northern species group, signi cantly more species show a negative trend
than the all-species group, when period 1 is compared to period 2. Furthermore, a
signi cantly lower proportion of the northern species remained stable, when period 2
is compared tot period 3 ( gure 3).
Di erences in trends between habitats
Within the species group of mesotrophic lakes and bogs, signi cantly less species show
a positive trend than the all species group and signi cantly more species show a stable
trend, when period 1 is compared to period 3 ( gure 4).
Within the ecological species groups of running waters and fenlands, no signi cant
di erences are found for the three trend categories.
Discussion
e results show that the Dutch dragon y fauna has recovered since the start of the
1990’s, which is in sharp contrast with some other groups of invertebrates as but-
Tim Termaat, Vincent J. Kalkman & Jaap H. Bouwman / BioRisk 5: 155–173 (2010)
160
Species Southern Northern Running
waters Lakes and
bogs Fenlands
Aeshna a nis x
Aeshna grandis xx
Aeshna isoceles xx
Aeshna juncea x
Aeshna mixta x
Aeshna subarctica xx
Aeshna viridis xx
Anax imperator x
Anax parthenope x
Brachytron pratense x
Calopteryx splendens x
Calopteryx virgo x
Ceriagrion tenellum xx
Coenagrion hastulatum xx
Coenagrion lunulatum xx
Coenagrion puella x
Coenagrion pulchellum x
Cordulegaster boltonii x
Cordulia aenea xx
Crocothemis erythraea x
Enallagma cyathigerum x
Erythromma lindenii x
Erythromma najas x
Erythromma viridulum xx
Gomphus avipes x
Gomphus pulchellus x
Gomphus vulgatissimus x
Ischnura elegans x
Ischnura pumilio x
Lestes barbarus xx
Lestes dryas x
Lestes sponsa xx
Lestes virens x
Lestes viridis xx
Leucorrhinia dubia x
Leucorrhinia pectoralis x
Leucorrhinia rubicunda xx
Libellula fulva xx
Libellula quadrimaculata xx
Ophiogomphus cecilia x
Orthetrum brunneum xx
Orthetrum cancellatum xxx
Orthetrum coerulescens x
Table 3. Categorisation of the species in ve di erent species groups.
Changes in the range of dragon ies in the Netherlands and the possible role... 161
Species Southern Northern Running
waters Lakes and
bogs Fenlands
Platycnemis pennipes x
Pyrrhosoma nymphula x
Somatochlora arctica xx
Somatochlora avomaculata x
Sympecma fusca xx
Sympecma paedisca xx
Sympetrum danae x
Sympetrum aveolum x
Sympetrum fonscolombii x
Sympetrum pedemontanum x
Sympetrum sanguineum x
Sympetrum vulgatum xx
ter ies and bees (Peeters and Reemer 2003; Swaay and Groenendijk 2005). Only 5
dragon y species have declined, while a majority of 39 species has increased and 16
species remained stable. Out of the 27 species placed on the red list in 1999 (Wasscher
1999) 17 show an increase, 4 a decrease, 1 remained stable and 3 are still extinct. For
the remaining 2 red-listed species (Coenagrion armatum and Leucorrhinia albifrons)
no trend was calculated, as they were only recorded in one period. Populations of
both species have recently been rediscovered (Van der Heijden 2001; De Boer and
Wasscher 2006) in the Netherlands and although they are extremely rare, there is no
evidence for an actual decline.
Two di erent causes can be pointed out for the increase or decrease of the di er-
ent species. e rst is climate change, the second is changes in the quality of habitats.
Climate change
e average temperature in the Netherlands in the last twenty years of the 20th
century was 0,7 degree higher than the average temperature of the rst twenty years
of the 20th century (KNMI 2006). Especially the spring temperature has shown
a strong increase. is increase in temperature caused several southern species to
expand their range northwards, becoming more common in the Netherlands. is
is at least the case for Lestes barbarus, Aeshna a nis, Anax parthenope, Crocothemis
erytraea, Orthetrum brunneum and Sympetrum fonscolombii. Coenagrion scitulum ex-
panded its range in northern France and Belgium and was rst found in the Neth-
erlands in 2003 (Goudsmits 2003). Also for more common southern species like
Lestes virens and Ceriagrion tenellum a positive e ect of increasing temperatures is
expected.
Whether or not higher temperatures also play a role in the negative trend shown
by some northern species is di cult to say, because the habitats of northern species are
Tim Termaat, Vincent J. Kalkman & Jaap H. Bouwman / BioRisk 5: 155–173 (2010)
162
Species RA
period
1
RA
period
2
RA
period
3
trend
1st to
2nd
period
trend
2nd
to 3rd
period
trend
1st to
3rd
period
Aeshna a nis Vander Linden, 1820 1 0,6 ++ - ++
Aeshna cyanea (O.F. Müller, 1764) 33,6 47,1 53,6 0 0 +
Aeshna grandis (Linnaeus, 1758) 36,3 36,3 40,9 0 0 0
Aeshna isoceles (O.F. Müller, 1767) 7,5 12,3 17,2 + + ++
Aeshna juncea (Linnaeus, 1758) 18,1 13,5 13,4 0 0 0
Aeshna mixta Latreille, 1805 21,9 54,9 61,9 + 0 ++
Aeshna subarctica Walker, 1908 0,4 0,9 0,5 ++ - +
Aeshna viridis (Eversmann, 1836) 1 4,2 6,4 ++ 0 ++
Anax imperator Leach, 1815 23,5 59,5 73,2 + 0 ++
Anax parthenope (Selys, 1839) 0,3 0,4 ++ + ++
Brachytron pratense (O.F. Müller, 1764) 17,8 20,3 30,3 0 + +
Calopteryx splendens (Harris, 1782) 33 32 32,4 0 0 0
Calopteryx virgo (Linnaeus, 1758) 5,2 3,2 3,1 - 0 -
Ceriagrion tenellum (de Villers, 1789) 11,9 8 13,8 - + +
Coenagrion armatum (Charpentier, 1840) 0,3
Coenagrion hastulatum (Charpentier, 1825) 4,3 1,9 2,4 - + -
Coenagrion lunulatum (Charpentier, 1840) 19,3 8,3 9,5 - + -
Coenagrion puella (Linnaeus, 1758) 54,9 57,7 62,2 0 0 0
Coenagrion pulchellum (Vander Linden, 1825) 50,8 48,5 49,8 0 0 0
Coenagrion scitulum (Rambur, 1842) 0,1
Cordulegaster boltonii (Donovan, 1807) 2 1,1 0,9 - - -
Cordulia aenea (Linnaeus, 1758) 28,8 22,7 24,7 0 0 0
Crocothemis erythraea (Brullé, 1832) 1,7 3,6 ++ ++ ++
Enallagma cyathigerum (Charpentier, 1840) 63,7 59,6 64,1 0 0 0
Erythromma lindenii (Selys, 1840) 2,8 2,7 4,6 + + ++
Erythromma najas (Hansemann, 1823) 28,3 44,3 42 + 0 +
Erythromma viridulum (Charpentier, 1840) 7,1 42,3 36,5 ++ 0 ++
Gomphus avipes (Charpentier, 1825) 2,8 ++ ++ ++
Gomphus pulchellus Selys, 1840 10 8,7 8,2 0 0 +
Gomphus vulgatissimus (Linnaeus, 1758) 2 2,1 3,9 ++ + ++
Hemianax ephippiger (Burmeister, 1839) 0,2
Ischnura elegans (Vander Linden, 1820) 79,3 93 90,5 0 0 0
Ischnura pumilio (Charpentier, 1825) 6,2 4,9 9,1 0 ++ ++
Lestes barbarus (Fabricius, 1798) 2,2 16,9 15,7 ++ 0 ++
Lestes dryas Kirby, 1890 14,7 14 11,7 0 0 0
Lestes sponsa (Hansemann, 1823) 62,9 50,9 48,2 0 0 0
Lestes virens (Charpentier, 1825) 5,1 7,1 12,3 + + ++
Lestes viridis (Vander Linden, 1825) 32,7 51,4 54,2 0 0 +
Leucorrhinia dubia (Vander Linden, 1825) 18,6 11,2 12,3 - + 0
Leucorrhinia pectoralis (Charpentier, 1825) 1,2 1,2 3,1 0 + ++
Leucorrhinia rubicunda (Linnaeus, 1758) 20,4 13,5 22,9 - + 0
Table 4. Relative abundance (RA) and trends for each species.
Changes in the range of dragon ies in the Netherlands and the possible role... 163
Species RA
period
1
RA
period
2
RA
period
3
trend
1st to
2nd
period
trend
2nd
to 3rd
period
trend
1st to
3rd
period
Libellula depressa Linnaeus, 1758 23,9 40,7 53,2 + + +
Libellula fulva O.F. Müller, 1764 6,8 6,5 8,5 0 0 0
Libellula quadrimaculata Linnaeus, 1758 65,8 56 64,5 0 0 0
Ophiogomphus cecilia (Fourcroy, 1785) 0,2 0,3 ++ + ++
Orthetrum brunneum (Fonscolombe, 1837) 1,6 1,2 ++ - ++
Orthetrum cancellatum (Linnaeus, 1758) 42,1 80,2 81,6 + 0 +
Orthetrum coerulescens (Fabricius, 1798) 1,7 4,1 3,2 ++ 0 ++
Platycnemis pennipes (Pallas, 1771) 17,2 18,6 18,4 + 0 +
Pyrrhosoma nymphula (Sulzer, 1776) 69,4 47,8 61 - + 0
Somatochlora arctica (Zetterstedt, 1840) 0,2 0,4 ++ ++ ++
Somatochlora avomaculata (Vander Linden,
1825) 0,1 0,7 1,7 + ++ ++
Somatochlora metallica (Vander Linden, 1825) 18,7 15,7 15,1 0 0 0
Sympecma fusca (Vander Linden, 1820) 0,4 6,2 8,3 ++ + ++
Sympecma paedisca (Brauer, 1877) 0,3 1 ++ ++ ++
Sympetrum danae (Sulzer, 1776) 51,4 45,6 45,7 0 0 0
Sympetrum depressiusculum (Selys, 1841) 1 0,5 0,1 0 - -
Sympetrum aveolum (Linnaeus, 1758) 24,4 38,4 20,2 ++ - +
Sympetrum fonscolombii (Selys, 1840) 0,4 4,8 6 ++ 0 ++
Sympetrum pedemontanum (Allioni, 1766) 1,4 1 1,7 0 + +
Sympetrum sanguineum (O.F. Müller, 1764) 37,1 64,3 58,3 + 0 +
Sympetrum striolatum (Charpentier, 1840) 13,2 39,2 41,8 + 0 +
Sympetrum vulgatum (Linnaeus, 1758) 38 44,5 48,3 0 0 +
more prone to negative in uences of other environmental factors. Five out of seven
northern species occur in mesotrophic lake and bog habitats, while there are no north-
ern species occurring in running waters. It is clear that habitat degradation is an impor-
tant factor to explain the results of the northern species group, possibly climate change
makes this decrease more severe.
e northern distribution of many southern species seems to be directly limited by
the summer temperatures, resulting in a direct expansion of their range when tempera-
ture permits (Appendix1). e southern border of northern species on the other hand
does not seem to be limited directly by temperatures, but seems to be determined by
habitats being absent more southerly and by competition with other species prevailing
in warmer climates.
e decrease of northern species as a result of increasing temperatures would in
that case be caused by degradation of habitats and by increasing competition from
southern species. is would result in a slow decline, which is far more di cult to
detect than the rapid increase shown by southern species.
Another negative e ect of increasing summer temperatures is increasing evapora-
tion, resulting in lower surface and ground water tables. is can lead to desiccation of
Tim Termaat, Vincent J. Kalkman & Jaap H. Bouwman / BioRisk 5: 155–173 (2010)
164
important vegetation structures in the riparian zone of lakes and the upstream stretches
of streams. is happens especially in late summer, when the rst and most vulnerable
larval instars of most species are present in the water. Furthermore, desiccation leads to
the stagnation of ground water in seepage fed lakes and streams, causing acidi cation.
Also the turn-over rate of organic matter increases when lake shores dry out, causing
nutrient enrichment.
Coenagrion hastulatum, Cordulegaster boltonii and Somatochlora arctica are
examples of threatened species which are known to react negatively on desic-
cation caused by human influences (e.g. intensive drainage in agricultural areas
and drinking water collection) (Groenendijk 2002; Groenendijk 2005; Ketelaar
2001a; Ketelaar 2001b; Wasscher 1999). It is expected that hot summers con-
tribute to this problem. On the other hand, temporary water specialist like Lestes
barbarus and Sympetrum flaveolum might have profited from waters becoming
shallower.
Changes in quality of habitats
e test failed to show that the species group of running water contains a signi -
cantly higher portion of increasing species than the all-species group. However, this
is probably due to the low number of species included in the group, making it
di cult to nd signi cant results. Of the ten included species ve show a strong
increase, two a moderate increase, one is stable and two show a decrease when the
rst period is compared with the third. Most striking is the comeback of Gomphus
avipes, which from 1996 onwards reoccupied all large river systems in the Nether-
lands ( gure 5), after an absence of more than 90 years (Kleukers and Reemer 1998;
Figure 1. Distribution of all tested species over the trend categories. ree di erent periods
were compared. Period 1 = 1980–1993, period 2 = 1994–1998, period 3 = 1999–2003.
Changes in the range of dragon ies in the Netherlands and the possible role... 165
Table 5. Results of χ2-tests of the observed proportions of trend categories within the di erent
species groups. *p<0,05; **p<0,01.
All spe-
cies
n=60
Southern species n=19 Northern species n=19
Ob-
served Ex-
pected pOb-
served Ex-
pected p
Period 1 compared to period 2
Number of increased
species 29 14 9.2 0.027* 4 3.4 0.641
Number of stabel /
decreased species 31 5 9.8 3 3.6
Number of decreased
species 8 1 2.5 0.301 3 0.9 0.022*
Number of stabel /
increased species 52 18 16.5 4 6.1
Number of stabel species 23 4 7.3 0.121 0 2.7 0.037*
Number of increased /
decreased species 37 15 11.7 7 4.3
Period 2 compared to period 3
Number of increased
species 23 8 7.3 0.735 5 2.7 0.072
Number of stabel /
decreased species 37 11 11.7 2 4.3
Number of decreased
species 6 2 1.9 0.939 1 0.7 0.705
Number of stabel /
increased species 54 17 17.1 6 6.3
Number of stabel species 31 9 9.8 0.708 1 3.6 0.048*
Number of increased /
decreased species 29 10 9.2 6 3.4
Period 1 compared to period 3
Number of increased
species 39 19 12.4 0.001** 4 4.6 0.663
Number of stabel /
decreased species 21 0 6.7 3 2.5
Number of decreased
species 5 0 1.6 0.189 2 0.6 0.053
Number of stabel /
increased species 55 19 17.4 5 6.4
Number of stabel species 16 0 5.1 0.009** 1 1.9 0.459
Number of increased /
decreased species 44 19 13.9 6 5.1
All spe-
cies n=
60
Species of running
waters n=10 Species of lakes and
bogs n=24 Species of fenlands
n=19
Ob-
served Ex-
pect-
ed
pOb-
served Ex-
pect-
ed
pOb-
served Ex-
pect-
ed
p
Period 1 compared to period 2
Number of increased
species 29 6 4.8 0.460 8 11.6 0.141 7 9.2 0.316
Tim Termaat, Vincent J. Kalkman & Jaap H. Bouwman / BioRisk 5: 155–173 (2010)
166
All spe-
cies n=
60
Species of running
waters n=10 Species of lakes and
bogs n=24 Species of fenlands
n=19
Ob-
served Ex-
pect-
ed
pOb-
served Ex-
pect-
ed
pOb-
served Ex-
pect-
ed
p
Number of stabel /
decreased species 31 4 5.2 16 12.4 12 9.8
Number of de-
creased species 8 2 1.3 0.535 6 3.2 0.093 1 2.5 0.301
Number of stabel /
increased species 52 8 8.7 18 20.8 18 16.5
Number of stabel
species 23 2 3.8 0.233 10 9.2 0.737 11 7.3 0.079
Number of increased
/ decreased species 37 8 6.2 14 14.8 8 11.7
Period 2 compared to period 3
Number of increased
species 23 4 3.8 0.914 10 9.2 0.737 5 7.3 0.281
Number of stabel /
decreased species 37 6 6.2 14 14.8 14 11.7
Number of de-
creased species 6 2 1.0 0.292 2 2.4 0.785 0 1.9 0.146
Number of stabel /
increased species 54 8 9.0 22 21.6 19 17.1
Number of stabel
species 31 4 5.2 0.460 12 12.4 0.870 14 9.8 0.055
Number of increased
/ decreased species 29 6 4.8 12 11.6 5 9.2
Period 1 compared to period 3
Number of increased
species 39 7 6.5 0.740 10 15.6 0.017* 12 12.4 0.866
Number of stabel /
decreased species 21 3 3.5 14 8.4 7 6.7
Number of de-
creased species 5 2 0.8 0.182 2 2.0 1000 0 1.6 0.189
Number of stabel /
increased species 55 8 9.2 22 22.0 19 17.4
Number of stabel
species 16 1 2.7 0.233 12 6.4 0.010* 7 5.1 0.316
Number of increased
/ decreased species 44 9 7.3 12 17.6 12 13.9
Bouwman and Kalkman 2005). One extinct species (Ophiogomphus cecilia) and one
absent species (Onychogomphus forcipatus) were found reproducing in the 1990’s,
in the river Roer in the south of the Netherlands (Geraeds 2000; Geraeds and Van
Schaik 2004). Platycnemis pennipes, Gomphus vulgatissimus, Orthetrum coerulescens,
Orthetrum brunneum and Sympetrum pedemontanum increased (van Eijk and Ket-
Changes in the range of dragon ies in the Netherlands and the possible role... 167
elaar 2004; van Delft 1998; Mensing 2002), while Calopteryx splendens remained
stable. Calopteryx virgo and Cordulegaster boltonii are the only rheophilic species
showing negative trends, however the observed numbers of these species have in-
creased recently and several new localities were found (Groenendijk 2002; Termaat
Figure 3. Distribution of the tested northern species over the trend categories. ree di erent
periods were compared. Period 1 = 1980–1993, period 2 = 1994–1998, period 3 = 1999–2003.
Figure 2. Distribution of the tested southern species over the trend categories. ree di erent
periods were compared. Period 1 = 1980–1993, period 2 = 1994–1998, period 3 = 1999–2003.
Tim Termaat, Vincent J. Kalkman & Jaap H. Bouwman / BioRisk 5: 155–173 (2010)
168
and Groenendijk 2005). In our opinion, these ndings leave no doubt that species
of running water have increased strongly since 1980. Water quality improvement
and restoration of the natural morphology of streams and rivers are likely to be the
important causes for it. Some species probably pro ted from the higher summer
temperatures as well. is is at least very likely for Orthetrum brunneum, O. coerule-
scens and Sympetrum pedemontanum.
Whereas the quality of running water habitats has improved, the threats for stagnant
water habitats such as mesotrophic lakes and bogs are still present. Eutrophication, dessi-
cation and habitat fragmentation are still factors which explain why relatively few species
in this species group show a positive trend. e intensity of eutrophication has reduced
in recent years (RIVM 2003), but in many cases this has not lead to the recovery of lakes
and bogs that have already been spoiled. e results of our analyses suggest that the nega-
tive trend of the species group of mesotrophic lakes and bogs stopped, but that they fail to
recover. Especially Coengrion hastulatum, a species of mesotrophic lakes and bogs, is still
declining in the Netherlands and is becoming increasingly endangered (Termaat 2006).
Conclusions
e analyses of the trends in the period 1980 to 2003 shows that the 55 Dutch drag-
on y species for which a trend could be calculated remained stable or increased during
Figure 4. Distribution of the tested species of mesotrophic lakes and bogs over the trend cat-
egories. ree di erent periods were compared. Period 1 = 1980–1993, period 2 = 1994–1998,
period 3 = 1999–2003.
Changes in the range of dragon ies in the Netherlands and the possible role... 169
that time period and that only 5 species have declined. Habitat degradation during the
larger part of the 20th century resulted in a degradation of the dragon y fauna in the
eighties of that century. Improved water quality and increasing summer temperatures
in the last two decades resulted in a revival of the Dutch dragon y fauna.
Although our analyses failed to show that the species group of running water con-
tains a signi cantly higher portion of increasing species than the all-species group, it is
clear that especially species of running water have increased since 1980. is is prob-
ably largely due to the improved water quality of running waters and the restoration of
the natural morphology of these systems.
e average temperature in the last twenty years of the 20th century was 0,7 °C
higher than those of the rst twenty years of the 20th century. As a result signi cantly
more species with a southern distribution show a positive trend when compared with
the all-species group.
Seven species very rare or absent prior to 1990 became established in the Nether-
lands, probably due to the increase in temperature. ree of these established them-
selves by means of large invasions. ese invasions were very e ective, showing once
more that dragon ies are highly capable of colonising new areas. No evidence could
Figure 5. e distribution of Gomphus avipes in the period 1996–2005. e species was not
found in the Netherlands from 1902 to 1995.
Tim Termaat, Vincent J. Kalkman & Jaap H. Bouwman / BioRisk 5: 155–173 (2010)
170
be provided to state that species with a northern distribution are decreasing due to the
higher temperatures. e habitats where these species live (mostly mesotrophic lakes
and bogs) have been strongly in uenced by eutrophication, acidi cation and desic-
cation in the 1960th and 1970th resulting in a decline of most of these species. is
decline might have masked the in uence of climate change.
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Appendix1
Southern species and invasions
Six southern species rare or absent in the 1980’s are now well recognised members of
the Dutch odonate fauna: Lestes barbarus, Erythromma lindenii, Aeshna a nis, Croco-
themis erytraea, Orthetrum brunneum and Sympetrum fonscolombii. Anax parthenope is
expected to become established in the coming years, as it recently became a regular
guest and has reproduced successfully. e way in which southern species became es-
tablished in the Netherlands di ers among the species. E. lindenii, C. erytraea ( gure
6) and to a lesser extent O. brunneum gradually expanded the northern border of
their range. e other three species L. barbarus, A. a nis, and S. fonscolombii became
established after invasions, being rare in the years preceding these invasions (see table
6). e invasion of Lestes barbarus started in July 1994 (Ketelaar 1994) During the
invasion records were made in most areas of the country with a strong emphasises on
the dunes and the Pleistocene areas. At the majority of these localities several (up to
40) individuals were found. Almost all records were made at shallow, warm waters such
as dried-out bogs and smaller dune lakes. In many cases the species established itself
at these localities. Probably several smaller invasions occurred since 1994 but these
went largely unnoticed as the species was already established. In the period since 1994
the species is found yearly in suitable habitat all over the Netherlands. Preceding the
1994 invasion the northern border of the distribution of L. barbarus was situated to
the south of the Netherlands. e invasion in 1994 therefore resulted in a northwards
expansion of its range of well over 300 km.
e invasion of A. a nis started mid July 1995. All 39 records from 1995 came
from the southern part of the Netherlands, most of them from the coastal dunes or
from the Pleistocene areas. Almost all individuals were found at drying or dried-out
waters, with low reeds or bulrushes. Of the 81 sexed specimens only four were females.
is might be partly due to the inconspicuous behaviour of the females. Since the 1995
Figure 6. e distribution of Crocothemis erythraea in the periods 1980–1993, 1994–1998
and 1999–2003, showing its gradual northwards expansion.
Changes in the range of dragon ies in the Netherlands and the possible role... 173
invasion the species is found several times a year in all parts of the Netherlands. e
rst proof of successful reproduction was found in 2005 (Wasscher 2005) although it
is likely that small (temporary) populations have existed since 1995.
In end May and begin June of 1996 a massive invasion of Sympetrum fonscolombii
reached Northwestern Europe (Lempert 1997; Dijkstra and Van der Weide 1997). As
with Lestes barbarus the species was recorded all over the country with a strong emphasis-
es on the dunes and the Pleistocene areas. Most records were made at unshaded, standing
waters with sparse vegetation and often sandy banks. e species managed to establish
itself at many of these localities. Since 1996 the species is found every year at numerous
localities across the country, although it has become less abundant than in 1996.
e invasions of L. barbarus, A. a nis, and S. fonscolombii have two things in
common:
1 During the invasion almost all specimens were found at suitable habitats and not
seldom successful reproduction was noticed in later years;
2 Most records during the years of the invasions referred to more than one specimen.
e three species which invaded e Netherland in 1994, 1995 and 1996 were rarely
seen at unsuitable sites. is stresses the fact that these species are highly capable of local-
ising suitable habitats. is is further emphasised by the fact that in most cases more than
one individual was found at a locality. ese species do not y in clustered groups mak-
ing it likely that the individuals from one locality all located the habitat on their own.
Probably these species used their ability to recognise polarized light combined with
visual cues on vegetation structure to detect suitable habitat from some height as has
been shown for some species of dragon ies (Corbett 1999). is makes that a relatively
high portion of the individuals taking part in the invasion is able to reproduce at a po-
tentially suitable location. ese examples show that at least these species are capable of
taking advantage of favourable circumstances in an extremely e ective way.
Species Established due to Number of records
in the 10 years prior
to invasion
Number of records
in year of invasion
Aeshna a nis Invasion in 1995 1 39
Anax parthenope Gradually (1)
Crocothemis erythraea Gradually
Erythromma lindenii Gradually
Lestes barbarus Invasion in 1994 14 79
Orthetrum brunneum Probably gradually
Sympetrum fonscolombii Invasion in 1996 1 135
Table 6. Southern species rare during the eighties which have become established since 1990.
e second column states whether or not the species became established during a large invasion
or gradually expanded northwards.
(1) Anax parthenope is not yet established but has become a regular guest and is likely to become
established in the future.
