Research Article |
Corresponding author: Pascale Zumstein ( zumstein@leuphana.de ) Academic editor: John Spence
© 2021 Pascale Zumstein, Helge Bruelheide, Andreas Fichtner, Andreas Schuldt, Michael Staab, Werner Härdtle, Hongzhang Zhou, Thorsten Assmann.
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:
Zumstein P, Bruelheide H, Fichtner A, Schuldt A, Staab M, Härdtle W, Zhou H, Assmann T (2021) What shapes ground beetle assemblages in a tree species-rich subtropical forest? In: Spence J, Casale A, Assmann T, Liebherr JК, Penev L (Eds) Systematic Zoology and Biodiversity Science: A tribute to Terry Erwin (1940-2020). ZooKeys 1044: 907-927. https://doi.org/10.3897/zookeys.1044.63803
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As woody plants provide much of the trophic basis for food webs in forests their species richness, but also stand age and numerous further variables such as vegetation structure, soil properties and elevation can shape assemblages of ground beetles (Coleoptera: Carabidae). However, the combined impact of these numerous variables on ground beetle diversity and community structure has rarely been studied simultaneously. Therefore, ground beetles were studied in 27 plots in a highly diverse and structurally heterogeneous subtropical forest ecosystem, the Gutianshan National Park (southeast China) using pitfall traps and flight interception traps. Both trapping methods collected partly overlapping species spectra. The arboreal fauna was dominated by lebiines and to a smaller extent by tiger beetles and platynines; the epigeic fauna comprised mostly representatives of the genus Carabus and numerous tribes, especially anisodactylines, pterostichines, and sphodrines. Ground beetle species richness, abundance, and biomass of the pitfall trap catches were analyzed with generalized linear mixed models (GLMMs), fitted with seven environmental variables. Four of these variables influenced the ground beetle assemblages: Canopy cover, herb cover, pH-value of the topsoil and elevation. Contrary to our expectations, woody plant species richness and stand age did not significantly affect ground beetle assemblages. Thus, ground beetles seem to respond differently to environmental variables than ants and spiders, two other predominantly predatory arthropod groups that were studied on the same plots in our study area and which showed distinct relationships with woody plant richness. Our results highlight the need to study a wider range of taxa to achieve a better understanding of how environmental changes affect species assemblages and their functioning in forest ecosystems.
Abundance, BEF-China, biomass, canopy cover, Carabidae, elevational gradient, herb cover, pH-value, species richness
Tropical and subtropical forests are among the world´s ecosystems with the highest biodiversity. A substantial part of this biodiversity consists of arthropods, which are involved in many ecosystem processes (
To analyze the effects of woody plant species richness on arthropod diversity in a real-world forest ecosystem, it is important to consider that environmental variables can also influence communities or assemblages of arthropods (
Ground beetles (Coleoptera: Carabidae) represent a highly diverse predatory taxon and are typical of forest ecosystems across latitudinal gradients (
The shaping variables of ground beetle assemblages in global biodiversity forest hotspots are poorly understood. In particular, the ground beetles of the southeast Chinese subtropics with summer rainfalls, which host particularly species-rich forests (
A study of ground beetles would reveal not only how this arthropod taxon responds to environmental variables, but the comparison with other important taxa (esp. spiders and ants) could provide a better understanding of how environmental variables affect the abundance and species diversity of predatory arthropods. Thus, since environmental variables can potentially influence ground beetle assemblages, we hypothesize that abundance, richness, and biomass of ground beetles increases with (H1) woody plant species richness and (H2) stand age in a subtropical forest in China. Moreover, we expect that (H3) the structural richness of vegetation and abiotic variables affect ground beetle abundance, richness, and biomass. Specifically, we investigate whether woody plant species richness, stand age of forests plots, structural richness of vegetation (cover of canopy and herb layer), and abiotic variables (elevation and soil pH) influence abundance, species richness, and biomass of ground beetles.
Gutianshan National Park (Gutianshan NP), formerly Gutianshan National Nature Reserve, is located in the western part of Zhejiang Province in southeast China (29°14'N, 118°07'E). The park is approximately 81 square kilometers in size and was established in 1975, first as a National Forest Reserve, to preserve parts of the old‐growth evergreen broad‐leaved forest in the region. The climate is typical for subtropical areas with an annual mean temperature of 15.3 °C and ~2000 mm mean precipitation per year, occurring mostly between March and September (
In 2008, 27 study plots, each measuring 30 m × 30 m, were established by a research consortium of Chinese and European scientists (
We sampled ground beetles using four pitfall traps in each plot, installed in the corners of the central 10 m × 10 m square (resulting in 108 traps). Traps were plastic cups with a diameter of 8.5 cm and a capacity of ~550 ml filled with 150 ml of preserving solution (40% ethanol, 20% glycerol, 10% acetic acid, 30% water). They were open continuously during the main vegetation period in 2009 (end of March to the beginning of September). Traps were emptied fortnightly (in total ten collections per trap) and catches were preserved in 70% ethanol until identification (
During plot establishment, a comprehensive set of environmental variables of biotic and abiotic habitat characteristics was collected (
All statistical analyses were conducted using the packages glmmTMB (
ln y = -8.92804283 + 2.5554921 ln x,
where: x is the measured body length of the specimen and y is the estimated body weight of the individual (
Model selection was based on likelihood-ratio tests starting with a fully saturated model that included all predictors and the interaction between woody species richness and stand age to test, if possible, species richness effects depended on the age of the forest plots. We sequentially removed non-significant (p > 0.05) terms and tested for assumptions of the best-fitting model following (
In total, we caught 258 ground beetle specimens in the pitfall traps, belonging to 22 species (Table
Collected ground beetles from pitfall traps of 27 plots in Gutianshan NP. For classification, we followed the systematics of the Palearctic catalogue (
Tribe | (Morpho-) Species | No. | Size (mm) | Elevation (m a.s.l.) |
---|---|---|---|---|
Anisodactylini | undet. spec. 1 | 60 | 8.9 | 348–903 |
undet. spec. 2 | 3 | 8 | 639 | |
Carabini | Carabus (Apotomopterus) davidis Deyrolle, 1878 | 5 | 35 | 566–679 |
Carabus (Isiocarabus) kiukiangensis Bates, 1888 | 20 | 30 | 348–903 | |
Carabus (Damaster) lafossei Feisthamel, 1845 | 5 | 42 | 566–679 | |
Brachinini | Pheropsophus (Stenaptinus) beckeri Jedlicka, 1930 | 1 | 14 | 647 |
Harpalini | Amara spec. 1 | 1 | 8 | 542 |
Harpalus spec. 1 | 1 | 12 | 617 | |
Lebiini | Calleida (Callidiula) spec. 1 | 1 | 12 | 617 |
Lachnoderma asperum Bates, 1883 | 1 | 8 | 880 | |
Pericalina, undet. 1 | 1 | 5 | 617 | |
Pentagonicini | Pentagonica spec. 1 | 10 | 4.5 | 251–679 |
Pentagonica spec. 2 | 1 | 5 | 542 | |
Perigonini | Perigona spec. 1 | 4 | 3 | 542–720 |
Pterostichini | Lesticus spec. 1 | 7 | 25.3 | 590–903 |
Lesticus spec. 2 | 43 | 28.1 | 251–903 | |
Pterostichus spec. 1 | 47 | 24.8 | 251–903 | |
Pterostichus spec. 2 | 3 | 11 | 419–670 | |
Sphodrini | Synuchus spec. 1 | 32 | 13.7 | 251–679 |
Synuchus spec. 2 | 10 | 10.9 | 251–903 | |
Cicindelini | Cylindera (Ifasina) kaleea Bates, 1863 | 1 | 9 | 880 |
Collyridini | Tricondyla macrodera Chaudoir, 1861 | 1 | 19 | 566 |
The number of ground beetle specimens in flight interception traps was lower than in pitfall traps. In total, we caught 49 individuals of six species (Table
Collected ground beetles from flight interception traps of 27 plots in Gutianshan NP. For classification, we followed
Tribe | (Morpho-) Species | No. | Size (mm) |
---|---|---|---|
Lebiini | Lachnoderma asperum Bates, 1883 | 1 | 8 |
Lioptera erotyloides Bates, 1883 | 1 | 13 | |
Coptodera (Coptoderina) spec. 1 | 42 | 7.5 | |
Pentagonicini | Pentagonica spec. 1 | 2 | 4.5 |
Platynini | undet. spec. 1 | 1 | 8 |
Collyridini | Tricondyla macrodera Chaudoir, 1861 | 2 | 19 |
Four of the seven environmental variables tested for effects on ground beetles in generalized linear mixed models were significantly related to the ground beetle assemblages. Canopy cover had a positive influence on species richness, abundance, and biomass of ground beetles (Table
Relationships between ground beetle abundance and canopy cover (A), herb cover (B) and pH-value of the soil (C). Black lines indicate significant relationships at p < 0.05 obtained from mixed-effects models (keeping other significant predictors fixed at their means) with grey areas indicating the 95% confidence intervals. Points represent observed values per trap. Note that some traps had similar abundance and predictor values. The fixed-effects explained 22% of the variation in ground beetle abundance.
Relationships between ground beetle species richness and canopy cover (A) and herb cover (B). Black lines indicate significant relationships at p < 0.05 obtained from mixed-effects models (keeping other significant predictors fixed at their means) with grey areas indicating the 95% confidence intervals. Points represent observed values per trap. Note that some traps had similar richness and predictor values. The fixed-effects explained 12% of the variation in ground beetle species richness.
Relationships between ground beetle biomass and canopy cover (A) and herb cover (B). Black lines indicate significant relationships at p < 0.05 obtained from mixed-effects models (keeping other significant predictors fixed at their means) with grey areas indicating the 95% confidence intervals. Points (slightly jittered to improve visibility) represent observed values per trap. The fixed-effects explained 30% of the variation in ground beetle biomass.
Results from mixed-effects models for ground beetle abundance, species richness, and biomass. P-values were obtained from likelihood-ratio tests starting with a full-saturated model and removing non-significant (p > 0.05) terms sequentially. Significant predictors (p < 0.05) are indicated in bold.
Abundance | Species richness | Biomass | ||||
---|---|---|---|---|---|---|
χ² | p-value | χ² | p-value | χ² | p-value | |
Woody species richness (WSR) | 0.07 | 0.787 | 0.04 | 0.849 | 1.44 | 0.230 |
Stand age | 0.33 | 0.565 | 0.00 | 0.961 | 1.17 | 0.280 |
Canopy cover | 4.28 | 0.039 | 3.90 | 0.048 | 4.98 | 0.026 |
Herb cover | 4.67 | 0.031 | 5.98 | 0.014 | 0.60 | 0.438 |
Herb species richness | 1.60 | 0.206 | 0.89 | 0.345 | 0.18 | 0.673 |
pH-value (topsoil) | 5.30 | 0.021 | 3.64 | 0.056 | 0.97 | 0.324 |
Elevation | 0.39 | 0.531 | 0.18 | 0.668 | 14.71 | <0.001 |
WSR * stand age | 0.01 | 0.941 | 0.19 | 0.664 | 2.41 | 0.120 |
Our study revealed that four environmental variables impacted on ground beetle assemblages at our sample sites. Contrary to our expectations, woody plant species richness (H1) and stand age (H2) did not influence ground beetle assemblages in this study. We did corroborate H3, as higher canopy cover led to increased species richness, abundance, and biomass of ground beetles, and because ground beetle abundance and species richness decreased with higher herb cover. Moreover, soil pH negatively influenced ground beetle abundance, and greater biomass of beetles was found at higher elevations.
Classical ecological theory such as the “enemies” hypothesis (
We found no relationship between woody plant species richness and species numbers, abundance, or biomass of ground beetles in Gutianshan NP. This result is consistent with those from numerous other studies on plants and arthropods, especially ground beetles (
The positive relationship between woody plant and ground beetle diversity found by
Greater closure of the canopy layer was associated with more beetle species and specimens. However, our results contrast findings from numerous studies in forests of boreal, temperate and Mediterranean climate zones, according to which the number of ground beetle species increases with decreasing canopy cover (
In contrast, herb cover had a negative influence on ground beetle abundance and species richness. Studies from forests in both temperate and Mediterranean climate regions have documented both negative and positive influences of the forest herb layer on the species richness of ground beetles (
The guild of predatory arthropods (Araneae, Chilopoda, Formicidae, cavity-nesting wasps and their parasitoids) in Gutianshan NP showed a significant decrease of both abundance and species richness with increasing elevation (
Our results for biomass indicate that beetle biomass within plots increases with elevation. This relationship is driven by the higher numbers of representatives of the genus Carabus (Fig.
Ground beetles are able to adapt to a wide range of varying pH-values (
The overall number of ground beetle specimens, species and biomass was relatively low in Gutianshan NP. Given the fact, that our study took place in a subtropical hotspot of vascular plant diversity, we expected higher numbers of ground beetles. For example, studies using the same sampling approach in Central European forests have reported 60 times more ground beetle specimens and 90 times more ground beetle biomass (
Pitfall trap catches for carabids seem to be low in most tropical evergreen forests (
Although only a few species were recorded in our flight interception traps, they represent guilds or taxonomic entities that are well known from the tropics (
The epigeic assemblages with their few species and individuals, but also the arboreal fauna with its specific morphological adaptations in Gutianshan NP resembles the ground beetle fauna typical for tropical forests. However, further study is required to achieve a better understanding of patterns of ground beetle species richness in subtropical forests.
We dedicate this work to the memory of the late Terry Erwin (1940–2020). He was one of the pioneers who studied how tree species diversity can affect the diversity of insects, especially ground beetles. One of his publications from a rainforest in Panama stimulated intensive research on tropical species diversity, particularly of arthropods. At the same time, Terry was one of the most dedicated entomologists we have ever met. His ecological work, as well as his contributions to natural history and conservation biology of carabids, has been very stimulating to our own studies. We are grateful for his influence and we will not forget him and his work.
We thank the administration of the Gutianshan National Park, and all BEF-China members for their support. We further thank Jiang Zaigen (Gutianshan) for help with trap maintenance, Marianne Peters (Leuphana University Lüneburg) for sorting trap catches, David D. Wrase (Gusow-Platkow), and Thierry Deuve (Natural History Museum Paris) for help with identification. We gratefully acknowledge funding by the German Research Foundation (DFG FOR891/1-3).
We also thank John Spence, Nigel Stork, and an anonymous reviewer for useful comments that helped improve this work.