Revista Chilena de Historia Natural ISSN: 0716-078X [email protected] Sociedad de Biología de Chile Chile

PARITSIS, JUAN; VEBLEN, THOMAS T. Temperature and foliage quality affect performance of the outbreak defoliator Ormiscodes amphimone (F.) (: ) in northwestern Patagonia, Argentina Revista Chilena de Historia Natural, vol. 83, núm. 4, 2010, pp. 593-603 Sociedad de Biología de Chile Santiago, Chile

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Revista Chilena de Historia Natural 83: 593-603, 2010 © Sociedad de Biología de Chile

RESEARCH ARTICLE

Temperature and foliage quality affect performance of the outbreak defoliator Ormiscodes amphimone (F.) (Lepidoptera: Saturniidae) in northwestern Patagonia, Argentina La temperatura y la calidad del follaje afectan el desempeño del defoliador epidémico Ormiscodes amphimone (F.) (Lepidoptera: Saturniidae) en el noroeste de la Patagonia argentina

JUAN PARITSIS1,* & THOMAS T. VEBLEN1 1 Biogeography Lab, Department of Geography, University of Colorado, Boulder, Campus Box 260, CO 80309-0260, USA *Corresponding author: [email protected]

ABSTRACT

In the temperate forests of Chile and Argentina the phytophagous Ormiscodes amphimone (F.) causes severe defoliation on the southern beech tree Nothofagus pumilio (Poepp. & Endl.) Krasser. The recent increase in defoliation frequency in some areas appears to be influenced by a warmer climate. To evaluate the effects of temperature and the spatial heterogeneity of foliage quality on the performance and relative consumption rate of O. amphimone in northwestern Patagonia, Argentina we conducted a factorial experiment. Larval performance was measured as relative growth rate, developmental time, larval survival, and pupal weight. Larvae of O. amphimone were reared under two constant temperature regimes (15 °C and 20 °C) and fed with two N. pumilio foliage types (from a mesic and from a xeric site). Larvae at the higher temperature and fed with leaves from the mesic site showed higher performance and consumption rate than larvae in the other treatments. Higher temperature and mesic foliage had positive effects on O. amphimone’s relative growth rate, development time and relative consumption rate. However, pupal weight was positively influenced by mesic foliage but not by temperature, and larval survival did not show significant differences among treatments. Our results preliminarily suggest that O. amphimone performance and consumption rate may increase under higher temperature conditions, especially in the mesic portions of the precipitation gradient. However, these findings should be carefully interpreted as further research is necessary to assess the influence of higher temperatures on the foliar quality of N. pumilio. Key words: herbivory, Nothofagus pumilio, outbreaks.

RESUMEN

En los bosques templados de Chile y Argentina la polilla fitófaga Ormiscodes amphimone (F.) genera severas defoliaciones sobre la lenga (Nothofagus pumilio [Poepp. & Endl.] Krasser). El reciente aumento en la frecuencia de defoliación en algunas áreas de la Patagonia parecería estar influenciada por un clima más cálido. Para evaluar los efectos de la temperatura y la heterogeneidad espacial en la calidad del follaje sobre el desempeño y la tasa de consumo relativo del defoliador O. amphimone en el noroeste de la Patagonia argentina llevamos a cabo un experimento factorial. El desempeño larval fue medido como tasa de crecimiento relativo, tiempo de desarrollo, supervivencia larval y peso de las pupas. Las larvas de O. amphimone fueron criadas bajo dos temperaturas constantes (15 °C y 20 °C) y alimentadas con dos tipos de follaje de N. pumilio (de un sitio mésico y de uno xérico). Las larvas criadas a la temperatura más alta y alimentadas con hojas del sitio mésico exhibieron desempeños y tasas de consumo más elevadas que las larvas en los otros tratamientos. La temperatura más alta y el follaje del sitio mésico tuvieron efectos positivos en la tasa de crecimiento relativo, el tiempo de desarrollo y la tasa de consumo relativo. Sin embargo, el peso de las pupas fue influenciado positivamente por el follaje mésico pero no por la temperatura, y la supervivencia larval no mostró diferencias significativas entre tratamientos. Nuestros resultados sugieren preliminarmente que el desempeño y la tasa de consumo de O. amphimone podrían aumentar bajo condiciones de temperatura más elevadas, especialmente en los sitios mésicos del gradiente de precipitación. Sin embargo, estos resultados deben ser interpretados en forma prudente ya que más estudios son necesarios para evaluar los efectos de temperaturas elevadas sobre la calidad foliar de N. pumilio. Palabras clave: defoliaciones, herbivoría, Nothofagus pumilio. 594 PARITSIS & VEBLEN

INTRODUCTION Spatially, O. amphimone defoliation events appear to occur more extensively towards the In the temperate forests of Chile and mesic portion of the distribution gradient of N. Argentina in South America, Ormiscodes pumilio. In a study conducted in study areas in amphimone (F.) (Saturniidae, ), northern and southern Patagonia (Nahuel a phytophagous moth species, causes severe Huapi and Los Glaciares National Parks, defoliation on the widely distributed southern respectively) defoliation occurred more beech tree, Nothofagus pumilio (Poepp. & extensively than expected towards the mid- to Endl.) Krasser (Bauerle et al. 1997, Baldini & high precipitation portions of the gradient Alvarado 2008, Paritsis et al. 2010). (Paritsis 2009). This spatial pattern is also Ormiscodes amphimone is one of the most supported by studies conducted in our study widespread Ormiscodes species in Chile and area that show higher incidence of chewing Argentina ranging from ca. 34° S in central on N. pumilio leaves at wetter sites Chile to 55° S in Tierra del Fuego (Lemaire compared to drier sites (Mazía et al. 2004, 2002, Angulo et al. 2004) and matching 2009). In one of these studies, the guild of leaf closely the distribution of N. pumilio. chewing insects (including defoliators such as Although O. amphimone has been reported to O. amphimone) was responsible for almost two feed on over 20 species of native and exotic thirds of foliar damage towards the mesic end plants (see Paritsis et al. 2010 for a species of the precipitation gradient, while it only list), it feeds preferentially on the broad- caused one third of foliar damage towards the leaved canopy tree N. pumilio (Baldini & xeric portion of the gradient (Mazía et al. 2004). Alvarado 2008), which is one of the most These observations suggest that mesic N. important native timber species in Patagonia pumilio forests could be more favorable for O. (Martínez-Pastur et al. 2010). amphimone herbivory than xeric forests, but the Defoliation caused during epidemic mechanisms responsible for the observed population levels of this moth apparently does spatial pattern of herbivory were not studied. not generate widespread mortality of mature Thus, the first necessary step to explore the N. pumilio trees, probably due to the short causes of this spatial pattern is to evaluate the duration of these outbreaks (i.e. one season; physiological response of O. amphimone to Veblen et al. 1996, Paritsis 2009). foliage from these two contrasting locations Nevertheless, defoliation significantly reduces along the precipitation gradient. N. pumilio’s radial growth (Paritsis et al. 2009) Temperature and host plant quality are key and has been suggested as a predisposing factors that have strong influences on factor for the partial crown dieback observed performance, acting either individually or in in multiple N. pumilio stands (Veblen et al. combination (Lindroth et al. 1997, Levesque et 1996). Furthermore, defoliation by this insect al. 2002, Kingsolver et al. 2006). For instance, is known to cause economic losses by killing the effects of temperature on consumption and saplings and reducing timber production and growth rates of herbivorous insects may be also by diminishing forest aesthetic value for significant when insects feed on diets of certain tourism (Bauerle et al. 1997, Baldini & quality but not on others (Kingsolver et al. Alvarado 2008). Since the late 20th century 2006). Consequently, insect responses to the there has been an increase in Ormiscodes synergistic effects of temperature and plant outbreak frequency in southern Patagonia quality may generate complex population (Paritsis & Veblen 2011) coinciding with the processes, such as colonization, extirpation, and well-documented climate warming in the outbreaks, which are difficult to predict without region that started in the mid-1970s (Villalba et understanding potential interactions between al. 2003). Although there is evidence implying temperature and plant quality. Furthermore, that warming favors the occurrence of O. responses of phytophagous insects to amphimone outbreaks (Paritsis & Veblen temperature, host plant quality, and to the 2011), the mechanisms involved in the interactions between these factors are highly apparent increase in the frequency of variable in space and time, which has important outbreaks over the past several decades implications for insect population dynamics remain largely unknown. (Karban & Agrawal 2002, Auslander et al. TEMPERATURE AND DIET EFFECTS ON A DEFOLIATOR 595

2003), particularly under current and future Patagonia, Argentina, where there is a steep west-to- east gradient of decreasing precipitation associated climate warming scenarios. Recent large-scale with the rain shadow effect of the Andean divide outbreaks of forest insects in the northern (Veblen et al. 1996). The climate in this region is hemisphere have been attributed to characterized by cold and wet winters, and mild but dry summers with the growing season occurring temperature increases and have been mainly from November to February. The mesic site is modulated by the spatial heterogeneity of the located at Paso Puyehue (40°43’ S; 71°55’ W; 1150 m) quality of the resource (i.e. host plants) over on a relatively flat area with a mean annual precipitation of ca. 3000 mm (Barros et al. 1983). This the landscape (Powers et al. 1999, Logan et al. is a relatively dense N. pumilio stand with an open 2003). However, the precise mechanisms understory of forbs and small shrubs (e.g., through which temperature and the spatial Adenocaulon chilensis Less., Ribes maguellanica Poer., Berberis serratodentata Lechl.). The xeric site is located heterogeneity of plant host quality may 67 km to the southeast at Cerro Otto (41°08’ S; 71°20’ influence population dynamics of phytophagous W; elev. 1120 m) on a northeast-facing slope with a insects are extremely diverse and thus, must be mean annual precipitation of ca. 1000 mm (Barros et al. 1983). This N. pumilio stand has a more open canopy assessed on a case specific basis. than the mesic site and the understory species are Despite the current importance of O. mainly shrubs such as Schinus patagonicus (Phil.) I. M. amphimone as a defoliator in the N. pumilio Johnst. and Berberis buxifolia Lam. forests of southern South America and its Experimental design potential to increase its impact on ecosystem processes under a warmer future, there are no The study was conducted during the 2006-2007 austral summer in the northern Patagonian Andes at Nahuel published studies specific to the ecology of Huapi National Park, Argentina. In mid-December 2006 this key species (Baldini & Alvarado 2008). we collected 12 family-groups of O. amphimone larvae, Consequently, we address the question of how each from a different female, at the mesic site Paso Puyehue. Family-groups had 40 to 120 larvae, which O. amphimone responds physiologically to the were in their second instar. Because females lay eggs combined effects of increased temperature and in discrete masses and larvae are gregarious until their the spatial variation of foliage quality in reach the 5th and last instar, we were certain that each group of larvae collected was the offspring of a single northwestern Patagonia. To evaluate the female. We divided each family-group into four response of O. amphimone to temperature and subgroups that were assigned to one of four N. pumilio foliage quality we conducted a combinations of temperature and foliage treatments; hence, family-group was not a factor in the experiment. laboratory experiment to examine the The 2 x 2 factorial design consisted of two temperature simultaneous effects of these two key variables treatments of 15 °C (low) and 20 °C (high), and two N. on the performance and consumption rate of pumilio foliage types (i.e. diets) collected from a mesic site and a xeric site. Foliage collection was conducted O. amphimone. Foliage quality was measured every four days or less in both sites and was preserved as foliar water content, leaf toughness, at 5 °C to provide constant fresh leaves to larvae. For nutrients, and total phenolics, all of which are all treatments, we reared larvae in growth chambers with a 14:10 L:D photoperiod. The low temperature key variables known to influence insect treatment was chosen to match the average summer performance (Mattson 1980, Scriber & Slansky (December to February) temperature recorded at the 1981, Ohmart & Edwards 1991, Lawrence et al. Bariloche meteorological station (41°09’ S, 71°16’ W; elev. 825 m; 1976-2006). The high temperature was 1997, Sanson et al. 2001). Our specific selected to approximately match the highest expected objective was to evaluate the independent and warming of ca. 4 °C over the 21st century predicted by interacting effects of two temperature regimes the A1Fl climate scenario of fossil fuel emissions used by the Inter-governmental Panel on Climate Change and two types of foliage of N. pumilio on the (IPCC 2007). performance (measured as relative growth Each replicate consisted of a group of 10 to 30 rate, development time, larval survival, and larvae to emulate the gregarious behavior of O. amphimone in natural conditions. We started the pupal weight) and relative consumption rate of experiment with 12 replicates for each of the four the outbreak defoliator O. amphimone. treatments representing 934 larvae. Groups of larvae (i.e. replicates) were kept in 1000 cm3 plastic containers each and fed at least every other day with fresh N. pumilio leaves, assuring constant foliage METHODS availability. At the fifth instar, when larvae become solitary in natural populations, each replicate was Study sites reduced to four larvae per container to simulate natural conditions. Because of parasitoid-related deaths, We selected two contrasting study sites from where N. sample size diminished to nine replicates per treatment pumilio foliage was collected. Both sites are located on by the end of the experiment. Nevertheless, parasitoid- the eastern slopes of the Andes in Northwestern caused deaths were minimal in the remaining nine 596 PARITSIS & VEBLEN replicates (i.e. ca. 10 %) and did not differ among the body of larvae) because these were not directly treatments (F = 0.23; df = 3, 32; P = 0.87). Voucher affected by the treatments. One week after pupation, all specimens were deposited at the Museo Nacional de the pupae were weighed and sexed. We used female Historia Natural in Santiago, Chile. pupal weight as a measure of herbivore performance since it is known to be a good indicator of fitness in non- Foliar quality assessment feeding adult Lepidoptera species (as is the case with O. amphimone) and is often linearly associated with egg Several measures of foliage quality were made: leaf number (Awmack & Leather 2002). The sex of the water content (% fresh mass), leaf toughness pupae was determined examining the ventral portion of (measured as strength to fracture; g mm-2), nitrogen (% the last abdominal segments (Tuskes et al. 1996) and dry mass), phosphorous (% dry mass), organic matter was verified at adult emergence for at least 30 % of the (% dry mass), and total phenolics content (% Gallic Acid pupae. Equivalents, dry mass). To characterize foliage quality To calculate foliage consumption rate we we collected samples from 11 N. pumilio individuals at conducted foliar consumption trials with recently each site in early January (i.e. early summer). We molted fifth-instar larvae. Small branches with fresh collected foliage from a mixture of saplings (ca. 70 %) leaves were weighed and placed in containers with the and mature trees (ca. 30 %) matching the proportion of larvae. After 48 hours, the branches with the remaining these types of foliage to larval diet. At the time of leaves were weighed again to calculate foliar mass foliage collection, leaves at both sites were fully consumed. To account for leaf wilting we weighed and expanded but not senescent; thus, differences in leaf placed foliage in control containers (i.e. without larvae) phenology between sites, which may be a confounding that were re-weighed after 48 hours. The percentage of factor in comparative studies (Mopper & Simberloff water lost by transpiration (weight/weight) was 1995), were not likely to bias foliar quality measures incorporated into the calculation of the relative between sites. Three small branches from different consumption rate (RCR), which is the wet weight of the orientations and heights were collected per replicate consumed foliage divided by the product of multiplying (i.e. tree). Foliage was preserved at ca. 5 °C for 48 the duration of feeding (days) by the larval mean wet hours until analyses were performed. Water content weight (calculated as: [initial weight + final weight] / was quantified gravimetrically by measuring the 2) (Bowers et al. 1991, Rath et al. 2003). We used wet- percentage of water in fresh leaves. The amount of weight because it has been suggested that it reflects force needed to fracture foliage (defined here as short term feeding responses of caterpillars more toughness) was assessed by randomly selecting 30 realistically than dry weight (Kingsolver 2000). mature leaves per individual and measuring the weight needed to punch each leave with a 2 mm2 steel rod Statistical analyses (Sanson et al. 2001). Organic matter was estimated by calcinating the samples and weighing the ashes Foliar quality variables from the mesic and the xeric (Schlesinger & Hasey 1981). Phosphorous was sites were compared using t-tests for independent assessed by sample mineralization (Richards 1993) and samples. Two-way analysis of covariance (ANCOVA) nitrogen was quantified using the semi-micro Kjeldahl was performed to determine if there were significant method (Bremner 1996). Total phenolics were differences in performance and foliar RCR among larvae measured as gallic acid equivalents using the Folin- reared under the different treatments and to evaluate Ciocalteu technique (Waterman & Mole 1994). potential interactions between treatments. Initial larval weight was used as a covariate to control for potential Bioassays differences among groups of larvae at the beginning of the experiment. Where significant effects existed, post- We evaluated O. amphimone performance as larval hoc pair-wise comparisons were conducted to examine growth rate, development time, percentage of larval differences among individual treatment combinations survival, and pupal weight. To examine the independent using Tukey post-hoc tests. All percentage data were as well as synergistic influence of the treatments on transformed with an arcsine square root to reduce larval growth rate we weighed larvae (in groups) every variance heterogeneity (Zar 1999). five days until pupation, and we estimated the individual larval weight per replicate as the ratio between total weight and number of larvae in the sampling unit. Hence, although larvae were not weighed individually, RESULTS all the nutritional indices in this study are calculated on a per larva basis using the average weight per sample. We calculated larval relative growth rate (RGR) per Foliar quality sampling unit at each five-day feeding period (Bowers et al. 1991, Rath et al. 2003). A mean value of RGR was Foliar water content and organic matter were subsequently obtained per treatment averaging the RGRs obtained at each five-day feeding period, which significantly higher in the mesic than in the ranged from eight to 15 depending on the treatment. xeric site (Table 1). Total phenolics were Wet larval weight was used instead of dry weight to significantly higher in foliage from the mesic avoid killing larvae and the consequent reduction in sample size. We quantified development time as the site than in foliage from the xeric site (Table mean number of days it took for each group of larvae to 1). Although marginally significant, leaf pupate from the beginning of the experiment (i.e. when toughness was slightly higher in the xeric than larvae were at their second instar). To calculate percentage of larval survival we excluded parasitoid- in the mesic site (Table 1). Leaf N and P caused mortality (easily identified by the conspicuous showed no significant difference between cocoon that the hymenopteran parasitoids form within foliage from the two sites (Table 1). TEMPERATURE AND DIET EFFECTS ON A DEFOLIATOR 597

Bioassays Larvae in the mesic-high temperature treatment showed the highest RCR among the Temperature and foliar quality affected most of four treatments, which was nearly twice that of the O. amphimone performance variables and larvae in the xeric-high temperature treatment consumption rate (Figs. 1A, 1B and 1C, Table and more than three times that of larvae in the 2). However, contrary to our expectations, no xeric-low temperature treatment (Fig. 2). significant interactions of temperature and There were no significant differences in RCR foliar quality were observed on any of the among the xeric-high, mesic-low, and xeric-low measured performance variables and temperature treatments (Fig. 2). consumption rate (Table 2). Larvae reared at the warmer temperature and fed with leaves from the mesic site had significantly higher DISCUSSION RGR than larvae in the other treatments (Fig. 1A, Table 2). In addition, larvae growing under Foliar quality the high temperature treatment pupated significantly earlier compared to those Water content and total phenolics were higher growing under the low temperature treatment and leaf toughness was lower in leaves from (48 ± 5 versus 67 ± 5 days, respectively; mean ± the mesic compared to the xeric site. SE) (Fig. 1B, Table 2). Larvae feeding on Generally, high water content and lower leaf mesic foliage pupated significantly earlier than toughness are considered to be characteristic those feeding on xeric foliage, indicating that of higher quality food for insect herbivores foliage quality also had a significant effect on (Schoonhoven et al. 2005), and thus may be development time (Fig. 1B, Table 2). Larval responsible for the positive effect of mesic survival rates were not significantly different foliage on the performance variables reported among treatments (Table 2). Finally, groups of here. Interestingly, the slightly higher larvae feeding on mesic foliage had concentration of total phenolics in the mesic significantly higher female pupal weight (1.07 foliage reported in the current study had no ± 0.05 g; mean ± SE) than larvae feeding on negative effects on O. amphimone xeric foliage (0.83 ± 0.02 g; mean ± SE) (Fig. performance. Potentially, the lack of negative 1C) but there was no significant effect of effects are related to the high chemical temperature on pupal weight (Table 2). diversity of defensive compounds of N. pumilio Temperature and foliar quality had a leaves (Thoison et al. 2004), which is not significant effect on the consumption rate of O. apparent when measuring total phenolics amphimone fifth-instar larvae (Fig. 2, Table 2). alone.

TABLE 1

Mean (± SE) Nothofagus pumilio foliar quality traits in the mesic and xeric sites (n = 11 trees per site). Percentages are based on foliar dry weight (except for water content). Media (± EE) de las características de calidad foliar de Nothofagus pumilio en el sitio mésico y en el xérico (n = 11 árboles por sitio). Los porcentajes están basados en peso seco (excepto para el contenido de agua).

Mesic Xeric t df P

Water content (%) 64.5 ± 0.4 61.1 ± 0.8 3.2 20 < 0.001 Toughness (g mm ≥) 41.3 ± 1.1 44.5 ± 1.3 -1.9 20 0.07 Nitrogen (%) 2.38 ± 0.05 2.24 ± 0.09 2.1 20 0.1 Phosphorus (%) 0.19 ± 0.01 0.2 ± 0.01 -0.7 20 0.1 Organic matter (%) 95.7 ± 0.13 93.5 ± 0.23 8.9 20 < 0.001 Total phenolics (% GAEa) 9.3 ± 0.4 7.9 ± 0.3 2.7 20 0.015 a Gallic Acid Equivalents 598 PARITSIS & VEBLEN

Fig. 1: (A) Mean (± SE) relative growth rate (RGR; see Methods for definition; g: grams; d: days) in the four treatments measured at five-day intervals. (B) Mean (± SE) development time (days to pupation) in the four treatments from the beginning of the experiment. (C) Mean (± SE) wet pupal weight (grams) of females for the four treatments. Treatments are: M, mesic foliage; X, xeric foliage; H, high temperature (20 °C); L, low temperature (15 °C). Bars designated with different letters indicate significant differences among treatments (Tukey test, P < 0.01). (A) Media (± EE) de la tasa de crecimiento relativo (RGR; ver Métodos para la definición; g: gramos; d: días) en los cuatro tratamientos, medida a intervalos de cinco días. (B) Media (± EE) del tiempo de desarrollo (días hasta el pupado) en los cuatro tratamientos desde el comienzo del experimento. (C) Media (± EE) del peso húmedo (gramos) de las pupas hembra en los cuatro tratamientos. Los tratamientos son: M, follaje mésico; X, follaje xérico; H, temperatura alta (20 °C); L, temperatura baja (15 °C). Las barras con letras diferentes indican diferencias significativas entre tratamientos (prueba de Tukey, P < 0.01). TEMPERATURE AND DIET EFFECTS ON A DEFOLIATOR 599

TABLE 2

Effects of temperature (high versus low) and foliage source (mesic versus xeric) on relative growth rate (RGR), development time, larval survival, female pupal weight, and relative consumption rate (RCR) tested by two-way ANCOVA (initial larval weight was used as a covariable). Efectos de la temperatura (alta versus baja) y de la procedencia del follaje (mésico versus xérico) sobre la tasa de crecimiento relativa (RGR), el tiempo de desarrollo, la supervivencia larval, el peso de pupas hembra y la tasa de consumo relativo (RCR) evaluados mediante ANCOVA de dos vías (el peso inicial de las larvas fue usado como covariable).

Source df F P

RGR Temperature 1, 32 20.69 < 0.001 Foliage 1, 32 23.93 < 0.001 Temperature x Foliage 1, 32 1.27 0.27 Initial weight 1, 32 10.80 0.003 Development time Temperature 1, 32 303.09 < 0.001 Foliage 1, 32 58.51 < 0.001 Temperature x Foliage 1, 32 1.12 0.28 Initial weight 1,32 4.65 0.039 Larval survival Temperature 1, 32 0.16 0.89 Foliage 1, 32 0.26 0.61 Temperature x Foliage 1, 32 2.91 0.09 Initial weight 1, 32 4.57 0.04 Female pupal weight Temperature 1, 32 0.05 0.82 Foliage 1, 32 13.82 0.001 Temperature x Foliage 1, 32 0.02 0.88 Initial weight 1, 32 0.82 0.37 RCR Temperature 1, 37 10.09 0.003 Foliage 1, 37 22.86 < 0.001 Temperature x Foliage 1,37 2.57 0.118 Initial weight 1,37 22.06 < 0.001

Although the reported variation in foliage In assessing food quality effects on insect quality between sites may have contributed to performance it is important that the study the observed differences in herbivore subjects do not have prior preference for any performance and consumption, it is probable of the food qualities offered (i.e. parental that other foliar traits, such as specific effects on feeding preference should be phenolic compounds (e.g., flavonoids), were minimal). Insects growing on certain diets may also important. Additionally, qualitative rather produce offspring that perform better on than quantitative variation in foliar nitrogen similar diets, even if these are of lower could be responsible for the observed nutritional quality (Rotem et al. 2003). Given differences in performance. Although that all the larvae in our experiment were generally not measured, variation in the collected at the mesic site, our experimental protein quality in a diet can significantly affect design may be limited in this aspect. In order the performance and survival of herbivorous to confirm that foliage from the mesic site insects (Felton 1996). Independently of which favors O. amphimone performance foliar traits are responsible for generating the independently from the origin of the larvae, we observed differences in herbivore would have to include individuals from the performance, it is clear that O. amphimone xeric site in our experiment. In practice, this larvae fed with foliage from the mesic site was not possible due to the extremely low showed higher performance and RCR than density of O. amphimone populations in the those fed with foliage from the xeric site. xeric N. pumilio forests. Exhaustive searches 600 PARITSIS & VEBLEN for O. amphimone egg clusters and larvae at temperature and foliage quality (e.g., Stamp & several mesic and xeric sites during three Bowers 1990, Lindroth et al. 1997, Levesque et consecutive seasons yielded a difference in al. 2002). Nevertheless, there were no egg cluster density of approximately 1:20 interactions between temperature and foliage (xeric to mesic). This observation suggests quality on O. amphimone performance. Most of that conditions in the xeric environments the previous studies that evaluated the sustain markedly lower densities of O. combined effects of temperature and foliage amphimone than mesic sites. Therefore, quality found some interaction between these although we cannot formally confirm that factors. The lack of interactions in the current foliage from the mesic site favors O. study may be related to the small differences amphimone performance independently of the in foliage quality between treatments, as origin of the larvae, our field observations and suggested by Levesque et al. (2002) in their Mazía et al. (2004, 2009) findings on the study of forest tent caterpillar Malacosoma incidence of herbivorous chewing insects disstria Hübner. imply that xeric foliage is less suitable for O. Although higher temperature significantly amphimone than mesic foliage. shortened the feeding period of O. amphimone, pupal weight was not reduced in the high Performance and consumption temperature treatments. One explanation for this observation is that although the feeding Higher temperature and mesic foliage stage is commonly shortened at higher increased RGR and consequently shortened temperatures, larvae have higher consumption development time of O. amphimone. Our rates, attaining similar pupal weight as those findings concur with multiple studies that have with a longer larval stage (a process known as found positive relationships between “compensatory feeding”; Slansky 1993). development time of lepidopteran species, and Compensatory feeding may explain why pupal

Fig. 2: Mean (± SE) relative consumption rate (RCR; see Methods for definition; g: grams; d: days) per fifth- instar larva per day for the four treatments: M, mesic foliage; X, xeric foliage; H, high temperature; L, low temperature. Different letters indicate significant differences among treatments (Tukey test, P < 0.05). Media (± EE) de la tasa de consumo relativo (RCR; ver Métodos para la definición; g: gramos; d: días) por larva por día en quinto instar en los cuatro tratamientos: M, follaje mésico; X, follaje xérico; H, temperatura alta; L, temperatura baja. Las letras diferentes indican diferencias significativas entre tratamientos (prueba de Tukey, P < 0.05). TEMPERATURE AND DIET EFFECTS ON A DEFOLIATOR 601 weight was not reduced in the mesic-high the same climatic trend in different portions of temperature treatment compared to the mesic- the species’ geographic range (Thomson et al. low temperature treatment in which larvae 1984, Swetnam & Lynch 1993). Consequently, experienced a longer feeding period. On the despite the likelihood that warming may other hand, the similar pupal weight of O. increase the performance and consumption of amphimone between the xeric-high O. amphimone in N. pumilio forests, there are temperature and xeric-low temperature important sources of uncertainty in predicting treatments cannot be entirely explained by future population dynamics of this defoliator compensatory feeding because larvae in the and the frequency and severity of defoliation xeric-high temperature treatment did not show events. significantly greater RCR than larvae in the Factors not examined in this study can also xeric-low temperature treatment. A potential have significant effects on O. amphimone explanation for the similar pupal weight population dynamics and/or N. pumilio between the two xeric foliage treatments may susceptibility to attack, which could override be related to larval assimilation efficiency. At the direct effects of temperature and food lower temperatures, assimilation efficiency quality. For instance, changes in temperature may have been reduced (Schroeder & Lawson regimes can influence pathogen and parasitoid 1992); thus, although larvae at the low incidence (Ayres & Lombardero 2000, temperature treatment had more time to feed, Stireman et al. 2005), which in turn can they gained less biomass due to low interact in complex ways with the direct effects assimilation efficiencies. of temperature. Furthermore, warmer temperatures may cause phenological Implications for O. amphimone population dy- asynchrony between larval emergence and namics budburst that may generate significant population fluctuations (van Asch & Visser Assuming that the general trends in the 2007). Warming trends may also affect plant responses to temperature and food quality we nutritional quality of foliage and defenses documented for O. amphimone under (Ayres & Lombardero 2000), which in turn laboratory conditions apply in natural may affect population dynamics of O. ecosystems, our results suggest that under the amphimone. Therefore, additional current and predicted temperature increase in experimentation with temperature influences Patagonia (Carril et al. 1997, Villalba et al. on predation rates, host plant quality 2003) the performance and consumption rate (including defenses) and phenological of O. amphimone may increase, primarily in synchrony are needed to better understand the areas located in the mesic portion of the Ormiscodes-Nothofagus system. Nevertheless, gradient. Although warming is commonly the findings of the current study combined expected to favor the occurrence of outbreak with documented and reconstructed events for many insect species (Robinet & defoliation events (Paritsis & Veblen 2011) Roques 2010), insect populations have been provide a preliminary expectation that shown to respond in multiple ways to climate warming temperatures will likely enhance the warming trends. While some species of performance and consumption rate of O. Lepidoptera, such as the pine processionary amphimone in northwestern Patagonia, moth (Thaumetopoea pityocampa [Denis & particularly in more mesic N. pumilio forests. Schiffermüller]) in north-central France, expanded their outbreak range to previously unaffected regions (Battisti et al. 2005); other ACKNOWLEDGEMENTS species, such as larch bud moth (Zeiraphera We are grateful to N. Lescano for lab assistance; M.D. diniana Gn.) in the Alps, have diminished the Bowers, C. Quintero, E. Gianoli and two anonymous frequency of outbreak events with warming, reviewers for useful comments on previous versions of apparently due to asynchrony between egg this manuscript; and M. Elgueta for identifying O. amphimone specimens. We thank S. Whitehead and C. hatch and budburst (Büntgen et al. 2009). Quintero for conducting the analysis for total Furthermore, outbreaks of the same phenolics. The Ecotono Laboratory of the Universidad Lepidoptera species may respond differently to del Comahue in Bariloche provided laboratory facilities 602 PARITSIS & VEBLEN to conduct this research, and the Argentinean National American region: An intercomparison of coupled Park Service granted permission for insect and plant general atmosphere-ocean circulation models. collection. This research was funded by a Dissertation International Journal of Climatology 17: 1613- Improvement Award 0602164 from the National 1633. Science Foundation of the U.S.A. and by a grant from FELTON GW (1996) Nutritive quality of plant protein: the Graduate School of the University of Colorado Sources of variation and insect herbivore (Beverly Sears Graduate Student Grant). J. Paritsis was responses. Archives of Insect Biochemistry and a Fulbright fellow while conducting part of this study. Physiology 32: 107-130. IPCC (2007) Climate change 2007: Synthesis report. In: Pachauri RK & A Reisinger (eds) IPCC Fourth Assessment Report: 26-73. Intergovernmental LITERATURE CITED Panel on Climate Change. Cambridge University Press, Cambridge. ANGULO AO, C LEMAIRE & TS OLIVARES (2004) KARBAN R & AA AGRAWAL (2002) Herbivore offense. Catálogo crítico e ilustrado de las especies de la Annual Review of Ecology and Systematics 33: familia Saturniidae en Chile (Lepidoptera: 641-664. Saturniidae). Gayana 68: 20-42. KINGSOLVER JG (2000) Feeding, growth and the AUSLANDER M, E NEVO & M INBAR (2003) The thermal environment of Cabbage White effect of slope orientation on plant growth, caterpillars, Pieris rapae L. Physiological and developmental instability and susceptibility to Biochemical Zoology 73: 621-628. herbivores. Journal of Arid Environments 55: KINGSOLVER JG, JG SHLICHTA, G RAGLAND & K 405-416. MASSIE (2006) Thermal reaction norms for AWMACK CS & SR LEATHER (2002) Host plant- caterpillar growth depend on diet. Evolutionary quality and fecundity in herbivorous insects. Ecology Research 8: 1-13. Annual Review of Entomology 47: 817-844. LAWRENCE RK, WJ MATTSON & RA HAACK (1997) VAN ASCH M & ME VISSER (2007) Phenology of White spruce and the spruce budworm: Defining forest caterpillars and their host trees: The the phenological window of susceptibility. importance of synchrony. Annual Review of Canadian Entomologist 129: 291-318. Entomology 52: 37-55. LEMAIRE C (2002) The Saturniidae of America. Les AYRES MP & MJ LOMBARDERO (2000) Assessing Saturniidae Americains. Druckhaus the consequences of global change for forest Frankenbach, Lindenberg. disturbance from herbivores and pathogens. LEVESQUE KR, M FORTIN & Y MAUFFETTE (2002) Science of the Total Environment 262: 263-286. Temperature and food quality effects on growth, BALDINI A & A ALVARADO (2008) Manual de plagas consumption and post-ingestive utilization y enfermedades del bosque nativo en Chile. efficiencies of the forest tent caterpillar Asistencia para la recuperación y revitalización Malacosoma disstria (Lepidoptera: de los bosques templados de Chile, con énfasis Lasiocampidae). Bulletin of Entomological en los Nothofagus caducifolios. FAO/CONAF, Research 92: 127-136. Santiago, Chile. LINDROTH RL, KA KLEIN, JDC HEMMING & AM BARROS V, V CORDÓN, C MOYANO, R MÉNDEZ, J FEUKER (1997) Variation in temperature and FORQUERA & O PICIO (1983) Cartas de dietary nitrogen affect performance of the gypsy precipitación de la zona oeste de las provincias moth (Lymantria dispar L.). Physiological de Río Negro y Neuquén. Technical Report, Entomology 22: 55-64. Facultad de Ciencias Agrarias, Universidad LOGAN JA, J RÉGNIÈRE & JA POWELL (2003) Nacional del Comahue, Cinco Saltos, Argentina. Assessing the impacts of global warming on BATTISTI A, M STASTNY, S NETHERER, C forest pest dynamics. Frontiers in Ecology and ROBINET, A SCHOPF, A ROQUES & A the Environment 1: 130-137. LARSSON (2005) Expansion of geographic MARTÍNEZ-PASTUR G, MV LENCINAS, PL PERI, JM range in the pine processionary moth caused by CELLINI & A MORETTO (2010) Long-term increased winter temperatures. Ecological forest management research in South Patagonia Applications 15: 2084-2096. - Argentina: Lessons from the past, challenges BAUERLE P, P RUTHERFORD & D LANFRANCO from the present. Revista Chilena de Historia (1997) Defoliadores de roble (Nothofagus Natural 83: 159-169. obliqua), raulí (N. alpina), coigue (N. dombeyi) y MATTSON WJ (1980) Herbivory in relation to plant lenga (N. pumilio). Bosque 18: 97-107. nitrogen content. Annual Review of Ecology and BOWERS MD, NE STAMP & ED FAJER (1991) Systematics 11: 119-161. Factors affecting calculation of nutritional MAZÍA CN, T KITZBERGER & EJ CHANETON (2004) indices for foliage-fed insects: An experimental Interannual changes in folivory and bird approach. Entomologia Experimentalis et insectivory along a natural productivity gradient Applicata 61: 101-116. in northern Patagonian forests. Ecography 27: BREMNER JM (1996) Nitrogen-total. In: Bigham JM 29-40. (ed) Methods of soil analysis. Part 3. Chemical MAZÍA CN, EJ CHANETON, T KITZBERGER & LA methods: 1085-1121. Soil Science Society of GARIBALDI (2009) Variable strength of top- America, Madison, WI. down effects in Nothofagus forests: Bird BÜNTGEN U, D FRANK, A LIEBHOLD, D JOHNSON, predation and insect herbivory during an ENSO M CARRER et al. (2009) Three centuries of event. Austral Ecology 34: 359-367. insect outbreaks across the European Alps. New MOPPER S & D SIMBERLOFF (1995) Differential Phytologist 182: 929-941. herbivory in an oak population: The role of plant CARRIL AF, CG MENÉNDEZ & MN NÚÑEZ (1997) phenology and insect performance. Ecology 76: Climate change scenarios over the South 1233-1241. TEMPERATURE AND DIET EFFECTS ON A DEFOLIATOR 603

OHMART CP & PB EDWARDS (1991) Insect herbivory (2005) Insect-plant biology. Oxford University on Eucalyptus. Annual Review of Entomology 36: Press, Oxford. 637-657. SCHROEDER L & J LAWSON (1992) Temperature PARITSIS J (2009) Insect defoliator outbreaks and effects on the growth and dry matter budgets of environmental heterogeneity in Nothofagus Malacosoma americanum. Journal of Insect forests in the Patagonian Andes. Ph.D. Thesis, Physiology 38: 743-749. Geography Department, University of Colorado, SCRIBER JM & F SLANSKY JR. (1981) The nutritional Boulder. ecology of immature insects. Annual Review of PARITSIS J, TT VEBLEN & T KITZBERGER (2009) Entomology 26: 183-211. Assessing dendroecological methods to SLANSKY F JR. (1993) Nutritional ecology: The reconstruct defoliator outbreaks on Nothofagus fundamental quest for nutrients. In: Stamp NE & pumilio in northwestern Patagonia, Argentina. TM Casey (eds) Caterpillars: Ecological and Canadian Journal of Forest Research 39: 1617- evolutionary constraints on foraging: 29-91. 1629. Chapman and Hall, New York. PARITSIS J & TT VEBLEN (2011) Dendroecological STAMP NE & MD BOWERS (1990) Variation in food analysis of defoliator outbreaks on Nothofagus quality and temperature constrain foraging of pumilio and their relation to climate variability in gregarious caterpillars. Ecology 71: 1031-1039. the Patagonian Andes. Global Change Biology STIREMAN JO, LA DYER, DH JANZEN, MS SINGER, 17: 239-253 JT LILL et al. (2005) Climatic unpredictability PARITSIS J, M ELGUETA, C QUINTERO & TT and parasitism of caterpillars: Implications of VEBLEN (2010) New host-plant records for the global warming. Proceedings of the National defoliator Ormiscodes amphimone (Fabricius) Academy of Sciences USA 102: 17384-17387. (Lepidoptera: Saturniidae). Neotropical SWETNAM TW & AM LYNCH (1993) Multicentury, Entomology 39: (in press). regional-scale patterns of western spruce POWERS JS, P SOLLINS, ME HARMON & JA JONES budworm outbreaks. Ecological Monographs 63: (1999) Plant-pest interactions in time and space: 399-424. A Douglas-fir bark beetle outbreak as a case THOISON O, T SÉVENET, HM NIEMEYER & GB study. Landscape Ecology 14: 105-120. RUSSELL (2004) Insect antifeedant compounds RATH SS, BC PRASAD & BRRP SINHA (2003) Food from Nothofagus dombeyi and N. pumilio. utilization efficiency in fifth instar larvae of Phytochemistry 65: 2173-2176. Antheraea mylitta (Lepidoptera: Saturniidae) THOMSON AJ, RF SHEPHERD, JWE HARRIS & RH infected with Nosema sp. and its effect on SILVERSIDES (1984) Relating weather to reproductive potential and silk production. outbreaks of western spruce budworm, Journal of Invertebrate Pathology 83: 1-9. Choristoneura occidentalis (Lepidoptera: RICHARDS JE (1993) Chemical characterization of Tortricidae) in British Columbia. Canadian plant tissue. In: Carter MR (ed) Soil sampling Entomologist 116: 375-381. and methods of analysis: 115-139. Lewis, Boca TUSKES PM, JP TUTTLE, & MC COLLINS (1996) The Raton. wild silk of North America: A natural ROBINET C & A ROQUES (2010) Direct impacts of history of the Saturniidae of the United States recent climate warming on insect populations. and Canada. Cornell University Press, Ithaca. Integrative Zoology 5: 132-142. VEBLEN TT, C DONOSO, T KITZBERGER & AJ ROTEM K, AA AGRAWAL & L KOTT (2003) Parental REBERTUS (1996) Ecology of southern Chilean effects in Pieris rapae in response to variation in and Argentinean Nothofagus forests. In: Veblen food quality: Adaptive plasticity across TT, RS Hill & J Read (eds) The ecology and generations? Ecological Entomology 28: 211-218. biogeography of Nothofagus forests: 293-353. SANSON G, J READ, N ARANWELA, F CLISSOLD & P Yale University Press, New Haven. PEETERS (2001) Measurement of leaf VILLALBA R, A LARA, JA BONINSEGNA, M biomechanical properties in studies of MASIOKAS, S DELGADO et al. (2003) Large- herbivory: Opportunities, problems and scale temperature changes across the southern procedures. Austral Ecology 26: 535-546. Andes: 20th-century variations in the context of SCHLESINGER WH & MM HASEY (1981) the past 400 years. Climate Change 59: 177-232. Decomposition of chaparral shrub foliage: WATERMAN PG & S MOLE (1994) Analysis of Losses of organic and inorganic constituents phenolic plant metabolites. Blackwell Scientific, from deciduous and evergreen leaves. Ecology Boston. 62: 762-774. ZAR JH (1999) Biostatistical Analysis. Prentice-Hall SCHOONHOVEN LM, JJA VAN LOON & M DICKE Press, Upper Saddle River.

Associate Editor: Ernesto Gianoli Received June 11, 2010; accepted September 27, 2010 604 PARITSIS & VEBLEN