Ground Beetle (Coleoptera: Carabidae) Assemblages in Conventional ...

COMMUNITY AND ECOSYSTEM ECOLOGY

Ground Beetle (Coleoptera: Carabidae) Assemblages in Conventional and Diversified Crop Rotation Systems MEGAN E. O’ROURKE,1,2 MATT LIEBMAN,3

AND

MARLIN E. RICE1

Environ. Entomol. 37(1): 121Ð130 (2008)

ABSTRACT Ground beetles (Coleoptera: Carabidae) are important in agro-ecosystems as generalist predators of invertebrate pests and weed seeds and as prey for larger animals. However, it is not well understood how cropping systems affect ground beetles. Over a 2-yr period, carabids were monitored two times per month using pitfall traps in a conventional chemical input, 2-yr, corn/soybean rotation system and a low input, 4-yr, corn/soybean/triticale-alfalfa/alfalfa rotation system. Carabid assemblages were largely dominated by a few species across all cropping treatments with Poecilus chalcites Say comprising ⬎70% of pitfall catches in both years of study. Overall carabid activity density and species richness were higher in the low input, 4-yr rotation compared with the conventionally managed, 2-yr rotation. There were greater differences in the temporal activity density and species richness of carabids among crops than within corn and soybean treatments managed with different agrichemical inputs and soil disturbance regimes. Detrended correspondence analysis showed strong yearly variation in carabid assemblages in all cropping treatments. The increase in carabid activity density and species richness observed in the 4-yr crop rotation highlights the potential beneÞts of diverse crop habitats for carabids and the possibility for managing natural enemies by manipulating crop rotations. KEY WORDS agro-ecology, beetle communities, biological control, generalist predators, natural enemies

With the intensiÞcation of agricultural production during the 20th century, agro-ecosystems have become increasingly dominated by chemically intensive, short rotation cropping systems (Pretty 1995). Concomitantly, many agricultural production practices such as tillage and pesticide use have been associated with the degradation of soil and water resources (National Research Council 1989). One approach for mitigating the environmental consequences of agricultural production is to diversify crop rotations. The possible beneÞts of diversiÞed cropping systems include reduced need for inorganic nitrogen additions when legumes are added to a rotation (Chalk 1998), reduced soil erosion and improved soil characteristics (Karlen et al. 1994), and reduced pest pressures (Brust and King 1994, Kratochvil et al. 2004, Teasdale et al. 2004). One way in which diversiÞed cropping systems might contribute to reduced pest pressures is through conservation of natural enemy populations. Carabids are an important group of generalist predator natural enemies that are commonly found in agro-ecosystems (Kromp 1999). They have been reported to consume a wide range of agricultural pest species including 1 Department of Entomology, Iowa State University, Ames, IA 50011. 2 Corresponding author, e-mail: [email protected]. 3 Department of Agronomy, Iowa State University, Ames, IA 50011.

both invertebrates and weed seeds (Toft and Bilde 2002). Carabids are also important prey species for many vertebrates such as birds and rodents and may contribute to the overall biotic diversity within agroecosystems (Holland 2002). Despite the importance of carabids in agroecosystems, impacts of crop management practices, including tillage and agrichemical use, on them are not well understood. A number of studies have underscored the importance of Þeld margins (French and Elliott 1999, Thomas and Marshall 1999) and refuges composed of perennial plants (Carmona and Landis 1999, Lee et al. 2001) for conserving carabids. However, within the crop habitat itself, there is conßicting evidence as to the consequences of tillage and pesticide regimen on carabids. Carcamo (1995) found that total carabid activity density in barley was higher with conventional tillage compared with reduced tillage, whereas Brust et al. (1986) found reduced levels of carabid activity density in conventional versus no-till corn and soybean. In laboratory experiments, it was determined that the herbicide metribuzin caused no direct mortality of Harpalus rufipes, whereas Þeld experiments showed that the combined effects of metribuzin and chisel plowing signiÞcantly reduced H. rufipes activity density (Zhang et al. 1998). In examining conventional versus organic management regimens, Melnychuk et al. (2003) found no signiÞcant effects on carabid activity density or species diversity,

0046-225X/08/0121Ð0130$04.00/0 䉷 2008 Entomological Society of America

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whereas Carcamo et al. (1995) found higher levels of carabid activity density and species diversity in organic systems. In this study, the main objectives were to understand how cropping systems affect carabid activity density and community characteristics. Within a crop, we hypothesized that management regimens using reduced levels of fertilizers and herbicide inputs would result in greater carabid activity density and species richness. We also hypothesized that increasing the diversity of crops within a rotation system would result in increased carabid activity density and species richness. To test these hypotheses, we compared carabid assemblages in a conventionally managed corn/ soybean rotation system with a low chemical-input corn/soybean/triticale-alfalfa/alfalfa rotation system.

Materials and Methods Cropping Systems. Crop rotations were established in 2002 on Clarion-Nicollet-Webster mixed loam soils at Iowa State UniversityÕs Marsden Farm, Boone Co., IA. Before the cropping systems experiment, the land had been commercially managed for corn (Zea mays L.) and soybean (Glycine max L. Merr.) production and planted to oat (Avena sativa L.) in 2001. The two cropping systems compared were a 2-yr corn/soybean rotation and a 4-yr corn/soybean/triticale (⫻Triticosecale Wittmack) underseeded with alfalfa (Medicago sativa L.)/alfalfa rotation. The experiment was laid out as a randomized complete block design with the two crops of the 2-yr rotation and the four crops of the 4-yr rotation present every year. There were four replicate blocks separated by ⬇15 m of mowed, mixed grasses (mostly Festuca spp.), and each treatment plot within the four blocks measured 18 by 84 m. The two cropping systems were managed for high yield, and the timing and quantity of inputs varied between years depending on soil nutrient tests, Þeld scouting, and weather conditions. Daily average temperatures from July through October were 18.9 and 18.5⬚C during 2003 and 2004, respectively, compared with an 18.6⬚C average temperature for the same period since 1950. Total rainfall from July through October 2003 and 2004 was 317 and 261 mm, respectively, compared with an average of 346 mm for the same time period since 1950. The 2-yr system received 3.35 times more inorganic nitrogen and 4.76 times more herbicide than the 4-yr rotation (Heggenstaller and Liebman 2006). However, mechanical cultivation to control weeds was greater in 4-yr corn and soybean than 2-yr corn and soybean. Nitrogen inputs were applied to corn and triticalealfalfa plots. Synthetic nitrogen fertilizer was applied to the corn phase of the 2-yr system at a rate of 150 and 110 kg N/ha in 2003 and 2004, respectively, based on soil test results. Synthetic nitrogen fertilizer was applied to corn in the 4-yr system at rates of 55 kg N/ha in 2003 and 70 kg N/ha in 2004, based on soil test results, and to triticale at a rate of 30 kg N/ha in both years. Organic N inputs were also applied to corn in

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the 4-yr rotation in the form of composted manure applied at a rate of 15 mg/ha (fresh weight). Herbicides were applied to corn and soybean. In 2-yr corn plots, metolachlor and isoxaßutole were applied at 1.60 and 0.11 kg (AI)/ha, respectively, preplant incorporated (PPI) in 2003 and preemergence (PRE) in 2004. A postemergence (POST), broadcast application of nicosulfuron, rimsulfuron, and mestrione, at 0.026, 0.013, and 0.07 kg AI)/ha, respectively, was also made to 2-yr corn plots in 2003. PPI and PRE herbicides were not applied to 4-yr corn plots. However, POST, banded applications of nicosulfuron, rimsulfuron, and mestrione at 0.013, 0.007, and 0.035 kg (AI)/ha were made in both 2003 and 2004 (materials were applied to only 50% of surface area; reported values indicate dosages to total plot area). Weeds were controlled in 2-yr soybean in 2003 with PPI metolachlor and in 2004 with PRE metolachlor applied at 1.60 kg (AI)/ha both years. In 2003, the 2-yr soybean treatment was also treated with POST broadcast bentazon and clethodim applied at 1.12 and 0.11 kg (AI)/ha, respectively. Chemical weed control in 4-yr soybean included PPI metolachlor in 2003 and PRE metolachlor in 2004 applied at 1.60 kg (AI)/ha in both years. The 4-yr soybean treatment also received POST banded ßumiclorac at 0.03 kg (AI)/ha in 2003 and POST banded bentazon at 0.56 kg (AI)/ha in 2004 (dosage to total plot area). The 2-yr rotation was chisel plowed every other year after corn harvest, whereas the 4-yr rotation was moldboard plowed in the fall after the alfalfa phase and chisel plowed after the corn phase of the rotation. In 2-yr corn, weeds were rotary hoed once in 2003, but no mechanical weed control was used in 2004. Fouryear corn received one rotary hoeing and two interrow cultivations in 2003 and one rotary hoeing and one inter-row cultivation in 2004. No mechanical weed control was used in 2-yr soybean, but 4-yr soybean received one rotary hoeing and one inter-row cultivation in 2003, and one rotary hoeing and two interrow cultivations in 2004. Weeds were mechanically controlled in triticale-alfalfa plots, receiving one stubble mowing of the underseeded alfalfa in August 2003 and 2004. Alfalfa plots were harvested three times in 2003 and four times in 2004. Sampling. Carabid activity density was monitored using pitfall traps. The abundance of adult beetles collected by pitfall traps reßects both the activity of adult carabids and their propensity for moving into traps and their population density in the surrounding environment (Thiele 1977, Southwood 1978). Traps were 1-liter plastic cups buried ßush to the soil surface containing a 20% propylene glycol preservative solution. Within each treatment plot, there were four pitfall traps placed at least 5 m from adjacent plots and ⬇18 m from each other and the grassy plot borders. In total, there were 96 pitfall traps in the experimental area (4 per plot ⫻ 6 treatment plots ⫻ 4 blocks). Pulsating sampling was used to collect carabids, where pitfall traps were open for 5 consecutive d, approximately every 2 wk (Sapia et al. 2006). Pulsating sampling minimized the time traps were open in the rain

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OÕROURKE ET AL.: GROUND BEETLE ASSEMBLAGES AND CROPPING SYSTEMS

and allowed for trap retrieval when tractors were in the Þeld. During 2003, traps were opened for nine 5-d periods between 23 May and 7 October. During 2004, traps were opened for eleven 5-d periods between 11 May and 6 October. On retrieval in the Þeld, pitfall trap contents were sieved through 1-mm mesh, placed in sealable plastic bags, and stored in a freezer until sorting. Carabid species were determined according to Lindroth (1969) and Bousquet and Larochelle (1993). Only adult beetles were identiÞed and recorded in this study. A voucher specimen collection was deposited in Iowa State UniversityÕs Department of Entomology Insect Museum. Statistical Analysis. Fisher exact tests were used to determine whether species trapped in only one treatment were more likely to be found in the triticalealfalfa and alfalfa treatments compared with the 2- and 4-yr corn and soybean treatments. Fisher exact tests were also used to determine whether species collected in only one treatment were more likely to be found in the 2-yr corn and soybean treatments than in the 4-yr corn, soybean, triticale-alfalfa, and alfalfa treatments (Sokal and Rohlf 1995). Four indices were calculated to evaluate cropping system effects on carabid beetle assemblages: activity density, species richness, SimpsonÕs diversity index, and SimpsonÕs evenness index. Activity density was the total number of carabids trapped. Species richness was the total number of carabid species trapped. SimpsonÕs diversity index indicates the probability of randomly picking two organisms from a sample that are different species and was calculated as 1 ⫺ 冱pi2 where pi is the proportion of species i in the community. SimpsonÕs evenness index ranges from 0 to 1 and increases as the proportion of each species in a sample nears equality; it was calculated as s/冱pi2, where s is the total number of species and pi is the proportion of species i in the community (Krebs 1999). SigniÞcant differences in assemblage indices among treatments were determined using analysis of variance (ANOVA), with year, crop treatment, and crop treatment by year interactions as Þxed effects and block as a random effect (PROC MIXED; SAS Institute 2002). Activity density and species richness were ln(x ⫹ 1) transformed. Multiple, pairwise treatment comparisons were all Tukey adjusted. Overall differences between the 2- and 4-yr crop rotations were evaluated using contrast statements. Detrended correspondence analysis (DCA) was conducted using the statistical software PC-ORD version 4.0 (McCune and Mefford 1999) to evaluate variations in carabid assemblages among cropping treatments and between 2003 and 2004. The nine most abundant beetle species, for which at least 50 specimens were collected over 2 yr, were treated as separate response variables, and all other beetles species were added together in the category other. DCA was conducted with a rescaling threshold of 0.0, and axes were detrended using 30 segments. In each analysis, the Þrst two axes were interpreted, and the proportion of variance explained by those axes was calculated from the correlations between ␹2 distances among

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samples in the original space and the Euclidean distances in ordination space (McCune and Mefford 1999). Differences in individual species responses to cropping treatments were evaluated separately over 2003 and 2004 using ANOVA with crop treatment as a Þxed factor, sample date as a repeated measure with compound symmetry covariance structure (samples from two consecutive dates are not assumed to be more correlated than samples on two random dates), and block as a random factor (PROC MIXED; SAS Institute 2002). Activity density of each beetle species was either ln(x ⫹ 1) transformed or sqrt(x) transformed, depending on which transformation caused data to appear more normally distributed. Probability values for posthoc multiple comparisons among cropping treatments were obtained using Tukey pairwise adjustments. Results Phenology. In both 2003 and 2004, the temporal pattern of carabid activity density was more similar within crops than among crops, despite differences in 2- and 4-yr rotation management. In 2- and 4-yr corn, carabid activity density peaked in mid-June and fell in early July when the canopy had Þlled in and the corn was entering the early silking phase of development (Figs. 1, C2 and C4, and 2, C2 and C4). In 2- and 4-yr soybean, carabid activity density was high in mid-June and did not reach consistent lows until early August when the soybean canopy had Þlled in (Figs. 1, S2 and S4, and 2, S2 and S4). In triticale-alfalfa plots, the temporal pattern of carabid activity density was distinctive in 2003, with more carabid species caught early in the season compared with the other cropping treatments. The drop in carabid activity density in triticale-alfalfa, in late July, corresponded to triticale harvest (Figs. 1, T4, and 2, T4). In alfalfa, carabid activity density remained higher, later in the season, than in other crops. Carabid catches were low in alfalfa after harvest, when the canopy was very open, peaked between alfalfa cuttings when the canopy regrew, and declined before the next harvest (Figs. 1, A4, and 2, A4). Assemblage. A total of 3,168 carabid beetles, representing 21 species, was collected in 2003. During 2004, a total of 3,556 carabids of 32 species was collected. The dominant carabid sampled was Poecilus chalcites, comprising ⬎70% of pitfall catches in both 2003 and 2004. According to Bousquet and Larochelle (1993), the single specimen of Anisodactylus caenus collected in 2004 in the triticale-alfalfa treatment represented the Þrst time this species had been collected in Iowa. Of the nine species of carabids captured in just one cropping treatment in 2003, they were just as likely to be trapped in the four corn and soybean treatments as the two triticale-alfalfa and alfalfa treatments (P ⬎ 0.50) and were just as likely to be trapped in 2-yr corn and soybean as 4-yr corn, soybean, triticale-alfalfa, and alfalfa rotation treatments (P ⬎ 0.50). However, in 2004, the 13 species trapped in only one treatment were encountered more often in the two triticalealfalfa and alfalfa treatments than the four corn and

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Fig. 1. Temporal patterns of adult P. chalcites, and the sum of all other adult carabid species captured per pitfall trap during 2003 in Boone Co., IA, in six crop ⫻ rotation system treatments (C2) corn, 2-yr; (S2) soybean, 2-yr; (C4) corn, 4-yr; (S4) soybean, 4-yr; (T4) triticale-alfalfa, 4-yr; (A4) alfalfa, 4-yr. Error bars represent SE of total beetle abundance at each sampling date.

soybean treatments (P ⬍ 0.01) but were not more likely to be trapped in 4-yr than 2-yr rotation treatments (P ⫽ 0.16; Table 1).

Different rotation management regimens did not signiÞcantly affect the activity density, species richness, SimpsonÕs evenness index, or SimpsonÕs diversity

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Fig. 2. Temporal patterns of adult P. chalcites, and the sum of all other adult carabid species captured per pitfall trap during 2004 in Boone Co., IA, in six crop ⫻ rotation system treatments: (C2) corn, 2-yr; (S2) soybean, 2-yr; (C4) corn, 4-yr; (S4) soybean, 4-yr; (T4) triticale-alfalfa, 4-yr; (A4) alfalfa, 4-yr. Error bars represent SE of total beetle abundance at each sampling date.

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Table 1. Relative abundance of ground beetle species collected in 2003 and 2004 at Iowa State University’s Marsden Farm, Boone Co., IA Species Poecilus chalcites Say Stenolophus comma F. Harpalus pensylvanicus DeGeer Poecilus lucublandus Say Harpalus herbivagus Say Anisodactylus sanctaecrucis F. Bembidion rapidum LeConte Scarites quadriceps Chaudoir Agonum placidum Say Pterostichus permundus Say Clivina bipustulata F. Clivina impressifrons LeConte Stenolophus ochropezus Say Harpalus calignosus F. Anisodactylus rusticus Say Cratacanthus dubius Palisot de Beauvois Chlaenius impunctifrons Say Galerita janus F. Cyclotrachelus sodalis LeConte Agonum cupripenne Say Anisodactylus harrisii LeConte Amara carinata LeConte Amara impuncticollis Say Harpalus erythropus Dejean Amara aeneopolita Casey Anisodactylus merula Germar Pterostichus commutabilis Motschulsky Pterostichus stygicus Say Calosoma externum Say Amara obesa Say Lebia viridis Say Chlaenius brevilabris LeConte Discoderus parallelus Haldeman Anisodactylus ovularis Casey Chlaenius tomentosus Say Anisodactylus caenus Say Chlaenius lithophilus Say

Percent total 2003a

2004b

70.1 9.4 5.1 2.3 2.0 1.6 1.2 1.2 1.1 1.0 0.9 0.8 0.8 0.5 0.3 0.3

71.8 1.9 0.5 9.0 0.5 1.3 0.4 6.3 0.3 4.4 0.5 0.2 ⬍0.1 0.1 0.2 0.0

0.3 0.2 0.2 0.2 0.1 0.1 0.1 0.1 ⬍0.1 ⬍0.1 ⬍0.1

0.1 0.1 1.1 0.1 0.2 0.5 ⬍0.1 0.0 ⬍0.1 ⬍0.1 ⬍0.1

⬍0.1 ⬍0.1 ⬍0.1 ⬍0.1 0.0 0.0 0.0 0.0 0.0 0.0

T4 A4 T4 C2 C4 C4 C4 S4 T4

⬍0.1 0.0 0.0 0.0 ⬍0.1 ⬍0.1 ⬍0.1 ⬍0.1 ⬍0.1 ⬍0.1

A4

T4

T4 A4 S2 A4 A4

T4 T4 T4 T4 T4 A4

Treatment abbreviations following data represent instances where a species was trapped exclusively in one treatment: (C2) corn-2yr, (S2) soybean-2yr, (C4) corn-4yr, (S4) soybean-4yr. (T4) triticale4yr, (A4) alfalfa-4yr. a A total of 3,168 individuals collected over nine sampling dates. b A total of 3,556 individuals collected over 11 sampling dates.

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index in the different rotation treatments of corn or soybean in 2003 and 2004. However, when contrasts were made between the 2- and 4-yr cropping systems over the 2 yr of the experiment, there was signiÞcantly greater activity density (t ⫽ 2.71, df ⫽ 33, P ⫽ 0.01) and number of species (t ⫽ 3.42, df ⫽ 33, P ⫽ 0.002) per year in the 4-yr system than in the 2-yr system. However, carabid evenness was greater in the 2-yr than the 4-yr system (t ⫽ 2.41, df ⫽ 33, P ⬍ 0.05), largely because of the overall increased activity density of P. chalcites in the 4-yr crop rotation. There were no signiÞcant differences in SimpsonÕs diversity between the 2- and 4-yr systems (Table 2). DCA of beetle assemblages in 2003 indicated that triticale-alfalfa treatments separated from the other cropping treatments along the Þrst DCA axis characterized by A. sanctaecrucis, H. pensylvanicus, H. herbivagus, and S. comma (Fig. 3). In 2004, both triticalealfalfa and alfalfa generally clustered toward H. pensylvanicus, H. herbivagus, P. lucublandus, and other less common species, whereas corn and soybean treatments tended to cluster more toward A. comma, P. pensylvanicus, A. sactaecrucis, and P. permundus (Fig. 4). For 2003 data, the Þrst axis explained 59% of carabid assemblage variance, whereas the second axis explained an additional 20%. For 2004 data, the Þrst DCA axis explained 62% of variance, whereas the second axis explained an additional 19%. DCA showed that carabid assemblages were different between 2003 and 2004 across all cropping treatments. In 2003, B. rapidum, H. pensylvanicus, H. herbivagus, and S. comma were generally more common than in 2004, when S. quadriceps, P. lucublandus, and P. permundus were more common. The Þrst DCA axis captured 26% of the variance in beetle assemblage, whereas the second axis captured an additional 52% of variation (Fig. 5). Species-Specific Effects. When the activity densities of individual species of carabid beetles in 2003 and 2004 were compared, little effect of rotation management regimen within a crop was detected. During 2003 and 2004, there were no differences in Tukey pairwise comparisons of individual speciesÕ activity density be-

Table 2. Activity density, species richness, Simpson’s evenness index, and Simpson’s diversity index estimates for adult carabid beetles in each cropping treatment and crop rotation in 2003 and 2004, Boone Co., IA

Cropping treatment Corn, 2-yr Corn, 4-yr Soybean, 2-yr Soybean, 4-yr Triticale-alfalfa, 4-yr Alfalfa, 4-yr Crop rotation 2-Yr 4-Yr

Activity densitya

Species richnessa

SimpsonÕs evenness

SimpsonÕs diversity

16.79 ⫾ 1.94a 28.34 ⫾ 2.08ab 37.22 ⫾ 4.47b 44.31 ⫾ 8.15b 36.97 ⫾ 7.64ab 47.69 ⫾ 9.39b

8.13 ⫾ 0.61a 9.88 ⫾ 0.91ab 8.38 ⫾ 0.68a 9.25 ⫾ 0.59ab 13.63 ⫾ 1.72b 11.63 ⫾ 0.65ab

0.37 ⫾ 0.04b 0.24 ⫾ 0.03ab 0.20 ⫾ 0.05a 0.18 ⫾ 0.02a 0.26 ⫾ 0.04ab 0.18 ⫾ 0.02a

0.62 ⫾ 0.05c 0.53 ⫾ 0.04bc 0.29 ⫾ 0.05a 0.35 ⫾ 0.05ab 0.61 ⫾ 0.07c 0.46 ⫾ 0.07abc

27.01 ⫾ 2.90A 39.33 ⫾ 3.65B

8.25 ⫾ 0.53A 11.09 ⫾ 0.72B

0.28 ⫾ 0.03B 0.21 ⫾ 0.01A

0.46 ⫾ 0.04A 0.49 ⫾ 0.02A

Values are cup per year ⫾ SE. Cropping treatment or crop rotation means followed by same letter within columns are not signiÞcantly different (P ⬎ 0.05); Tukey pairwise comparison test. a Activity density and species richness comparisons performed on ln(x ⫹ 1)-transformed data.

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Axis 1 Fig. 3. First two axes of detrended correspondence analysis of adult carabid assemblages in four replicate blocks of six cropping treatments in 2003. C2, corn, 2-yr; S2, soybean, 2-yr; C4, corn, 4-yr; S4, soybean, 4-yr; T4, triticale-alfalfa, 4-yr; A4, alfalfa, 4-yr. ASA, A. sanctaecrucis; BRA, B. rapidum; HHE, H. herbivagus; HPE, H. pensylvanicus; OTH, sum of all other species with ⬍50 specimens collected; PCH, P. chalcites; PLU, P. lucublandus; PPE, P. permundus; SCO, S. comma; SQU, S. quadriceps.

tween the 2- and 4-yr rotation corn treatments (Table 3). Between 2- and 4-yr rotation soybean, there was only one instance when the activity density of a carabid species was signiÞcantly different. In 2004, pitfall catches of S. quadriceps were 2.24 times higher in the 4-yr compared with the 2-yr rotation soybean (t ⫽ 2.96, df ⫽ 194, P ⫽ 0.04). This difference was not detected in 2003 but may have been caused by the overall low catches of S. quadriceps in 2003, making it difÞcult to detect the effects of management regimen (Table 3). Among all six cropping treatments, certain species of carabid beetles showed uniquely high patterns of activity density in the triticale-alfalfa and alfalfa treatments. In 2003, there were signiÞcantly more S. comma, A. sanctaecrucis, H. herbivagus, and other beetles collected in the triticale-alfalfa treatment compared with any other treatment (P ⬍ 0.05). In 2004, there were signiÞcantly more P. lucublandus and H.

Fig. 4. First two axes of detrended correspondence analysis of adult carabid assemblages in four replicate blocks of six cropping treatments in 2004. C2, corn, 2-yr; S2, soybean, 2-yr; C4, corn, 4-yr; S4, soybean, 4-yr; T4, triticale-alfalfa, 4-yr; A4, alfalfa, 4-yr. ASA, A. sanctaecrucis; BRA, B. rapidum; HHE, H. herbivagus; HPE, H. pensylvanicus; OTH, sum of all other species with ⬍50 specimens collected; PCH, P. chalcites; PLU, P. lucublandus; PPE, P. permundus; SCO, S. comma; SQU, S. quadriceps.

herbivagus collected in the alfalfa treatment compared with other treatments (P ⬍ 0.05; Table 3). Discussion Poecilus chalcites was the dominant species of adult carabid encountered in this study, comprising ⬎70% of the beetles captured in both 2003 and 2004. P. chalcites can consume a large variety of soft-bodied insects of economic importance (Larochelle and Lariviere 2003) and is common in agricultural Þelds of the midwestern United States (Kirk 1971, Esau and Peters 1975, Best and Beegle 1977, Best et al. 1981, Wiedenmann et al. 1992). The Þve most abundant adult carabid species sampled comprised ⬇85% of catches in both years. This result agrees with a worldwide review by Luff (2002) of 119 datasets of Carabidae in agricultural habitats where the Þve most abundant species averaged 84% of total pitfall trap captures. However, compared with natural habitats, this dominance structure is highly skewed and has been attributed to high levels of disturbances in agricultural production, including crop harvest and till-

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Fig. 5. First two axes of detrended correspondence analysis of adult carabid assemblages in 2003 (X) and 2004 (O). ASA, A. sanctaecrucis; BRA, B. rapidum; HHE, H. herbivagus; HPE, H. pensylvanicus; OTH, sum of all other species with ⬍50 specimens collected; PCH, P. chalcites; PLU, P. lucublandus; PPE, P. permundus; SCO, S. comma; SQU, S. quadriceps.

Table 3.

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age, which are intolerable for many carabid species (Thiele 1977). The strong effects of crop on carabid assemblage and activity density seen in this study support the results of numerous other researchers (Tonhasca 1993, Ellsbury et al. 1998, Zhang et al. 1998, Honek and Jarosik 2000, Ward and Ward 2001, Butts et al. 2003, Melnychuk et al. 2003, Witmer et al. 2003). Crops likely affect carabids through modiÞcation of microclimatic factors, such as temperature and humidity, and through disturbance factors such as harvest and tillage schedules (Thiele 1977, Holland 2002). Similar crop phenology and management may explain why the temporal activity density and assemblages of carabids were relatively similar in corn and soybean but dissimilar in those crops compared with triticale-alfalfa and alfalfa treatments. In addition to differences in carabid assemblages among crops, results of this study also emphasized yearly differences in carabid activity density. Of the nine most abundant species trapped in this study, six species, including S. comma, H. pensylvanicus, P. lucublandus, H. herbivagus, S. quadriceps, and P. permundus, were variably abundant between years. Other studies have also found high variability in carabid activity density among years (French and Elliott 1999, Irmler 2003, French et al. 2004). Over the course of 9 yr of pitfall trapping in one Þeld, Irmler (2003) found signiÞcant correlations between the activity density of approximately one half the species examined with either yearly precipitation or temperature. Weather variation may have been a factor in the current study with ⬇2.5 cm more rainfall per month between April and September in 2004 than in 2003 and daily high

Carabid species’ responses to crop rotation systems in 2003 and 2004 at Iowa State University’s Marsden Farm, Boone Co., IA

Speciesa 2003 Anisodactylus sanctaecrucis Bembidion rapidumb Harpalus herbivagus Harpalus pensylvanicus Poecilus chalcites Poecilus lucublandus Pterostichus permundus Scarites quadriceps Stenolophus commab Otherc 2004 Anisodactylus sanctaecrucis Bembidion rapidumb Harpalus herbivagus Harpalus pensylvanicus Poecilus chalcites Poecilus lucublandus Pterostichus permundusb Scarites quadriceps Stenolophus commab Other

Corn, 2-yr

Corn, 4-yr

Soybean, 2-yr

Soybean, 4-yr

Triticalealfalfa, 4-yr

Alfalfa, 4-yr

0.1 ⫾ 0.1a 0.0 ⫾ 0.0a 0.1 ⫾ 0.1a 1.2 ⫾ 0.4ab 10.6 ⫾ 2.5a 0.8 ⫾ 0.2 0.0 ⫾ 0 0.1 ⫾ 0.1 2.3 ⫾ 0.4a 1.1 ⫾ 0.1a

0.1 ⫾ 0.1a 0.0 ⫾ 0a 0.1 ⫾ 0.1a 1.9 ⫾ 0.6ab 17.2 ⫾ 0.6ab 1.5 ⫾ 0.6 0.8 ⫾ 0.5 0.9 ⫾ 0.3 2.4 ⫾ 0.5a 1.5 ⫾ 0.4a

0.0 ⫾ 0.0a 0.8 ⫾ 0.4ab 0.1 ⫾ 0.1a 0.6 ⫾ 0.2a 36.2 ⫾ 5.8bc 0.6 ⫾ 0.3 0.9 ⫾ 0.9 0.2 ⫾ 0.1 1.5 ⫾ 0.5a 1.7 ⫾ 0.2a

0.2 ⫾ 0.1a 0.1 ⫾ 0.1a 0.4 ⫾ 0.3a 1.0 ⫾ 0.2a 27.3 ⫾ 6.2bc 0.3 ⫾ 0.2 0.1 ⫾ 0.1 0.3 ⫾ 0.1 1.7 ⫾ 0.3a 2.0 ⫾ 0.5a

2.5 ⫾ 1.0b 0.7 ⫾ 0.3ab 2.8 ⫾ 0.5b 3.3 ⫾ 0.3b 14.8 ⫾ 3.9ab 0.6 ⫾ 0.2 0.1 ⫾ 0.1 0.6 ⫾ 0.2 10.1 ⫾ 4.6b 3.6 ⫾ 0.6b

0.3 ⫾ 0.1a 0.9 ⫾ 0.2b 0.4 ⫾ 0.2a 2.3 ⫾ 1.1ab 32.8 ⫾ 8.6c 0.9 ⫾ 0.4 0.1 ⫾ 0.1 0.2 ⫾ 0.1 0.6 ⫾ 0.2a 2.1 ⫾ 0.6a

0.9 ⫾ 0.5 0.0 ⫾ 0.0 0.0 ⫾ 0.0a 0.1 ⫾ 0.1 7.1 ⫾ 1.5a 2.2 ⫾ 1.0a 2.9 ⫾ 1.5b 1.5 ⫾ 0.4a 0.4 ⫾ 0.2ab 0.8 ⫾ 0.3ab

1.2 ⫾ 0.7 0.0 ⫾ 0.0 0.0 ⫾ 0.0a 0.1 ⫾ 0.1 19.4 ⫾ 2.1ab 0.9 ⫾ 0.1a 3.2 ⫾ 1.7b 2.1 ⫾ 0.7a 2.4 ⫾ 0.7b 1.0 ⫾ 0.4ab

0.2 ⫾ 0.1 0.0 ⫾ 0.0 0.1 ⫾ 0.1a 0.1 ⫾ 0.1 27.4 ⫾ 7.3b 0.7 ⫾ 0.3a 0.6 ⫾ 0.3ab 1.9 ⫾ 0.4a 0.4 ⫾ 0.3ab 0.6 ⫾ 0.3a

0.3 ⫾ 0.1 0.0 ⫾ 0.0 0.1 ⫾ 0.1a 0.1 ⫾ 0.1 45.8 ⫾ 14.8b 1.1 ⫾ 0.5a 2.4 ⫾ 0.3b 4.3 ⫾ 1.3b 0.3 ⫾ 0.1a 0.9 ⫾ 0.3ab

0.1 ⫾ 0.1 0.8 ⫾ 0.5 0.1 ⫾ 0.1a 0.4 ⫾ 0.1 26.7 ⫾ 13.3b 2.2 ⫾ 0.9a 0.1 ⫾ 0.1a 1.6 ⫾ 0.5a 0.5 ⫾ 0.2ab 2.4 ⫾ 1.0bc

0.4 ⫾ 0.1 0.1 ⫾ 0.1 0.8 ⫾ 0.4b 0.3 ⫾ 0.2 34.0 ⫾ 18.0b 12.9 ⫾ 3.4b 0.6 ⫾ 0.3ab 2.7 ⫾ 0.8ab 0.3 ⫾ 0.2a 2.7 ⫾ 1.0c

Values are mean no. cup per plot ⫾ SE. Means followed by same letter or without letters within rows are not signiÞcantly different (P ⬎ 0.05); Tukey pairwise comparison test. Statistcs performed on ln(x ⫹ 1)-transformed data unless indicated by b for speciesÕ data that were sqrt(x) transformed. c Other refers to the sum of all carabid species where ⬍50 specimens were collected over 2003 and 2004. a

February 2008


temperatures averaging 5.5⬚C cooler in 2004 during the warmest summer month of August (Midwest Regional Climate Center 2005). The small effect of reduced levels of fertilizer and herbicide applications on carabids was in contrast to our original hypothesis and the Þndings of other authors that reduced chemical inputs would lead to increased carabid activity density and species richness (Fan et al. 1993, Carcamo et al.1995). For example, Carcamo et al. (1995) found signiÞcantly higher activity density and species richness of carabids in an organic versus conventionally managed crop rotation where the main treatment differences were nitrogen and herbicide applications in the conventional rotation. One possible explanation for not seeing a greater effect of management in our study is that Þeld plots were not large enough (18 by 84 m) compared with the dispersal ability of carabids (Wallin and Ekbom 1988), allowing beetles to colonize plots from Þeld margins. Another explanation is that the increased soil disturbance to control weeds in the 4-yr corn and soybean negated any beneÞt for carabids of reduced herbicide and inorganic fertilizer inputs. It is also possible that differences between 2- and 4-yr corn and soybean treatments will develop over time as the rotation system progresses for more years and differences in soil characteristics develop (Grandy et al. 2006). In this study, carabid activity density and species richness were higher in triticale-alfalfa and alfalfa plots than in corn and soybean plots. Activity density and species richness were also generally higher in the 4-yr rotation than in the 2-yr rotation, because of the incorporation of triticale-alfalfa and alfalfa crops into the rotation (Table 2). This supports our original idea that increasing the diversity of crops in a rotation may support a greater number of carabid species. Species richness was enhanced, in particular, by species only trapped a few times. In a study of carabids in a variety of crops in the Netherlands, Booij (1994) also found that species richness was higher in crops with early and persistent ground cover. These results indicate that perennial crops such as alfalfa, and crops that form a canopy early in the growing season, such as triticale, may provide important refuges for carabid biodiversity without taking agricultural land out of production. In addition to emphasizing the importance of crop habitat for supporting carabid populations and the value of perennial crops for conserving species, results of this study have also emphasized the relative tolerance of carabids to noninsecticidal management practices such as herbicides, fertilizers, and mechanical weed control. However, further research over a broader geographic region will be necessary to test the robustness of these conclusions, which may depend on the underlying composition of carabid species in a region. Studies investigating carabid dispersal will greatly aid in understanding the scale at which results of this and other carabid studies are applicable; markrecapture and radio-telemetry have indicated that carabids are capable of moving tens of meters a day

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(Best et al. 1981, Wallin and Ekbom 1988), and ßight capacity among species is highly variable (Lindroth 1969). It will also be important to further study the factors structuring carabid assemblages across landscapes because it seems that the dominance structure of carabid assemblages can vary widely, even in similar habitats and over small geographic areas (Kirk 1971, 1975, Irmler 2003). Acknowledgments This research was funded by USDA NRI Grant 02-3532012175 and the Entomology and Agronomy Departments and the Plant Sciences Institute at Iowa State University. We thank K. Larsen for invaluable assistance in identifying carabid species, F. Menalled, P. Westerman, D. Sundberg, and A. Heggenstaller for ideas and assistance in collecting samples, and many summer employees who helped to collect data.

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