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Effect of elevation on the insect herbivory of Mongolian oaks in the high mountains of southern South Korea
Journal of Asia-Pacific Entomology 22 (2019) 957–962
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Effect of elevation on the insect herbivory of Mongolian oaks in the high mountains of southern South Korea
T
Jae-Cheon Sohna, Nang-Hee Kimb, Sei-Woong Choic,
⁎
a
Department of Science Education, Gongju National University of Education, Gongju, Chungnam 32553, Republic of Korea Division of Industrial Insect, National Institute of Agricultural Sciences, Rural Development Administration, Wanju, Jeonbuk 55365, Republic of Korea c Department of Environmental Education, Mokpo National University, Muan, Jeonnam 58554, Republic of Korea b
ARTICLE INFO
ABSTRACT
Keywords: Elevational gradient Feeding guilds Insect-feeding damage types Island Mongolian oak
Elevation is strongly associated with the diversity and ecology of plants and animals. We explored how elevation affects herbivores on one of the major cool-temperate trees, Quercus mongolica, in southern South Korea. The feeding activities of insect herbivores were measured through insect-feeding damage on leaves. Of 78 types of insect-feeding damage that were observed from Jirisan Mountain (Mount.) and Hallasan Mount. in Korea, 61.6% was associated with externally feeding insects. The sum of feeding damages per leaf was significantly higher on Jirisan Mount. than on Hallasan Mount., and higher at higher elevation in both mountains. Two feeding guilds, externally feeding, and piercing and sucking were strongly related with elevation, but the relationship was opposite depending on feeding guild. Leaf damage by the internal feeding guild showed no effect of elevation at the two mountains. These study results showed that insect herbivory responds to elevational differences in temperate forests, and that such response can vary among feeding guilds.
Introduction Plants and herbivorous insects comprise a large proportion of terrestrial biodiversity and their extant diversity is most likely due to the evolution of various interactions between them (Hougen-Eitzman and Rausher, 1994; Winkler and Mitter, 2008; Futuyma and Agrawal, 2009). Foliar damage is defined as the removal or deformation of foliar tissues not only by physical forces but also chemical interactions from insects, other arthropods and pathogenic fungi. In particular, insectfeeding damage is any trace involving the feeding activity of terrestrial arthropods (insects and mites), sometimes followed by host healing process or by fungal infection. It is often distinctive and diagnosable in relation to the functional morphology of damage-makers (Labandeira et al., 2007). A morpho-type system of the damage can serve as an indicator of diversity in plant-arthropod interactions. Such a system has been used to study the effects of extant or ancient environmental gradients on insect herbivory (Wilf and Labandeira, 1999; Currano et al., 2008, 2010; Adams et al., 2010) and the evolutionary diversification of the insect groups (Labandeira, 2006). Insect herbivory is known to be influenced by biotic or abiotic factors (Schoonhoven et al., 2005). Biotic factors affecting insectmediated damage on plants include trophic cascades (Kaplan and Denno, 2007), existing species diversity (Alalouni et al., 2014), and the ⁎
physiological conditions of host plants (Leckey et al., 2014). Insectfeeding damage on plants varies according to physical environmental conditions such as temperature (Garibaldi et al., 2011), humidity (Fernandes and Price, 1988), and solar radiation (Lowman, 1985; Reynolds and Crossley, 1997). Increasing efforts have been made to monitor environmental changes through insect-feeding damage to plants (Adams et al., 2010; DeLucia et al., 2012; Carvalho et al., 2014). Oaks (Quercus spp.) are common trees in northern temperate vegetation (Nixon, 1993). They play a fundamental role in terrestrial ecosystems as hosts for numerous insect herbivores that are an important food source for other high-trophic animals (Leach and Givnish, 1999; Swiecki and Bernhardt, 2006). About eleven species of oaks that differ in morphological and physiological traits are distributed in Korea (Chang et al., 2012). The Mongolian oak (Quercus mongolica Fisch. ex Ledeb.) is one of the main components in the East Asian deciduous forests (Chen and Huang, 1998) and it is also quite common in Korean cool-temperate mountains (Park, 2014; Kong et al., 2014). This study is part of a long-term project intended to model possible responses of plant-insect interactions in Korea upon global climate change. Mongolian oak is regarded as one of the Korean plants that could be threatened by climate change (Lee et al., 2014). We examined insect-feeding damage on Mongolian oak at two high-elevation mountains in the southern part of South Korea: Jirisan Mountain (Mount.)
Corresponding author. E-mail address: [email protected] (S.-W. Choi).
https://doi.org/10.1016/j.aspen.2019.08.004 Received 10 June 2019; Received in revised form 6 August 2019; Accepted 8 August 2019 Available online 09 August 2019 1226-8615/ © 2019 Korean Society of Applied Entomology. Published by Elsevier B.V. All rights reserved.
Journal of Asia-Pacific Entomology 22 (2019) 957–962
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Fig. 1. (a) Map of the study sites in Jirisan Mountain and Hallasan Mountain, South Korea (A: Seongsamjae, B: Sangseonam, C: Sajebi Hill, D: lower Yongsil). (b) Monthly average temperatures in 2015 from Namwon (gray circles and lines) and Seogwipo (open circles and black lines) adjacent to Jirisan Mountain and Hallasan Mountain respectively. (c) Monthly accumulated precipitation in 2015 from Namwon (white bars) and Seogwipo (black bars).
(max elevation 1915 m above sea level) and Hallasan Mount. (max elevation 1950 m a.s.l.). We investigated 1) whether there is significant difference of insect feeding damage to oak trees along elevational gradients in two high mountains, and 2) whether there is any difference in the relative abundance of each functional feeding-damage group between the two mountains.
of 140, 106, 199 and 131 leaves were sampled from SSJ, SSA, SJB, and LYS, respectively. Feeding traces associated with feeding activities of insects and mites on the leaves were counted under a stereoscope (Leica EZ4, Leica Co.) and photographed as necessary, using a digital camera (Nikon D30, Nikon Co.) attached to a stereoscope (Leica L2, Leica Co.). Types of insect-feeding damage (hereafter abbreviated as DT [= damage type]) were determined using their morphological characteristics, positions on the leaves, and interactions with the foliar venation. The feeding traces were categorized referring to Labandeira et al. (2007), with some modification (Sohn et al., 2017): hole feeding (HF), skeletonization (SK), marginal feeding (MF), surface feeding (SF), piercing/sucking (PS), mining (MI), and galling (GA). Four traces, oviposition, seed predation, fungal, and incertae sedis were excluded from the present study because we focused on arthropod-mediated foliar damage. Of the feeding categories, skeletonization was also excluded because of its rare occurrence in the data. An illustrated catalog of the feeding traces can be found in Sohn et al. (2017). Three feeding guilds were assigned: external feeding (SF, MF, HF, SK), internal feeding (MI, GA), and piercing/sucking (PS). We sorted each feeding trace of insects and other arthropods into a morphotype (DT) using presence (1) and absence (0) and summed these DTs for each leaf. We compared total numbers of DTs and three feeding guilds (EF, IF, and PS) from each site and mountains using ANOVA and t-test implemented in SPSS, 2017 (IBM ver. 25).
Materials and methods We examined the insect herbivory on Mongolian oak trees (Quercus mongolica) occurring in two high mountains: Jirisan Mount. on the mainland of Korea and Hallasan Mount. on Jejudo Island (Fig. 1). Two high elevation sites on each mountain were selected for sampling of the leaves of Mongolian oak (Fig. 1). Mongolian oaks occur in relatively high elevations between 600–1400 m on Jirisan Mount. and between 1200–1400 m on Hallasan Mount. (Kim and Kil, 2000). Considering these distributional ranges of the trees, on Jirisan Mount., the Seongsamjae (SSJ) and Sangseonam (SSA) sites were sampled (Table 1). These sites are both riparian, mixed-deciduous forests facing north. On Hallasan Mount., the Sajebi Hill site (SJB) and the lower Yongsil site (LYS) are riparian, mixeddeciduous forest facing north and west, respectively (Table 1). Oak leaves were collected on 12 September 2015 on Hallasan Mount. and on 21 September 2015 on Jirisan Mount. We sampled the oak leaves at autumn since insect herbivory was accumulated on leaves after leaf unfolding. Only branches at breast height (about 1.2 m above the ground) were considered and six branches with all leaves attached were sampled from three randomly-chosen trees. To minimize possible edge effects, trees at least 10 m away from trails were surveyed. Leaves of all ages were detached from the collected branches, flattened using a standard plant press (BioQuip Co., USA), and stored in a freezer. A total
Results A high percentage of foliar damage was observed at both mountains: 99.6% (245 from 246 leaves) and 96.4% (318 from 330 leaves) showed
Table 1 Site information of four study sites of two mountains of southern South Korea. Mountain
Site name (acronym)
GPS
Jirisan
Seongsamjae (SSJ) Sangseonam (SSA) Sajebi Hill (SJB) Lower Yongsil (LYS)
35°18′20.8″N 35°17′31.5″N 33°22′32.2″N 33°20′54.8″N
Hallasan
127°30′44.6″E 127°29′39.4″E 126°29′58.8″E 126°29′47.6″E
Elevation
Forest type
Tree coverage of Quercus mongolica (%)
1073 682 1410 1210
Mixed-deciduous Mixed-deciduous Mixed-deciduous Mixed-deciduous
40 <1 25 20
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feeding t = 15.69, P < .001, internal feeding t = 1.78, P = .07) (Fig. 4). There was no difference of piercing /sucking damage between two mountains (HL 2.27 ± 1.00, JR 2.34 ± 1.16, t = 0.75, P = .46). The relationship between feeding guilds and elevation showed a consistent pattern at both mountains: external feeding guild was negatively related with elevation and piercing and sucking guild was positively related (Fig. 5). However, leaf damage by the internal feeding guild showed no effect of elevation at the two mountains. Discussion Elevational gradients have been regarded as good proxies when studying the relationships between thermal environment and insect herbivory (Coley and Barone, 1996; Alonso, 1999; Miller et al., 2009; Adams and Zhang, 2009). Those studies revealed a higher intensity of insect herbivory as altitude decreases. Our results partly agreed with this previous finding: the diversity of sum of DTs per leaf was higher in the order of SSA > SSJ in Jirisan Mount. and LYS > SJB in Hallasan Mount. (Figs. 2–4). However, this conclusion remains tentative since our study could not cover all elevational zones in each mountain system because of the narrow altitudinal distribution of Q. mongolica. The level of herbivory on plants is hypothesized by associational resistance (Root, 1973) and associational susceptibility (Barbosa et al., 2009) and both hypotheses are dependent on the breadth of the herbivore's diet and plant species composition (Castagneyrol et al., 2013). Additionally, the herbivory pattern of Q. mongolica was closely associated with seasonal changes in leaf traits such as tannin and nitrogen contents of the tree species (Yoshida, 1985; Kudo, 1996). Thus, the full understanding of mechanism of foliar damage on Mongolian oak needs ecology of herbivores and plant composition of the study sites. In tropical forests, leaf-chewing insects represent the majority of insect herbivores (Novotny et al., 2010). Our results showed that a high proportion of external feeding in the total insect herbivory also occurs in temperate forests (Figs. 3–4). The total amount of external feeding in both mountains was lower at the higher elevation site. Among external feeding, the feeding damage varied depending on the type: marginal feeding damage was the only functional feeding category that responded to elevational gradient in both mountains, whereas hole feeding and surface feeding showed partial responses to the elevational gradient of Hallasan Mount. and Jirisan Mount., respectively. Because of widespread mouthpart and behavioral convergence in the resident insect population, several species of externally feeding insects can cause the same DT to their host plants (Wilf, 2008). This often leads to mismatches between the diversity of leaf-chewing insects and the feeding damage they cause. Carvalho et al. (2014) reported that external feeding damage can be further differentiated once actual feeding activity by the makers is considered. Such subdivision may help improve our understanding of the among-site variation in the external feeding damage that was observed in the present study. In contrast to external feeding, our results showed that internal feeding damage, leaf mining (MI) and gall formation (GA) were unaffected by elevation at both mountains (Fig. 5). The two major internal feeding modes in our study, galling and leaf mining, occurred primarily as one type per leaf and the abundance of gall types on Q. mongolica were not significantly different in our study sites. This result is interesting, given the overall low abundance of DTs on Hallasan Mount. In general, endophytic feeding traces are species-specific and can thus exhibit high variation according to environmental gradients (Crespi et al., 1997; Wilf and Labandeira, 1999; Bairstow et al., 2010). However, Sinclair and Hughes (2008) noted that there was no clear correlation between the diversity of leaf-mining insects and altitudinal gradients. The piercing/sucking damage exhibited significantly lower richness of DTs per leaf at the relatively lower altitudes in both mountains (Fig. 5). This result contradicts the previous observations indicating the lower abundance and diversity of sap-feeding insects at higher latitudes
Fig. 2. Box plot of sum of leaf damages per leaf at two mountains (Hallasan Mountain, SJB: Sajebi Hill, LYS: lower Yongsil, Jirisan Mountain, SSJ: Seongsamjae, SSA: Sangseonam) of southern South Korea. Different alphabet above each bar indicates the significant difference at P < .001.
foliar damages at Jirisan Mount. and Hallasan Mount., respectively. Sum of foliar damage types (DTs) per leaf was significantly higher at Jirisan Mount. (9.72 ± 3.14) than Hallasan Mount. (6.36 ± 2.26) (t = 14.88, P < .001, Fig. 2). Sum of DTs per leaf at four sites was significantly different (F = 77.56, d.f. =3, P < .001), and that of higher elevation was higher at both mountains: Hallasan Mount. SJB (6.57 ± 2.36) > LYS (6.05 ± 2.08), Jirisan Mount. SSJ (10.08 ± 3.00) > SSA (9.26 ± 3.27) (Fig. 2). A total of 78 DTs were assigned to seven functional feeding categories ranked by richness in the order of SF (35.9%), MF (15.4%), MI (15.4%), PS (12.8%), GA (10.3%), HF (9.0%), and SK (1.3%) (Table 2). On Hallasan Mount., foliar damage by external feeding was significantly higher at the lower elevation site, LYS (3.47 ± 1.62) than SJB (2.57 ± 1.38) (t = 5.16, P < .001), but foliar damage by piercing/sucking was opposite, significantly higher at the higher elevation site SJB 2.54 ± 0.94 than LYS (1.81 ± 0.93, t = 6.59, P < .001) (Figs. 3–4). There were no significant differences of foliar damage by internal feeding (SJB 1.00 ± 0.00, LYS 1.00 ± 0.00) between the two sites. On Jirisan Mount., foliar damage by external feeding was significantly higher at the lower elevation site, SSA (6.47 ± 2.54) than at SSJ (5.09 ± 2.15) (t = 4.55, P < .001), while that by piercing/ sucking was opposite (SSJ 2.88 ± 1.05, SSA 1.44 ± 0.65, t = 11.09, P < .001) (Figs. 3–4). There was no difference of foliar damage by internal feeding between the two sites (SSA 1.31 ± 0.62, SSJ 1.15 ± 0.40, t = 1.67, P = .09). Between the two mountains, the foliar damage by external and internal feeding was higher at Jirisan Mount. (external feeding 5.69 ± 2.42, internal feeding 1.25 ± 0.54) than at Hallasan Mount. (external feeding 2.91 ± 1.51, internal feeding 1.00 ± 0.00)(external Table 2 Summary of damage types (DTs) sorted by functional feeding categories at four research sites in Hallasan and Jirisan Mountains. Feeding guild
External feeding Internal feeding Piercing/ sucking
Surface feeding Marginal feeding Hole feeding Skeletonization Mining Galling
Hallasan Mount.
Jirisan Mount.
SJB
LYS
SSJ
SSA
14 10 3 1 2 4 7
15 12 7 0 0 3 8
17 12 4 1 8 3 9
18 12 6 1 7 3 8
Total
28 12 7 1 12 8 10
SJB: Sajebi Hill, LYS: lower Yongsil, SSJ: Seongsamjae, SSA: Sangseonam. 959
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Fig. 3. Sum of leaf damages at two mountains (Hallasan Mountain, SJB: Sajebi Hill, LYS: lower Yongsil, Jirisan Mountain, SSJ: Seongsamjae, SSA: Sangseonam) of southern South Korea. Feeding types are hole feeding (HF), surface feeding (SF), marginal feeding (MF), piercing/sucking (PS), mining (MI) and galling (GA) and feeding guilds are EF (leaves showing external feeding damages from the examined leaves), IF (leaves showing internal feeding damages) and PS (leaves showing piercing/sucking damages).
(Kozlov et al., 2015). The damage caused by sap-sucking insects is often recognized after the associated microbial infestation leaves pathogenic marks. The lower diversity of piercing/sucking damage observed at low-elevation sites (SSA and LYS) from our study may reflect better plant defenses against fungal or bacterial pathogens (Zhang et al., 2015). Our results showed that the diversity of foliar damage by herbivorous insects differed between the two surveyed mountains. The sum of DTs occurring in each leaf of Q. mongolica was nearly two times higher on Jirisan Mount. than Hallasan Mount. (Figs. 2–3). The relatively few observed DTs at Hallasan Mount. seem to partly reflect the geographical setting of the mountain, which is located on an island and
the higher elevation. This relatively low insect diversity on Hallasan Mount. was also observed. Thein and Choi (2016) compared the insect diversity attracted to light traps at both mountains and found that the insect diversity on Hallasan Mount. was lower than that on Jirisan Mount. Island ecosystems are characterized by a lower species density than the mainland (Fisher, 2004). Joy and Crespi (2012) observed a high diversity of gall-inducing flies on islands. The diversity of internally feeding insects is better defined by hygrothermal stress than thermal stress alone (Fernandes and Price, 1988; Fernandes et al., 2004). Hallasan Mount. experienced more precipitation than Jirisan Mount. did in 2015 (Fig. 1). The diversity of leaf-mines in our results may reflect the better performance of the mine-makers on Jirisan Fig. 4. Average of sum of leaf damages per leaf in six feeding guilds at the four research sites (Hallasan Mountain – SJB: Sajebi Hill, LYS: lower Yongsil, Jirisan Mountain – SSJ: Seongsamjae, SSA: Sangseonam) of southern South Korea. Hole feeding (HF), surface feeding (SF), marginal feeding (MF), piercing/sucking (PS), mining (MI) and galling (GA) were shown. Skeletonization was so rare that it was excluded from the comparison. Black bars and lines indicate mean and standard deviation of sum at each site respectively. Letters in lower case above the bars indicate significant differences of sum among the sites measured using Tukey's HSD.
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Declaration of Competing Interest None. Acknowledgements We thank the students at the Ecological Research Laboratory of Mokpo National University (Muan) for their help in collecting samples. The first author appreciates Dr. Conrad Labandeira (National Museum of Natural History, Smithsonian Institution, Washington, DC) for providing several valuable references for this study. All field work was conducted with the permission of the Korea National Park Service. This work was supported by the Korea Research Fellowship program funded by the Ministry of Science, ICT and Future Planning through the National Research Foundation of Korea (2015035581) and the research grant of National Research Foundation of Korea (2018R1D1A1B07046637). References Adams, J.M., Zhang, Y., 2009. Is there more insect folivory in warmer temperate climates? A latitudinal comparison of insect folivory in eastern North America. J. Ecol. 97, 933–940. Adams, J.M., Brusa, A., Ahn, S., Ainuddin, A.N., 2010. Present-day testing of a paleoecological pattern: is there really a latitudinal difference in leaf-feeding insect-damage diversity? Rev. Palaeobot. Palynol. 162, 63–70. Alalouni, U., Brandl, R., Auge, H., Schädler, M., 2014. Does insect herbivory on oak on the diversity of tree stands? Basic Appl. Ecol. 15, 685–692. Alonso, C., 1999. Variation in herbivory by Yponomeuta mahalebella on its only host plant Prunus mahaleb along an elevational gradient. Ecol. Entomol. 24, 371–379. Bairstow, K.A., Clarke, K.L., McGeoch, M.A., Andrew, N.R., 2010. Leaf miner and plant galler species richness on Acacia: relative importance of plant traits and climate. Oecologia 163, 437–448. Barbosa, P., Hines, K., Kaplan, I., Martinson, H., Szezepaniec, A., Szendrei, Z., 2009. Associational resistance and associational susceptibility: having right or wrong neighbors. Annu. Rev. Ecol. Evol. Syst. 40, 1–20. Carvalho, M.R., Wilf, P., Barrios, H., Windsor, D.M., Currano, E.D., Labandeira, C.C., Jaramillo, C.A., 2014. Insect leaf-chewing damage tracks herbivore richness in modern and ancient forest. PLoS One 9, e94950. Castagneyrol, B., Giffard, B., Péré, C., Jactel, H., 2013. Plant apparency, an overlooked driver of associational resistance to insect herbivory. J. Ecol. 101, 418–429. Chang, C.-S., Kim, H., Gil, H.-Y., 2012. A Field Guide to Korean Woody Plants. Designpost Publishing Co, Paju, Korea. Chen, H.Y., Huang, C.J., 1998. Quercus. In: Chinese Academy of Sciences (Ed.), Flora Republicae Popularis Sinicae. vol. 22. Science Press, Beijing, pp. 213–332. Coley, P.D., Barone, J.A., 1996. Herbivory and plant defences in tropical forests. Annu. Rev. Ecol. Syst. 27, 305–335. Crespi, B.J., Carmean, D.A., Chapman, T.W., 1997. Ecology and evolution of galling thrips and their allies. Annu. Rev. Entomol. 42, 51–71. Currano, E.D., Wilf, P., Wing, S.L., Labandeira, C.C., Lovelock, E.C., Royer, D.L., 2008. Sharply increased insect herbivory during the Paleocene-Eocene thermal maximum. Proc. Natl. Acad. Sci. U. S. A. 105, 1960–1964. Currano, E.D., Labandeira, C.C., Wilf, P., 2010. Fossil insect folivory tracks paleotemperature for six million years. Ecol. Monogr. 80, 547–567. DeLucia, E.H., Nabity, P.D., Zavala, Z.A., Berenbaum, M.R., 2012. Climate change: resetting plant-insect interactions. Plant Physiol. 160, 1677–1685. Fernandes, G.W., Price, P.W., 1988. Biogeographical gradients in galling species richness: tests of hypotheses. Oecologia 76, 161–167. Fernandes, G.W., Caldeira Castro, F.M., Faria, M.L., Marques, E.S.A., Barcelos Greco, M.K., 2004. Effects of hygrothermal stress, plant richness, and architecture on mining insect diversity. Biotropica 36, 240–247. Fisher, E., 2004. Island ecosystems: conservation and sustainable use: problems and challenges. Int. J. Isl. Aff. (Special Issue), 9–14. Futuyma, D.J., Agrawal, A.A., 2009. Macroevolution and the biological diversity of plants and herbivores. Proc. Natl. Acad. Sci. U. S. A. 106, 18054–18061. Garibaldi, L.A., Kitzberger, T., Ruggiero, A., 2011. Latitudinal decrease in folivory within Nothofagus pumilio forests: dual effect of climate on insect density and leaf traits. Glob. Ecol. Biogeogr. 20, 609–619. Hougen-Eitzman, D., Rausher, M.D., 1994. Interactions between herbivorous insects and plant-insect coevolution. Am. Nat. 143, 677–697. Joy, J.B., Crespi, B.J., 2012. Island phytophagy: explaining the remarkable diversity of plant-feeding insects. Proc. R. Soc. B 279, 3250–3255. Kaplan, I., Denno, R.F., 2007. Interspecific interactions in phytophagous insects revisited: a quantitative assessment of competition theory. Ecol. Lett. 10, 977–994. Kim, J.-E., Kil, B.-S., 2000. The Mongolian Oak Forest in Korea. Wonkwang University Press, Iksan, Korea. Kong, W.-S., Kim, K., Lee, S., Park, H., Cho, S.-H., 2014. Distribution of high mountain plants and species vulnerability against climate change. J. Environ. Imp. Assess. 23, 119–136. Kozlov, M.V., Stekolshchikov, A.V., Söderman, G., Labina, E.S., Zverev, V., Zvereva, E.L.,
Fig. 5. Sum of leaf damages (DTs) per leaf by three feeding guilds at two different elevations of two mountains of southern South Korea, Hallasan Mountain (HL, red dot with broken line) and Jirisan Mountain (JR, blue dot with line). (A) External feeding guild, (B) Internal feeding guild, and (C) Piercing and sucking guild. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)
Mount., where there is stronger hygrothermal stress (Fig. 1). However, as thermal and water stress can vary by site, micro-climatic data specific to each research site will be needed to test the hypotheses explaining the diversity of leaf-mining and galling insects. Overall, our results support the elevational effect on the diversity of insect-feeding damage, although a broader elevational range needs to be investigated. For this purpose, a community-based, rather than a single host plant-based approach seems to be desirable, as the Mongolian oak shows a narrow elevational distribution. The responses of insect herbivory along environmental gradients at the two mountains differed in each feeding guild. The DT caused by externally feeding insects were affected by elevation to various extents. The piercing and sucking damage was relatively more abundant at lower altitudes. Our study provided a promising example of using observed insect feeding damage to monitor the responses of insect herbivory to environmental changes in temperate montane ecosystems. Environmental gradients are involved in several biotic and abiotic factors, the relative contributions of which need further research. Moreover, as insect herbivory can differ among plant species, more case studies with temperate flora should be conducted to generalize and thus validate the patterns found in the present study. 961
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J.-C. Sohn, et al. 2015. Sap-feeding insects on forest trees along latitudinal gradients in northern Europe: a climate-driven patterns. Glob. Chang. Biol. 21, 106–116. Kudo, G., 1996. Herbivory pattern and induced responses to simulated herbivory in Quercus mongolica var. grosseserrata. Ecol. Res. 11, 183–289. Labandeira, C.C., 2006. The four phases of plant-arthropod associations in deep time. Geol. Acta 4, 409–438. Labandeira, C.C., Wilf, P., Johnson, K.R., Marsh, F., 2007. Guide to insect (and other) damage types on compressed plant fossils, version 3.0. Smithsonian Institution, Washington, DC, USA. Leach, M., Givnish, T., 1999. Gradients in the composition, structure, and diversity of remnant oak savannas in southern Wisconsin. Ecol. Monogr. 69, 353–374. Leckey, E.H., Smith, D.M., Nufio, C.R., Fornash, K.F., 2014. Oak-insect herbivore interactions along a temperature and precipitation gradient. Acta Oecol. 61, 1–8. Lee, Y.G., Sung, J.H., Chun, J.H., Shin, M.Y., 2014. Effect of climate changes on the distribution of productive areas for Quercus mongolica in Korea. J. Kor. For. Soc. 103, 605–612. Lowman, M.D., 1985. Temporal and spatial variability in insect grazing of the canopies of five Australian rainforest tree species. Aust. J. Ecol. 10, 7–24. Miller, T.E.X., Louda, S.M., Rose, K.A., Eckberg, J.O., 2009. Impacts of insect herbivory on cactus population dynamics: experimental demography across an environmental gradient. Ecol. Monogr. 79, 155–172. Nixon, K.C., 1993. Infrageneric classification of Quercus (Fagaceae) and typification of sectional names. Ann. For. Sci. 50, s25–s34. Novotny, V., Miller, S.E., Baje, L., Balagawi, S., Basset, Y., Cizek, L., Dem, F., Drew, R.A.I., Hulcr, J., Leps, J., Lewi, O.T., Pokon, R., Stewart, A.J.A., Samuelson, G.A., Weiblen, G.D., 2010. Guild-specific patterns of species richness and host specialization in plant-herbivore food webs from a tropical forest. J. Anim. Ecol. 79, 1193–1203. Park, J.H., 2014. Phytochemical variation of Quercus mongolica Fisch. ex Ledeb. and Quercus serrata Murray (Fagaceae) in Mt. Jiri, Korea – their taxonomical and ecological implications. Kor. J. Environ. Ecol. 28, 574–587.
Reynolds, B.C., Crossley, D.A., 1997. Spatial variation in herbivory by forest canopy arthropods along an elevation gradient. Environ. Entomol. 26, 1232–1239. Root, R.B., 1973. Organization of a plant-arthropod association in simple and diverse habitats: the fauna of collards (Brassica oleracea). Ecol. Monogr. 43, 95–124. Schoonhoven, L.M., van Loon, J.J.A., Dicke, M., 2005. Insect-Plant Biology, 2nd edition. Oxford University Press, Oxford, UK. Sinclair, R.J., Hughes, L., 2008. Incidence of leaf mining in different vegetation types across rainfall, canopy cover and latitudinal gradients. Austral Ecol. 33, 353–360. Sohn, J.-C., Kim, N.-H., Choi, S.-W., 2017. Morphological and functional diversity of foliar damage on Quercus mongolica Fisch. ex Ledeb. (Fagaceae) by herbivorous insects and pathogenic fungi. J. Asia-Pac. Biodivers. 10, 489–508. SPSS, 2017. IBM SPSS Statistics, Ver. 25. IBM Corp. Swiecki, T.J., Bernhardt, E.A., 2006. A field guide to insects and diseases of California Oaks, general technical report PSW-GTR-197. In: Pacific Southwest Research Station. Forest Service, U.S. Department of Agriculture, Albany, CA, USA. Thein, P.P., Choi, S.-W., 2016. Forest insect assemblages attracted to light trap on two high mountains (Mt. Jirisan and Mt. Hallasan) in South Korea. J. For. Res. 27, 1203–1210. Wilf, P., 2008. Insect-damaged fossil leaves record food web response to ancient climate change and extinction. New Phytol. 178, 486–502. Wilf, P., Labandeira, C.C., 1999. Response of plant-insect associations to PaleoceneEocene warming. Science 284, 2153–2156. Winkler, I.S., Mitter, C., 2008. The phylogenetic dimension of insect/plant interactions: a summary of recent evidence. In: Tilmon, K. (Ed.), Specialization, Speciation, and Radiation: The Evolutionary Biology of Herbivorous Insects. University of California Press, Berkeley, USA, pp. 240–263. Yoshida, K., 1985. Seasonal populations trends of macrolepidopterous larvae on oak trees in Hokkaido, northern Japan. Kontyu 53, 125–133. Zhang, N., Tonsor, S.J., Traw, M.B., 2015. A geographic cline in leaf salicylic acid with increasing elevation in Arabidopsis thaliana. Plant Signal. Behav. 10, e992741.
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Full length article
Effect of elevation on the insect herbivory of Mongolian oaks in the high mountains of southern South Korea
T
Jae-Cheon Sohna, Nang-Hee Kimb, Sei-Woong Choic,
⁎
a
Department of Science Education, Gongju National University of Education, Gongju, Chungnam 32553, Republic of Korea Division of Industrial Insect, National Institute of Agricultural Sciences, Rural Development Administration, Wanju, Jeonbuk 55365, Republic of Korea c Department of Environmental Education, Mokpo National University, Muan, Jeonnam 58554, Republic of Korea b
ARTICLE INFO
ABSTRACT
Keywords: Elevational gradient Feeding guilds Insect-feeding damage types Island Mongolian oak
Elevation is strongly associated with the diversity and ecology of plants and animals. We explored how elevation affects herbivores on one of the major cool-temperate trees, Quercus mongolica, in southern South Korea. The feeding activities of insect herbivores were measured through insect-feeding damage on leaves. Of 78 types of insect-feeding damage that were observed from Jirisan Mountain (Mount.) and Hallasan Mount. in Korea, 61.6% was associated with externally feeding insects. The sum of feeding damages per leaf was significantly higher on Jirisan Mount. than on Hallasan Mount., and higher at higher elevation in both mountains. Two feeding guilds, externally feeding, and piercing and sucking were strongly related with elevation, but the relationship was opposite depending on feeding guild. Leaf damage by the internal feeding guild showed no effect of elevation at the two mountains. These study results showed that insect herbivory responds to elevational differences in temperate forests, and that such response can vary among feeding guilds.
Introduction Plants and herbivorous insects comprise a large proportion of terrestrial biodiversity and their extant diversity is most likely due to the evolution of various interactions between them (Hougen-Eitzman and Rausher, 1994; Winkler and Mitter, 2008; Futuyma and Agrawal, 2009). Foliar damage is defined as the removal or deformation of foliar tissues not only by physical forces but also chemical interactions from insects, other arthropods and pathogenic fungi. In particular, insectfeeding damage is any trace involving the feeding activity of terrestrial arthropods (insects and mites), sometimes followed by host healing process or by fungal infection. It is often distinctive and diagnosable in relation to the functional morphology of damage-makers (Labandeira et al., 2007). A morpho-type system of the damage can serve as an indicator of diversity in plant-arthropod interactions. Such a system has been used to study the effects of extant or ancient environmental gradients on insect herbivory (Wilf and Labandeira, 1999; Currano et al., 2008, 2010; Adams et al., 2010) and the evolutionary diversification of the insect groups (Labandeira, 2006). Insect herbivory is known to be influenced by biotic or abiotic factors (Schoonhoven et al., 2005). Biotic factors affecting insectmediated damage on plants include trophic cascades (Kaplan and Denno, 2007), existing species diversity (Alalouni et al., 2014), and the ⁎
physiological conditions of host plants (Leckey et al., 2014). Insectfeeding damage on plants varies according to physical environmental conditions such as temperature (Garibaldi et al., 2011), humidity (Fernandes and Price, 1988), and solar radiation (Lowman, 1985; Reynolds and Crossley, 1997). Increasing efforts have been made to monitor environmental changes through insect-feeding damage to plants (Adams et al., 2010; DeLucia et al., 2012; Carvalho et al., 2014). Oaks (Quercus spp.) are common trees in northern temperate vegetation (Nixon, 1993). They play a fundamental role in terrestrial ecosystems as hosts for numerous insect herbivores that are an important food source for other high-trophic animals (Leach and Givnish, 1999; Swiecki and Bernhardt, 2006). About eleven species of oaks that differ in morphological and physiological traits are distributed in Korea (Chang et al., 2012). The Mongolian oak (Quercus mongolica Fisch. ex Ledeb.) is one of the main components in the East Asian deciduous forests (Chen and Huang, 1998) and it is also quite common in Korean cool-temperate mountains (Park, 2014; Kong et al., 2014). This study is part of a long-term project intended to model possible responses of plant-insect interactions in Korea upon global climate change. Mongolian oak is regarded as one of the Korean plants that could be threatened by climate change (Lee et al., 2014). We examined insect-feeding damage on Mongolian oak at two high-elevation mountains in the southern part of South Korea: Jirisan Mountain (Mount.)
Corresponding author. E-mail address: [email protected] (S.-W. Choi).
https://doi.org/10.1016/j.aspen.2019.08.004 Received 10 June 2019; Received in revised form 6 August 2019; Accepted 8 August 2019 Available online 09 August 2019 1226-8615/ © 2019 Korean Society of Applied Entomology. Published by Elsevier B.V. All rights reserved.
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Fig. 1. (a) Map of the study sites in Jirisan Mountain and Hallasan Mountain, South Korea (A: Seongsamjae, B: Sangseonam, C: Sajebi Hill, D: lower Yongsil). (b) Monthly average temperatures in 2015 from Namwon (gray circles and lines) and Seogwipo (open circles and black lines) adjacent to Jirisan Mountain and Hallasan Mountain respectively. (c) Monthly accumulated precipitation in 2015 from Namwon (white bars) and Seogwipo (black bars).
(max elevation 1915 m above sea level) and Hallasan Mount. (max elevation 1950 m a.s.l.). We investigated 1) whether there is significant difference of insect feeding damage to oak trees along elevational gradients in two high mountains, and 2) whether there is any difference in the relative abundance of each functional feeding-damage group between the two mountains.
of 140, 106, 199 and 131 leaves were sampled from SSJ, SSA, SJB, and LYS, respectively. Feeding traces associated with feeding activities of insects and mites on the leaves were counted under a stereoscope (Leica EZ4, Leica Co.) and photographed as necessary, using a digital camera (Nikon D30, Nikon Co.) attached to a stereoscope (Leica L2, Leica Co.). Types of insect-feeding damage (hereafter abbreviated as DT [= damage type]) were determined using their morphological characteristics, positions on the leaves, and interactions with the foliar venation. The feeding traces were categorized referring to Labandeira et al. (2007), with some modification (Sohn et al., 2017): hole feeding (HF), skeletonization (SK), marginal feeding (MF), surface feeding (SF), piercing/sucking (PS), mining (MI), and galling (GA). Four traces, oviposition, seed predation, fungal, and incertae sedis were excluded from the present study because we focused on arthropod-mediated foliar damage. Of the feeding categories, skeletonization was also excluded because of its rare occurrence in the data. An illustrated catalog of the feeding traces can be found in Sohn et al. (2017). Three feeding guilds were assigned: external feeding (SF, MF, HF, SK), internal feeding (MI, GA), and piercing/sucking (PS). We sorted each feeding trace of insects and other arthropods into a morphotype (DT) using presence (1) and absence (0) and summed these DTs for each leaf. We compared total numbers of DTs and three feeding guilds (EF, IF, and PS) from each site and mountains using ANOVA and t-test implemented in SPSS, 2017 (IBM ver. 25).
Materials and methods We examined the insect herbivory on Mongolian oak trees (Quercus mongolica) occurring in two high mountains: Jirisan Mount. on the mainland of Korea and Hallasan Mount. on Jejudo Island (Fig. 1). Two high elevation sites on each mountain were selected for sampling of the leaves of Mongolian oak (Fig. 1). Mongolian oaks occur in relatively high elevations between 600–1400 m on Jirisan Mount. and between 1200–1400 m on Hallasan Mount. (Kim and Kil, 2000). Considering these distributional ranges of the trees, on Jirisan Mount., the Seongsamjae (SSJ) and Sangseonam (SSA) sites were sampled (Table 1). These sites are both riparian, mixed-deciduous forests facing north. On Hallasan Mount., the Sajebi Hill site (SJB) and the lower Yongsil site (LYS) are riparian, mixeddeciduous forest facing north and west, respectively (Table 1). Oak leaves were collected on 12 September 2015 on Hallasan Mount. and on 21 September 2015 on Jirisan Mount. We sampled the oak leaves at autumn since insect herbivory was accumulated on leaves after leaf unfolding. Only branches at breast height (about 1.2 m above the ground) were considered and six branches with all leaves attached were sampled from three randomly-chosen trees. To minimize possible edge effects, trees at least 10 m away from trails were surveyed. Leaves of all ages were detached from the collected branches, flattened using a standard plant press (BioQuip Co., USA), and stored in a freezer. A total
Results A high percentage of foliar damage was observed at both mountains: 99.6% (245 from 246 leaves) and 96.4% (318 from 330 leaves) showed
Table 1 Site information of four study sites of two mountains of southern South Korea. Mountain
Site name (acronym)
GPS
Jirisan
Seongsamjae (SSJ) Sangseonam (SSA) Sajebi Hill (SJB) Lower Yongsil (LYS)
35°18′20.8″N 35°17′31.5″N 33°22′32.2″N 33°20′54.8″N
Hallasan
127°30′44.6″E 127°29′39.4″E 126°29′58.8″E 126°29′47.6″E
Elevation
Forest type
Tree coverage of Quercus mongolica (%)
1073 682 1410 1210
Mixed-deciduous Mixed-deciduous Mixed-deciduous Mixed-deciduous
40 <1 25 20
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feeding t = 15.69, P < .001, internal feeding t = 1.78, P = .07) (Fig. 4). There was no difference of piercing /sucking damage between two mountains (HL 2.27 ± 1.00, JR 2.34 ± 1.16, t = 0.75, P = .46). The relationship between feeding guilds and elevation showed a consistent pattern at both mountains: external feeding guild was negatively related with elevation and piercing and sucking guild was positively related (Fig. 5). However, leaf damage by the internal feeding guild showed no effect of elevation at the two mountains. Discussion Elevational gradients have been regarded as good proxies when studying the relationships between thermal environment and insect herbivory (Coley and Barone, 1996; Alonso, 1999; Miller et al., 2009; Adams and Zhang, 2009). Those studies revealed a higher intensity of insect herbivory as altitude decreases. Our results partly agreed with this previous finding: the diversity of sum of DTs per leaf was higher in the order of SSA > SSJ in Jirisan Mount. and LYS > SJB in Hallasan Mount. (Figs. 2–4). However, this conclusion remains tentative since our study could not cover all elevational zones in each mountain system because of the narrow altitudinal distribution of Q. mongolica. The level of herbivory on plants is hypothesized by associational resistance (Root, 1973) and associational susceptibility (Barbosa et al., 2009) and both hypotheses are dependent on the breadth of the herbivore's diet and plant species composition (Castagneyrol et al., 2013). Additionally, the herbivory pattern of Q. mongolica was closely associated with seasonal changes in leaf traits such as tannin and nitrogen contents of the tree species (Yoshida, 1985; Kudo, 1996). Thus, the full understanding of mechanism of foliar damage on Mongolian oak needs ecology of herbivores and plant composition of the study sites. In tropical forests, leaf-chewing insects represent the majority of insect herbivores (Novotny et al., 2010). Our results showed that a high proportion of external feeding in the total insect herbivory also occurs in temperate forests (Figs. 3–4). The total amount of external feeding in both mountains was lower at the higher elevation site. Among external feeding, the feeding damage varied depending on the type: marginal feeding damage was the only functional feeding category that responded to elevational gradient in both mountains, whereas hole feeding and surface feeding showed partial responses to the elevational gradient of Hallasan Mount. and Jirisan Mount., respectively. Because of widespread mouthpart and behavioral convergence in the resident insect population, several species of externally feeding insects can cause the same DT to their host plants (Wilf, 2008). This often leads to mismatches between the diversity of leaf-chewing insects and the feeding damage they cause. Carvalho et al. (2014) reported that external feeding damage can be further differentiated once actual feeding activity by the makers is considered. Such subdivision may help improve our understanding of the among-site variation in the external feeding damage that was observed in the present study. In contrast to external feeding, our results showed that internal feeding damage, leaf mining (MI) and gall formation (GA) were unaffected by elevation at both mountains (Fig. 5). The two major internal feeding modes in our study, galling and leaf mining, occurred primarily as one type per leaf and the abundance of gall types on Q. mongolica were not significantly different in our study sites. This result is interesting, given the overall low abundance of DTs on Hallasan Mount. In general, endophytic feeding traces are species-specific and can thus exhibit high variation according to environmental gradients (Crespi et al., 1997; Wilf and Labandeira, 1999; Bairstow et al., 2010). However, Sinclair and Hughes (2008) noted that there was no clear correlation between the diversity of leaf-mining insects and altitudinal gradients. The piercing/sucking damage exhibited significantly lower richness of DTs per leaf at the relatively lower altitudes in both mountains (Fig. 5). This result contradicts the previous observations indicating the lower abundance and diversity of sap-feeding insects at higher latitudes
Fig. 2. Box plot of sum of leaf damages per leaf at two mountains (Hallasan Mountain, SJB: Sajebi Hill, LYS: lower Yongsil, Jirisan Mountain, SSJ: Seongsamjae, SSA: Sangseonam) of southern South Korea. Different alphabet above each bar indicates the significant difference at P < .001.
foliar damages at Jirisan Mount. and Hallasan Mount., respectively. Sum of foliar damage types (DTs) per leaf was significantly higher at Jirisan Mount. (9.72 ± 3.14) than Hallasan Mount. (6.36 ± 2.26) (t = 14.88, P < .001, Fig. 2). Sum of DTs per leaf at four sites was significantly different (F = 77.56, d.f. =3, P < .001), and that of higher elevation was higher at both mountains: Hallasan Mount. SJB (6.57 ± 2.36) > LYS (6.05 ± 2.08), Jirisan Mount. SSJ (10.08 ± 3.00) > SSA (9.26 ± 3.27) (Fig. 2). A total of 78 DTs were assigned to seven functional feeding categories ranked by richness in the order of SF (35.9%), MF (15.4%), MI (15.4%), PS (12.8%), GA (10.3%), HF (9.0%), and SK (1.3%) (Table 2). On Hallasan Mount., foliar damage by external feeding was significantly higher at the lower elevation site, LYS (3.47 ± 1.62) than SJB (2.57 ± 1.38) (t = 5.16, P < .001), but foliar damage by piercing/sucking was opposite, significantly higher at the higher elevation site SJB 2.54 ± 0.94 than LYS (1.81 ± 0.93, t = 6.59, P < .001) (Figs. 3–4). There were no significant differences of foliar damage by internal feeding (SJB 1.00 ± 0.00, LYS 1.00 ± 0.00) between the two sites. On Jirisan Mount., foliar damage by external feeding was significantly higher at the lower elevation site, SSA (6.47 ± 2.54) than at SSJ (5.09 ± 2.15) (t = 4.55, P < .001), while that by piercing/ sucking was opposite (SSJ 2.88 ± 1.05, SSA 1.44 ± 0.65, t = 11.09, P < .001) (Figs. 3–4). There was no difference of foliar damage by internal feeding between the two sites (SSA 1.31 ± 0.62, SSJ 1.15 ± 0.40, t = 1.67, P = .09). Between the two mountains, the foliar damage by external and internal feeding was higher at Jirisan Mount. (external feeding 5.69 ± 2.42, internal feeding 1.25 ± 0.54) than at Hallasan Mount. (external feeding 2.91 ± 1.51, internal feeding 1.00 ± 0.00)(external Table 2 Summary of damage types (DTs) sorted by functional feeding categories at four research sites in Hallasan and Jirisan Mountains. Feeding guild
External feeding Internal feeding Piercing/ sucking
Surface feeding Marginal feeding Hole feeding Skeletonization Mining Galling
Hallasan Mount.
Jirisan Mount.
SJB
LYS
SSJ
SSA
14 10 3 1 2 4 7
15 12 7 0 0 3 8
17 12 4 1 8 3 9
18 12 6 1 7 3 8
Total
28 12 7 1 12 8 10
SJB: Sajebi Hill, LYS: lower Yongsil, SSJ: Seongsamjae, SSA: Sangseonam. 959
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Fig. 3. Sum of leaf damages at two mountains (Hallasan Mountain, SJB: Sajebi Hill, LYS: lower Yongsil, Jirisan Mountain, SSJ: Seongsamjae, SSA: Sangseonam) of southern South Korea. Feeding types are hole feeding (HF), surface feeding (SF), marginal feeding (MF), piercing/sucking (PS), mining (MI) and galling (GA) and feeding guilds are EF (leaves showing external feeding damages from the examined leaves), IF (leaves showing internal feeding damages) and PS (leaves showing piercing/sucking damages).
(Kozlov et al., 2015). The damage caused by sap-sucking insects is often recognized after the associated microbial infestation leaves pathogenic marks. The lower diversity of piercing/sucking damage observed at low-elevation sites (SSA and LYS) from our study may reflect better plant defenses against fungal or bacterial pathogens (Zhang et al., 2015). Our results showed that the diversity of foliar damage by herbivorous insects differed between the two surveyed mountains. The sum of DTs occurring in each leaf of Q. mongolica was nearly two times higher on Jirisan Mount. than Hallasan Mount. (Figs. 2–3). The relatively few observed DTs at Hallasan Mount. seem to partly reflect the geographical setting of the mountain, which is located on an island and
the higher elevation. This relatively low insect diversity on Hallasan Mount. was also observed. Thein and Choi (2016) compared the insect diversity attracted to light traps at both mountains and found that the insect diversity on Hallasan Mount. was lower than that on Jirisan Mount. Island ecosystems are characterized by a lower species density than the mainland (Fisher, 2004). Joy and Crespi (2012) observed a high diversity of gall-inducing flies on islands. The diversity of internally feeding insects is better defined by hygrothermal stress than thermal stress alone (Fernandes and Price, 1988; Fernandes et al., 2004). Hallasan Mount. experienced more precipitation than Jirisan Mount. did in 2015 (Fig. 1). The diversity of leaf-mines in our results may reflect the better performance of the mine-makers on Jirisan Fig. 4. Average of sum of leaf damages per leaf in six feeding guilds at the four research sites (Hallasan Mountain – SJB: Sajebi Hill, LYS: lower Yongsil, Jirisan Mountain – SSJ: Seongsamjae, SSA: Sangseonam) of southern South Korea. Hole feeding (HF), surface feeding (SF), marginal feeding (MF), piercing/sucking (PS), mining (MI) and galling (GA) were shown. Skeletonization was so rare that it was excluded from the comparison. Black bars and lines indicate mean and standard deviation of sum at each site respectively. Letters in lower case above the bars indicate significant differences of sum among the sites measured using Tukey's HSD.
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Declaration of Competing Interest None. Acknowledgements We thank the students at the Ecological Research Laboratory of Mokpo National University (Muan) for their help in collecting samples. The first author appreciates Dr. Conrad Labandeira (National Museum of Natural History, Smithsonian Institution, Washington, DC) for providing several valuable references for this study. All field work was conducted with the permission of the Korea National Park Service. This work was supported by the Korea Research Fellowship program funded by the Ministry of Science, ICT and Future Planning through the National Research Foundation of Korea (2015035581) and the research grant of National Research Foundation of Korea (2018R1D1A1B07046637). References Adams, J.M., Zhang, Y., 2009. Is there more insect folivory in warmer temperate climates? A latitudinal comparison of insect folivory in eastern North America. J. Ecol. 97, 933–940. Adams, J.M., Brusa, A., Ahn, S., Ainuddin, A.N., 2010. Present-day testing of a paleoecological pattern: is there really a latitudinal difference in leaf-feeding insect-damage diversity? Rev. Palaeobot. Palynol. 162, 63–70. Alalouni, U., Brandl, R., Auge, H., Schädler, M., 2014. Does insect herbivory on oak on the diversity of tree stands? Basic Appl. Ecol. 15, 685–692. Alonso, C., 1999. Variation in herbivory by Yponomeuta mahalebella on its only host plant Prunus mahaleb along an elevational gradient. Ecol. Entomol. 24, 371–379. Bairstow, K.A., Clarke, K.L., McGeoch, M.A., Andrew, N.R., 2010. Leaf miner and plant galler species richness on Acacia: relative importance of plant traits and climate. Oecologia 163, 437–448. Barbosa, P., Hines, K., Kaplan, I., Martinson, H., Szezepaniec, A., Szendrei, Z., 2009. Associational resistance and associational susceptibility: having right or wrong neighbors. Annu. Rev. Ecol. Evol. Syst. 40, 1–20. Carvalho, M.R., Wilf, P., Barrios, H., Windsor, D.M., Currano, E.D., Labandeira, C.C., Jaramillo, C.A., 2014. Insect leaf-chewing damage tracks herbivore richness in modern and ancient forest. PLoS One 9, e94950. Castagneyrol, B., Giffard, B., Péré, C., Jactel, H., 2013. Plant apparency, an overlooked driver of associational resistance to insect herbivory. J. Ecol. 101, 418–429. Chang, C.-S., Kim, H., Gil, H.-Y., 2012. A Field Guide to Korean Woody Plants. Designpost Publishing Co, Paju, Korea. Chen, H.Y., Huang, C.J., 1998. Quercus. In: Chinese Academy of Sciences (Ed.), Flora Republicae Popularis Sinicae. vol. 22. Science Press, Beijing, pp. 213–332. Coley, P.D., Barone, J.A., 1996. Herbivory and plant defences in tropical forests. Annu. Rev. Ecol. Syst. 27, 305–335. Crespi, B.J., Carmean, D.A., Chapman, T.W., 1997. Ecology and evolution of galling thrips and their allies. Annu. Rev. Entomol. 42, 51–71. Currano, E.D., Wilf, P., Wing, S.L., Labandeira, C.C., Lovelock, E.C., Royer, D.L., 2008. Sharply increased insect herbivory during the Paleocene-Eocene thermal maximum. Proc. Natl. Acad. Sci. U. S. A. 105, 1960–1964. Currano, E.D., Labandeira, C.C., Wilf, P., 2010. Fossil insect folivory tracks paleotemperature for six million years. Ecol. Monogr. 80, 547–567. DeLucia, E.H., Nabity, P.D., Zavala, Z.A., Berenbaum, M.R., 2012. Climate change: resetting plant-insect interactions. Plant Physiol. 160, 1677–1685. Fernandes, G.W., Price, P.W., 1988. Biogeographical gradients in galling species richness: tests of hypotheses. Oecologia 76, 161–167. Fernandes, G.W., Caldeira Castro, F.M., Faria, M.L., Marques, E.S.A., Barcelos Greco, M.K., 2004. Effects of hygrothermal stress, plant richness, and architecture on mining insect diversity. Biotropica 36, 240–247. Fisher, E., 2004. Island ecosystems: conservation and sustainable use: problems and challenges. Int. J. Isl. Aff. (Special Issue), 9–14. Futuyma, D.J., Agrawal, A.A., 2009. Macroevolution and the biological diversity of plants and herbivores. Proc. Natl. Acad. Sci. U. S. A. 106, 18054–18061. Garibaldi, L.A., Kitzberger, T., Ruggiero, A., 2011. Latitudinal decrease in folivory within Nothofagus pumilio forests: dual effect of climate on insect density and leaf traits. Glob. Ecol. Biogeogr. 20, 609–619. Hougen-Eitzman, D., Rausher, M.D., 1994. Interactions between herbivorous insects and plant-insect coevolution. Am. Nat. 143, 677–697. Joy, J.B., Crespi, B.J., 2012. Island phytophagy: explaining the remarkable diversity of plant-feeding insects. Proc. R. Soc. B 279, 3250–3255. Kaplan, I., Denno, R.F., 2007. Interspecific interactions in phytophagous insects revisited: a quantitative assessment of competition theory. Ecol. Lett. 10, 977–994. Kim, J.-E., Kil, B.-S., 2000. The Mongolian Oak Forest in Korea. Wonkwang University Press, Iksan, Korea. Kong, W.-S., Kim, K., Lee, S., Park, H., Cho, S.-H., 2014. Distribution of high mountain plants and species vulnerability against climate change. J. Environ. Imp. Assess. 23, 119–136. Kozlov, M.V., Stekolshchikov, A.V., Söderman, G., Labina, E.S., Zverev, V., Zvereva, E.L.,
Fig. 5. Sum of leaf damages (DTs) per leaf by three feeding guilds at two different elevations of two mountains of southern South Korea, Hallasan Mountain (HL, red dot with broken line) and Jirisan Mountain (JR, blue dot with line). (A) External feeding guild, (B) Internal feeding guild, and (C) Piercing and sucking guild. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)
Mount., where there is stronger hygrothermal stress (Fig. 1). However, as thermal and water stress can vary by site, micro-climatic data specific to each research site will be needed to test the hypotheses explaining the diversity of leaf-mining and galling insects. Overall, our results support the elevational effect on the diversity of insect-feeding damage, although a broader elevational range needs to be investigated. For this purpose, a community-based, rather than a single host plant-based approach seems to be desirable, as the Mongolian oak shows a narrow elevational distribution. The responses of insect herbivory along environmental gradients at the two mountains differed in each feeding guild. The DT caused by externally feeding insects were affected by elevation to various extents. The piercing and sucking damage was relatively more abundant at lower altitudes. Our study provided a promising example of using observed insect feeding damage to monitor the responses of insect herbivory to environmental changes in temperate montane ecosystems. Environmental gradients are involved in several biotic and abiotic factors, the relative contributions of which need further research. Moreover, as insect herbivory can differ among plant species, more case studies with temperate flora should be conducted to generalize and thus validate the patterns found in the present study. 961
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J.-C. Sohn, et al. 2015. Sap-feeding insects on forest trees along latitudinal gradients in northern Europe: a climate-driven patterns. Glob. Chang. Biol. 21, 106–116. Kudo, G., 1996. Herbivory pattern and induced responses to simulated herbivory in Quercus mongolica var. grosseserrata. Ecol. Res. 11, 183–289. Labandeira, C.C., 2006. The four phases of plant-arthropod associations in deep time. Geol. Acta 4, 409–438. Labandeira, C.C., Wilf, P., Johnson, K.R., Marsh, F., 2007. Guide to insect (and other) damage types on compressed plant fossils, version 3.0. Smithsonian Institution, Washington, DC, USA. Leach, M., Givnish, T., 1999. Gradients in the composition, structure, and diversity of remnant oak savannas in southern Wisconsin. Ecol. Monogr. 69, 353–374. Leckey, E.H., Smith, D.M., Nufio, C.R., Fornash, K.F., 2014. Oak-insect herbivore interactions along a temperature and precipitation gradient. Acta Oecol. 61, 1–8. Lee, Y.G., Sung, J.H., Chun, J.H., Shin, M.Y., 2014. Effect of climate changes on the distribution of productive areas for Quercus mongolica in Korea. J. Kor. For. Soc. 103, 605–612. Lowman, M.D., 1985. Temporal and spatial variability in insect grazing of the canopies of five Australian rainforest tree species. Aust. J. Ecol. 10, 7–24. Miller, T.E.X., Louda, S.M., Rose, K.A., Eckberg, J.O., 2009. Impacts of insect herbivory on cactus population dynamics: experimental demography across an environmental gradient. Ecol. Monogr. 79, 155–172. Nixon, K.C., 1993. Infrageneric classification of Quercus (Fagaceae) and typification of sectional names. Ann. For. Sci. 50, s25–s34. Novotny, V., Miller, S.E., Baje, L., Balagawi, S., Basset, Y., Cizek, L., Dem, F., Drew, R.A.I., Hulcr, J., Leps, J., Lewi, O.T., Pokon, R., Stewart, A.J.A., Samuelson, G.A., Weiblen, G.D., 2010. Guild-specific patterns of species richness and host specialization in plant-herbivore food webs from a tropical forest. J. Anim. Ecol. 79, 1193–1203. Park, J.H., 2014. Phytochemical variation of Quercus mongolica Fisch. ex Ledeb. and Quercus serrata Murray (Fagaceae) in Mt. Jiri, Korea – their taxonomical and ecological implications. Kor. J. Environ. Ecol. 28, 574–587.
Reynolds, B.C., Crossley, D.A., 1997. Spatial variation in herbivory by forest canopy arthropods along an elevation gradient. Environ. Entomol. 26, 1232–1239. Root, R.B., 1973. Organization of a plant-arthropod association in simple and diverse habitats: the fauna of collards (Brassica oleracea). Ecol. Monogr. 43, 95–124. Schoonhoven, L.M., van Loon, J.J.A., Dicke, M., 2005. Insect-Plant Biology, 2nd edition. Oxford University Press, Oxford, UK. Sinclair, R.J., Hughes, L., 2008. Incidence of leaf mining in different vegetation types across rainfall, canopy cover and latitudinal gradients. Austral Ecol. 33, 353–360. Sohn, J.-C., Kim, N.-H., Choi, S.-W., 2017. Morphological and functional diversity of foliar damage on Quercus mongolica Fisch. ex Ledeb. (Fagaceae) by herbivorous insects and pathogenic fungi. J. Asia-Pac. Biodivers. 10, 489–508. SPSS, 2017. IBM SPSS Statistics, Ver. 25. IBM Corp. Swiecki, T.J., Bernhardt, E.A., 2006. A field guide to insects and diseases of California Oaks, general technical report PSW-GTR-197. In: Pacific Southwest Research Station. Forest Service, U.S. Department of Agriculture, Albany, CA, USA. Thein, P.P., Choi, S.-W., 2016. Forest insect assemblages attracted to light trap on two high mountains (Mt. Jirisan and Mt. Hallasan) in South Korea. J. For. Res. 27, 1203–1210. Wilf, P., 2008. Insect-damaged fossil leaves record food web response to ancient climate change and extinction. New Phytol. 178, 486–502. Wilf, P., Labandeira, C.C., 1999. Response of plant-insect associations to PaleoceneEocene warming. Science 284, 2153–2156. Winkler, I.S., Mitter, C., 2008. The phylogenetic dimension of insect/plant interactions: a summary of recent evidence. In: Tilmon, K. (Ed.), Specialization, Speciation, and Radiation: The Evolutionary Biology of Herbivorous Insects. University of California Press, Berkeley, USA, pp. 240–263. Yoshida, K., 1985. Seasonal populations trends of macrolepidopterous larvae on oak trees in Hokkaido, northern Japan. Kontyu 53, 125–133. Zhang, N., Tonsor, S.J., Traw, M.B., 2015. A geographic cline in leaf salicylic acid with increasing elevation in Arabidopsis thaliana. Plant Signal. Behav. 10, e992741.
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