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ABSTRACT Across many ecosystems, increases in species biodiversity generally results in greater resource acquisition by consumers. Few studies examining the impacts of consumer diversity on

resource capture have focused on terrestrial herbivores, however, especially taxa that feed belowground. Here we conducted field mesocosm experiments to examine the effects of variation in

species richness and composition within a community of wireworm herbivores on wheat plant productivity. Our experiments involved wireworm communities consisting of between one and three

species, with all possible combinations of species represented. We found that the presence of wireworms reduced plant biomass and seed viability, but wireworm species richness did not impact

these plant metrics. Species identity effects were strong, as two species, _Limonius californicus_ and _Selatosomus pruininus_, had significantly stronger impacts on plants compared to _L.

infuscatus_. Communities with either of the two most impactful species consistently had the greatest impact on wheat plants. The effects of wireworms were thus strongly dependent on the

particular species present rather than the overall diversity of the wireworm community. More broadly, our study supports the general finding that the identity of particular consumer species

within communities often has greater impacts on ecosystem functioning than species richness. SIMILAR CONTENT BEING VIEWED BY OTHERS TREE PHYTOCHEMICAL DIVERSITY AND HERBIVORY ARE HIGHER IN

THE TROPICS Article 27 June 2024 GLOBALLY CONSISTENT RESPONSE OF PLANT MICROBIOME DIVERSITY ACROSS HOSTS AND CONTINENTS TO SOIL NUTRIENTS AND HERBIVORES Article Open access 14 June 2023

EXOTIC PLANTS ACCUMULATE AND SHARE HERBIVORES YET DOMINATE COMMUNITIES VIA RAPID GROWTH Article Open access 11 May 2021 INTRODUCTION Across a diverse array of ecosystems, greater consumer

species richness generally increases the consumption of shared resources1,2,3,4,5. This positive relationship between biodiversity and resource capture is often attributed to one of two

mechanisms, species complementarity or species identity effects4,5,6,7. Species complementarity occurs when consumer species feed on unique resources in space or time, such that more diverse

communities consume more resources by feeding across diverse niches4,5,6,7. Species identity effects or ‘sampling effects’, in contrast, arise when more species-rich communities are more

likely to contain highly impactful (i.e., species that consume significantly more resources than an average species) species by chance alone, resulting in greater resource

consumption4,5,6,7. One approach to demonstrate complementarity among consumer species is to explore the niche breadth of each species and identify unique niches available to each8; if

species occupy distinct niches, complementarity can occur8. Another approach is to directly manipulate niche complementarity among consumers, and experimentally determine if greater

complementarity promotes resource consumption9,10. Both of these approaches, however, require complex experimental designs that are often not practical for many systems. A more common

approach is to compare resource consumption in diverse consumer communities with that of the single most impactful species6,7. With this approach, if the diverse consumer community

significantly depletes resource levels below that of the most impactful species, complementarity is inferred6,7, but if not then identity effects are inferred. While empirical studies of

consumer diversity and resource consumption have identified both species complementarity and identity effects1,2,3,4,5, meta-analyses have shown that species identity effects are more

prevalent1. To date, however, studies on the consumer diversity-resource consumption relationship have focused almost exclusively on predator-prey or aquatic systems1. Few studies have

focused on interactions between herbivore diversity and plant productivity in terrestrial ecosystems. Thus, whether patterns of diversity strengthening resource consumption seen in

predator-prey1,2,3,4,5,6,7,8,9,10,11,12 and aquatic13,14,15,16 systems, and the underlying mechanisms, hold for terrestrial herbivore-plant systems remains largely unknown. Here we

investigated the relationship between herbivore diversity and plant productivity in a system consisting of wireworms and wheat plants. Wireworms, the larvae of click beetles (Coleoptera:

Elateridae), are a group of generalist herbivores that feed voraciously belowground on the seeds, roots, and stems of wild and cultivated plants. Wireworms cause significant economic damage

to crops and natural systems across a wide range of climates17,18,19,20. In wheat cropping systems of the Pacific Northwestern United States, wireworms have become the most economically

damaging insect pest18,19. The distribution of wireworm species, and the composition of wireworm communities, varies considerably across regions based on environmental conditions and crop

type17,18. In agricultural ecosystems, for example, many fields often contain a single wireworm species, while others in the same region contain a diverse mixture of species (although the

mechanisms driving this variability remain largely unknown)18. However, despite this variability, the impact of variation in wireworm species diversity and identity on plants remains

virtually unknown, although there is reason to expect that this variability is biologically important. For example, wireworm species can differ greatly in their feeding ecology17,19,20.

Different species can feed at varying depths within the soil profile18, which might lead to spatial niche partitioning between species. Moreover, different species vary in their seasonal

activity patterns17,19,20, which might promote temporal niche partitioning among species. Thus, we hypothesized that greater wireworm diversity might increase plant resource consumption

through spatial and/or temporal niche partitioning. We conducted a field mesocosm experiment to test whether the diversity and composition of wireworm communities mediated their impacts on

wheat plant productivity. Our experiments involved the three most common species in agricultural fields of Washington State, USA; these species accounted for nearly 90% of wireworms

collected in regional surveys of 160 fields throughout the Pacific Northwest18. These three species are responsible for inflicting significant economic damage to cereal crops in the Pacific

Northwest, with up to 70% yield losses in highly infested fields18. We tested whether the impacts of the three wireworm species on wheat plants differed when they were present singly or in

diverse communities. By using a substitutive experimental design we also isolated and measured wireworm identity and diversity effects. Our results shed light on the effects of belowground

herbivore diversity and species identity on plant productivity. RESULTS EFFECTS OF HERBIVORE PRESENCE AND DIVERSITY ON WHEAT PRODUCTIVITY We conducted a field mesocosm experiment to

determine the impacts of wireworm species richness and identity on wheat plant productivity. The presence of wireworms significantly reduced plant biomass both above- and belowground (Fig.

1A,B; Table 1). Seed viability was also significantly reduced when wireworms were present (Fig. 2A; Table 1). Other metrics of plant productivity (the number of produced seed heads, grain

weight) were not significantly impacted by the presence of wireworms (Figs 1 and 2; Table 1). While the presence of wireworms strongly impacted plant productivity, wireworm species richness

did not significantly impact aboveground (Fig. 1A; Table 1) or root biomass (Fig. 1B; Table 1). Seed viability, however, was significantly reduced when wireworms were present as single

species compared to within diverse communities (Fig. 2A; Table 1). The number of produced seed heads and grain weight were not significantly impacted by wireworm species richness (Figs 1 and

2; Table 1). EXAMINING EFFECTS OF WIREWORM SPECIES IDENTITY AND COMPLEMENTARITY We compared the impacts of single wireworm species to diverse communities on wheat plants to determine if

variation across our treatments was due to species identity or complementarity effects. We found no significant differences between observed plant productivity in diverse communities and the

expected productivity based on the averages of each wireworm species present singly (Table 2). This provides further evidence that wireworm diversity did not impact plant productivity.

However, we found that two wireworm species, _L. californicus_ and _S. pruininus_, had significantly greater negative impacts on plant productivity when present alone or in a two-species

community with only these two species, compared to other wireworm compositions (Table 2, Figs 3, 4, 5 and 6). We observed significant species identity effects for above- and belowground

biomass, the number of produced seed heads, seed viability, and grain weight (Table 2). For each of these metrics, _L. infuscatus_ was the least impactful species, while _L. californicus_

and _S. pruininus_ were significantly more impactful when present alone or in a two-species community without _L. infuscatus_ (Figs 3, 4, 5 and 6). Two-species communities with _L.

infuscatus_ and either _L. californicus_ or _S. pruininus_ consistently had significantly lower impacts than communities with _L. californicus_ and _S. pruininus_ (Figs 3, 4, 5 and 6).

DISCUSSION Over the past several decades a considerable amount of empirical research has focused on the effects of species diversity on ecosystem functioning1,2,3,4,5. Studies investigating

consumer diversity and resource capture have generally demonstrated strong positive impacts of diversity, although more evidence exists for species identity effects than complementarity as

the primary underlying mechanism1. For example, numerous multi-predator studies have found that greater predator diversity enhances the suppression of prey resources because the most

voracious predators are more likely to be present in diverse compared with simple communities1,4,21. The biodiversity of aquatic herbivores has also been shown to generally promote

consumption of plant tissue due to strong identity effects13,14,15,16. However, to date few studies have examined effects of the diversity of terrestrial consumer communities on plant

consumption. Our results show that the identity of herbivorous wireworm species mediated impacts on wheat productivity. Wireworms were impactful herbivores in our experiments, reducing plant

biomass and reproductive capacity. These direct impacts on yield observed here might be further magnified in the field situations, as plants with less developed root systems are more

susceptible to lodging22, an indirect effect of wireworm feeding. However, we did not find that wireworm diversity increased the depletion of wheat plant resources. Rather, two impactful

wireworm species, _L. californicus_ and _S. pruininus,_ caused greater deleterious effects on wheat productivity compared to diverse communities or a third species, _L. infuscatus_.

Moreover, two-species communities containing both _L. californicus_ and _S. pruininus_ exerted stronger deleterious effects on multiple plant productivity metrics than other diverse

communities that included _L. infuscatus_. The initial abundance of _L. californicus_ and _S. pruininus_ was lower in the two- or three-species communities containing _L. infuscatus_ due to

our substitutive design, which may have in turn weakened impacts on plants. Previous work shows that the distribution of wireworm species, and the composition of wireworm communities,

differs considerably across agroecosystems of the Pacific Northwestern United States based on environmental variation18,19. Although little is known about the feeding ecology of _S.

pruininus_, _L. californicus_ and _L. infuscatus_ differ significantly in their feeding modes19. _Limonius infuscatus_ actively feeds on wheat plants primarily from seeding (typically April

or May) through the month of June, after which it declines in activity (although some feeding occurs throughout the season), whereas _L. californicus_ larvae remain highly active for the

entire season, from seeding through harvest (typically August or September)19. We thus expected that temporal niche partitioning between different wireworm species might lead to stronger

impacts on plants when wireworms were present in diverse communities. Different wireworm species also can feed at varying depths within the soil profile19, which could promote spatial niche

partitioning when wireworms were present in diverse communities. However, we found that the biodiversity of wireworm communities did not increase depletion of wheat plant resources in our

mesocosms. It is possible that the nature of our mesocosms, which contained only a single plant species as resource, obscured potential complementarity between wireworm species. Previous

work in predator-prey systems, for example, has shown that the diversity of the resource base can have considerable impacts on the biodiversity-ecosystem functioning relationship. In a

system with predators feeding on aphids on collard plants, for example, coccinellid beetles forage on leaf edges while parasitoid wasps forage on leaf centers, leading to spatial

complementarity and a positive relationship between predator diversity and aphid consumption10. However, when caterpillars are introduced to the system this complementarity is reduced

because caterpillars chew holes in leaf centers (creating edges for coccinellids), and species identity effects become prevalent due to increased niche overlap between predators10.

Similarly, Finke and Snyder9 demonstrated positive effects of consumer complementarity on resource consumption only when the resource base was diverse. In that study, the authors took

advantage of host fidelity between parasitoid wasps and aphids, which allowed them to independently manipulate predator niche breadth (generalists vs. specialists) and resource (aphid)

diversity. They found that resource exploitation increased only with greater diversity of specialist parasitoids when different species consumed different aphid species, demonstrating strong

complementary effects9. Conversely, our study manifested a high degree of niche overlap due to the presence of a single plant resource, potentially diminishing the ability of wireworms to

partition resources. However, further research should be carried out in order to verify such hypothesis. Our results support large-scale field trials showing that _L. californicus_ is a more

damaging species for commercial wheat producers in the Pacific Northwestern United States than _L. infuscatus_23. _Limonius californicus_ feeds actively throughout the season, while _L.

infuscatus_ is limited in activity to early months, which could contribute to the greater damage potential of _L. californicus_ over the course of an entire growing season. _L. californicus_

is also less impacted by seed-applied insecticides than _L. infuscatus_19,23, which can lead to greater damage caused by _L. californicus._ It remains unclear, however, whether _S.

pruininus_ causes more or less damage to commercial wheat crops than the two _Limonius_ species. This is because the _Limonius spp._ were believed to be the primary economically important

species in the Pacific Northwest23, and thus research to date focused primarily on these species. Only recently, when large-scale surveys were performed throughout this region, was _S.

pruininus_ discovered in high abundance18; however, detailed studies of the economic significance of this pest have yet to be performed and were one motivating reason for this study.

However, the spatial distribution of wireworm species tends to remain fairly consistent within fields over multiple seasons18. Sampling can thus provide producers with a reliable indicator

of which species to expect in order to guide management. While our results suggest that _L. californicus_ and _S. pruininus_ likely require more aggressive management than _L. infuscatus_,

our experiments were conducted at a single level of wireworm abundance. Variation in wireworm abundance, in conjunction with the species present, would likely ultimately dictate the most

successful management strategy. Indeed, studies of consumer diversity and resource consumption have shown that abundance may mediate the impacts of biodiversity8. When abundance of consumers

is low, competition is relaxed and the impacts of diversity might be marginalized because there may be enough resources available even for species competing in the same niche. However, when

consumer density is high, resource competition intensifies and only species that occupy distinct niches will contribute additively to resource consumption (i.e., a positive effect of

biodiversity can occur)8. It is possible that at higher wireworm densities we would have observed stronger diversity effects than were observed here. Future work should attempt to determine

how field-level variation in wireworm abundance, diversity, and species composition mediate the productivity of wheat and other commercial crops. Our results are in line with the broader

literature on relationships between consumer biodiversity and resource acquisition which shows that the identity of herbivores is critical for plant performance and abundance1. Herbivorous

wireworms likely pose greater threats to wheat production when communities consist of a single dominant consumer species (_L. californicus_ or _S. pruininus_) or the right mixture of species

(e.g., _L. californicus_ and _S. pruininus_) rather than a complex of multiple species or a less impactful species (_L. infuscatus_). More studies of terrestrial herbivores would be

beneficial to place our research in a broader context, but such studies are still under-represented in the literature1. Further examining the relationship between herbivore diversity and

plant productivity in natural and managed ecosystems would provide considerable benefits for our understanding of the functioning of terrestrial ecosystems and for the development of

integrated pest management strategies. METHODS EXPERIMENTAL SETUP We conducted a field mesocosm experiment to evaluate the impacts of three wireworm species, _L. infuscatus_, _L.

californicus_, and _Selatosomus pruininus_ on wheat plants, _Triticum aestivum_. Wheat is a predominant crop grown in the Pacific Northwestern United States and a highly suitable host for

wireworms18,19,23. The experiment was conducted at the Washington State University Tukey Orchard in Pullman, Washington, USA. Experimental units were plastic containers (60 cm long, 45 cm

wide, 40 cm deep) with small drainage holes (0.3 mm in diameter) drilled in the bottom to allow water drainage. These holes are small enough that they prevented the escape of wireworms.

Cages were installed in the ground, leveling the top of the container with the soil surface, and filled with previously excavated soil. Wheat seeds (variety Louise) used in the experiments

were commercially purchased. All plants were sown in growth chambers for 7d (Feekes’ growth stage 1) with a 16:8 h light:dark period at a light intensity of 600 μE m−2 s−1 and a temperature

regime of 20:18 °C (light:dark)24,25. They were then transplanted to the field mesocosms on May 7th, 2014 and allowed 3d to acclimate before wireworms were added. Each container received 10

wheat plants (2 rows of 5 plants) with in-row and between-row spacing of 8 and 20 cm, respectively. Plants were watered every 2 to 3d throughout the experiment. After wheat plants had

acclimated, we added wireworms to cages with the the following treatments that varied in species richness and composition: (1) control (six replicates without wireworms), (2) one wireworm

species (six replicates of each of the three species present alone), (3) two wireworm species (six replicates of each of the three unique species pairs), and (4) three wireworm species

(twelve replicates with all three wireworm species). We thus fully replicated all possible combinations of species composition and diversity from our community of three species. Wireworms

used in our experiments were field collected within 2 wk of the initiation of the experiments using bait traps18 and identified to species26,27. Larvae were collected from fallowed field sat

Washington State University Wilke Research and Extension Farm, Davenport, WA and Washington State University Lind Dryland Research Station, Lind, WA. All wireworms were housed without food

for 10d before introducing them to field mesocosms. Twelve randomly chosen large larvae (> = 9 mm in size) were assigned to each experimental mesocosms; this density is within the normal

range observed in fields reporting yield loss from wireworms19. Single-species treatments received 12 individuals of a single species, two-species treatments received 6 individuals of each

of the two wireworm species, and three-species treatments included 4 individuals of each of the three wireworm species. This substitutive design allowed us to vary species composition and

diversity with the same overall abundance in each mesocosm. Each experimental unit was maintained until the wheat was mature and ready to harvest. DATA COLLECTION Plants were harvested on

September 27th 2014 and the following five measures of plant productivity were measured: (1) aboveground dry weight (shoot dry weight), (2) belowground dry weight (root dry weight), (3) the

number of produced seed heads, (4) seed viability, and (5) grain weight. All plants were first harvested at the base near the soil. The aboveground matter was collected and the number of

produced seed heads was counted. The samples were then dried in an oven at 100 °C for 48 h and weighed. To calculate grain weight, all seeds from each plant were weighed28. Ten randomly

selected seeds were then germinated on blotter paper, moistened with tap water, and placed in a growth chamber at 20 °C for 7d, after which seed viability (% germination) was assessed in

accordance with procedures developed by the Association of Official Seed Analysts (AOSA)29. Only viable seedlings were counted30. To record root-biomass, we extracted root cores from the

soil by sifting all the soil out of each mesocosm and washing the residual soil off with water. All roots were then air-dried for 2 h and sorted between paper towels for accurate biomass

determination. Prepared samples were oven-dried at 100 °C for 48 h and then weighed. DATA ANALYSES We first analyzed the effect of wireworm presence on plant productivity using

non-parametric Wilcoxon rank-sum tests due to non-normality in the response variables. In these analyses wireworm presence (present or absent) was our explanatory variable and each metric of

plant productivity (except seed viability) was analyzed separately as a response. This allowed us to determine whether wireworms impacted plant productivity across all levels of composition

and diversity. We then used non-parametric Kruskal-Wallis tests31, followed by posthoc Dunn’s tests, to assess whether wireworm richness (1, 2, or 3 species) impacted each plant

productivity metric except seed viability. To analyze impacts of wireworm presence and biodiversity on seed viability we used logistic regression models, where seed germination (yes or no)

was the binary response. For all of these analyses, when the overall model was significant, comparisons of treatment means were performed using posthoc pairwise likelihood ratio contrasts.

These analyses were conducted in JMP32. To assess whether species complementarity or species identity effects were predominant, for each unique diverse assemblage _j_ we measured

non-transgressive (_D__T_) and transgressive (_D__max_) over-yielding as follows7: where _O__j_ is the observed plant productivity in the diverse community _j_, _E__j_ is the expected plant

productivity of the diverse community _j_ (the average productivity across all species in the community), and _M_ is the plant productivity in the monoculture that had the most impactful

species (in our case the wireworm species that caused the most damage to wheat). Separate analyses were conducted for each metric of plant productivity. Non-transgressive overyielding

indicates that plant productivity observed in a diverse wireworm community differed from the average productivity when these species were present singly; _D__T_ thus indicates the net impact

of diversity7. If _D__T_ values are significantly below 0, it indicates that diverse wireworm communities reduced plant productivity more than species present alone; _D__T_ values greater

than 0 would indicate that diverse communities had significantly lower impact on plant productivity than single wireworm species. Transgressive overyielding, _D__max_, occurs when the

effects of a diverse community exceeds that of the most impactful species. In this case, if _D__max_ values are significantly below 0, it indicates that diverse wireworm communities reduced

plant productivity more than the single most impactful species present alone (i.e., transgressive overyielding occurs); _D__max_ values significantly greater than 0 would indicate that the

single most impactful species had greater impacts on plant productivity than a diverse community (i.e., species identity effects predominate). If both _D__T_ are _D__max_ are significantly

negative, it would indicate a positive effect of diversity driven by species complementarity. If _D__T_ is significantly negative but _D__max_ is insignificant, it would indicate a positive

effect of diversity driven by a species identity effect. In contrast, if _D__max_ is significantly positive but _D__T_ is not significant, it would indicate that species identity effects

mediated impacts of wireworms on plant productivity (such that the single most impactful species exerted stronger detrimental effects on plant community than the diverse community) but that

diversity itself was not significant. We calculated _D__T_ and _D__max_ for each plant productivity metric (including seed viability which was treated as a percentage). We then used

one-sample _t_-tests to assess whether the distribution of these values calculated across all of the unique two- and three-species communities differed significantly from 0. This analysis

allowed us to detect if overyielding occurred, and whether species identity played a dominant role in wireworm communities. These analyses were conducted in JMP32. ADDITIONAL INFORMATION HOW

TO CITE THIS ARTICLE: Milosavljević, I. _et al_. The identity of belowground herbivores, not herbivore diversity, mediates impacts on plant productivity. _Sci. Rep._ 6, 39629; doi:

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ACKNOWLEDGEMENTS We thank Kayla Fillion, Jacob Cohen, Laura Rafferty, Isabel Brofsky, Derek Appel, Deb Pehrson, and Cameron Burt for technical assistance. Special thanks go to Arron H.

Carter and Walter S. Sheppard for their comments on the manuscript. This project was supported by grants from the Washington Grain Commission and the USDA NIFA, award 2016-70006-25829, to DC

and AE. AUTHOR INFORMATION AUTHORS AND AFFILIATIONS * Washington State University Entomology, 166 FSHN Bldg, Pullman, 99164, WA, USA Ivan Milosavljević & David W. Crowder * Washington

State University Extension, 205 W Main, Ritzville, 99169, WA, USA Aaron D. Esser * Department of Plant, Soil and Entomological Sciences, University of Idaho, 875 Perimeter Drive, Moscow,

83844-2339, ID, USA Nilsa A. Bosque-Pérez Authors * Ivan Milosavljević View author publications You can also search for this author inPubMed Google Scholar * Aaron D. Esser View author

publications You can also search for this author inPubMed Google Scholar * Nilsa A. Bosque-Pérez View author publications You can also search for this author inPubMed Google Scholar * David

W. Crowder View author publications You can also search for this author inPubMed Google Scholar CONTRIBUTIONS I.M., A.E., N.B.P., and D.C. designed the research. I.M. and A.E. conducted the

experiments. I.M. and D.C. analyzed the data. I.M. wrote the manuscript with edits from A.E., N.B.P., and D.C. ETHICS DECLARATIONS COMPETING INTERESTS The authors declare no competing

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ARTICLE CITE THIS ARTICLE Milosavljević, I., Esser, A., Bosque-Pérez, N. _et al._ The identity of belowground herbivores, not herbivore diversity, mediates impacts on plant productivity.

_Sci Rep_ 6, 39629 (2016). https://doi.org/10.1038/srep39629 Download citation * Received: 18 May 2016 * Accepted: 25 November 2016 * Published: 22 December 2016 * DOI:

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