Range geography and temperature variability explain cross-continental convergence in range and phenology shifts in a model insect taxon
Figures
Representation of temporal and geographical limits characterizing the ecological niche of a hypothetical odonate species.
Points show 250 individuals according to their Julian day of emergence, latitudinal position, and temperatures to which each individual is exposed. Points represent historical observations (T1), plus signs show observations following a shift toward earlier emergence dates after warming (T2a), and triangle symbols show observations following a shift toward higher latitudes after warming (T2b). Species could also shift both range and phenology in response to warming (T2c). Warm and cool colors show hot and cold temperatures, respectively.
Distribution of northern range limit shifts (A) kilometers and emergence phenology shift (B) Julian day of 76 European and North American odonate species between a recent time period (2008–2018) and a historical time period (1980–2002).
Anisoptera (dragonflies) are shown in pink, Zygoptera (damselflies) are shown in blue.
Relationship between range shifts and emergence phenology shifts among North American and European odonate species (N = 66; model R2 = 17.08 for generalized linear model [GLM], 14.9% for Markov Chain Monte Carlo generalized linear mixed model [MCMCglmm]).
For reference, the shaded area shows mean latitudinal range shifts of terrestrial taxa as reported by Lenoir et al. (calculated as the yearly mean dispersal rate of 1.11 ± 0.96 km per year over 38 years).
p-values and coefficients of 1000 generalized linear model (GLM) iterations testing whether range shifts as calculated from random datasets predict the range shifts measured in the study.
Each point shows the results of a single GLM model, with measured range shifts as the dependent variable and randomized range shifts as the independent variable.
Observed range shifts in km from the equator, against randomized predicted values according to four random datasets.
Points represent species, and each pane contains a different set of random data in calculations of randomized range shifts. There is no consistent relationship among 1000 iterations.
p-values and coefficients of 1000 generalized linear model (GLM) iterations testing whether phenology shifts as calculated from random datasets predict the phenology shifts measured in the study.
Each point shows the results of a single GLM model, with measured phenology shifts as the dependent variable and randomized phenology shifts as the independent variable.
Observed phenology shifts in Julian day, against randomized predicted values according to four random datasets.
Points represent species, and each pane contains a different set of random data in calculations of randomized phenology shifts. There is no consistent relationship among 1000 iterations.
Panels A and B show the trace and density estimates of a phylogenetic mixed effects model exploring the relationship between range and phenology shifts in North American and European odonates (N = 66).
150,000 iterations were run to produce these results. These plots verify model convergence and absence of autocorrelation within the explanatory variables.
Panels A and B show the trace and density estimates of a phylogenetic mixed effects model testing whether ecological traits, and geographic and climatic attributes predict range shifts in North American and European odonates (N = 76).
150,000 iterations were run to produce these results. Results of the best model, according to DIC, are shown here. These plots verify model convergence and absence of autocorrelation within the explanatory variables.
Richness of 76 odonate species sampled in North America and Europe in the historic period (1980–2002; panes A and C) and the recent period (2008–2018; panes B and D).
Species richness per 100 × 100 km quadrat is shown in panes A and B, while panes C and D show species richness per 200 × 200 km quadrat. Dark red indicates high species richness, while light pink indicates low species richness.
Tables
Fixed effects estimates and associated statistics from the generalized linear model and generalized mixed effects model (accounting for phylogeny; for credible intervals, see Appendix 1—table 4) of the relationship between range shifts and emergence phenology change.
The continent term shows effects of the North American continent compared to the European continent as the reference level. N gives the number of species involved in the model, and an asterisk indicates statistical significance of the variable in question (p-value <0.05). The pseudo R2 type is Nagelkerke, 1991.
| Phenology shift (N = 66) | ||||
|---|---|---|---|---|
| GLM | MCMCglmm | |||
| Predictors | Est. | p | Post.m | p |
| (Intercept) | 0.12 | 0.53 | 0.12 | 0.53 |
| Range shift | −0.45 | <0.01* | −0.45 | <0.01* |
| Continent | −0.22 | 0.44 | −0.22 | 0.44 |
| Model evaluation | ||||
| AIC/DIC | 185.39 | 185.43 | ||
| Null model | 193.13 | 193.12 | ||
| Pseudo R2 | 17.08% | 14.90% | ||
Fixed effects estimates and associated statistics from the generalized linear model and generalized mixed effects model (accounting for phylogeny; for credible intervals, see Appendix 1—table 4) of drivers of odonate range shifts.
N indicates the number of modeled species, an asterisk indicates statistical significance of the variable in question, and a dash symbol shows that the variable was excluded from the final model. The pseudo R2 type is Nagelkerke, 1991. For the categorical variables breeding habitat type and range geography, we used lotic habitat type and Northern range as reference levels, respectively.
| Range shift (N = 76) | ||||
|---|---|---|---|---|
| GLM | MCMCglmm | |||
| Predictors | Est. | p | Post.m | p |
| (Intercept) | −0.65 | 0.018 | −0.65 | 0.022 |
| Widespread distribution | 0.34 | 0.32 | 0.34 | 0.31 |
| Southern distribution | 0.95 | 0.002 | 0.95 | 0.004 |
| T° variability | −0.38 | 0.0005 | −0.38 | 0.002 |
| Model evaluation | ||||
| AIC/DIC | 202.8 | 202.9 | ||
| Null model | 218.7 | 218.7 | ||
| Pseudo R2 | 26.60% | 23.70% | ||
| Phylogenetic signal | ||||
| Pagel’s lambda (p) | 0.0057 (0.89) | |||
| Blomberg’s K (p) | 0.11 (0.47) | |||
Samples of 76 North American and European odonate species from between 1980 and 2018 followed our criteria for quality observation records for inclusion in our analysis of geographical shifts.
Species northern range limits (NRL) are shown in this table, as well as range limit shifts. All range limit values are shown in kilometers from the equator. We used the 10 most northern points of sampling in each time period to identify species’ NRL, as detailed in the Methods section of the main text.
| Species | Continent | NRL (1980–2002) | NRL (2008–2018) | NRL shift |
|---|---|---|---|---|
| Aeshna constricta | North America | 5500.81 | 5692.6 | 191.79 |
| Aeshna cyanea | Europe | 6880.39 | 7018.26 | 137.87 |
| Aeshna eremita | North America | 7527.81 | 7394.66 | –133.16 |
| Aeshna grandis | Europe | 7504.84 | 7607.68 | 102.83 |
| Aeshna interrupta | North America | 7235.65 | 7286.83 | 51.18 |
| Aeshna juncea | Europe | 7747.56 | 7812.16 | 64.6 |
| Aeshna mixta | Europe | 6566.18 | 6776.3 | 210.12 |
| Aeshna umbrosa | North America | 6691.19 | 6209.63 | –481.55 |
| Anax imperator | Europe | 6263.92 | 6548.57 | 284.65 |
| Anax junius | North America | 5539.31 | 5666.11 | 126.8 |
| Argia apicalis | North America | 4922.17 | 5219.38 | 297.22 |
| Argia fumipennis | North America | 5235.2 | 5168.12 | –67.08 |
| Argia moesta | North America | 5533.74 | 5301.98 | –231.77 |
| Basiaeschna janata | North America | 5649.43 | 5655.77 | 6.34 |
| Brachytron pratense | Europe | 6737.42 | 6905.46 | 168.04 |
| Calopteryx maculata | North America | 5329.56 | 5359.13 | 29.57 |
| Calopteryx virgo | Europe | 7275.9 | 7549.35 | 273.45 |
| Ceriagrion tenellum | Europe | 5900.55 | 5950.63 | 50.08 |
| Coenagrion hastulatum | Europe | 7528.94 | 7651.51 | 122.57 |
| Coenagrion mercuriale | Europe | 5913.57 | 5867.06 | –46.52 |
| Coenagrion puella | Europe | 6904.7 | 6869.58 | –35.12 |
| Coenagrion pulchellum | Europe | 7076.45 | 7152.81 | 76.36 |
| Coenagrion resolutum | North America | 7516.44 | 7408.7 | –107.73 |
| Cordulegaster boltonii | Europe | 7237.43 | 7346.93 | 109.49 |
| Cordulia aenea | Europe | 7400.12 | 7434.02 | 33.9 |
| Cordulia shurtleffii | North America | 7499.82 | 7421.98 | –77.84 |
| Enallagma antennatum | North America | 5037.73 | 5347.01 | 309.28 |
| Enallagma basidens | North America | 4768.61 | 4850.05 | 81.44 |
| Enallagma carunculatum | North America | 5950.86 | 5592.47 | –358.38 |
| Enallagma civile | North America | 5322.59 | 5473.78 | 151.19 |
| Enallagma cyathigerum | Europe | 7594.97 | 7733.06 | 138.09 |
| Enallagma ebrium | North America | 6341.31 | 5907.69 | –433.62 |
| Enallagma exsulans | North America | 5655.94 | 5253.94 | –402 |
| Enallagma hageni | North America | 6113.97 | 5865.52 | –248.45 |
| Enallagma signatum | North America | 5208.92 | 5281.09 | 72.17 |
| Epitheca cynosura | North America | 5541.19 | 5582.56 | 41.37 |
| Erythemis simplicicollis | North America | 5271 | 5292.65 | 21.65 |
| Erythromma najas | Europe | 7171.87 | 7372.13 | 200.25 |
| Gomphus vulgatissimus | Europe | 6890.76 | 7010.12 | 119.37 |
| Hetaerina americana | North America | 5044.41 | 5244.49 | 200.08 |
| Ischnura cervula | North America | 5973.57 | 5526.83 | –446.74 |
| Ischnura hastata | North America | 4725.07 | 4897.71 | 172.65 |
| Ischnura perparva | North America | 5608.92 | 5438.53 | –170.4 |
| Ischnura posita | North America | 5084.08 | 5143.79 | 59.71 |
| Ischnura pumilio | Europe | 6213.77 | 6769.62 | 555.85 |
| Ischnura verticalis | North America | 5579.68 | 5750.9 | 171.22 |
| Ladona julia | North America | 5908.68 | 5871.84 | –36.83 |
| Lestes congener | North America | 6240.48 | 5803.75 | –436.74 |
| Lestes disjunctus | North America | 7294.75 | 7314.26 | 19.51 |
| Lestes dryas | Europe | 6824.89 | 7108.33 | 283.44 |
| Lestes rectangularis | North America | 5263.85 | 5552.64 | 288.79 |
| Lestes unguiculatus | North America | 5803.91 | 6030.62 | 226.71 |
| Leucorrhinia dubia | Europe | 7675.72 | 7749.01 | 73.29 |
| Leucorrhinia hudsonica | North America | 7500.27 | 7446.85 | –53.42 |
| Libellula depressa | Europe | 6810.85 | 7015.37 | 204.52 |
| Libellula fulva | Europe | 6602.18 | 6882.5 | 280.32 |
| Libellula luctuosa | North America | 5337.86 | 5320.1 | –17.76 |
| Libellula pulchella | North America | 5556.31 | 5692.14 | 135.83 |
| Orthetrum coerulescens | Europe | 6744.55 | 6903.01 | 158.46 |
| Pachydiplax longipennis | North America | 5495.02 | 5467.11 | –27.92 |
| Pantala flavescens | North America | 5190.25 | 5510.15 | 319.9 |
| Perithemis tenera | North America | 4929.38 | 5192.47 | 263.09 |
| Plathemis lydia | North America | 5539.41 | 5594.8 | 55.38 |
| Platycnemis pennipes | Europe | 6934.22 | 7125.72 | 191.5 |
| Pyrrhosoma nymphula | Europe | 7131.07 | 7313.37 | 182.3 |
| Rhionaeschna californica | North America | 5641.53 | 5458.21 | –183.32 |
| Rhionaeschna multicolor | North America | 5581 | 5477.34 | –103.66 |
| Somatochlora metallica | Europe | 7718.67 | 7743.21 | 24.54 |
| Somatochlora semicircularis | North America | 6533.02 | 5994.13 | –538.89 |
| Sympetrum corruptum | North America | 5585.68 | 5733.2 | 147.52 |
| Sympetrum danae | Europe | 7268.54 | 7565.29 | 296.75 |
| Sympetrum internum | North America | 7179.45 | 7121.38 | –58.07 |
| Sympetrum pallipes | North America | 5655.65 | 5527.84 | –127.8 |
| Sympetrum sanguineum | Europe | 6663.43 | 6970.56 | 307.13 |
| Sympetrum striolatum | Europe | 6972.22 | 7098.74 | 126.52 |
| Sympetrum vulgatum | Europe | 6897.33 | 7274.78 | 377.45 |
Sixty-six species sampled across North America and Europe between 1980 and 2018 followed our criteria for quality observation records for inclusion in our analysis of emergence phenology shifts.
Mean phenological shifts (PS) are measured in the number of Julian days comparing both time periods, as estimated using the Weibull distribution (see Methods). We also report the number of 200 × 200 quadrats used to calculate phenology estimates per species.
| Species | Number of quadrats | Mean PS |
|---|---|---|
| Aeshna cyanea | 37 | –8.05 |
| Aeshna grandis | 43 | 6.73 |
| Aeshna juncea | 34 | –1.11 |
| Aeshna mixta | 22 | –12.95 |
| Aeshna umbrosa | 8 | 27.42 |
| Anax imperator | 27 | 4.05 |
| Anax junius | 19 | –12.21 |
| Argia fumipennis | 8 | –3.39 |
| Argia moesta | 11 | –7.62 |
| Basiaeschna janata | 2 | –4.69 |
| Brachytron pratense | 24 | –8.18 |
| Calopteryx maculata | 15 | –4.14 |
| Calopteryx virgo | 41 | 4.35 |
| Ceriagrion tenellum | 14 | –3.88 |
| Coenagrion hastulatum | 20 | –4.97 |
| Coenagrion mercuriale | 11 | 5.80 |
| Coenagrion puella | 33 | –1.00 |
| Coenagrion pulchellum | 29 | 1.94 |
| Coenagrion resolutum | 2 | 0.33 |
| Cordulegaster boltonii | 34 | 4.08 |
| Cordulia aenea | 31 | –7.72 |
| Cordulia shurtleffii | 4 | 1.78 |
| Enallagma basidens | 2 | 0.52 |
| Enallagma carunculatum | 8 | 5.10 |
| Enallagma civile | 11 | 1.82 |
| Enallagma cyathigerum | 46 | –9.81 |
| Enallagma ebrium | 7 | –1.34 |
| Enallagma exsulans | 8 | –2.83 |
| Enallagma hageni | 5 | –4.79 |
| Enallagma signatum | 6 | 1.51 |
| Epitheca cynosura | 4 | –8.82 |
| Erythemis simplicicollis | 15 | 0.01 |
| Erythromma najas | 35 | –4.82 |
| Gomphus vulgatissimus | 12 | –9.14 |
| Hetaerina americana | 6 | –10.15 |
| Ischnura cervula | 3 | 10.65 |
| Ischnura perparva | 2 | 8.85 |
| Ischnura posita | 12 | –5.55 |
| Ischnura pumilio | 14 | –0.97 |
| Ischnura verticalis | 16 | 2.39 |
| Ladona julia | 9 | 4.29 |
| Lestes congener | 9 | 6.03 |
| Lestes disjunctus | 4 | 10.48 |
| Lestes dryas | 6 | 5.13 |
| Lestes rectangularis | 12 | 0.81 |
| Leucorrhinia dubia | 18 | –6.05 |
| Leucorrhinia hudsonica | 4 | –13.17 |
| Libellula depressa | 30 | –6.13 |
| Libellula fulva | 16 | –2.50 |
| Libellula luctuosa | 15 | –5.11 |
| Libellula pulchella | 14 | –6.43 |
| Orthetrum coerulescens | 22 | 4.11 |
| Pachydiplax longipennis | 13 | –3.84 |
| Perithemis tenera | 5 | –13.60 |
| Plathemis lydia | 14 | 0.30 |
| Platycnemis pennipes | 30 | –0.40 |
| Pyrrhosoma nymphula | 39 | –19.40 |
| Rhionaeschna californica | 2 | –8.41 |
| Rhionaeschna multicolor | 4 | –11.68 |
| Somatochlora metallica | 31 | 7.91 |
| Sympetrum danae | 32 | –3.34 |
| Sympetrum internum | 5 | 3.05 |
| Sympetrum pallipes | 3 | 9.67 |
| Sympetrum sanguineum | 28 | –13.30 |
| Sympetrum vulgatum | 16 | –13.56 |
Ecological and geographical traits of 76 North American and European odonate species used in this work.
Field guides (Cannings, 2002; Jones et al., 2008; Paulson, 2012) and existing trait databases (Powney et al., 2014; Waller et al., 2019) were used to build this dataset. Habitat type represents species’ breeding habitat and can have a value of lentic, lotic, or both types. Distribution shows the general geographic position of each species’ range, which can be widespread (W), southern (S), northern (N), southern and widespread (S–W), or northern and widespread (N–W). Oviposition type corresponds to egg laying inside plants (endophytic) as opposed to directly in water or on plants (exophytic). Body size is measured as body length in mm. In the case that body length was given as a maximum and minimum value, we used the average of both values.
| Species | Habitat | Distribution | Flight | Oviposition | Body size |
|---|---|---|---|---|---|
| Aeshna constricta | Both | W | 2.5 | Endophytic | 69 |
| Aeshna cyanea | Lentic | S | 3 | Endophytic | 71.5 |
| Aeshna eremita | Both | N–W | 3 | Endophytic | 72.5 |
| Aeshna grandis | Both | N | 4 | Endophytic | 73.5 |
| Aeshna interrupta | Both | W | 3 | Endophytic | 66.5 |
| Aeshna juncea | Lentic | N | 4.5 | Endophytic | 75.5 |
| Aeshna mixta | Both | S | 2.5 | Endophytic | 60 |
| Aeshna umbrosa | Both | W | 3 | Endophytic | 68.5 |
| Anax imperator | Lentic | S | 2.5 | Endophytic | 76.5 |
| Anax junius | Both | S–W | 7 | Endophytic | 74 |
| Argia apicalis | Both | S–W | 4 | Endophytic | 36.5 |
| Argia fumipennis | Both | S–W | 3.5 | Endophytic | 31.5 |
| Argia moesta | Lotic | S–W | 3 | Endophytic | 39.5 |
| Basiaeschna janata | Both | W | 1 | Endophytic | 59 |
| Brachytron pratense | Lentic | S | 2 | Endophytic | 58.5 |
| Calopteryx maculata | Lotic | S–W | 3 | Endophytic | 48 |
| Calopteryx virgo | Lotic | W | 3.5 | Endophytic | 47 |
| Ceriagrion tenellum | Both | S | 3 | Endophytic | 30 |
| Coenagrion hastulatum | Lentic | N | 2.5 | Endophytic | 32 |
| Coenagrion mercuriale | Lotic | S | 2.5 | Endophytic | 29.5 |
| Coenagrion puella | Lentic | S | 3.5 | Endophytic | 34 |
| Coenagrion pulchellum | Both | S | 2 | Endophytic | 36 |
| Coenagrion resolutum | Lentic | N–W | 2.5 | Endophytic | 30 |
| Cordulegaster boltonii | Lotic | W | 3.5 | Endophytic | 77 |
| Cordulia aenea | Lentic | S | 2 | Exophytic | 51 |
| Cordulia shurtleffii | Both | N–W | 2 | Exophytic | 46 |
| Enallagma antennatum | Both | S–W | 2 | Endophytic | 30 |
| Enallagma basidens | Both | S–W | 4.5 | Endophytic | 24.5 |
| Enallagma carunculatum | Both | W | 3.5 | Endophytic | 31.5 |
| Enallagma civile | Both | S–W | 3.5 | Endophytic | 33.5 |
| Enallagma cyathigerum | Both | W | 3.5 | Endophytic | 32 |
| Enallagma ebrium | Both | N–W | 2.5 | Endophytic | 31 |
| Enallagma exsulans | Both | S–W | 3.5 | Endophytic | 34 |
| Enallagma hageni | Both | N–W | 2.5 | Endophytic | 30 |
| Enallagma signatum | Both | S–W | 2.5 | Endophytic | 32.5 |
| Epitheca cynosura | Both | S–W | 2.5 | Endophytic | 40.5 |
| Erythemis simplicicollis | Both | S–W | 2.5 | Endophytic | 41 |
| Erythromma najas | Both | S | 3 | Endophytic | 33 |
| Gomphus vulgatissimus | Lotic | S | 2 | Exophytic | 47.5 |
| Hetaerina americana | Lotic | S–W | 5 | Endophytic | 42 |
| Ischnura cervula | Both | W | 6 | Endophytic | 27.5 |
| Ischnura hastata | Lentic | S–W | 3.5 | Endophytic | 24 |
| Ischnura perparva | Both | S–W | 5 | Endophytic | 26.5 |
| Ischnura posita | Both | S–W | 3.5 | Endophytic | 25 |
| Ischnura pumilio | Lentic | S | 3 | Endophytic | 29 |
| Ischnura verticalis | Both | W | 3.5 | Endophytic | 26.5 |
| Ladona julia | Lentic | N–W | 2 | Endophytic | 41.5 |
| Lestes congener | Lentic | W | 2.5 | Endophytic | 36.5 |
| Lestes disjunctus | Both | W | 2.5 | Endophytic | 37.5 |
| Lestes dryas | Lentic | S | 2 | Endophytic | 37.5 |
| Lestes rectangularis | Both | S–W | 2.5 | Endophytic | 45 |
| Lestes unguiculatus | Both | W | 3 | Endophytic | 37.5 |
| Leucorrhinia dubia | Lentic | N | 2.5 | Exophytic | 33.5 |
| Leucorrhinia hudsonica | Lentic | N–W | 2 | Endophytic | 29.5 |
| Libellula depressa | Lentic | S | 2.5 | Exophytic | 43.5 |
| Libellula fulva | Lentic | S | 2 | Exophytic | 43.5 |
| Libellula luctuosa | Lentic | S–W | 2.5 | Exophytic | 46 |
| Libellula pulchella | Both | W | 2.5 | Endophytic | 54.5 |
| Orthetrum coerulescens | Lotic | S | 3 | Exophytic | 40.5 |
| Pachydiplax longipennis | Both | S–W | 3 | Endophytic | 35.5 |
| Pantala flavescens | Both | S | 3 | Exophytic | 48.5 |
| Perithemis tenera | Both | S–W | 4.5 | Exophytic | 22.5 |
| Plathemis lydia | Both | S–W | 3 | Exophytic | 45 |
| Platycnemis pennipes | Lotic | S | 2.5 | Endophytic | 36 |
| Pyrrhosoma nymphula | Lentic | W | 1.5 | Endophytic | 34.5 |
| Rhionaeschna californica | Lentic | S–W | 4 | Endophytic | 60.5 |
| Rhionaeschna multicolor | Both | S–W | 2 | Endophytic | 67 |
| Somatochlora metallica | Both | W | 1.5 | Exophytic | 53 |
| Somatochlora semicircularis | Lentic | W | 2 | Exophytic | 49.5 |
| Sympetrum corruptum | Both | S–W | 5 | Exophytic | 40.5 |
| Sympetrum danae | Lentic | W | 2 | Exophytic | 31.5 |
| Sympetrum internum | Lentic | W | 4 | Exophytic | 33.5 |
| Sympetrum pallipes | Both | S–W | 2 | Endophytic | 36 |
| Sympetrum sanguineum | Lentic | S | 3.5 | Exophytic | 36.5 |
| Sympetrum striolatum | Both | W | 5 | Exophytic | 39.5 |
| Sympetrum vulgatum | Lentic | S | 2 | Exophytic | 37.5 |
Credible intervals of all MCMCglmm models testing predictions regarding the range and phenology shifts across 66 odonate species in North America and Europe.
These models are detailed in Model information and statements of the Supplementary Information.
| Lower credible interval | Upper credible interval | |
|---|---|---|
| Phenological shifts ~ range shifts | ||
| (Intercept) | –0.26 | 0.49 |
| Range shifts | –0.71 | –0.16 |
| Continent | –0.75 | 0.30 |
| Range shifts ~ range geography + T° variability | ||
| (Intercept) | –1.22 | –0.12 |
| Southern range | 0.36 | 1.56 |
| Widespread | –0.32 | 1.08 |
| T° variability | –0.60 | –0.18 |