A paradox of latitudinal leaf defense strategies in deciduous and evergreen broadleaved trees

A paradox of latitudinal leaf defense strategies in deciduous and evergreen broadleaved trees Ecol Res DOI 10.1007/s11284-018-1614-0 ORIGINAL ARTICLE Saihanna Saihanna Tomoe Tanaka • • Yu Okamura Buntarou Kusumoto • • Takayuki Shiono Toshihide Hirao Yasuhiro Kubota Masashi Murakami A paradox of latitudinal leaf defense strategies in deciduous and evergreen broadleaved trees Received: 21 September 2017 / Accepted: 9 April 2018 The Author(s) 2018, corrected publication July 2018 Abstract The classical ‘‘low latitude–high defense’’ species exhibited opposite latitudinal defense patterns. hypothesis is seldom supported by empirical evidence. In The ‘‘low latitude high defense’’ hypothesis included a this context, we tested latitudinal patterns in the leaf paradoxical aspect in chemical and physical defense defense traits of deciduous broadleaved (DB) and ever- traits across broadleaved tree species. To reconcile green broadleaved (EGB) tree species, which are ex- paradoxical defense strategies along the latitudinal gra- pected to affect herbivore diversity. We examined the co- dient, we conclude that interactive correlations among occurrence of leaf defense traits (tannin and phenol leaf traits are controlled by leaf longevity, which differs content, leaf mechanical strength, leaf dry matter con- between DB and EGB tree species. tent, leaf mass per area, and leaf thickness) in 741 broadleaved tree species and their correlations with Keywords Chemical defense Æ Phenol Æ Physical species geographical range in East Asian island flora. We defense Æ Plant–animal interactions Æ Tannin discovered contrasting latitudinal defense strategy gra- dients in DB and EGB tree species. DB species employed chemical defenses (increasing tannin and phenol con- Introduction tent) at higher latitudes and physical defenses (softer and thinner leaves) at lower latitudes, whereas EGB tree Biologicalinteractions amongorganisms arebelieved widely to intensify at lower latitudes (Lewinsohn and Roslin 2008), leading to the development of latitudinal diversity gradient Electronic supplementary material The online version of this article (LDG) hypotheses to explain large–scale biodiversity pat- (https://doi.org/10.1007/s11284-018-1614-0) contains supplemen terns (Dobzhansky 1950; MacArthur 1972; Pennings and tary material, which is available to authorized users. Silliman 2005). As plants and herbivores comprise at least The original version of this article was revised due to a retrospec- 40% of global terrestrial biodiversity (Price 2002), evalua- tive Open Access order. tion of the consequences of plant–herbivore interaction on the LDG should attract much interest (Marquis et al. 2012). S. Saihanna Æ Y. Okamura Æ M. Murakami (&) Faculty of Science, Chiba University, Chiba, Japan Several studies have examined the ‘‘low latitude high de- E-mail: muramasa@faculty.chiba-u.jp fense’’ (LLHD) hypothesis (Bolser and Hay 1996)which Tel.: +81-43-260-3929 posits that plant species distributed at lower latitudes will show higher degrees of defense (Dobzhansky 1950,Coley T. Tanaka Æ T. Shiono Æ Y. Kubota (&) and Aide 1991,Schmitt et al. 1995). Although these studies Faculty of Science, University of the Ryukyus, Nishihara, Okinawa, Japan havebeenconducted withtheaim ofconfirmingalatitudinal E-mail: kubota.yasuhiro@gmail.com gradient in defense strength (Moles et al. 2011), few have Tel.: +81-98-895-8561 found support for the hypothesis. Moles et al. (2011) performed a meta–analysis of de- B. Kusumoto Center for Strategic Research Project, University of the Ryukyus, fense trait data, both chemical (tannins and phenols, fla- Nishihara, Okinawa, Japan vonoids, alkaloids etc.) and physical (physical toughness, extrafloral nectaries etc.) defense traits, across a wide range T. Hirao of latitude, and found conflicting trends in response to Chichibu Forest, Graduate School of Agricultural and Life Sciences, The University of Tokyo, Chichibu, Saitama, Japan predictions based on the LLHD hypothesis, with increas- ing and decreasing gradients, as well as nonsignificant Y. Kubota trends, in plant defense traits across latitudes. One pitfall of Marine and Terrestrial Field Ecology, Tropical Biosphere Research this study is the large bias caused by variation in various Center, University of the Ryukyus, Nishihara, Okinawa, Japan plant functional types among individual studies (Sitch et al. function as defense against herbivores: tannin and phenol 2003), which reduced the statistical power to detect or contents (%), leaf mechanical strength (g cm ), leaf dry identify specific latitudinal gradients in the targeted trait matter content (LDMC, %), leaf mass per area (LMA, variables. For the broadleaved (BL) tree species, several gcm ), and leaf thickness (lm). To build a dataset of leaf functional types (or groups), e.g., trees or shrubs, N fixers defense traits, we collected five replicate trees over the or not, are recognized (Wright et al. 2004; Kattge et al. distributional range of each species across the East Asian 2011). Among them, the contrast between deciduous islands, including the Ryukyu Islands. The latitudinal broadleaved (DB) and evergreen broadleaved (EGB) tree range of samplings was from 24Nto45N. Four shoots species should be the most evident (Wright et al. 2004). For with leaves were collected from each five-tree, and average example, Wright et al. (2005) showed clear contrast be- values of each tree individual were calculated (Shiono et al. tween DB and EGB tree species in leaf longevity along 2015). In the field, we harvested shoots with healthy and latitude. Thus, the separation of these functional types, fully mature leaves. In the laboratory, we visually inspected namely DB vs. EGB, might clarify the conflicting trends in the collected shoots to exclude immature and senescent latitudinal gradient in plant defense traits. On the other leaves and carefully selected the samples for chemical hand, many empirical studies were based on trait data for analysis. LDMC and leaf thickness were measured fol- particular planttaxa in phylogenetically narrowranges(see lowing the protocols of Cornelissen et al. (2003). Leaf supplemental tables in Moles etal. 2011; Anstett et al. 2016; mechanical strength was measured using a ‘‘penetrometer’’ seealsoMoleset al. 2013),whichmaymakethe detectionof (Feeny 1970). Although Aranwela et al. (1999) showed the latitudinal gradients in defense strategies difficult. bias of using different area of fracture surface of punching As the defense strategies of each plant species, par- rod (Onoda et al. 2011), in the present study, all the ticular set of multiple defense traits were observed. mechanical strength of leaves was measured by the stan- Agrawal and Fishbein (2006) proposed the defense syn- dardized penetrometer made by M. Murakami. The drome concept, in which several sets or combinations of diameter of steel punching rod was 3 mm, thus the area of defense traits are selected convergently as a syndrome. fracture surface was 7.07 mm and punch perimeter was For example, they found three defense strategies in As- 9.42 mm. A proanthocyanidin assay was performed to clepias plants: high physical and chemical defense with determine tannin concentrations, using a commercially high nutrition, tolerance/escape, and low nutritional available quebracho powder as the standard (Julkunen- quality. Therefore, multiple functional traits should be Tiitto 1985). The Folin–Ciocalteu method was used to examined simultaneously to explore plant defense determine the total phenol content (Waterman and Mole strategies relevant to herbivores (Levin and York 1978). 1994) with a tannic acid (Wako Co. Ltd., Tokyo, Japan) Thus, a comprehensive dataset including the entire spe- serving as the standard. The distribution data for woody cies assemblage in the focal region for multiple sets of plant species were collected from botanical literature on functional leaf traits should help us to rigorously exam- the flora of Japan. Data collection methods are described ine the LLHD hypothesis (see also Anstett et al. 2016). in detail in Kubota et al. (2015). To test the LLHD hypothesis, we compiled a dataset of plant defense traits by thoroughly sampling BL tree species across the East Asian continental archipelago from the Statistical analysis Hokkaido to Iriomote Islands (Maeshiro et al. 2013;Ku- sumoto et al. 2014; Shiono et al. 2015). In the present study, The relationships between leaf defense traits and the we first examined trait co–occurrence with respect to the distributional range of each plant species were examined chemical and mechanical defense strategies of each plant for BL tree species as a whole, and separately for DB species using ordination. We then explored the latitudinal and EGB tree species. The average values of five repli- gradients of multiples of leaf defense trait of DB and EGB cates for each tree species were used for the following tree species by path analysis. Our goal is to clarify which leaf analyses. Although intraspecific variations in leaf de- traits show the latitudinal gradients, and how are the fense traits, and even intraspecific gradients in these directions of the gradient both for DB and EGB tree species. traits along latitude, were reported (Moles et al. 2013), Although the dominant theory is the LLHD (Dobzhansky the shortage of within species replicates prevent us to 1950;Coley andAide 1991), we expect that much complex examine these trends. To assess multivariate relation- trendswillbeobserveddepends ontheplantfunctionaltypes ships among leaf defense traits, we performed principal as well as the leaf defense traits examined. component analysis (PCA) which deals with collinearity among multiple leaf traits (Pearse and Hipp 2012). Then, we developed full SEM model a priori based on the Materials and methods latitudinal effects on all the leaf defense traits and pos- sible correlations among the traits (Fig. 1). The fit of Plant functional traits and latitudinal species distribu- SEM was assessed by a X goodness-of-fit test of the tion model, the root mean square error of approximation (RMSEA) and the comparative fit index (CFI). A sat- We examined 272 EGB and 469 DB tree species, a total of isfactory model fit was indicated by: (1) a non-significant 741 BL tree species. We focused on leaf traits that might X goodness-of-fit test (a = 0.05), (2) CFI > 0.9, and Fig. 1 The distribution of leaf defense traits across latitude for deciduous and evergreen broad–leaved tree species. The signs (+, ) after the trait codes show the direction of latitudinal trends in the path analysis (Fig. 2), respectively. LDMC shows leaf dry mass content, and LMA shows leaf mass per area (3) lower 90% confidence intervals (CIs) of the first axis and 27% was explained by the second axis. RMSEA < 0.05 (Zhang et al. 2013, Blackburn et al. In a separate PCA of DB species, 31% of the total 2016). Based on species distributional data, we analyzed variance was explained by the first axis, which distin- the relationships between latitude (1 intervals) and the guished species with low LMA values from those with trait values of species distributed at the focal latitudes. high LDMC values. The second axis, which distin- The integer values of latitude at the lower limits was guished species with high mechanical defense trait values given for the all analysis. All variables used in path from those with high tannin and phenol content values, analyses were standardized (Legendre and Legendre explained 27% of the variation. The PCA of EGB spe- 1998) by subtracting the mean and dividing by the cies showed that 29% of the total variance was explained standard deviation. by the first axis, which separated species with low LMA All analyses were conducted in the R 3.3.2 statistical values from those with high leaf mechanical strength platform (R Development Core Team 2016). The SEMs (Fig. S1, Table 1). The second axis, which ordinated were calculated with the R package ‘‘lavaan 0.5–16’’ species with high chemical defense trait values and those (Rosseel, 2012), and the packages ‘‘stats’’ and ‘‘MASS’’ with low mechanical defense trait values, explained 27% (R Development Core Team 2016) were used for PCA of the variation. The vectors for chemical and mechan- and other analyses. ical defense traits were at right angles to each other for DB and EGB tree species, indicating the independence of those variables. Results Relationships among functional leaf traits Path analysis The effects of latitude on leaf traits contrasted markedly Among the BL tree species overall, the PCA results showed that 31% of the total variance was explained by between DB and EGB species (Figs. 2, 3). Positive lati- Table 1 The results of principal component analysis on broad-leaved (BL), evergreen (EGB) and deciduous (DB) tree species BL EGB DB PC1 (40) PC2 (70) PC3 (84) PC1 (38) PC2 (67) PC3 (84) PC1 (40) PC2 (64) PC3 (79) Tannin 0.09  0.58  0.42  0.15 0.57  0.34 0.34  0.46  0.45 Phenol 0.15  0.59  0.30  0.24 0.54  0.37 0.45  0.37  0.32 Strength 0.51 0.19 0.08  0.48  0.30 0.17 0.33 0.35 0.29 LDMC 0.35  0.39 0.68  0.35 0.37 0.67 0.51  0.15 0.49 Thickness 0.46 0.34  0.51  0.42  0.40  0.51 0.16 0.63  0.60 LMA 0.61 0.04 0.06  0.62  0.05 0.06 0.53 0.34 0.08 The explanatory powers and the cumulative contributions (%) of each factor were shown. LDMC shows leaf dry mass content, and LMA shows leaf mass per area tudinal effects on tannin and phenol content were de- and DB tree species demonstrated contrasting latitudi- tected in DB species, whereas a negative effect on tannin nal gradients in mechanical and chemical defense traits. and no effect on phenol was detected in EGB species. We Among the mechanical defense traits, EGB species also observed contrasting latitudinal effects on leaf showed increasing trends in leaf mechanical strength and mechanical strength and thickness; these effects were thickness along the latitudinal gradient, with tougher negative for DB species and positive in leaf mechanical and thicker leaves occurring at higher latitudes. DB strength and no effect in leaf thickness for EGB species. species showed the opposite trend, with softer and Effects on LDMC were positive in DB and EGB species. thinner leaves occurring at higher latitudes. Although Upon removal of the effects of latitude on individual Onoda et al. (2011) also observed the positive trends in leaf traits, the interactive correlations among leaf traits leaf mechanical strength along latitude for the woody were fairly similar in DB and EGB species (Fig. 2). species, the present analysis on EGB and DB tree species These trends were consistent even when the phylogenetic showed contrasting trends between them. Among the bias was removed using phylogenetic independent con- chemical defense traits, EGB species exhibited a trasts (PICs; Table S1; Felsenstein 1985). decreasing trend along the latitudinal gradient in tannin content, whereas DB species showed increasing trends with latitude in tannin and phenol content. These results Discussion indicate greater chemical defenses at lower latitudes in EGB species and greater physical defenses at lower lat- itudes in DB species. Thus, the LLHD hypothesis should We found significant latitudinal gradients in leaf defense traits in both EGB and DB tree species. However, EGB accommodate a paradoxical aspect in the latitudinal Fig. 2 Results of a structural equation model (SEM) depicting hypothesized causal relationships among leaf defense traits and the effects of latitude on them. The positive effects or interactions are indicated by solid lines, while the negative effects or interactions are indicated by broken lines. The dashed lines show the non–significant paths. The deciduous (DB) and evergreen (EGB) tree species were separately examined. LDMC shows leaf dry mass content, and LMA shows leaf mass per area. Standardized coefficients are provided for each path with significant (P < 0.05) effect. For DB; df =1, P value (X ) = 0.150 (indicating close model-data fit). For EGB; df =2, P value (X ) = 0.249 (again indicating close model-data fit) observed them in only three of 45 pairwise comparisons. Moles et al. (2013) argued that this low incidence of significant correlations in pairwise comparisons might partly be explained by the bias in the measurement of defense traits, but not the allocation of resources that might drive trade–offs, in the majority of included studies. However, the present results show much clearer trends in correlations among leaf defense traits, likely due to the separate analyses of DB and EGB tree species and the comprehensive dataset of leaf defense traits obtained by thorough sampling (see ‘‘Discussion’’ in Moles et al. 2013). One possible explanation for the contrasting trends in physical and chemical defense traits shown in both DB and EGB tree species is ‘‘trade-off’’ between these traits. Classical examinations on defense strategies considered defenses as singleton strategies, and assumed the trade– offs among different antiherbivore strategies (Steward and Keeler 1988; Herms and Mattson 1992). However, in the present study, we can observe the independent trends between physical and chemical leaf defense traits in PCA (Fig. S1, Table 1). These suggested that the contrasting trends of these leaf traits along the latitude were not trade-off but independent responses between physical and chemical leaf defense traits. These para- doxical trends in defense strategies observed in DB and EGB tree species could be explained by trends in leaf longevity along temperature gradients. Wright et al. (2005) and Kikuzawa et al. (2013) found decreasing trends in leaf longevity among EGB tree species along a temperature gradient, and opposing trends in DB tree species (Fig. 1). They also detected a positive correlation between leaf longevity and leaf mass per area, which is generally correlated positively with leaf thickness, a surrogate for physical defense. Thus, EGB-specific higher physical defense (or DB-specific lower physical defense) at higher latitudes likely is a by-product of or reflects a correlation with the leaf longevity gradient along the temperature gradient (Fig. 1). Latitudinal gradients in leaf defense traits could be driven not only by herbivory, but also by abiotic conditions, e.g., soil fertility or UV radiations (Moles et al. 2011). Although Fig. 3 Schematic relationships of latitudinal gradients of leaf this study examined multiple defense traits simultane- longevity, chemical defense, and physical defense between decid- ously across a wide range of species, broader and more uous (DB, dashed lines) and evergreen (EGB, dotted lines) broad consistent measurements of plant functional traits may leaved trees species. The pattern shown in the panel for leaf longevity was derived from the Kikuzawa et al. (2013) be needed to obtain a better understanding of plant defense strategies. gradients in chemical and physical defense traits across Furthermore, the correlative patterns among leaf DB and EGB tree species. defense traits were consistent between DB and EGB tree One possible explanation for these trends involves species when the covariate effect of latitude was removed trade–offs between leaf defense traits along latitudinal by path analysis (Fig. 2). These results suggest the gradients, which would limit total costs of defense existence of a fixed core structure in multiple defense against herbivores and might lead to contrasting pat- traits. LMA showed consistent positive correlations with terns in latitudinal trends in chemical and mechanical other leaf defense traits, suggesting that it has a defen- defense traits (Eichenberg et al. 2015). In the present sive function or just correlate with them. 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This study was supported by the Japan Cornwell WK, Craine JM, Dobrin BH, Duarte L, Durka W, Society for the Promotion of Science (no. 22405006, no. 15H04424, Elser J, Esser G, Estiarte M, Fagan WF, Fang J, Ferna´ ndez- no.15K16153, no. 15K14607) and Program for Advancing Strate- ´ Mendez F, Fidelis A, Finegan B, Flores O, Ford H, Frank D, gic International Networks to Accelerate the Circulation of Ta- Freschet GT, Fyllas NM, Gallagher RV, Green WA, Gutierrez lented Researchers, the Japan Society for the Promotion of Science AG, Hickler T, Higgins S, Hodgson JG, Jalili A, Jansen S, Joly to YK. C, Kerkhoff AJ, Kirkup D, Kitajima K, Kleyer M, Klotz S, Knops JMH, Kramer K, Kuhn I, Kurokawa H, Laughlin D, Open Access This article is distributed under the terms of the Lee TD, Leishman M, Lens F, Lenz T, Lewis SL, Lloyd J, Creative Commons Attribution 4.0 International License (http:// Llusia´ J, Louault F, Ma S, Mahecha MD, Manning P, Massad creativecommons.org/licenses/by/4.0/), which permits use, duplica T, Medlyn B, Messier J, Moles AT, Mu¨ ller SC, Nadrowski K, tion, adaptation, distribution and reproduction in any medium or Naeem S, Niinemets U,No¨ llert S, Nuske A, Ogaya R, Oleksyn format, as long as you give appropriate credit to the original J, Onipchenko VJ, Onoda Y, Ordon˜ ez J, Overbeck G, Ozinga author(s) and the source, provide a link to the Creative Commons WA, Patin˜ o S, Paula S, Pausas JG, Pen˜ uelas J, Phillips OL, license and indicate if changes were made. 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A paradox of latitudinal leaf defense strategies in deciduous and evergreen broadleaved trees

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Ecol Res DOI 10.1007/s11284-018-1614-0 ORIGINAL ARTICLE Saihanna Saihanna Tomoe Tanaka • • Yu Okamura Buntarou Kusumoto • • Takayuki Shiono Toshihide Hirao Yasuhiro Kubota Masashi Murakami A paradox of latitudinal leaf defense strategies in deciduous and evergreen broadleaved trees Received: 21 September 2017 / Accepted: 9 April 2018 The Author(s) 2018, corrected publication July 2018 Abstract The classical ‘‘low latitude–high defense’’ species exhibited opposite latitudinal defense patterns. hypothesis is seldom supported by empirical evidence. In The ‘‘low latitude high defense’’ hypothesis included a this context, we tested latitudinal patterns in the leaf paradoxical aspect in chemical and physical defense defense traits of deciduous broadleaved (DB) and ever- traits across broadleaved tree species. To reconcile green broadleaved (EGB) tree species, which are ex- paradoxical defense strategies along the latitudinal gra- pected to affect herbivore diversity. We examined the co- dient, we conclude that interactive correlations among occurrence of leaf defense traits (tannin and phenol leaf traits are controlled by leaf longevity, which differs content, leaf mechanical strength, leaf dry matter con- between DB and EGB tree species. tent, leaf mass per area, and leaf thickness) in 741 broadleaved tree species and their correlations with Keywords Chemical defense Æ Phenol Æ Physical species geographical range in East Asian island flora. We defense Æ Plant–animal interactions Æ Tannin discovered contrasting latitudinal defense strategy gra- dients in DB and EGB tree species. DB species employed chemical defenses (increasing tannin and phenol con- Introduction tent) at higher latitudes and physical defenses (softer and thinner leaves) at lower latitudes, whereas EGB tree Biologicalinteractions amongorganisms arebelieved widely to intensify at lower latitudes (Lewinsohn and Roslin 2008), leading to the development of latitudinal diversity gradient Electronic supplementary material The online version of this article (LDG) hypotheses to explain large–scale biodiversity pat- (https://doi.org/10.1007/s11284-018-1614-0) contains supplemen terns (Dobzhansky 1950; MacArthur 1972; Pennings and tary material, which is available to authorized users. Silliman 2005). As plants and herbivores comprise at least The original version of this article was revised due to a retrospec- 40% of global terrestrial biodiversity (Price 2002), evalua- tive Open Access order. tion of the consequences of plant–herbivore interaction on the LDG should attract much interest (Marquis et al. 2012). S. Saihanna Æ Y. Okamura Æ M. Murakami (&) Faculty of Science, Chiba University, Chiba, Japan Several studies have examined the ‘‘low latitude high de- E-mail: muramasa@faculty.chiba-u.jp fense’’ (LLHD) hypothesis (Bolser and Hay 1996)which Tel.: +81-43-260-3929 posits that plant species distributed at lower latitudes will show higher degrees of defense (Dobzhansky 1950,Coley T. Tanaka Æ T. Shiono Æ Y. Kubota (&) and Aide 1991,Schmitt et al. 1995). Although these studies Faculty of Science, University of the Ryukyus, Nishihara, Okinawa, Japan havebeenconducted withtheaim ofconfirmingalatitudinal E-mail: kubota.yasuhiro@gmail.com gradient in defense strength (Moles et al. 2011), few have Tel.: +81-98-895-8561 found support for the hypothesis. Moles et al. (2011) performed a meta–analysis of de- B. Kusumoto Center for Strategic Research Project, University of the Ryukyus, fense trait data, both chemical (tannins and phenols, fla- Nishihara, Okinawa, Japan vonoids, alkaloids etc.) and physical (physical toughness, extrafloral nectaries etc.) defense traits, across a wide range T. Hirao of latitude, and found conflicting trends in response to Chichibu Forest, Graduate School of Agricultural and Life Sciences, The University of Tokyo, Chichibu, Saitama, Japan predictions based on the LLHD hypothesis, with increas- ing and decreasing gradients, as well as nonsignificant Y. Kubota trends, in plant defense traits across latitudes. One pitfall of Marine and Terrestrial Field Ecology, Tropical Biosphere Research this study is the large bias caused by variation in various Center, University of the Ryukyus, Nishihara, Okinawa, Japan plant functional types among individual studies (Sitch et al. function as defense against herbivores: tannin and phenol 2003), which reduced the statistical power to detect or contents (%), leaf mechanical strength (g cm ), leaf dry identify specific latitudinal gradients in the targeted trait matter content (LDMC, %), leaf mass per area (LMA, variables. For the broadleaved (BL) tree species, several gcm ), and leaf thickness (lm). To build a dataset of leaf functional types (or groups), e.g., trees or shrubs, N fixers defense traits, we collected five replicate trees over the or not, are recognized (Wright et al. 2004; Kattge et al. distributional range of each species across the East Asian 2011). Among them, the contrast between deciduous islands, including the Ryukyu Islands. The latitudinal broadleaved (DB) and evergreen broadleaved (EGB) tree range of samplings was from 24Nto45N. Four shoots species should be the most evident (Wright et al. 2004). For with leaves were collected from each five-tree, and average example, Wright et al. (2005) showed clear contrast be- values of each tree individual were calculated (Shiono et al. tween DB and EGB tree species in leaf longevity along 2015). In the field, we harvested shoots with healthy and latitude. Thus, the separation of these functional types, fully mature leaves. In the laboratory, we visually inspected namely DB vs. EGB, might clarify the conflicting trends in the collected shoots to exclude immature and senescent latitudinal gradient in plant defense traits. On the other leaves and carefully selected the samples for chemical hand, many empirical studies were based on trait data for analysis. LDMC and leaf thickness were measured fol- particular planttaxa in phylogenetically narrowranges(see lowing the protocols of Cornelissen et al. (2003). Leaf supplemental tables in Moles etal. 2011; Anstett et al. 2016; mechanical strength was measured using a ‘‘penetrometer’’ seealsoMoleset al. 2013),whichmaymakethe detectionof (Feeny 1970). Although Aranwela et al. (1999) showed the latitudinal gradients in defense strategies difficult. bias of using different area of fracture surface of punching As the defense strategies of each plant species, par- rod (Onoda et al. 2011), in the present study, all the ticular set of multiple defense traits were observed. mechanical strength of leaves was measured by the stan- Agrawal and Fishbein (2006) proposed the defense syn- dardized penetrometer made by M. Murakami. The drome concept, in which several sets or combinations of diameter of steel punching rod was 3 mm, thus the area of defense traits are selected convergently as a syndrome. fracture surface was 7.07 mm and punch perimeter was For example, they found three defense strategies in As- 9.42 mm. A proanthocyanidin assay was performed to clepias plants: high physical and chemical defense with determine tannin concentrations, using a commercially high nutrition, tolerance/escape, and low nutritional available quebracho powder as the standard (Julkunen- quality. Therefore, multiple functional traits should be Tiitto 1985). The Folin–Ciocalteu method was used to examined simultaneously to explore plant defense determine the total phenol content (Waterman and Mole strategies relevant to herbivores (Levin and York 1978). 1994) with a tannic acid (Wako Co. Ltd., Tokyo, Japan) Thus, a comprehensive dataset including the entire spe- serving as the standard. The distribution data for woody cies assemblage in the focal region for multiple sets of plant species were collected from botanical literature on functional leaf traits should help us to rigorously exam- the flora of Japan. Data collection methods are described ine the LLHD hypothesis (see also Anstett et al. 2016). in detail in Kubota et al. (2015). To test the LLHD hypothesis, we compiled a dataset of plant defense traits by thoroughly sampling BL tree species across the East Asian continental archipelago from the Statistical analysis Hokkaido to Iriomote Islands (Maeshiro et al. 2013;Ku- sumoto et al. 2014; Shiono et al. 2015). In the present study, The relationships between leaf defense traits and the we first examined trait co–occurrence with respect to the distributional range of each plant species were examined chemical and mechanical defense strategies of each plant for BL tree species as a whole, and separately for DB species using ordination. We then explored the latitudinal and EGB tree species. The average values of five repli- gradients of multiples of leaf defense trait of DB and EGB cates for each tree species were used for the following tree species by path analysis. Our goal is to clarify which leaf analyses. Although intraspecific variations in leaf de- traits show the latitudinal gradients, and how are the fense traits, and even intraspecific gradients in these directions of the gradient both for DB and EGB tree species. traits along latitude, were reported (Moles et al. 2013), Although the dominant theory is the LLHD (Dobzhansky the shortage of within species replicates prevent us to 1950;Coley andAide 1991), we expect that much complex examine these trends. To assess multivariate relation- trendswillbeobserveddepends ontheplantfunctionaltypes ships among leaf defense traits, we performed principal as well as the leaf defense traits examined. component analysis (PCA) which deals with collinearity among multiple leaf traits (Pearse and Hipp 2012). Then, we developed full SEM model a priori based on the Materials and methods latitudinal effects on all the leaf defense traits and pos- sible correlations among the traits (Fig. 1). The fit of Plant functional traits and latitudinal species distribu- SEM was assessed by a X goodness-of-fit test of the tion model, the root mean square error of approximation (RMSEA) and the comparative fit index (CFI). A sat- We examined 272 EGB and 469 DB tree species, a total of isfactory model fit was indicated by: (1) a non-significant 741 BL tree species. We focused on leaf traits that might X goodness-of-fit test (a = 0.05), (2) CFI > 0.9, and Fig. 1 The distribution of leaf defense traits across latitude for deciduous and evergreen broad–leaved tree species. The signs (+, ) after the trait codes show the direction of latitudinal trends in the path analysis (Fig. 2), respectively. LDMC shows leaf dry mass content, and LMA shows leaf mass per area (3) lower 90% confidence intervals (CIs) of the first axis and 27% was explained by the second axis. RMSEA < 0.05 (Zhang et al. 2013, Blackburn et al. In a separate PCA of DB species, 31% of the total 2016). Based on species distributional data, we analyzed variance was explained by the first axis, which distin- the relationships between latitude (1 intervals) and the guished species with low LMA values from those with trait values of species distributed at the focal latitudes. high LDMC values. The second axis, which distin- The integer values of latitude at the lower limits was guished species with high mechanical defense trait values given for the all analysis. All variables used in path from those with high tannin and phenol content values, analyses were standardized (Legendre and Legendre explained 27% of the variation. The PCA of EGB spe- 1998) by subtracting the mean and dividing by the cies showed that 29% of the total variance was explained standard deviation. by the first axis, which separated species with low LMA All analyses were conducted in the R 3.3.2 statistical values from those with high leaf mechanical strength platform (R Development Core Team 2016). The SEMs (Fig. S1, Table 1). The second axis, which ordinated were calculated with the R package ‘‘lavaan 0.5–16’’ species with high chemical defense trait values and those (Rosseel, 2012), and the packages ‘‘stats’’ and ‘‘MASS’’ with low mechanical defense trait values, explained 27% (R Development Core Team 2016) were used for PCA of the variation. The vectors for chemical and mechan- and other analyses. ical defense traits were at right angles to each other for DB and EGB tree species, indicating the independence of those variables. Results Relationships among functional leaf traits Path analysis The effects of latitude on leaf traits contrasted markedly Among the BL tree species overall, the PCA results showed that 31% of the total variance was explained by between DB and EGB species (Figs. 2, 3). Positive lati- Table 1 The results of principal component analysis on broad-leaved (BL), evergreen (EGB) and deciduous (DB) tree species BL EGB DB PC1 (40) PC2 (70) PC3 (84) PC1 (38) PC2 (67) PC3 (84) PC1 (40) PC2 (64) PC3 (79) Tannin 0.09  0.58  0.42  0.15 0.57  0.34 0.34  0.46  0.45 Phenol 0.15  0.59  0.30  0.24 0.54  0.37 0.45  0.37  0.32 Strength 0.51 0.19 0.08  0.48  0.30 0.17 0.33 0.35 0.29 LDMC 0.35  0.39 0.68  0.35 0.37 0.67 0.51  0.15 0.49 Thickness 0.46 0.34  0.51  0.42  0.40  0.51 0.16 0.63  0.60 LMA 0.61 0.04 0.06  0.62  0.05 0.06 0.53 0.34 0.08 The explanatory powers and the cumulative contributions (%) of each factor were shown. LDMC shows leaf dry mass content, and LMA shows leaf mass per area tudinal effects on tannin and phenol content were de- and DB tree species demonstrated contrasting latitudi- tected in DB species, whereas a negative effect on tannin nal gradients in mechanical and chemical defense traits. and no effect on phenol was detected in EGB species. We Among the mechanical defense traits, EGB species also observed contrasting latitudinal effects on leaf showed increasing trends in leaf mechanical strength and mechanical strength and thickness; these effects were thickness along the latitudinal gradient, with tougher negative for DB species and positive in leaf mechanical and thicker leaves occurring at higher latitudes. DB strength and no effect in leaf thickness for EGB species. species showed the opposite trend, with softer and Effects on LDMC were positive in DB and EGB species. thinner leaves occurring at higher latitudes. Although Upon removal of the effects of latitude on individual Onoda et al. (2011) also observed the positive trends in leaf traits, the interactive correlations among leaf traits leaf mechanical strength along latitude for the woody were fairly similar in DB and EGB species (Fig. 2). species, the present analysis on EGB and DB tree species These trends were consistent even when the phylogenetic showed contrasting trends between them. Among the bias was removed using phylogenetic independent con- chemical defense traits, EGB species exhibited a trasts (PICs; Table S1; Felsenstein 1985). decreasing trend along the latitudinal gradient in tannin content, whereas DB species showed increasing trends with latitude in tannin and phenol content. These results Discussion indicate greater chemical defenses at lower latitudes in EGB species and greater physical defenses at lower lat- itudes in DB species. Thus, the LLHD hypothesis should We found significant latitudinal gradients in leaf defense traits in both EGB and DB tree species. However, EGB accommodate a paradoxical aspect in the latitudinal Fig. 2 Results of a structural equation model (SEM) depicting hypothesized causal relationships among leaf defense traits and the effects of latitude on them. The positive effects or interactions are indicated by solid lines, while the negative effects or interactions are indicated by broken lines. The dashed lines show the non–significant paths. The deciduous (DB) and evergreen (EGB) tree species were separately examined. LDMC shows leaf dry mass content, and LMA shows leaf mass per area. Standardized coefficients are provided for each path with significant (P < 0.05) effect. For DB; df =1, P value (X ) = 0.150 (indicating close model-data fit). For EGB; df =2, P value (X ) = 0.249 (again indicating close model-data fit) observed them in only three of 45 pairwise comparisons. Moles et al. (2013) argued that this low incidence of significant correlations in pairwise comparisons might partly be explained by the bias in the measurement of defense traits, but not the allocation of resources that might drive trade–offs, in the majority of included studies. However, the present results show much clearer trends in correlations among leaf defense traits, likely due to the separate analyses of DB and EGB tree species and the comprehensive dataset of leaf defense traits obtained by thorough sampling (see ‘‘Discussion’’ in Moles et al. 2013). One possible explanation for the contrasting trends in physical and chemical defense traits shown in both DB and EGB tree species is ‘‘trade-off’’ between these traits. Classical examinations on defense strategies considered defenses as singleton strategies, and assumed the trade– offs among different antiherbivore strategies (Steward and Keeler 1988; Herms and Mattson 1992). However, in the present study, we can observe the independent trends between physical and chemical leaf defense traits in PCA (Fig. S1, Table 1). These suggested that the contrasting trends of these leaf traits along the latitude were not trade-off but independent responses between physical and chemical leaf defense traits. These para- doxical trends in defense strategies observed in DB and EGB tree species could be explained by trends in leaf longevity along temperature gradients. Wright et al. (2005) and Kikuzawa et al. (2013) found decreasing trends in leaf longevity among EGB tree species along a temperature gradient, and opposing trends in DB tree species (Fig. 1). They also detected a positive correlation between leaf longevity and leaf mass per area, which is generally correlated positively with leaf thickness, a surrogate for physical defense. Thus, EGB-specific higher physical defense (or DB-specific lower physical defense) at higher latitudes likely is a by-product of or reflects a correlation with the leaf longevity gradient along the temperature gradient (Fig. 1). Latitudinal gradients in leaf defense traits could be driven not only by herbivory, but also by abiotic conditions, e.g., soil fertility or UV radiations (Moles et al. 2011). Although Fig. 3 Schematic relationships of latitudinal gradients of leaf this study examined multiple defense traits simultane- longevity, chemical defense, and physical defense between decid- ously across a wide range of species, broader and more uous (DB, dashed lines) and evergreen (EGB, dotted lines) broad consistent measurements of plant functional traits may leaved trees species. The pattern shown in the panel for leaf longevity was derived from the Kikuzawa et al. (2013) be needed to obtain a better understanding of plant defense strategies. gradients in chemical and physical defense traits across Furthermore, the correlative patterns among leaf DB and EGB tree species. defense traits were consistent between DB and EGB tree One possible explanation for these trends involves species when the covariate effect of latitude was removed trade–offs between leaf defense traits along latitudinal by path analysis (Fig. 2). These results suggest the gradients, which would limit total costs of defense existence of a fixed core structure in multiple defense against herbivores and might lead to contrasting pat- traits. LMA showed consistent positive correlations with terns in latitudinal trends in chemical and mechanical other leaf defense traits, suggesting that it has a defen- defense traits (Eichenberg et al. 2015). In the present sive function or just correlate with them. 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Our evalu- northern willows: methods for the analysis of certain phenolics. ation of LLHD hypothesis that was characterized by a J Agr Food Chem 33:213–217 paradoxical aspect in chemical and physical defense Kattge J, Diaz S, Lavorel S, Prentice IC, Leadley P, Bo¨ nisch G, Garnier E, Westoby M, Reich PB, Wright IJ, Cornelissen JHC, traits suggests the importance of more detailed explo- Violle C, Harrison SP, van Bodegom PM, Reichstein M, En- ration of separate plant functional groups to test this quist BJ, Soudzilovskaia NA, Ackerly DD, Anand M, Atkin O, hypothesis. Bahn M, Baker TR, Baldocchi D, Bekker R, Blanco C, Blonder B, Bond WJ, Bradstock R, Bunker DE, Casanoves F, Caven- Acknowledgements We are grateful to the two anonymous review- der-Bares J, Chambers JQ, Chapin FS, Chave J, Coomes D, ers for helpful comments. This study was supported by the Japan Cornwell WK, Craine JM, Dobrin BH, Duarte L, Durka W, Society for the Promotion of Science (no. 22405006, no. 15H04424, Elser J, Esser G, Estiarte M, Fagan WF, Fang J, Ferna´ ndez- no.15K16153, no. 15K14607) and Program for Advancing Strate- ´ Mendez F, Fidelis A, Finegan B, Flores O, Ford H, Frank D, gic International Networks to Accelerate the Circulation of Ta- Freschet GT, Fyllas NM, Gallagher RV, Green WA, Gutierrez lented Researchers, the Japan Society for the Promotion of Science AG, Hickler T, Higgins S, Hodgson JG, Jalili A, Jansen S, Joly to YK. C, Kerkhoff AJ, Kirkup D, Kitajima K, Kleyer M, Klotz S, Knops JMH, Kramer K, Kuhn I, Kurokawa H, Laughlin D, Open Access This article is distributed under the terms of the Lee TD, Leishman M, Lens F, Lenz T, Lewis SL, Lloyd J, Creative Commons Attribution 4.0 International License (http:// Llusia´ J, Louault F, Ma S, Mahecha MD, Manning P, Massad creativecommons.org/licenses/by/4.0/), which permits use, duplica T, Medlyn B, Messier J, Moles AT, Mu¨ ller SC, Nadrowski K, tion, adaptation, distribution and reproduction in any medium or Naeem S, Niinemets U,No¨ llert S, Nuske A, Ogaya R, Oleksyn format, as long as you give appropriate credit to the original J, Onipchenko VJ, Onoda Y, Ordon˜ ez J, Overbeck G, Ozinga author(s) and the source, provide a link to the Creative Commons WA, Patin˜ o S, Paula S, Pausas JG, Pen˜ uelas J, Phillips OL, license and indicate if changes were made. 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