Environmental control of emergence patterns: Case study of changes in hourly and daily emergence of...

RESEARCH ARTICLE

Environmental control of emergence patterns:Case study of changes in hourly and dailyemergence of aquatic insects at constantand variable water temperatures

Marija Ivković1*, Marko Miliša1*, Ana Previšić1, Aleksandar Popijač2,3 and Zlatko Mihaljević1

1 Faculty of Science, Division of Biology, Department of Zoology, University of Zagreb, Zagreb, Croatia2Oikon Ltd., Institute for Applied Ecology, Zagreb, Croatia3Geonatura Ltd., Zagreb, Croatia

The aim of this study was to determine which environmental factors influence emergence ofinsects at two contrasting habitats: one with constant and onewith variable water temperature.We hypothesized that emergence of holometabolous insects is triggered bywater temperaturewhere temperature variations occur, while light is the main stimulus for emergence at site withconstant water temperature. We expected that for the emergence of hemimetabolous insects,some additional environmental stimuli might be required. We also expected weatherconditions to be more important at sites that lack variations in water temperature. To test ourhypotheses we placed six pyramid-type emergence traps at the two sites. Emergent aquaticinsects were collected at 8-h intervals over a 13-day period, during peak emergence formost ofthe target species. Most taxa emerged during the afternoon at both sites. Only Hydropsychesaxonica/instabilis emerged nocturnally. At the site with constant water temperature,emergence of Drusus croaticus was stimulated by length of sunlight period. Emergence ofProtonemura auberti was promoted by higher air temperature and humidity of the day before.Brachyptera tristis emerged in higher numbers when humidity and cloudiness were high thepreceding day. At site with variable water temperature, an increase in water temperature, witha threshold at 16°C, was a significant factor for the emergence of Hemerodromia unilineata.This study gives new insight into the complexity of relationships between aquatic insectemergence patterns and environmental drivers, and show that light and weather conditionstrigger emergence of most insects under constant water temperature conditions, whiletemperature is a dominant trigger at variable water temperature habitat.

Received: May 3, 2012Revised: January 22, 2013Accepted: March 7, 2013

Keywords:Diptera / Plecoptera / Spring / Sunlight / Trichoptera / Weather signals

1 Introduction

The importance of understanding insect emergencepatterns lies in the fact that emergence is a prime link

between aquatic and terrestrial ecosystems and theemerged adults are an important food resource for manyterrestrial animals [1, 2]. Photoperiod and water tempera-ture are generally considered as the most influentialemergence stimuli [3–7]. Longer photoperiod accelerateslarval development and therefore emergence starts earlierthan under normal light conditions [6, 8]. Photoperiodicregulation of emergence has been documented for somestoneflies (Plecoptera), caddisflies (Trichoptera), andsome Diptera [5, 8–10]. It can be an especially important

Handling Editor: Saulyegul Avlyush

Correspondence: Dr. Marija Ivković, Faculty of Science, Divisionof Biology, Department of Zoology, University of Zagreb,Rooseveltov trg 6, HR-10000 Zagreb, CroatiaE-mail: [email protected]: þ385-1-4826260 *These two authors contributed equally to this work.

International Review of Hydrobiology 2013, 98, 104–115 DOI 10.1002/iroh.201301483

© 2013 WILEY‐VCH Verlag GmbH & Co. KGaA, Weinheim 104

emergence trigger in habitats with a constant temperatureregime, such as springs [5, 6].

An increase in water temperature (where it occurs)induces the emergence of many groups of insects [6, 11].Laboratory studies have shown that altered water temper-atures can induce premature or delayed emergence [6,12]. These findings are corroborated in natural environ-ments where emergence occurs earlier in abnormallywarm years and later in cold years [6, 13–16]. Manyadditional environmental factors influence dynamics ofinsect emergence on daily basis, but detailed studies onthese factors are lacking.

An important issue for emergence is the difference in lifehistories and reception of different environmental stimulibetween holometabolous and hemimetabolous insects.The former, presumably, cannot perceive some of theoutside conditions due to submersed pupating stage, whilethe latter are able to explore outside conditions prior toemergence [5, 17]. This aspect is especially important inhabitats where water temperature is less variable andother environmental stimuli must therefore trigger theemergence.

The present study examines, on a daily basis, theemergence patterns of various groups of aquatic insects attwo sites with different water temperature regimes. Themain objective of this study was to determine whichenvironmental parameters are the most influential stimulifor daily insect emergence and if this varies depending ontemperature regime.

Our main hypotheses regarding holometabolousinsects is that water temperature is the key stimulus foremergence in a variable water temperature habitat, whilelight intensity is the main stimulus for emergence in aconstant water temperature habitat. For hemimetabolousinsects, some additional stimuli, such as humidity orchanges in air temperature may be required. We expectweather conditions to be more important at sites that lackvariations in water temperature.

2 Materials and methods

2.1 Study site

The study was carried out at Plitvice Lakes National Park,located in the karst region of the Dinarid Mountains,Croatia. The Plitvice Lakes system consists of 16oligotrophic, dimictic and fluvial lakes divided by tufabarriers (tufa is a porous calcium carbonate deposit thatdevelops in carbonate-supersaturatedwater, where calcitecrystals are deposited on immersed objects) [18–20]. Thestreams Bijela rijeka and Crna rijeka form the Matica River,which is the main surface-water source of the lakes. Twosampling sites were selected to attain two different settings

in terms of water temperature regime. The first samplingsite was at the spring of Bijela rijeka (constant watertemperature) and the second site at the tufa barrierLabudovac (variable water temperature; Fig. 1). The springreach is open while a dense riparian canopy characterizesthe tufa barrier. Annual physical and chemical character-istics of the water at the sampling sites are given in Table 1.

2.2 Sampling protocol

At each site, six pyramid-type emergence traps wereinstalled during the 13-day sampling period (from May 21,until June 3, 2008). This period of the year was selected forthe study because most insects emerge at that time [21–23]. The traps were placed in a manner that ensuresrepresentative sampling of emergence from all the micro-habitats present at the respective site (Table 1). Each trapwas a 50 cm tall, four-sided pyramid with a base of45 cm � 45 cm, fastened to the streambed in a way thatallowed free movement of larvae in and out of the samplingarea. The side frames of the traps were covered with 1 mmmesh netting. A collection container filled with preservative(2% formaldehyde with detergent) was placed at thetip of each trap. Containers were emptied at 8-h interval(intervals were from 6 to 14 h, 14 to 22 h, and 22 to6 h) over 13 days. Emerged insects collected from allemergence traps during 8-h intervals, at each site, werepooled. Specimens were preserved in 80% ethanol.

Insects were identified to the lowest feasible taxonomiclevel based on Malicky [24] for caddisflies; Kaćanski andZwick [25], Kis [26], and Graf and Schmidt-Kloiber [27]for stoneflies; Bauernfeind and Humpesch [28] formayflies; Nilsson [29] for identification of dipteran families;Collin [30] for the dipteran family Empididae; Knoz [31] forthe dipteran family Simuliidae; Krek [32] for the dipteranfamily Psychodidae; Roskošný and Gregor [33] for thedipteran family Muscidae, and Kuhnt [34] for identificationto beetle families. The dipteran family Chironomidae andbeetle family Scirtidae were not identified to the speciesbecause of insufficient identification keys and taxonomistsfor those groups.

Caddisflies species Hydropsyche saxonica McLachlanand Hydropsyche instabilis (Curtis) were pooled (taxonH. saxonica/instabilis) for the analyses, as the females ofthese species could not be distinguished.

Environmental variables analyzed in this study werewater temperature, air temperature, humidity, precipitation,cloudiness, hours of sunlight, and discharge. Environmen-tal data were collected simultaneously with the emergencesampling. HOBO Pendant Temperature Data Logger(Part UA-001-XX, Bourne, Massachusetts, USA) mea-sured water temperature. Air temperature and humiditywere measured using a Digi-tech 4 – LD1558 radiocontrolled weather station. Data on other parameters used

International Review of Hydrobiology 2013, 98, 104–115 Changes in daily emergence of aquatic insects


in statistical analyses, such as precipitation, cloudiness,discharge, and hours of sunlight, were obtained from theMeteorological and Hydrological Institute of Croatia.Moon phase data were taken from Annual AstronomicalMagazine [35].

2.3 Statistical methods

The influence of environmental variables on insectemergence was evaluated for two separate data sets: atthe 8-h interval (n ¼ 38) and the daily (n ¼ 12) level.Analyses were carried out comparing numbers of emergedspecimens at a given sampling time with the environmentaldata recorded at the beginning of the respectiveemergence interval. Only taxa representing 1% or more

of the total catch in emergence traps were taken intoconsideration. To detect differences in insect emergencerelated to the time of day, analysis of variance (ANOVA)was used with the post hoc Tukey HSD test.

Multiple regression was used to explore the relationshipbetween the environmental predictors and emergence ofeach taxon. Multiple regression was carried out separatelyfor the available 8-h environmental measurements and forall environmental data expressed as daily mean values.Water temperature was omitted from the predictor list atthe spring site since there was virtually no variability of thisfactor during the study (Table 1). For the 8-h periodanalyses, humidity, air temperature, and discharge weretested as environmental predictors against the emergenceat both sites; water temperature was tested only at tufa

Figure 1. Study area in the Plitvice Lakes National Park, Croatia.

M. Ivković et al. International Review of Hydrobiology 2013, 98, 104–115

106 © 2013 WILEY‐VCH Verlag GmbH & Co. KGaA, Weinheim

barrier. For daily analyses, all available environmentalpredictors, were tested against the emergence at bothsites. Variance inflation factor (VIF) for all the environmen-tal predictors were lower than 10, so no multicollinearitywas established. All the data were log-transformed andanalyses were carried out using Statistica (version 8.0,Statsoft, Inc., Tulsa, Oklahoma, USA).

Canonical correspondence analysis (CCA) was used toordinate emergence of all taxa in respect to all availableenvironmental variables using the daily data set. Thisordination method was applied to analyze communitypatterns that could not be uncovered with multipleregression. CCA was conducted using CANOCO (Canocofor Windows, version 4.02, GLW-CPRO, Wageningen,The Netherlands). All data were log-transformed and rarespecies were down-weighted. The statistical significanceof the relationship between all species and all variableswas tested using theMonte Carlo permutation test with 999permutations. In total CCA analysis was performed on fivetaxa (Protonemura auberti, Brachyptera tristis, Drususcroaticus, Berdeniella sp. nov., and Chironomidae) andseven environmental variables (air temperature, humidity,discharge, moon phase, hours of sunlight, precipitation,and cloudiness) for the constant water temperature site.For the variable water temperature site CCA analysiswas performed on seven taxa (Protonemura intricata,H. saxonica/instabilis, Rhyacophila tristis, Hemerodromiaunilineata, Simulium angustipes, Chironomidae, andScirtidae) and eight environmental variables (water andair temperature, humidity, discharge, moon phase, hoursof sunlight, precipitation, and cloudiness).

We have not considered our sampling as replicatedover time since the nature of emergence process isdistinctly peaking. In addition, each sampling event duringthe day is distinct by its time of day so they cannot beregarded as replicates. On the other hand short-termapproach and only two sites may seemingly yield to fewdata. We believe that this problem cannot be tackledappropriately since similar habitats that would carry thesame environmental conditions during the same time inemergence progression of same species are not available.

3 Results

During the study period, we recorded specimens belongingto six different insect orders (Ephemeroptera, Plecoptera,Trichoptera, Diptera, Coleoptera, and Hymenoptera). Intotal, 34 species belonging to the orders Ephemeroptera,Plecoptera, and Trichoptera were identified. Specimens ofthe orders Diptera and Coleoptera were identified only tothe family level, with the exception of dipteran familiesEmpididae, Simuliidae, Psychodidae, andMuscidae, whichwere identified to the species and genus level (Table 2).

Five taxa met the 1% of catch criterion at the spring siteand were analyzed further: B. tristis (Klapálek), P. aubertiIllies, D. croaticus Marinković-Gospodnetić, Berdeniellasp. nov., and Chironomidae. At the tufa barrier seven taxamet the criterion: P. intricata (Ris), H. saxonica/instabilis,R. tristis Pictet, Hemerodromia unilineata Zetterstedt,Simulium (Eusimulium) angustipes Edwards, Chironomi-dae, and Scirtidae.

Table 1. Characterization of the sampling sites

Site Spring Tufa barrier

Latitude N 44°5000500 N 44°5201700

Longitude E 15°3304300 E 15°3505900

Altitude (m) 720 630Substrate Pebbles and sand (50%),

moss (30%), macrophytes (20%)Pebbles (15%), moss on tufa (50%),

tufa with detritus (35%)Water temperature (°C) Min 7.4 2.5

Max 7.8 20.5O2 (mg L�1) Min 7.6 6.7

Max 11.8 12.3O2 (%) Min 65.2 59.7

Max 101.8 139.2pH Min 6.9 6.8

Max 7.8 8.7Conductivity (µS cm�1) Min 463 366

Max 505 426Alkalinity (mg L�1 CaCO3) Min 235 210

Max 295 260

Annual ranges are given.



3.1 Constant water temperature site

No taxa exhibited nocturnal emergence; the majorityemerged during afternoon and during morning (Fig. 2).

One-way ANOVA showed that the emergence ofP. auberti,D. croaticus, and Chironomidae differed significantly inrespect to time of day (F ¼ 17.471, p < 0.001; F ¼ 7.780,p ¼ 0.001; F ¼ 3.608, p ¼ 0.037, respectively; N ¼ 38

Table 2. Total number of emerged individuals per taxon collected during the study

Taxon Spring Tufa barrier

EphemeropteraLeptophlebiidae Paraleptophlebia submarginata (Stephens, 1835) 2Ephemeridae Ephemera danica (Müller, 1764) 5

PlecopteraTaeniopterygidae Brachyptera tristis (Klapálek, 1901)a) 9Nemouridae Nemoura cinerea (Retzius, 1783) 3

Nemurella pictetii (Klapálek, 1900) 3 2Protonemura auberti (Illies, 1954)a) 91Protonemura intricata (Ris, 1902)a) 15

Leuctridae Leuctra nigra (Olivier, 1811) 1Perlodidae Isoperla inermis [25] 5

TrichopteraRhyacophilidae Rhyacophila dorsalis plitvicensis (Kučinić & Malicky, 2002) 3

Rhyacophila tristis (Pictet, 1834)a) 21Glossosomatidae Synagapetus krawanyi (Ulmer, 1938) 2Philopotamidae Philopotamus variegatus (Scopoli 1763) 1Hydropsychidae Hydropsyche instabilis (Curtis, 1834) <<a),b) 4

Hydropsyche saxonica (McLachlan, 1884) <<a),b) 72Hydropsyche saxonica/instabilis ,,a),b) 77

Polycentropodidae Polycentropus flavomaculatus (Pictet, 1834) 5Psychomyiidae Lype reducta (Hagen, 1868) 3

Tinodes dives (Pictet, 1834) 6Limnephilidae Drusus croaticus (Marinković-Gospodnetić, 1971)a) 60

Limnephilus lunatus (Curtis 1834) 1Limnephilus rhombicus (Linneaus, 1758) 1Potamophylax nigricornis (Pictet, 1834) 3Micropterna sequax (McLachlan, 1875) 1

Goeridae Lithax niger (Hagen, 1859) 1Silo pallipes (Fabricus, 1781) 1

Sericostomatidae Notidobia ciliaris (Linneaus, 1761) 3Beraeidae Beraeamyia schmidi (Botosaneanu 1960) 1

DipteraPedicidae 3Psychodidae Berdeniella sp. nov.a) 8

Pericoma sp. 4Dixidae 4Simuliidae Simulium (Eusimulium) angustipes (Edwards 1915)a) 15Chironomidaea) 620 392Empididae Chelifera precabunda [30] 1

Chelifera stigmatica (Schiner 1862) 2Hemerodromia unilineata (Zetterstedt, 1842)a) 126Clinocera stagnalis (Haliday, 1833) 1

Muscidae Limnophora sp. 2Coleoptera Scirtidaea) 14Hymenoptera 1

a) Taxa that amounted to more than 1% of total catch.b)Hydropsyche species were analyzed cumulatively.



df. ¼ 2). TheHSDpost hoc test showed that the emergenceof P. auberti was significantly higher during late day thanduring the night. The same trend was observed inChironomidae. Emergence of D. croaticus was significantlylower during night compared to both daylight periods.

Multiple regression analysis of taxa emergence againstthe available 8-h period environmental measurementsuncovered significant positive relationship between emer-gence of P. auberti and air temperature. Multiple regres-

sion on pooled daily emergence against daily means of allenvironmental data showed negative relationships be-tween amount of sunlight per day andmoon phase with theemergence of Berdeniella sp. nov. Conversely, the sameenvironmental parameters were positive stimuli for emer-gence of D. croaticus. Additionally, precipitation positivelyaffected the emergence of B. tristis (Table 3).

The eigenvalues for the two CCA axes (Fig. 3) were0.061 and 0.040, p (all axes) ¼ 0.02 and they explained

Figure 2. Emergence dynamics with respect to time of day and weather conditions at constant water temperature siteduring the study period. (a) Brachyptera tristis and Berdeniella sp. nov. (b) Protonemura auberti and Drusus croaticus(c) Chironomidae.



71% of the of species–environment relation. Axis 1 washighly correlated with cloudiness (R ¼ �0.734) and axis 2with discharge (R ¼ 0.732). P. auberti and B. tristisemerged in higher numbers during periods of higherdischarge, higher humidity, greater cloudiness, and rain onthe previous day. D. croaticus emerged in higher numberswhen there were more hours of sunlight. Berdeniella sp.nov. and Chironomidae showed no strong relationship withany of the tested environmental variable.

3.2 Variable water temperature site

Water temperature range during the study period variedbetween 11.9 and 17.6°C. Mean day–night variation inwater temperature was 1.0°C (variation range 0.1–2.3°C).

Most taxa emerged in the afternoon and in the morning,with the exception of H. saxonica/instabilis. Emergence ofH. saxonica/instabilis, H. unilineata, and Chironomidaevaried significantly with respect to time of day categories(F ¼ 4.677, p ¼ 0.015; F ¼ 5.959, p ¼ 0.005; F ¼ 6.626,

p ¼ 0.003, respectively; N ¼ 39, d.f. ¼ 2). The HSD testshowed that the emergence of H. saxonica/instabilis is thehighest during night and the lowest during the late day. Theopposite pattern was found for the emergence of H.unilineata, as emergence was significantly lower duringnight than during both day periods. Chironomidaepreferentially emerged during daylight periods (Fig. 4).

According to the multiple regression in the 8-h intervalmeasurements, humidity positively affected emergence ofH. unilineata. Multiple regression on pooled daily dataproduced statistically significant relationships only foremergence of H. unilineata. Increasing water and airtemperature positively stimulate H. unilineata emergence(Table 3). Moreover, we found that emergence ofH. unilineata only began if water temperature was above16°C, and increased rapidly after that threshold (Fig. 4).

The eigenvalues for the two CCA axes (Fig. 5) were0.138 and 0.079, p (all axes) ¼ 0.001, and explained79.6% of the species–environment relation. Axis 1 washighly correlated with moon phase (R ¼ 0.935) and water

Table 3. Multiple regression results

Spring Tufa barrier

P.auberti

B.tristis

D.croaticus CHI

Berdeniellasp. nov.

P.intricata

H.sax/ins

R.tristis

H.unilineata

S.angustipes CHI SCI

8-h-intervalsWater T b �0.17 �0.05 0.16 0.46 �0.28 0.01 0.03

p 0.744 0.917 0.741 0.235 0.581 0.988 0.951Air T b 0.59 0.22 �0.14 0.45 �0.09 0.42 �0.63 0.01 0.51 0.47 0.28 �0.34

p 0.036 0.421 0.633 0.116 0.767 0.242 0.069 0.987 0.063 0.18 0.428 0.308Discharge b 0.3 0.25 0.31 0.21 �0.3 �0.27 �0.21 0.48 �0.25 0.18 �0.16 �0.49

p 0.098 0.181 0.103 0.264 0.118 0.458 0.54 0.167 0.36 0.603 0.641 0.15Humidity b 0.31 0.33 �0.37 0.16 0.06 0.32 �0.68 �0.29 0.58 0.05 0.06 �0.17

p 0.271 0.246 0.204 0.587 0.838 0.373 0.053 0.387 0.033 0.888 0.854 0.608Daily means

Water T b �1.3 0.19 �0.23 1.19 2.29 0.53 �0.93p 0.513 0.941 0.882 0.025 0.436 0.784 0.516

Air T b �0.09 �0.95 0.36 0.75 0.16 �0.84 �1.33 �0.64 �0.88 �0.57 �0.81 �1.78p 0.912 0.172 0.429 0.35 0.774 0.501 0.44 0.524 0.016 0.746 0.513 0.11

Discharge b 0.21 0.18 0.27 0.21 �0.69 �0.75 �0.16 0.59 �0.4 1.29 0.22 �1.09p 0.656 0.633 0.334 0.648 0.092 0.452 0.901 0.461 0.067 0.384 0.816 0.179

Humidity b 0.74 �0.66 1.04 0.43 �0.45 �3.06 �1.7 �0.21 �0.17 0.81 �1.19 �0.35p 0.558 0.51 0.184 0.724 0.615 0.129 0.458 0.873 0.536 0.729 0.477 0.76

Sun b 0.37 0.17 2.1 �0.98 �1.54 0.58 0.01 0.6 �0.08 �1.38 1.02 �0.41p 0.635 0.783 0.007 0.235 0.04 0.527 0.992 0.428 0.607 0.329 0.301 0.532

Cloudiness b �0.92 �0.11 �1.07 �1.43 1.13 2.65 0.49 �0.16 0.26 �1.14 1.43 �1.14p 0.518 0.92 0.213 0.32 0.287 0.149 0.81 0.897 0.332 0.607 0.374 0.331

Precipitation b �0.84 1.76 �0.65 �0.66 0.91 2.65 0.49 �0.48 0.34 �1.01 1.14 1.01p 0.299 0.033 0.175 0.388 0.141 0.091 0.762 0.619 0.148 0.563 0.367 0.284

Moon b 1.99 �1.37 3.07 1.55 �2.83 �3.31 �0.96 �0.12 �0.64 1.28 �1.1 �2.54p 0.198 0.247 0.013 0.283 0.036 0.18 0.734 0.943 0.128 0.674 0.603 0.16

Bold numbers are statistically significant.CHI, Chironomidae; H. sax/ins, Hydropsyche saxonica/instabilis; SCI, Scirtidae.



temperature (R ¼ �0.890) and axis 2 with humidity(R ¼ 0.458). H. unilineata emerged in higher numberswhen water temperature is higher. H. saxonica/instabilisemerged in higher numbers when humidity was higher,and water and air temperatures were lower. The Black flyS. angustipes emerged in higher numbers when dischargewas higher and Scirtidae emerged in higher numbers whenthere were more hours of sunlight. R. tristis and P. intricataand Chironomidae showed no preference to any one ofthe tested stimuli.

4 Discussion

4.1 Constant water temperature site

Our results concerning weather preferences for emer-gence of the stoneflies P. auberti and B. tristis (i.e., cloud

cover and precipitation with consequent higher humidity,discharge, and air temperature as main signals for theiremergence) confirm previous studies [5, 17]. In addition,emergence of P. auberti on sunny days, but only when thespring was not receiving direct illumination, is in accor-dance with findings of Riederer [36], supporting ourhypothesis that stoneflies depend on weather signals foremergence. Moreover, Riederer [36] reported that thestonefly P. intricata emerges during the day, when nighttemperatures are too low and humidity is high enoughduring the day for successful emergence. Similar temper-ature and humidity conditions (cold nights and sufficientday humidity at Plitvice Lakes) could be plausible reasonsfor the daytime emergence of P. auberti in our study.

In temperate and tropical regions, most caddisfliesemerge at night [37, 38] while in arctic regions emergenceonly occurs during the day [39].D. croaticus is a cold-waterstenotherm [40] and its diurnal activity, in some way, mustbe a response to environmental variables. In arcticstreams, one of the primary factors triggering emergenceis light intensity [39]. The same might be true in constantwater temperature habitats, such as springs. Additionally,Malicky [10] reported that some caddisfly species of thesame genus exhibited a high degree of photoperiodicdependence, under relatively constant water temper-atures. Even though the study did not measure the lightintensity directly, but rather the duration of clear skies anddaily duration of sunlight, it can be reasonably assumedthat the main stimulus for emergence ofD. croaticus is lightintensity. Emergence ofBerdeniella sp. nov. subsequent tofewer hours of sunlight was likely caused by the generalpreference of Psychodidae for higher humidity and lack ofdirect sunlight [32].

Most springtime Chironomidae emerged during thebrightest part of the day [41–44] which is consistent withour study. Emergence of Chironomidae during theinvestigated period was not significantly related to anyof the other environmental variables studied, in line with thestudy by Siqueira et al. [45]. In absence of fluctuation inwater temperature, sunlight regime could be the mainstimulus responsible for differences in emergence ofholometabolous aquatic insects, whereas for hemimetab-olous insects, air temperature and humidity play animportant role in emergence.

4.2 Variable water temperature site

Stimuli for emergence of H. unilineata have not previouslybeen reported. In our study, emergence began afteraveragewater temperature of the day before exceeded 16°C, hence, it might be regarded as the threshold tempera-ture for emergence of this species [4, 46].

At the tufa barrier, H. saxonica/instabilis emergedmostly at night, corresponding to other reports of

Figure 3. CCA ordination of the six most abundant taxaand selected environmental variables at constant watertemperature site. Air Tem, air temperature; Dis, discharge;Moon, moon phase; Prec, precipitation; Hum, humidity;Cloud, cloudiness; Sun, hours of sunlight.



nocturnal emergence of caddisflies in temperate re-gion [37, 38]. Additionally, water temperature has beenstipulated as the most important trigger for caddisflyemergence [47–49]. We did not observe water tempera-ture as an important stimulus. However, our results maybe tentative because of the nocturnal emergence regime.During the night water temperature drops up to 2.3°C andthis may have obscured the importance of temperature

for emergence in statistical analyses (temperature rangeduring our study was 5.7°C). To confirm temperature asthe most important trigger when nocturnal emergenceoccurs a laboratory experiment sensu Tobias [49] shouldbe implemented.

To our knowledge, there are no previous reports of dailystimuli for emergence of S. angustipes and familyScirtidae, but we cannot derive firm conclusions on

Figure 4. Emergence dynamics with respect to time of day and weather conditions at variable water temperature site duringthe study period. (a) Rhyacophila tristis, Simulium angustipes, Protonemura intricata, and Scirtidae (b) Hydropsychesaxonica/instabilis and Hemerodromia unilineata (c) Chironomidae.



emergence stimuli for these species due to very lownumbers of collected specimens. Chironomidae emergedwith similar patterns as they do at water temperatureconstant site.

The only hemimetabolous species analyzed at thevariablewater temperature site was the stoneflyP. intricata,which emerged during the day, in line with the findingsof Riederer [36]. Low temperatures probably preventnocturnal and early morning emergence and sufficientday humidity allows it during the day.

At the variable water temperature site, emergencepatterns of some holometabolous taxa showed a strongrelationship with water temperature. High seasonalfluctuations of water temperature are typical for this habitattype [22]. Thus, the key importance of water temperatureas an environmental driver of insect emergence in sucha habitat is not surprising [5, 6]. However, stonefliesexhibited similar emergence patterns at both sitesindependent on variability in water temperature, suggest-ing that the same environmental factors, including airtemperature and humidity, stimulate emergence of thesehemimetabolous insects, though this needs to be con-firmed in future studies.

Aquatic insect species collected at constant andvariable water temperature sites exhibited differentemergence patterns due to the different environmental

conditions at each site. Composition and structure ofaquatic insect communities generally differ considerably inhabitats with marked differences in key environmentalfactors (e.g., [50]). Thus, direct comparison of environ-mental factors influencing aquatic insects’ emergencebetween two selected habitat types is not possible.However, this study has provided new insight into thecomplexity and diversity of relationships between aquaticinsect emergence patterns and intraday environmentalinfluences in habitats differentiated by their water temper-ature regime.

We would like to thank Prof. Dr. Mladen Kerovec forfinancial support. We are more than grateful to MiljenkoIvković for collecting the majority of samples, as withouthim, this study would not have been possible.We sincerelythank Vlatka Mičetić for identifying collected Coleoptera.We thank Dr. Jan Ježek for confirming our identifications ofPsychodidae. We thank Dr. Adrian Plant on his helpfulcomments on English style. We are grateful to the PlitviceLakes National Park authorities for their permission toconduct field sampling. We thank the Meteorological andHydrological Institute of Croatia for providing meteorologi-cal and hydrological data. This study was supported by theCroatian Ministry of Science, Education and Sports asa part of project No. 119-1193080-3076: Invertebratetaxonomy, ecology and biogeography of Croatian aquaticecotones.

5 References

[1] Nakano, S., Murakami, M., Reciprocal subsidies: Dynamicinterdependence between terrestrial and aquatic foodwebs. Proc. Natl. Acad. Sci. USA 2001, 98, 166–170.

[2] Power, M. E., Rainey, W. E., Food webs and resourcesheds: Towards spatially delimiting trophic interactions, in:Hutchings, M. J., John, M. J., Stewart, A. J. A. (Eds.), TheEcological Consequences of Environmental Heterogeneity,Blackwell Science, Malden 2000, 291–314.

[3] Corbet, P. S., Temporal patterns of emergence in aquaticinsects. Can. Entomol. 1964, 96, 264–279.

[4] Hynes, H. B. N., The Ecology of Running Waters, LiverpoolUniversity Press, Liverpool 1972.

[5] Hynes, H. B. N., Biology of Plecoptera. Annu. Rev. Entomol.1976, 21, 135–153.

[6] Sweeney, B. H., Factors influencing life-history patterns ofaquatic insects, in: Resh, V. H. Rosenberg, D. M. (Eds.), TheEcology of Aquatic Insects, Praeger Scientific, New York1984, 56–100.

[7] Tauber, M. J., Tauber, C. A., Natural daylengths regulateinsect seasonality by two mechanisms. Nature 1975, 258,711–712.

[8] Nebeker, A. V., Effect of water temperature on nymphalfeeding rate, emergence, and adult longevity of thestonefly Pteronarcys dorata. J. Kans. Entomol. Soc.1971, 44, 21–26.

Figure 5. CCA ordination of the seven most abundanttaxa and selected environmental variables at variablewater temperature site. Water Tem, water temperature; AirTem, air temperature; Dis, discharge; Moon, moon phase;Prec, precipitation; Hum, humidity; Cloud, cloudiness; Sun,hours of sunlight.



[9] Danks, H. V., Life history and biology of Einfeldia synchrona(Diptera: Chrironomidae). Can. Entomol. 1971, 103, 1597–1606.

[10] Malicky, H., Artificial illumination of a Mountain Streamin Lower Austria: Effect of constant daylength on thephenology of the Caddisflies (Trichoptera). Aquat. Insects1981, 3, 25–32.

[11] Beck, S. D., Insect Photoperiodism, 2nd edn., AcademicPress, New York 1980.

[12] Sweeney, B. H., Vannote, R. L., Ephemerella mayflies ofWhite Clay Creek: Bioenergetic and ecological relationshipamong six coexisting species.Ecology 1981, 62, 1353–1369.

[13] Gledhill, T., The Ephemeroptera, Plecoptera and Trichopteracaught by emergence traps in two streams during 1958.Hydrobiologia 1960, 15, 179–188.

[14] Illies, J., Emergenz 1969 im Breitenbach. Schlitzer pro-duktionsbiologische Studien (1). Arch. Hydrobiol. 1971, 69,14–59.

[15] Langford, T. E., The emergence of insects from a British riverwarmed by power station cooling-water. PART II. Theemergence patterns of some species of Ephemeroptera,Trichoptera and Megaloptera in relation to water temperatureand river flow, upstreamand downstream of the coolingwateroutfalls. Hydrobiologia 1975, 47, 91–133.

[16] Wagner, R., Gathmann, O., Long-term studies on aquaticDance Flies (Diptera, Empididae) 1983–1993: Distributionand size patterns along the stream, abundance changesbetween years and the influence of environmental factors onthe community. Arch. Hydrobiol. 1996, 137, 385–410.

[17] Komatsu, T., Studies on the ecology of the snow-insects II.Relation between the seasonal and annual occurrence of thesnow-stoneflies (Plecoptera) and the environmental con-ditions. Jap. J. Ecol. 1972, 22, 134–140.

[18] Chafetz, H. S., Folk, R. L., Travertines: Depositionalmorphology and bacterially constructed constituent. J.Sediment. Petrol. 1984, 54, 289–316.

[19] Miliša, M., Matoničkin Kepčija, R., Radanović, I., Ostojić, A.,Habdija, I., The impact of aquatic macrophyte (Salix sp. andCladium mariscus (L.) Pohl.) removal on habitat conditionsand macroinvertebrates of tufa barriers (Plitvice Lakes,Croatia). Hydrobiologia 2006, 573, 183–197.

[20] Riding, R., Classification of microbial carbonates. in: Riding,R. (Ed.), Calcareous Algae and Stromatolites, Springer-Verlag, Berlin 1991, 21–51.

[21] Ivković, M., Mičetić Stanković, V., Mihaljević, Z., Emergencepatterns and microhabitat preference of aquatic dance flies(Empididae; Clinocerinae and Hemerodromiinae) on alongitudinal gradient of barrage lake system. Limnologica2012, 42, 43–49.

[22] Previšić, A., Kerovec, M., Kučinić, M., Emergence andcomposition of Trichoptera from karst habitats, PlitviceLakes region, Croatia. Int. Rev. Hydrobiol. 2007, 92, 61–83.

[23] Popijač, A., Sivec, I., Diversity and distribution of stoneflies inthe area of Plitvice Lakes National Park and along theMediterranean river Cetina (Croatia), in: Staniczek A. H.(Ed.), Proceedings of the 12th International Conference onEphemeroptera and the 16th International Symposiumon Plecoptera, International Perspectives in Mayfly andStonefly Research, Stuttgart 2008. Aqua. Insects 31, 2009,731–742.

[24] Malicky, H., Atlas of European Trichoptera, Springer,Dordrecht 2004.

[25] Kaćanski, D., Zwick, P., Neue und wenig bekanntePlecopteren aus Jugoslawien. Mitt. Schweiz Entomol. Ges.1970, 43, 1–16.

[26] Kis, B., Plecoptera, Fauna Republicii Socialiste România,Insecta Volumul VIII Fascicula 7, Editura Academiei Repub-licii Socialiste România, Bucureşti 1974.

[27] Graf, W., Schmidt-Kloiber, A., Plecoptera – Steinfliegen,Skriptum zum Spezialpraktikum Plecoptera, Anleitung zurBestimmung für Fortgeschrittene, Institut für Hydrobiologieund Gewässermanagement, BOKU, Wien 2003.

[28] Bauernfeind, E., Humpesch, U., Die Eintagsfliegen Zentra-leuropas (Insecta: Ephemeroptera), Bestimmung und Öko-logie, Verlag des Naturhistorischen Museums Wien, Wien2001.

[29] Nilsson, A., Aquatic Insects of North Europe, A TaxonomicHandbook, Volume 2, Odonata, Diptera, Apollo Books,Stenstrup 1997.

[30] Collin, J. E., British Flies, Empididae: Empidinae (Part) andHemerodrominae. Part III, At the University Press, Cam-bridge 1961.

[31] Knoz, J., To Identification of Czechoslovakian Black-flies (Dipter, Simuliidae). Folia Přírodovědecké FaklutyUniversity J.E. Purkyně v Brně. Biologia 1965, 5, 1–54;þ425 Abb.

[32] Krek, S., Psychodidae (Diptera, Insecta) Balkanskog Poluo-toka, Fedreracija Bosne i Hercegovine, Ministarstvo Obra-zovanja, Nauke, Kulture i Sporta, Studentska ŠtamparijaUniverziteta Sarajevo, Sarajevo 1999.

[33] Roskošný, R., Gregor, F., Insecta: Diptera: Muscidae.Süßwasserfauna vonMitteleuropa 21/29, Elsevier, SpectrumAkademischer Verlag, Heidelberg 2004,

[34] Kuhnt, P., Illustrierte Bestimmungs-Tabellen der KäferDeutschlands, E. Schweizerbart’sche Verlagsbuchhand-lung, Stuttgart 1913.

[35] Hržina, D., Bolid, Astronomical Yearbook for the Year 2008,Kerschoffset, Zagreb 2007 (in Croatian).

[36] Riederer, R. A. A., Emergence behaviour of somemayflies and stoneflies (Insects: Ephemeroptera andPlecoptera). Verh. Int. Ver. Theor. Angew. Limnol. 1985,22, 3260–3264.

[37] Jackson, J. K., Swarming and longevity of selected adultaquatic insects from a Sonoran Desert Stream. Am. Midl.Nat. 1988, 119, 344–352.

[38] Morgan, N. C., Waddell, A. B., Diurnal variation in theemergence of some aquatic insects. J. R. Entomol. Soc.London 1961, 113, 123–137.

[39] Baryshev, I. A., Diurnal dynamics of emergence of Caddisflies Agapetus ochripes curt and Hydroptila tineoides Dalm.in the Far North (InderaRiver, Kola Peninsula, Russia).Russ.J. Ecol. 2008, 39, 379–381.

[40] Previšić, A., Walton, C., Kučinić, M., Mitrikeski, P. T.,Kerovec, M., Pleistocene divergence of Dinaric Drususendemics (Trichoptera, Limnephilidae) in multiple micro-refugia within the Balkan Peninsula. Mol. Ecol. 2009, 18,634–647.

[41] Jacobsen, O. W., Feeding behaviour of breeding WigeonAnas penelope in relation to seasonal emergence andswarming behaviour of Chironomids. Ardea 1991, 79, 409–418.

[42] Oliver, D. R., Life history of the Chironomidae. Annu. Rev.Entomol. 1971, 16, 211–229.



[43] Pinder, A. M., Trayler, K. M., Mercer, J. M., Arena, J.,Davis, J. A., Diel periodicities of adult emergence of someChironomids (Diptera: Chironomidae) and a mayfly (Ephem-eroptera: Caenidae) at a western Australian wetland. J. Aust.Entomol. Soc. 1993, 32, 129–135.

[44] Wartinbee, D. C., Diel emergence patterns of lotic Chirono-midae. Freshwater Biol. 1979, 9, 147–156.

[45] Siqueira, T., de Oliveira Roque, F., Trivinho-Strixino, S.,Phenological patterns of neotropical lotic chironomids: Isemergence constrained by environmental factors? Aust.Ecol. 2008, 33, 902–910.

[46] Macan, T. T., Maudsley, R., The temperature of a MoorlandFishpond. Hydrobiologia 1966, 27, 1–22.

[47] Fey, J. M., Die Aufheizung eines Mittelgebirgsflusses undihre Auswirkungen auf die Zoozönose – dargestellt an derLenne (Sauerland). Arch. Hydrobiol. (Suppl) 1977, 53, 307–363.

[48] Hogg, I. D., Williams, D. D., Response of stream inverte-brates to a global-warming thermal regime: An ecosystem-level manipulation. Ecology 1996, 77, 395–407.

[49] Tobias, W., Zur Schlüpfrhytmik von Köcherfliegen (Trichop-tera). Oikos 1967, 18, 55–75.

[50] Moog, O., Fauna Aquatica Austriaca, Edition 2002,Wassserwrtschaftskataster, Bundesministerium für Land-und, Forstwirtschaft, Umwelt und Wasserwirtschaft, Vienna2002.



Environmental control of emergence patterns: Case study of changes in hourly and daily emergence of...

Documents

Transcript of Environmental control of emergence patterns: Case study of changes in hourly and daily emergence of...