Ecological Entomology (2013), DOI: 10.1111/een.12047

Solar radiation directly affects larval performanceof a forest insect

A N D R E A B A T T I S T I,1 L O R E N Z O M A R I N I,1 A N D R E A P I T A C C O 1

and S T I G L A R S S O N2 1DAFNAE–Entomology, University of Padova, Legnaro, Italy and 2Department of

Ecology, Swedish University of Agricultural Sciences, Uppsala, Sweden

Abstract. 1. Solar radiation can affect the performance of insect herbivores directlyby increasing body temperature, or indirectly through alteration of either host plantquality or natural enemy activity.

2. To test for the direct effect of solar radiation on larval performance, young Pinussylvestris trees growing on the island of Gotland (Sweden) were assigned to one offour shading treatments for the whole duration of the first larval instar of the northernpine processionary moth Thaumetopoea pinivora .

3. There was a strong, linear relationship between shading and the temperature ofthe first-instar colonies of T. pinivora , resulting in higher growth of the larvae exposedto full sunlight, but there were no effects on developmental rate or larval mortality.Putative negative effects of UV radiation on the larvae are not consistent with highergrowth in full sunlight, but it is possible that UV effects might have modulated theresponse.

4. Thaumetopoea pinivora has a strong preference for light and open pine stands,i.e. habitats with frequent intense incoming solar radiation. The data in the presentstudy suggest that the opportunity for young larvae to bask in the sun during coldspring weather is an important determinant of the spatial distribution of T. pinivora .

Key words. Lepidoptera, northern pine processionary moth, Scots pine, shading,temperature size rule, Thaumetopoea pinivora .

Introduction

Temperature is one of the most important factors affecting theperformance of ectotherms (Angilletta, 2009). Small animals,such as insects, often experience body temperatures thatdiffer substantially from the ambient air temperature (ClusellaTrullas et al ., 2007). This is mainly explained by the highsurface area-to-volume ratio that facilitates heat exchangewith the environment. To be able to overcome harsh thermalconditions, some insects are able to modulate such an effect byliving within other organisms (Kuhrt et al ., 2005) or formingaggregations of many individuals (Pimentel et al ., 2011).

Solar radiation is an important determinant of air temper-ature but has rarely been considered in studies addressing itscontribution to the body temperature of insect larvae (Willmer& Unwin, 1981; Battisti et al ., 2005; Anthes et al ., 2008).

Correspondence: Andrea Battisti, DAFNAE–Entomology,University of Padova, Agripolis, 35020 Legnaro, Italy. E-mail:andrea.battisti@unipd.it

Solar radiation varies greatly with the microhabitat, especiallyin structurally complex ecosystems such as forests (VandeVelde et al ., 2011). An intriguing fact is that insects seem toadjust their thermoregulatory behaviour by selecting microhab-itats in order to maximize growth (Coggan et al ., 2011). Solarradiation is also an important component of climate change,although the local effects are less easy to predict than tem-perature because of the high number of factors determiningcloudiness (Solomon, 2007).

The combination of temperature and solar radiation has oftenbeen invoked to explain the distribution and abundance ofinsects at various spatial scales (Bryant & Shreeve, 2002; Kuhrtet al ., 2006). A few studies have addressed the direct effects ofsolar radiation on temperature and performance of insects. Forinstance, several tent-spinning Lepidoptera from temperate orarctic ecosystems exhibit a positive relationship between radi-ation intensity, temperature gain, and performance (Joos et al .,1988; Bennett et al ., 1999; Danks, 2004; Battisti et al ., 2005).

The northern pine processionary moth Thaumetopoeapinivora Treitschke (Lepidoptera Notodontidae), which feeds

© 2013 The Royal Entomological Society 1

2 A. Battisti et al.

on pine needles, is strongly dependent on solar radiation inorder to enhance body temperature during the first larvalinstar (Ronnas et al ., 2010). The duration of the larval instarsof this species differs from those of most other Lepidoptera,with young larvae living much longer (first instar: 41 days,min–max 20–58) than late-instar larvae (fifth instar: 17 days,min–max 10–23) (Montoya & Robredo, 1972). Hatching(in Sweden) takes place in early spring and this means thatfirst-instar larvae are exposed to low temperatures for a longtime. The larvae are gregarious and bask in the sun, generallyon a bud or a twig, to increase their body temperature. In fieldexperiments, at solar radiation levels above 100 W m−2, thethermal excess of colonies has been found to vary between 4and 6 ◦C above the ambient temperature, and the magnitudeof the increase is positively related to colony size (Ronnaset al ., 2010).

Thaumetopoea pinivora has a clear preference for sparse andopen Pinus sylvestris L. stands, forest edges, and isolated trees(Aimi et al ., 2008). We hypothesized that solar radiation canbe an important determinant of the spatial distribution of thisspecies, as it appears to be for the sister species Thaumetopoeapityocampa (Battisti et al ., 2005) and other Lepidoptera (VandeVelde et al ., 2011). We tested this hypothesis in a fieldexperiment where we manipulated solar radiation in the fieldby imposing various degrees of shading on small trees duringthe entire duration of the first larval instar. This designaimed to simulate various degrees of canopy closure and thusreduced the opportunities for larvae to increase their bodytemperatures by basking in the sun. In addition to affectinglarval performance positively through excess temperature,solar radiation may also affect larvae negatively throughoxidative stress (Meng et al ., 2009; Zhang et al ., 2011) andreduction in food quality due to a UV-induced increase inthe concentrations of defensive chemicals (Rousseaux et al .,2004; Demkura et al ., 2010). The main goal of this experimentwas to understand which environmental factor can explainthe preference of T . pinivora for open habitats. Because UVinduction is likely to decrease larval performance in open areas,rather than increasing it, we considered it highly unlikely thatUV induction is important in explaining the preference of T .pinivora for open areas. Thus, we did not specifically analyzethis factor, but were aware that predicted positive effectsof temperature excess could be counterbalanced by negativeeffects from putative UV-induced changes in food quality.

We expected to obtain different degrees of body temperaturereduction in colonies that were feeding on trees with differentlevels of shading. Life-history traits were expected to varyaccordingly. In particular, larval development rate and growthrate vary with temperature (Chown & Gaston, 2010), and bothtraits are potentially important in determining demographicprocesses (Larsson, 2002) and thus spatial distribution. Adultbody size is negatively related to temperature if the sensitivityfor growth is lower than that for development (van der Have &de Jong, 1996; Zuo et al ., 2012). This is the situation observedmost often in ectotherms, which obey to the temperature–sizerule (TSR) in about 80% of cases (Gibert & de Jong,2001; Walters & Hassell, 2006; Zuo et al ., 2012). When thesensitivity for development is lower than that for growth,

however, a larger body size and more rapid developmentare achieved when temperatures are higher. This situationhas been observed in a number of species and seems to beexplained by mechanisms associated with cell growth anddifferentiation (Walters & Hassell, 2006). If growth rate turnsout to be more sensitive than developmental rate, larvae wouldbecome bigger more rapidly and thus could be less exposedto mortality factors, such as predation. Because generalistarthropod predators appear to be an important limiting factorfor first-instar T . pinivora (Aimi et al ., 2008; Ronnas et al .,2010), we hypothesized that larger larvae would better escapepredation (Remmel et al ., 2011). In this paper, by manipulatingthe daytime temperature by artificial shading, we were able toexamine how development and growth rates are affected ina species where basking in the sun by first-instar larvae is aprominent life-history trait.

Materials and methods

Study organism

The northern pine processionary moth T. pinivora isassociated with P. sylvestris in Europe; populations areconcentrated around the Baltic Sea but also occur in thewestern Alps and in the Spanish highlands (Cassel-Lundhagenet al ., 2013). In recent years, an outbreak of T . pinivora hasoccurred on the island of Gotland, off the east coast of southernSweden (Ronnas et al ., 2011).

Thaumetopoea pinivora has a 2-year development cycleon the Swedish island of Gotland where the experiment wascarried out. Adults emerge from the cocoons in the soil inmid- to late July. Females live for only a few days. Theeggs are laid in batches on pine needles shortly after femaleemergence, and hatch in April the following year when themonthly mean daily temperature varies between 1.9 and 6.6 ◦C(period 1970–2008, weather station Hoburgen, 56◦55′19”N,18◦09′02′′E, 33 m a.s.l.).

A female usually lays all her eggs (about 150) in one batchor two batches close together. The size of the first-instar colonyvaries greatly, with a mean of 112 individuals (Ronnas et al .,2010). The neonate larvae form a compact colony very closeto the eggs. The larvae feed on mature needles, even lateinstars when current-year needles have developed. The larvaeare nocturnal feeders and the colonies spend most of the dayresting on the tree. Because the temperature during early larvaldevelopment is low, the first two instars take almost 2 monthsto complete. Later instars develop faster as the temperatureincreases (Aimi et al ., 2008). In late July, fifth-instar larvaeleave the trees in typical head-to-tail processions to searchfor suitable sites in the soil for cocoon spinning. The pupaeoverwinter and remain in the soil until July the following year.

Shading experiment

The experiment was intended to test the influence ofshading on larval performance. We employed a randomizedblock design with five blocks and four treatments per

© 2013 The Royal Entomological Society, Ecological Entomology, doi: 10.1111/een.12047

Effects of solar radiation on larval performance 3

block. Each block covered approximately 0.1 ha and thewhole experimental area was 2 ha. Within each block, weselected four isolated, small-stature (1.5–2.0 m) trees; naturallyoccurring colonies of T . pinivora are frequently found on thissize of tree. Distances between trees within blocks were about15 m, and always much shorter than the distances betweenblocks (about 100 m). Every tree within a block was randomlyassigned to one of the four treatments: control (no shading),30% shading, 60% shading, and 90% shading. Shading wasachieved by surrounding each tree with a metal frame thathad a roof made of shade netting of an appropriate density(Artes Politecnica Schio Italia, Bartex 30, Bartex 60, Bartex90, colour black, www.artespolitecnica.it), which affects thewhole light spectrum (Castellano et al ., 2006). The shadedarea was 2.2 × 2.2 m and the height of the frame was 2 m.The shading effect was complete during the daytime, althoughdirect sunlight reached the trees for a maximum of about halfan hour each at dawn and dusk.

In March 2009, all naturally occurring egg batches wereremoved from the experimental trees together with the needleson which they had been laid. Additional egg batches werecollected from nearby trees until the number needed for theexperiment was reached. All egg batches were taken to thelaboratory and their length was determined. Batches of averagelength (15 mm, with about 100 eggs; cf. Aimi et al ., 2008)were separated and immediately returned to the field wherethey were placed on the experimental trees (three batchesper tree). The needles carrying the batches were fixed witha thin wire to terminal pine shoots (i.e. grown out in 2008)in the upper half of the tree, on equidistant branches. The eggbatches were checked every second day to detect hatching.The shading treatment started as soon as the first hatchingwas observed (18 April). Hatching was over on 24 Aprilwhen the hatched egg batches were collected and taken tothe laboratory. The scales covering the egg batches wereremoved so eggs could be inspected. Precise data on initialcolony size were obtained by counting hatching holes in eggs.The mean (± SD) group size was found to be 99.3 ± 20.9larvae (n = 60) with no differences found among treatments(F (3,52) = 1.44, P = 0.24).

The newly hatched colonies were inspected every secondday during daylight, when they usually form close groupsbasking on pine shoots (Ronnas et al ., 2010). As soon asthe larvae in a colony started to moult to the second instar(starting on 14 May, ending on 6 June), the twig carrying thecolony was collected and immediately taken to the laboratorywhere it was frozen at −20 ◦C. The larvae in the colony weregently separated from the twig, and counted. As most of thelarvae (96.6%) were in the second instar, we concluded that themoulting was synchronous within a colony. There was a smalldifference in the proportion of second-instar larvae between thecontrol (97.9%) and the maximum shading treatment (95.2%),but this was not significant (t-test, P = 0.22). Larvae weredried (24 h at 60 ◦C) and weighed. Survival of the first-instar larvae and individual dry weight were then calculated.Developmental time was defined as the time elapsed from thefirst egg hatching to the first observation of moulting into thesecond instar.

Bioclimatic measurements

A bioclimatic station was deployed in the same area atthe beginning of the experiment on a separate tree equippedwith the shading frame, and on a control tree nearby, withthe aim of determining the degree to which shading affectsa colony’s ability to accumulate heat (temperature excess),as compared with the ambient temperature. The tempera-ture of the colonies was measured as described by Ronnaset al . (2010). The station included four precision fine-wire(∼ 0.1 mm) chromel–constantan Teflon-insulated thermocou-ples (model TT-E-36; Omega Engineering, Inc., Stamford,Connecticut), which were inserted inside four colonies, two onthe shaded tree and two on the control tree. Air temperature andRH were measured with an HMP-45 probe (Vaisala, Helsinki,Finland), housed in a non-ventilated standard shield at a heightof 2 m. Wind speed and direction were measured at the sameheight with a WindSonic 2-axis ultrasonic anemometer (Gill,Lymington, U.K.). Incoming solar radiation was measured withan LI-200 pyranometer (Li-Cor, Lincoln, Nebraska) placedabove the tree canopy, while a CNR1 net radiometer (Kipp& Zonen, Delft, The Netherlands) placed under the shade net-ting measured downward and upward short- and long-waveradiation fluxes at the average height of the colonies. All thesensors were read every 1 s by a CR23X datalogger (Camp-bell Scientific, Shepshed, Loughborough, U.K.). The probesinserted inside the colonies were checked at regular intervals(1–2 h) throughout the experiment. Data on colony tempera-tures refer to situations when the tip of the probe was clearly inthe correct position, i.e. not visible from the outside. Becausewe used the same tree to measure the effects of different shad-ing treatments, the shade netting was changed every 2–3 days.

Data analysis

The thermal response of colonies to the shading treat-ment was analysed by calculating the temperature differencebetween the colonies and the air temperature, as described byRonnas et al . (2010). Measurements taken on different daysand for different treatment conditions were pooled accord-ing to solar radiation (day, > 100 W m−2; night, < 100 W m−2).Because it was not possible to obtain simultaneous mea-surements of the colony temperature in the different shad-ing treatments, the measurements were taken on differentdays under similar temperature (8.9 ◦C, SD 0.49), humidity(50.6%, SD 11.5), radiation (541 W m−2, SD 35.1), and windspeed (1.5 ms, SD 8.2) conditions (anova, F (3,116) = 0.88,p = 0.44, F (3,116) = 1.08, p = 0.10, F (3,116) = 1.88, p = 0.14,F (3,116) = 1.32, p = 0.27, respectively). The measurementswere then used to compare colony temperatures for 30 mea-surements per treatment by means of anova.

The variables used in the analysis were divided into twogroups. The performance variables (larval survival, individualdry weight, and developmental time) were analysed as such.Linear mixed models (LMMs) were used with shadingtreatment as a fixed effect and tree within block as a randomfactor. To test the shading effect, we used sequential F -tests(Pinheiro & Bates, 2000). We were able to use LMMs because

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4 A. Battisti et al.

the model residuals approximated a normal distribution andexhibited variance homogeneity. All the LMMs were estimatedusing the lme (in nlme package) function in r, version2.12.1 (R Development Core Team, 2010) with the restrictedmaximum likelihood (REML) estimation method.

Results

The shading negatively affected temperature excess ofT. pinivora colonies during the day; the opposite was trueat night, but the difference was much smaller, although sig-nificant (anova, F (3,116) = 183.8, P < 0.01). The temperatureexcess of the colonies fully exposed to solar radiation was 5.4times higher than for those with 90% shading, while during thenight the shaded larvae experienced a temperature about 1 ◦Chigher than those that were fully exposed (Fig. 1). Tempera-ture excess differed when all the treatments were considered(Tukey’s honest significance test, P < 0.01), but there was nosignificant difference between the unshaded and 30% shadingtreatments when they were considered as a pair (Tukey’s hon-est significance test, P = 0.53). Absolute temperatures of all thetreatment pairs were different under both day and night-timeconditions (Tukey’s honest significance test, P < 0.01).

The performance of the colonies was affected by the shadingtreatment only as far as individual dry weight was concerned;larvae ready to moult to the second instar on shaded trees werelighter than those on unshaded trees, and the weight decreasedprogressively as shading increased (F 3,19 = 9.33, P < 0.001)(Fig. 2). We were unable to identify any significant effect ofshading on larval developmental time (mean 34.5 days, SD 2.7)(F (3,52) = 1.27, P = 0.29) (Fig. 2). Shading treatments had noeffect on survival of the first-instar larvae (67.9%, SD 11.5)(F (3,52) = 0.57, P = 0.63).

Discussion

We found a strong linear relationship between shading and thetemperature excess of the first-instar colonies of T. pinivora ,resulting in higher body weight of the colonies feeding onunshaded trees. The colonies, however, exhibited a similardevelopmental time irrespective of treatment. These findingswere surprising and fall between the two hypotheses relatedto the relative temperature threshold values for growth anddevelopment (Walters & Hassell, 2006), providing no evidenceto support the TSR (Chown & Gaston, 2010). Instead, thedata lend support to the alternative hypothesis that predictsgreater body size at higher temperatures, although supportfor this was only partial because developmental time did notchange with shading intensity. Basking in the sun can thusbe interpreted as a means of optimizing growth under thegenerally unfavourable conditions associated with an earlyhatching time in a cold climate. In addition, early hatchinghas been suggested as a means of escaping from generalistpredators (Aimi et al ., 2008; Ronnas et al ., 2010), and thus thegreater size achieved by the larvae for the same developmentaltime should further increase their capacity to resist predation(Ronnas et al ., 2010; Remmel et al ., 2011). These data support

-2

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0

1

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3

4

5

6

7

8

9

0 30 60 90

ΔT °

C

Shading %

daynight

Fig. 1. Temperature difference between the Thaumetopoea pinivoracolonies and shielded ambient air under natural conditions (0%shading) and three shading treatments (30 measurements for eachtreatment). Vertical bars are SDs; for the night-time data, the barsare hidden by the dots.

the proposition that the distribution of sun-basking insectsunder harsh climatic conditions, such as neonate T . pinivora onGotland, is governed by their ability to enhance their thermalmicroenvironment and thereby their life-history performance.

The experiment was designed to test the net effects of solarradiation on the larvae and was specifically aimed at exploringthe consequences of variable temperature excess. Thus, wecannot know to what extent a putative UV-induced larvaloxidative stress (Meng et al ., 2009; Zhang et al ., 2011) andreduction in food quality (Rousseaux et al ., 2004; Foggo et al .,2007; Ballare et al ., 2012) contributed to the results. However,the clear positive effect of radiation, and temperature excess,on larval body weight does show that UV effects, at the most,can modify the positive effect that radiation has on larvalperformance through better basking opportunities. Thus, thebenefit from achieving higher temperature clearly outweighsthe putative cost of larval oxidative stress and feeding onlower-quality food.

The reduced solar radiation, and lower temperatures,affected larval performance in a way that does not conformwith the TSR (Angilletta et al ., 2004; Zuo et al ., 2012).We offer the following tentative explanations for this. Ourtreatment system has two important features that need to beconsidered. First, the shading reduced daytime temperature ofthe colonies under sunny conditions, whereas it had marginaleffects on the night-time temperature. Because the larvae arenight feeders (Montoya & Robredo, 1972), the food intake andinitial assimilation took place under similar temperature con-ditions for those on shaded and unshaded trees, or may haveslightly favoured the individuals on shaded trees that expe-rienced a marginally higher temperature, perhaps associatedwith a better food quality because of a lower amount of UV-induced defences (Demkura et al ., 2010). Secondly, shadingdecreased the temperature during the day by about 6 ◦C. Thelarvae are likely to convert food gathered during the night intobody mass during the day (Yang & Stamp, 1995), as is alsothe case for the night-feeding T . pityocampa , whose perfor-mance is strongly reduced if the larvae are not exposed to a

© 2013 The Royal Entomological Society, Ecological Entomology, doi: 10.1111/een.12047

Effects of solar radiation on larval performance 5

Fig. 2. Mean weight (a) and developmental time (b) of first-instarThaumetopoea pinivora larvae under increasing shading. Vertical barsare SDs.

minimum daytime temperature (Battisti et al ., 2005). Thus, wetentatively conclude that a decrease in solar radiation reducesgrowth rate more than development rate, resulting in a partialreverse of the TSR.

Larval survival was not affected by shading. We did notexpect an increase in the direct mortality as a result of shading,but indirect effects through increased predation mortality wereconsidered possible (Ronnas et al ., 2010). The fact thatdevelopmental time was not prolonged in shaded coloniesmay explain why this did not occur. Larvae in shaded treesattained a smaller size and were potentially more vulnerable toarthropod predators (Remmel et al ., 2011), but were obviouslynot predated to a greater extent than the larger larvae. Thusthe possibility of an interaction between shading effects onlife-history traits and predation mortality, as discussed in theintroduction, was not realized. It is difficult to know whetheror not this reflects a real outcome of predation events, becausethe experiment was not specifically designed to study predationprocesses: rigorous predation experiments need to accountfor spatial and temporal variation in the predator community,which was beyond the scope of this study.

Our data were related to first-instar T . pinivora larvae.Focusing on this instar is important for at least three reasons:(i) sun basking is particularly pronounced during the first-instar

larval stage when the temperature on Gotland is low, similarto the forest tent caterpillar in spring (Joos et al ., 1988) or toarctic insects (Bennett et al ., 1999; Danks, 2004); (ii) in gen-eral, larvae of many herbivorous insects suffer especially highmortality in early instars (Hawkins et al ., 1997; Zalucki et al .,2002), and T . pinivora is no exception (Aimi et al ., 2008;Ronnas et al ., 2010); and (iii) in T . pinivora the first instaris the longest of the five developmental stages, an unusualsituation in lepidopterans (Montoya & Robredo, 1972; Zaluckiet al ., 2002), and thus young larvae in this species are exposedto mortality factors for an unusually long period. We thus con-clude that, in the T . pinivora system on Gotland, the first instaris likely to be a key to understanding processes at the popu-lation level, such as the spatial distribution of the population.

Our finding that the first-instar colonies of T . pinivoraperform better on unshaded than shaded trees contributespotentially important knowledge to the understanding of thespatial distribution of this species. We acknowledge that manyfactors contribute to the spatial distribution of organisms(Gaston, 2003) but, as discussed earlier, there are good reasonsto assume that the performance of first-instar larvae is a keyfactor in understanding the local distribution of T . pinivora .Assuming that our shading treatments can be consideredproxies of pine stands of varying densities, it is reasonableto conclude that the poorer larval performance in shadedhabitats should select for females avoiding dense stands foroviposition, even if, at present, we do not understand theunderlying mechanisms of the postulated fitness loss in shadedenvironments. Indeed, data from the Gotland population showthat T . pinivora have a clear preference for sparse and openpine stands, forest edges, and isolated trees (Aimi et al ., 2008).

In conclusion, our data suggest that solar radiation has amore important role in determining performance of insectlarvae than was previously thought, and thus potentiallyinfluences habitat preference (Bryant et al ., 2002; Kuhrt et al .,2005; Anthes et al ., 2008) and population dynamics (Selaset al ., 2004; Anttila et al ., 2010). UV-B radiation is a factorthat can negatively affect insect performance, through themodification of the chemical defence system of host plants(Rousseaux et al ., 2004; Selas et al ., 2004; Foggo et al .,2007; Anttila et al ., 2010; Ballare et al ., 2011). It wouldbe interesting, but was beyond the scope of this study, torelate the positive direct effects of solar radiation to thenegative indirect effects due to UV induction of lower-quality plant tissue. This trade-off probably results in differentoutcomes in different systems, e.g. due to insect response totemperature, plant susceptibility to UV radiation, and insectsensitivity to variable plant chemistry. It is important toexamine further how this trade-off varies among populationsystems to obtain a better understanding of abiotic influenceson insect population dynamics, particularly in the context ofclimate change (Klapwijk et al ., 2012).

Acknowledgements

We warmly acknowledge the help of many people whocontributed to the organization of the field experiment, in

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6 A. Battisti et al.

particular Tomas Lundmark for the design and constructionof the metal frames, Per Goran Boden for permission to setup the experiment on his land, and Cecilia Ronnas, CaterinaVillari, Fernanda Colombari, Luigi Masutti, and MassimoFaccoli for their help during the fieldwork. We warmly thankKarl Gotthard for valuable comments on an earlier version ofthe manuscript, and two anonymous reviewers for constructivecomments. The research was funded through the BACCARAproject (Biodiversity and Climate Change: a Risk Analysis)from the European Community’s Seventh Framework Pro-gramme (FP7/2007–2013) under grant agreement no. 226299,and by The Swedish Research Council for Environment,Agricultural Sciences and Spatial Planning.

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Accepted 15 May 2013

© 2013 The Royal Entomological Society, Ecological Entomology, doi: 10.1111/een.12047