Environment vs. Plant Ontogeny: Arthropod Herbivory Patterns on European Beech Leaves along the Vertical Gradient of Temperate Forests in Central Germany
Abstract
:1. Introduction
2. Materials and Methods
2.1. Study Site
2.2. Microclimate and Leaf Trait Data
2.3. Herbivory Data
2.4. Statistical Analyses
3. Results
3.1. Herbivore Feeding Traces
3.2. Feeding Trace Composition
3.3. Effects of Microclimate, Leaf Traits, and Plant Ontogenetic Stage
4. Discussion
5. Conclusions
Acknowledgments
Author Contributions
Conflicts of Interest
Appendix A
Appendix B
Site | Beech | Leaf-Chewing | Sap-Sucking | Leaf-Mining | Gall-Inducing | ||||
---|---|---|---|---|---|---|---|---|---|
Individuals | Small Circles | Labyrinth | Whitish Spots | Tubular Mine | Leaf Edge Gall | Haired Vein Gall | Pannose Spot | Ovate Gall | |
WB-N | juvenile (US) | + | + | + | + | + | + | ||
adult (LC) | + | + | + | + | + | + | |||
adult (UC) | + | + | + | + | + | + | |||
WB-S | juvenile (US) | + | + | + | + | + | + | + | |
adult (LC) | + | + | + | + | + | + | + | ||
adult (UC) | + | + | + | + | + | + | |||
TE-N | juvenile (US) | + | + | + | + | + | + | + | + |
adult (LC) | + | + | + | + | + | + | + | ||
adult (UC) | + | + | + | + | + | + | + | + | |
TE-S | juvenile (US) | + | + | + | + | + | + | + | + |
adult (LC) | + | + | + | + | + | + | + | + | |
adult (UC) | + | + | + | + | + | + | |||
KBVB-N | juvenile (us) | + | + | + | + | + | + | + | |
adult (lc) | + | + | + | + | + | + | + | ||
adult (uc) | + | + | + | + | + | + | |||
KBVB-S | juvenile (US) | + | + | + | + | + | + | + | + |
adult (LC) | + | + | + | + | + | + | |||
adult (UC) | + | + | + | + | + | + | |||
SS-N | juvenile (US) | + | + | + | + | + | + | + | + |
adult (LC) | + | + | + | + | + | ||||
adult (UC) | + | + | + | + | + | + | + | ||
SS-S | juvenile (US) | + | + | + | + | + | + | + | |
adult (LC) | + | + | + | + | + | + | |||
adult (UC) | + | + | + | + | + | + | |||
HGB-N | juvenile (US) | + | + | + | + | + | + | ||
adult (LC) | + | + | + | + | + | ||||
adult (UC) | + | + | + | + | + | ||||
HGB-S | juvenile (US) | + | + | + | + | + | + | + | + |
adult (LC) | + | + | + | + | + | + | + | ||
adult (UC) | + | + | + | + | |||||
BB-N | juvenile (US) | + | + | + | + | + | + | ||
adult (LC) | + | + | + | + | + | + | |||
adult (UC) | + | + | + | + | + | + | |||
BB-S | juvenile (US) | + | + | + | + | + | + | + | + |
adult (LC) | + | + | + | + | + | + | + | ||
adult (UC) | + | + | + | + | + | + | + | ||
HB-N | juvenile (US) | + | + | + | + | + | + | + | |
adult (LC) | + | + | + | + | + | + | + | ||
adult (UC) | + | + | + | + | + | + | + | ||
HB-S | juvenile (US) | + | + | + | + | + | + | ||
adult (LC) | + | + | + | + | + | + | |||
adult (UC) | + | + | + | + | + | + | |||
FK-N | juvenile (US) | + | + | + | + | + | + | ||
adult (LC) | + | + | + | + | + | + | |||
adult (UC) | + | + | + | + | + | + | |||
FK-S | juvenile (US) | + | + | + | + | + | + | ||
adult (LC) | + | + | + | + | + | + | |||
adult (UC) | + | + | + | + | + | + | + | ||
HDB-N | juvenile (US) | + | + | + | + | + | + | + | |
adult (LC) | + | + | + | + | + | ||||
adult (UC) | + | + | + | + | + | + | + | ||
HDB-S | juvenile (US) | + | + | + | + | + | + | ||
adult (LC) | + | + | + | + | + | + | |||
adult (UC) | + | + | + | + | |||||
EL-N | juvenile (US) | + | + | + | + | + | + | ||
adult (LC) | + | + | + | + | + | + | |||
adult (UC) | + | + | + | + | + | + | + | ||
EL-S | juvenile (US) | + | + | + | + | + | + | + | |
adult (LC) | + | + | + | + | + | + | + | + | |
adult (UC) | + | + | + | + | + | + | + |
Appendix C
Parameter | Beech Individual | ||
---|---|---|---|
Juvenile (US) | Adult (LC) | Adult (UC) | |
Microclimate: | |||
temperature (°C) 1 | 17.9 (17.6,18.2) a | 18.8 (18.6,19.1) b | 19.9 (19.6,20.6) c |
relative air humidity (%) 2 | 83 (80,86) a | 74 (72,76) b | 69 (68,70) c |
Leaf traits: | |||
SLA (m2 kg−1) 2 | 38 (35,42) a | 28 (24,33) b | 16 (15,18) c |
leaf area (cm2) 2 | 23 (21,24) a | 30 (23,34) b | 20 (19,23) a |
N (mg g−1) 1 | 22 (21,24) a | 23 (22,24) a | 21 (20,22) b |
C (mg g−1) 1 | 475 (472,748) a | 478 (476,480) b | 483 (481,486) c |
C/N ratio (g g−1) 2 | 21.3 (19.8,22.1) a | 21.0 (19.7,22.2) a | 23.4 (22.5,24.4) b |
chlorophyll (CCI) 1 | 13.8 (12.6,14.3) a | 13.5 (13.1,15.6) a | 13.2 (12.0,14.2) a |
Appendix D
- Call: metaMDS(comm = species, k = 2)
- global Multidimensional Scaling using monoMDS
- Data: wisconsin(sqrt(species))
- Distance: bray
- Dimensions: 2
- Stress: 0.1870401
- Stress type 1, weak ties
- Two convergent solutions found after 20 tries
- Scaling: centring, PC rotation, halfchange scaling
- Species: expanded scores based on ‘wisconsin(sqrt(species))
- ***VECTORS
- NMDS1 NMDS2 r2 Pr(>r)
- temp_dayav 0.99872 -0.05053 0.2489 0.001 ***
- humid_dayav -0.99926 0.03837 0.4612 0.001 ***
- SLA -0.97297 -0.23095 0.4257 0.001 ***
- Ctotal 0.99002 -0.14094 0.1665 0.006 **
- Ntotal -0.63438 -0.77302 0.1605 0.008 **
- C.N 0.65518 0.75547 0.1729 0.007 **
- chloro -0.87043 -0.49229 0.0544 0.234
- Permutation: free
- Number of permutations: 999
- 3 observations deleted due to missingness
- ***VECTORS
- NMDS1 NMDS2 r2 Pr(>r)
- temperature 0.99872 -0.05051 0.2489 0.001 ***
- humidity -0.99926 0.03836 0.4612 0.001 ***
- SLA -0.97296 -0.23095 0.4257 0.001 ***
- C 0.99002 -0.14094 0.1665 0.007 **
- N -0.63438 -0.77302 0.1605 0.009 **
- C.N 0.65518 0.75548 0.1729 0.005 **
- Permutation: free
- Number of permutations: 999
- 3 observations deleted due to missingness
Appendix E
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Feeding Trace 1 | Description | Guild 2 | Leaf Side 3 | Probable Arthropod Species 1 |
---|---|---|---|---|
(a) Exophagous: | ||||
windows | scraping damage on leaf surface | ch | Diurnea fagella (Denis and Schiffermüller, 1775) | |
small circles | missing leaf area as small circles | ch | Orchestes fagi (Linnaeus, 1758) | |
labyrinth | missing leaf area in form of labyrinths | ch | Phyllobius argentatus (Linnaeus, 1758) | |
whitish spots | leaf flecked with whitish spots | s | ADS | Fagocyba cruenta (Herrich-Schäffer, 1838) |
wax wool | waxed threads on leaf surface | s | ABS | Phyllaphis fagi (Linnaeus, 1767) |
(b) Endophagous: | ||||
tubular mine | tubular shaped mine between lateral veins | m | ABS | Phyllonorycter maestingella (Müller, 1764) |
oval mine | oval shaped mine between lateral veins | m | ABS | Phyllonorycter messaniella (Zeller, 1846) |
line crossing veins | wide corridor mine crossing lateral veins | m | Stigmella hemargyrella (Kollar, 1832) | |
line between veins | zigzag mine between lateral veins | m | Stigmella tityrella (Stainton, 1854) | |
leaf edge gall | gall causing rolled-up leaf edges | g | Acalitus stenaspis (Nalepa, 1891) | |
haired vein gall | haired gall along lateral leaf veins | g | ADS | Aceria nervisequa (Canestrini, 1891) |
pannose spot | pannose spot between lateral veins | g | ABS | Aceria nervisequa faginea (Nalepa, n.d.) |
haired brownish gall | cylindrical, haired brownish gall | g | ADS | Hartigiola annulipes (Hartig, 1839) |
ovate gall | ovate, acuminated gall (green to red) | g | ADS | Mikiola fagi (Hartig, 1839) |
pleated gall | swollen, pleated leaf tissue forming a pouch | g | ADS | Phegomyia fagicola (Kieffer, 1901) |
Feeding Guild | Feeding Trace | Attack Leaves (%) | ||
---|---|---|---|---|
Overall | Juvenile Beech | Adult Beech | ||
leaf-chewing | small circles | 36 (29,65) a | 39 (30,54) a | 35 (28,72) a |
labyrinth | 0 (0,7) b,c | 6 (0,13) b | 0 (0,2) b,d | |
sap-sucking | whitish spots | 41 (27,60) a | 72 (59,78) a | 32 (23,49) a |
leaf-mining | tubular mine | 0 (0,2) c | 3 (2,4) b | 0 (0,0) b |
gall-inducing | leaf edge gall | 9 (1,24) d,e | 1 (0,4) b | 19 (3,32) c,d,e |
haired vein gall | 7 (2,16) d | 2 (1,4) b | 12 (5,21) e | |
pannose spot | 18 (7,35) e | 6 (4,12) b | 30 (15,42) a,c | |
ovate gall | 6 (2,13) b,d | 8 (3,15) b | 13 (4,21) d,e |
Model | d.f. | F-Values 1,2 | ||||||||
---|---|---|---|---|---|---|---|---|---|---|
Parameters | Exophagous | Endophagous | ||||||||
n. | d. | Small Circles | Labyrinth | Whitish Spots | Tubular Mine | Leaf Edge Gall | Haired Vein Gall | Pannose Spot | Ovate Gall | |
humidity | 1 | 55 | 1.29 | |||||||
N content | 1 | 55 | 0.98 | |||||||
N content + stage | 2 | 54 | 20.50 *** | 16.99 *** | 14.62 *** | 18.15 *** | ||||
CN + stage | 2 | 54 | 17.72 *** | 21.08 *** | 16.31 *** | 17.25 *** | ||||
stage | 1 | 55 | 0.19 | 9.79 ** | 30.85 *** | 37.25 *** | 17.96 *** | 18.64 *** | 27.56 *** | 1.33 |
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Stiegel, S.; Mantilla-Contreras, J. Environment vs. Plant Ontogeny: Arthropod Herbivory Patterns on European Beech Leaves along the Vertical Gradient of Temperate Forests in Central Germany. Insects 2018, 9, 9. https://doi.org/10.3390/insects9010009
Stiegel S, Mantilla-Contreras J. Environment vs. Plant Ontogeny: Arthropod Herbivory Patterns on European Beech Leaves along the Vertical Gradient of Temperate Forests in Central Germany. Insects. 2018; 9(1):9. https://doi.org/10.3390/insects9010009
Chicago/Turabian StyleStiegel, Stephanie, and Jasmin Mantilla-Contreras. 2018. "Environment vs. Plant Ontogeny: Arthropod Herbivory Patterns on European Beech Leaves along the Vertical Gradient of Temperate Forests in Central Germany" Insects 9, no. 1: 9. https://doi.org/10.3390/insects9010009