Increased Stream Productivity
with Warming Supports Higher
Trophic Levels☆
Elísabet Ragna Hannesdóttir*,1, Gísli Már Gíslason*, Jón S. Ólafsson†,
Ólafur Patrick Ólafsson*, Eoin J. O’Gorman{,}
*Institute of Life and Environmental Sciences, University of Iceland, Reykjavı́k, Iceland
†
Institute of Freshwater Fisheries, Reykjavı́k, Iceland
{
School of Biological and Chemical Sciences, Queen Mary University of London, London, United Kingdom
}
Imperial College London, Silwood Park Campus, Ascot, Berkshire, United Kingdom
1
Corresponding author: e-mail address: [email protected]
Contents
1. Introduction
2. Methods
2.1 Research site
2.2 Field and laboratory methods
2.3 Data handling and statistical analysis
3. Results
3.1 Stream temperature
3.2 Stream macrophytes
3.3 Macroinvertebrate life cycles and growth rates
3.4 Macroinvertebrate growth rate, biomass and production
3.5 Brown trout biomass
4. Discussion
4.1 Hengill as a model system
4.2 Stream macrophytes
4.3 Macroinvertebrate life cycles and growth rates
4.4 Macroinvertebrate biomass and production
4.5 Brown trout biomass
5. Conclusion
Acknowledgements
Appendix A. Length–Weight Relationships Used to Estimate Dry Mass of
Macroinvertebrates
Appendix B. Head-Width Measurements for Instar Separation in Each Stream
References
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The chapter does not require any permission.
Advances in Ecological Research, Volume 48
ISSN 0065-2504
http://dx.doi.org/10.1016/B978-0-12-417199-2.00005-7
#
2013 Elsevier Ltd
All rights reserved.
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Elísabet Ragna Hannesdóttir et al.
Abstract
Metabolic theory predicts that warming will increase the energetic demands of organisms, with especially strong effects on larger individuals. Mean individual body size
should therefore decline, which also implies a loss of biomass at higher trophic levels.
If resources are plentiful and easily assimilated, however, the required to persist in
warmer environments may be attained, leading to faster growth rates and an overall
increase in the biomass of apex predators. Here, we investigated the response of different trophic groups to increasing temperature in a system of geothermal streams in
Iceland, exposed to a temperature gradient of 5–21 C. These streams provide an ideal
natural experiment for isolating the effects of warming in multispecies systems, as they
have broadly similar geographical and physicochemical features. The macrophyte cover
increased significantly with increasing stream temperature, suggesting a greater
resource pool for macroinvertebrates (either through direct grazing or feeding on epiphytes). This was reflected by a greater number of generations in 1 year among
macroinvertebrates: species in the coldest streams were either uni- or bivoltine, while
those in the warmer streams were mostly bivoltine or multivoltine. Differences in phenology were also seen among streams, with emergence of adults limited mostly to the
summer months in the colder streams, but occurring year-round in the warmer streams.
Macroinvertebrates also grew faster with increasing temperature, contributing to
greater population biomass and secondary production in the warmer streams. This
increase in prey availability likely produced more favourable conditions for top predators in the warmer streams, leading to an increasing biomass of brown trout with
increasing temperature. These findings suggest that warming does not necessarily
favour the small in aquatic ecosystems, with high-resource availability, faster reproductive and growth rates and greater production all contributing to meet the highmetabolic demands of apex predators in warmer environments.
1. INTRODUCTION
Global-average surface warming is projected to range from 0.6 to
4.0 C by the end of the twenty-first century compared to 1980–1999
values (Solomon et al., 2007). The greatest warming is projected for winter
in the Arctic, with an increase of 4.3–11.4 C (Christensen et al., 2007).
Climate-change-induced alterations to biota have already been detected
across multiple levels of organisation (e.g. from individuals to ecosystems)
and these are expected to accelerate over the next century (CAFF, 2010).
Species have exhibited altered phenology as a result of environmental
warming, including earlier emergence dates (Hogg and Williams, 1996;
Kearney et al., 2010; Parmesan and Yohe, 2003; Thackeray et al.,
2010). The distribution of a wide range of taxonomic groups is shifting
Increased Stream Productivity with Warming Supports Higher Trophic Levels
287
in elevation or expanding polewards in response to warming (Chen et al.,
2011; Colwell et al., 2008; Hickling et al., 2006; Parmesan et al., 1999;
Rosenzweig et al., 2007). Taxa with a northern distribution have tended
to either move polewards in the southern range margin with warming or to
contract their range (Hickling et al., 2005). Recent evidence also suggests
that reduced body size, both within and among species, may be a universal
ecological response to global warming in aquatic systems, and it has been
hypothesised that this may be due to underlying metabolic constraints
operating on individual organisms (Daufresne et al., 2009; Gardner
et al., 2011; Sheridan and Bickford, 2011; but see O’Gorman et al.,
2012). Given that energy is the fundamental currency of ecology and that
body size determines the structure and dynamics of multispecies systems,
and aquatic food webs, in particular, it is imperative that we improve
our understanding and predictions of these effects of warming on natural
systems if we are to anticipate the future consequences of climate change
(Woodward et al., 2010a).
It is widely recognised that large consumer species, and particularly top
predators, are likely to be most susceptible to the impacts of global warming,
either through increased energy requirements (Kordas et al., 2011;
McDonald et al., 1996; Petchey et al., 1999), multiple predator effects
(Barton and Schmitz, 2009), and/or temporal mismatch with their prey
(Edwards and Richardson, 2004; Durant et al., 2007; Winder and
Schindler, 2004). Metabolic rate scales exponentially with temperature, such
that the energy demands of consumers increase dramatically with warming
(Gillooly et al., 2001). The metabolic theory of ecology (Brown et al., 2004;
West et al., 2003), although still controversial, may provide at least a useful
heuristic framework for interpreting the mechanism(s) underlying so-called
temperature-size rules in ecology (Angilletta and Dunham, 2003; Atkinson,
1994; James, 1970). For instance, increases in energetic requirements may be
counter-balanced by decreases in body mass with warming, maintaining the
flow of energy through food webs (Woodward et al., 2010a). Thus, in
resource-limited ecosystems, there should be (all else being equal) a tendency towards (a) reduced mean body size (and biomass) of individual species, as suggested by James’s rule and the temperature-size rule (Atkinson,
1994; James, 1970) and/or (b) a shift towards smaller-sized species within
a community, supporting Bergmann’s rule (Bergmann, 1847), with emigration or extinction of large predators. However, if resources are plentiful, the
energy requirements of larger species may be met, maintaining the overall
structure of the ecosystem.
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Elísabet Ragna Hannesdóttir et al.
Environmental warming may reduce resource availability in terrestrial
environments, with lower precipitation and extreme summer heat leading
to widespread declines in primary productivity (Ciais et al., 2005; Phillips
et al., 2009; Zhao and Running, 2010). Ocean productivity has also been
demonstrated to decline with recent increases in climatic temperature
(Behrenfeld et al., 2006; Hoegh-Guldberg and Bruno, 2010), albeit with
regional variation (Sarmiento et al., 2004). However, the evidence from
freshwater ecosystems appears to reflect an increase in resource availability
with warming: microcosm experiments have shown that warmed communities become dominated by autotrophs and bacterivores (Petchey et al.,
1999), while outdoor mesocosm experiments show that warming caused
an increased prevalence of small-bodied phytoplankton with faster turnover
rates, contributing to higher gross primary productivity (Yvon-Durocher
et al., 2010, 2011). However, the same experiments also resulted in reduced
abundance of larger predatory benthic invertebrates in response to warming
(Dossena et al., 2012). Previous research on natural warming experiments in
Iceland has demonstrated a change in primary producer assemblages, with a
shift from diatom to bryophyte-dominated communities after a 6 C temperature increase (Gudmundsdottir et al., 2011), with associated increases in
whole-ecosystem gross primary productivity (Demars et al., 2011). While it
should be noted that increased productivity in freshwater ecosystems with
warming is not ubiquitous (e.g. McDonald et al., 1996), this general trend
may imply a divergence from observations in other ecosystems and raises the
possibility of differential survival success for higher trophic-level organisms
in the face of global warming.
Growth rate generally increases with warming up to an optimum temperature, above which development and growth decelerate (Angilletta
et al., 2004; Deutsch et al., 2008; Frazier et al., 2006; Reynolds and
Benke, 2005; Taylor, 1981). All species live optimally within a certain temperature range; some are stenothermal and restricted to a narrow range,
while others are eurythermal, that is, have a wide temperature tolerance
(Sweeney, 1984). Many studies have shown a shift in freshwater invertebrate
community composition with warming (Dossena et al., 2012; Friberg
et al., 2009; Lessard and Hayes, 2003; Snorrason et al., 2011; Woodward
et al., 2010b), with cold-water species replaced by more thermophilic species (Daufresne et al., 2004). Cold-adapted species already living at high latitudes and elevations have limited options and are likely to disappear if they
cannot adapt to higher temperatures, making Arctic and sub-Arctic regions
especially vulnerable (Somero, 2010). Eurytherms and warm-adapted
Increased Stream Productivity with Warming Supports Higher Trophic Levels
289
stenotherms are likely to invade new areas by expanding their range (Dukes
and Mooney, 1999; Walther et al., 2002), with faster growth and development also likely (Deutsch et al., 2008; Frazier et al., 2006; Sweeney, 1984;
Tokeshi, 1995), but this is obviously only possible if they can colonise
from the regional species pool. Invertebrates and other small taxa may have
greater flexibility than vertebrates, as they may be able to complete more
generations per year (Oliver, 1971). An increase in mean annual stream
temperature could, however, cause premature emergence of adults (Harper
and Peckarsky, 2006; Hogg and Williams, 1996; Li et al., 2011), even in winter when sudden drops in air temperatures can be lethal (Nebeker, 1971),
although evidence from industrial warming of British rivers suggests that such
responses are not ubiquitous (Langford, 1975; Langford and Aston, 1972).
Alternatively, rapid growth and development could lead to greater secondary
production, sustaining community structure in the face of higher energetic
requirements with warming (Brown et al., 2004). Thus, short-term responses
to warming might include changes in growth and developmental rates of individual species that can tolerate the increase in temperature, which could be
reflected in phenological changes in voltinism and emergence patterns.
A more coherent whole community response would likely occur over a longer time period, as population structures and thus interactions between organisms in the community become altered.
The study of invertebrate life cycles under warming offers an ideal avenue to explore the response of growth, development, emergence and production to potential impacts of climate change. However, most studies of
temperature effects on invertebrate life cycles have been conducted in the
laboratory (Becker, 1973; Elliott, 1987; Reynolds and Benke, 2005) or
along temperature gradients in the same stream (Aston, 1968; Langford,
1971). Whole-stream warming experiments are extremely rare, but have
been important for determining changes in growth and emergence under
more natural conditions (Hogg and Williams, 1996; Li et al., 2011), with
ongoing experiments likely to provide new insights in the coming years
(O’Gorman et al., 2012). Geothermal streams have also been identified as
ideal natural systems for studying the future impacts of global warming on
aquatic environments (Friberg et al., 2009), especially in Arctic regions,
which have been recognised as early warning signals for change at lower latitudes (Woodward et al., 2010b). There is a pressing need for investigations
of invertebrate life cycles in such natural systems (Resh and Rosenberg,
2010), particularly in light of future climate-change scenarios (Christensen
et al., 2007), and this can complement other more experimental approaches
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Elísabet Ragna Hannesdóttir et al.
such as those using field-based mesocosms (Ledger et al., 2013; Stewart
et al., 2013).
Temperature-induced changes in secondary production, whether they
are mediated by resource availability, life cycles or macroinvertebrate biomass, may play an important role in the sustainability of higher trophic-level
organisms. Conversely, if large vertebrate predators such as fish are not
excluded from warmer environments by excessive energy demands or thermal limits, they may have the capacity to suppress the biomass, growth and
production of macroinvertebrates. The relative importance of bottom-up
and top-down control has long been debated in aquatic ecosystems
(Hillebrand, 2002; Hunter and Price, 1992; Terborgh, 1988; Wilson,
1987), and more recently in the context of climatic or warming effects
( Jochum et al., 2012; O’Gorman et al., 2012). Thus, by linking the relative
importance of warming impacts on basal resources, primary consumers and
apex predators, we can begin to tease apart the contribution of bottom-up
and top-down processes to the sustainability of ecosystem structure in the
face of climate change.
Here, we assess the impact of warming on multiple trophic levels in a
geothermally heated system of streams in Iceland. This system consists of
a series of streams close to one other, which are heated to different degrees
by geothermal activity (see Section 2). While the long-term evolutionary
adaptations of organisms to these streams of different temperature does
not allow investigation of short-term responses to rapid warming, the system
acts as a useful space-for-time substitution (cf. Meerhoff et al., 2012) for
exploring population- and community-level responses to warmer waters.
This is relevant at a global scale, by generalising responses of freshwater ecosystems to the impacts of increasing stream temperature, but it is also particularly relevant at regional and local scales, given the predicted susceptibility
of northern latitude ecosystems to rapid warming over the coming century
(Christensen et al., 2007). Thus, our study facilitates prediction of how species dominance, life cycles and the productivity of freshwater organisms may
be altered by environmental warming in the near future.
We examined the effect of stream temperature on multiple trophic levels
in the Hengill system by quantifying the percentage cover of macrophytes
and the biomass of macroinvertebrates and fish along the temperature gradient, building on earlier work in this catchment-scale ‘natural experiment’
(Demars et al., 2011; Friberg et al., 2009; Gudmundsdottir et al., 2011;
Hannesdóttir et al., 2012; O’Gorman et al., 2012; Perkins et al., 2012;
Woodward et al., 2010b). We also determined the population dynamics
Increased Stream Productivity with Warming Supports Higher Trophic Levels
291
of the intermediate trophic group by analysing the life cycles of the dominant macroinvertebrate taxa: four chironomid taxa, one simuliid species,
one trichopteran species and one species of gastropod. The life cycles of
two of the chironomid species have previously been described in detail elsewhere (Hannesdóttir et al., 2012), but here they form part of the more
extensive multispecies analysis. We describe their voltinism and timing of
emergence, as well as the relationship between growth rates and temperature. Finally, we estimate secondary production and link this to the lower
(i.e. primary producers) and higher (i.e. fish) trophic levels. We test the following hypotheses:
1. Resource availability, measured as the percentage cover of macrophytes,
will increase with increasing temperature in these freshwater streams.
2. The growth and development rates of the macroinvertebrates will
increase along the temperature gradient of the streams, which will be
reflected in changes in voltinism (i.e. univoltine becoming bi- or multivoltine) and emergence pattern, with the completion of more generations per year and earlier emergence over a longer period.
3. Macroinvertebrate biomass and production will increase with increasing
temperature in response to hypothesis 1 and 2.
4. Fish biomass will decrease with increasing temperature due to higher
metabolic demands.
2. METHODS
2.1. Research site
The study was carried out in the Hengill geothermal area of southwest
Iceland (64 030 N: 021 180 W, 350–420 m above sea level), approximately
30 km east of the capital Reykjavı́k (Fig. 1). The Hengill geothermal field
is a high-temperature area, with thermal readings of over 200 C in the
uppermost 1 km of the Earth’s crust and about 50 clusters of hot springs distributed over an area of 50 km2 (Árnason et al., 1967). Here, first-order
spring-fed streams can be found, some of which are geothermally influenced
to a varying degree, thus differing in temperature (Table 1). All of the
streams run into the River Hengladalsá. Due to the logistical constraints
of repeatedly sampling streams throughout the year, just seven were selected
for intensive research in this study. The streams were all in close proximity to
each other (5–1000 m). Four of the streams were geothermally influenced
(IS6, IS1, IS5 and IS8), while three were not (IS11, IS7 and IS9). The geothermally influenced streams are referred to as the ‘warm’ streams, while the
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Elísabet Ragna Hannesdóttir et al.
Figure 1 Map of Iceland showing the research site at Hengill (black square). From the
seven streams that were repeatedly sampled for macroinvertebrates, four streams (IS1,
IS5, IS6 and IS8) were geothermally influenced, while the remaining three (IS7, IS9 and
IS11) were not. Two additional streams (streams IS14 and IS17) and the River
Hengladalsá were part of the study on brown trout. These two streams were located
in Innstidalur valley. All the streams run into the River Hengladalsá. The arrow shows
the direction of flow. Scale bar 100 m. Drawing was based on aerial photographs with
permission from Samsýn ehf.
Table 1 Annual (from September 2006 to August 2007), winter (December, January and
February) and summer (June, July and August) temperatures ( C; mean standard
deviation), with differences (diff ) between summer and winter for all the streams
sampled for invertebrates
Annual
Winter
Summer
Diff.
Min.
Max.
IS11
5.3 3.8
2.0 1.1
10.4 2.4
8.3
1.6
12.2
IS7
5.4 1.4
4.5 0.8
6.6 1.3
2.1
4.1
7.1
IS9
9.7 2.8
7.9 1.3
13.1 1.9
5.2
7.2
14.2
IS6
13.3 3.4
10.1 3.9
16.4 1.5
6.3
7.1
17.2
IS1
13.5 4.1
10.5 1.3
17.7 3.0
7.2
8.9
19.4
IS5
16.1 1.5
15.2 1.0
17.6 1.1
2.4
14.9
18.5
IS8
21.3 1.0
20.9 1.0
22.0 0.8
1.0
19.9
22.7
The minimum (Min.) and maximum (Max.) monthly average temperatures are also shown for
each stream.
Increased Stream Productivity with Warming Supports Higher Trophic Levels
293
ambient streams are referred to as the ‘cold’ streams. Despite the geothermal
influence, all the streams are otherwise broadly comparable in water chemistry, with any (minor) differences being independent of temperature
(Friberg et al., 2009; O’Gorman et al., 2012; Rasmussen et al., 2011).
The majority of the streams are located in the Miðdalur, where the valley
floor is dominated by moss and grassland (Gudjónsson et al., 2005). As no
woody vegetation is found in the area, input of coarse allochthonous material to the streams is small (Friberg et al., 2009). Brown trout (Salmo trutta,
Linnaeus 1758) is the only fish species that has been recorded in the streams
and River Hengladalsá (Friberg et al., 2009). The streams at Hengill
encompass the thermal limits of brown trout (Table 1): the lower lethal temperature for salmonids in freshwater is slightly below 0 C, while the upper
lethal temperature for brown trout is approximately 25 C ( Jonsson and
Jonsson, 2011).
2.2. Field and laboratory methods
Water temperature in the seven streams (Table 1) was recorded with a logger
(TidbiT, Onset 32K StowAway, USA) every 30 min over the sampling
period. Annual averages were calculated, along with mean summer ( June,
July and August) and winter (December, January and February) temperatures for each stream. Annual averages were used for the majority of analyses,
but the estimation of secondary production necessitated the use of monthly
averages. Annual temperature fluctuation was determined as the difference
between summer and winter averages. During studies on brown trout, temperature data from an additional two cold streams (IS14 and IS17) and the
River Hengladalsá were based on five spot measurements taken in the time
period from 15 May to 24 September 2006. Note that these were not part of
the seven shown in Table 1, which were used for the more intensive sampling of macroinvertebrates through the year.
Benthic samples were collected with a Surber sampler (KC mini Surber
sampler) with a frame size of 14 14 cm (approximately 0.02 m2) and a
200 mm mesh-aperture net. Samples were collected over a 1.5-year period
(March 2006 to August 2007) in two streams (IS6 and IS7) and for 1 year
(September 2006 to August 2007) in the remainder (IS1, IS5, IS8, IS9
and IS11), but note that production estimates (see below) were calculated
for the same time period in all streams. Samples were collected from the
stream bed at random coordinates along 15–25 m reaches and preserved
in 70% ethanol. Five samples were collected for each sampling occasion from
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Elísabet Ragna Hannesdóttir et al.
each stream. Within each frame of the Surber sampler, the main types of macrophytes were identified and their cover estimated before sampling invertebrates. The cover was estimated to the nearest 10%. Each sample was
collected by vigorously disturbing the substrate within the frame of the
Surber sampler for approximately 30 s. Invertebrates were counted and
identified using a Leica MZ 12.5 dissecting microscope (80 magnification).
The width of the larval head capsule was measured with 0.01 mm accuracy
for Chironomidae and Simuliidae (100 magnification) and 0.025 mm
accuracy for Trichoptera (40 magnification), using an ocular graticule.
Larval body length was measured with 0.5 mm accuracy. The shell length
of the gastropod Radix balthica (Linnaeus 1758) (synonym Radix peregra
(Müller 1774) (Anderson, 2005)) was measured to the nearest 0.5 mm.
For each sample, a subsample of approximately 100 chironomid larvae
were mounted on a microscope glass in Hoyer’s medium (Anderson,
1954) using a 10-mm circular coverslip. If the number was less than 100
in a sample, then all were mounted and identified. The larvae were identified
using a Leica DM4000 high-power microscope using a magnification of
400–1000 . All the chironomid pupae and pupal exuviae were identified.
The simuliid and trichopteran larvae could be identified using a dissecting
microscope and therefore did not necessitate mounting like the chironomid
larvae. Between 50 and 100 simuliid larvae from each sample were measured
and identified. All the simuliid pupae in the samples were identified. The
presence of I instar simuliid larvae, which was based on the presence of
an egg burster (i.e. a spine on the surface of the exoskeleton of the embryo,
which is used to break the egg membrane at hatching and is only found on
newly hatched larvae), was noted. The abundance of chironomid and
simuliid prepupae, identified from the swollen prothorax and the presence
of wing disks, was also noted. All trichopteran larvae found in the
samples were measured and identified. Approximately 250 individuals of
R. balthica were measured for each month and stream, but when fewer
were present all were measured. The presence of egg masses of R. balthica
in the samples was recorded.
Some of the major chironomid species were reared from larvae in order
to identify them to species level and verify identification. Larvae that
were collected in the field were reared individually on small Petri dishes
in the laboratory, as recommended by Cranston (1982). The pupal skins
of the genus Micropsectra were identified as Micropsectra atrofasciata (Kieffer
1911) but Thienemanniella Kieffer 1911 pupal skins could not be identified
to species level, as was the case with the specimens previously recorded
Increased Stream Productivity with Warming Supports Higher Trophic Levels
295
in Iceland (Hrafnsdottir, 2005). Keys used for identification of chironomid
larvae were by Cranston (1982), Wiederholm (1983) and Schmid
(1993). Chironomid pupae and pupal exuviae were identified to the lowest
taxonomic level (genera/species) under a dissecting microscope using the
identification keys by Langton (1991), Wiederholm (1986) and Wilson
and Ruse (2005). Keys by Peterson (1977) and Peterson and Kondratieff
(1994) were used in the blackfly identifications. A key by Gislason (1979)
was used to identify caddisfly larvae. The Website www.faunaeur.org
(Fauna-Europaea, 2012) was used as a reference to invertebrate taxonomy.
The brown trout (S. trutta) were caught by electrofishing with one pass
from five streams (IS1, IS5, IS8, IS14 and IS17) and the River Hengladalsá
from 15 to 30 May 2006, where 400 trout in total were tagged with PITs
(passive integrated transponders), and released at the site where they were
caught. In September 2006 and June 2007, electrofishing was repeated in
the same streams and in River Hengladalsá. In the River Hengladalsá, the
electrofishing was performed 50 m up- and downstream from the confluence of each stream. In the warm streams (IS1, IS5 and IS8), electrofishing
was done in the whole stream, while in the cold streams (IS14 and IS17), a
stretch of 150 m upstream from the confluence with the River Hengladalsá
was electrofished. The surface area that was electrofished in each stream and
river was calculated from length and width measurements, where the total
length was measured, as well as the width at 10 m intervals. The trout were
weighed upon capture to the closest 0.1 g using a portable electronic mass
balance and their length was measured to the nearest mm.
2.3. Data handling and statistical analysis
The relationship between average annual percentage macrophyte cover and
stream temperature was determined by linear regression analysis. Relationships between individual species of macrophytes and temperature were also
explored. The contribution of macrophyte taxa to the total cover was determined by examining relative proportions of the main taxa for each stream,
based on annual averages. The regression was performed on untransformed
data, since the tests for normality and homogeneity of variance were passed.
The larval instars were determined by plotting a frequency histogram of
the head widths for every chironomid, simuliid and caddisfly taxa, where
each peak represents an instar (Daly, 1985). The use of head-width measurements for instar determination is the most commonly used measurement
(McCauley, 1974). The instars of the blackfly species Simulium (Psilozia)
296
Elísabet Ragna Hannesdóttir et al.
vittatum Zetterstedt 1838 could not be distinguished from frequency histograms of the head-capsule widths, because they did not show distinct peaks.
The larvae were therefore assigned to seven groups of equal size on a linear
scale, the same as the previously proposed number of instars for the species
(Crosskey, 1990). The frequency histogram of the head widths of the genus
Thienemanniella showed only three peaks instead of four. The head width of
III instar larvae has been reported to be on average 107.3 mm, while the head
width for IV instar larvae averaged from 132.5 to 177.4 mm depending on
the species (Schmid, 1993). Based on these measurements, we assigned the
group with the largest head widths (i.e. 3rd peak) as being IV instar larvae
and the middle group (2nd peak) to III instar larvae. The first group
(1st peak) was likely a combination of I to II instar larvae, although the
smallest larvae might have been missed during sieving and sorting, due to
their small size. The proportion of each instar/group, pupae (for chironomids and simuliids) and pupal exuviae (for chironomids) for each month
of sampling was calculated for the determination of the life cycles. The presence of pupae and pupal exuviae was used to estimate the timing of emergence. When pupal exuviae were found in the samples, we knew that the
adults had recently emerged. The proportion of each size class (0.5 mm
interval) of R. balthica was also calculated and used in life-cycle analysis. Note
that in the description of life cycles, additional data from June of one year and
July of another year were also used to draw inferences about annual patterns
in life history.
The instantaneous biomass growth rate (mg mg1 d1) of each invertebrate species was calculated as (ln Mf ln Mi)/t, after Huryn and Wallace
(1986), where Mf and Mi are the final and initial body masses spanning a generation, respectively, and t is the duration of a generation in days. Body
masses (mg) were estimated from the length measurements; according to
a mixture of newly generated and established length–weight relationships
(see Appendix A). For bivoltine species and those that were putatively multivoltine (i.e. with two summer generations plus the winter generation), the
growth rate of the generation extending over winter was calculated. The
growth rates for the summer generations could not be calculated, because
they could not be separated or because of the overlap between the winter
and summer generations. In a few cases, the number of individuals for certain species was too low for the calculation of growth rates, or too complex,
that is, overlapping summer generations. The relationship between geometric mean growth rate and annual average temperature was determined
Increased Stream Productivity with Warming Supports Higher Trophic Levels
297
using linear regression analysis. Taxa for which growth rate could only be
calculated in one stream (and so at one temperature) were excluded from
this analysis. The data complied with normality and constant variance, so
remained untransformed for this analysis. The different growth rates of each
taxon in separate streams were explored with regard to the temperature gradient. For taxa that showed differences in voltinism in different streams, the
average growth rates were calculated for the univoltine and bivoltine
populations separately, for comparison between the two.
The standing crop biomass (dry weight mg m2) of chironomid, simuliid
and trichopteran larvae and the gastropod R. balthica was estimated for each
sampling occasion. Here, biomass is simply the product of mean body mass
and abundance; with L–W relationships used to estimate body mass from
length measurements (see Appendix A). The annual average biomass of each
of the measured taxa was calculated along with the annual average
macroinvertebrate biomass. The contribution of each of the measured
taxa to the macroinvertebrate biomass was calculated along with relative
proportions. The relationship between average annual biomass of macroinvertebrates and stream temperature was explored using linear regression
analysis. Relationships between individual macroinvertebrate species and
temperature were also explored in the same fashion. The relationship
between average annual biomass of invertebrates and macrophyte cover
was explored with linear regression. The biomass data were transformed
to logarithmic scale (log10), as the log-linear regression was a better fit than
a linear regression, where assumptions of normality and equal variance
were met.
Secondary production of macroinvertebrates was estimated according to
Huryn and Wallace (1986). Here, production was calculated as IGR (Bf þ Bi)/2 t, where IGR is the instantaneous growth rate at a given sampling occasion (estimated from average stream temperature between the
sampling occasions and the growth rate versus temperature relationship
described above), Bf and Bi are the standing crop biomasses on the current
and previous sampling occasions (as described above), respectively, and t is
the time between sampling occasions in days. The production values for
each time interval were summed together to calculate the annual production. As the sampling period (September 2006 to August 2007) was less than
a full year (i.e. 365 days), the data were corrected for annual production
(expressed as mg m2 yr1). The relationship between secondary production and stream temperature was explored using linear regression analysis,
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Elísabet Ragna Hannesdóttir et al.
where secondary production was transformed to log10 to better fit the data,
where assumptions of normality and equal variance were met.
In May 2006, trout population sizes in the streams were estimated with
mark-recapture method. Population sizes on later dates were estimated from
the ratio between the total catches of electrofished trout in September 2006
and June 2007 with the May 2006 catches in each stream. The densities in
the streams were the product of estimated population sizes and the surface
area that was electrofished, and was expressed as individuals per m2. The
trout biomass (g m2) was calculated by multiplying the average body mass
by the density of trout for each stream and sampling date. The relationship
between trout biomass and stream temperature was explored using linear
regression analysis for all 3 months of sampling (May 2006, September
2006 and June 2007). The relationship between trout density and stream
temperature was also explored with linear regression analysis for all 3 months.
These regressions were performed on untransformed data, since the test for
normality and constant variance passed. Second- and third-order polynomial regressions were also tested, but they did not significantly improve
upon the linear model (ANOVA, P > 0.05). The age of the trout was determined from a frequency histogram of trout fork lengths, where each cohort
was well defined.
Graphics were prepared using the programme C2 version 1.6.6,
SigmaPlot version 8.02 and version 9.0, Xara X version 1.0b and GIMP version 2.6.11. Statistical analysis was performed using SigmaStat version 3.1
and R version 2.14.0.
3. RESULTS
3.1. Stream temperature
The water temperature differed between streams, ranging from an annual
average of 5.3 to 9.7 C in the three cold streams (IS7, IS9 and IS11) and
from 13.3 to 21.3 C in the four warm streams (IS1, IS5, IS6 and IS8)
(Table 1). Annual temperature fluctuations were small in streams IS5, IS7
and IS8, where the average difference in summer and winter values ranged
from 1.0 to 2.4 C (Table 1). The remaining streams, IS1, IS6, IS9 and IS11,
showed larger annual temperature fluctuations, with an average temperature
difference ranging from 5.2 to 8.3 C between summer and winter values
(Table 1). During the study on brown trout, the average temperature was
8.0 C in stream IS14, 7.9 C in stream IS17 and 14.8 C in the River
Hengladalsá, based on spot measurements.
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299
3.2. Stream macrophytes
Macrophyte cover was higher in the warmer streams (Fig. 2), with the bryophyte species Fontinalis antipyretica Hedw. dominating, except in stream IS6
where filamentous green algae and the cyanobacterium Nostoc spp. were
dominant. The bryophyte species Jungermannia exsertifolia Steph. was the
dominant species in the coldest stream IS7, while in the other cold streams,
IS11 and IS9, filamentous green algae were dominant (Fig. 2). The macrophyte cover in the cold streams ranged from 12% to 20%, while in the
warmer streams it ranged from 22% to 83%. There was a significant increase
in total macrophyte cover (linear regression: y ¼ 4.409x 13.310,
F1,5 ¼ 15.246, P ¼ 0.011, r2adj ¼ 0.70) and the cover of F. antipyretica (linear
regression: y ¼ 4.643x 34.184, F1,5 ¼ 19.811, P ¼ 0.007, r2adj ¼ 0.76) with
increasing water temperature (Fig. 3).
3.3. Macroinvertebrate life cycles and growth rates
Chironomids dominated in the cold streams, where Eukiefferiella minor,
Eukiefferiella claripennis (Lundbeck 1898), Orthocladius frigidus (Zetterstedt
1838), Thienemanniella spp. and Diamesa spp. Meigen 1835 were most abundant. In the geothermal streams, R. balthica and S. vittatum were dominant
along with the chironomid taxa E. minor, E. claripennis, Orthocladius oblidens
(Walker 1856) and M. atrofasciata.
The size distribution of the chironomid head-capsule widths enabled us
to separate the chironomid larvae into four instars for most taxa, and five
instars for the trichopteran larvae, where their range increased with each
instar (Fig. 4, see tables in Appendix B). For some taxa (e.g. Thienemanniella
spp.), the separation between I and II instar was difficult based on
Figure 2 Average annual (A) and relative (B) macrophyte composition (%) for each
stream, showing the dominant taxa with the remainder in the category ‘other’.
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Figure 3 Relationship between macrophyte cover (%) and stream temperature ( C) (A)
and cover of F. antipyretica and stream temperature (B), based on average values over
1 year (September 2006 to August 2007). The equations for the regression line are
shown as well as the r2adj value and P value for the relationships. The * in (B) is placed
just above two points which fall on top of each other, so that only one point is visible.
head-width measurements. First-instar larvae of the genus Orthocladius van
der Wulp, 1874 could not be identified to species level and were therefore
excluded from the analysis. The body length of larvae overlapped between
instars and could not be used for the determination of instars (Fig. 4).
3.3.1 Eukiefferiella claripennis and Eukiefferiella minor
The life cycles of two chironomid species, E. claripennis (Lundbeck 1898)
and E. minor (Edwards 1929), which were found in all the streams sampled,
have already been described in detail (Hannesdóttir et al., 2012).
E. claripennis was univoltine in the two coldest streams and bivoltine in
the warmer ones (Hannesdóttir et al., 2012) (Table 2). The growth rate
of E. claripennis increased from an average of 0.0117 mg mg1 d1 for the
univoltine population in the two coldest streams to 0.0137 mg mg1 d1
for the winter generation of the bivoltine populations in the warmer streams
(Table 3). E. minor was bivoltine in all streams (Table 2) and was putatively
multivoltine in four out of the seven streams, three of which were warm.
The emergence pattern of E. minor was different between streams, with
emergence during the warmest period in the colder streams and continuous
emergence in one of the warm streams (as also shown in Hannesdóttir
et al., 2012). The average growth rates of the winter generations of
E. minor was higher for the populations with at least two generations per
year (0.0156 mg mg1 d1) than populations that were bivoltine
(0.0135 mg mg1 d1) (Tables 2 and 3).
Figure 4 Length (mm) against head width (mm) of six Chironomidae taxa (E. claripennis, E. minor, O. frigidus, O. oblidens, Thienemanniella spp. and
M. atrofasciata), one Simuliidae species (S. vittatum) and one Trichoptera species (P. cingulatus). Note that the scales on the x-axis for P. cingulatus are
in mm and not in mm as for the other taxa. The instars are shown for each species using Roman numerals, except for S. vittatum, which had to be assigned
to seven evenly divided groups.
Table 2 Voltinism of six Chironomidae taxa, one Simuliidae species, one Trichoptera species and one Gastropoda species for seven streams
IS7 (5.4 C)
IS9 (9.7 C)
IS6 (13.3 C)
IS1 (13.5 C)
IS5 (16.1 C)
IS8 (21.3 C)
Taxa/streams
IS11 (5.3 C)
Chironomidae
Eukiefferiella claripennis*
Univoltine
Univoltine
Bivoltine
Bivoltine
Bivoltine
Bivoltine þ
Bivoltine
Eukiefferiella minor*
Bivoltine
Bivoltine þ
Bivoltine
Bivoltine þ
Bivoltine þ
Bivoltine þ
Bivoltine
Orthocladius frigidus
Bivoltine
Bivoltine
Bivoltine
Too few
Too few
Too few
Too few
Orthocladius oblidens
Too few
Too few
Too few
Bivoltine þ
Bivoltine þ
Bivoltine þ
Too few
Thienemanniella spp.
Univoltine
Univoltine
Bivoltine
Too few
Too few
Too few
Too few
Micropsectra atrofasciata
Too few
Too few
Too few
Too few
Bivoltine þ
Bivoltine þ
Too few
Univoltine
?Univoltine
Bivoltine
Bivoltine
Bivoltine
Bivoltine
Too few
Univoltine
Univoltine
Too few
Too few
Absent
Absent
Too few
Too few
Too few
Too few
?Univoltine
Univoltine
Bivoltine
Too few
Simuliidae
Simulium vittatum
Trichoptera
Potamophylax cingulatus
Mollusca
Radix balthica
Annual average temperatures are shown beside the names of each stream. In some cases, individuals were too few or absent for the determination of life cycles. Life cycles
of species marked with an asterisk have already been described in detail (Hannesdóttir et al., 2012). A question mark refers to an uncertainty regarding the voltinism. Taxa
with at least two generations per year are referred to as ‘bivoltineþ’.
Table 3 Growth rates (mg mg1 day1) of invertebrates from seven streams
IS7 (5.4 C)
IS9 (9.7 C)
IS6 (13.3 C)
Taxa/streams
IS11 (5.3 C)
IS1 (13.5 C)
IS5 (16.1 C)
IS8 (21.3 C)
Chironomidae
Eukiefferiella claripennis
0.0123
0.0110
Too few
0.0152
0.0121
Complex
Too few
Eukiefferiella minor
0.0145
0.0164
0.0124
Complex
0.0178
0.0127
Too few
Orthocladius frigidus
Too few
0.0169
Too few
Too few
Too few
Too few
Too few
Orthocladius oblidens
Too few
Too few
Too few
Complex
Complex
Complex
Complex
Thienemanniella spp.
0.0084
0.0069
0.0104
Too few
Too few
Too few
Too few
Micropsectra atrofasciata
Too few
Too few
Too few
Too few
0.0108
0.0111
Too few
Too few
Too few
Too few
0.0124
0.0140
0.0156
Too few
Too few
0.0188
Too few
Too few
Absent
Absent
Too few
Too few
Too few
Too few
Unclear
0.0097
Unclear
Too few
Simuliidae
Simulium vittatum
Trichoptera
Potamophylax cingulatus
Mollusca
Radix balthica
Annual average temperatures are shown beside each stream name. For bivoltine species and species with at least two generations per year (see Table 2), the growth rate of
the generation extending over winter was calculated. In some cases, the number of individuals was too low for the calculation of growth rates, while the taxa were absent
from some streams. Growth rates could not be calculated in some streams due to overlapping generations (referred to as complex) or an unclear pattern in the life history
(referred to as unclear). Additionally, there were too few individuals of most taxa over winter in IS8, preventing growth rate measurements in this stream.
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3.3.2 Orthocladius frigidus
O. frigidus (Zetterstedt 1838) had the highest abundances in the three cold
streams (IS7, IS9 and IS11) and was one of the dominant species in stream
IS7, while its density was low in the warm streams. The larvae could be distinctly separated into instars II, III and IV based on their head-width measurements, the range increasing with each instar (Fig. 4; Table B1). The
body length of the instars overlapped considerably (Fig. 4).
O. frigidus was bivoltine in stream IS7, with a long winter generation
(8–9 months) and a short summer generation (3–4 months), with continuous
emergence from May to September (Fig. 5). In September, the majority of
larvae were II instar larvae, and continued to be so until April, where II and
III instar larvae dominated. From May to July, instars II to IV were present
along with pupae and pupal exuviae, with IV instar larvae representing the
highest proportion. In August, II instar larvae dominated. The life-cycle pattern of O. frigidus was similar in both summers in stream IS7. In the other
cold streams, IS9 and IS11, the life-cycle patterns resembled the one in
stream IS7: O. frigidus was thus assumed to be bivoltine in all three streams.
The growth rate of the winter generation of this species could only be calculated for stream IS7 (Table 3), because the number of individuals in the
other streams was too low.
3.3.3 Orthocladius oblidens
O. oblidens (Walker 1856) had the highest abundances in the warm streams
(IS1, IS5, IS6 and IS8), with low densities in the three cold streams (IS11, IS7
and IS9). The life cycle of this species could only be determined for individuals from the warm streams. The size of the larval head capsules showed a
good distinction between instars II, III and IV, with little overlap and the
size range increased with each instar (Fig. 4; Table B2). The body length
of larvae overlapped between instars (Fig. 4).
During most sampling months, instars II to IV were present (Fig. 6), indicating a non-seasonal life cycle with overlapping generations in the warm
streams. Emergence was over a long period, with pupae and pupal exuviae
recorded from February to August, with the highest proportion in May.
There was no emergence during winter. Determining the exact number
of generations completed in one year is difficult due to this pattern, but
we assume that the species has at least two overlapping generations per year,
perhaps due to an unsynchronized life cycle, which would explain the presence of instars II to IV in most months of sampling. This uncertainty in
determining the number of generations is expressed in Table 2, where
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305
Figure 5 Life cycle of O. frigidus in stream IS11 (annual average 5.3 C), IS7 (annual
average 5.4 C) and IS9 (annual average 9.7 C). Proportion (0–1) of each instar, labelled
by Roman numerals (II–IV), along with pupae (P) and pupal exuviae (Ex) is shown for
each month. The number of individuals (n) used in the life-cycle analysis is shown
for each month. A plus sign refers to the presence of pupae and/or pupal exuviae.
the species is described as being ‘bivoltine þ’, implying that it could have
two or more generations per year. The number of individuals in stream
IS8 was generally low through the year, making interpretations difficult.
Due to the overlapping generations of this species, the growth rates could
not be calculated (Table 3).
Figure 6 Life cycle of O. oblidens in stream IS6 (annual average 13.3 C), IS1 (annual average 13.5 C), IS5 (annual average 16.1 C) and IS8
(annual average 21.3 C). All other information as in Fig. 5.
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307
3.3.4 Micropsectra atrofasciata
M. atrofasciata was most abundant in the warmer streams, although it was
found in all the streams. It was the dominant chironomid species in the warm
stream IS1. The instars could be separated by plotting the frequency histogram of the head-capsule widths (Fig. 4; Table B3). There was an overlap in
the length between instars (Fig. 4).
M. atrofasciata has at least two generations per year in stream IS1: one
winter generation extending from late summer/autumn to May and a short
summer generation from May to August (Fig. 7). There is a possibility of
more than one generation being completed during the summer because
of continuous emergence from May to August 2007 (based on the presence
of pupae and pupal exuviae) with overlapping generations. A similar life
cycle can also be found in stream IS5. The number of individuals found
in streams IS6 and IS8 was low during winter and spring, while those in
the cold streams were low in all seasons except summer, making interpretations difficult. Growth rates for this species could only be calculated for
two warm streams, due to the low density in remaining streams (Table 3).
3.3.5 Thienemanniella spp
Thienemanniella spp. was one of the dominant taxa in the three colder streams
(IS7, IS9 and IS11). This genus could not be identified to species level, thus
more than one species could have occurred in the streams. The size distribution of the head-capsule width of Thienemanniella spp. showed three peaks
(Fig. 4; Table B4).
Thienemanniella spp. was univoltine in streams IS7 and IS11, completing
one generation per year (Fig. 8). A new generation appeared in July 2007,
overlapping with the previous generation. First/second-instar larvae were
present during the autumn, growing to III instar during the winter/early
spring, with the IV instar appearing in April. Emergence occurred during
the summer from May to August. In stream IS9, Thienemanniella spp. was
most likely bivoltine, with a long winter generation (September to May)
and a short summer generation ( June to July/August). In stream IS9, I to
II instar larvae were present from September to December, growing to
III instar larvae in February, and reaching IV instar in March. In May, IV
instar larvae were dominant and pupae and pupal exuviae were present.
In June and July, II to IV instar larvae were present, along with pupae
and pupal exuviae in July. The growth rate of Thienemanniella spp. increased
from an average of 0.0077 mg mg1 d1 for the univoltine population in the
two coldest streams (IS11 and IS7) to 0.0104 mg mg1 d1 for the winter
Figure 7 Life cycle of M. atrofasciata in stream IS6 (annual average 13.3 C), IS1 (annual average 13.5 C), IS5 (annual average 16.1 C) and IS8
(annual average 21.3 C). All other information as in Fig. 5.
Increased Stream Productivity with Warming Supports Higher Trophic Levels
309
Figure 8 Life cycle of Thienemanniella spp. in stream IS11 (annual average 5.3 C), IS7
(annual average 5.4 C) and IS9 (annual average 9.7 C). Note that instars I and II could
not be separated. All other information as in Fig. 5.
generation of the bivoltine population in stream IS9 (Table 3), which had
the highest annual average temperature of the cold streams (Table 1).
3.3.6 Simulium vittatum
S. vittatum was the dominant blackfly species in the streams at Hengill. It was
common in the warm streams (IS6, IS1, IS5 and IS8), but was found in low
abundances in the colder streams (IS11, IS7 and IS9). Simulium (Eusimulium)
aureum Fries 1824, Simulium (Nevermannia) vernum Macquart 1826 and
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Elísabet Ragna Hannesdóttir et al.
Prosimulium (Prosimulium) ursinum (Edwards 1935) were also recorded in the
colder streams in low abundances, similar to S. vittatum. The instars of
S. vittatum could not be distinguished by examining a frequency histogram
of head-capsule width (Fig. 2) and were therefore assigned to seven groups as
described above.
In stream IS11 and IS7, S. vittatum likely completed one generation per year
(Fig. 9), with few larvae found in spring and early summer, making life-cycle
analysis difficult. The larvae were small during early autumn, growing through
the winter, and emerging in August 2007 (based on the presence of prepupae
and pupae). Another generation began in July 2007, overlapping with the previous generation. In streams IS1, IS5, IS6 and IS9, S. vittatum was bivoltine,
with a long winter generation and a short summer generation, with pupae
found mostly in spring and summer. In stream IS8, few larvae were found from
December 2006 to May 2007 making life-cycle analysis difficult for this stream.
Pupae were found in September 2006, February 2007, June 2007 and August
2007. Due to the low number of individuals recorded in the cold streams, the
growth rates of the univoltine population of S. vittatum could not be calculated
and compared to the growth rates of the winter generations of the bivoltine
populations in the warm streams. The growth rates of the winter generation
of the bivoltine populations increased with increasing stream temperature in
the warm streams, with an increase from 0.0124 to 0.0156 mg mg1 d1
(Table 3).
3.3.7 Radix balthica
The snail, R. balthica, was one of the dominant species in the warmer streams,
but was found in low abundances in the cold streams. The life cycle of
R. balthica could not be described in the three cold streams (IS7, IS11 and
IS9) due to the low density of the species.
In stream IS1, R. balthica completed one generation per year, growing
from May through winter, reaching their maximum size of 9.0 mm in June,
with one generation overlapping with the previous year’s generation
(Fig. 10). In this stream, egg masses were found from May to August
2007. Small individuals were first observed in May, which had the highest
proportion of individuals of 5.5 and 6.5 mm. The highest proportion of
small individual (1.0 mm) was recorded in June, where snails of different
sizes (from 1.0 to 9.0 mm) were recorded. The life cycle of R. balthica
in stream IS6 resembled the one in stream IS1, which both differed from
IS5, where the species completed two generations per year. One generation
lasted from July to March, where the snails reached their maximum size
Figure 9 Life cycle of S. vittatum in streams IS11 (annual average 5.3 C), IS7 (annual average 5.4 C), IS9 (annual average 9.7 C), IS6 (annual
average 13.3 C), IS1 (annual average 13.5 C), IS5 (annual average 16.1 C) and IS8 (annual average 21.3 C). Proportion (0–1) of each group
(from one to seven) along with pupae (P) is shown for each month. The number of individuals (n) used in the life-cycle analysis is shown for
each month. A plus sign refers to the presence of pupae.
Figure 10 Life cycle of R. balthica from stream IS6 (annual average 13.3 C), IS1 (annual average 13.5 C), IS5 (annual average 16.1 C) and IS8
(annual average 21.3 C). Proportion (0–1) of each size group (0.5 mm intervals) is shown for each month on the y-axis. The number of individuals (n) used in the life-cycle analysis is shown for each month.
Increased Stream Productivity with Warming Supports Higher Trophic Levels
313
(6.5 mm) in March. The other generation was from April to August, where
the snails reached their maximum length (6.0 mm) in June and July. The two
generations overlapped in July and August. In stream IS8, egg masses were
found in April and June 2007. The life cycle of R. balthica could not be determined for this stream with certainty but there was evidence of overlapping
generations during most of the year. The growth rate of R. balthica could
only be calculated for one stream (Table 3).
3.3.8 Potamophylax cingulatus
Potamophylax cingulatus was the only trichopteran species recorded in the
streams at Hengill and was most abundant in the cold streams (IS7, IS11 and
IS9), with only three individuals recorded in two warm streams (IS6 and
IS8) and none in the remaining streams (IS1 and IS5). No pupae were found
in the streams, which could be due to the low density of the species. The size
distribution of the head-capsule widths enabled us to separate the larvae into
five instars (Fig. 4). The head-capsule widths ranged between 0.35 and
2.13 mm, and did not overlap. The range of head-capsule widths increased
with each instar (Fig. 4; Table B5). The body length of the larvae ranged from
1.5 to 20.0 mm and overlapped between instars (Fig. 4; Table B5).
P. cingulatus was univoltine in streams IS7 and IS11 (Fig. 11), where the
larvae hatched from eggs in July, August and September (based on the presence of I instar larvae), with the main hatch in August. The larvae grew
through to February, where only V instar larvae were found and remained
at that stage until April/May. As no larvae were recorded in May and June in
stream IS7, we assume that during this period the V instar larvae pupated and
started emerging as adults, then mated and oviposited into the stream. Flight
traps were not used in this study and therefore the exact timing of the flight
period could not be determined. The number of individuals recorded from
stream IS9 was too low for life-cycle analysis, and only a few individuals
were recorded from streams IS6 and IS8. The growth rate of the species
could only be calculated for one stream (Table 3), due to the low number
of individuals recorded in the other streams.
In the cold streams, 29.6% of taxa included in the life-cycle analysis were
univoltine, 29.6% were bivoltine, 3.7% had at least two generations per year
and the rest (37.0%) could not be determined due to the low density of
individuals recorded in the streams (Table 2). In the warm streams, 5.9%
of taxa were univoltine, 50.0% were bivoltine (i.e. 23.5% bivoltine and
26.5% with at least two generations per year) and the rest (44.1%) could
not be determined.
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Figure 11 Life cycle of P. cingulatus in stream IS11 (annual average 5.3 C) and stream
IS7 (annual average 5.4 C). The five larval instars are shown using Roman numerals from
I to V. The Proportion (0–1) of each larval stage is expressed on the y-axis. The number of
individuals (n) in each month is shown.
3.4. Macroinvertebrate growth rate, biomass and production
There was a significant linear relationship between geometric mean growth
rate of macroinvertebrates and average annual stream temperature (linear
regression: y ¼ 0.0002396x þ 0.009758, F1,4 ¼ 12.05, P ¼ 0.026, r2adj ¼ 0.69;
Fig. 12). The chironomid Thienemanniella spp. in stream IS7 had the slowest
Increased Stream Productivity with Warming Supports Higher Trophic Levels
315
Figure 12 Geometric mean growth rate of macroinvertebrates (mg mg1 d1) plotted
against annual average stream temperature ( C). Species for which growth rate could
only be calculated in one stream (and so at one temperature) were excluded from the
calculation of mean growth rate. The equation for the regression line is shown as well as
the r2adj value and P value for the relationship.
growth rate (0.0069 mg mg1 day1; Table 3). The trichopteran P. cingulatus
in stream IS7 had the fastest growth rate (0.0188 mg mg1 day1; Table 3),
but this species was excluded from the calculation of geometric mean growth
rate because its growth was only documented in one stream (R. balthica and
O. frigidus were excluded for the same reason).
The average annual standing biomass of the major macroinvertebrate
taxa was higher in the warmer streams than in the cold ones (Fig. 13).
The snail R. balthica contributed most to the total biomass in all streams,
up to 96%, except in the cold stream IS7, where chironomid larvae dominated. Simuliid larval biomass contributed from 3% to 16% of the total and
had higher biomasses in the warm streams. The caddisfly species P. cingulatus,
which was mostly restricted to the cold streams, contributed up to 36% of
the total biomass in one of the cold streams. The total biomass and the biomass of R. balthica increased significantly with increasing temperature (linear
regression for total biomass: log10(y) ¼ 0.08797x þ 2.35831, F1,5 ¼ 35.93,
P ¼ 0.002, r2adj ¼ 0.85, Fig. 14A; R. balthica: log10(y) ¼ 0.2011x þ 0.44791,
F1,5 ¼ 10.59, P ¼ 0.023, r2adj ¼ 0.62, Fig. 14B). There was also a significant
increase in macroinvertebrate biomass (log10 transformed) with an increase
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Figure 13 Average annual standing biomass (dry weight mg m2) (A) and relative biomass (%) (B) of major invertebrate taxa for each stream.
Figure 14 Relationship between log10 invertebrate biomass (mg m2) and temperature
(A) and log10 biomass of R. balthica and temperature (B), based on average annual
values. The equations for the regression line are shown as well as the r2adj value and
P value for the relationships.
in percentage macrophyte cover (linear regression: log10(y) ¼
0.016467x þ 2.763153, F1,5 ¼ 19.32, P ¼ 0.007, r2adj ¼ 0.75; Fig. 15).
Finally, there was a significant increase in secondary production (log10 transformed) with increasing stream temperature (linear regression: log10(y) ¼
0.08920x þ 2.93308, F1,4 ¼ 11.85, P ¼ 0.026, r2adj ¼ 0.68; Fig. 16).
3.5. Brown trout biomass
The trout population in the streams was composed of 0þ, 1 þ and 2 þ year
classes, based on the length measurements. The maximum size of the
trout that were caught by electrofishing ranged from 17.0 to 24.7 cm
in the streams. There was a significant linear relationship between density
of trout and stream temperature in May 2006 (linear regression:
Increased Stream Productivity with Warming Supports Higher Trophic Levels
317
Figure 15 Relationship between invertebrate biomass (mg m2) in log10 scale and
macrophyte cover (%), based on average annual values. The equation for the regression
line is shown as well as the r2adj value and P value for the relationship.
Figure 16 Relationship between log10 of secondary production (mg m2 yr1) and
stream temperature ( C). The equation for the regression line is shown as well as the
r2adj value and P value for the relationship.
y ¼ 0.08880x 0.72347, F1,4 ¼ 15.92, P ¼ 0.016, r2adj ¼ 0.75), but not in
September 2006 (P ¼ 0.095) or June 2007 (P ¼ 0.059). There was a significant increase in the biomass of brown trout with increasing water temperature in May 2006 (linear regression: y ¼ 2.4315 22.6284, F1,4 ¼ 8.42,
318
Elísabet Ragna Hannesdóttir et al.
Figure 17 Relationship between trout biomass (g m2) and water temperature ( C) in
May 2006. The temperature values are the monthly averages for three streams (IS1, IS5
and IS8) and spot measurements for streams IS14 and IS17 and the River Hengladalsá.
The equation for the regression line is shown as well as the r2adj value and P value for the
relationship. The * is placed just above two points which fall on top of each other, so that
only one point is visible.
P ¼ 0.044, r2adj ¼ 0.60, Fig. 17), but the relationship was non-significant in
September 2006 (P ¼ 0.198) and June 2007 (P ¼ 0.094).
The responses of each major trophic group to increasing temperature, as
observed in this study, are summarised in Fig. 18. This includes (1) the greater
percentage cover of macrophytes; (2) the increased voltinism, growth rate,
biomass and production of macroinvertebrates; and (3) the greater biomass
of brown trout with increasing temperature. A key to the hypothesis tested
in each case and the related figures in the chapter is also provided.
4. DISCUSSION
The data presented here demonstrate the impacts of higher temperature on multiple trophic levels in a geothermally heated stream system in
Iceland (Fig. 18). Macrophyte cover increased significantly with warming,
providing more habitat structure and edible resources for grazing
macroinvertebrates. Life-cycle analysis revealed that macroinvertebrates
grew faster in the warmer streams and completed more generations per year,
resulting in greater biomass and secondary production. This increase in
Increased Stream Productivity with Warming Supports Higher Trophic Levels
319
Figure 18 Conceptual figure highlighting the main findings of the study. The general
response to temperature for key characteristics of three major trophic groups are provided: fish, macroinvertebrates and basal resources (ordered by trophic height in the
figure). The hypotheses tested in each case are listed, mapping onto the numbers provided at the end of the introduction. A list of figures relating to each observed trend is
also shown. Line drawings adapted from images on Wikimedia Commons.
resource availability supported a greater biomass of the apex trout predator in
the warmest streams. These results highlight the possibility for resourcedriven dynamics to challenge the more typical expectations of metabolic
theory (Brown et al., 2004; West et al., 2003) and temperature-size rules
(Angilletta et al., 2004; Atkinson, 1994; James, 1970) in the face of environmental warming. These findings also lend credence to recent theoretical
models, which suggest that these rules may be modulated by competition
and other biotic interactions in natural systems (Reuman et al., 2013).
4.1. Hengill as a model system
Geothermal streams are often perceived as unique habitats with a distinct
invertebrate community (Brock and Brock, 1966; Lamberti and Resh,
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Elísabet Ragna Hannesdóttir et al.
1983, 1985; Ólafsson et al., 2010). Yet, the streams found at Hengill in Iceland are unaffected by the high concentrations of chemicals more often associated with other geothermal systems, and they contain many species more
typical of the general European (and to a lesser extent N. American) biota
(Friberg et al., 2009; O’Gorman et al., 2012). Thus, the comparison of the
ecology of the freshwater streams of different temperatures at Hengill provides a tool for projecting future global warming trends at high latitudes
(Christensen et al., 2007), as well as providing useful sentinel systems for
inferring future change in more temperate regions (Woodward et al.,
2010b). The data presented in this chapter give an insight into the potential
changes in life histories of invertebrates following global warming, along
with information on changes in different trophic levels as temperature
increases. Thus, studies such as this one are critically important because they
give insight into vulnerable ecosystems in a changing world, and they complement the array of correlational, experimental and modelling approaches
that are increasingly being brought to bear to address climate change in multispecies systems ( Jeppesen et al., 2012; Ledger et al., 2013; Meerhoff et al.,
2012; O’Gorman et al., 2012; Peck et al., 2012; Stewart et al., 2013).
It should be noted that the communities in the warm streams have likely
adapted to these temperatures as a new equilibrium over evolutionary time,
so short-term warming of a previously cold stream could lead to different
(transient) patterns than we see in this study. A whole-stream warming
experiment currently underway at Hengill will test this potential disparity
in future studies (see O’Gorman et al., 2012), as it is important to gain a
clearer understanding of the rates at which ecological versus physical change
operate and to be able to better identify the point at which transient dynamics shift into a new equilibrium state as the climate changes (Stewart
et al., 2013).
4.2. Stream macrophytes
In the warmer streams, the macrophyte cover was higher than in the cold
streams, as predicted by our first hypothesis (Figs. 2 and 3). This increase
in basal resource is also supported by some previous work in the system,
which shows that epilithic diatoms decrease in prevalence with increasing
temperature (O’Gorman et al., 2012) as the system switches to one dominated by macrophytes in the warmer streams (Gudmundsdottir et al.,
2011). The reduction in epilithic diatom biomass may be driven by increased
grazing pressure from R. balthica (O’Gorman et al., 2012), which becomes
Increased Stream Productivity with Warming Supports Higher Trophic Levels
321
more abundant with increasing temperature (Figs. 13 and 14B), or through
increased shading from the more widespread cover of macrophytes. The net
effect is an overall increase in the gross primary productivity of the streams
(Demars et al., 2011), implying more resources to support higher trophic
levels (Fig. 15). While grazing macroinvertebrates such as R. balthica are
unlikely to feed directly on macrophytes, they will graze heavily on their
associated epiphytes (Brönmark, 1985; Lodge, 1986; Underwood and
Thomas, 1990). Data on the biomass of epiphytes in the streams are not currently available, however, so the exact proportion of edible primary producers remains unknown at present.
The increased macrophyte cover with warming also provides threedimensional habitat in these otherwise shallow, two-dimensional streams,
creating more colonisable space and shelter from water flow (Gregg and
Rose, 1982; Taniguchi et al., 2003; Thomaz et al., 2008) and predation pressure ( Jacobsen et al., 1997; Padial et al., 2009; Rantala et al., 2004; Roca
et al., 1993). The bryophyte species F. antipyretica accounted for the majority
of the macrophytes recorded in the warmer streams. A higher biomass of
aquatic bryophytes can result in a higher density of invertebrates (Lee and
Hershey, 2000; Stefansson et al., 2006), with some species of Fontinalis previously shown to harbour enormous numbers of epiphytic fauna (Brusven
et al., 1990; Maurer and Brusven, 1983). Bryophytes not only provide additional substrate for invertebrates, but also a surface for the growth of epiphytic algae, which may create positive feedback for primary productivity
(although negative effects through shading of macrophytes by epiphytes
are also possible; Asaeda et al., 2004; Köhler et al., 2010). Epiphytes on bryophytes are also an important dietary source for grazing invertebrates (Lee and
Hershey, 2000; Tall et al., 2006a,b), contributing to increased secondary
productivity. The epiphytic fauna on bryophytes and higher plants could
account for a considerable proportion of the algal community of the warm
streams, but additional research is necessary to verify this.
F. antipyretica has been found to thrive in environments with elevated
CO2 concentrations (Maberly, 1985). Ecosystem respiration has been
shown to increase with increasing temperature in Hengill (Perkins et al.,
2012), with the warm streams shown to be net sources of CO2 (Demars
et al., 2011). Thus, the elevated levels of CO2 in the warm streams may also
favour bryophyte dominance at warmer temperatures. Experimental manipulation of macrophyte cover and quantification of associated epiphytes
across the temperature gradient at Hengill may help to identify the relative
contribution of edible resource versus three-dimensional habitat structure to
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Elísabet Ragna Hannesdóttir et al.
higher trophic-level processes. For example, artificial plants could be added
to reaches in cold streams, with removal of large macrophyte patches in
reaches of warm streams to address the bottom-up mechanism driving the
observed increase in macroinvertebrate biomass (Fig. 14A).
4.3. Macroinvertebrate life cycles and growth rates
Detailed ‘natural experiment’ and manipulative field studies on
macroinvertebrate life cycles under different temperature regimes are critical
to our understanding of future climate-change impacts on freshwater ecosystems if we are to identify early warning indicators of climate change, yet
there is a paucity of such studies (but see Hogg and Williams, 1996). To date,
in high-latitude systems, most emphasis has been placed on the dominant
families in rivers and lakes, namely, Chironomidae (Lindegaard and
Jonasson, 1979; Stefánsson, 2005) and Simuliidae (Gı́slason, 1985;
Gı́slason and Gardarsson, 1988; Gı́slason and Jóhannsson, 1991).
Lindegaard (1992) gave a good account of the life cycles of many invertebrates found in Lake Thingvallavatn. Other studies have focused on the life
cycle of gastropods (Snorrason, 2000) and caddis flies (Gı́slason, 1978a,b,
1992, 1993; Gı́slason and Sigfússon, 1987; Gislason et al., 1990). As such,
the current study provides valuable information on macroinvertebrate life
cycles not only from the point of view of warming impacts but also as baseline data for vulnerable sub-Arctic ecosystems, in general (Christensen
et al., 2007).
The average growth rate of macroinvertebrates was higher with increasing temperature (Fig. 12), resulting in the completion of more generations
per year in the warm streams (Table 2). For the four taxa, E. claripennis,
E. minor, Thienemanniella spp. and S. vittatum, for which voltinism and
growth rates could be calculated over all or part of the temperature gradient,
related patterns between these two properties could be determined (Tables 2
and 3). The univoltine populations of E. claripennis and Thienemanniella spp.
in the two coldest streams grew slower than the winter generation of the
bivoltine populations in the warmer streams. The growth rate of the winter
generation of S. vittatum in the warm streams was faster with increasing temperature. For E. minor, the populations with at least two generations per year
(in the warm streams) grew faster than ones that had just two generations per
year (in the cold streams). These findings support our second hypothesis,
which proposed that individual taxa would grow faster and complete more
generations per year in streams with higher water temperatures. For the
Increased Stream Productivity with Warming Supports Higher Trophic Levels
323
remaining taxa, the link between voltinism and growth rates was hard to
establish due to insufficient data resulting from the very low abundances
in these nutrient-poor systems.
Faster growth and development rates also had implications for adult
emergence from the aquatic ecosystem. For the chironomids and simuliids,
the timing of emergence differed between streams, where emergence was
mostly limited to spring and summer in the cold streams. The period of
emergence was longer for some taxa in the warm streams, with some taxa
emerging even in winter. This also supports our second hypothesis, which
proposed that timing of emergence would change with increasing temperature of the streams, with earlier emergence and lasting over a longer period.
Earlier emergence may have important consequences for adult survival rate
if air temperatures prove to be lethal (Nebeker, 1971), particularly in geothermal stream systems such as Hengill, where the in-stream water temperature does not necessarily reflect that of the surrounding terrestrial
environment. Alternatively, if the adult phase is equipped to deal with
low air temperatures, the increased productivity of these geothermal streams
may provide an important source of energy to the terrestrial system during
the harshest period of the year. Indeed, some invertebrate species are tolerant
of freezing temperatures, such as the chironomid species Diamesa mendotae
(Bouchard et al., 2006). Future insights into the interplay between the terrestrial and aquatic environments in geothermal ecosystems would be a valuable addition to our understanding of such dynamics, especially for attempts
at describing bioclimatic envelopes for predicting future range shifts of entire
populations across all life stages.
Many of the life-cycle patterns shown for chironomids in this study are
supported by, or help to, shed light on previous research from Iceland.
E. claripennis is bivoltine in River Dælisá in SW Iceland, but is predicted
to be univoltine in some years due to the late emergence of the first generation (Stefánsson, 2005). The shift from univoltine to bivoltine life history
with increasing temperature in this species at Hengill suggests that the
response at River Dælisá may be driven by inter-annual variation in temperature (Table 2; Hannesdóttir et al., 2012). E. minor can be bivoltine or have
two flight periods per year in many rivers and lakes in Iceland (Gardarsson
et al., 2000; Gislason et al., 1995; Jonsson et al., 1986; Lindegaard, 1992;
Stefánsson, 2005). Its bivoltine nature across the temperature gradient at
Hengill (see Table 2) suggests that major changes in life history are unlikely
with warming, although differences in emergence pattern were observed
between streams and multivoltine populations may have occurred
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Elísabet Ragna Hannesdóttir et al.
(Hannesdóttir et al., 2012). The chironomid species O. frigidus was bivoltine
in the cold streams at Hengill in accordance with other studies from Iceland
(Lindegaard, 1992). O. oblidens is bivoltine, with summer emergence in the
littoral zone of Lake Thingvallavatn (Lindegaard, 1992), as in the warm
streams at Hengill. However, the number of flight periods for O. oblidens
varies from one to two in River Laxá, NE Iceland, demonstrating spatial
and temporal variation (Gislason et al., 1995). Thienemanniella sp. cf. morose
has two generations per year (Lindegaard, 1992) in Lake Thingvallavatn,
while in River Dælisá Thienemanniella sp. is univoltine (Stefánsson, 2005).
This reflects the flexible voltinism of Thienemanniella spp. in the cold streams
at Hengill (see Table 2). Micropsectra spp. has two generations per year in Lake
Thingvallavatn (Lindegaard, 1992) as in the warmer streams in Hengill. In
River Laxá, however, M. atrofasciata showed a temporal and spatial variation
in flight periods, with up to two flight periods per year (Gislason et al., 1995).
Several studies from Iceland suggest the potential for increased productivity or temperature change to alter the life history of naturally occurring
species. Studies in River Laxá have shown that S. vittatum can differ in
the number of generations completed in 1 year within the same river
(Gı́slason and Jóhannsson, 1991). A part of the population of S. vittatum
was bivoltine close to the outlet of Lake Mývatn (Gı́slason and
Jóhannsson, 1991), while further downstream, the species completed just
one generation per year, where drifting food was less abundant than at
the outlet (Gı́slason and Jóhannsson, 1991). These variations in voltinism
are thought to be related to resource availability, with larvae closer to the
lake outlet receiving more food compared to the downstream sites
(Gı́slason and Jóhannsson, 1991), reflecting the change from bivoltine in
the warmer streams at Hengill to univoltine in the less productive cold
streams (see Table 2; Figs. 2 and 16). R. balthica was univoltine in two of
the warm streams but bivoltine in a warmer stream. Warming of approximately 10 C above ambient temperature during summer in Lake
Thingvallavatn, due to warm effluents from a nearby geothermal power
plant, seemed to benefit R. balthica, with higher survival rate and a shorter
life cycle, where the snails managed to reproduce after 1 year instead of the
2-year semelparous life cycle typical in the cooler lake waters (Lindegaard,
1992; Snorrason, 2000; Snorrason et al., 2011).
The only Trichoptera species recorded in the streams at Hengill was
P. cingulatus, which completed one generation per year, reflecting the broad
life-history patterns in Iceland reported by Gı́slason (1977, 1992). In a previous study at Hengill, adult P. cingulatus were caught in a flight trap placed
Increased Stream Productivity with Warming Supports Higher Trophic Levels
325
by stream IS7 (Fig. 1), from mid-June to early September in 2002 (Ólafsson
et al., 2010). Otto (1971) found that P. cingulatus had a 1-year life cycle in a
small stream in south Sweden, but with a later estimated flight period than in
Hengill. Only a few P. cingulatus larvae were recorded in two warm streams
over the whole sampling period and since the species has never been
recorded from geothermal streams before, even though the species was
extensively studied from 1974 to 1978 (Gı́slason, 1977, 1981), these individuals seem unlikely to represent a viable population.
4.4. Macroinvertebrate biomass and production
The faster growth rate of macroinvertebrates (see Fig. 12) most likely contributed to the observed higher biomass of macroinvertebrates with increasing stream temperature (Figs. 13 and 14). Previous studies have also
demonstrated a reduction in the time required for growth and development
of freshwater insect larvae with warming (Hogg and Williams, 1996;
Konstantinov, 1958a), suggesting that this may be a highly predictable
response within normal thermal limits (Oliver, 1971). A faster growth rate
may also imply a smaller size at maturity, as predicted by temperature-size
theory (Atkinson, 1994; Daufresne et al., 2009) and demonstrated in previous research (Hogg and Williams, 1996; Konstantinov, 1958b). However,
there is equivocal evidence for the expected temperature-size response in
Hengill, with many macroinvertebrate species increasing in size with
warming or showing no response (O’Gorman et al., 2012), suggesting that
temperature is not the sole factor contributing to our results. Consumer–
resource dynamics may play an important role in our understanding of these
exceptions to temperature-size rules in natural systems and require further
exploration of warming impacts on body size.
The net effect of faster growth rates and higher macroinvertebrate biomasses with rising stream temperature was an overall increase in secondary
production in the system (Fig. 16), supporting our third hypothesis. Secondary production is the rate of generation of heterotrophic biomass, driven by
the transfer of organic matter between trophic levels (Benke, 1984) and is
recognised as a means of quantifying the influence of stream-dwelling invertebrates on ecosystem processes, with significant influences on nutrient
cycling, organic matter processing and energy flow through food webs
(Benke and Wallace, 1980; Fisher and Gray, 1983). Changes in basal
resources can alter secondary production dramatically (Wallace et al.,
1997), and there is a clear indication that increased availability of
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Elísabet Ragna Hannesdóttir et al.
macrophytic food and habitat led to an increase in macroinvertebrate biomass, and thus secondary production, in the Hengill system (Fig. 15). These
bottom-up effects have previously been linked to an increase in maximum
food-chain length ( Jenkins et al., 1992) and may ultimately play a key role in
sustaining the populations of brown trout in the warmer streams.
4.5. Brown trout biomass
There was an increase in the biomass of trout in the warmer streams
(Fig. 17), in contrast to our fourth hypothesis, suggesting that it is mediated
by increases in both primary and secondary production with warming (see
Fig. 18). Invertebrate production can limit the recruitment of brown trout
(Einarsson et al., 2006), whereas they can attain a large body size in rivers
where production of benthic invertebrates is high (Steingrı́msson and
Gı́slason, 2002). The trout at Hengill fed mainly on the dominant invertebrate taxa, namely, chironomids in the colder streams and R. balthica and
S. vittatum in the warmer streams (O’Gorman et al., 2012; Woodward
et al., 2010b). Previous research on the diet of trout from Icelandic rivers
suggests that Chironomidae decrease in prevalence with increasing fish size,
while R. balthica becomes a more important component of the diet
(Steingrı́msson and Gı́slason, 2002). The average body mass of trout at
Hengill increases with warming (O’Gorman et al., 2012), in contrast to
some other systems ( Jonsson et al., 1991), suggesting that this shift in diet
with stream temperature may also partly be a product of optimal predator–
prey body-mass ratios (Petchey et al., 2008), that is, the larger gape of bigger
trout allows them to feed more optimally on snails, which provide more
energy per capita than the much smaller chironomids. Larger individuals have
higher energy demands under warming (Gillooly et al., 2001; West et al.,
2003), so a plentiful prey supply in the warm streams is crucial to the persistence of trout. Intriguingly, aquarium experiments on brown trout have
shown that when food is plentiful, warming can present benefits that outweigh the extra metabolic costs (Elliott, 1975a,b), that is, high-energy
demands can be met, allowing the trout to grow more rapidly and reach sexual maturity at a younger age. Additionally, the increased macrophyte cover
with increasing temperature may have offered trout greater protection from
predators, such as the duck species goosander (Mergus merganser), which has
been observed on the River Hengladalsá during the study period, and the
American mink (Mustela vison), which is found in the vicinity of Hengill
although it was not seen in the locality during the study. We expect
Increased Stream Productivity with Warming Supports Higher Trophic Levels
327
predation pressure to be low, therefore, but further work is required to
confirm this.
There is compelling evidence that bottom-up control plays a key role in
driving many of the dynamics observed under warming in the Hengill system. The macrophyte cover was low in the cold streams, reflected in the low
biomass and production of macroinvertebrates. Trout were rare and small in
the cold streams, despite the thermal regime falling well within the temperature tolerance of the species (Jonsson and Jonsson, 2011). In contrast, trout
were larger (see O’Gorman et al., 2012) and much more abundant in the
warm streams, where they had more readily available resources among
macroinvertebrate prey (Figs. 13 and 14) to sustain their metabolic demands.
This suggests that the Hengill system is resource driven, but the influence of
top-down control is likely to increase in tandem, as larger trout consume a
greater amount of prey. This raises the question whether observed effects in
the warmer streams are due to temperature and/or the influence of these
large apex predators, which are orders of magnitude larger than the next biggest predators, such as V instar P. cingulatus, Clinocera stagnalis (Haliday 1833),
Dicranota sp. Zetterstedt 1838 or Muscidae (O’Gorman et al., 2012). This
highlights the difficulty in separating out bottom-up and top-down effects
in aquatic ecosystems (Hillebrand, 2002; Hunter and Price, 1992; Terborgh,
1988; Wilson, 1987), which can really only be achieved through manipulative field experiments.
5. CONCLUSION
According to this study, invertebrates that can tolerate an increase in
temperature with climate warming may grow faster and complete more generations per year, while the pattern of emergence may also change. Shifts in
the timing of life-cycle events can cause a mismatch with other trophic levels
(Giménez, 2011; Thackeray et al., 2010), which could lessen the overlap in
the temporal distribution of consumers and resources resulting in phenological uncoupling of links in the food web (Giménez, 2011; Thackeray et al.,
2010). Invertebrates emerging in winter could face unfavourable conditions
(Nebeker, 1971), including cold air temperatures and low primary production (O’Gorman et al., 2012). This could lead to higher mortality rates, with
food a limiting resource. Species intolerant of climate warming are likely to
disappear, or move further north or to higher elevations (Chen et al., 2011;
Colwell et al., 2008; Hickling et al., 2006; Parmesan et al., 1999). As most
species are limited to a narrow temperature range, climate warming will
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Elísabet Ragna Hannesdóttir et al.
result in major changes in macroinvertebrate assemblages. The dominant
species that remain may reach considerable levels of biomass, supporting
increased secondary production and higher trophic levels. But the loss of
native diversity will likely have detrimental impacts on overall levels of ecosystem functioning (Balvanera et al., 2006; Cardinale et al., 2006), as well as
reducing the resilience of the community to further environmental or
anthropogenic disturbances (Montoya et al., 2006; Yachi and Loreau, 1999).
ACKNOWLEDGEMENTS
Our gratitude goes to Aron D. Jónasson, Brynjar R. Ómarsson, Guðni Guðbergsson, Hafsteinn
B. Einarsson, Haukur Hauksson, Helinja Ruiter, Hlynur Bárðarsson, Kristinn Ó. Kristinsson,
Leó A. Guðmundsson, Nikolai Friberg, Ólafur P. Jónsson, Ragnhildur Friðriksdóttir, Svala
Jónsdóttir, Sæmundur A. Halldórsson and Viktor B. Pálsson for field and/or laboratory
assistance. Thanks to Rakel Gudmundsdóttir for joint fieldwork and collaboration in the
Eurolimpacs project. Thanks to staff and students of the Institute of Freshwater Fisheries and
of the Institute of Life and Environmental Sciences. Our appreciation goes to Professor
Leonard C. Ferrington Jr. and The Chironomidae Research Group at the University of
Minnesota. Thanks to Samsýn ehf for providing maps of the research area. And thanks to
Francois Edwards and an anonymous referee for improving the chapter. The municipality of
Ölfus is thanked for permitting research in the Hengill area. Research grants from the
European Union (Eurolimpacs project GOCECT-2003-505540), the Icelandic Centre for
Research (Icelandic Research Fund for Graduate Students no. 60230006), the University of
Iceland Research Fund, the University of Iceland Assistantship Grant, the International
Student Exchange Programs (ISEP) and the UK’s Natural Environmental Research Council
(NERC grant NE/I009280/1) are gratefully acknowledged.
APPENDIX A. LENGTH–WEIGHT RELATIONSHIPS
USED TO ESTIMATE DRY MASS
OF MACROINVERTEBRATES
Length–dry mass regression equations were used when estimating the
standing crop biomass of major invertebrate taxa, both from the literature
(for chironomids and trichopteran larvae) and determined from Hengill
(for simuliid larvae and R. balthica). Simuliid larvae and R. balthica were collected with a kick net in July 2009 from all the streams. Individuals were
picked from the samples and kept refrigerated and aerated until measurements were made on live specimens over the days following sampling.
The shell length of R. balthica and total body length of S. vittatum larvae were
measured and sorted into size classes. Measurements for R. balthica were performed to the nearest 0.5 mm and for S. vittatum to the nearest 1.0 mm. Glass
vials were dried in an oven for 1 h at 60 C and cooled in a desiccator before
they were individually weighed on a Mettler Toledo classic scale with
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Increased Stream Productivity with Warming Supports Higher Trophic Levels
0.1 mg precision. The invertebrates were placed in the vials, the larger ones
individually and the smallest ones in groups of 5–20 to make measurements
possible. The specimens were then dried in an oven for 24 h at 60 C and
cooled in a desiccator before weighing. The dry weight was calculated using
the formula: dry weight ¼ dry weight (sample) dry weight (vial). The relationship between size and mass was determined with a power equation,
W ¼ aLb, where W ¼ individual mass, L ¼ shell length for R. balthica and
body length for S. vittatum, a ¼ a constant and b ¼ the slope of the regression
(Table A1). The size range of R. balthica was from 1.5 to 11.5 mm and for
S. vittatum from 1.0 to 6.0 mm.
Table A1 Length–weight (L–W) regression equations both from the literature and
determined in this study
Taxa
Dim.
Refs.
L–W relationship
Chironomidae
BL
Benke et al. (1999)
y ¼ 0.0018x2.617
Limnephilidae
BL
Benke et al. (1999)
y ¼ 0.0040x2.933
Radix balthica
BL
Determined
y ¼ 0.1002x2.6575
(R2 ¼ 0.9583, N ¼ 303)
Simuliidae
BL
Determined
y ¼ 0.0025x3.0676
(R2 ¼ 0.9174, N ¼ 76)
The dimension measured was body length for chironomid, simuliid and trichopteran larvae and shell
length for R. balthica, measured in mm. The weight was dry weight measured in mg. The coefficient
of determination (R2) is shown for L–W relationships established at Hengill.
APPENDIX B. HEAD-WIDTH MEASUREMENTS FOR
INSTAR SEPARATION IN EACH STREAM
Table B1 Head-width (mm) range (Min., Max.), average (Av.), standard deviation (Stdev.)
and number of individuals measured (n) for O. frigidus in streams IS11, IS7 and IS9 for
instars II to IV
Head width (mm)
n
Av.
II
119
124
III
51
IV
33
Stdev.
Min.
Max.
9
101
162
224
18
172
263
408
28
344
476
IS11
330
Elísabet Ragna Hannesdóttir et al.
IS7
II
417
124
8
101
162
III
293
232
19
172
284
IV
385
418
32
304
537
II
42
120
11
91
152
III
41
224
18
182
273
IV
76
408
33
334
506
IS9
Table B2 Head-width (mm) range (Min., Max.), average (Av.), standard deviation (Stdev.)
and number of individuals measured (n) for O. oblidens in streams IS6, IS1, IS5, IS8 for
instars II to IV
Head width (mm)
n
Av.
II
100
114
III
183
IV
Stdev.
Min.
Max.
7
101
132
196
14
152
243
235
337
20
263
405
II
152
111
9
91
122
III
251
195
13
162
243
IV
225
337
23
263
405
II
99
108
8
91
132
III
165
188
13
152
223
IV
123
327
17
263
375
II
106
118
7
101
142
III
179
202
11
172
233
IV
33
340
27
263
385
IS6
IS1
IS5
IS8
331
Increased Stream Productivity with Warming Supports Higher Trophic Levels
Table B3 Head-width (mm) range (Min., Max.), average (Av.), standard deviation (Stdev.)
and number of individuals measured (n) for M. atrofasciata in all the streams for
each instar
Head width (mm)
n
Av.
Stdev.
Min.
Max.
IS11
I
13
63
4
61
71
II
57
105
8
91
132
III
24
170
11
142
192
IV
34
267
10
253
294
I
3
61
0
61
61
II
17
105
8
91
122
III
27
165
13
132
192
IV
32
278
17
243
304
I
10
65
5
61
71
II
44
100
6
81
111
III
35
165
12
142
203
IV
17
264
7
253
273
I
31
66
5
61
71
II
207
103
6
81
122
III
248
163
8
142
182
IV
177
253
13
223
294
I
26
63
5
51
71
II
438
100
6
81
111
III
593
162
9
122
192
IV
306
256
14
213
304
IS7
IS9
IS6
IS1
332
Elísabet Ragna Hannesdóttir et al.
IS5
I
4
63
5
61
71
II
61
101
8
81
122
III
128
163
8
132
182
IV
173
264
13
223
294
I
18
64
5
61
71
II
112
103
7
91
111
III
106
163
9
142
203
IV
22
258
14
223
273
IS8
Table B4 Head-width (mm) range (Min., Max.), average (Av.), standard deviation (Stdev.)
and number of individuals measured (n) for Thienemanniella spp. in streams IS11, IS7
and IS9 for each instar, where instars I and II are shown together, as they could not be
separated based on head-width measurements
Head width (mm)
n
Av.
Stdev.
Min.
Max.
IS11
I–II
200
73
6
51
81
III
221
113
7
91
132
IV
230
175
11
142
253
I–II
210
75
6
51
81
III
248
113
8
91
132
IV
319
177
10
142
253
I–II
174
71
6
51
81
III
105
111
9
91
132
IV
310
173
8
152
223
IS7
IS9
333
Increased Stream Productivity with Warming Supports Higher Trophic Levels
Table B5 Head-width (mm) and body-length (mm) range (Min., Max.), average (Av.),
standard deviation (Stdev.) and number of individuals measured (n) for P. cingulatus in
stream IS7 for each instar
n
Av.
Stdev.
Min.
Max.
Head width (mm)
I
62
0.398
0.015
0.350
0.425
II
92
0.605
0.031
0.500
0.675
III
39
0.946
0.057
0.800
1.050
IV
23
1.412
0.090
1.250
1.550
V
22
1.870
0.102
1.675
2.025
Body length (mm)
I
57
2.8
0.5
1.5
3.5
II
78
4.9
0.7
3.5
6.5
III
31
7.0
1.2
4.5
8.5
IV
18
10.3
1.8
6.0
13.5
V
18
15.0
3.3
9.0
20.0
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