Variation of Body Size in Rice Water Weevil (Coleoptera: Curculionidae) and Its Associations with Population Biology

Variation of Body Size in Rice Water Weevil (Coleoptera: Curculionidae) and Its Associations with... Life history characteristics help us to determine the ability of invasive species to establish and thrive in an exotic environment. However, so far, there have been very few reports concerning geographic variation in the body size of invasive insects and the associations between body size variation and population biology. In this study, we surveyed the geographic variation in body size of an invasive agricultural pest, the rice water weevil Lissorhoptrus oryzophilus Kuschel (Coleoptera: Curculionidae), in China. Its body size variation was found to follow Bergmann’s rule, a size cline related to latitude/altitude in which weevils tended to be larger in higher latitude/altitude localities. Moreover, using adults of different body size within populations, we also characterized the relationship between body size and some population traits of this weevil, including reproduction, food consumption, cold tolerance, and agility. The results showed that, large and mid-size adults (within populations) tended to consume more rice leaves, and larger adults also laid more and longer eggs, when compared with smaller adults. However, smaller adults appeared to have higher agility. In conclusion, body size of rice water weevil varies significantly with geography, and body size variation (within populations) may affect life history traits. Key words: phenotypic plasticity, body size, adaptation, reproduction Life history characteristics are among the major factors affecting sizes (Blanckenhorn 2000, Gotthard et al. 2007). In contrast, under the invasiveness of alien insects (Hemptinne et al. 2012, Seiter and conditions of limited resources or environmental stresses, small Kingsolver 2013). For example, insects that have high reproductive body size can be more beneficial, allowing insects to become hardier potential and strong resistance to environmental stresses are more against starvation (Couvillon and Dornhaus 2010, Blanckenhorn likely to establish in a new geographic range (Wan and Yang 2016). 2011), be more resistant to high temperatures (Carroll and Quiring Thus, determining associations of life history traits with invasiveness 1993), have more investment to immunity (Busso et al 2017), and be is crucial for risk analysis and management of non-native species. more favored in male mating competition (Blanckenhorn et al 1995, Body size can affect insects’ performance and adaptation. For Yasuda and Dixon 2002). example, for a given insect species, large females may enjoy more Body size of insects can increase with latitude (elevation), dis- reproductive advantages than small females, such as higher fecund- playing a Bergmann’s rule (BR), or decrease with latitude, display- ity and mating capacity (Honěk 1993, Blay and Yuval 1999, ing a converse Bergmann rule (CBR), both of which are common in Durocher-Granger et  al. 2011). Larger individuals may also have nature (Blanckenhorn and Demont 2004, Pincheira-Donoso 2010, greater movement ability (Yang 2000). In particular, larger individ- Shelomi 2012). BR and CBR clines are presumably caused by tem- uals are potentially more tolerant to cold because they may have a perature and season length, respectively (Blanckenhorn and Demont larger fat reserve (Ellers et al. 1998, Colinet et al. 2007), slower heat 2004). Besides, other factors such as genetic variation, voltinism, loss owing to a smaller surface-to-volume ratio (Smith et al. 2000, humidity, food supply and natural enemies can also influence the Merrick and Smith 2004), or a higher warming-up rate (Stone 1993), body size clines across latitudes (Chown and Klok 2003, Scharf et al. which support them to have a higher survival rate during overwin- 2009, Horne et al. 2017). tering (Kovacs and Goodisman 2012, Baranovska and Knapp 2014). However, despite the knowledge described above, only a few However, despite the overwhelming evidence for benefits, being studies have focused on body size in invasive insects, which include larger is costly and insects generally do not evolve toward larger the carabid beetle Merizodus soledadinus (Guerin-Ménéville) © The Author(s) 2018. Published by Oxford University Press on behalf of Entomological Society of America. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/ licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For Downloaded from https://academic.oup.com/jinsectscience/article-abstract/18/1/4/4818352 by Ed 'DeepDyve' Gillespie user commercial re-use, please contact journals.permissions@oup.com on 16 March 2018 2 Journal of Insect Science, 2018, Vol. 18, No. 1 (Coleoptera: Carabidae) (Laparie et al. 2010, 2013), the leafminer by rice water weevil in China. The weevil has spread to more northern fly Liriomyza huidobrensis (Blanchard) (Diptera: Agromyzidae) and southern regions beyond this range, but these populations were (Tantowijoyo and Hoffmann 2011), the big-headed ant not used in our study because of the difficulty of finding them in recent Pheidole megacephala (Fabricius) (Hymenoptera: Formicidae) years due to effective control or relatively low natural density. (Wills et al. 2014), and the cabbage white butterfly Pieris rapae Within 48 h after collection, 100 adults were randomly sampled (L.) (Lepidoptera: Pieridae) (Seiter and Kingsolver 2013). from each population, and 4 morphometric traits were measured for Moreover, so far, very few reports have examined geographic vari- each adult: length of the pronotum (Prnt-L), length of the elytra (Elt- ation in the body size of invasive insects, and little is known about L), width of the elytra (Elt-W), and distance from the fore-pronotum the associations of body size with their performance and adaptation. to the end of the elytra (Bd-L) (Fig. 2). Of them, elytral length has been Knowledge of this field is important for evaluating the invasiveness of frequently used for studies of coleopteran body size (e.g., Schmitz et alien species and their adaptive ability to new environments. al. 2000, Smith et al. 2000, Hernández et al. 2011, Knapp and Uhnava The rice water weevil Lissorhoptrus oryzophilus Kuschel 2014). The other three have also been shown to be relevant with body (Coleoptera: Curculionidae) is one of the most important pests of size (Cook 1993, Smith et al. 2000, Fowler et al. 2015). As we did not rice in east Asia (Chen et al. 2005, Wan and Yang 2016). Adults feed know which trait(s) would be most reasonable for rice water wee- on rice leaves leaving typical longitudinal scars and larvae consume vil, we first measured each of them and then screened for the best roots, ultimately leading to yield loss (Stout et al. 2002). This weevil one using principal component analysis (see Statistical Analysis). The is native to North America, and since the late 1950s has expanded measurements were performed under a stereo microscope (Nikon into the northwestern United States (California) and Asian countries SMZ-645, Japan) equipped with an ocular micrometer. Each individ- like Japan, North Korea, South Korea, and China (Saito et al. 2005). ual was gripped at the body with forceps, fixed on the object stage, It reproduces parthenogenetically in all of non-native regions, and and then measured. The morphometric data were averaged within thus, all of the adults are females (Huang et  al. 2017). In China, populations, and the association of body size with geography was this weevil was first detected in 1988 (Tanghai, Hebei Province) and analyzed as described in the statistical analysis section. has since spread to 24 provinces. It is univoltine in northern China where single-cropping rice is grown; newly emerged adults first feed Comparisons of the Supercooling Points of in rice fields or adjacent habitats and then move to overwintering L. oryzophilus Adults of Different Body Sizes sites before rice is harvested. However, it is bivoltine in the southern The supercooling point (SCP), termed as the temperature at which body regions growing double-cropping rice, where the second generation water begins to crystallize when exposed to freezing temperatures, is generally has a low density due to the formation of diapause in the often used as an indicator of insect cold-hardiness (Sinclair et al. 2015). majority of first-generation adults (Zhu et  al. 2005, Huang et  al. Overwintering L.  oryzophilus adults were collected from Xiangxiang 2017). So far, little is known about body size variation in this weevil. and Tongcheng from 19 December to 23 Decemeber 2014, when the In this study, we first surveyed several morphological traits of rice adults were in diapause but had not experienced the local lowest winter water weevil adults in different geographic populations, with the aim of temperatures, which generally occur during January. For each popu- determining whether body size varies with geography. After detecting lation, adults were measured using the method described above, and significant geographic variation in body size, we assessed the possible then sorted into three groups: large, mid-size, and small adults, which biological significance of this variation. To do this, we compared adults accounted for ca. 15, 70, and 15% of total adults, respectively. These of different body sizes within populations, as within-population vari- percentages fit for the fact that large and smaller individuals were much ation in insect body size is a relatively common response to changed fewer than moderately-sized individuals. Next, 18–22 adults were environmental conditions (e.g., temperature and food quality), and this randomly sampled from each group, and the SCP of each adult was type of body size variation can also have major effects on insects’ per- measured using a 4-pathway supercooling-point determination sys- formance (Navarro-Campos et al. 2011, Garrad et al. 2016). We, thus, tem (Senyi, Jiangsu Economic Development Co., Ltd., Nanjing, China) assess characteristics of within-population adults to provide a basis for according to the manufacturer’s instructions. During the measurements, the analysis of body size variation at the geographic level. the weevil abdomen was fixed to the tip of a semiconductor thermal probe with sellotape and then wrapped in absorbent cotton. The SCP was compared among the three groups within population. Materials and Methods Adult Collection and Morphometric Measurements Comparisons of Leaf Consumption, Reproduction, Rice water weevil adults (all female) were collected from six locations and Survival of L. oryzophilus Adults of Different in China during April–June in 2014 and 2015. Locations are >750 km Body Sizes apart; Yuanping and Xundian have an elevation of >800 m, while the others have an elevation below 100 m (Table 1, Fig. 1). These locations Two groups of adult collected during second time for all weevils represent the major rice growing regions or the regions heavily invaded of overwintered adults, which were collected from Xiangxiang and Table 1. Information about the geographic locations where rice water weevils were collected and evaluated County, province Latitude, longitude; elevation Year the weevil was first found Collection date Tanghai, Hebei 39°17′N, 118°28′E; 5 m 1988 12 June 2014; 25 April 2015 Yuanping, Shanxi 38°42′N, 112°46′E; 824 m 2003 27 May 2014; 18 May 2015 Tongcheng, Anhui 31°12′N, 117°01′E; 48 m 2001 26 May 2014; 29 April 2015 Yueqing, Zhejiang 28°03′N, 120°59′E; 7 m 1993 15 May 2014 Xiangxiang, Hunan 27°48′N, 112°38′E; 68 m 2005 5 May 2014; 25 April 2015 Xundian, Yunnan 25°32′N, 103°20′E; 1871 m 2007 11 May 2014 Downloaded from https://academic.oup.com/jinsectscience/article-abstract/18/1/4/4818352 by Ed 'DeepDyve' Gillespie user on 16 March 2018 Journal of Insect Science, 2018, Vol. 18, No. 1 3 Yuanping during late April of 2016 and early May of 2016, respec- hatching success was also observed as described previously (Chen tively, were used separately in this experiment. For each popula- et al. 2012), using eggs deposited on three different dates for each tion, adults were first sorted into large, mid-size, and small groups body-size group, with nine replicates each consisting of 28–50 eggs as described above, and then 15–18 adults were randomly sampled deposited by at least 10 females. When observations ended, total from each group to observe their feeding, oviposition, and survival, leaf consumption (cumulative length of feeding scars), total number with each adult serving as a single replicate. The adults were reared of eggs deposited, ovipositional period, adult survival duration, egg individually in glass tubes (2.5 cm diameter, 24 cm length) contain- length and hatching percentage were determined and subsequently ing tap water to a depth of 5 cm and one 20-d-old rice plant (cultivar compared among body size groups. Nei 5 You 8015, Zhejiang Nongke Seed Co., Ltd., Hangzhou, China). The tubes were kept in chambers at 26 ± 1°C and 60–70% humidity Comparisons of the Agility of L. oryzophilus Adults with a photoperiod of 16:8 (L:D) h. The plants were replaced every 4 of Different Body Sizes d; the lengths of adult feeding scars on the plants were measured and Six groups of overwintered adults were collected from Xiangxiang, the eggs in the leaf sheaths were counted. Moreover, at least 10 eggs Tongcheng, and Yuanping from late March to early July of 2015 and were randomly sampled for each adult around the middle oviposi- were used separately in this experiment (Fig. 3). The adults were first tional stage, and their lengths were measured under a stereo micro- sorted into large, mid-size, and small groups and then agility assays scope (Nikon SMZ-645, Japan) with an ocular micrometer. Egg were performed for the large and small groups. We took the flip time of adults as an indicator of their agility (see Jiang et al. 2007). Adult individuals oriented ventral-side up were allowed to fall freely from a height of 5 cm to the center of a flat filter paper (9.0 cm diameter; Wohua Fliter Paper Co., Ltd., Hangzhou, China). The wee- vils flipped to right their position; the time required by the weevils to flip (hereafter ‘flip time’) was recorded with a stop watch. This procedure was repeated twice in succession for each weevil. At least 20 weevils were measured for each body-size group. If a weevil failed to right itself within 5 min, testing of the individual was terminated and its flip time was excluded from the analysis. For each successful weevil, the two measured flip times were averaged and the mean was used for data analysis. To reduce error, large and small adults were measured alternately. Flip time was compared between the large and small adults within each population. Statistical Analysis All data analyses were performed using the statistical software sys- Fig. 1. Collection locations for the rice water weevils used in this study. tem SPSS v.20 (IBM SPSS Statistics, 2011). Because morphometric variables may be correlated to each other, principal component ana- lysis (PCA) was first performed to replace the four original variables (Prnt-L, Elt-L, Elt-W, and Bd-L) with new variables, i.e., principal components. Then, the first principal components (PC1s) of each population were used as dependent variables, and one-way analysis of variance (ANOVA) was performed to test the significance of body size variation with geography, at the significance level (P) 0.05. Such an analysis was performed separately for the data of 2014 and 2015. Moreover, for each population, t-tests were performed to compare body size between the 2 yr. Fig.  3. Flip times (mean  ±  SE) of large and small rice water weevil adults collected from Xiangxiang (XX), Tongcheng (TC), and Yuanping (YP) in 2015. Fig.  2. Measurements of morphological traits of adult Lissorhoptrus The numbers of adults subjected to data analysis are given at the bottom oryzophilus. of the columns. An asterisk indicates significant difference (P < 0.05, t-test). Downloaded from https://academic.oup.com/jinsectscience/article-abstract/18/1/4/4818352 by Ed 'DeepDyve' Gillespie user on 16 March 2018 4 Journal of Insect Science, 2018, Vol. 18, No. 1 One-way ANOVA was used to analyze the relationships be- F = 0.528; df = 2, 58; P = 0.592, and Tongcheng: F = 1.073; df = 2, 55; tween body size and adult SCP, leaf consumption, egg production, P = 0.349), and differently sized adults had similar SCPs (Table 4). ovipositional period, survival duration, egg length and hatching percentage. Prior to ANOVA, data were tested for homogeneity of Comparisons of Leaf Consumption, Reproduction, variance (Levene test), and the following transformations were made and Survival of L. oryzophilus Adults of Different previously: the leaf consumption data were square-root transformed, Body Sizes egg numbers were square-root transformed (x + 1), and egg hatch- Large and mid-size adults consumed more rice leaf tissue than ing percentages were arcsine square-root transformed. Means were small adults, and the difference was statistically significant in the compared by performing Tukey’s honest significant difference (HSD) Xiangxiang population. The number of eggs deposited was signifi- post hoc tests at P = 0.05. cantly related to body size in both Xiangxiang and Tanghai popula- Data of flip time was first tested for homogeneity of variance, tions (Table 5). Large and mid-size Xiangxiang adults deposited 65.1 and then compared between large and small adults by performing and 49.3% more eggs, respectively, than small adults, while large t-tests at P = 0.05. and mid-size Tanghai adults deposited 100 and 40.0% more eggs. Egg length was significantly related to adult body size, and the eggs produced by large and mid-size adults tended to be longer than those Results produced by small adults. None of the other traits, including ovipo- Geographic Variation of L. oryzophilus Adult sitional period, adult survival duration, and egg hatching percentage, Body Size differed significantly across adult body sizes (Table 5). Values of each measured morphometric traits were given in Table 2. PCA showed that the PC1s explained 82.9% (in 2014) and 87.9% Comparisons of the Agility of L. oryzophilus Adults (in 2015) of the total variance and were correlated positively with all of Different Body Sizes four morphometric variables (Supp Table 1 [online only]). Therefore, Of the six groups of adults tested for flip time, only the group col- PC1s were retained for comparison among populations. Besides, lected from Tongcheng in late March displayed a significant differ - Bd-L (length of pronotum + elytra) exhibited the highest correlation ence between large and small adults, whose average flip times were with PC1s (Supp Table 1 [online only]), thus it was chosen as a rep- 38 and 22  s, respectively. Data from all other locations and dates, resentative indicator of body size for the analyses below. except the Xiangxiang June-24 adults, suggested that larger adults ANOVA showed that body size varied significantly with geog- require more time to flip (Fig. 3). raphy in both years (2014: F  =  10.361; df  =  5, 594; P  <  0.001, 2015: F  =  20.412; df  =  3, 396; P  <  0.001). In 2014, body size in the Yuanping (northern) population was similar to those in the Discussion Tanghai (northern) and Xundian (southern but with high eleva- The ability of invasive insects to colonize and spread in new geo- tion, Table 1) populations but significantly larger than in the other graphic ranges is related to morphological, physiological, or behav- three (southern) populations. In 2015, body size in the Yuanping ioral traits (Piiroinen et  al. 2011, Laparie et  al. 2013). We found population was significantly larger than in the other three popu- that the adult body size of rice water weevil, an invasive insect pest lations. In contrast, in both years, the Tongcheng and Xiangxiang in east Asia, varied significantly with geography. Adults of northern (southern) populations were significantly smaller in body size than (Tanghai and Yuanping) populations and a population at high eleva- the Yuanping and Tanghai (northern) populations. For each popu- tion (Xundian) tended to be larger than those from southern popu- lation, no significant difference was found in body size between lations (Tongcheng and Xiangxiang), exhibiting a body size pattern the 2 yr (Tanghai: t  =  0.801; df  =  191.700; P  =  0.424, Yuanping: of Bergmann’s rule. t  = –1.062; df  =  198; P  = 0.290, Tongcheng: t  = –0.936; df  =  198; It is not clear what ecological factors cause the geographical vari- P = 0.351, and Xiangxiang: t = 0.982; df = 198; P = 0.328; Table 3). ation in L.  oryzophilus adult body size. According to Bergmann’s rule (Blanckenhorn and Demont 2004), temperature can be specu- Comparisons of the SCPs of L. oryzophilus Adults of lated as a major cause. Other factors may also play a role, such as Different Body Sizes the quality of host plant the larvae feed on, as this will vary with rice We measured the SCPs of adults with different body sizes collected variety or/and phenology. from Xiangxiang and Tongcheng. Within each population, the SCPs Within populations, large L. oryzophilus adults did not have sig- of adults did not vary significantly with body size (Xiangxiang: nificantly lower SCPs than small adults, and there was no consistent Table 2. The morphometric traits measured in rice water weevil adults from different geographic populations Year Geographic population No. of adults Prnt-L (mm) Elt-L (mm) Elt-W (mm) Bd-L (mm) 2014 Tanghai 100 0.724 ± 0.002 2.302 ± 0.005 1.438 ± 0.004 3.031 ± 0.006 Yuanping 100 0.731 ± 0.002 2.322 ± 0.007 1.455 ± 0.005 3.055 ± 0.008 Tongcheng 100 0.715 ± 0.004 2.260 ± 0.009 1.385 ± 0.007 2.977 ± 0.011 Yueqing 100 0.715 ± 0.003 2.297 ± 0.010 1.397 ± 0.006 3.011 ± 0.013 Xiangxiang 100 0.711 ± 0.003 2.279 ± 0.010 1.395 ± 0.006 2.989 ± 0.012 Xundian 100 0.712 ± 0.002 2.333 ± 0.009 1.432 ± 0.006 3.044 ± 0.011 2015 Tanghai 100 0.745 ± 0.003 2.359 ± 0.007 1.410 ± 0.005 3.042 ± 0.009 Yuanping 100 0.759 ± 0.003 2.382 ± 0.008 1.453 ± 0.004 3.075 ± 0.008 Tongcheng 100 0.741 ± 0.003 2.317 ± 0.007 1.393 ± 0.006 2.994 ± 0.010 Xiangxiang 100 0.735 ± 0.003 2.343 ± 0.008 1.383 ± 0.006 2.990 ± 0.011 Downloaded from https://academic.oup.com/jinsectscience/article-abstract/18/1/4/4818352 by Ed 'DeepDyve' Gillespie user on 16 March 2018 Journal of Insect Science, 2018, Vol. 18, No. 1 5 Table  3. PC1 values (mean ± SE) for rice water weevils from six fecundity observed in the laboratory may be not fully realized populations under natural conditions (Gotthard et al. 2007), the real extent of body size affecting fecundity might differ to certain degree from the Populations PC1 in 2014 PC1 in 2015 one observed under laboratory controlled conditions. Therefore, the body size and fecundity associations, and the advantages of Tanghai 0.19 ± 0.07abA 0.10 ± 0.08bA Yuanping 0.43 ± 0.08aA 0.55 ± 0.09aA large size should be much more complicated than expected and Tongcheng –0.43 ± 0.11dA –0.29 ± 0.10cA need further research in the future. Yueqing –0.09 ± 0.11bcd – Body size can affect insect activities, such as foraging Xiangxiang –0.23 ± 0.09cdA –0.37 ± 0.11cA (Greenleaf et al. 2007, Guédot et al. 2009), moving (Marden and Xundian 0.13 ± 0.10abc – Kramer 1995, Yang 2000, Samejima and Tsubaki 2010, García and Sarmiento 2012, Cooper et  al. 2013), competition (Moya- Means within a column followed by the same lowercase letter are not sig- Laraño et  al. 2007), and avoiding attack by natural enemies nificantly different (P  > 0.05, Tukey’s test). Means within a row followed by (Remmel and Tammaru 2009). By increasing body, thorax and/ the same capital letter are not significantly different (P > 0.05, t test) or wing size, insects may increase mobility, which, in turn, affects their adaptability to diverse environments (Saastamoinen 2007, Table 4. SCPs (mean ± SE, °C) of L. oryzophilus adults of different Laparie 2013). We found that larger L.  oryzophilus adults had body sizes longer and wider elytra (Table 2). However, it is unclear whether Populations Adult group Bd-L (mm) SCP (°C) such adults would have higher flight capacity and have advan- tages in flight-supported activities over adults with small elytra. Xiangxiang Large 3.092 ± 0.007(22)a −14.2 ± 1.1(22)a In our flip-time observations, small adults were found to be more Mid-size 2.908 ± 0.005(20)b −14.4 ± 1.1(20)a agile (righting their body position more rapidly) than large adults. Small 2.614 ± 0.023(19)c −15.7 ± 1.1(19)a This agility might have advantages, such as allowing small adults Tongcheng Large 3.168 ± 0.006(18)a −18.1 ± 0.6(18)a to more easily escape from attacks of natural enemies. This pro- Mid-size 3.010 ± 0.004(20)b −16.0 ± 1.1(20)a vides valuable empirical evidence for the benefits of small size Small 2.807 ± 0.024(20)c −17.0 ± 1.1(20)a in insects, which has intrigued the interest of some researchers (Blanckenhorn 2000, Chown and Gaston 2010). Means within a column followed by the same letter are not significantly dif- ferent (P > 0.05, Tukey’s HSD test). Numbers in parentheses are the numbers In summary, L.  oryzophilus has successfully invaded a large of adults observed. geographic area in China and exhibits geographic variation in adult body size, which increases with altitude. Moreover, by stud- association between SCP and body size (Table 4). To confirm this re- ying within-population adults of different body size, we showed sult, we further measured the overall SCP in Xiangxiang, Tongcheng that body size is relevant with this weevil’s population biology: and Tanghai adults (not sorted in size groups), which indicated that larger weevils consume more leaf area, lay more and larger eggs, the Tanghai adults (with large body size) had a significantly higher but are less agile than small weevils. Yet, due to the limit of our SCP (–14.3  ±  0.6°C) than Tongcheng adults (–16.7  ±  0.6°C, the observations, we do not know whether such associations also smallest weevils among the populations analyzed; unpublished data). existed among various geographic populations. To be noted, geo- Moreover, in one of our previous studies, the Yueqing (southern) graphic variation in body size and associated life history traits adults were found to have a SCP below –20°C during early winter reflect different life history strategies appropriate to and shaped (Zhang et al. 2004). Combining these findings, we suggest that body by the environmental conditions present in different geographic size might be not associated with cold tolerance in this weevil. The locations. Certainly, results obtained from within-population lack of such an association has also been reported in other insect studies cannot be used to infer the biological significance of body species (Quarles et  al. 2005, Clarke et  al. 2013). The result needs size variation among geographic populations. Despite this, our to be confirmed using other measurements of cold tolerance, such study is valuable describing for the first time associations between as lower lethal temperature, which can provide information about body size and biological traits in rice water weevil. In the future, the survival likelihood of tested insects under given temperatures transplantation experiments are to be performed, that is, putting (Sinclair et al. 2015). weevils originating from one population to the environmental One of the most important findings of our study was that conditions experienced by other populations and then measuring larger L.  oryzophilus adults within populations tended to lay the biology traits. Moreover, such experiments will also allow us more eggs than smaller adults (Table  5), as found in a number of to learn whether the variation of body size in this weevil is the other insects (Honěk 1993, Visser 1994, Kim 1997, Sagarra et al. result of phenotypic plasticity or is the result of genetic variation 2001, Marshall et al. 2013). Moreover, large and mid-size weevils among populations (local adaptation). In addition, as voltinism tended to produce larger eggs than small weevils (Table  5). Thus, may affect patterns of insect body size (Blanckenhorn and Demont we suggest that body size is positively associated with reproductive 2004, Horne et al. 2017), we need to learn whether this weevil’s performance of this weevil. However, it is not clear whether such body size, as well as possible consequences of body size and size an association also exists among geographic populations. That is, variation, will change in southern China. There it originally had do weevils at higher latitudes (elevations), where they are larger two annual generations, but in future, this will shift because rice is than in southern regions, have a higher fecundity? To resolve this increasingly grown in a single season which can only support one question, two factors have to be taken into account. One factor is weevil generation per year (Zhu et al. 2005, Huang et al. 2017). that cooler temperatures at higher latitudes could be less suitable There aspects will be studied in the future, once a viable of method for reproduction. This might potentially reduce the overall repro- artificially rearing these weevils has been developed. Although ductive capacity of large adults. This may mask effects of body rearing has been attempted, the specificity of larvae and pupae’s size and accordingly larger weevils (at higher latitudes) may not oxygen-intake system has so far proved difficult to simulate con- have as high fecundity as expected. Another factor is, because the sistently in the laboratory (Zhang et al. 2006). Downloaded from https://academic.oup.com/jinsectscience/article-abstract/18/1/4/4818352 by Ed 'DeepDyve' Gillespie user on 16 March 2018 6 Journal of Insect Science, 2018, Vol. 18, No. 1 Supplementary Data Supplementary data are available at Journal of Insect Science online. Acknowledgments This research was financially supported by the National Key Research and Development Program of China (2016YFC1200600). References Cited Baranovska, E. and M. Knapp. 2014. Small-scale spatiotemporal variability in body size of two common carabid beetles. Cent. Eur. J. Biol. 9: 476–494. Blanckenhorn, W. U. 2000. The evolution of body size: what keeps organisms small? Q. Rev. Biol. 75: 385–407. Blanckenhorn, W. U. and M.  Demont. 2004. Bergmann and converse Bergmann latitudinal clines in arthropods: two ends of a continuum? Annual Meeting of the Society for Integrative and Comparative Biology. New Orleans, LA. Integr. Comp. Biol. 44: 413–424. Blanckenhorn, W. U., R. F. Preziosi, and D. 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Feeding, reproduction and survival traits (mean ± SE) of L. oryzophilus adults with different body sizes Populations Adult group/ Bd-L (mm) Adult leaf Avg. no. of Ovipositional Adult survival Egg length (mm) Egg hatch percentage ANOVA value consumption (cm) eggs deposited period (days) duration (days) Xiangxiang Large 3.152 ± 0.007(18)a 139.8 ± 10.4(18)ab 46.9 ± 3.6(16)a 20.1 ± 1.7(17)a 26.4 ± 2.1(18)a 0.95 ± 0.02(17)ab 83.9 ± 1.2(329)a Mid-size 2.900 ± 0.007(18)b 154.7 ± 8.8(17)a 42.4 ± 4.4(17)a 19.9 ± 2.0(17)a 31.2 ± 1.9(17)a 0.99 ± 0.02(17)a 81.0 ± 1.9(328)a Small 2.663 ± 0.020(18)c 118.2 ± 6.2(17)b 28.4 ± 3.6(15)b 15.1 ± 1.5(15)a 26.7 ± 1.6(17)a 0.93 ± 0.02(14)b 87.0 ± 2.9(208)a F 379.710 4.399 5.804 2.487 1.926 4.290 2.123 df 2, 51 2, 49 2, 45 2, 46 2, 49 2, 45 2, 22 P 0.000* 0.017* 0.006* 0.094 0.157 0.020* 0.144 Tanghai Large 3.178 ± 0.005(15)a 178.6 ± 8.0(11)a 85.7 ± 13.8(11)a 21.6 ± 1.1(11)a 35.6 ± 1.3(11)a 0.93 ± 0.01(15)a 91.0 ± 2.0(396)a Mid-size 3.024 ± 0.004(15)b 171.3 ± 4.5(14)a 60.0 ± 8.4(14)ab 19.0 ± 1.1(14)a 35.4 ± 1.2(14)a 0.93 ± 0.01(14)a 90.5 ± 0.6(341)a Small 2.873 ± 0.010(15)c 157.2 ± 7.6(15)a 42.9 ± 5.1(11)b 20.3 ± 1.5(13)a 35.0 ± 1.3(14)a 0.89 ± 0.01(14)a 86.7 ± 2.0(354)a F 460.688 2.587 4.622 1.023 0.047 3.511 2.012 df 2, 42 2, 37 2, 33 2, 35 2, 36 2, 40 2, 24 P 0.000* 0.089 0.017* 0.370 0.954 0.039* 0.156 Numbers in parentheses are the numbers of adults or eggs observed. 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Guo (eds.), and the search for universal macroecological patterns: taking Bergmann’s Biology and management of invasive alien species in agriculture and for- rule back to its endothermic origin. Theory Biosci. 129: 247–253. estry. Science Press, Beijing, China. Downloaded from https://academic.oup.com/jinsectscience/article-abstract/18/1/4/4818352 by Ed 'DeepDyve' Gillespie user on 16 March 2018 http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Journal of Insect Science Oxford University Press

Variation of Body Size in Rice Water Weevil (Coleoptera: Curculionidae) and Its Associations with Population Biology

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Abstract

Life history characteristics help us to determine the ability of invasive species to establish and thrive in an exotic environment. However, so far, there have been very few reports concerning geographic variation in the body size of invasive insects and the associations between body size variation and population biology. In this study, we surveyed the geographic variation in body size of an invasive agricultural pest, the rice water weevil Lissorhoptrus oryzophilus Kuschel (Coleoptera: Curculionidae), in China. Its body size variation was found to follow Bergmann’s rule, a size cline related to latitude/altitude in which weevils tended to be larger in higher latitude/altitude localities. Moreover, using adults of different body size within populations, we also characterized the relationship between body size and some population traits of this weevil, including reproduction, food consumption, cold tolerance, and agility. The results showed that, large and mid-size adults (within populations) tended to consume more rice leaves, and larger adults also laid more and longer eggs, when compared with smaller adults. However, smaller adults appeared to have higher agility. In conclusion, body size of rice water weevil varies significantly with geography, and body size variation (within populations) may affect life history traits. Key words: phenotypic plasticity, body size, adaptation, reproduction Life history characteristics are among the major factors affecting sizes (Blanckenhorn 2000, Gotthard et al. 2007). In contrast, under the invasiveness of alien insects (Hemptinne et al. 2012, Seiter and conditions of limited resources or environmental stresses, small Kingsolver 2013). For example, insects that have high reproductive body size can be more beneficial, allowing insects to become hardier potential and strong resistance to environmental stresses are more against starvation (Couvillon and Dornhaus 2010, Blanckenhorn likely to establish in a new geographic range (Wan and Yang 2016). 2011), be more resistant to high temperatures (Carroll and Quiring Thus, determining associations of life history traits with invasiveness 1993), have more investment to immunity (Busso et al 2017), and be is crucial for risk analysis and management of non-native species. more favored in male mating competition (Blanckenhorn et al 1995, Body size can affect insects’ performance and adaptation. For Yasuda and Dixon 2002). example, for a given insect species, large females may enjoy more Body size of insects can increase with latitude (elevation), dis- reproductive advantages than small females, such as higher fecund- playing a Bergmann’s rule (BR), or decrease with latitude, display- ity and mating capacity (Honěk 1993, Blay and Yuval 1999, ing a converse Bergmann rule (CBR), both of which are common in Durocher-Granger et  al. 2011). Larger individuals may also have nature (Blanckenhorn and Demont 2004, Pincheira-Donoso 2010, greater movement ability (Yang 2000). In particular, larger individ- Shelomi 2012). BR and CBR clines are presumably caused by tem- uals are potentially more tolerant to cold because they may have a perature and season length, respectively (Blanckenhorn and Demont larger fat reserve (Ellers et al. 1998, Colinet et al. 2007), slower heat 2004). Besides, other factors such as genetic variation, voltinism, loss owing to a smaller surface-to-volume ratio (Smith et al. 2000, humidity, food supply and natural enemies can also influence the Merrick and Smith 2004), or a higher warming-up rate (Stone 1993), body size clines across latitudes (Chown and Klok 2003, Scharf et al. which support them to have a higher survival rate during overwin- 2009, Horne et al. 2017). tering (Kovacs and Goodisman 2012, Baranovska and Knapp 2014). However, despite the knowledge described above, only a few However, despite the overwhelming evidence for benefits, being studies have focused on body size in invasive insects, which include larger is costly and insects generally do not evolve toward larger the carabid beetle Merizodus soledadinus (Guerin-Ménéville) © The Author(s) 2018. Published by Oxford University Press on behalf of Entomological Society of America. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/ licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For Downloaded from https://academic.oup.com/jinsectscience/article-abstract/18/1/4/4818352 by Ed 'DeepDyve' Gillespie user commercial re-use, please contact journals.permissions@oup.com on 16 March 2018 2 Journal of Insect Science, 2018, Vol. 18, No. 1 (Coleoptera: Carabidae) (Laparie et al. 2010, 2013), the leafminer by rice water weevil in China. The weevil has spread to more northern fly Liriomyza huidobrensis (Blanchard) (Diptera: Agromyzidae) and southern regions beyond this range, but these populations were (Tantowijoyo and Hoffmann 2011), the big-headed ant not used in our study because of the difficulty of finding them in recent Pheidole megacephala (Fabricius) (Hymenoptera: Formicidae) years due to effective control or relatively low natural density. (Wills et al. 2014), and the cabbage white butterfly Pieris rapae Within 48 h after collection, 100 adults were randomly sampled (L.) (Lepidoptera: Pieridae) (Seiter and Kingsolver 2013). from each population, and 4 morphometric traits were measured for Moreover, so far, very few reports have examined geographic vari- each adult: length of the pronotum (Prnt-L), length of the elytra (Elt- ation in the body size of invasive insects, and little is known about L), width of the elytra (Elt-W), and distance from the fore-pronotum the associations of body size with their performance and adaptation. to the end of the elytra (Bd-L) (Fig. 2). Of them, elytral length has been Knowledge of this field is important for evaluating the invasiveness of frequently used for studies of coleopteran body size (e.g., Schmitz et alien species and their adaptive ability to new environments. al. 2000, Smith et al. 2000, Hernández et al. 2011, Knapp and Uhnava The rice water weevil Lissorhoptrus oryzophilus Kuschel 2014). The other three have also been shown to be relevant with body (Coleoptera: Curculionidae) is one of the most important pests of size (Cook 1993, Smith et al. 2000, Fowler et al. 2015). As we did not rice in east Asia (Chen et al. 2005, Wan and Yang 2016). Adults feed know which trait(s) would be most reasonable for rice water wee- on rice leaves leaving typical longitudinal scars and larvae consume vil, we first measured each of them and then screened for the best roots, ultimately leading to yield loss (Stout et al. 2002). This weevil one using principal component analysis (see Statistical Analysis). The is native to North America, and since the late 1950s has expanded measurements were performed under a stereo microscope (Nikon into the northwestern United States (California) and Asian countries SMZ-645, Japan) equipped with an ocular micrometer. Each individ- like Japan, North Korea, South Korea, and China (Saito et al. 2005). ual was gripped at the body with forceps, fixed on the object stage, It reproduces parthenogenetically in all of non-native regions, and and then measured. The morphometric data were averaged within thus, all of the adults are females (Huang et  al. 2017). In China, populations, and the association of body size with geography was this weevil was first detected in 1988 (Tanghai, Hebei Province) and analyzed as described in the statistical analysis section. has since spread to 24 provinces. It is univoltine in northern China where single-cropping rice is grown; newly emerged adults first feed Comparisons of the Supercooling Points of in rice fields or adjacent habitats and then move to overwintering L. oryzophilus Adults of Different Body Sizes sites before rice is harvested. However, it is bivoltine in the southern The supercooling point (SCP), termed as the temperature at which body regions growing double-cropping rice, where the second generation water begins to crystallize when exposed to freezing temperatures, is generally has a low density due to the formation of diapause in the often used as an indicator of insect cold-hardiness (Sinclair et al. 2015). majority of first-generation adults (Zhu et  al. 2005, Huang et  al. Overwintering L.  oryzophilus adults were collected from Xiangxiang 2017). So far, little is known about body size variation in this weevil. and Tongcheng from 19 December to 23 Decemeber 2014, when the In this study, we first surveyed several morphological traits of rice adults were in diapause but had not experienced the local lowest winter water weevil adults in different geographic populations, with the aim of temperatures, which generally occur during January. For each popu- determining whether body size varies with geography. After detecting lation, adults were measured using the method described above, and significant geographic variation in body size, we assessed the possible then sorted into three groups: large, mid-size, and small adults, which biological significance of this variation. To do this, we compared adults accounted for ca. 15, 70, and 15% of total adults, respectively. These of different body sizes within populations, as within-population vari- percentages fit for the fact that large and smaller individuals were much ation in insect body size is a relatively common response to changed fewer than moderately-sized individuals. Next, 18–22 adults were environmental conditions (e.g., temperature and food quality), and this randomly sampled from each group, and the SCP of each adult was type of body size variation can also have major effects on insects’ per- measured using a 4-pathway supercooling-point determination sys- formance (Navarro-Campos et al. 2011, Garrad et al. 2016). We, thus, tem (Senyi, Jiangsu Economic Development Co., Ltd., Nanjing, China) assess characteristics of within-population adults to provide a basis for according to the manufacturer’s instructions. During the measurements, the analysis of body size variation at the geographic level. the weevil abdomen was fixed to the tip of a semiconductor thermal probe with sellotape and then wrapped in absorbent cotton. The SCP was compared among the three groups within population. Materials and Methods Adult Collection and Morphometric Measurements Comparisons of Leaf Consumption, Reproduction, Rice water weevil adults (all female) were collected from six locations and Survival of L. oryzophilus Adults of Different in China during April–June in 2014 and 2015. Locations are >750 km Body Sizes apart; Yuanping and Xundian have an elevation of >800 m, while the others have an elevation below 100 m (Table 1, Fig. 1). These locations Two groups of adult collected during second time for all weevils represent the major rice growing regions or the regions heavily invaded of overwintered adults, which were collected from Xiangxiang and Table 1. Information about the geographic locations where rice water weevils were collected and evaluated County, province Latitude, longitude; elevation Year the weevil was first found Collection date Tanghai, Hebei 39°17′N, 118°28′E; 5 m 1988 12 June 2014; 25 April 2015 Yuanping, Shanxi 38°42′N, 112°46′E; 824 m 2003 27 May 2014; 18 May 2015 Tongcheng, Anhui 31°12′N, 117°01′E; 48 m 2001 26 May 2014; 29 April 2015 Yueqing, Zhejiang 28°03′N, 120°59′E; 7 m 1993 15 May 2014 Xiangxiang, Hunan 27°48′N, 112°38′E; 68 m 2005 5 May 2014; 25 April 2015 Xundian, Yunnan 25°32′N, 103°20′E; 1871 m 2007 11 May 2014 Downloaded from https://academic.oup.com/jinsectscience/article-abstract/18/1/4/4818352 by Ed 'DeepDyve' Gillespie user on 16 March 2018 Journal of Insect Science, 2018, Vol. 18, No. 1 3 Yuanping during late April of 2016 and early May of 2016, respec- hatching success was also observed as described previously (Chen tively, were used separately in this experiment. For each popula- et al. 2012), using eggs deposited on three different dates for each tion, adults were first sorted into large, mid-size, and small groups body-size group, with nine replicates each consisting of 28–50 eggs as described above, and then 15–18 adults were randomly sampled deposited by at least 10 females. When observations ended, total from each group to observe their feeding, oviposition, and survival, leaf consumption (cumulative length of feeding scars), total number with each adult serving as a single replicate. The adults were reared of eggs deposited, ovipositional period, adult survival duration, egg individually in glass tubes (2.5 cm diameter, 24 cm length) contain- length and hatching percentage were determined and subsequently ing tap water to a depth of 5 cm and one 20-d-old rice plant (cultivar compared among body size groups. Nei 5 You 8015, Zhejiang Nongke Seed Co., Ltd., Hangzhou, China). The tubes were kept in chambers at 26 ± 1°C and 60–70% humidity Comparisons of the Agility of L. oryzophilus Adults with a photoperiod of 16:8 (L:D) h. The plants were replaced every 4 of Different Body Sizes d; the lengths of adult feeding scars on the plants were measured and Six groups of overwintered adults were collected from Xiangxiang, the eggs in the leaf sheaths were counted. Moreover, at least 10 eggs Tongcheng, and Yuanping from late March to early July of 2015 and were randomly sampled for each adult around the middle oviposi- were used separately in this experiment (Fig. 3). The adults were first tional stage, and their lengths were measured under a stereo micro- sorted into large, mid-size, and small groups and then agility assays scope (Nikon SMZ-645, Japan) with an ocular micrometer. Egg were performed for the large and small groups. We took the flip time of adults as an indicator of their agility (see Jiang et al. 2007). Adult individuals oriented ventral-side up were allowed to fall freely from a height of 5 cm to the center of a flat filter paper (9.0 cm diameter; Wohua Fliter Paper Co., Ltd., Hangzhou, China). The wee- vils flipped to right their position; the time required by the weevils to flip (hereafter ‘flip time’) was recorded with a stop watch. This procedure was repeated twice in succession for each weevil. At least 20 weevils were measured for each body-size group. If a weevil failed to right itself within 5 min, testing of the individual was terminated and its flip time was excluded from the analysis. For each successful weevil, the two measured flip times were averaged and the mean was used for data analysis. To reduce error, large and small adults were measured alternately. Flip time was compared between the large and small adults within each population. Statistical Analysis All data analyses were performed using the statistical software sys- Fig. 1. Collection locations for the rice water weevils used in this study. tem SPSS v.20 (IBM SPSS Statistics, 2011). Because morphometric variables may be correlated to each other, principal component ana- lysis (PCA) was first performed to replace the four original variables (Prnt-L, Elt-L, Elt-W, and Bd-L) with new variables, i.e., principal components. Then, the first principal components (PC1s) of each population were used as dependent variables, and one-way analysis of variance (ANOVA) was performed to test the significance of body size variation with geography, at the significance level (P) 0.05. Such an analysis was performed separately for the data of 2014 and 2015. Moreover, for each population, t-tests were performed to compare body size between the 2 yr. Fig.  3. Flip times (mean  ±  SE) of large and small rice water weevil adults collected from Xiangxiang (XX), Tongcheng (TC), and Yuanping (YP) in 2015. Fig.  2. Measurements of morphological traits of adult Lissorhoptrus The numbers of adults subjected to data analysis are given at the bottom oryzophilus. of the columns. An asterisk indicates significant difference (P < 0.05, t-test). Downloaded from https://academic.oup.com/jinsectscience/article-abstract/18/1/4/4818352 by Ed 'DeepDyve' Gillespie user on 16 March 2018 4 Journal of Insect Science, 2018, Vol. 18, No. 1 One-way ANOVA was used to analyze the relationships be- F = 0.528; df = 2, 58; P = 0.592, and Tongcheng: F = 1.073; df = 2, 55; tween body size and adult SCP, leaf consumption, egg production, P = 0.349), and differently sized adults had similar SCPs (Table 4). ovipositional period, survival duration, egg length and hatching percentage. Prior to ANOVA, data were tested for homogeneity of Comparisons of Leaf Consumption, Reproduction, variance (Levene test), and the following transformations were made and Survival of L. oryzophilus Adults of Different previously: the leaf consumption data were square-root transformed, Body Sizes egg numbers were square-root transformed (x + 1), and egg hatch- Large and mid-size adults consumed more rice leaf tissue than ing percentages were arcsine square-root transformed. Means were small adults, and the difference was statistically significant in the compared by performing Tukey’s honest significant difference (HSD) Xiangxiang population. The number of eggs deposited was signifi- post hoc tests at P = 0.05. cantly related to body size in both Xiangxiang and Tanghai popula- Data of flip time was first tested for homogeneity of variance, tions (Table 5). Large and mid-size Xiangxiang adults deposited 65.1 and then compared between large and small adults by performing and 49.3% more eggs, respectively, than small adults, while large t-tests at P = 0.05. and mid-size Tanghai adults deposited 100 and 40.0% more eggs. Egg length was significantly related to adult body size, and the eggs produced by large and mid-size adults tended to be longer than those Results produced by small adults. None of the other traits, including ovipo- Geographic Variation of L. oryzophilus Adult sitional period, adult survival duration, and egg hatching percentage, Body Size differed significantly across adult body sizes (Table 5). Values of each measured morphometric traits were given in Table 2. PCA showed that the PC1s explained 82.9% (in 2014) and 87.9% Comparisons of the Agility of L. oryzophilus Adults (in 2015) of the total variance and were correlated positively with all of Different Body Sizes four morphometric variables (Supp Table 1 [online only]). Therefore, Of the six groups of adults tested for flip time, only the group col- PC1s were retained for comparison among populations. Besides, lected from Tongcheng in late March displayed a significant differ - Bd-L (length of pronotum + elytra) exhibited the highest correlation ence between large and small adults, whose average flip times were with PC1s (Supp Table 1 [online only]), thus it was chosen as a rep- 38 and 22  s, respectively. Data from all other locations and dates, resentative indicator of body size for the analyses below. except the Xiangxiang June-24 adults, suggested that larger adults ANOVA showed that body size varied significantly with geog- require more time to flip (Fig. 3). raphy in both years (2014: F  =  10.361; df  =  5, 594; P  <  0.001, 2015: F  =  20.412; df  =  3, 396; P  <  0.001). In 2014, body size in the Yuanping (northern) population was similar to those in the Discussion Tanghai (northern) and Xundian (southern but with high eleva- The ability of invasive insects to colonize and spread in new geo- tion, Table 1) populations but significantly larger than in the other graphic ranges is related to morphological, physiological, or behav- three (southern) populations. In 2015, body size in the Yuanping ioral traits (Piiroinen et  al. 2011, Laparie et  al. 2013). We found population was significantly larger than in the other three popu- that the adult body size of rice water weevil, an invasive insect pest lations. In contrast, in both years, the Tongcheng and Xiangxiang in east Asia, varied significantly with geography. Adults of northern (southern) populations were significantly smaller in body size than (Tanghai and Yuanping) populations and a population at high eleva- the Yuanping and Tanghai (northern) populations. For each popu- tion (Xundian) tended to be larger than those from southern popu- lation, no significant difference was found in body size between lations (Tongcheng and Xiangxiang), exhibiting a body size pattern the 2 yr (Tanghai: t  =  0.801; df  =  191.700; P  =  0.424, Yuanping: of Bergmann’s rule. t  = –1.062; df  =  198; P  = 0.290, Tongcheng: t  = –0.936; df  =  198; It is not clear what ecological factors cause the geographical vari- P = 0.351, and Xiangxiang: t = 0.982; df = 198; P = 0.328; Table 3). ation in L.  oryzophilus adult body size. According to Bergmann’s rule (Blanckenhorn and Demont 2004), temperature can be specu- Comparisons of the SCPs of L. oryzophilus Adults of lated as a major cause. Other factors may also play a role, such as Different Body Sizes the quality of host plant the larvae feed on, as this will vary with rice We measured the SCPs of adults with different body sizes collected variety or/and phenology. from Xiangxiang and Tongcheng. Within each population, the SCPs Within populations, large L. oryzophilus adults did not have sig- of adults did not vary significantly with body size (Xiangxiang: nificantly lower SCPs than small adults, and there was no consistent Table 2. The morphometric traits measured in rice water weevil adults from different geographic populations Year Geographic population No. of adults Prnt-L (mm) Elt-L (mm) Elt-W (mm) Bd-L (mm) 2014 Tanghai 100 0.724 ± 0.002 2.302 ± 0.005 1.438 ± 0.004 3.031 ± 0.006 Yuanping 100 0.731 ± 0.002 2.322 ± 0.007 1.455 ± 0.005 3.055 ± 0.008 Tongcheng 100 0.715 ± 0.004 2.260 ± 0.009 1.385 ± 0.007 2.977 ± 0.011 Yueqing 100 0.715 ± 0.003 2.297 ± 0.010 1.397 ± 0.006 3.011 ± 0.013 Xiangxiang 100 0.711 ± 0.003 2.279 ± 0.010 1.395 ± 0.006 2.989 ± 0.012 Xundian 100 0.712 ± 0.002 2.333 ± 0.009 1.432 ± 0.006 3.044 ± 0.011 2015 Tanghai 100 0.745 ± 0.003 2.359 ± 0.007 1.410 ± 0.005 3.042 ± 0.009 Yuanping 100 0.759 ± 0.003 2.382 ± 0.008 1.453 ± 0.004 3.075 ± 0.008 Tongcheng 100 0.741 ± 0.003 2.317 ± 0.007 1.393 ± 0.006 2.994 ± 0.010 Xiangxiang 100 0.735 ± 0.003 2.343 ± 0.008 1.383 ± 0.006 2.990 ± 0.011 Downloaded from https://academic.oup.com/jinsectscience/article-abstract/18/1/4/4818352 by Ed 'DeepDyve' Gillespie user on 16 March 2018 Journal of Insect Science, 2018, Vol. 18, No. 1 5 Table  3. PC1 values (mean ± SE) for rice water weevils from six fecundity observed in the laboratory may be not fully realized populations under natural conditions (Gotthard et al. 2007), the real extent of body size affecting fecundity might differ to certain degree from the Populations PC1 in 2014 PC1 in 2015 one observed under laboratory controlled conditions. Therefore, the body size and fecundity associations, and the advantages of Tanghai 0.19 ± 0.07abA 0.10 ± 0.08bA Yuanping 0.43 ± 0.08aA 0.55 ± 0.09aA large size should be much more complicated than expected and Tongcheng –0.43 ± 0.11dA –0.29 ± 0.10cA need further research in the future. Yueqing –0.09 ± 0.11bcd – Body size can affect insect activities, such as foraging Xiangxiang –0.23 ± 0.09cdA –0.37 ± 0.11cA (Greenleaf et al. 2007, Guédot et al. 2009), moving (Marden and Xundian 0.13 ± 0.10abc – Kramer 1995, Yang 2000, Samejima and Tsubaki 2010, García and Sarmiento 2012, Cooper et  al. 2013), competition (Moya- Means within a column followed by the same lowercase letter are not sig- Laraño et  al. 2007), and avoiding attack by natural enemies nificantly different (P  > 0.05, Tukey’s test). Means within a row followed by (Remmel and Tammaru 2009). By increasing body, thorax and/ the same capital letter are not significantly different (P > 0.05, t test) or wing size, insects may increase mobility, which, in turn, affects their adaptability to diverse environments (Saastamoinen 2007, Table 4. SCPs (mean ± SE, °C) of L. oryzophilus adults of different Laparie 2013). We found that larger L.  oryzophilus adults had body sizes longer and wider elytra (Table 2). However, it is unclear whether Populations Adult group Bd-L (mm) SCP (°C) such adults would have higher flight capacity and have advan- tages in flight-supported activities over adults with small elytra. Xiangxiang Large 3.092 ± 0.007(22)a −14.2 ± 1.1(22)a In our flip-time observations, small adults were found to be more Mid-size 2.908 ± 0.005(20)b −14.4 ± 1.1(20)a agile (righting their body position more rapidly) than large adults. Small 2.614 ± 0.023(19)c −15.7 ± 1.1(19)a This agility might have advantages, such as allowing small adults Tongcheng Large 3.168 ± 0.006(18)a −18.1 ± 0.6(18)a to more easily escape from attacks of natural enemies. This pro- Mid-size 3.010 ± 0.004(20)b −16.0 ± 1.1(20)a vides valuable empirical evidence for the benefits of small size Small 2.807 ± 0.024(20)c −17.0 ± 1.1(20)a in insects, which has intrigued the interest of some researchers (Blanckenhorn 2000, Chown and Gaston 2010). Means within a column followed by the same letter are not significantly dif- ferent (P > 0.05, Tukey’s HSD test). Numbers in parentheses are the numbers In summary, L.  oryzophilus has successfully invaded a large of adults observed. geographic area in China and exhibits geographic variation in adult body size, which increases with altitude. Moreover, by stud- association between SCP and body size (Table 4). To confirm this re- ying within-population adults of different body size, we showed sult, we further measured the overall SCP in Xiangxiang, Tongcheng that body size is relevant with this weevil’s population biology: and Tanghai adults (not sorted in size groups), which indicated that larger weevils consume more leaf area, lay more and larger eggs, the Tanghai adults (with large body size) had a significantly higher but are less agile than small weevils. Yet, due to the limit of our SCP (–14.3  ±  0.6°C) than Tongcheng adults (–16.7  ±  0.6°C, the observations, we do not know whether such associations also smallest weevils among the populations analyzed; unpublished data). existed among various geographic populations. To be noted, geo- Moreover, in one of our previous studies, the Yueqing (southern) graphic variation in body size and associated life history traits adults were found to have a SCP below –20°C during early winter reflect different life history strategies appropriate to and shaped (Zhang et al. 2004). Combining these findings, we suggest that body by the environmental conditions present in different geographic size might be not associated with cold tolerance in this weevil. The locations. Certainly, results obtained from within-population lack of such an association has also been reported in other insect studies cannot be used to infer the biological significance of body species (Quarles et  al. 2005, Clarke et  al. 2013). The result needs size variation among geographic populations. Despite this, our to be confirmed using other measurements of cold tolerance, such study is valuable describing for the first time associations between as lower lethal temperature, which can provide information about body size and biological traits in rice water weevil. In the future, the survival likelihood of tested insects under given temperatures transplantation experiments are to be performed, that is, putting (Sinclair et al. 2015). weevils originating from one population to the environmental One of the most important findings of our study was that conditions experienced by other populations and then measuring larger L.  oryzophilus adults within populations tended to lay the biology traits. Moreover, such experiments will also allow us more eggs than smaller adults (Table  5), as found in a number of to learn whether the variation of body size in this weevil is the other insects (Honěk 1993, Visser 1994, Kim 1997, Sagarra et al. result of phenotypic plasticity or is the result of genetic variation 2001, Marshall et al. 2013). Moreover, large and mid-size weevils among populations (local adaptation). In addition, as voltinism tended to produce larger eggs than small weevils (Table  5). Thus, may affect patterns of insect body size (Blanckenhorn and Demont we suggest that body size is positively associated with reproductive 2004, Horne et al. 2017), we need to learn whether this weevil’s performance of this weevil. However, it is not clear whether such body size, as well as possible consequences of body size and size an association also exists among geographic populations. That is, variation, will change in southern China. There it originally had do weevils at higher latitudes (elevations), where they are larger two annual generations, but in future, this will shift because rice is than in southern regions, have a higher fecundity? To resolve this increasingly grown in a single season which can only support one question, two factors have to be taken into account. One factor is weevil generation per year (Zhu et al. 2005, Huang et al. 2017). that cooler temperatures at higher latitudes could be less suitable There aspects will be studied in the future, once a viable of method for reproduction. This might potentially reduce the overall repro- artificially rearing these weevils has been developed. Although ductive capacity of large adults. This may mask effects of body rearing has been attempted, the specificity of larvae and pupae’s size and accordingly larger weevils (at higher latitudes) may not oxygen-intake system has so far proved difficult to simulate con- have as high fecundity as expected. Another factor is, because the sistently in the laboratory (Zhang et al. 2006). 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Feeding, reproduction and survival traits (mean ± SE) of L. oryzophilus adults with different body sizes Populations Adult group/ Bd-L (mm) Adult leaf Avg. no. of Ovipositional Adult survival Egg length (mm) Egg hatch percentage ANOVA value consumption (cm) eggs deposited period (days) duration (days) Xiangxiang Large 3.152 ± 0.007(18)a 139.8 ± 10.4(18)ab 46.9 ± 3.6(16)a 20.1 ± 1.7(17)a 26.4 ± 2.1(18)a 0.95 ± 0.02(17)ab 83.9 ± 1.2(329)a Mid-size 2.900 ± 0.007(18)b 154.7 ± 8.8(17)a 42.4 ± 4.4(17)a 19.9 ± 2.0(17)a 31.2 ± 1.9(17)a 0.99 ± 0.02(17)a 81.0 ± 1.9(328)a Small 2.663 ± 0.020(18)c 118.2 ± 6.2(17)b 28.4 ± 3.6(15)b 15.1 ± 1.5(15)a 26.7 ± 1.6(17)a 0.93 ± 0.02(14)b 87.0 ± 2.9(208)a F 379.710 4.399 5.804 2.487 1.926 4.290 2.123 df 2, 51 2, 49 2, 45 2, 46 2, 49 2, 45 2, 22 P 0.000* 0.017* 0.006* 0.094 0.157 0.020* 0.144 Tanghai Large 3.178 ± 0.005(15)a 178.6 ± 8.0(11)a 85.7 ± 13.8(11)a 21.6 ± 1.1(11)a 35.6 ± 1.3(11)a 0.93 ± 0.01(15)a 91.0 ± 2.0(396)a Mid-size 3.024 ± 0.004(15)b 171.3 ± 4.5(14)a 60.0 ± 8.4(14)ab 19.0 ± 1.1(14)a 35.4 ± 1.2(14)a 0.93 ± 0.01(14)a 90.5 ± 0.6(341)a Small 2.873 ± 0.010(15)c 157.2 ± 7.6(15)a 42.9 ± 5.1(11)b 20.3 ± 1.5(13)a 35.0 ± 1.3(14)a 0.89 ± 0.01(14)a 86.7 ± 2.0(354)a F 460.688 2.587 4.622 1.023 0.047 3.511 2.012 df 2, 42 2, 37 2, 33 2, 35 2, 36 2, 40 2, 24 P 0.000* 0.089 0.017* 0.370 0.954 0.039* 0.156 Numbers in parentheses are the numbers of adults or eggs observed. 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