Figures
Abstract
Aphidophagous coccinellids (ladybeetles) are important providers of herbivore suppression ecosystem services. In the last 30 years, the invasion of exotic coccinellid species, coupled with observed declines in native species, has led to considerable interest in the community dynamics and ecosystem function of this guild. Here we examined a 24-year dataset of coccinellid communities in nine habitats in southwestern Michigan for changes in community function in response to invasion. Specifically we analyzed their temporal population dynamics and species diversity, and we modeled the community’s potential to suppress pests. Abundance of coccinellids varied widely between 1989 and 2012 and became increasingly exotic-dominated. More than 71% of 57,813 adult coccinellids captured over the 24-year study were exotic species. Shannon diversity increased slightly over time, but herbivore suppression potential of the community remained roughly constant over the course of the study. However, both Shannon diversity and herbivore suppression potential due to native species declined over time in all habitats. The relationship between Shannon diversity and herbivore suppression potential varied with habitat type: a positive relationship in forest and perennial habitats, but was uncorrelated in annual habitats. This trend may have been because annual habitats were dominated by a few, highly voracious exotic species. Our results indicated that although the composition of the coccinellid community in southwestern Michigan has changed dramatically in the past several decades, its function has remained relatively unchanged in both agricultural and natural habitats. While this is encouraging from the perspective of pest management, it should be noted that losses of one of the dominant exotic coccinellids could result in a rapid decline in pest suppression services if the remaining community is unable to respond.
Citation: Bahlai CA, Colunga-Garcia M, Gage SH, Landis DA (2013) Long-Term Functional Dynamics of an Aphidophagous Coccinellid Community Remain Unchanged despite Repeated Invasions. PLoS ONE 8(12): e83407. https://doi.org/10.1371/journal.pone.0083407
Editor: Martin Heil, Centro de Investigación y de Estudios Avanzados, Mexico
Received: September 17, 2013; Accepted: November 8, 2013; Published: December 13, 2013
Copyright: © 2013 Bahlai et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: This work was funded by grant #1027253 from the National Science Foundation's Long Term Ecological Research program. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors have declared that no competing interests exist.
Introduction
Aphidophagous coccinellids (ladybeetles, order Coleoptera) are a well-studied group of insects [1,2]. Coccinellids are economically important for their ability to suppress pest herbivores, and their ubiquity and charismatic appearance has led to public interest in their conservation [1]. Over the last 30 years the addition of multiple exotic species to the North American coccinellid community, coupled with observed declines in native species, has led to renewed interest in the ecosystem function of this guild [2].
Aphidophagous coccinellids have been under systemic surveillance at the Long Term Ecological Research (LTER) site at Kellogg Biological Station since 1989. This community has been invaded four times in the last 28 years. Coccinella septempunctata, a European species [3], arrived in 1985; Harmonia axyridis, an Asian species [4], was first detected in 1994; Hippodamia variegata, a Eurasian species [5], was first captured in 1999; and Propylea quatuordecimpunctata, a European species [6], has been in the region since 2007.
Prior studies have shown that coexisting coccinellid species partition habitat use in space and time and thus function complimentarily [7]. This allows for more effective resource partitioning and less direct competition between predators [8]. Thus, in a situation with limited competition between native and exotic species, herbivore suppression services offered by a coccinellid community are expected to increase with biodiversity, that is, the addition of exotics may improve herbivore suppression services, provided native species are not extirpated. Moreover, exotic species would be expected to have negligible effect on the diversity of a community if the exotic species effectively replaced a native species with respect to its level of dominance. However, exotic species which are able to outcompete native species are not necessarily superior biological control agents [9,10]. Superior competitors may instead out-compete native species by interfering with the ability of the native species to acquire resources [11]. It has not yet been demonstrated how exotic species affect ecosystem services provided by the coccinellid community (i.e. aphidophagy), over the long term [2], although several studies have documented declines in particular aphid populations in the short term following the establishment of exotic coccinellids [12-14]. From a theoretical perspective, it is expected that exotic species that use resources differently or have greater phylogenetic distinctiveness would have larger impacts on ecosystem functions [15,16], and thus, in the case of coccinellid invasions in landscapes that are already well exploited by native coccinellids, the impact on community function would be expected to be minimal.
In order to estimate the changes in the ability of the coccinellid community to suppress herbivores before and after invasion, a reliable metric must be used. Bahlai et al. [17] developed the natural enemy unit (NEU), a metric for quantifying the herbivore suppression potential of a resident natural enemy community based on the voracity and abundance of individual species. This metric provides a tool to estimate the predation capacity of the coccinellid community, with the assumption that competitive interactions do not reduce the overall voracity. Thus, this metric allows herbivore suppression potential (i.e.: the maximum number of prey items a resident natural enemy guild is capable of consuming, under ideal conditions) to be evaluated relative to ecosystem characteristics such as biodiversity, and disturbances like invasions. Although competitive interactions between natural enemies are not explicitly considered by this metric, a model using NEUs to represent the herbivore suppression of diverse natural enemy guild corresponded well to field-observed aphid suppression when it was assumed the herbivore suppression potential was the upper asymptote of a type III functional response [18]. Thus, the metric provides the most realistic estimation of realized herbivore suppression by coccinellids in prey-rich environments.
While numerous prior studies have examined aphidophagous coccinellid communities in North America [2,7,12,13,19-29], almost all of the comprehensive, systemic multiyear studies focus on a single crop; predominantly on cultivated herbaceous host habitats [2]. In contrast, our study documented the coccinellid community in southern Michigan from 1989 to 2012 in nine habitats, representing not only one of the longest durations of continuous coccinellid surveillance, but also presents the most diverse set of habitats monitored in a single study. These data also represent a rare case where detailed observations were taken before, during and after the invasion of several species using a standard protocol [11]. In the present paper, we examine herbivore suppression and diversity function in these invaded coccinellid communities over 24 years.
Methods
Description of study site and classification of habitats
All studies occurred at Michigan State University’s Kellogg Biological Station (KBS) in southwestern Michigan (42°24’N, 85°24’W) at 288 m elevation. Coccinellid surveillance data were collected starting in 1989 at the KBS Long Term Ecological Research (LTER) site as part of the Main Cropping System Experiment (MCSE) and forest sites. See http://lter.kbs.msu.edu/research/long-term-experiments/main-cropping-system-experiment/ and http://lter.kbs.msu.edu/research/long-term-experiments/successional-and-forest-sites/ for a detailed experimental design. The MCSE consists of seven treatments including treatments of annual field crops (maize, soybeans and wheat) in annual rotation under 4 levels of management intensity (conventional, no-till, reduced input, and biologically based), as well as alfalfa, poplar and early successional vegetation (i.e. abandoned agricultural fields). Each treatment is replicated six times with individual plot sizes of 1 ha. Observations are taken from five permanent sampling stations within each treatment-replicate combination. Instead of grouping by management intensity for this analysis, coccinellid abundance data from the MCSE were grouped by the particular host crop planted in that treatment-replicate combination in a given observation-year combination. Forest sampling began in 1993, at sites within 3 km of the MCSE on the KBS. Forest types included: 40-60 year old conifer forest plantations, late successional deciduous forest, and successional forests occurring on abandoned agricultural land. Three 1 ha replicates of each forest type are monitored at five sampling stations, as in the MCSE. The LTER experiment continues to date. Detailed agronomic records for the site are available at http://lter.kbs.msu.edu/datatables/150. Coccinellid abundance data is available online at http://lter.kbs.msu.edu/datatables/67. A relational database in MS Access® integrating coccinellid data with the relevant environmental and agronomic records used in this analysis is available from the authors by request.
To monitor coccinellids, un-baited two-sided yellow cardboard sticky cards (Pherocon, Zoecon, Palo Alto CA) are suspended at 1.2 m above ground at each sampling station [29]. Each week, coccinellids on the sticky cards are identified using a pictorial key, counted, recorded, and then removed from sticky cards. Sticky cards are replaced every two weeks. The length of the sampling period within the growing season averaged 14 weeks (with a standard error of one week, and minimum and a maximum of 8 and 22 weeks respectively). Variation depended on the availability of labor, crop type, and weather.
For analyses and data presentation, individual habitats (i.e. dominant plant community occurring in a treatment block) were grouped into three habitat types: annual crops, perennial crops, and forest habitats. Annual crops were all dominated by annual herbaceous plants, grown in near monoculture, and included maize, wheat, and soybeans. Habitats classed as perennial crops included poplar, alfalfa, and managed early successional. Managed early successional habitats were included in this group because, although this community is not a crop per se, it is a community resulting from abandoned crop land, occurring within a crop matrix, and managed to maintain their early successional stage (e.g., yearly spring burnings). Finally, forest habitats included coniferous, deciduous, and successional forest.
Coccinellid abundance data
The relative abundance of 13 species of aphidophagous coccinellids (Table 1) as measured by sticky trap capture of adults was used in the analysis. Species were included if they were recorded in the surveys, and had been recorded in the literature as consuming aphids. The majority of coccinellids recorded are primarily aphidophagous, but Coleomegilla maculata, an omnivorous species that also feeds on pollen [30], and Chilocorus stigma, a scale specialist that incidentally feeds on aphids [31], were included in the analysis. Two other coccinellids, Brachiacantha ursina, and Psyllobora vigintimaculata, are only known to eat scale insects and fungi, respectively [32], and were excluded from the analysis.
Species | Common name | Origin* | % total capture | Notes |
---|---|---|---|---|
Adalia bipunctata | Two-spotted | Native | <1 | |
Coccinella septempunctata | Seven-spotted | Exotic | 41 | First observed at site in 1985, prior to initiation of study |
Coleomegilla maculata | Pink or Spotted | Native | 19 | |
Chilocorus stigma | Twice-stabbed | Native | 1 | |
Coccinella trifasciata | Three-banded | Native | <1 | |
Cycloneda munda | Polished | Native | 4 | Sometimes recorded as Cycloneda sp., C. munda is the only species in this genus known from this locality |
Hippodamia tredecimpuncta | Thirteen-spotted | Native | <1 | Last observed at site in 2002 |
Harmonia axyridis | Multicolored Asian or Harlequin | Exotic | 28 | First trapped in 1994 |
Hippodamia convergens | Convergent | Native | <1 | |
Hippodamia glacialis | Glacial | Native | <1 | First trapped in 1994 |
Hippodamia parenthesis | Parenthesis | Native | 2 | |
Hippodamia variegata | Variegated | Exotic | 1 | First trapped in 1999 |
Propylea quatuor-decimpunctata | Fourteen-spotted | Exotic | 1 | First trapped in 2007 |
Data were examined at two different temporal resolutions to gain insight into both real-time interactions and between season trends. First, the sum of all captures from each sampling station in a given week, in a given treatment by replicate combination, was called ‘weekly average,’ and the sum of all captures in a given treatment over a calendar year, was referred to as ‘yearly total.’ Data were further subdivided into sets of ‘all coccinellids’ and ‘native species only’ to detect differences in diversity and function of native coccinellids compared to the community as a whole. To aide in data visualization, a Gaussian smoother with a span of 3 units was used to produce smoothing curves. To reduce the likelihood of erroneous conclusions from a large dataset with numerous sources of variation, α=0.01 was observed for all analyses.
Diversity analysis
The Shannon Index (Shannon’s H) was used to examine trends in diversity of the coccinellid community at the site over time [33]. A Shannon Index was computed for the species distribution at each observation and then this value was used as the dependent variable in several analyses examining the Shannon Index by each habitat type. One way ANOVA or, if data did not meet assumptions of ANOVA, Kruskal-Wallis one way analysis of variance on ranks were performed using SigmaPlot 11.0.0.75 For Windows (Systat Software Inc.) for Shannon Index by habitat for both datasets. Weighted least square regressions were conducted in R 2.15.3 [34] to detect linear trends in Shannon Indices over the observation period. Regressed data points were weighted by number of traps reporting in a given replicate-week combination, or yearly total number of traps in a habitat, for weekly and yearly datasets, respectively.
Herbivore suppression potential model
The herbivore suppression potential of the observed community was modeled by weighting each species by its relative voracity, after Bahlai et al. [17]. Herbivore suppression potential is computed in natural enemy units (NEU), where 1 NEU is the number of predators or parasitoids required to kill 100 of a particular pest insect in 24h. Thus,
for N species, where ni is number of individuals of species i, and Vi is the voracity of species i, expressed as the number of target prey (in this case, aphids) consumed in 24h, divided by 100.
Voracity of adult coccinellids
To estimate the voracity of each coccinellid species, literature values of average aphid consumption rates were used. If a study reported aphid consumption rates for each sex for a given species, a 1:1 sex ratio was assumed and the average of the consumption rates are reported. Where multiple sources were available, the highest estimate of voracity was used, except when the highest estimate was dramatically higher than all other published values; then the top two estimates were averaged. The voracity values used to estimate herbivore suppression potential for all aphidophagous coccinellids examined in this study (obtained from the literature) are provided in Table 2.
Coccinellid Species | Prey Species | Voracity (Vi) | Reference |
---|---|---|---|
Adalia bipunctata | Myzus persicae | 0.172 | Ellingsen [50] |
Coccinella septempunctata | Aphis glycines (82.5), Diuraphis noxia (43.1) | 0.628 | Xue et al. [51], Michels and Flanders [52] |
Coleomegilla maculata | “prey”, including aphids and mites | 0.350 | Lucas et al. [53] |
Chilocorus stigma | Incidental feeding on aphids, scale specialist | ~0.000 | Muma [31] |
Coccinella trifasciata | Acyrthosiphon pisum | 0.320 | Yadava and Shaw [54]* |
Cycloneda munda | Toxoptera citricida | 0.384 | Morales and Burandt [55]** |
Hippodamia tredecimpunctata | Diuraphis noxia | 0.189 | Michels and Flanders [52]*** |
Harmonia axyridis | Aphis glycines (88.5), Myzus persicae (45.8) | 0.672 | Xue et al. [51], Soares et al. [56] |
Hippodamia convergens | Acyrthosiphon pisum | 0.440 | Yadava and Shaw [54]* |
Hippodamia glacialis | Acyrthosiphon pisum | 0.440 | Yadava and Shaw [54]*, **** |
Hippodamia parenthesis | Acyrthosiphon pisum | 0.320 | Yadava and Shaw [54]* |
Hippodamia variegata | Diuraphis noxia | 0.237 | Michels and Flanders [52]*** |
Propylea quatuordecimpunctata | Diuraphis noxia | 0.200 | Michels and Flanders [52]*** |
Analysis of herbivore suppression services and relationship with biodiversity
To detect linear trends in herbivore suppression potential over the observation period, one way ANOVA or, if data did not meet assumptions of ANOVA, Kruskal-Wallis one way analysis of variance on ranks were performed for herbivore suppression potential by habitat for both datasets. Least square regressions weighted by the number of reporting traps were performed herbivore suppression potential were examined using data at the weekly resolution only. A least-square linear regression analysis was performed comparing the Shannon Index to herbivore suppression potential for captured coccinellids for each habitat type on the weekly average dataset. Year was treated as a factor in the analysis to account for year-to-year variability in overall coccinellid occurrence. ANOVA was performed on the regression model to determine if the interaction of Shannon diversity and herbivore suppression potential differed between habitats.
Results
Coccinellid abundance data
Between 1989 and 2012, 739,047 individual observations were recorded (species by trap) in the KBS LTER coccinellid database, 61,377 traps were monitored, and 57,813 aphidophagous coccinellids corresponding to thirteen species were captured.
Community structure and dynamics
Coccinellid community structure varied markedly over the course of the study (Figure 1). The proportion of total captured coccinellids for each species from 1989 to 2012 is given in Table 1, and the proportional abundance by year of species accounting for ≥1% of total captures is given in Figure 1. Over the entire study, C. septempunctata, and more recently, H. axyridis comprised the two dominant species, together accounting for more than 69% of total captures. Prior to 1996, C. maculata was frequently observed to be co-dominant with C. septempunctata, but has declined in importance since, typically only representing greater than 20% of the captures in years when maize is planted at the site. The relative abundance of each of these three dominant species varied from year to year (Figure 1). The two most recent additions to the community, H. variegata and P. quatuordecimpunctata, are rapidly increasing in dominance. Although absolute proportions of each species captured varied dramatically by year, the community was increasingly dominated by exotic species over the course of the study. Native species represented 49.8% of captures in the first five years of the study. However, between 2008 and 2012, native species represented only 27.9% of the captures, with more than two thirds of these captures corresponding to C. maculata.
Proportional abundance of most common coccinellid species by year. Data were collected at Kellogg Biological Station, Hickory Corners, MI, 1989-2012.
Total coccinellid abundance also varied widely by year over the course of the study (Figure 2). On average, coccinellid captures were highest in annual crops, followed closely by captures in perennial crops, while the trapping rate in forest habitats was consistently lower than that in either annual or perennial crop habitats (Figure 2).
Average trap captures per year of aphidophagous coccinellids at Kellogg Biological Station, Hickory Corners, MI, 1989-2012, in the annual and perennial crop habitats and in the adjacent forest habitat.
Diversity analysis
Shannon diversity varied between habitat types at the weekly resolution, but not at the yearly resolution of the data (weekly: H2 =860.7, p<0.01, yearly: H2=7.03, p=0.03, Table 3). In a given week, the greatest diversity was observed in annual crops and the lowest diversity was observed in forest habitats. A positive linear trend in Shannon diversity by year was observed at the weekly resolution in annual and perennial crops (annual: slope=0.0102 ±0.0008, p<0.01; perennial: slope=0.0053± 0.0008, p<0.01), but no trends were observed in forest (Figure 3A), nor in Shannon diversity over time within individual habitat groups at the yearly resolution (Figure 3B). When Shannon diversity of only native species was examined at the weekly resolution, a significant linear decrease over time was observed in annual and perennial crop habitats (annual: slope=-0.0031 ±0.0004, p<0.01; perennial: slope=-0.0058± 0.0004, p<0.01), however, no linear relationship was observed in forest habitats (Figure 3C). At a yearly resolution, no significant trends were observed in native coccinellid Shannon diversity (Figure 3D).
Habitat type | Shannon's H | Herbivore suppression potential (NEU), | ||||
---|---|---|---|---|---|---|
Median (Mean), weekly data | Median (Mean), yearly data | Median (Mean), per trap per week | ||||
All species | ||||||
Annual | 0.00 (0.34) | a | 0.97 (0.97) | a | 0.4 (0.6) | a |
Perennial | 0.00 (0.32) | a | 1.18 (1.20) | a | 0.3 (0.5) | b |
Forest | 0.00 (0.07) | b | 1.01 (1.09) | a | 0.0 (0.1) | c |
Native species only | ||||||
Annual | 0.00 (0.12) | a | 0.79 (0.81) | a | 0.0 (0.1) | a |
Perennial | 0.00 (0.12) | a | 1.29 (1.25) | b | 0.0 (0.1) | b |
Forest | 0.00 (0.03) | b | 0.81 (0.80) | a | 0.0 (0.0) | c |
Shannon index of aphidophagous coccinellid community by habitat type at Kellogg Biological Station, Hickory Corners, MI, 1989-2012, showing observed values (symbols) and 3 yr smoothed (lines) data. A) Shannon index analyzed at weekly resolution, all species. B) Shannon index analyzed at yearly resolution, all species. C) Shannon index analyzed at weekly resolution, native species only. D) Shannon index analyzed at yearly resolution, native species.
Herbivore suppression services and relationship with biodiversity
Herbivore suppression potential of the full coccinellid community varied between habitats (Kruskal-Wallis, H2=1610.6, p<0.01, Table 3). Herbivore suppression potential was highest in annual crops, and lowest in forests.
No significant trend was observed in the modeled herbivore suppression potential of the coccinellid community over time in any of the habitat groups (Figure 4A). Herbivore suppression potential due to native species exhibited a significant linear decrease over time in annual and perennial crop habitats (annual: slope=-0.0030 ±0.0007, p<0.01; perennial: slope=-0.0074± 0.0005, p<0.01) but no trend was observed in forest habitats (Figure 4B).
Herbivore suppression potential (in natural enemy units, NEU) of aphidophagous coccinellid community by habitat type at Kellogg Biological Station, Hickory Corners, MI, 1989-2012, showing observed values (symbols) and 3 yr smoothed (lines) data. A) Herbivore suppression potential of all species. B) Herbivore suppression potential due to native species only. Note that the scale of the chart excludes one outlier: a value of 0.95 NEU in annual crops in 1999.
Herbivore suppression potential was examined as a function of Shannon diversity index in three habitat types (Figure 5). The relationship between herbivore suppression potential and Shannon diversity varied between habitats (F 2, 9374 = 24.2, p<0.01); the relationship was positive in perennial and forest habitats (slope =0.24±0.4, 0.47±0.9, respectively) but no significant relationship was found in annual habitats.
Herbivore suppression potential as a function of Shannon diversity index in three habitat types. For clarity, plotted points represent the average herbivore suppression potential per trap per year vs. the average Shannon index for each repetition by a crop type by sampling week combination in a given year. Regression lines are based on weighted regression of weekly observations. Regression lines marked with an asterisk indicate significant slopes at α=0.01.
Discussion
Coccinellid community dynamics
The pattern of long-term co-dominance between several species observed in this study is common in coccinellid communities (i.e., most are dominated by two to four species) although the composition of the group of dominant species may vary with location and time [35]. This co-dominance pattern is not dependent on the invasion or disturbance status of the guild. Similar co-dominance patterns have been observed in a diversity of pre-invasion coccinellid communities [19,22,24,36,37], as well as post-invasion communities [13,25].
Certain coccinellid species tend to dominate captures in areas where they are established. In our study, for instance, C. septempunctata, H. axyridis and C. maculata were among the dominant species in the coccinellid communities when they were present in the community [2,14,23,36,38,39]. P. quatuordecimpunctata has been increasing in its relative abundance since its arrival in the system, and it may join the aforementioned co-dominant species, as it, too, is known to co-dominate the coccinellid community in its native range [40].
Biodiversity and herbivore suppression potential
Net biodiversity of the coccinellid community changed very little over the course of our study. In annual and perennial crop habitats, we observed a small increase in weekly, but not yearly Shannon diversity despite the introduction of three exotic species over the course of the study (Figure 3A, B). Diversity of natives declined in annual and perennial crop habitats at a weekly resolution, and no net change to native diversity was observed over the course of this study at the yearly resolution. This suggests that although native species are still present and just as likely to be captured over the course of a year, they are less likely to be captured within a given week. This result is similar to what has been observed in previous studies. In a review by Harmon et al. [2] combining the observations of several North American coccinellid invasions, the number of native species in an assemblage did not change in response to the addition of an exotic species (i.e., it was rare to observe a complete elimination of a native species associated with the introduction of an exotic species). The diversity index associated with native species only decreased slightly, on average, after the establishment of an exotic species [2].
Modeled herbivore suppression potential of the community also changed very little in response to invasion (Figure 4). Acorn [41] suggested that the interpretation of coccinellid invasion data has been influenced by attitudes against ‘biological pollution’ even though ecological change (of the kind resulting from native species being displaced by exotics) does not yield a loss of function. Our data support this assertion, at least from the standpoint of preserving the function of aphidophagy. We estimated very little change in the long term herbivore suppression potential across our experimental landscape over the course of the study (Figure 4A). However, there was a period of increased variability in herbivore suppression potential immediately after the introduction of soybean aphid, Aphis glycines, in 2000. This introduction is known to change the resource structure for coccinellids at landscape scales [42]. During the acute invasion phase of this aphid from 2000 to 2006, coccinellid densities reached higher peaks, and were even more variable than what is typically observed (Figure 2). At this time, a brief depression in overall diversity of the coccinellid community was also observed (Figure 3B), as a single exotic species (H. axyridis) became hyper-dominant. Soybean aphid is a preferred prey item of H. axyridis and the arrival of this aphid biotically facilitated the invasion of this exotic coccinellid [43]. Soybean aphid outbreaks have since decreased in frequency, and there is evidence that, since 2007, this prey item is no longer acting as a significant driver of population dynamics of H. axyridis [44].
Diversity was significantly and positively related to herbivore suppression potential in perennial and forest habitats, but was uncorrelated in annual crops (Figure 5). This observation has important implications for biological control in these systems. When coccinellid species are partitioned into spatiotemporal niches, intraspecific competition will be more important than interspecific competition in the population dynamics of a species, intraguild predation will be uncommon, and prey suppression will increase with diversity of the community [7]. The exception to this may be in landscapes with less plant diversity, such as annual cropping systems, which provide a lower diversity of habitats and, in turn, prey species. In this case, a coccinellid species particularly adapted to the particular prey resource available may essentially dominate the entire habitat, to the exclusion of other species. However, functional diversity, that is, the partitioning of resources between consumers with different resource use patterns, is more important than simple biodiversity in determining the level of resource exploitation when resources themselves are diverse [45].
Sampling methodology
Fewer coccinellids were collected in forest habitats than in perennial or annual habitats over the duration of the study. This might be due, at least in part, to decreased efficiency of our trapping design when located in arboreal habitats (see methods). Nevertheless, more coccinellids were captured in managed early successional habitats (within the Main Cropping System Experiment) than in successional forests. The fact that these two types of successional habitats were structurally similar may indicate that indeed fewer coccinellids were present in forest habitats. Although yellow sticky cards are imperfect estimators of relative abundance of coccinellids [46], they represent a cost effective, consistent sampling unit. This characteristic makes them a useful methodology when employed in long term studies, which may be otherwise biased by personnel turnover or inconsistent sampling. Also, the fact they are permanently placed in the field may increase the probability of capturing rare species as they move through the landscape. It is important to note that between habitat and between species comparisons may be affected by the varying trap efficiency for a given species in a given habitat, and thus the strongest evidence for ecological change results from within species, within habitat trends.
Conclusions
Despite repeated invasions and a dramatic change in overall composition of the coccinellid community in southwestern Michigan, we find little evidence to suggest a change in function of aphidophagy. Our estimates of biodiversity and herbivore suppression potential, and the overall population dynamics of the community as a whole suggest that this community is currently functioning much as it was at the initiation of this study, and to other similar systems [13,19,22,24,25,36,37].
Long term studies of invaded systems are essential because the impact of exotic species may change over time. Our study confirms prior observations that exotic coccinellids negatively impact community diversity during the acute phases of their invasion (i.e., when they often singly dominate the coccinellid community for several years) [2,47]. Afterwards, the community diversity returns to a ‘new normal’ with several co-dominant species which variably alternate in relative abundance. This variation depends on opportunistic responses to environmental conditions, but is also likely influenced by a given species’ characteristic population fluctuations.
Non-native species that are superior competitors are known to negatively affect the diversity and abundance of closely related or functionally similar native species. However, the direct impact of exotic species on ecosystem functions is more variable depending on the degree of functional overlap and phylogenetic relatedness between the exotic species and the native species that are displaced [11,15]. In guilds of functionally similar predators, capacity for herbivore consumption is controlled by the availability of prey, and is less dependent on the identity of the members of the guild [25]. This does not mean that the loss of native coccinellid biodiversity is without concern, however. Although a low diversity of exotic species may provide equivalent service, native coccinellids provide resilience of herbivore suppression services in a landscape: when prey populations in agricultural systems escape control by exotics, native species quickly colonize pest outbreak areas [14]. Members of insect communities with large body sizes, like the two dominant exotic species at our study site, tend to be among the most functionally efficient members of the community (Table 2), and may also be more prone to local extinction [48]. If native coccinellids continue to decline, and any of the dominant exotic coccinellids which are now very important providers of herbivore suppression service were lost, major disruption to the pest suppression services offered by a landscape could be observed.
Acknowledgments
The authors would like to thank William Snyder and Helen Roy for helpful comments offered on an earlier draft of this manuscript, and two anonymous reviewers whose insights will help direct future analyses involving this coccinellid community. We acknowledge the numerous field assistants for weekly field data collection and data preservation. We also thank the KBS-LTER Management Team for their assistance with trapping logistics and information management.
Author Contributions
Conceived and designed the experiments: SHG MCG. Performed the experiments: SHG MCG. Analyzed the data: CAB. Wrote the manuscript: CAB DAL.
References
- 1. Gardiner MM, Allee LL, Brown PMJ, Losey JE, Roy HE et al. (2012) Lessons from lady beetles: accuracy of monitoring data from US and UK citizen-science programs. Frontiers in Ecology and the Environment: Online Preprint. doi:https://doi.org/10.1890/110185.
- 2. Harmon JP, Stephens E, Losey J (2007) The decline of native coccinellids (Coleoptera: Coccinellidae) in the United States and Canada. Journal of Insect Conservation 11: 85-94. doi:https://doi.org/10.1007/s10841-006-9021-1.
- 3. Hodek I, Michaud JP (2008) Why is Coccinella septempunctata so successful? (A point-of-view). European Journal of Entomology 105: 1-12.
- 4.
Koch RL (2003) The multicolored Asian lady beetle, Harmonia axyridis: A review of its biology, uses in biological control, and non-target impacts. Journal of Insect Science 3: 1-16. Available online at: doi:10.1672/1536-2442(2003)003[0001:TMOAAE]2.0.CO;2. PubMed: 15841218.
- 5. Gordon RD (1987) The first North American records of Hippodamia variegata (Goeze) (Coleoptera: Coccinellidae). Journal of the New York Entomological Society 95: 307-309.
- 6. Dysart RJ (1988) The European lady beetle Propylea quatuordecimpunctata: new locality records for North America (Coleoptera: Coccinellidae). Journal of the New York Entomological Society 96: 119-121.
- 7. Snyder WE (2009) Coccinellids in diverse communities: Which niche fits? Biological Control 51: 323-335. doi:https://doi.org/10.1016/j.biocontrol.2009.05.010.
- 8. Straub CS, Snyder WE (2008) Increasing enemy biodiversity strengthens herbivore suppression on two plant species. Ecology 89: 1605-1615. doi:https://doi.org/10.1890/07-0657.1. PubMed: 18589525.
- 9. Williams T (1996) Invasion and displacement of experimental populations of a conventional parasitoid by a heteronomous hyperparasitoid. Biocontrol Science and Technology 6: 603-618. doi:https://doi.org/10.1080/09583159631244.
- 10. Yao DS, Chant DA (1989) Population growth and predation interference between two species of predatory phytoseiid mites (Acarina: Phytoseiidae) in interactive systems. Oecologia 80: 443-455. doi:https://doi.org/10.1007/BF00380065.
- 11. Reitz SR, Trumble JT (2002) Competitive displacement among insects and arachnids. Annu Rev Entomol 47: 435-465. doi:https://doi.org/10.1146/annurev.ento.47.091201.145227. PubMed: 11729081.
- 12. Brown MW, Miller SS (1998) Coccinellidae (Coleoptera) in apple orchards of eastern West Virginia and the impact of invasion by Harmonia axyridis. Entomological News 109: 143-151.
- 13. Alyokhin A, Sewell G (2004) Changes in a lady beetle community following the establishment of three alien species. Biological Invasions 6: 463-471. doi:https://doi.org/10.1023/B:BINV.0000041554.14539.74.
- 14. Evans EW (2004) Habitat displacement of North American ladybirds by an introduced species. Ecology 85: 637-647. doi:https://doi.org/10.1890/03-0230.
- 15. Ricciardi A, Atkinson SK (2004) Distinctiveness magnifies the impact of biological invaders in aquatic ecosystems. Ecology Letters 7: 781-784. doi:https://doi.org/10.1111/j.1461-0248.2004.00642.x.
- 16. Ricciardi A, Hoopes MF, Marchetti MP, Lockwood JL (2013) Progress toward understanding the ecological impacts of nonnative species. Ecological Monographs 83: 263-282. doi:https://doi.org/10.1890/13-0183.1.
- 17. Bahlai CA, Xue Y, McCreary CM, Schaafsma AW, Hallett RH (2010) Choosing organic pesticides over synthetic pesticides may not effectively mitigate environmental risk in soybeans. PLOS ONE 5: e11250. doi:https://doi.org/10.1371/journal.pone.0011250. PubMed: 20582315.
- 18. Bahlai CA, Weiss RM, Hallett RH (2013) A mechanistic model for a tritrophic interaction involving soybean aphid, its host plants, and multiple natural enemies. Ecological Modelling 254: 54-70. doi:https://doi.org/10.1016/j.ecolmodel.2013.01.014.
- 19. Putman WL (1964) Occurrence and food of some Coccinellids (Coleoptera) in Ontario peach orchards. Canadian Entomologist 96: 1149-1155. doi:https://doi.org/10.4039/Ent961149-9.
- 20. Smith BC (1971) Effects of various factors on the local distribution and density of coccinellid adults on corn (Coleoptera: Coccinellidae). Canadian Entomologist 103: 1115-1120. doi:https://doi.org/10.4039/Ent1031115-8.
- 21. Finlayson CJ, Landry KM, Alyokhin AV (2008) Abundance of native and non-native lady beetles (Coleoptera: Coccinellidae) in different habitats in Maine. Annals of the Entomological Society of America 101: 1078-1087. doi:https://doi.org/10.1603/0013-8746-101.6.1078.
- 22. Kieckhefer RW, Elliott NC (1990) A 13-year survey of the aphidophagous Coccinellidae in maize fields in eastern South Dakota. Canadian Entomologist 122: 579-581. doi:https://doi.org/10.4039/Ent122579-5.
- 23. Kieckhefer R, Elliott N, Beck D (1992) Aphidophagous coccinellids in alfalfa, small grains, and maize in eastern South Dakota. Great Lakes Entomologist 25: 15-23.
- 24. Elliott NC, Kieckhefer RW (1990) Dynamics of aphidophagous coccinellid assemblages in small grain fields in eastern South Dakota. Environmental Entomology 19: 1320-1329.
- 25. Elliott N, Kieckhefer R, Kauffman W (1996) Effects of an invading coccinellid on native coccinellids in an agricultural landscape. Oecologia 105: 537-544. doi:https://doi.org/10.1007/BF00330017.
- 26. Hesler LS, Kieckhefer RW, Beck DA (2001) First record of Harmonia axyridis (Coleoptera: Coccinellidae) in South Dakota and notes on its activity there and in Minnesota. Entomological News 112: 264-270.
- 27. Hesler LS, Kieckhefer RW (2008) Status of exotic and previously common native coccinellids (Coleoptera) in South Dakota landscapes. Journal of the Kansas Entomological Society 81: 29-49. doi:https://doi.org/10.2317/JKES-704.11.1.
- 28. Brown MW (2003) Intraguild responses of aphid predators on apple to the invasion of an exotic species, Harmonia axyridis. BioControl 48: 141-153. doi:https://doi.org/10.1023/A:1022660005948.
- 29. Maredia K, Gage S, Landis D, Wirth T (1992) Ecological observations on predatory Coccinellidae (Coleoptera) in southwestern Michigan. Great Lakes Entomologist 25: 265-270.
- 30. Hodek I (1973) Biology of Coccinellidae. The Hague: Dr. W Junk N. V. Publishers: 260.
- 31. Muma MH (1955) Some ecological studies on the twice-stabbed lady beetle Chilocorus stigma (Say). Annals of the Entomological Society of America 48: 493-498.
- 32.
Marshall SA (2006) Insects- their natural history and diversity: with a photographic guide to insects of Eastern North America. Richmond Hill: Firefly Books Inc.. p. 720.
- 33.
Zuur AF, Ieno EN, Smith GM (2007) Analysing ecological data; M Gail KK, J. SametA. TsiatisW. Wong. New York: Springer. p. 672.
- 34.
R Development Core Team (2012) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing. Vienna, Austria. p. 2.15.3.
- 35.
Hodek I, Honek A (1996) Ecology of Coccinellidae. Kluwer Academic Publishers, Dordrecht.
- 36. Foott WH (1973) Observations on Coccinellidae in corn fields in Essex county, Ontario. Proceedings of the Entomological Society of Ontario 104: 16-21.
- 37. Gagné WC, Martin JL (1968) The insect ecology of red pine plantations in central Ontario: v. The Coccinellidae (Coleoptera). Canadian Entomologist 100: 835-846. doi:https://doi.org/10.4039/Ent100835-8.
- 38. Evans EW, Soares A, Yasuda H (2011) Invasions by ladybugs, ladybirds, and other predatory beetles. BioControl 56: 597-611. doi:https://doi.org/10.1007/s10526-011-9374-6.
- 39. Brown PMJ, Frost R, Doberski J, Sparks TIM, Harrington R et al. (2011) Decline in native ladybirds in response to the arrival of Harmonia axyridis: early evidence from England. Ecological Entomology 36: 231-240. doi:https://doi.org/10.1111/j.1365-2311.2011.01264.x.
- 40. Radwan Z, Lövei GL (1983) Structure and seasonal dynamics of larval, pupal, and adult coccinellid (Col., Coccinellidae) assemblages in two types of maize fields in Hungary. Zeitschrift für Angewandte Entomologie 96: 396-408.
- 41. Acorn J (2007) Invasion of the seven-spotted certainty snatchers. American Entomologist 53: 191-192.
- 42.
Ragsdale DW, Voegtlin DJ, O'Neil RJ (2004) Soybean aphid biology in North America. Annals of the Entomological Society of America 97: 204-208. Available online at: doi:10.1603/0013-8746(2004)097[0204:SABINA]2.0.CO;2.
- 43. Heimpel G, Frelich L, Landis D, Hopper K, Hoelmer K et al. (2010) European buckthorn and Asian soybean aphid as components of an extensive invasional meltdown in North America. Biological Invasions 12: 2913-2931. doi:https://doi.org/10.1007/s10530-010-9736-5.
- 44. Knapp AK, Smith MD, Hobbie SE, Collins SL, Fahey TJ et al. (2012) Past, present, and future roles of long-term experiments in the LTER Network. BioScience 62: 377-389. doi:https://doi.org/10.1525/bio.2012.62.4.9.
- 45. Finke DL, Snyder WE (2008) Niche partitioning increases resource exploitation by diverse communities. Science 321: 1488-1490. doi:https://doi.org/10.1126/science.1160854. PubMed: 18787167.
- 46. Musser FR, Nyrop JP, Shelton AM (2004) Survey of predators and sampling method comparison in sweet corn. J Econ Entomol 97: 136-144. doi:https://doi.org/10.1603/0022-0493-97.1.136. PubMed: 14998137.
- 47. Turnock WJ, Wise IL, Matheson FO (2003) Abundance of some native coccinellines (Coleoptera: Coccinellidae) before and after the appearance of Coccinella septempunctata. Canadian Entomologist 135: 391-404. doi:https://doi.org/10.4039/n02-070.
- 48. Larsen TH, Williams NM, Kremen C (2005) Extinction order and altered community structure rapidly disrupt ecosystem functioning. Ecol Lett 8: 538-547. doi:https://doi.org/10.1111/j.1461-0248.2005.00749.x. PubMed: 21352458.
- 49. Gordon RD (1985) The Coccinellidae (Coleoptera) of America North of Mexico. Journal of the New York Entomological Society 93: i-912.
- 50. Ellingsen IJ (1969) Fecundity, aphid consumption and survival of the aphid predator Adalia bipunctata L. (Col., Coccinellidae). Norsk Entomol Tidsskr 16: 91-95.
- 51. Xue Y, Bahlai CA, Frewin A, Sears MK, Schaafsma AW et al. (2009) Predation by Coccinella septempunctata and Harmonia axyridis (Coleoptera: Coccinellidae) on Aphis glycines (Homoptera: Aphididae). Environ Entomol 38: 708-714. doi:https://doi.org/10.1603/022.038.0322. PubMed: 19508779.
- 52. Michels G, Flanders R (1992) Larval development, aphid consumption and oviposition for five imported coccinellids at constant temperature on Russian wheat aphids and greenbugs. Southwestern Entomologist 17: 233-243.
- 53. Lucas E, Gagne I, Coderre D (2002) Impact of the arrival of Harmonia axyridis on adults of Coccinella septempunctata and Coleomegilla maculata (Coleoptera: Coccinellidae). Eur J Entomol 99: 457-463.
- 54. Yadava CP, Shaw FR (1968) The preferences of certain coccinellids for pea aphids, leafhoppers, and alfalfa weevil larvae. Journal of Economic Entomology 61: 1104-1105.
- 55. Morales JOS, Burandt CL (1985) Interactions between Cycloneda sanguinea and the brown citrus aphid: adult feeding and larval mortality. Environmental Entomology 14: 520-522.
- 56. Soares AO, Coderre D, Schanderl H (2004) Dietary self-selection behaviour by the adults of the aphidophagous ladybeetle Harmonia axyridis (Coleoptera: Coccinellidae). Journal of Animal Ecology 73: 478-486. doi:https://doi.org/10.1111/j.0021-8790.2004.00822.x.