Research Article |
Corresponding author: Lara Redolfi De Zan ( lara.redolfi@gmail.com ) Academic editor: Giuseppino Sabbatini Peverieri
© 2017 Federico Romiti, Lara Redolfi De Zan, Sarah Rossi de Gasperis, Massimiliano Tini, Davide Scaccini, Matteo Anaclerio, Giuseppe Maria Carpaneto.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Romiti F, Redolfi De Zan L, Rossi de Gasperis S, Tini M, Scaccini D, Anaclerio M, Carpaneto G (2017) Latitudinal cline in weapon allometry and phenology of the European stag beetle. In: Campanaro A, Hardersen S, Sabbatini Peverieri G, Carpaneto GM (Eds) Monitoring of saproxylic beetles and other insects protected in the European Union. Nature Conservation 19: 57-80. https://doi.org/10.3897/natureconservation.19.12681
|
Animal body size commonly exhibits a remarkable variation in response to environmental conditions. Latitude, when correlated with temperature, rainfall and seasonality, represents one of the main determinants of variation in body size, as well as in allometry. It has long been recognised that populations of larger body size are found in colder environments (Bergmann’s Rule), a cornerstone of evolutionary ecology. However, the way in which latitude might influence investment in exaggerated weapons of animals has received little attention. The European stag beetle Lucanus cervus (Linnaeus, 1758) is the focus of this study. Males of this species exhibit exaggerated mandibles, mainly used as weapons during intra-sexual conflicts. Five populations ranging from northern Italy to the southern limit of the distribution of L. cervus were analysed. Combining morphological and phenological data, latitudinal variation in body size, weapon investment and activity period of the adults were evaluated. The analysis of the allometry of mandibles strongly supported the presence of two male morphs. Large males (major morph) invest significantly more in weapons compared to males of the minor morph. Consistent with Bergmann’s Rule, these results confirmed that the stag beetle body size increased at higher latitudes (N) and that this increase in size triggers an arms race which leads to further exaggeration of male weapons which is particularly evident in major males. In this morph, the mandible allometric coefficient line was steeper for the northern populations. The activity period also varied with latitude, beginning later at lower latitudes. Characterisation and comparison of adult phenologies provide valuable data to be used in the design of monitoring programmes for this threatened species and are important for modelling the species responses to climate change.
morphometry, exaggerated traits, animal weapons, geographic variation, secondary sexual characters
Variation in animal body size has always attracted considerable interest from biologists. Populations and species can exhibit remarkable variation in body size, as well as in other traits, in response to different environmental conditions (
The ecology of ectotherms is particularly affected by latitude as temperature has a strong influence on their biology (
A total of 767 males of L. cervus were sampled during the breeding season between May and August in the summer 2012–2016. Captures were performed with an entomological net (Ø = 50 cm, telescopic handle = 2 m), by hand and with emergence traps placed on possible oviposition sites detected by means of radio-telemetry. Sampling activities were undertaken in five localities of Italy (Figure
Climate data were obtained for the study sites from WorldClim – Global Climate Data site (http://www.worldclim.org/). Mean (MEA), minimum (MIN) and maximum (MAX) monthly temperatures (C°) and monthly total precipitations (PRE) (mm) of the study sites were downloaded according to their coordinates using the geographic coordinate system WGS84 (not projected) in decimal degrees. The data provided by the web site (section “Current”) are interpolations of observed data, representative of fifty years (1950-2000) and thus represent monthly averages of the selected variables. Data were downloaded with the highest spatial resolution available: 30 seconds, which correspond to cells of 0.86 km2 at the equator (often referred as 1-Km spatial resolution) (
All the biometric variables were natural log transformed (Ln) and checked for normal distribution, as well as the climate variables and phenology, using Shapiro-Wilk normality test, prior to applying any parametric test.
To analyse the variance in climate variables between sites, ANOVA and Tukey HSD tests were performed. The correlation between latitude and climate variables was investigated with the Pearson correlation test. Two discriminant (or classification) techniques were used to categorise sites into groups taking into account their climate variables as predictor characteristics. Both the principal component analysis (PCA) and the linear discriminant analysis (LDA) were applied to the sites’ climate. PCA tries to retain most of the variability in the data, whereas LDA (MASS R package) looks for the combination of the climate variables that give maximum separation between the centres of the site data, minimising the variation within each site. The data were transformed, centred and scaled (caret R package) prior to the application of LDA (
For the allometric analysis of male mandibles, the elytron length was used as an independent variable, mainly for three reasons: (i) its proven high correlation coefficient with mandible length (
To investigate the phenology of the species in each site, it was considered that the adult activity period lasted from the first day of capture to the last one. For the sampling sites with more than a year’s field work (i.e., for BOF, FEL and CRO), the first and last capture date were taken into account, irrespective of the year. In this way, the phenology was dependent on site, rather than be year-dependent. Dates were then transformed into a number in Microsoft Excel 2010, maintaining a fictitious year to avoid any transformation error. Otherwise, inputting the same date for the different years, for example 25/05/2015 and 25/05/2014, different numbers could have resulted i.e. 42149 and 41784 respectively. To test if the phenology varies with latitude, the Kruskal-Wallis test and the Mann-Whitney post-hoc test for pairwise comparison were used.
Despite the Ln transformation of the biometric variables, some maintained a non-normal distribution (MONN = 109: LnML, w = 0.972, p = 0.020; BOFN = 82: LnML, w = 0.958, p = 0.009; TOCN = 75: LnBM, w = 0.960, p = 0.019; LnEL, w = 0.964, p = 0.033; FELN = 357: LnBM, w = 0.991, p = 0.021; LnML, w = 0.966, p< 0.01). Climate variables and phenological data were normally distributed (See Suppl. material
Amongst the analysed climate variables, the monthly total precipitations showed a positive correlation with latitude (Pearson’s test: r = 0.32, p = 0.013). The ANOVA results indicated no significant differences between sites as regard their monthly temperatures (MEA: DF = 4, f = 0.29, p = 0.88; MIN: DF =4, f = 0.32, p = 0.86; MAX: DF = 4, f = 0.28, p = 0.89), but a significant variation in the variance of the monthly total precipitations (PRE: DF = 4, f = 6.56, p< 0.01). The Tukey HSD test indicated a clear difference in the total monthly precipitations (pMONvsBOF< 0.01, pMONvsCRO< 0.01, pMONvsFEL< 0.01, pMONvsTOC< 0.01), with the highest values recorded in MON (See Suppl. material
Scatterplots for the variation of climate variables amongst the sites: A first two principal components of the PCA B first two linear discriminants of the LDA. The percentage of variance explained by each axis was reported in brackets.
Summary of the results of the first 3 principal components (PC) and linear discriminants (LD) of principal component analysis and linear discriminant analysis, respectively.
A | PC1 | PC2 | PC3 |
---|---|---|---|
Standard deviation | 1.7303 | 0.9998 | 0.0797 |
Proportion of Variance | 0.7485 | 0.2499 | 0.0015 |
Cumulative Proportion | 0.7485 | 0.9984 | 1 |
B | LD1 | LD2 | LD3 |
Proportion of trace | 0.9197 | 0.0712 | 0.0090 |
Cumulative Proportion | 0.9197 | 0.9909 | 0.9999 |
The result for the pooled dataset regarding the scaling relationship between mandible length (LnML) and elytron length (LnEL), indicated the presence of a switch point at 22.19 mm of elytron length (± 1.01 mm) (Table
Scatterplots of the allometric relationship between mandible (LnML) and elytron (LnEL) length, with the top ranked model superimposed on the basis of its AIC score. The pooled dataset illustrates the trend of the scaling relationship for all the analysed populations. The allometric trajectory of each population was reported in subsequent scatterplots.
Summary of the models results, obtained by fitting segmented and linear regressions to the scaling relationship between mandible length and elytron length for the pooled dataset (A) and for each population separately (B).
Dataset | Model | AIC | ΔAIC | Adj. R2 | p | DF | SP (± SE) | SL Minor (± SE) | SL Major (± SE) | ANOVA between models | |
---|---|---|---|---|---|---|---|---|---|---|---|
A | Pooled | Segmented | -680.01 | 62.09 | 0.71 | <0.01 | 759 | 3.10 (± 0.01) | 1.78 (± 0.11) | 3.29 (± 0.15) | DF = 1, F = 34.34, P <0.01 |
Linear | -617.92 | 0.69 | <0.01 | 761 | |||||||
B | MON | Segmented | -136.94 | 16.73 | 0.86 | <0.01 | 105 | 3.13 (± 0.02) | 1.92 (± 0.21) | 3.64 (± 0.31) | DF = 1, F = 10.99, P <0.01 |
Linear | -120.21 | 0.83 | <0.01 | 107 | |||||||
BOF | Linear | -38.20 | 1.31 | 0.68 | <0.01 | 80 | DF = 1, F = 1.30, P = 0.28 | ||||
Segmented | -36.88 | 0.68 | <0.01 | 78 | 3.04 (± 0.07) | 1.77 (± 0.54) | 2.74(± 0.31) | ||||
CRO | Segmented | -212.50 | 7.47 | 0.75 | 136 | 2.99 (± 0.03) | 0.66 (± 0.69) | 2.48 (± 0.15) | DF = 1, F = 5.80, P <0.01 | ||
Linear | -205.04 | 0.73 | 138 | ||||||||
TOC | Segmented | -107.99 | 1.07 | 0.70 | <0.01 | 71 | 3.02 (± 0.05) | 1.23 (± 0.37) | 2.26 (± 0.30) | DF = 1, F = 2.48, P = 0.09 | |
Linear | -106.92 | 0.69 | <0.01 | 73 | |||||||
FEL | Segmented | -455.77 | 35.36 | 0.77 | <0.01 | 353 | 3.10 (± 0.01) | 1.80 (± 0.14) | 3.28 (± 0.19) | DF = 1, F = 20.57, P <0.01 | |
Linear | -420.41 | 0.74 | <0.01 | 355 |
Allometric coefficient (± 95% confidence intervals) between weapon (LnML) and body size (LnEL) in relation to latitude for minor males and major males of Lucanus cervus.
The populations exhibited a significant variation in adult activity period (Kruskal-Wallis: hc = 114.3, p< 0.01). In particular, the comparison amongst sites highlighted a significant shift in the phenology between the sites close to the Alps (MON and BOF) and those close to the Apennines (CRO, TOC and FEL) (Mann-Whitney: pMONvsFEL< 0.01; pMONvsTOC< 0.01; pMONvsCRO< 0.01; pBOFvsFEL< 0.01; pBOFvsTOC< 0.01; pBOFvsCRO< 0.01) and an insignificant difference for the other comparisons (Mann-Whitney: pMONvsBOF = 0.96; pTOCvsFEL = 0.91; pTOCvsCRO = 0.06; pFELvsCRO = 0.36).
The results revealed a clear distinction between the studied sites, according to the combination of their climate variables. The northernmost site (MON) was shown to be the rainiest locality, with the lowest monthly temperatures (MIN, MEA and MAX). This is in accordance with the updated climate classification map of
The analysis of mandible allometry on the pooled dataset strengthens the results obtained by
The latitudinal cline in body size has been one of the most widely observed patterns in nature and has interested biologists for over 150 years. Animal body size, according to Bergmann’s Rule, increases with latitude. By studying five populations which span the Italian distribution of the species, a geographical variation in mandible and body size in the stag beetle L. cervus was identified. These results indicate that males of this species invest relatively more in weaponry size at high latitudes, leading to a further exaggeration of this SSC. On the contrary, the size of the post-prothoracic segments did not exhibit a latitudinal cline. As well as defining the allometric coefficient slope for male weaponry, it was shown that the breeding season varies with latitude, beginning later on (late June) at lower latitudes. Characterisation and comparison of adult phenologies, besides being crucial for modelling the insects’ response to climate change, provided valuable data for the conservation and monitoring of a threatened species and are also used as flagship and umbrella species for the conservation of saproxylic fauna in Europe.
We thank two anonymous referees for their helpful comments on an earlier version of the manuscript. We are grateful to Diego Fontaneto for his suggestions about how to obtain climate data and to Manuele Bazzichetto, Gianluca Poeta and Alessandro Albani for their graphical support.
Special issue published with the contribution of the LIFE financial instrument of the European Union.
Box 1. Stag beetle researchers are invited to send us morphometric data on L. cervus, including at least: mandible length, elytron length and body mass, measured as in