The Pennsylvania State University

The Graduate School

Department of Entomology

EFFECTS OF MANAGEMENT ON ARTHROPOD COMMUNITIES IN

ORGANIC AND CONSERVATION AGRICULTURAL SYSTEMS IN

PENNSYLVANIA AND MEXICO

A Dissertation in

Entomology and International Agriculture and Development

Ariel N. Rivers

 2016 Ariel N. Rivers

Submitted in Partial Fulfillment of the Requirements for the Degree of

Doctor of Philosophy

May 2016

The dissertation of Ariel N. Rivers was reviewed and approved* by the following:

Mary E. Barbercheck Professor of Entomology Dissertation Advisor Co-Chair of Committee

Edwin Rajotte Professor of Entomology Co-Chair of Committee

William Curran Professor of Weed Science

John Tooker Professor of Entomology

Gary Felton Professor of Entomology Head of the Department of Entomology

*Signatures are on file in the Graduate School

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ABSTRACT

Conservation agriculture, a system relying on crop rotations, mulch, and minimal soil disturbance, is widely recognized for benefits to soil quality, stabilizing crop yields, and altering plant-insect interactions. In particular, each of these practices affects the soil-dwelling arthropod assemblage in a particular way by influencing the microenvironment at the soil surface, with potential consequences for predatory and pest arthropods. To better understand the effects of conservation agriculture practices on local arthropod assemblages, biological control potential, and crop damage, here I compare two North American conservation agriculture cropping systems: a soybean (Glycine max L. Merr.), wheat (Triticum aestivum L.), and corn (Zea mays L.) rotation grown under organic management in central Pennsylvania, U.S.A, and a rotation of corn and wheat in central Mexico. In both systems, primary inversion tillage was reduced compared to conventional practices for the area. In Pennsylvania, the cash crops were no-till planted into a rolled cover crop mulch of either hairy vetch (Vicia villosa Roth) and triticale (x Triticosecale

Wittmack) planted together preceding corn, or cereal rye (Secale cereale L.) preceding soybean.

Additionally, in Pennsylvania, the cover crops were managed by a roller-crimper at three dates

(early, middle, or late) relative to standard dates for the area to allow for cash crop planting. In

Mexico, the cash crops were planted into the previous years’ crop residue, which was cut and left in the field after harvest.

In both systems, we measured arthropod activity-density by pitfall trap, biological control potential (predation) by implementing sentinel traps baited with live waxworms (Galleria mellonella F.), density of herbivorous arthropods at the soil surface, and damage by herbivorous invertebrates to the cash crops. Predatory arthropods in particular were affected by the conservation agriculture practices in both systems, with the type of residue affecting the activity- density, diversity, and function of particular predators, including ground and tiger beetles

(Coleoptera: Carabidae) in Pennsylvania, and ants in Mexico (Hymenoptera: Formicidae).

Predation rates were relatively high in both systems, with differences within systems depending on year, crop, and residue. Herbivore density and plant damage also depended on crop, but lower herbivore density correlated with higher predator activity-density in Pennsylvania. Likewise, certain types of crop damage, in particular cutting by lepidopteran larva, decreased with increased activity-densities of predatory arthropods. In Pennsylvania in particular, certain practices had a stronger influence on results than others; for instance, predatory arthropod activity-density was significantly greater in corn planted into a rolled mat of hairy vetch-triticale as compared to soybean planted into a rolled mat of cereal rye. In contrast, shallow high residue cultivation in corn and soybean was not a strong factor influencing the local arthropod assemblage at the time we sampled in Pennsylvania. The comparison of these two systems allows for an opportunity to understand the complexities of conservation agriculture and the potential for this system to conserve and augment predatory arthropods while contributing to pest control in low-input agricultural systems in North America.

TABLE OF CONTENTS

List of Tables ...... viii

List of Figures ...... xi

Acknowledgements ...... xiv

Chapter 1 Introduction ...... 1

Invertebrate crop pests in cover crop-based rotational no-till ...... 4 Arthropod generalist predators in agroecosystems ...... 9 Outline ...... 12 References ...... 15

Chapter 2 Cover crop-based rotational no-till augments predators and reduces plant damage during transition to organic management ...... 22

Abstract ...... 22 Introduction ...... 24 Materials and Methods ...... 28 Site description ...... 28 Experimental design and field operations ...... 28 Predatory arthropod community ...... 30 Biological control potential ...... 31 Plant damage and herbivores ...... 32 Data analysis ...... 33 Results ...... 36 Predatory arthropod community ...... 36 Biological control potential ...... 37 Plant damage and herbivores ...... 38 Discussion ...... 43 Conclusion ...... 49 Acknowledgements ...... 50 References ...... 51 Tables ...... 56 Figures ...... 61

Chapter 3 Cover crop management effects on Carabidae (Coleoptera) in a rotational no- till system in transition to organic production ...... 66

Abstract ...... 66 Introduction ...... 68 Materials and Methods ...... 71 Site Description ...... 71 Experimental Design and Field Operations...... 71 Data Collection ...... 73

Data Analysis ...... 75 Results ...... 77 Time in organic management ...... 77 Cover crop identity and management ...... 78 Discussion ...... 81 Conclusion ...... 86 Acknowledgements ...... 88 References ...... 89 Tables ...... 94 Figures ...... 100

Chapter 4 Cover crop species and termination alters arthropod community composition and sentinel predation in an organically managed reduced tillage cropping system ...... 104

Abstract ...... 104 Introduction ...... 106 Materials and Methods ...... 109 Site Description ...... 109 Experimental Design and Field Operations...... 109 Data Collection ...... 111 Data Analysis ...... 115 Results ...... 119 Predatory arthropod activity-density and diversity ...... 119 Carabidae activity-density and diversity ...... 120 Community composition of predatory arthropods ...... 121 Carabidae community composition ...... 122 Biological control potential ...... 123 Discussion ...... 125 Conclusion ...... 131 Acknowledgements ...... 132 References ...... 133 Tables ...... 137 Figures ...... 145

Chapter 5 Conservation agriculture affects arthropod community composition in a rainfed maize-wheat system in central Mexico ...... 152

Abstract ...... 152 Introduction ...... 154 Materials and methods ...... 157 Site description ...... 157 Experimental design and field operations ...... 157 Characterization of ground-dwelling arthropods ...... 159 Biological control potential ...... 160 Crop damage and yield ...... 161 Data analysis ...... 161 Results ...... 164 Characterization of ground-dwelling arthropods ...... 164 Biological control potential ...... 167

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Crop damage and yield ...... 168 Discussion ...... 169 Conclusion and recommendations ...... 174 Acknowledgements ...... 175 References ...... 176 Tables ...... 180 Figures ...... 184

Chapter 6 Conclusion ...... 188

References ...... 191 Appendix A Supplementary materials for Chapter 2 ...... 192 Appendix B Supplementary materials for Chapter 3 ...... 196 Appendix C Supplementary materials for Chapter 4 ...... 200 Appendix D Supplementary materials for Chapter 5 ...... 203

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LIST OF TABLES

Table 2-1. Management and sampling dates during the three years of the experiment...... 56

Table 2-2. Activity-densities and trophic groups of invertebrates captured by pitfall trap during the three years of the experiment...... 57

Table 2-3. Mean (± SEM) predatory group evenness during the three years of the experiment, in each of the cover crop treatments. According to post hoc tests of means, differences by year within each cover crop in that same row are indicated by lower case letters (p ≤ 0.05). Significantly different values between each cover crop within each year (column) are indicated by upper case letters. Values were arcsine square root transformed prior to analysis, but untransformed data are shown here...... 58

Table 2-4. Mean (± SEM) proportions per plot of damage by herbivores to cash crops planted into rolled cover crops, for both cover crop treatments combined and per cover crop termination date treatment. Damage assessments were conducted in a 0.813 m2 quadrat; damage reflects herbivory to corn in hairy vetch- triticale and to soybean in cereal rye. Within each cover crop (row), significantly different values (p ≤ 0.05) are indicated by lower case letters. Values were arcsine square root transformed prior to analysis, but untransformed data are shown here...... 59

Table 2-5. Mean (± SEM) slug and caterpillar densities per plot in 2012 and 2013 combined. Density assessments were conducted in a 0.813 m2 quadrat. Within each cover crop (row), significantly different values (p ≤ 0.05) are indicated by lower case letters. Significantly different values within each termination date treatment (column) are indicated by upper case letters. Values were log10 (x+1) transformed prior to analysis, but untransformed data are shown here...... 60

Table 3-1. Field operations and sampling dates by each entry of the crop rotation...... 94

Table 3-2. Total activity-densities by year of ground beetle species representing greater than 1% of total captures, during the three-year experiment...... 95

Table 3-3. Yearly mean (± SEM) across treatments of response variables tested by mixed effects models. Values with different letters within the same row are significantly different at p<0.05...... 96

Table 3-4. Mean (± SEM) per plot across treatments and years by crop of response variables tested by mixed effects models. Values with different letters in the same row are significantly different at p<0.05...... 97

Table 3-5. Accumulated three-year means (± SEM) for the significant response variables within each crop, tested by mixed effects models. Means with different letters in the same row are significantly different at p<0.05...... 98

Table 4-1. Relevant field operations and sampling dates during the experiment...... 137

Table 4-2. Accumulated activity-density of predatory arthropods captured by pitfall trap in each living and rolled cover crop treatment, for all termination date treatments...... 138

Table 4-3. Means (± SEM) per treatment of predator activity-density, evenness and richness tested by mixed model analysis, by cover crop, cover crop stage, and termination date. Different letters within the same row indicate significant differences (p ≤ 0.05) between cover crops at that stage and planting date according to Tukey’s post hoc test of means...... 139

Table 4-4. Accumulated numbers of adult carabid beetles representing greater than 1% of total by cover crop and cover crop stage...... 140

Table 4-5. Mean (± SEM) per treatment of carabid activity-density, evenness, and richness tested by mixed model analysis, by cover crop, cover crop stage, and termination date...... 141

Table 4-8. Response variables, model coefficients and ANOVA F and p-values for best fitting multiple linear regression models to predict predation, in each cover crop and stage. Significant explanatory variables for each cover crop and stage (p ≤ 0.05) are indicated in bold and italics...... 144

Table 5-1. Mean activity-density, richness, and evenness (± SEM) for arthropod trophic groups in maize prior to planting and after crop emergence, and mid- season visual assessments of arthropods on the soil surface...... 180

Table 5-2. Mean activity-density, richness, and evenness (± SEM) for arthropod trophic groups in wheat prior to planting and after crop emergence, and mid- season visual assessments of arthropods on the soil surface...... 181

Table 5-3. ANOVA table for the explanatory variables for the best fitting models in maize for predicting in-field sentinel predation. Models were selected by

Akaike’s Information Criteria (AIC) prior to planting and after crop emergence, and with time included as a random variable...... 182

Table 5-4. ANOVA table for the explanatory variables for the best fitting models in wheat for predicting in-field sentinel predation. Models were selected by Akaike’s Information Criteria (AIC) prior to planting and after crop emergence, and with time included as a random variable...... 183

LIST OF FIGURES

Figure 2-1. Mean (± SEM) predator activity-density (a.) and group richness (b.) in each year of the experiment. Within each graph, bars with different letters are significantly different at p ≤ 0.05 according to post hoc tests of means. Values were log10 (x+1) transformed prior to analysis, but untransformed data are shown here...... 61

Figure 2-2. Principal response curve (PRC) by crop across the three years of the experiment, with wheat set as the control treatment. Taxa on the right axis have a significant relationship to the principal response (species score ≥ 0.5). HVT = Rolled hairy vetch and triticale, Rye = Cereal rye...... 62

Figure 2-3. Mean proportion of damaged waxworms (± SEM) in sentinel predation assays during each year of the experiment, combined across cover crop and planting date treatments. According to post hoc tests of means, bars with different letters are significantly different at p ≤ 0.05. Values were arcsine square root transformed prior to analysis, but untransformed data are shown here...... 63

Figure 2-4. Correlations between the activity-density of predatory arthropods and the proportion of damaged waxworms (biological control potential) in HVT (F1,142 = 26.4, p < 0.001, r = 0.40), cereal rye (F1,142 = 8.2, p = 0.005, r = 0.234), and wheat (F1,142 = 11.95, p = 0.001, r = 0.279). Analyses included data for all years and experimental treatments. Activity-densities were log10 (x+1) and proportions were arcsine square root transformed prior to analysis, but untransformed data are shown here. HVT = Rolled hairy vetch and triticale...... 64

Figure 2-5. Significant (p ≤ 0.05) linear regressions relating predator activity-density to estimated early season soybean population in the rolled cereal rye cover crop treatment (a.); total caterpillar density in hairy vetch-triticale (HVT) (b.); and total slug density in cereal rye (c.) and in HVT (d.). In figure a, analyses included data for all years and experimental treatments in cereal rye. In figures b-d., densities were only measured in 2012 and 2013, and analyses were only conducted on those years for all experimental treatments within each cover crop. Predator activity- densities and caterpillar densities were log10 (x+1) prior to analysis, but untransformed data are shown here...... 65

Figure 3-1. Principal response curve (PRC) by crop across the three years of the experiment, with wheat set as the control treatment (a.). Note that axes are on different scales, and only one species had a significant relationship to the principal response (species score ≥ 0.5). HVT = Rolled hairy vetch and triticale, Rye = Cereal rye...... 100

Figure 3-2. Accumulated total activity-densities (n = 144) for the 5 most abundant species for each crop, summed for the three year duration of the experiment. HVT = Rolled hairy vetch and triticale, Rye = Cereal rye...... 101

Figure 3-3. Rarefaction curve by crop treatment. Overlapping 95% confidence intervals (not shown) indicate the total number of species captured in each crop

xii

are not significantly different. HVT = Rolled hairy vetch and triticale, Rye = Cereal rye...... 102

Figure 3-4. Principal response curve (PRC) for each year in rolled hairy vetch and triticale (HVT) by termination date treatment (early, middle or late relative to standard cover crop termination dates in central Pennsylvania), with the early termination date set as control. Note that axes are on different scales, and only two species had a response that matches the PRC (species score ≥ 0.5)...... 103

Figure 4-1. Mean (± SEM) per treatment (n = 16) of accumulated total predator activity-density by cover crop, cover crop stage, and termination date. Cover crop species are significantly different (p < 0.001). HVT = Rolled hairy vetch and triticale mixture; Rye = Cereal rye...... 145

Figure 4-2. Rarefaction curve for predatory arthropod taxa captured by pitfall trap in each living and rolled cover crop. HVT = Rolled hairy vetch and triticale, Rye = Cereal rye...... 146

Figure 4-3. Mean (± SEM) per treatment (n = 16) of accumulated total adult carabid activity-density by cover crop, cover crop stage, and termination date. HVT = Rolled hairy vetch and triticale mixture; Rye = Cereal rye...... 147

Figure 4-4. Rarefaction curve for carabids captured by pitfall trap in each living and rolled cover crop. HVT = Rolled hairy vetch and triticale, Rye = Cereal rye...... 148

Figure 4-5. Significant redundancy analyses (RDA) constrained by planting date and cultivation treatments for taxa (indicated by ᴼ) present in more than 25% of pitfall traps before and after cover crop management. Only planting date treatment (indicated by ▲) was significant (p ≤ 0.05) in each RDA. Axes indicate the percentage of variance explained by each axis; vectors represent significant environmental variables (p ≤ 0.05). HVT = HVT = Rolled hairy vetch and triticale; Rye = Rolled cereal rye. CEC-Mg = Percent of base saturation of Magnesium...... 149

Figure 4-6. Significant redundancy analyses (RDA) constrained by planting date and cultivation treatments for carabid species representing greater than 3% of accumulated activity-densities. Only planting date treatment (indicated by ▲) was significant (p ≤ 0.05) in each RDA. Axes indicate the percentage of variance explained by each axis; vectors represent significant environmental variables (p ≤ 0.05). HVT = HVT = Rolled hairy vetch and triticale; Rye = Rolled cereal rye. CEC- K: Percent of base saturation of Potassium...... 150

Figure 4-7. Mean (± SEM) proportion of predated waxworms by cover crop, cover crop stage, and termination date (n = 16)...... 151

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intervals for significant main effects (P ≤ 0.05). NT: No-till; CT: Conventional tillage; K: Residue retained in field; R: Residue removed from field. Full CA treatments are NT-K; full conventional are CT-R...... 184

Figure 5-2. Nonmetric multidimensional scaling (NMDS) ordination plots (3 dimensions with the first two axes shown, Bray-Curtis distance) for the maize arthropod community captured by pitfall trap prior to crop planting (a.) and after crop emergence (b.). Only predatory and herbivorous groups and significant environmental variables (P ≤ 0.05) are shown. Ellipses represent 95% confidence intervals for significant main effects (P ≤ 0.05). NT: No-till; CT: Conventional tillage; K: Residue retained in field; R: Residue removed from field. Full CA treatments are NT-K; full conventional are CT-R...... 185

Figure 5-3. Mean proportion of predator-damaged sentinel waxworms for both sampling dates (n = 80) in maize (a.) and wheat (b.). Treatments with different letters are significantly different by post hoc comparisons of means with Tukey’s honest significant difference test at P ≤ 0.05. Single dots represent potential outliers. Full CA treatments are no-till with residue retained; full conventional are conventional tillage with residue removed...... 186

Figure 5-4. Mean percent of damage by fall armyworm in maize (a.), and mean dry weight grain yield (kg ha-1) in maize (a.) and wheat (b.). Means with different letters are significantly different at the treatment level at P ≤ 0.05 according to Tukey honestly significant different test of means. Full CA treatments are no-till with residue retained; full conventional are conventional tillage with residue removed...... 187

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ACKNOWLEDGEMENTS

A number of people have contributed to the completion of this dissertation, to whom I owe an immeasurable amount of gratitude. I would like to thank my committee members, Drs.

Mary Barbercheck, Ed Rajotte, Bill Curran, and John Tooker, for their knowledge and guidance throughout my doctorate. I would especially like to thank Mary for tolerating my laughs and tears for four years, for providing me with the autonomy to follow my path, and for supporting me in all of my endeavors. I also want to thank Ed for the constant encouragement. All members of the

Barbercheck Lab also deserve my gratitude, Katie Ellis and Christy Mullen in particular, for providing me with field support, advice, and friendship. The ROSE team was hugely helpful as well, with a specific shout out to Clair Keene for help with navigating the project, and John

Wallace for help with data analysis.

The work I conducted in Mexico would not have been possible without the assistance of a number of people, including Drs. Deanna Behring and Melanie Miller-Foster, who provided ample support, advice, and encouragement. Drs. Nele Verhulst and Bram Govaerts were instrumental in helping me complete my work in Mexico, and I am so appreciative to them for the opportunity. The Sustainable Intensification/Conservation Agriculture team at CIMMYT also provided field support, laughter, food, and friendship, and I feel fortunate to have had the opportunity to work with that group. I also want to thank Dr. Gary Felton for his continued support of the INTAD program at Penn State (and, graduate students in Entomology in general).

This work would not have been possible without a graduate student grant from the

Northeast Sustainable Agriculture Research and Education Program, a Borlaug Fellowship in

Global Food Security, funding though the USDA National Institute of Food and Agriculture,

Organic Research and Extension Initiative (award number 2009-51300-05656), and financial support from the Department of Entomology.

Additionally, I cannot thank all of the people who have contributed to my well-being while at Penn State, as so many people have significantly impacted my time over the last four years. The Department of Entomology and the INTAD community deserve special recognition for tolerating my loud laughter. My level-headed colleague, Loren Rivera-Vega could always assuage any doubts I may have had about my capability to complete this dissertation, and I could not have done it without her. Any successes I may have from here on are hers to share. My neighbors, roommates, office mates, and peers are some of the greatest friends I could ask for, and I thank them for being on my team. Finally, I want to thank my family: Grampa and Gramma for showing me the world beyond Livermore, and helping me understand that it was my world too; my parents for helping me to be who I am; Leesh and Vic, for helping me laugh in ways that only siblings can; and Potún, for giving a girl all the love she could ask for.

Chapter 1

Introduction

Globally, the need to increase food, feed and fiber production to support a growing human population is a matter of great concern, but agriculture is frequently criticized for its contribution to environmental degradation (Crowder and Jabbour, 2014; Ratnadass et al., 2012).

Several management strategies have emerged that have the potential to reduce the environmental impacts of agriculture, including conservation agriculture in Latin America and elsewhere, and organically managed agriculture in the United States (Brouder and Gomez-Macpherson, 2014;

Delate and Cambardella, 2004; Erenstein et al., 2012; Jat et al., 2012; USDA, 2015a). Both management approaches propose reducing disturbances in the field (e.g., tillage, applications of agrochemicals), and increasing on-farm diversity (e.g., through crop rotations and companion cropping), and are associated with long-term benefits to agroecosystem quality while eventually resulting in yields comparable or higher to those of conventional systems (Booij, 1994; Crowder et al., 2010; Delate and Cambardella, 2004; Eyre et al., 2012; Ratnadass et al., 2012; USDA,

2015a; Verhulst et al., 2011).

While conservation agriculture is defined by the Food and Agriculture Organization

(FAO) of the United Nations as a series of practices (crop rotations, reduced soil disturbance, and retention of organic matter on the soil surface), growers are not legally mandated to perform any specific activities if they choose to pursue conservation agriculture (Knowler and Bradshaw,

2007). On the contrary, organic agriculture in the United States is regulated, and while the amount of time in organic agriculture largely dictates the productivity of the system, the initial three-year transition period poses unique challenges for growers adopting organic management practices (Delate and Cambardella, 2004; Lundgren et al., 2006; Tu et al., 2006). Managing pests

(i.e., insects, weeds, and diseases) is a particular area of concern, as many of the practices adopted during the transition may have yet to reach maximum efficiency (Carr et al., 2013; Delate and

Cambardella, 2004; Lundgren et al., 2006). As mandated by the National Organic Program

(NOP), organic growers must rely on a list of approved management practices (e.g., for pest management: crop rotations, mulches, tillage, and other cultural practices) to achieve and maintain organic certification, which is often associated with price premiums in U.S. markets

(Greene and McBride, 2015). Prior to receiving certification, growers must first manage their operations organically for a three-year transition period, during which the products cannot be sold as organic (USDA, 2015a). Without the price premiums, but with additional costs associated with certification, transitioning growers are in need of ways to maximize the pest control potential of their system, while minimizing labor and additional inputs (Delate and Cambardella, 2004;

Lundgren et al., 2006; Tu et al., 2006). Transitioning growers may thus experiment with the type and timing of field operations—crop rotations, planting date, mulches, and tillage—to manage pests, including both insects and weeds, so long as each practice is preapproved by their organic certifying agent (USDA, 2015a).

Pests and their management vary regionally for transitioning and organic growers, with weed management remaining a critical challenge for organic grain growers in the Mid-Atlantic region of the U.S. (Mirsky et al., 2012; Mischler et al., 2010a). Grain growers in this area typically use tillage for weed suppression, but due to concerns for reduced soil quality, and the cost and labor associated with tillage, some transitioning growers are seeking alternatives (Carr et al., 2013; Mirsky et al., 2012). Organic cover crop-based rotational no-till is thus emerging as a management system in organic agriculture, which allows for the reduction of tillage through the retention of organic mulches at the soil surface, drawing comparisons to conservation agriculture as practiced outside of the U.S. (Erenstein et al., 2012; Mirsky et al., 2012). In organic cover crop-based rotational no-till, as practiced by many growers in the Mid-Atlantic, growers plant a

2 cover crop in the fall, then manage that cover crop in the spring using a roller-crimper, an implement that simultaneously rolls the cover crop to the ground while “crimping” the stem to kill the plant (Mirsky et al., 2012; Mischler et al., 2010a; Ward et al., 2011). Rolled cover crops create a weed-suppressive mat through which weeds are unable to emerge. Weed seed is also less likely to reach the soil surface, which is protected by the barrier of the cover crop mat (Keene,

2015; Mirsky et al., 2012).

Many factors associated with cover crop-based rotational no-till will affect the efficacy of this management system for controlling weeds in organically managed agroecosystems.

Importantly, choice of cover crop and the length of time it is allowed to mature, the rotation of the cash crops implemented in the system (e.g., the order of the grain crops), planting date of cash crops (which is generally dependent on termination date of the cover crop), and the type and timing of tillage, are all areas warranting further research (Davis, 2010; Mirsky et al., 2013;

Mischler et al., 2010a, 2010b; Nord et al., 2012; Ward et al., 2011). Additionally, the impact of this system on arthropod communities during the organic transition remains largely unexplored, and is an area in critical need of research. For instance, a dense mat of organic matter at the soil surface has the potential to provide habitat for invertebrates, some of which are pests, with differential effects on the pest depending on the species of the crop from which the mulch was created (Hammond and Cooper, 1993; Mischler et al., 2010b). However, timing of cover crop termination by rolling will influence the amount of cover crop biomass at the soil surface, and thus the amount of habitat for any invertebrate pests, and termination can be timed to avoid particular pests in time (Hammond and Cooper, 1993; Mischler et al., 2010b; Nord et al., 2012).

Further, a rolled cover crop mat may also contribute to augmenting the predators of pest invertebrates, for example, the diverse and economically significant ground beetles (Coleoptera:

Carabidae) (Larochelle and Larivière, 2003; Nelson et al., 2004; Prasifka et al., 2006; Renkema et al., 2012). Thus, if the rolled mat of cover crops can contribute to augmenting a robust ground-

3 dwelling predator community, potential concern for an increase in invertebrate pests may be reduced.

While organic cover crop-based rotational no-till is promising as a management strategy for suppressing weeds during the transition to organic, further information is needed regarding the effect of the production system (the use of cover crops, rolling those cover crops, crop rotations, reducing tillage compared to standard organic systems, and timing of all of these activities) on arthropod communities. The potential for this system to augment crop invertebrate pests specifically is a major concern, but further studies are necessary regarding the interactions between pests, their potential predators, and the cropping system. In light of the need for these studies, here I review the significant invertebrate pests as affected by cover crop-based rotational no-till, and arthropod generalist predators in organic agriculture. This information then provides the basis for the research presented within this dissertation.

Invertebrate crop pests in cover crop-based rotational no-till

Agroecosystems are highly manipulated, unnatural systems in which a grower has the potential to choose any number of factors associated with the operation, e.g., location of a particular field in relationship to landscape features (slopes, tree lines, roads, etc.), planned biodiversity in the system (e.g., the crops she uses, crop rotations, companion cropping), the timing of operations, and the inputs she may use (Altieri, 1999; Gardiner et al., 2010; Trichard et al., 2014). However, growers do not have the option of choosing the inherent biodiversity within the system, including the crop pests which may feed on her crop, and because of the unnatural concentration of crop plants within the landscape, these crops are likely to experience herbivory from crop pests (Altieri, 1999). This idea, the resource conservation hypothesis, suggests that monocultures of a specific crop are subject to invasions by herbivores because of the nature of the

4 low diversity and readily available resources for native or introduced herbivores which may be present in the landscape (Letourneau, 1987; Root, 1973). While fields of concentrated crops are subject to herbivory, not all herbivores are crop pests, and not all crop pests will cause economic damage to a crop (Crawley, 2002; Letourneau, 1987; Price et al., 1980). However, several invertebrate pests cause damage in organic cropping systems in Pennsylvania, and the broader mid-Atlantic region, potentially resulting in reduced crop populations and yield (Curran and

Lingenfelter, 2015; Fleischer and Hutchinson, 2015; Mischler et al., 2010b).

In mid-Atlantic organic agronomic cropping systems, and especially in organic cover crop-based rotational no-till, early season invertebrate pests may be of particular concern due to the conditions provided by the system (e.g., high amounts of organic residue at the soil surface)

(Hammond and Cooper, 1993). Seeds are not protected by chemical seed treatments in organic systems, thus increasing the potential for feeding damage by seed pests, e.g., seedcorn maggots,

Delia platura Meigen (Diptera: Anthomyiidae), immediately after planting, which could result in reduced germination and lower crop populations (Judge and McEwen, 1970; USDA, 2015b).

Additionally, once the crop germinates, the small seedlings are subject to feeding damage by soil- dwelling invertebrates, including several species of slugs (Mollusca) and lepidopteran larva, e.g., black cutworms, Agrotis ipsilon Hufnagel and the fall armyworm, Spodoptera frugiperda J.E.

Smith (Lepidoptera: Noctuidae) (Douglas, 2012; Hammond and Cooper, 1993; Ibrahim and

Hower, 1979; Mischler et al., 2010b; Tillman et al., 2004). These invertebrates are all generalist herbivores, and will potentially feed on any number of grain crops, including corn (Zea mays L.) and soybeans (Glycine max L. Merr.), and their populations may be augmented or reduced by various practices within cover crop-based rotational no-till (Hammond and Cooper, 1993;

Hammond, 1991; House and Stinner, 1983; Ibrahim and Hower, 1979; Mischler et al., 2010b).

While seed pests have the potential to reduce crop populations in any agroecosystem, organic cover crop based-rotational no-till provides specific conditions which could favor the

5 development of seedcorn maggots (Hammond and Cooper, 1993; Ibrahim and Hower, 1979;

Judge and McEwen, 1970). These flies will feed on many field crop seeds and seedlings, and have been known to overwinter as adults, emerge in the spring, and may oviposit adjacent to small soybean plants when given a choice (Higley and Pedigo, 1984; Ibrahim and Hower, 1979).

To determine the effect of soil disturbance on seedcorn maggots, Hammond (1997) compared no- till systems with tilled, and systems with less frequent soil disturbances (i.e., no-till) had fewer adult seedcorn maggots compared to systems with more tillage events. However, when tillage is reduced in some systems, high levels of residue may remain on the soil surface, as is in the case in cover crop-based rotational no-till. Hammond and Cooper (1993) found that in such environments, the moist soils provided by the residues, as well as high levels of decomposing organic matter, provide an ideal environment for oviposition by adult females. Ibrahim and

Hower (1979) suggest that the specific reasons females may prefer to oviposit in moist, high residue environments at the base of soybeans is not well known, but that soybean germination may result in microbial activity that is attractive to the females. This is further supported by

Hough-Goldstein and Bassler's (1988) suggestion that any type of disturbance results in microbial activity which releases volatiles from bacteria and other microbes that adult females may find attractive. Thus, while reducing tillage may serve to reduce the populations of seedcorn maggots in cover crop-based rotational no-till, other aspects of the system may augment numbers of the crop pest. Likewise, while Hammond (1997) highlights that increasing tillage always increased seedcorn maggots in the corn-soybean rotation they studied in Ohio, he emphasizes that reducing tillage may augment the populations of other pests, including slugs and lepidopteran larva.

Throughout the mid-Atlantic, including in central Pennsylvania, slugs have become serious pests for field crop growers practicing no- and reduced tillage (Barratt et al., 1994; Byers and Calvin, 1994; Douglas and Tooker, 2012). Four species may occupy field crops in the region—the gray garden slug (Deroceras reticulatum Müller), marsh slug (Deroceras laeve

Müller), dusky slug (Arion subfuscus Draparnaud), and banded slug (Arion fasciatus Nilsson)— with the gray garden slug causing much of the economic damage in field crops (from here,

“slugs” will refer to any of these four slug species or combination of) (Barratt et al., 1994;

Douglas and Tooker, 2012; Howlett, 2012). Slugs may feed on seeds, as well as on leaf tissue between the veins of many field crops, which reduces the surface area of the leaf and potentially leads to reduced crop growth (Byers and Calvin, 1994; Douglas and Tooker, 2012). While some crop plants may grow out of the damage, yield may still be reduced (Barratt et al., 1994; Byers and Calvin, 1994; Douglas and Tooker, 2012). Because slugs prefer moist, cool weather, and activity may be reduced in warm temperatures, the conditions provided by cover crop-based rotational no-till in the early season is ideal for augmenting slug numbers (Barratt et al., 1994;

Willis et al., 2008). However, slugs are hermaphrodites, with individual, but inconsistent, patterns for mating depending on species (Douglas and Tooker, 2012; Willis et al., 2008). Thus, because eggs, juveniles, and adults may be present throughout the growing season, tillage can contribute to the control of slugs regardess of when it occurs (Barratt et al., 1994; Hammond, 1997; Willis et al., 2008). Slugs may also feed on a number of non-crop resources, including crop residues, soil organic matter, and various weed species, all of which may be readily available in cover crop- based rotational no-till, further increasing the potential for higher slug densities in such a system

(Cook et al., 1996; Hammond and Stinner, 1987; Kozłowski and Kozłowska, 2008; Miles et al.,

1931; Mirsky et al., 2012; Pallant, 1972).

Like slugs, lepidopteran larvae may benefit from the increase in favorable habitat associated with cover crop-based rotational no-till. A number of lepidopteran larvae may become pestiferous in organic agroecosystems, but black cutworms and fall armyworms may be augmented by aspects of the system, including the increase in favorable habitat, and these species are frequently present in central Pennsylvania (Curran and Lingenfelter, 2015; Fleischer and

Hutchinson, 2015; Schipanski et al., 2014). In particular, Mischler et al. (2010b) suggest that high

7 abundances of black cutworms at early termination dates of a hairy vetch cover crop by rolling resulted in reduced stands of corn planted into the rolled cover crop. Adult black cutworms oviposit in crop fields prior to planting, and the generalist caterpillars thus emerge into a readily available food source once the crop is growing (Sherrod et al., 1971). The specific factors affecting oviposition are still not well understood, however, moist areas with abundant plant cover are expected to play a role in female preferences, with some weeds being preferred as an oviposition site over corn or wheat (Triticum aesitivum L.) (Busching and Turpin, 1976; Sherrod et al., 1971). Additionally, newly emerged black cutworm larvae may survive for several days by eating residues prior to emergence of the crop plant (Showers et al., 1985). Some researchers have suggested that cover crops may provide additional habitat in which adult lepidopterans may oviposit, but minimal research exists which quantifies the impact of cover crops on lepidopteran larvae, especially in organically managed cropping systems (Showers, 1997). Thus, the response of lepidopteran larvae to organic cover crop-based rotational no-till is an additional area warranting further research.

In spite of the potential of cover crop-based rotational no-till to augment several invertebrate crop pests, the presence of these pests does not always result in economic damage to crops. A number of factors may affect the potential for an herbivorous insect to become pestiferous, but in many agroecosystems, including in organic systems, generalist arthropods have the potential to suppress the numbers of these pests (Lundgren and Fergen, 2011; Prasifka et al.,

2006). Like the herbivores reviewed here, many important predatory groups, including spiders and harvestmen (Arachnida: Araneae, Opiliones), ground and rove beetles (Coleoptera:

Carabidae, Staphylinidae), and ants (Hymenoptera: Formicidae) may also all be augmented or affected in various ways by organic cover crop-based rotational no-till.

Arthropod generalist predators in agroecosystems

In contrast to the resource conservation hypothesis, which suggests that the concentrated resources provided by agricultural monocultures result in prime habitat for herbivores (Root,

1973), the natural enemies hypothesis suggests that in more diverse systems, an increase in crop and non-crop resources will result in an increase in predators and parasitoids, and thus, greater pest control (Andow, 1991; Letourneau, 1987; Root, 1973). Similarly, diversity-stability theory suggests that more diverse systems are more resilient to any type of disturbance (e.g., tillage, or invasion by invertebrate pests) (Andow, 1991; Elton, 1958; Odum, 1953; McCann, 2000). As such, the diverse habitat associated with cover crop-based rotational no-till (i.e., crop rotations and mulch at the soil surface), may reduce the potential for pest invasions, augment arthropod generalist predators, and increase the stability of the system through time.

A number of generalist predators are present in any given agroecosystem; however, for a number of reasons, the ground and tiger beetles (Coleoptera: Carabidae) are considered one of the more important groups of generalist predators (Lövei and Sunderland, 1996; McCravy and

Lundgren, 2011). With over 2,400 species in America north of Mexico, carabids are easily identifiable due to the availability of keys and ample museum collections (Larochelle and

Larivière, 2003). While gaps exist in the knowledge associated with individual species, much is known about the natural history of the family (Larochelle and Larivière, 2003). Consequently, carabids are often used as indicators of environmental quality, as a diverse and abundant community may be indicative of a habitat able to provide multiple ecosystem services, while being somewhat resilient to disturbances (Andow, 1991; Booij, 1994; Szysko et al., 2000; Ward et al., 2011). Carabids not only suppress invertebrate pests, but many also feed on weed seeds, further contributing to pest control in organic agroecosystems (Lövei and Sunderland, 1996;

Ward et al., 2011). Although some may be herbivores, e.g., Stenolophus comma (Fabricius) has

9 been noted to feed on seed corn, many carabids are omnivores, feeding on any variety of available resources, including lepidopteran larvae, insect eggs, slugs, and Collembola. S. comma is in fact mostly carnivorous (Douglas et al., 2014; Larochelle and Larivière, 2003). Carabids are also associated with human activities and easily able to colonize novel habitats in agroecosystems, and as a result, some have been introduced from other continents through human activities with positive effects on pest control (Larochelle and Larivière, 2003; Symondson et al.,

2002). However, the colonizing efficiency of some carabids should not negate the need for conservation of this important family, and agroecosystems, especially those managed as organic, can play a significant role in providing habitat for the group, and subsequently, benefits for pest control (Booij, 1994; Eyre et al., 2012; Lundgren and Fergen, 2011). Further, since they primarily reside and forage on the soil surface, carabids are heavily impacted by agricultural field activities

(Larochelle and Larivière, 2003).

With specific requirements for crop rotations, fertility and soil management, and pest control, organically managed agriculture may augment carabids in a number of ways (Letourneau and Bothwell, 2008; USDA, 2015a). Eyre et al. (2012) identified a benefit to carabid activity- density and diversity associated with organic fertility and pest management as compared to what they define as conventional, suggesting that the reduction in chemical pesticide applications and an increase in organic matter at the soil surface were both contributing factors (Bengtsson et al.,

2005; Letourneau and Bothwell, 2008). The effect of crop species was actually more influential than the production system on the ground beetle community, suggesting that specific crops and the order in which they are planted may be equally as important (Eyre et al., 2012). Individual ground beetle species will respond differently to different crops based on their own behavior, e.g. individual preferences for prey, microclimates, habitat structure, foraging efficiency, stage at overwintering etc., and a species may thus choose among adjacent crops depending on when a crop is planted, treated for pests, fertilized, the way it shades the soil, etc. (Döring and Kromp,

2003; Lundgren et al., 2006; Prasifka et al., 2006; Russon and Woltz, 2014; Ward et al., 2011).

Several researchers have suggested, for example, that cereal grains provide a benefit to carabids because of the relatively fewer number of disturbances compared to corn or soybean, as cereal grains are not as frequently treated for pests or tilled, and may be relatively undisturbed during times that spring-breeders are active, or other species are overwintering (Booij, 1994). Thus, understanding the interactions between various ground beetle species and the cropping system is necessary to fully maximize the potential for this group to serve as pest control agents in an organically managed system.

The biological control potential of other generalist predators also depends on their presence in the field, which has been correlated to increased habitat availability and complexity in some agroecosystems (Riechert and Bishop, 1990; Stinner and House, 1990). In testing the effect of wheat straw mulch on the activity of spiders and their food resources, Schmidt and Rypstra

(2010) found that more complex habitats—those with both soybeans and a wheat straw mulch compared to plots with only wheat straw, only soybeans, or bare soil—featured less variable microclimates with lower average temperatures and higher humidity than less complex habitats.

These conditions could provide a more stable environment for generalist predators, many of which prefer moist and cool habitats (Jorgensen and Toft, 1997; Larochelle and Larivière, 2003;

Shearin et al., 2008; Stinner and House, 1990). Similarly, plots with both soybeans and wheat straw mulch contained higher numbers and diversity of spiders and their food resources than any of the less structurally diverse plots (Schmidt and Rypstra, 2010). Much research has focused on the local habitat as a resource for spiders (Gardiner et al., 2010), but increasingly, researchers are focusing on non-habitat resources as factors affecting the predatory ability of spiders (Kuusk and

Ekbom, 2010; Nyffeler and Sunderland, 2003). For example, extrafloral nectaries and pollen are both receiving attention as important food items for spiders, which have long been thought of as exclusively predatory, and these alternative food items may increase spiders’ ability to find and

11 capture prey items (Carvell et al., 2015; Heil, 2015; Peterson et al., 2010). As such, the additional habitat available to spiders in cover crop-based rotational no-till, as well as the additional resources provided by cover crops (pollen, extrafloral nectaries), may contribute to augmenting spiders and other natural enemies, and their potential to serve as predators of crop pests.

Many other generalist predators are relevant within cover crop-based rotational no-till, and may be affected by any number of management activities associated with the system. While the conservation of predatory taxa is an important ecosystem service of organic management, the conservation of the interactions between predators and their prey items (specifically, invertebrate crop pests), is particularly important for organic growers (Altieri, 1999; Memmott et al., 2007).

Few researchers have evaluated the potential for predators to suppress invertebrate crop pests in organic transitions, and especially in organic cover crop-based rotational no-till, but we generally understand that as the abundance of the predators increase, so too does their predation on insects and weed seeds (Lundgren et al., 2006; Thomas et al., 2009; Winqvist et al., 2012). In some cases, predators may feed on each other (intraguild predation), resulting in a reduced biological control potential in agroecosystems, but in highly diverse environments with small farms, like that of central Pennsylvania, this may be less of a concern (Finke and Denno, 2002; Letourneau,

1987; Prasad and Snyder, 2006; Snyder et al., 2006; Straub et al., 2008). Regardless, the interactions between predators, their prey, and the cropping system warrants further research, especially during the organic transition in cover crop-based rotational no-till systems.

Outline

This dissertation further explores arthropod predator and pest dynamics in high residue, reduced tillage, corn-based agroecosystems. Chapters 2 through 4 evaluate the effect of a cover crop-based rotational no-till system during the transition to certified organic management on

12 arthropod communities in central Pennsylvania. We implemented a rotation of corn – soybean – wheat, with a hairy vetch (Vicia villosa Roth) planted with triticale (x Triticosecale Wittmack) cover crop mixture preceding corn, and a cereal rye (Secale cereale L.) cover crop preceding soybean. The cover crops were managed by a roller-crimper to allow for cash crop planting at three dates relative to standard cover crop control dates for the area (early, middle, and late), and we implemented a high residue cultivation treatment annually in corn and soybean. In contrast,

Chapter 5 evaluates the arthropod communities in a long-term conservation agriculture trial in central Mexico, in which conventional pest control tactics (i.e., insecticides and herbicides) are typically implemented. That system incorporated a corn-wheat rotation, and compares conventional tillage for the area with zero tillage, and retention or removal of the previous years’ crop residues. Combined, this research provides implications for conservation of arthropod predators and management of crop pests in organically and conventionally managed agroecosystems.

Chapter 2 of this dissertation focuses on the ground-dwelling arthropod community, with a particular emphasis on generalist predators and the important herbivores (slugs and lepidopteran larva). This chapter also evaluates the effect of cover crop-based rotational no-till on the biological control potential of the system (the potential for predators to control insect pests) and damage by herbivores to the cash crops (corn and soybean). Additionally, I evaluated the role of predators in minimizing crop damage.

Chapter 3 focuses on the important predatory group, Carabidae, and the changes in the abundance and diversity of this family as a result of organic management during the transition and cover crop-based rotational no-till.

Chapter 4 explores the ground-dwelling arthropod community before and after cover crop management by rolling in the final year of the experiment. For this chapter, I focus on the predatory arthropods, including carabid species, biological control potential (predation), and

13 evaluate different environmental factors, e.g., cover crop height, soil moisture, which affect the community composition and predation.

In Chapter 5, I provide the first examination of the effect of the long-term conservation agriculture trial in central Mexico on predatory arthropods, herbivores, predation, and insect damage to corn and wheat.

Finally, Chapter 6 draws comparisons between the two agroecosystems, discusses implications for growers, and provides recommendations for future research.

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Chapter 2

Cover crop-based rotational no-till augments predators and reduces plant damage during transition to organic management

Abstract

In many regions of the United States, organic grain growers are interested in minimizing soil disturbance associated with tillage to reduce labor and other management costs, and limit the detrimental effects on soil quality. Cover crop-based rotational no-till, a system in which cash crops are no-till planted into a mat of rolled cover crops, is emerging as an option for growers to meet multiple objectives. However, aspects of the system warrant further study, including the potential for the rolled mat to provide habitat for invertebrates, especially when this system is implemented during the mandated three-year transition to certified organic management. As part of a larger initiative to evaluate cover crop-based rotational no-till in central Pennsylvania, we studied the effect of time in organic management, cover crop species and cover crop termination date on predatory arthropod activity-density, diversity and community composition during the three-year transition to organic management. We also assessed biological control potential of the system, herbivore density, and damage by herbivorous invertebrates to two cash crops, corn (Zea mays L.) and soybean (Glycine max (L.) Merr.), with the full entry, three-year rotation comprised of corn, soybean, and wheat (Triticum aestivum L.). A mixture of hairy vetch (Vicia villosa Roth) and triticale (x Triticosecale Wittmack) preceded corn, and cereal rye (Secale cereale L.) preceded soybean as winter cover crops. The overwintering cover crops were terminated by rolling on three dates (early, middle, and late), and corn and soybean were no-till planted through the mat created by the rolled cover crops. Wheat was planted on a single date in each year into

22 tilled soil. Predatory arthropods were sampled by pitfall trap two weeks after termination of the two cover crops, and in mid-June in wheat. At a time corresponding with pitfall trapping, biological control potential was measured by sentinel assays containing live larvae of the greater waxworm (Galleria mellonella F.). Caterpillar and slug densities were assessed in corn and soybean by searching the ground for living specimens. Corn and soybean population and damage by invertebrates were assessed approximately three weeks after cash crop planting. Predatory arthropod activity-density, richness, and biological control potential increased in the third year of organic management (p ≤ 0.05). Herbivore density was highly variable, but lower caterpillar densities in hairy vetch-triticale, and lower slug density in both rolled cover crop treatments, correlated with a significant increase in predator activity-density, regardless of year or planting date treatment (p ≤ 0.05). Delaying cover crop termination date (cash crop planting date) had no effect on the predatory arthropod community, but herbivore density was lower, and delaying termination date increased cutting damage in certain crop years (p ≤ 0.05). An intermediate termination date may provide a balance between increasing predator activity-density and achieving herbivore pest control.

Introduction

In many regions of the United States, organic and transitioning grain growers are interested in minimizing soil disturbance associated with frequent inversion tillage to reduce labor and other management costs, and to limit the detrimental effects of soil disturbance on soil quality

(Mirsky et al., 2012; Teasdale et al., 2007). In organic grain production systems, tillage serves multiple purposes; for example, growers may use various forms of tillage to incorporate crop residues and fertilizers, prepare seed beds, and control weeds. In spite of the many uses of tillage, frequent inversion tillage can destroy soil structure, reduce biodiversity, and contribute to losses of fertile topsoil by erosion (Hammond and Stinner, 1987; Kladivko, 2001; Lewis et al., 2011).

As tillage is one of the primary forms of weed control in organic systems, weed management remains a significant challenge for growers choosing to operate in no-till and reduced tillage systems (Bond and Grundy, 2001; Mirsky et al., 2012). An emerging approach to reducing tillage in organic grain production involves the use of cover crop-based rotational no-till, a system in which winter cover crops are rotated with annual grain crops, and tillage occurs on only a semi- regular basis (Teasdale et al., 2007). However, appropriately timing management activities, including terminating the winter cover crop and, subsequently, planting the cash crop, is essential to maximize the efficacy of cover crop-based rotational no-till (Hammond and Cooper, 1993;

Mischler et al., 2010).

Winter cover crops provide a variety of benefits and are increasingly recognized for their potential to contribute to pest control, for example, by providing habitat for beneficial insects that contribute to pest insect and weed control (Blubaugh and Kaplan, 2015; Shearin et al., 2008;

Ward et al., 2011). In a cover crop-based rotational no-till system, the winter cover crops may be managed by a roller-crimper, an implement which rolls the crop to the ground while crimping the stems to kill the crop (Carr et al., 2013; Mirsky et al., 2012). The rolled cover crop creates a

24 mulch layer at the soil surface, and the subsequent cash crop is no-till planted into the rolled cover crop mulch. Provided the winter cover crop produced enough biomass prior to termination, the mulch can effectively contribute to weed suppression prior to cash crop canopy closure by limiting the potential for weeds to emerge through the mulch or preventing weed seed from contacting the soil surface (Mischler et al., 2010).

When appropriately managed, cover crop-based rotational no-till may provide corn and soybean yields comparable to county averages in the mid-Atlantic, however, minimizing variability in the system remains a challenge (Mirsky et al., 2012). In particular, cash crop planting date must be early enough to allow for an appropriate length of growing season for the cash crop in the temperate mid-Atlantic, but late enough to allow for effective control of the cover crop (Mirsky et al., 2009; Mischler et al., 2010). Likewise, invertebrates in the early- season, including lepidopteran larvae and seedcorn maggots (Delia platura Meigen, Diptera:

Anthomyiidae), may reduce crop establishment by feeding on unprotected seeds or seedlings

(Hammond and Cooper, 1993; Mischler et al., 2010; USDA, 2015a). The high residue environment created by the rolled cover crop mat may provide additional sites for oviposition and refuge from predators for crop pests, while also providing favorable a microclimate (Hammond and Cooper, 1993; House and Alzugaray, 1989; Karban et al., 2013; Landis et al., 1987; Sherrod et al., 1971). For example, Mischler et al. (2010b) evaluated four termination dates of a hairy vetch (Vicia villosa Roth) cover crop by rolling, into which corn (Zea mays L.) was no-till planted in a cover crop-based rotational no-till system in central Pennsylvania. These researchers suggested that later termination dates of the cover crop resulted in higher corn populations and yields (Mischler et al., 2010). They attribute crop losses at the two earliest termination dates to high incidence of black cutworm (Agrotis ipsilon Hufnagel, Lepidoptera: Noctuidae), which feed on corn at the soil surface, killing the plant (Mischler et al., 2010).

At later termination and planting dates, a combination of factors may prevent losses by

25 early-season pests in cover crop-based rotational no-till, one of which is the presence of ground- dwelling generalist predatory arthropods, such as spiders (Araneae) and ground and tiger beetles

(Coleoptera: Carabidae) (Clark et al., 1994; Hammond and Cooper, 1993; Lundgren and Fergen,

2011). In organic agriculture, the presence of these predators is vital, as they can minimize economic damage by invertebrate pests, and contribute to weed suppression by consuming weed seeds (Larochelle and Larivière, 2003; Lundgren et al., 2006; Shearin et al., 2008). While organic growers can manipulate the agroecosystem at the landscape level to provide additional habitat for these predators, e.g., by creating beetle banks between fields, within field management can have significant impacts on the predators, thereby affecting their potential to contribute to pest suppression (Chaplin-Kramer et al., 2011; Clark et al., 1993; Lundgren et al., 2006). For example, reducing tillage and other in-field disturbances have been associated with augmented predator numbers, as tillage can bury the predators or force them to migrate out of the field (House and

Stinner, 1983; Kladivko, 2001). Growers may also manipulate the timing of key activities, e.g., planting of the cash or cover crops, to maximize the availability of habitat available to predators during important periods of activity, like oviposition (Blubaugh and Kaplan, 2015; Thorbek and

Bilde, 2004; Ward et al., 2011). Finally, organic management is strongly associated with increased abundance of generalist predators, in part due to the mandated ban on the use of synthetic chemical pesticides according to the U.S. National Organic Program standards

(Crowder et al., 2010; Letourneau and Bothwell, 2008; USDA, 2015b).

While management practices may impact predatory arthropods directly, conditions created in cover crop-based rotational no-till may also affect predator communities indirectly by providing habitat resources that differ from those systems without high levels of residue at the soil surface (Prasifka et al., 2006; Schmidt and Rypstra, 2010). Henneron et al. (2015) evaluated a long-term (14 year) conservation agriculture trial in northern Europe, a system similar to cover crop-based rotational no-till in that crop residues are retained on the soil surface and with

26 minimal soil disturbance, for the effect on soil organisms as compared to low residue systems typical for the area. The predatory arthropod groups Araneae, Carabidae, and Staphylinidae

(Coleoptera) responded in a strong, positive way to conservation agriculture practices compared to conventional management, which involved regular stubble plowing (10 cm depth) and chemical fertilization that the conservation agriculture treatments did not receive (Henneron et al.,

2015). Additionally, the increased presence of generalist predators in agroecosystems significantly corresponds with an increased consumption of insect eggs, lepidopteran larva

(caterpillars), and weed seeds (Grieshop et al., 2012; Lundgren et al., 2006; Pfannenstiel and

Yeargan, 2002; Shearin et al., 2008).

One area that warrants further research in organic agriculture, and especially in cover crop-based rotational no-till, is the effect that predators have on the potential to reduce crop damage (Letourneau and Bothwell, 2008). It is well established that organic management contributes to the conservation of generalist predators, and that these predators will feed upon pest insects and weed seeds. However, less is known regarding the potential for predators to control herbivorous invertebrates, thus contributing to pest suppression in early-season crop populations. As such, as part of a larger initiative to evaluate the potential for implementing cover crop-based rotational no-till grain production in the mid-Atlantic region of the U.S. during the mandated three-year transition to certified organic management, we assessed the effects of this approach on the ground-dwelling arthropod community. We hypothesized that with increased time in organic management, cover crop-based rotational no-till would augment ground-dwelling generalist predatory arthropods, with concomitant increases in biological control potential, and a reduction in early-season damage to cash crops (corn and soybean) planted into rolled cover crops

(hairy vetch-triticale and cereal rye, respectively). We also evaluated the effect of two cover crop treatments in comparison to winter wheat in our experiment, and termination of the two cover crops by rolling at three different termination dates at the time of corn and soybean planting.

Materials and Methods

Site description

This research was conducted at the Russell E. Larson Agricultural Research Center in

Centre County, Pennsylvania (40°43′23″N, 77°55′44″W) at 376 meters above sea level (USGS,

2014). Mean annual precipitation in the area was approximately 1006 mm between 1981 and

2010, with approximately 547 mm of precipitation on average during the growing season of May through October (NOAA, 2014). Mean monthly temperatures ranged between -2.7 and

22.3°Celsius (C), with an annual mean of 10.1°C in the years 1981 through 2010 (NOAA, 2014).

The total area of the Reduced-Tillage Organic Systems Experiment (hereafter, ROSE, for convenience) site is approximately 4 hectares, and during the experiment, the site was managed for transition to certified organic production (USDA, 2015d). Soils at the site are representative of the Hagerstown Soil Series according to the United States Department of Agriculture, Natural

Resources Conservation Service soil classification system, a silt loam classified as prime farmland (Soil Survey Staff, 2014).

Experimental design and field operations

We designed the experiment to test the effect of multiple agronomic practices on insect and weed dynamics in an organic cover crop-based rotational no-till system (Mirsky et al., 2013).

The three-year experiment (2011 to 2013) consisted of four blocks of a full entry design, with the total cropping area in each block amounting to 6020 m2 (2006 m2 per crop). Each of the four blocks within the experiment contained three cropping strips representing one crop in the three- year rotation, with three cash crops—corn (Zea mays L.), soybean (Glycine max (L.) Merr.), and wheat (Triticum aestivum L.)—planted in every growing season during the years 2011 to 2013.

Crops were rotated annually with a cover crop with a complete rotation as follows: corn, cereal rye (Secale cereale L.), soybean, winter wheat, and hairy vetch (Vicia villosa Roth) planted together with triticale (× Triticosecale Wittmack). The cover crops were planted into tilled ground in the fall, with a seeding rate of 34 kg seed ha-1 each for hairy vetch and triticale, and 189 kg seed ha-1 for cereal rye. In the spring, we rolled the cover crops prior to, or at the time of, planting of corn or soybean (Table 3–1). Corn and soybean were no-till planted into the residue mat created by the rolled cover crop at 84,000 seeds ha-1 and 556,000 seeds ha-1, respectively.

Winter wheat was seeded at a rate of 163 kg seed ha-1 into soil that was moldboard plowed, disked, and field cultivated following harvest of soybean. The wheat grain was then harvested as a cash crop the following summer, with wheat residues remaining in the field (Table 2–1).

Within each planting date subplot, the plots were further split to compare the effects of high-residue inter-row cultivation as compared to no cultivation in the corn and soybean (335 m2 per cultivation treatment). The high residue cultivator is equipped with a no-till coulter to cut the residue, which is followed by a single 50 cm wide sweep to sever emerged weeds while leaving the surface residue relatively undisturbed. The cultivation treatment was used to supplement the weed suppression provided by the cover crop mulch and each plot was cultivated twice about one week apart (Table 3–1). In soybean, the treatments receiving cultivation were planted in 76 cm rows, while the no-cultivation treatments were planted in 38 cm rows. Both corn treatments were planted in 76 cm rows. Because we did not evaluate all treatments within the ROSE experiment, the final design for our study resulted in four replicate plots per block for each crop, termination date and cultivation treatment, with each plot measuring 18.3 m by 9.1 m (167 m2).

Predatory arthropod community

To characterize the arthropod community, we employed a series of pitfall traps in the early part of the May – October growing season. We deployed two pitfall traps in each 18.3 m by

9.1 m plot, consisting of a one-liter plastic deli container buried level with the soil surface into which we placed a 50 mL plastic specimen cup, filled with 30-mL ethylene glycol as a killing agent and preservative. Inside the opening of the deli container, we placed a funnel (114 mm in diameter) to facilitate insect movement into the specimen cup and to exclude larger animals from entering the trap (Weeks and McIntyre, 1997). Traps remained open for 72 hours, after which the samples were removed from the field and brought to a laboratory for processing and identifications.

For all termination dates of the cover crops, we timed pitfall trapping to occur approximately one week after the emergence of corn and soybean in the years 2011-2013, which occurred approximately two weeks after rolling hairy vetch-triticale, and three weeks after rolling cereal rye. We conducted a single pitfall-trapping event approximately one month prior to wheat harvest, regardless of the termination date treatments of the crops preceding wheat. At the time of trapping in the rolled cover crops, the soil was completely covered by a dense mat of cover crop residue created by the roller-crimper. In the treatments planted with hairy vetch-triticale (this combination of plants hereafter abbreviated as HVT), hairy vetch represented the bulk of the mulch biomass, with the hairy vetch stems creating a tangled mat of dense organic matter which could be easily lifted off the soil surface as a single piece. In the cereal rye treatments, the cereal rye stems were rolled parallel to the crop rows, with each stem aligned in relatively the same direction as other stems. Both corn and soybean were at growth stage V1 at the time of pitfall sampling (Nafziger, 2009; Nordby, 2004).

After trapping, we removed the pitfall traps from the field and returned the pitfall

30 samples to the laboratory, removed all arthropods from the specimen cups, preserved them in

80% ethanol, and counted and identified each arthropod to family in the case of the following groups: Cantharidae, Carabidae, Coccindellidae, Elateridae, Histeridae, Staphylinidae

(Coleoptera); Geocoridae, Nabidae, Reduviidae (Hemiptera); Formicidae (Hymenoptera); and

Gryllidae (Orthoptera). All other groups were identified to order. We classified the dominant trophic group of each arthropod according to their predominant feeding preferences described in the literature, by the following designations: predatory, feeding primarily on animal materials; omnivorous, feeding on both animal and plant materials; herbivorous, feeding primarily on plant materials, including crop seeds; and decomposers, feeding primarily on decomposing plant matter and other detritus (Johnson and Triplehorn, 2004; Lundgren, 2009). For the purposes of our research, we consider arthropods which may feed on weed seeds as predators, as they could provide a beneficial ecosystem service to organic agriculture, including species within Gryllidae,

Formicidae, and Carabidae (Lundgren, 2009). We classified microarthropods as Collembola and mites (Acari), and macroarthropods as all other groups, a distinction we chose to emphasize due to the different ecological roles of these groups, and because we only identified Collembola and mites in the final two years of the experiment (Kladivko, 2001; Weeks and McIntyre, 1997). We archived voucher specimens at the Frost Entomological Museum at the Pennsylvania State

University.

Biological control potential

To determine the biological control potential of the generalist arthropod predator community on populations of early-season pests, we conducted in-field assays with traps baited with live last-instar waxworm larvae (Galleria mellonella F.). We used two non-targeted traps

(sentinel traps) in each treatment plot, consisting of a cardboard substrate baited with five lab-

31 reared larvae affixed with a 1.5 x 2.5 cm length of double-sided hem tape (Aleene’s ©). The cardboard substrate was placed on the ground, and surrounded by a cylinder of 19-gauge hardware cloth to exclude larger animals, and covered by a petri dish painted white to protect the waxworms from rain. The traps were placed in close proximity to pitfall traps, and left in the field for the 24 hours prior to each pitfall-trapping event. After 24 hours, we collected the cards and returned to the laboratory to assess feeding damage by invertebrates. We counted the number of damaged and undamaged larvae to determine the proportion of predated waxworms. Trapping was repeated in the same manner in the 24 hours directly after each pitfall-trapping event.

Plant damage and herbivores

In each year of the experiment, we assessed early-season crop population and damage by plant-feeding invertebrates to the two cash crops (corn and soybean) planted into the rolled cover crops (HVT and cereal rye, respectively). In a total area of 0.813 m2 in each plot, we counted the total number of cash crop seedlings to obtain crop population. In each crop, we counted the number of plants exhibiting damage by slugs (Mollusca), as indicated by feeding between leaf veins with an intact epidermis (Douglas and Tooker, 2012). We also counted damage by chewing invertebrates on each seedling, which would result in complete removal of leaf tissue, generally on leaf margins. Finally, we counted the number of plants that had experienced feeding by cutting insects (typically, lepidopteran larva). In corn, the damage would result in a series of holes in the whorl of the small plant. In soybean, we classified cutting damage as plants that were completely chewed off at the base where the plant emerged from the soil. In each case of damage, we counted the total number of plants exhibiting any amount of damage, but we did not classify the amount of damage on each plant. We timed the crop population and damage assessments to cash crop stage, and not to calendar date; corn plants were typically at growth stage V4 during damage

32 assessments (Nafziger, 2009), and soybean plants were typically at growth stage V1 (Nordby,

2004).

In the final two years of the experiment, we also completed absolute assessments of the total number of caterpillars (lepidopteran larvae) and slugs at the soil surface within the same size quadrat (0.813 m2), although we conducted these prior to the damage assessments. We timed these assessments with a flight of true armyworm (Pseudaletia unipuncta Haworth, Lepidoptera:

Noctuidae) in 2012, and approximately 5 days prior to pitfall trapping in 2013. We gently searched through the rolled cover crop residue and on the soil surface to count all caterpillars and slugs within each quadrat. In 2012, the caterpillars were identified to species in the field, but not in 2013 as the numbers were much lower in that year. Corn plants were typically at V2, and soybeans at VC at the time of sampling (Nafziger, 2009; Nordby, 2004).

Data analysis

We conducted all analyses in R: A language and environment for statistical computing (R

Core Team, 2013). We used linear mixed models (function lme) in the nlme package (Pinheiro et al., 2013) to determine differences between treatments and predatory arthropod activity-densities

(summed for all taxa we identified as predatory for each treatment), predator group richness,

Smith-Wilson evenness (Smith and Wilson, 1996), biological control potential (sentinel predation rates), and herbivore densities (caterpillar and slug in the final two years of the project). Foliar predators were captured at rates of less than 1% of total macroarthropods, and were thus included in the various response variables for total predators, and for the herbivorous invertebrates, all analyses were conducted on the sum total of each group (caterpillars or slugs). For each response variable, we specified a model incorporating the following fixed effects: year, cover crop, and cover crop termination date (early, middle, and late), and interactions between those variables.

We included block nested within sampling Julian day as a random effect to control for differences in sampling date, as we wanted to separate differences attributed to termination date treatment and those we anticipated because of greater arthropod activity later in the growing season.

Additionally, because we sampled each treatment on different days, non-treatment factors may have affected pitfall captures and predation, e.g., weather.

We conducted linear mixed models to determine treatment effects on crop populations and damage by herbivorous invertebrates to the corn and soybean cash crops. For each damage assessment, we specified a linear model including year, cover crop, termination date, and the interactions as fixed effects, and block nested within Julian day for the date we sampled crop damage as a random effect. Corn and soybean are planted at different rates due to crop characteristics, and we analyzed the crop populations separately (with year, termination date, and the interaction as fixed effects). Crop populations were converted to estimated number of plants per hectare prior to analysis, and we conducted analyses on the proportion of total plants exhibiting damage for each herbivory assessment.

In all of our mixed models, we had the potential to explore the effect of cultivation on the arthropod community as a component of this research, but in preliminary analyses, cultivation treatment was consistently insignificant as an explanatory variable affecting the arthropod community, likely due to the timing of when cultivation occurred in relationship to our sampling efforts (in late July in corn and soybean annually, and we always conducted pitfall sampling prior to that). Thus, all analyses were collapsed across cultivation treatment. We conducted post hoc pairwise tests of means between each treatment level using Tukey’s honest significant difference test. All count data was log10 (x + 1), except crop populations which met model assumptions, and all proportions were square root arcsine transformed to meet assumptions of normality and equality of variances (Gotelli and Ellison, 2004; Ives, 2015; Kutner et al., 2005).

To test the relationship between predatory arthropod activity-density and biological control potential (the proportion of waxworms exhibiting feeding damage in our sentinel assays) we used linear regression and obtained a Pearson’s correlation coefficient, indicated as r in the results (Kutner et al., 2005). For each crop, we conducted separate analyses using the transformed values of total predator activity-density and proportion of damaged waxworms. We used the same analyses to relate total predatory activity-density to the density of slugs and caterpillars, crop populations, and plant damage.

We used principal response curves (PRC) using the prc function in the vegan package of

R to determine macroarthropod community responses through time during the experiment, excluding Collembola and mites in these analyses (Oksanen et al., 2015; R Core Team, 2013; van den Brink and ter Braak, 1999). To compare changes in the whole macroarthropod community through the three years of the experiment, we conducted PRCs on the main effect of crop treatment, with wheat set as control to characterize differences between the standing crop and the two rolled cover crops. Taxa were only included in the analyses if they were present in greater than 25% of the samples, a threshold we selected to exclude disproportionate effects of rare species (McCune and Grace, 2002). We transformed the species activity-densities using the

Hellinger transformation prior to conducting the PRCs (Legendre and Gallagher, 2001; van den

Brink and ter Braak, 1999), and we used a Monte Carlo permutations (4999 permutations) to test the overall significance of each PRC. For the visualized PRC, we show only species with weights greater than or equal to an absolute value of 0.5, which indicates a strong response to the treatments analyzed in the PRC (van den Brink and ter Braak, 1999).

Results

Predatory arthropod community

During the three years of the experiment, we captured a total of 13,688 predatory macroarthropods by pitfall trap (Table 2–2), with the most abundant taxa including Araneae

(spiders, 16.8% of total arthropods excluding Collembola and mites), Staphylinidae (Coleoptera,

8.7%), Carabidae (Coleoptera, 6.5%), Formicidae (Hymenoptera, 5.5%), and Opiliones (5.1%).

Year (F2,354 = 21.0, p < 0.0001), cover crop treatment (F2,354 = 57.8, p < 0.0001), and cover crop termination date (F2,374 = 5.7, p = 0.004) were all significant in our linear mixed model. However, according to post hoc test of means, differences between means were only significant for year

(Figure 2–1a), with mean (± standard error) predatory arthropod activity-density significantly higher in 2013 (46.9 ± 1.9) than in both 2012 (23.9 ± 0.95) and 2011 (24.1 ± 1.7).

The diversity of predatory arthropods, as measured by richness and Smith-Wilson evenness of predatory taxa, was similarly affected by treatments (Figure 2–1b, Table 2–3).

Richness (number of predatory orders or families) was significantly affected by year (F2,354 =

20.2, p < 0.0001) and cover crop (F2,354 = 9.4, p = 0.000). At the experimental site, according to post hoc test of means, mean (± SEM) predator richness per plot significantly (p ≤ 0.05) increased by the third year of the experiment (6.4 ± 0.1) compared to 2012 (4.8 ± 0.1) and 2011 (4.6 ± 0.1).

The full mixed model for predator evenness included significant terms for year (F2,354 = 6.0, p =

0.003), cover crop treatment (F2,354 = 4.5, p = 0.012), and the interaction between year and cover crop (F4,354 = 23.5, p < 0.0001). The differences were primarily driven by the significant (p ≤

0.05) differences between year within cereal rye (Table 2–3), with mean predator evenness higher in 2013 (0.89 ± 0.02) than both 2012 (0.48 ± 0.02) and 2011 (0.54 ± 0.03).

According to principal response curves, the arthropod community was significantly affected by our cover crop treatment (F6,423 = 22.6, p < 0.001, Figure 2–2). Time in organic management (year) accounted for 11.0% and cover crop treatment accounted for 21.6% of the variance within the macroarthropod community, respectively. The compositional changes through time were due to the differences in the principle responses of five groups: Araneae (species score:

-0.88), unidentified Coleoptera (-0.87), Formicidae (0.94), Gryllidae (0.61), and Opiliones (0.49), with the latter three groups responding to wheat, and the first two groups associated with HVT and cereal rye. The macroarthropod community responded similarly to the two rolled cover crops

(HVT and cereal rye), but by the third year of the experiment, the macroarthropod communities in the two rolled cover crops are more similar to wheat.

Biological control potential

Biological control potential, as measured by proportion of live sentinel waxworms exhibiting feeding damage, indicated that moderate levels of predation occurred throughout the experimental site. In mixed model analyses, only year significantly affected predation (F2,354 =

17.7, p < 0.0001), with an increase in predation from 2012 to 2013 (p < 0.05, Figure 2–3) according to post hoc tests of means. Cover crop treatment and termination date did not significantly affect predation across the three years of the experiment. However, total predatory arthropod activity-density significantly correlated with the proportion of damaged waxworms in each cover crop treatment during the three years of the experiment, with a general increase in the amount of predation as the activity-density of predators increased (Figure 2–4). The correlation was strongest in HVT (F1,142 = 26.4, p < 0.001, r = 0.396), and weaker but still significant in both cereal rye (F1,142 = 8.2, p = 0.005, r = 0.234), and in wheat (F1,142 = 11.95, p = 0.001, r = 0.279).

Plant damage and herbivores

In assessments of early-season cash crop populations, we analyzed the two cash crops

(corn planted into rolled HVT and soybean planted into rolled cereal rye), separately due to the difference in planting rate of the two cash crops. In both cash crops, year was the only significant response variable affecting mean estimated number of corn (F2,108 = 11.3, p < 0.0001) and soybean (F2,108 = 11.3, p < 0.0001) plants per hectare. In the rolled HVT cover crop, mean estimated number of corn plants per hectare (± SEM) was significantly higher (p ≤ 0.05) in both

2011 (80,103.2 ± 1274.0) and 2013 (72,329.7 ± 1,656.2) than in 2012 (50,708.0 ± 1,888.7). In the rolled cereal rye cover crop, mean soybean populations per hectare (± SEM) were significantly different (p ≤ 0.05) in every year of the experiment according to post hoc tests of means, with mean estimated number of soybean plants per hectare higher in 2013 (506,565.2 ± 9,323.7) than

2012 (420,438.9 ± 15,541.6) and 2011(353,772.0 ± 14,844.1).

In our assessments of herbivory by invertebrates, the proportion of cash crop plants exhibiting slug (Mollusca) damage in a 0.813 m2 quadrat was higher than the proportion of plants exhibiting either chewing or cutting (Table 2–4). However, due to our methods, we cannot say if the amount of damage on each plant differed; a plant with slug damage may have experienced less total damage by slugs than damage by chewing or cutting insects. Slug damage on the two cash crops varied by year (F2,208 = 24.4, p < 0.0001), with significantly higher (p ≤ 0.05) mean proportion of damage per plot in 2012 (0.78 ± 0.02) as compared to both 2011 (0.64 ± 0.03) and

2013 (0.59 ± 0.02). Cover crop treatment also affected damage by slugs (F1,208 = 68.9, p <

0.0001), with a significantly higher (p < 0.0001) mean proportion of slug damaged corn plants in the rolled HVT (0.80 ± 0.02) than damaged soybean in the rolled cereal rye (0.54 ± 0.02). Slug damage was also affected by cover crop termination date (F2,208 = 6.7, p = 0.002, Table 2–4), with significantly more slug damage (p = 0.01) in the late termination date (0.77 ± 0.02) as compared

38 to the early date (0.56 ± 0.03). Similarly, the density of slugs at the soil surface was higher in

2012 (a total of 414) than in 2013 (a total of 57). As such, slug density was significantly affected by year (F1,143 = 157.5, p < 0.0001, Table 2–5) and cover crop treatment (F1,143 = 17.3, p =

0.0001), with significantly more mean slugs per 0.813 m2 (p < 0.0001) in 2012 (4.3 ± 0.3) than

2013 (0.6 ± 0.1), and significantly more slugs (p < 0.0001) in rolled HVT (3.2 ± 0.4) than in rolled cereal rye (1.7 ± 0.3).

Compared to the other types of damage to the cash crops that we measured, the proportion of plants (both corn and soybean combined) exhibiting cutting damage was lower

(Table 2–4), but was also significantly affected by year (F2,208 = 34.0, p < 0.0001) and by the cover crop treatment into which the cash crops were planted (F1,208 = 565.5, p < 0.0001). Cutting damage in all treatments combined at the experimental site significantly decreased (p < 0.001) in each year, with a mean proportion of damaged plants (± SEM) of 0.19 (± 0.02) in 2011, 0.17 (±

0.02) in 2012, and 0.13 (± 0.01) in 2013. A significantly higher proportion (p < 0.0001) of corn planted into rolled HVT exhibited leaves with cutting damage (0.27 ± 0.01) compared to soybean planted into rolled cereal rye and cut at the soil surface (0.06 ± 0.00). Several other response variables significantly affected the proportion of plants with cutting damage: cover crop termination date (F2,208 = 6.6, p = 0.002); the year by termination date interaction (F2,208 = 34.7, p

< 0.0001); cover crop by termination date (F2,208 = 6.5, p = 0.002); and year by cover crop and termination date (F4,208 = 20.7, p < 0.0001, Table 2–4). The proportion of corn plants with cutting damage decreased with later cover crop termination dates in both 2012 and 2013, but increased with termination date in 2011. Within each year, post hoc tests of means only indicated a significant difference (p ≤ 0.01) between the mean proportions of corn plants with cutting damage at different termination dates in 2011 (Table 2–4), with a higher proportion of corn plants with cutting damage in the late (0.43 ± 0.01) and middle (0.40 ± 0.01) termination dates as compared to the early (0.09 ± 0.02). The mean proportion of soybean plants cut at the soil surface was more

39 variable across the years and planting dates, with only a significant difference (p ≤ 0.01) in 2011 between the late (0.04 ± 0.01) and middle (0.13 ± 0.08) planting dates, and no difference between the early termination date and the either two treatments (0.7 ± 0.01).

The mean proportion of cash crops damaged by chewing invertebrates was also significantly affected by year (F2,208 = 254.5, p < 0.0001); mean (± SEM) proportion of plants in all treatments with chewing damage was significantly higher (p < 0.0001) in 2013 (0.55 ± 0.02) compared to both years, and 2012 (0.48 ± 0.02) compared to 2011 (0.15 ± 0.01). Proportion of cash crops damaged by chewing also varied by cover crop treatment (F1,208 = 12.8, p = 0.000,

Table 2–4), with a higher mean proportion (p < 0.0001) of corn planted into rolled HVT (0.42 ±

0.02) exhibiting chewing damage than the mean proportion of soybean planted into rolled cereal rye (0.36 ± 0.02). The mean proportion of cash crops exhibiting chewing damage also increased when these cash crops were planted into rolled cover crops terminated at later dates (F2,243 = 9.6, p = 0.001), with both the late (0.49 ± 0.03) and middle (0.37 ± 0.02) termination dates exhibiting a higher proportion of plants affected by chewing (p < 0.003) than the early termination date

(0.32 ± 0.02). The effect of year and termination date also depended on the cover crop, however, as the full interaction between the three response variables was also significant (F4,208 = 11.3, p <

0.0001), with the proportion of chewed corn plants increasing with each delay in termination date of HVT in 2012 (p < 0.02), and increasing from the early to late termination of HVT date in 2013

(p < 0.01, Table 2–4). The mean proportion of soybean plants cut at the soil surface significantly increased (p < 0.01) with each delay in termination of cereal rye in 2011, and in 2013, was significantly higher in the late termination date of cereal rye than in the middle and the early termination dates (Table 2–4).

Caterpillar (Lepidoptera larvae) density at the soil surface (in 0.813 m2) in the final two years of the experiment differed by year. In 2012, we identified a total of 285 caterpillars in the absolute assessments, with the two most abundant groups being true armyworms (Pseudaletia

40 unipuncta Haworth), at 61.4% of the total, and variegated cutworms (Peridroma saucia Hubner) at 13.0% of the total. In 2013, we only counted a total of 20 caterpillars. Year was thus significant in the model (F1,143 = 184.9, p < 0.0001), with more mean caterpillars (±SEM) per plot in 2012

(3.0 ± 0.4) than in 2013 (0.2 ± 0.1, p < 0.0001). Cover crop treatment also affected caterpillar density (F1,143 = 34.2, p < 0.0001, Table 2–5), with significantly more mean caterpillars (±SEM) per plot in rolled HVT (2.5 ± 0.4) than in rolled cereal rye (0.7 ± 0.1, p < 0.0001). Cover crop termination date also significantly influenced caterpillar density (F2,8 = 35.0, p = 0.0001), with the two later termination dates (middle: 1.1 ± 0.2; late: 0.2 ± 0.1) both having significantly less total mean caterpillars (±SEM) than the early termination date (3.4 ± 0.6, p ≤ 0.01). Within each crop, the same patterns held, with a decrease with each delay in termination date (cover crop by termination date interaction: F2,143 = 5.7, p = 0.004), and a decrease from 2012 to 2013 (cover crop by year interaction: F1,143 = 5.8 p = 0.017, Table 2–5).

For all treatments and years combined, we conducted linear regressions to determine relationships between predatory arthropods and various metrics related to crop population, herbivory, and herbivore density, with varied results. The estimated number of soybean plants in the rolled cereal rye cover crop (Figure 2–5a) was positively and significantly correlated with the number of predatory arthropods (F1,142 = 31.3, p < 0.0001, r = 0.425), and the proportion of soybean plants cut at the soil surface (planted into cereal rye) was also significantly and negatively correlated with predator activity-density (F1,142 = 4.8, p = 0.03, r = -0.182). In rolled

HVT, caterpillar density was significantly and negatively correlated with the activity-density of predatory arthropods (F1,94 = 29.1, p < 0.0001, r = -0.486, Figure 2–5b). Lower density of slugs in the final two years of the experiment significantly correlated with greater activity-density of all predatory arthropods in both rolled HVT (F1,94 = 25.6, p < 0.0001, r = -0.462) and rolled cereal rye (F1,94 = 31.1, p < 0.0001, r = -0.498, Figure 2–5c,d). However, the proportion of chewed corn planted into rolled HVT (F1,142 = 38.1, p < 0.0001, r = 0.460) and chewed soybean planted into

rolled cereal rye (F1,142 = 41.6, p < 0.0001, r = 0.476) were both significantly and positively correlated with predator activity-density.

Discussion

As part of a larger initiative to evaluate the potential for cover crop-based rotational no- till to reduce tillage in organically managed grain cropping systems of the mid-Atlantic region of the U.S., we studied the effect of this system on predatory arthropods and herbivory in central

Pennsylvania. We hypothesized that with increased time in organic management, cover crop- based rotational no-till would augment ground-dwelling generalist predatory arthropods, with concomitant increases in biological control potential, and a reduction in damage to cash crops

(corn and soybean) planted into rolled cover crops (hairy vetch-triticale and cereal rye, respectively). We also evaluated the effect of two different cover crops as compared to winter wheat, and termination of the two cover crops by rolling at three different termination dates

(early, middle, and late) in preparation for corn and soybean planting. Time in organic management (year) was consistently significant for many of our response variables, including predatory arthropod activity-density and diversity, biological control potential, and herbivore density and feeding damage on corn and soybean. The effects of cover crop species and termination date were highly variable depending on the year and the response variable.

In accordance with our first hypothesis, predatory arthropod activity was affected by time in organic management, with a significant increase in total predatory arthropod activity-density and predator group richness by the third year of the experiment across the cover crops, and higher predator evenness in the rolled cereal rye cover crop than in rolled hairy vetch planted with triticale. Others have identified similar trends in organically-managed agroecosystems, with an increase in abundance and diversity of many different invertebrate groups with time in organic management (Bengtsson et al., 2005; Jonason et al., 2011). The elimination of synthetic chemical pesticide use in organic agriculture, including the absence of insecticide-treated seeds, may contribute to these increases (Letourneau and Bothwell, 2008; USDA, 2015a, 2015b). We did not

43 have a chemical-based control with which to compare our organically-managed treatments to determine the relative contribution of this aspect of organic management to changes in predatory arthropod activity-density and diversity, but we can infer from other studies conducted in central

Pennsylvania. As an example, Leslie et al. (2010) evaluated the effect of three different chemical insecticide treatments (a neonicotinoid seed treatment, a soil applied pyrethroid, and a combination of both) on non-target Coleoptera in field corn at the Russell E. Larson Agricultural

Research Center in 2003 and 2004. More carabids were captured during the growing season in an insecticide-free control as compared to the three chemical control strategies, with a significant difference in the second year of the experiment between the insecticide-free control (mean of approximately 5 carabids per trap) and all other treatments (mean of approximately 2 to 4 beetles per trap) (Leslie et al., 2010). For comparison, in corn planted into the rolled hairy vetch-triticale, we captured a mean (± SEM) of 2.9 (± 0.4), 5.0 (± 0.5), and 11.4 (± 0.9) carabids in 2011, 2012, and 2013, respectively. Leslie et al. (2010) attribute the reduced abundance of carabids in the insecticide treatments directly to the insecticides, and this negative response has been confirmed by numerous lab studies showing toxicity of both neonicotinoids (Douglas et al., 2014; Mullin et al., 2005) and pyrethroids to carabids and other predatory arthropods (Coats et al., 1979; Croft and Whalon, 1982; Guedes et al., 2016). While we did capture more carabids in our experiment than Leslie et al. (2010), even as compared to their insecticide-free control, a variety of factors beyond chemical use differed between their experiment and our own (e.g., year, crop rotations, tillage regimes, cover crops). Regardless, the comparison suggests that an in-field reduction in chemical insecticide use in central Pennsylvania may contribute to augmenting predatory arthropod abundance.

In addition to the restriction on synthetic pesticide use, other requirements of certified organic management may contribute to an increase in invertebrate numbers, e.g., the requirements for crop diversity in time through crop rotations (USDA, 2015c). Different crops will provide

44 different resources for predatory arthropods, e.g., habitat, supplemental prey (Birkhofer et al.,

2008; Diehl et al., 2012), and we therefore hypothesized that any changes in the predatory arthropod community through time would depend on the cover crop treatment. According to post hoc tests of means, predator activity-density and richness were not significantly different between cover crops, as expected. However, because sampling was timed relative to cover crop termination, which was dependent on cover crop phenology, we sampled arthropods in each cover crop on a different date. We used a fairly conservative mixed model to account for any potential differences associated with those sampling dates, i.e., sampling date was included as a random factor in the mixed models to account for any non-treatment related differences in sampling dates, like weather and insect phenology. As such, if sampled on the same date, we may have detected differences in the predator activity-density and richness for each rolled cover crop.

While cover crop species did not affect activity-density or richness of predatory arthropods, predator group evenness varied between the two rolled cover crops, with significantly higher evenness in hairy vetch-triticale as compared to cereal rye in 2012, and the opposite trend in 2013. This result indicates that activity-densities of certain predatory arthropods may differ between cover crops even though the total activity-density may not differ significantly. Many of the same taxa are present in both cover crops (Table 2–2), but certain taxa are present in higher numbers in hairy vetch-triticale than in cereal rye, e.g., the carabids. However, while activity- densities are generally lower in cereal rye, in 2013, two less common taxa, including Gryllidae

(Orthoptera) and Nabidae (Hemiptera) were present in higher numbers in cereal rye than in hairy vetch-triticale, and likely contributed to the more even community in cereal rye in 2013 as compared to rolled HVT. Similarly, principal response curve indicated that certain taxa responded to cover crop treatments, with Formicidae, Gryllidae, and Opiliones responding to wheat, and unidentified Coleoptera and Araneae responding to hairy vetch-triticale. A number of factors may drive these interactions between specific arthropod taxa and crops; for example, while the rolled

45 hairy vetch-triticale mat may provide refuge space and prey for Araneae (Birkhofer et al., 2008;

Schmidt and Rypstra, 2010), Formicidae may prefer the ability to move about unencumbered on the bare ground in wheat (Andersen, 2000; Grieshop et al., 2012; Thompson, 1990). Additionally, where residue at the soil surface is abundant, predators have adequate niche space to occupy and prey to capture within a local area, potentially reducing the mobility of these predators and affecting the efficiency of trap captures in each cover crop (Lang, 2000; Lundgren et al., 2006).

In spite of the differences in the arthropod community between cover crops, especially in the first two years of the experiment, the arthropod communities in each cover crop began to converge in the final year of our experiment (Figure 2–2). Additionally, compared to the first year of our experiment, biological control potential as determined by sentinel predation was also higher in the third year of our experiment as compared to the first, as we hypothesized (Figure 2–

3). Linear regressions show a relationship between predator activity-density and predation in each cover crop (Figure 2–4). It is thus apparent that regardless of the crop species in which a predator resides, the arthropods we identified as predatory in this system may contribute to biological control. With the potential for cover crop-based rotational no-till to provide habitat for early- season pests (Mischler et al., 2010), the provision of biological control is an important ecosystem service of this system. Pitfall traps are thought to overestimate the densities of carabids and

Lycosidae (Araneae), while underestimating staphylinids and Linyphiidae (Araneae) in complex environments, potentially resulting in no relationship between pitfall trap captures and biological control potential (Hatten et al., 2007; Lang, 2000; Lundgren et al., 2006). As such, the relationship between pitfall captures of predatory arthropods and predation is an important result in our experiment.

We hypothesized that time in organic management would be associated with a decrease in herbivory and herbivore density. Only the proportion of corn and soybean exhibiting cutting damage consistently decreased with each year of organic management during our experiment,

46 with a variable response in slug damage, and an increase in the proportion of chewed plants

(Table 2–4). Chewing damage is a concern and can contribute to reduced photosynthesis in cash crops (Bardner and Fletcher, 1974). Slugs are a serious issue in mid-Atlantic reduced tillage cropping systems (Douglas and Tooker, 2012), and cutting damage associated with black cutworms is suspected to reduce early-season crop stands (Mischler et al., 2010; Sherrod et al.,

1971). Our observation that the proportion of plants exhibiting cutting damage lessened with time in organic management further suggests that the increasing abundances of predators over time may have contributed to increased biological control. Some studies have linked increased predatory arthropods to reduced numbers of herbivorous insects as we also did in our study

(Nelson et al., 2004), and others have not been able to show a relationship between predators and reduced number of pests (Renkema et al., 2012). Few studies have linked predatory activity to reduced plant damage as we have (Letourneau and Bothwell, 2008).

Herbivore density is highly variable depending on year (Kennedy and Storer, 2000), and we found higher densities of caterpillars and slugs in 2012 than in 2013. This difference in densities between the two years may have contributed to the reduced corn populations in 2012.

Likewise, in the years that herbivory responded to the cover crop termination date/planting date of the cash crops treatments, herbivory increased with later corn planting dates, and was more variable in soybean (Table 2–4). Some predators and herbivores in central Pennsylvania are likely to become more active as the temperatures rise in the early growing season, and thus, this increase in herbivory with later termination dates is not surprising (Douglas, 2012; Grettenberger,

2015). For example, Douglas (2012) identified an increase in slug activity-density through June,

2011 in corn in central Pennsylvania. In our experiment, the numerically, but not significantly, higher activity-density of predators with later planting dates may have contributed to reducing herbivore numbers even though herbivory increased herbivory with later planting dates. For this reason, this increased herbivory may not be reflected in the cash crop yields, as yield was

47 sometimes highest in the later planting dates in both corn and soybean (supplementary information; Keene, 2015). Planting date may be a more appropriate strategy for overcoming insect pest issues in corn rather than soybean, however, as we did see fewer responses to planting date treatment in soybean than in corn.

Conclusion

The increase in predatory arthropods, and the correlations we established between predators and predation, higher early-season soybean populations, and lower slug density, may be indicative of an important functional response of predators to the management practices we employed in this system. However, connecting the response of cash crop yield to these various metrics is necessary before we can make any substantial conclusions about the performance of this system as it relates to the ground-dwelling arthropod community. Additionally, a variety of agronomic issues not discussed here are likely to have a greater effect on yields than do early- season arthropods, e.g., cover crop competition from inadequate cover crop control at early termination dates. Keene (2015) suggests that the middle cover crop termination and cash crop planting date may be most appropriate for organic cover crop based rotational no-till in central

Pennsylvania, as it may balance cover crop control with a growing season of moderate length.

According to our results, the middle cover crop termination date may also provide an adequate balance between high numbers of predators and predation, while not maximizing herbivory or herbivore density, thus potentially supporting an organic growers pest control needs.

Acknowledgements

This research was supported by a grant through the United States Department of

Agriculture, Organic Research and Education Initiative. A. Rivers also received a graduate student grant through the Northeast Sustainable Agriculture Research and Education program to supplement the main research conducted in the experimental site. The authors wish to thank

Robert Davidson, Carnegie Museum of Natural History, Pittsburgh, Pennsylvania for confirming

Carabidae identifications, Mark Dempsey and Clair Keene for support with data analysis and technical support, and Drs. John Tooker, Bill Curran, Ed Rajotte, and Ebony Murrell for suggestions on an earlier version of the manuscript.

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Tables

Table 2-1. Management and sampling dates during the three years of the experiment. 2011 2012 2013 Hairy Vetch and Triticale (HVT)a Cereal Rye Wheat Field Operations Early Middle Late Early Middle Late Planted winter crop 3-Sep 3-Sep 3-Sep 18-Oct 18-Oct 18-Oct 24-Oct Rolled cover crop 31-May 8-Jun 15-Jun 11-May 21-May 1-Jun Planted cash crop 1-Jun 9-Jun 16-Jun 25-May 6-Jun 11-Jun Rolled cover crop 25-May 6-Jun 11-Jun Herbivore density assessments 8-Jun 21-Jun 26-Jun Pitfall trapping 27-Jun 1-Jul 11- Jul 11-Jun 25-Jun 2-Jul 17-Jun Plant damage assessments 22-Jun 1-Jul 8-Jul 19/20-Jun 28-Jun 8-Jul Harvested cash crop 7-Oct 7-Oct 7-Oct 11-Oct 11-Oct 11-Oct 16-Jul Wheat Hairy Vetch and Triticale Cereal Rye Early Middle Late Early Middle Late Planted winter crop 24-Oct 1-Sep 1-Sep 1-Sep 15-Oct 15-Oct 15-Oct Rolled cover crop 25-May 7-Jun 15-Jun 24-May 29-May 4-Jun Planted cash crop 31-May 7-Jun 15-Jun 31-May 3-Jun 17-Jun Rolled cover crop 11-Jun 14-Jun 22-Jun 31-May 3-Jun 17-Jun Herbivore density assessments 14-Jun 20-Jun 26-Jun 20-Jun 21-Jun 3-Jul Pitfall trapping 20-Jun 25-Jun 25-Jun 2-Jul 24-Jun 24-Jun 9-Jul Plant damage assessments 27-Jun 3-Jul 3-Jul 25/26-Jun 27/28-Jun 11-Jul Harvested cash crop 7-Jul 1-Oct 1-Oct 1-Oct 5-Oct 5-Oct 5-Oct Cereal Rye Wheat Hairy Vetch and Triticale Early Middle Late Early Middle Late Planted winter crop 22/23-Sep 22/23-Sep 22/23-Sep 25-Oct 30-Aug 30-Aug 30-Aug Rolled cover crop 25-May 2-Jun 13-Jun 1-Jun 6-Jun 18-Jun Planted cash crop 26-May 3-Jun 14-Jun 1-Jun 6-Jun 18-Jun Rolled cover crop 12-Jun 13-Jun 26-Jun Herbivore density assessments 19-Jun 26-Jun 1/2-Jul Pitfall trapping 13-Jun 27-Jun 11- Jul 18-Jun 24-Jun 1-Jul 5-Jul Plant damage assessments 13-Jun 23-Jun 6-Jul 24-Jun 2-Jul 8-Jul Harvested cash crop 18-Oct 18-Oct 18-Oct 9-Jul 23-Sep 23-Sep 23-Sep a HVT and cereal rye were rolled cover crops at time of pitfall sampling.

Table 2-2. Activity-densities and trophic groups of invertebrates captured by pitfall trap during the three years of the experiment. Taxon and Life Stage Trophic HVT Cereal Rye Wheat Order Familyab Group 2011c 2012 2013 2011 2012 2013 2011 2012 2013 Total Diplopoda Decomposer 166 61 95 173 24 58 122 513 31 1,243 Coleoptera Chrysomelidae (A) Herbivore 42 38 41 6 4 3 3 12 2 151 Coleoptera Curculionidae (A) Herbivore 50 15 20 1 6 6 - 3 14 115 Hemiptera Aphididae Herbivore 14 3 31 55 60 118 11 19 57 368 Lepidoptera Herbivore 2 14 17 2 2 10 1 15 9 72 Orthoptera Caelifera Herbivore 5 27 86 3 34 62 4 25 29 275 Thysanoptera Herbivore 108 56 181 24 70 57 82 348 65 991 Mollusca Herbivore 71 332 131 72 116 33 2 84 92 933 Collembola - 9,456 7,153 - 4,464 4,338 - 4,888 3,316 33,615 Acari - 1,510 4,840 - 1,282 2,428 - 2,727 5,498 18,285 Coleoptera Scarabaeidae (A) Omnivore 20 13 17 10 17 11 13 10 18 129 Coleoptera Unidentified (A/L) 326 681 574 208 375 211 91 250 225 2,941 Diptera 224 486 977 123 150 490 238 525 1,705 4,918 Hemiptera Unidentified 35 136 143 16 63 191 42 144 161 931 Hymenoptera Unidentified 230 164 559 59 158 705 149 362 1,313 3,699 Araneae Predator 919 748 851 344 479 528 340 372 391 4,972 Coleoptera Carabidae (A/L) Predator 153 312 564 80 99 152 58 162 344 1,924 Coleoptera Coccinellidae (A/L) Predator 8 4 63 10 4 19 80 30 41 259 Coleoptera Histeridae (A) Predator - 2 43 ------45 Coleoptera Staphylinidae (A/L) Predator 110 240 483 43 51 82 106 167 1,279 2,561 Hemiptera Nabidae Predator 1 - 17 1 9 41 1 3 12 85 Hymenoptera Formicidae Predator 77 45 129 58 70 111 687 237 226 1,640 Opiliones Predator 55 20 268 54 42 225 133 169 541 1,507 Orthoptera Gryllidae Predator 24 2 10 7 16 57 111 136 224 587 Rare Groups d 8 7 33 6 11 7 4 11 46 133 Total Predatory Macrorthropods e 1,352 1,378 2,448 602 780 1,220 1,520 1,287 3,101 13,688 Total Macroarthropods 2,581 3,075 5,202 1,285 1,747 3,144 2,276 3,513 6,733 29,556 a For holometabolous groups: A = Adult; L = Larvae. We did not distinguish between nymphs and adults for hemimetabolous groups. b Groups indicated as unidentified include all members of that order not identified to family, e.g., unidentified Coleoptera might include Nitidulidae if captured. c n = 48 in each year. d Rare groups were those captured in only one year or crop, including some predatory arthropods (Chilopoda, Cantharidae, Elateridae (Coleoptera), Reduviidae (Hemiptera), Geocoridae (Hemiptera), Isopoda, Mecoptera, Neuroptera, Pseudoscorpiones, Psocoptera, and Thysanura). e Macroarthropods = all groups excluding Collembola and Acari

2011 2012 2013 n = 48 a n = 48 n = 48 Hairy Vetch-Triticale (HVT) 0.56 (0.18) A 0.76 (0.02) A 0.70 (0.02) A Cereal Rye 0.54 (0.03) Aa 0.48 (0.02) Ba 0.89 (0.02) Bb Wheat 0.76 (0.02) A 0.72 (0.03) AB 0.64 (0.03) AB a n indicates the number of samples.

Table 2-4. Mean (± SEM) proportions per plot of damage by herbivores to cash crops planted into rolled cover crops, for both cover crop treatments combined and per cover crop termination date treatment. Damage assessments were conducted in a 0.813 m2 quadrat; damage reflects herbivory to corn in hairy vetch-triticale and to soybean in cereal rye. Within each cover crop (row), significantly different values (p ≤ 0.05) are indicated by lower case letters. Values were arcsine square root transformed prior to analysis, but untransformed data are shown here. Early a Middle Late Both Cover Crops Slug damage b* 0.56 (0.03) a 0.68 (0.21) ab 0.77 (0.21) b Cut plants* 0.14 (0.01) a 0.17 (0.01) b 0.17 (0.01) b Chewed plants c* 0.31 (0.02) a 0.37 (0.02) b 0.49 (0.03) ac

Hairy Vetch-Triticale Slug damage 0.70 (0.03) 0.80 (0.02) 0.90 (0.01) Cut plants - all years d 0.23 (0.02) a 0.30 (0.01) b 0.28 (0.02) b Cut plants - 2011 0.09 (0.02) a 0.40 (0.01) b 0.43 (0.01) b Cut plants - 2012 0.33 (0.02) 0.26 (0.01) 0.22 (0.02) Cut plants - 2013 0.28 (0.02) 0.23 (0.02) 0.18 (0.02) Chewed plants - all Years 0.30 (0.02) 0.44 (0.03) 0.52 (0.03) Chewed plants - 2011 0.16 (0.24) 0.16 (0.01) 0.26 (0.03) Chewed plants - 2012 0.35 (0.04) a 0.56 (0.05) b 0.61 (0.04) b Chewed plants - 2013 0.40 (0.03) a 0.60 (0.03) ab 0.69 (0.04) b

Cereal Rye Slug damage 0.42 (0.03) 0.56 (0.02) 0.65 (0.03) Cut plants - all years e 0.06 (0.01) 0.05 (0.01) 0.07 (0.01) Cut plants - 2011 0.07 (0.01) ab 0.04 (0.01) a 0.13 (0.02) b Cut plants - 2012 0.08 (0.01) 0.08 (0.01) 0.05 (0.01) Cut plants - 2013 0.02 (0.00) 0.02 (0.00) 0.02 (0.00) Chewed plants - all years 0.32 (0.04) 0.31 (0.02) 0.46 (0.04) Chewed plants - 2011 0.00 (0.00) a 0.14 (0.02) b 0.15 (0.02) b Chewed plants - 2012 0.49 (0.03) 0.35 (0.03) 0.49 (0.03) Chewed plants - 2013 0.48 (0.02) a 0.43 (0.04) a 0.74 (0.03) b * According to post hoc tests of means, densities were also different between cover crops when collapsed across cover crop termination date (p ≤ 0.05), see text for means. a n = 96 for measures in both cover crops across all three years; n = 48 for measures in each cover crop, collapsed across all three years; n = 16 for measures in each cover crop for each year. b Slug damage: proportion of plants exhibiting plant tissue removal between leaf veins c Chewing damage: removal of leaf tissue by chewing insects, generally on leaf margins d Cutting damage in corn planted into rolled hairy vetch-triticale: plants exhibiting a series of holes in the whorl of the small plant, indicative of feeding by lepidopteran larva e Cutting damage in soybean planted into rolled cereal rye: plants that were completely chewed off at the base where the plant emerged from the soil

Caterpillar Density* Hairy Vetch-Triticale 5.2 (1.1) Aa 1.9 (0.4) Ab 0.3 (0.1) c Cereal Rye 1.7 (0.4) Ba 0.3 (0.1) Bb 0.6 (0.0) b * According to post hoc tests of means, mean slug densities were different between cover crops when collapsed across cover crop termination date, see text for means.

Figures

a.) Predatory Arthropod Activity-Density b.) Group Richness b 50 7 b

6 40 a 5 a 30 a a 4

20 3 Mean (± Mean SEM) 2 10 1

0 0 2011 2012 2013 2011 2012 2013

0.5 b

0.4

)

0.3 ±SEM ab

Mean( 0.2 a

0.1

0.0 2011 2012 2013

a.) HVT b.) Cereal Rye c.) Wheat

1.0 1.0 1.0

0.8 0.8 0.8

0.6 0.6 0.6

0.4 0.4 0.4

0.2 0.2 0.2

Proportion of Damaged Waxworms

0.0 0.0 0.0 0 50 100 150 0 50 100 150 0 50 100 150 Total Predator Activity-Density

a.) Rye: Crop Population b.) HVT: Caterpillar Density

600

Total per Plot per Total

200

0 0

Total Plants per Plot (1,000) Plot per Plants Total 0 10 20 30 40 50 60 70 0 20 40 60 80 100

c.) Rye: Slug Density d.) HVT: Slug Density

Total per Plot per Total Plot per Total

0 0

0 10 20 30 40 50 60 70 0 20 40 60 80 100

Total Predator Activity-Density Total Predator Activity-Density Figure 2-5. Significant (p ≤ 0.05) linear regressions relating predator activity-density to estimated early season soybean population in the rolled cereal rye cover crop treatment (a.); total caterpillar density in hairy vetch-triticale (HVT) (b.); and total slug density in cereal rye (c.) and in HVT (d.). In figure a, analyses included data for all years and experimental treatments in cereal rye. In figures b-d., densities were only measured in 2012 and 2013, and analyses were only conducted on those years for all experimental treatments within each cover crop. Predator activity-densities and caterpillar densities were log10 (x+1) prior to analysis, but untransformed data are shown here.

Chapter 3

Cover crop management effects on Carabidae (Coleoptera) in a rotational no- till system in transition to organic production

Abstract

Organic grain growers rely on cultural practices and biological control to regulate pests, and the implementation and timing of cultural practices can affect many characteristics of the cropping system as a habitat for natural enemies of arthropod pests. Ground beetles (Coleoptera:

Carabidae) in particular are important insect and weed-seed predators, and are sensitive to crop rotations, tillage, and environmental complexity. In a reduced tillage system in transition to organic management, we evaluated the effect of cover crop species and termination date, crop rotation, and high-residue cultivation on ground and tiger beetle (Coleoptera: Carabidae) activity- density, community composition, and trophic group. The full entry, three-year experiment included a sequence of corn (Zea mays L.), soybean (Glycine max (L.) Merr.), and wheat

(Triticum aestivum L.). A mixture of hairy vetch (Vicia villosa Roth) and triticale (x Triticosecale

Wittmack) preceded corn, and cereal rye (Secale cereale L.) preceded soybean. The overwintered cover crops were terminated by rolling, and corn and soybean were no-till planted through the mat created by the rolled cover crops to compare three cover crop termination dates (early, middle, and late). Wheat was planted on a single date in each year into tilled soil. Carabids were sampled using pitfall traps two weeks after termination of the two cover crop treatments, and in mid-June in wheat. Carabid activity-density and species richness increased during the three-year transition, and community evenness increased by the third. Crop species influenced carabid community composition, and by the third year, the carabid community was comparable between

66 wheat and hairy vetch-triticale. The late cover crop termination date was positively associated with higher activity-densities of large carabids in rolled hairy vetch-triticale and rolled cereal rye; carnivorous beetles in rolled hairy vetch-triticale; and granivorous beetles in rolled cereal rye.

Although high-residue cultivation did not occur in wheat, only in wheat was the effect of high- residue cultivation significant, with the proportion of small beetles significantly higher in cultivated treatments and the proportion of large beetles significantly higher in treatments without high-residue cultivation. Results have strong implications for management during the transition to organic, including the importance of plant residue, reduced tillage and late cover crop termination dates for augmenting carabid populations.

Introduction

In the United States, transition to certified organic production requires a three-year transition during which the crop must be managed according to the USDA national organic standards (USDA, 2015). To manage pests during the transition and after, organic growers must rely on biological processes, such as biological control of pests by natural enemies, and cultural and mechanical practices, such as planting at specific times to avoid pests and using inversion tillage and inter-row cultivation to control weeds. As such, the practices implemented during this transition may differentially affect pest and beneficial organisms, resulting in variable risk for crop losses associated with pest damage (Delate and Cambardella, 2004; Lundgren et al., 2006;

Smith et al., 2011; USDA, 2015). The choice of specific management practices during the transition can thus inadvertently or intentionally affect key natural enemies, resulting in an increase or decrease in pest suppression.

The initial transition to organic production and continuing organic management can increase the abundance and diversity of beneficial arthropods in general, and Carabidae

(Coleoptera) beetles, specifically (Bengtsson et al., 2005; Dritschilo and Wanner, 1980; Lundgren et al., 2006; Pfiffner and Niggli, 1996; Purtauf et al., 2005). Carabid beetles are predators of arthropods and weed seeds, and contribute to pest suppression in organically-managed systems, helping to minimize weed and insect pest pressures (Lundgren et al., 2006; Menalled et al., 2007;

Ward et al., 2011). However, while carabids may be augmented by certain practices employed by organic growers, e.g., the inclusion of a cover crops (Carmona and Landis, 1999; Shearin et al.,

2008; Ward et al., 2011), practices that are used for managing pests may contribute to reducing carabid abundance and diversity, e.g., the use of inversion tillage for weed control (Hatten et al.,

2007; Holland and Reynolds, 2003; Mirsky et al., 2012; Thorbek and Bilde, 2004).

Inversion and various forms of cultivation, such as blind cultivation and inter-row cultivation, are widely used as important means of weed control in many organic systems

(Bàrberi, 2002; Mirsky et al., 2012). In addition to the potential negative effects on soil-dwelling organisms, tillage and other types of soil disturbances have been associated with other negative outcomes, e.g., reduced soil quality, the potential for erosion, and higher management costs for labor and fuel (Hatten et al., 2007; Mirsky et al., 2012; Smith et al., 2011). As such, many organic growers are seeking alternatives to reduce their reliance on tillage for weed control (Mirsky et al.,

2013, 2012), and cover crop-based rotational no-till is emerging as a potential option. In rotational no-till systems, a grower occasionally and strategically uses inversion tillage for weed control or fertility management, while relying on other management practices to assist in pest suppression (Mirsky et al., 2012). Specifically, in parts of the rotation, a weed-suppressive mulch is created by a cover crop killed by a roller-crimper, into which cash crops are no-till planted

(Davis, 2010; Mirsky et al., 2012; Mischler et al., 2010a; Ward et al., 2011). The number of primary tillage events in these systems can be reduced by half or more in comparison to those managed with multiple annual tillage and cultivation events, and organic growers may gain soil quality benefits without allowing the weed seedbank to increase (Davis et al., 2005; Menalled et al., 2001).

The efficacy of cover crop-based rotational no-till as a pest management strategy is largely dictated by management, with the species of cover crop and timing of management practices, e.g., termination of cover crop and inversion tillage if implemented, contributing to the success of the system (Mischler et al., 2010a; Smith et al., 2011; Ward et al., 2011). Depending on the location, 5,000 to 10,000 kg ha-1 of rolled cover crop biomass is necessary at the soil surface to effectively suppress weeds, but the amount of rolled biomass remaining after termination is dependent on cover crop species, planting date, and termination date (Davis, 2010;

Mirsky et al., 2011, 2009; Mischler et al., 2010a; Nord et al., 2012). Additionally, the cover crop

69 must be mature enough to allow termination by the roller-crimper, but not so mature as to set seed that will result in volunteer weedy cover crops (Davis, 2010; Mirsky et al., 2009; Mischler et al.,

2010a).

Due to the properties of the rolled cover crop mulch and a reduction in soil disturbance, a cover crop-based rotational no-till system may provide diverse resources in space and time for ground dwelling natural enemies, including carabids (Blubaugh and Kaplan, 2015; Mathews et al., 2004). This approach to pest management thus has strong potential, especially for organically- managed agroecosystems, by conserving and augmenting populations of carabid beetles.

However, the initial crop, and crop sequence, in the transition can have long-term implications for pest control potential, as certain crops may be more efficient in attracting and retaining carabids

(Lundgren et al., 2006). Likewise, the timing of management practices, including cover crop termination date, can affect the amount and availability of resources and the habitat (Blubaugh and Kaplan, 2015). Here we report on a study that examined the interacting effects of initial cash crop and timing of management practices on the carabid community in a cover crop-based rotational no-till feed and forage cropping system in central Pennsylvania, USA. We hypothesized that over the course of the three-year transition to organic management, that: activity-density and diversity of carabid beetles will increase in each crop treatment with each additional year of organic management; functional traits, such as size, trophic group, and community composition of carabids will increase from year one of the organic transition to year three; and cover crop treatment and termination date of the cover crops will dictate community composition.

Materials and Methods

Site Description

This research was conducted at the Russell E. Larson Agricultural Research Center in

Centre County, Pennsylvania (40°43′23″N, 77°55′44″W) at 376 meters above sea level (USGS,

2014). Mean annual precipitation in the area was approximately 1006 mm between 1981 and

2010, with approximately 547 mm of precipitation on average during the growing season of May through October (NOAA, 2014). Mean monthly temperatures ranged between -2.7 and

22.3°Celsius (C), with an annual mean of 10.1°C in the years 1981 through 2010 (NOAA, 2014).

The experiments were part of a larger study, the Reduced-Tillage Organic Systems Experiment

(hereafter, ROSE, for convenience); the total area of the site was approximately 4 hectares, and during the experiment, the ROSE site was managed for transition to certified organic production.

Soils at the site are representative of the Hagerstown Soil Series according to the USDA, Natural

Resources Conservation Service soil classification system, a silt loam classified as prime farmland (Soil Survey Staff, 2014).

Experimental Design and Field Operations

We designed the experiment to test the effect of multiple agronomic practices on insect and weed dynamics, and included several experimental treatments, including crop variety, planting date, and high-residue cultivation (Mirsky et al., 2013). The three-year experiment consisted of four blocks of a full entry design, with the total cropping area in each block amounting to 6020 m2 (2006 m2 per crop). Each of the four blocks within the experiment contained three cropping strips representing one crop in the three-year rotation, with three cash crops: corn (Zea mays L.), soybean (Glycine max (L.) Merr.), and wheat (Triticum aestivum L.)

71 planted in every growing season during the years 2011 to 2013. Crops were rotated annually with a cover crop with a complete rotation as follows: corn, cereal rye (Secale cereale L.), soybean, winter wheat, and hairy vetch (Vicia villosa Roth) planted together with triticale (× Triticosecale

Wittmack). The cover crops were planted into tilled ground in the fall, with a seeding rate of 34 kg seed ha-1 each for hairy vetch and triticale, and 189 kg seed ha-1 for cereal rye. In the spring, we rolled the cover crops prior to, or at the time of, planting of corn or soybean (Table 3–1). Corn and soybean were no-till planted into the residue mat created by the rolled cover crop at 84,000 seeds ha-1 and 556,000 seeds ha-1, respectively. Winter wheat was seeded at a rate of 163 kg seed ha-1 into soil that was moldboard plowed, disked, and field cultivated following harvest of soybean. The wheat grain was then harvested as a cash crop the following summer, with wheat residues remaining in the field (Table 3–1).

In the four blocks, each crop strip represented a split-split-split plot, but we did not evaluate all of the treatments for this experiment. Of the splits we studied, the first split divided the whole plot into three subplots, in which the cover crops (hairy vetch-triticale or cereal rye) were managed by a roller-crimper (with each subplot area equaling 669 m2 per crop). Both cover crops were rolled at three termination dates (hereafter, termination date treatment) to allow for corn and soybean planting at three planting dates (early, middle, and late) relative to a typical planting date used by organic growers in the region, and based on cover crop phenology

(Mischler et al., 2010b; Nord et al., 2012). Within each termination date treatment, the calendar date differed for the two cover crop treatments.

72 provided by the cover crop mulch and each plot was cultivated twice about one week apart (Table

3–1). In soybean, the treatments receiving cultivation were planted in 76 cm rows, while the no- cultivation treatments were planted in 38 cm rows. Both corn treatments were planted in 76 cm rows. Because we did not evaluate all treatments within the ROSE experiment, the final design for our study resulted in four replicate plots per block for each crop, termination date and cultivation treatment, with each plot measuring 18.3 m by 9.1 m (167 m2).

Data Collection

To characterize the carabid community, we deployed two pitfall traps simultaneously in each 18.3 m by 9.1 m plot in the early part of the May – October growing season (Table 3–1).

Each trap consisted of a one-L plastic deli container buried level with the soil surface into which we placed a 50 mL plastic specimen cup, filled with 30 mL ethylene glycol as a killing agent and preservative. Inside the opening of the deli container, we placed a funnel (114 mm in diameter) to facilitate insect movement into the specimen cup and to exclude larger animals from entering the trap (Weeks and McIntyre, 1997). Traps remained open for 72 hours, after which the samples were removed from the field and brought to a laboratory for processing and identifications, and traps were removed from the field after sampling.

For all cover crop termination dates, we timed pitfall trapping to occur approximately one week after the emergence of corn and soybean in the years 2011-2013, which occurred approximately two weeks after rolling hairy vetch-triticale, and three weeks after rolling cereal rye. We conducted a single pitfall-trapping event approximately one month prior to wheat harvest, regardless of the termination date treatments of the crops preceding wheat. At the time of trapping in the rolled cover crops, the soil was completely covered by a dense mat of cover crop residue created by the roller-crimper. We moved the mat to expose the soil to place the pitfall

73 trap, then returned the mat to natural conditions after the trap was placed. In the treatments planted with hairy vetch-triticale (this combination of plants hereafter abbreviated as HVT), hairy vetch represented the bulk of the mulch biomass, with the hairy vetch stems creating a tangled mat of dense organic matter which could be easily lifted off the soil surface as a single piece. In the cereal rye treatments, the cereal rye stems were rolled parallel to the crop rows, with each stem aligned in the same direction relative to the others. Both corn and soybean were at growth stage V1 at the time of pitfall sampling (Nafziger, 2009; Nordby, 2004).

After trapping, we returned the pitfall samples to the laboratory, removed all Carabidae adults from the trap, preserved them in 80% ethanol, and counted and identified them to species using identification keys in Bosquet (2010) and local reference collections. Two species within the genera Amara, A. impuncticollis Say and A. littoralis Mannerheim, are difficult to identify to species without dissections, and we included these two species at the higher taxonomic level of

Amara impuncticollis group, with the group considered as a single species due to similarities in morpholgical and behavioral characteristics (Bosquet, 2010; Larochelle and Larivière, 2003).

Information regarding the ecology, behavior, phenology and size of the adults of each species was collected from various sources (Bohan et al., 2011; Bosquet, 2010; Dearborn et al., 2014;

Larochelle and Larivière, 2003; Lundgren, 2009). We classified adult carabids into trophic groups according to their predominant feeding preferences described in the literature, by the following designations: carnivorous, feeding primarily on animal tissues; omnivorous, feeding on both animal and plant tissues; and herbivorous, feeding primarily on plant materials, including seeds

(Lundgren, 2009). Size classes were assigned as follows: small, less than 5 mm; medium, between 5-10 mm; and large, greater than 10 mm (Eyre et al., 2012). We archived voucher specimens at the Carnegie Museum of Natural History and at the Frost Entomological Museum at the Pennsylvania State University.

Data Analysis

Mean activity-density (the relative measure of presence and movement of arthropods captured by pitfall traps), species richness, Smith-Wilson evenness, and proportions of each trophic group and size class of adult carabids were analyzed using a general linear mixed effects two-way ANOVA model using PROC GLIMMIX in SAS version 9.3 (Lang, 2000; SAS Institute,

2014). We examined nine combinations of cover crop treatment and year (crop-year, e.g., wheat

2011) and the six combinations of the termination date treatment and cultivation treatment (e.g., early-no cultivation) as single fixed effects. Random effects were specified as an overall residual effect, as block by year variance component and block by initial crop variance component. We used lsmeans statements using the Tukey method to conduct post hoc tests of means to isolate differences within year, and within the crop, cover crop termination date, and high-residue cultivation treatments. All activity-densities were log10 (x + 1) and all proportions were square root arcsine transformed to meet assumptions of normality and equality of variances prior to use in all analyses conducted in PROC GLIMMIX (Gotelli and Ellison, 2004; Ives, 2015; Kutner et al., 2005).

To describe patterns within the entire carabid community, we used statistical analyses in

R: A language and environment for statistical computing (R Core Team, 2013). We compared expected species richness by crop and pooled across the three years using rarefaction in the

BiodiversityR package (Kindt and Coe, 2005). Using the random method, by which sites are added in a random order, the smoothed rarefaction curves allow for comparison of the number of species expected at a given site for each crop. This allows for comparisons between crops based on the number of plots (sites) sampled, and significance was determined by non-overlapping confidence intervals (Gotelli and Colwell, 2001).

We used principal response curves (PRC) using the prc function in the vegan package of

R to determine community responses through time during the experiment (Oksanen et al., 2015;

R Core Team, 2013; van den Brink and ter Braak, 1999). To compare changes in the carabid community through the three years of the experiment, we conducted PRCs on the main effect of crop treatment, with wheat set as control to characterize differences between the standing crop and the two rolled cover crops. Separately, we analyzed each of the crop treatments individually through the three-year experiment, by the main effects of high-residue cultivation, with no cultivation set as the control, and termination date of the cover crop, with early termination date set as the control. Species were only included in the analyses if they had an activity-density greater than 1% of the total for the subset of the data in each analysis. We selected this threshold to exclude disproportionate effects of rare species (McCune and Grace, 2002). We transformed the species activity-densities using the Hellinger transformation prior to conducting the PRCs

(Legendre and Gallagher, 2001; van den Brink and ter Braak, 1999), and we used a Monte Carlo simulation with 4999 permutations to test the overall significance of each PRC. We present only significant PRCs showing only species with weights greater than or equal to an absolute value of

0.5 (van den Brink and ter Braak, 1999).

To further isolate associations between carabid species and treatment, we conducted an indicator analysis using the multipatt function in the indicspecies package (De Cáceres and

Legendre, 2009). Multipatt calculates an indicator value (IndVal) for each species, which is the product of the specificity (S) value for each species, the probability that a site with a specific species belongs to the treatment specified, and the fidelity (F) of a species, the probability that a species will be found in sites belonging to a treatment. Associations with a specific treatment are reported based on the highest IndVal for each species; we restricted the analyses to only allow associations with one cover crop by termination and planting date treatment (De Cáceres, 2013).

Results

Time in organic management

A total of 1,786 individual carabids in 47 species were collected during the three years of the experiment and across the experimental site (Table 3–2), with more than half (56%) of the carabid beetles captured in the final year of the experiment. Bembidion quadrimaculatum oppositum Say, a small, endemic and cosmopolitan beetle, was the most abundant species, accounting for 49% of the total individuals captured at the experimental site (Table 3–2). The main effect of crop-year was significant for total activity-density at the site (F8,50 = 29.41, p <

0.0001) and the number of species captured (richness) (F8,51 = 27.42, p < 0.0001). Both total activity-density and richness consistently increased during the three years of the experiment according to post hoc tests of means (p < 0.01, Table 3–3). The main effect of crop-year was also significant for Smith-Wilson evenness (F8,66 = 5.15, p < 0.0001), with post hoc tests of means indicating a higher mean activity-density in the third year as compared to years 1 (t = 4.66, p =

0.00) and 2 (t = 2.56, p = 0.03) of the experiment. The mean size of carabid beetles shifted over time (Table 3–3), with the proportion of medium (5 – 10 mm) carabids significant at the main effect of crop-year (F8,69 = 2.58, p = 0.02), with a significantly higher proportion of medium carabids in the third year compared to the first year (t = 9.416, p = 0.02). There were no significant changes in the proportions of carabid beetles by trophic group during the three years of the experiment.

According to principal response curves, the composition of the carabid community responded to within and between crop treatment factors across the three years of the experiment

(Figure 3–1, F1,423 = 27.63, p < 0.001). The compositional changes through time were due to the differences in the principle responses of Bembidion quadrimaculatum oppositum Say (species

77 weight of -1.75) to crop, with this species also having the highest activity-density at the site

(Table 2). Time in organic management (year) accounted for 10.6% and crop treatment accounted for 5.12% of the variance within the carabid community, respectively. In years 1 and 2 of the experiment, the coefficients for the rolled cover crops were closer to each other than to wheat, indicating that these treatments may be more comparable than either treatment is to wheat (Figure

3–1). However, by the third year of the experiment, the rolled cereal rye treatment had diverged from the other two crop treatments, with fewer B. quadrimaculatum oppositum captured in rolled cereal rye in 2013 compared to the other two crop treatments (38, as compared to 224 in HVT, and 209 in wheat).

Cover crop identity and management

More than half of the individual carabid beetles (54%) were collected in the rolled HVT, with 29% and 16% collected in the standing wheat and rolled cereal rye, respectively, during the three years of the experiment (Figure 3–2). The rarefaction curves for the three crop treatments indicate that we approached an adequate sampling effort with regard to the number of species collected for each of the crop treatments (Figure 3–3), but that in rolled HVT, fewer sites (traps) were necessary to obtain any given number of species compared to rolled cereal rye and wheat.

Based on overlapping 95% confidence intervals in the rarefaction curves (not shown, Figure 3–3), the total number of species captured in each crop treatment across the three years of the experiment were not significantly different, with 33 in rolled cereal rye, and 34 in both rolled

HVT and wheat.

The three-year mean activity-density and species richness differed significantly among each of the three crop treatments (Table 3–4), with activity-density significantly higher in rolled

HVT than in rolled cereal rye (t = -11.33, p < 0.0001) and wheat (t = -7.25, p < 0.0001), and

78 significantly higher in wheat than rolled cereal rye (t = 4.08, p < 0.0001). The crop treatments also differed in community composition (Figure 3–2), as indicated by a significantly higher

Smith-Wilson evenness and proportion of medium carabids in rolled HVT as compared to both rolled cereal rye (t = -2.21, p = 0.03) and wheat (t = -3.35, p = 0.00, Table 3–4), and a significantly higher proportion of carnivores in rolled cereal rye compared to wheat (t = -2.03, p =

0.04, Table 3–4). This difference in community composition also explains why the total numbers of carabid species captured in each cover crop treatment were comparable (Figure 3–3), but the mean numbers of species captured in each cover crop treatment were significantly different

(Table 3–4).

This strong response of the carabid community to crop treatment was also apparent in the differential effect of the cover crop termination date on the accumulated three-year means within the cover crop treatments (Table 3–5). In rolled HVT, the three-year mean activity-density significantly increased through time with later cover crop termination dates, with higher activity densities in the late termination date compared to the middle termination date (t = -3.02, p = 0.00) and early termination date (t = -5.55, p < 0.0001), and middle compared to early (t = -2.53, p =

0.01). However, the proportion of small carabids was significantly lower in the late termination date compared to the middle (t = 2.70, p = 0.01) and early (t = 2.78, p = 0.01), while the proportion of large carabids was significantly higher in the late compared to the middle (t = -3.04, p = 0.00) and early (t = -2.70, p = 0.01) termination dates (Table 3–5). The proportion of carnivorous carabids was significantly higher in the late compared to the middle termination date in rolled HVT (t = -2.15, p = 0.03).

The termination date affected the carabids in rolled cereal rye (Table 3–5), with a decrease in the proportion of small carabids in the late compared to the middle (t = 2.56, p = 0.01) and early termination dates (t = 2.63, p = 0.01). The proportion of large carabids increased from the early to late termination date (t = -3.00, p = 0.00), and middle to late (t = -2.11, p = 0.04), as

79 did the proportion of granivorous carabids from the early to late (t = -2.31, p = 0.02) and middle to late (t = -2.84, p = 0.01). Species richness increased with the late compared to the early termination date in rolled cereal rye (t = -4.22, p < 0.0001). Only in wheat was the effect of high- residue cultivation significant; because of the experimental design, wheat, by the third year of the experiment, was the only crop to have followed two crops in which high-residue cultivation had occurred. In wheat, the proportion of small carabids was significantly higher (t = -2.80, p = 0.01), and the proportion of large carabids was significantly lower (t = 2.97, p = 0.00) in treatments, which had previously received cultivation compared to treatments which had not previously received cultivation.

Within each termination date treatment, only the principal response of rolled HVT was significant (Figure 3–4, F1,135 = 10.09, p < 0.001), indicating that termination date of the rolled

HVT cover crop was a significant driver in the composition of the carabid community within this cover crop. Time in organic management accounted for 12.3% and termination date treatment accounted for 9.8% of the variance in the community, respectively. Two species had strong responses that corresponded to the PRC: B. quadrimaculatum oppositum (weight = -0.74) and

Chlaenius tricolor tricolor Dejean (weight = 1.08). In indicator analysis, both of these species were associated with rolled HVT. B. quadrimaculatum oppositum was associated with the middle termination date in HVT, and C. tricolor tricolor was associated with the late termination date

(Table 3–6). Of the remaining 13 species of carabid beetles showing a significant relationship to a crop and termination date, 10 of those species were associated with rolled HVT (Table 3–6).

While not all the species associated with HVT had high values for specificity (probability that the species was captured in a treatment) to cover crop and termination date, both B. quadrimaculatum oppositum and C. tricolor tricolor had high values for fidelity (probability that a treatment contains a species), e.g., 54.41% of C. tricolor tricolor were captured in late HVT (specificity), and 66.67% of the traps included that species (fidelity).

Discussion

During the transition to certified organic production, cultural practices may determine the potential for successful pest management, as certain practices may conserve and augment populations of carabid beetles (Lundgren et al., 2006). We hypothesized that carabid activity- density and diversity would increase during a three-year transition to organic management at a site that had previously been managed with occasional insecticide use. At our site, carabid beetle activity-density, species richness, and community evenness increased, with a significant increase in the proportion of medium-sized beetles and no significant site-wide changes in the proportion of each trophic group of the beetles. As expected, the management practices we evaluated during the transition, namely, the use of different cover crop species, and multiple termination dates of the cover crops, largely dictated community composition, with a significant effect of high-residue cultivation only detectable in wheat. High-residue cultivation occurred in the corn and soybean preceding wheat, and resulted in a significantly higher proportion of smaller carabids in the cultivated treatments as compared to uncultivated, likely due to the potential for small organisms to better tolerate soil disturbances (Holland, 2004; Szysko et al., 2000). Our results confirm those observed in other studies, in that cover crops (Shearin et al., 2008), crop identity (Russon and

Woltz, 2014), mulch (Renkema et al., 2012), reduced tillage (Clark et al., 2006), and altered timing and type of management practices (Thorbek and Bilde, 2004) have each been identified as significant factors affecting carabid species. Minimal research exists, however, on the effect of this high residue environment within the organic transition on carabid beetles in a cover crop- based rotational no-till system, and on the timing of management practices during the transition, and the results we present here are novel in that regard.

We identified a significant trend in each additional year of organic management for increased activity-density and species richness, which is understandable considering other

81 researchers have suggested that at least four years are necessary for arthropod populations to stabilize to any changes in environmental conditions (Sabais et al., 2011). Increases in species richness and activity-densities in organic agriculture have been attributed to fewer disturbances, e.g., application of agrochemicals, higher soil quality and resultant soil biodiversity, and increases in weed abundance and thus diversity of resources, e.g., microclimate, habitat, seed and arthropod prey (Birkhofer et al., 2008; Diehl et al., 2012; Frank et al., 2011; Guy et al., 2008; Kielty et al.,

1996). However, carabids in our experiment responded differently to each crop treatment during the transition, as indicated by the principal response curves, and the type and timing of management activities preceding pitfall trapping in each of the crops may play a significant role in our results (Blubaugh and Kaplan, 2015; Cole et al., 2002; Lundgren and Fergen, 2011;

Lundgren et al., 2006). In a study to evaluate weed management tactics during the organic transition in fresh-market tomatoes, Blubaugh and Kaplan (2015) identified a significantly higher seasonal activity-density of Harpalus pensylvanicus Dejean adults, an important weed-seed predator, in no-till treatments with a cereal rye cover crop managed by a roller-crimper than in treatments with tillage or with tillage and a living mulch of crimson clover (Trifolium incarnatum

L.). The authors suggest that adult female Harpalus spp. prefer to oviposit in sites that have not been tilled for at least one growing season and with abundant plant cover. This suggestion was supported by significantly higher captures of Harpalini larvae where weed cover, and thus potential food resources, was abundant (Blubaugh and Kaplan, 2015). Cover crops were planted into tilled ground in our experiment, but among our treatments, the hairy vetch-triticale treatment in our system is planted earliest in the fall (early September, Table 3–1), after which no disturbances occurred in the field until spring. Cereal rye and wheat are both planted later than hairy vetch-triticale, in mid- to late October. Considering that many fall-breeding carabids are active as early as August and carabid activity has been known to decrease by October in some regions (Carmona and Landis, 1999; Shearin et al., 2008), this later disturbance and shorter

82 period for crop growth prior to winter may limit the amount of ground cover available as a resource to carabids in the fall (Blubaugh and Kaplan, 2015). While the growth habits of cereal rye and wheat are likely to be similar in the fall, cereal rye was subjected to several more field disturbances in the spring prior to pitfall trapping, including two rolling events. Because the hairy vetch-triticale treatment is also subject to rolling in the spring, the earlier establishment of the hairy vetch-triticale in the fall may play a significant role in attracting carabids prior to winter.

The environment directly above the soil differed between the rolled cover crops and the standing wheat, and between the two rolled cover crops, which might have contributed to differences in trap captures between the crops. Lang (2000) suggested that pitfall traps are less efficient in more complex environments, which Lundgren et al. (2006) attribute to the greater stability of the microenvironment and the potential for more niche space to occupy, suggesting that carabids are less likely to be mobile in more complex habitats. However, where cover crop biomass at the soil surface was highest in our experiment, in the hairy vetch-triticale (three year residue biomass mean of 6,228.4 kg ha-1), carabid activity-density was higher than in the treatments with only slightly less residue biomass (6123.3 kg ha-1 in the cereal rye) and no residue

(wheat) (Keene, 2015). Similarly, in the cover crop termination date treatments, the early termination date treatments had significantly less biomass than the late termination date in all but one treatment year (hairy vetch-triticale in year one) (Keene, 2015), and total mean carabid activity-density significantly increased with each termination date in hairy vetch-triticale.

As such, it may not be the structural complexity of the residue per sé, but the environment which it creates that is driving carabid community dynamics. Shearin et al. (2008) identified less seasonal variability in temperature and relative humidity in treatments with a cover crop residue as compared to fallow treatments in a mark-recapture experiment with Harpalus rufipes DeGeer, which was captured in significantly higher percentages in cover crop treatments than in fallow treatments. We did not measure temperature and relative humidity at our site, but

83 mean soil moisture was higher in cover crop treatments (20.2% in hairy vetch-triticale and 19.0% in cereal rye) than in our wheat treatments (15.8%), from which we could infer that the environment provided by the various treatments was potentially different.

By the third year of our experiment, the composition of the carabid community is more similar between the rolled hairy vetch-triticale treatments and wheat, where the soil would not have had a cover crop residue at the time of pitfall trapping, than between the two rolled cover crop treatments (Figure 3–1). This indicates that the differences, or similarities, within the carabid communities between crops may be a function of the individual carabid species themselves, rather than characteristics of the habitat. Döring and Kromp (2003) make a similar suggestion in central European cropping systems, and propose that breeding season (e.g., spring or fall), wing dimophism, and humidity preference will in part determine a species’ association with either an organic or conventional system. These authors propose, in part, that macropterous species with a high dispersal power and spring breeders with an adult autumn population benefit from organic management. Two of the species for which we observed increases in activity-density from year one to three of our experiment, Poecilus chalcites (Say) and Poecilus lucublandus (Say) (Table

3–2), meet this criteria, in that both are spring breeders and macropterous and submacropterous, respectively (Larochelle and Larivière, 2003). Pitfall traps are somewhat biased toward species that are mobile during the time trapping takes places, which in our case, is spring breeders (Lang,

2000).

According to Döring and Kromp's (2003) analyses, feeding preference is also a significant driver of species’ associations to a cropping system, with some predominantly granivorous genera, e.g., Amara and Harpalus, benefitting from organic cropping systems compared to conventional ones (Döring and Kromp, 2003). Because weed management is challenging in organic agriculture, Döring and Kromp (2003) suggest that the additional cover and seeds provided by weeds may provide more food resources for these species. In our system,

84 the proportion of granivorous species did not increase with additional years of organic management; however, numerically, the total site-wide activity-densities of the granivorous carabids increased from 9 in year one of the experiment to 72 in year three. Likewise, mean site- wide total weed biomass increased from 4.43 to 14.38 kg ha-1 during the course of our experiment with differential effects depending on cover crop and termination date treatments, indicating that weed resources may affect carabid community dynamics at some level. Conversely, one granivorous species, Harpalus affinis Shrank was strongly associated with wheat in our system

(Figure 3–2, Table 7), where weed biomass was considerably lower than in the other two crop treatments, with 2.05 kg ha-1 in wheat, and 18.75 in hairy vetch-triticale and 19.75 in cereal rye

(mean total biomass for the last two years of the experiment, as weed biomass was not measured in wheat in the first year). This further indicates that carabid community dynamics in our experiment were likely affected by some combination of organic management and timing of field operations, habitat complexity, availability of prey, and the characteristics of individual carabid species.

Conclusion

Balancing the risks and benefits associated with cropping system and pest management choices during the transition to organic management is essential for growers. A low intensity system, which may require fewer inputs in time, fuel, and labor, while maximizing the long-term biological control potential of the system, could be beneficial for growers during the transition

(Delate and Cambardella, 2004; Smith et al., 2011). In our cover crop-based rotational no-till system, we identified significant differences associated with cover crop species and management during the three-year transition to organic management. While these results could indicate specific benefits of using one cover crop mixture as compared to an individual carabid species, it is more important to note that the crop with which a producer starts, and thus ends, an organic transition may be significant for future pest management due to the strong crop-year effect of any given cover crop species on carabids. Regardless of the point of entry into the rotation with which our experiment began, however, the organic transition resulted in significant gains in carabid activity-density and abundance, indicating the benefit of organic management to the conservation of this important beneficial group of insects.

To fully understand the benefits of cover crops to carabid conservation and pest management, it would be worthwhile to lengthen the experimental time of a cover crop-based rotational no-till system. Thus, continuing the rotation beyond three years could provide additional information regarding the key factors influencing the carabid associations with each cover crop (e.g., fall planting date). Additionally, understanding the significant characteristics of each cover crop as it relates to the carabid community (e.g., amount of biomass in the fall, differences in microhabitat complexity, availability of prey associated with each crop, etc.) could provide additional information regarding the ways in which organic cover crop-based rotational no-till may be manipulated to further conserve carabids for pest management. For example, the

86 associations of each of the species within our system (e.g., HVT terminated at a middle or late date), and the potential for these species to contribute to pest suppression, could be an additional benefit of choosing a particular cover crop for organic growers.

Acknowledgements

This research was supported by a grant through the United States Department of

Robert Davidson, Carnegie Museum of Natural History, Pittsburgh, Pennsylvania for confirming

Carabidae identifications, Bryan Vinyard, USDA-ARS, for development of the statistical model in SAS, Mark Dempsey and Clair Keene for support with data analysis and technical support, and

Drs. John Tooker, Bill Curran, Ed Rajotte, and Ebony Murrell for suggestions on an earlier version of the manuscript.

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Tables

Table 3-1. Field operations and sampling dates by each entry of the crop rotation. Cropping Year 2011 2012 2013 Winter Cover Crop a Hairy Vetch and Triticale (HVT) Cereal Rye Wheat Cover Crop Termination Date Early Middle Late Early Middle Late Planted winter crop 3-Sep 3-Sep 3-Sep 18-Oct 18-Oct 18-Oct 24-Oct Rolled cover crop 31-May 8-Jun 15-Jun 11-May 21-May 1-Jun Planted cash crop 1-Jun 9-Jun 16-Jun 25-May 6-Jun 11-Jun Rolled cover crop 25-May 6-Jun 11-Jun Pitfall trapping 27-Jun 1-Jul 11- Jul 11-Jun 25-Jun 2-Jul 17-Jun High residue cultivation 5-Jul 14-Jul 20-Jul 28-Jun 5-Jul 11-Jul High residue cultivation 5-Jul 11-Jul 18-Jul Harvested cash crop 7-Oct 7-Oct 7-Oct 11-Oct 11-Oct 11-Oct 16-Jul

Winter Cover Crop Wheat Hairy Vetch and Triticale (HVT) Cereal Rye Cover Crop Termination Date Early Middle Late Early Middle Late Planted winter crop 24-Oct 1-Sep 1-Sep 1-Sep 15-Oct 15-Oct 15-Oct Rolled cover crop 25-May 7-Jun 15-Jun 24-May 29-May 4-Jun Planted cash crop 31-May 7-Jun 15-Jun 31-May 3-Jun 17-Jun Rolled cover crop 11-Jun 14-Jun 22-Jun 31-May 3-Jun 17-Jun Pitfall trapping 20-Jun 25-Jun 25-Jun 2-Jul 24-Jun 24-Jun 9-Jul High residue cultivation 28-Jun 5-Jul 11-Jul 16-Jul 16-Jul 22-Jul High residue cultivation 5-Jul 11-Jul 18-Jul 18-Jul 18-Jul 25-Jul Harvested cash crop 7-Jul 1-Oct 1-Oct 1-Oct 5-Oct 5-Oct 5-Oct

Winter Cover Crop Cereal Rye Wheat Hairy Vetch and Triticale (HVT) Cover Crop Termination Date Early Middle Late Early Middle Late Planted winter crop 22/23-Sep 22/23-Sep 22/23-Sep 25-Oct 30-Aug 30-Aug 30-Aug Rolled cover crop 25-May 2-Jun 13-Jun 1-Jun 6-Jun 18-Jun Planted cash crop 26-May 3-Jun 14-Jun 1-Jun 6-Jun 18-Jun Rolled cover crop 12-Jun 13-Jun 26-Jun Pitfall trapping 13-Jun 27-Jun 11- Jul 18-Jun 24-Jun 1-Jul 5-Jul High residue cultivation 5-Jul 14-Jul 20-Jul 8-Jul 16-Jul 17-Jul High residue cultivation 14-Jul 20-Jul 28-Jul 12-Jul 18-Jul 19-Jul Harvested cash crop 18-Oct 18-Oct 18-Oct 9-Jul 23-Sep 23-Sep 23-Sep a In this full-entry design, we planted every crop in every year, with a full rotation as follows: hairy vetch and triticale – corn – cereal rye – soybean – wheat

Table 3-2. Total activity-densities by year of ground beetle species representing greater than 1% of total captures, during the three-year experiment.

Trophic % of 2011 2012 2013 Sizea Groupb Total n = 144 n = 144 n = 144 Bembidion quadrimaculatum oppositum (Say) S O 49.05 146 259 471 Chlaenius tricolor tricolor (Dejean) L C 11.42 16 132 56 Poecilus chalcites (Say) L C 7.39 6 12 114 Poecilus lucublandus (Say) L C 3.47 5 3 54 Pterostichus melanarius (Illiger) L O 3.30 9 5 45 Bembidion rapidum (LeConte) S C 2.86 7 25 19 Amara impuncticollis group M G 2.63 1 19 27 Clivina bipustulata (Fabricius) S O 2.02 2 10 24 Pterostichus mutus (Say) L C 1.96 7 2 26 Cicindela sexguttata (Fabricius) L C 1.90 20 9 5 Agonum punctiforme (Say) M O 1.68 5 2 23 Harpalus affinis (Shrank) L G 1.40 6 2 17 Bembidion mimus (Hayward) S C 1.23 5 6 11 Other Carabidae 9.69 24 37 112 Total Number of Individuals 259 523 1,004 Number of Species 26 30 43 a Size classes: S = Small (0 – 5 mm); M = Medium (5 – 10 mm); L = Large (>10 mm) b Trophic Groups: C = Mostly carnivorous; G = Mostly granivorous; O = Mostly omnivorous

Table 3-3. Yearly mean (± SEM) across treatments of response variables tested by mixed effects models. Values with different letters within the same row are significantly different at p<0.05.

2011 2012 2013 n=144a n=144 n=144 Total activity-density 1.80 (0.18) a 3.63 (0.29) b 6.97 (0.53) c Proportion of smallb 0.59 (0.04) 0.55 (0.03) 0.52 (0.03) Proportion of medium 0.05 (0.02) a 0.08 (0.02) ab 0.10 (0.01) b Proportion of large 0.35 (0.04) 0.37 (0.03) 0.38 (0.03) Proportion of carnivoresc 0.32 (0.04) 0.40 (0.03) 0.34 (0.03) Proportion of granivores 0.06 (0.02) 0.07 (0.02) 0.06 (0.01) Proportion of omnivores 0.62 (0.04) 0.53 (0.03) 0.60 (0.03) Species richness 1.10 (0.09) a 1.82 (0.11) b 3.33 (0.20) c Smith-Wilson Evenness 0.41 (0.04) a 0.55 (0.04) a 0.72 (0.03) b a n indicates number of treatment plots (samples) b Size classes: S = Small (0 – 5 mm); M = Medium (5 – 10 mm); L = Large (>10 mm) c Trophic Groups: Carnivores = Mostly carnivorous; Omnivores = Mostly omnivorous; Granivores = Mostly granivorous

Rolled HVTa Rolled Cereal Rye Wheat n = 144 b n = 144 n = 144 Total activity-density 6.74 (0.48) a 2.01 (0.16) b 3.65 (0.39) c Proportion of smallc 0.56 (0.03) 0.50 (0.04) 0.59 (0.04) Proportion of medium 0.10 (0.02) a 0.08 (0.02) b 0.05 (0.01) b Proportion of large 0.34 (0.03) 0.42 (0.04) 0.36 (0.03) Proportion of carnivores d 0.39 (0.03) ab 0.41 (0.04) a 0.27 (0.03) b Proportion of omnivores 0.56 (0.03) 0.52 (0.04) 0.65 (0.03) Proportion of granivores 0.05 (0.01) 0.08 (0.02) 0.08 (0.02) Species richness 3.08 (0.20) a 1.47 (0.11) b 1.71 (0.11) c Smith-Wilson evenness 0.67 (0.03) a 0.51 (0.04) b 0.50 (0.04) b a HVT = Rolled hairy vetch and triticale b n indicates number of treatment plots (samples) c Size classes: S = Small (0 – 5 mm); M = Medium (5 – 10 mm); L = Large (>10 mm) d Trophic Groups: Carnivores = Mostly carnivorous; Omnivores = Mostly omnivorous; Granivores = Mostly granivorous

Termination date Earlya Middle Late n = 48 n = 48 n = 48 Rolled HVT Total activity-density 3.73 (0.43) a 7.10 (0.88) b 9.40 (0.90) c

Proportion of small 0.63 (0.06) a 0.65 (0.04) a 0.41 (0.05) b Proportion of large 0.29 (0.05) a 0.23 (0.02) a 0.47 (0.04) b Proportion of carnivores 0.40 (0.06) ab 0.29 (0.03) b 0.46 (0.04) a Species richness 2.15 (0.24) a 3.19 (0.37) a 3.90 (0.39) b

Rolled Cereal Rye

Proportion of small 0.57 (0.07) a 0.58 (0.07) a 0.39 (0.06) b Proportion of large 0.32 (0.07) a 0.39 (0.07) a 0.52 (0.06) b Proportion of granivores 0.04 (0.02) a 0.03 (0.02) a 0.14 (0.04) b Species richness 1.19 (0.17) a 1.46 (0.19) ab 1.75 (0.20) b

Cultivation treatment HRC b No -HRC n = 72 n = 72 Wheat Proportion of small 0.68 (0.05) a 0.50 (0.05) b Proportion of large 0.26 (0.04) a 0.45 (0.05) b a Early, middle, and late reflect cover crop termination dates in anticipation of cash crop planting at standard dates for each crop in central Pennsylvania. b HRC = High residue cultivation.

Table 3-6. Significant indicator species for each crop and termination date, according to the multipatt function in indicspecies package of R, with the method restricted to selecting only one treatment per species. Trophic Termination Ind. Val Sizea Groupb Cropc Date Sd Fd Statistice Pf Bembidion mimus S C HVT Middle 0.3636 0.1458 0.230 0.020 Bembidion quadrimaculatum oppositum S O HVT Middle 0.1986 0.7708 0.391 0.003 Bembidion rapidum S C HVT Middle 0.3137 0.1875 0.243 0.019 Poecilus chalcites L C HVT Middle 0.2576 0.3333 0.293 0.011 Trechus quadristriatus S O HVT Middle 0.4667 0.1250 0.242 0.009 Agonum punctiforme M O HVT Late 0.5333 0.2780 0.380 0.001 Amara aenea M G HVT Late 0.5000 0.1667 0.289 0.002 Amara impuncticollis group M G HVT Late 0.3404 0.1875 0.253 0.015 Chlaenius tricolor tricolor L C HVT Late 0.5441 0.6667 0.602 0.001 Clivina bipustulata S O HVT Late 0.5000 0.2292 0.339 0.001 Poecilus lucublandus L C HVT Late 0.3226 0.2708 0.296 0.002 Pterostichus mutus L C HVT Late 0.6000 0.2500 0.387 0.001 Cicindela punctulata L C Rye Late 1.0000 0.0625 0.250 0.013 Cicindela sexguttata L C Wheat Early 0.4706 0.2500 0.343 0.001 Harpalus affinis L G Wheat Middle 0.3600 0.1875 0.260 0.005 a Size classes: S = Small (0 – 5 mm); M = Medium (5 – 10 mm); L = Large (>10 mm) b Trophic Groups: Carnivores = Mostly carnivorous; Omnivores = Mostly omnivorous; Granivores = Mostly granivorous c HVT = HVT = Rolled hairy vetch and triticale; Rye = Rolled cereal rye d Specificity (S) is the probability that a site with a specific species belongs to the treatment specified; fidelity (F) is the probability that a species will be found in sites belonging to that treatment (e.g., 100% of Cicindela punctulata were found in late cereal rye, but only 6.25% of the sites contained the species) e Ind. Val Statistic: Indicator value, the product of specificity and fidelity f P = p-value, reports the significant treatment association for a given taxa, based on the highest indicator value for any given treatment

Figures

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Figure 3-3. Rarefaction curve by crop treatment. Overlapping 95% confidence intervals (not shown) indicate the total number of species captured in each crop are not significantly different. HVT = Rolled hairy vetch and triticale, Rye = Cereal rye.

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Chapter 4

Cover crop species and termination alters arthropod community composition and sentinel predation in an organically managed reduced tillage cropping system

Abstract

In organic agroecosystems, the practices that growers use can create habitats that affect arthropods and therefore, biological control potential. We evaluated the effect of cover crop species and termination by a roller-crimper on the ground-dwelling predatory arthropod community and biological control potential in a cropping system in transition to organic production in central Pennsylvania, USA. We compared two cover crop treatments, hairy vetch

(Vicia villosa Roth) planted together with triticale (× Triticosecale Wittmack) and cereal rye

(Secale cereale L.) planted as a monoculture. We terminated the cover crops by roller-crimper on three dates (early, middle, and late) based on cover crop phenology and standard practices for cash crop planting in the area. We characterized the pre- and post-termination ground-dwelling arthropod community using pitfall traps, and assessed biological control potential using sentinel assays with live larvae of the greater waxworm (Galleria mellonella F.). The most abundant predator groups, Araneae, Opiliones, Staphylinidae, and Carabidae were significantly associated with the hairy vetch and triticale cover crop treatment, and total predatory arthropod activity- density was significantly higher in the hairy vetch and triticale treatment than in cereal rye (p <

0.05). Termination or termination date within each of the cover crop treatments did not significantly affect activity-density or diversity of the ground-dwelling predators; however, specific taxa were associated with cover crop stage and termination dates. Biological control potential did not differ significantly between any of the termination date treatments, but 104 environmental variables predicted the rate of predation in each treatment. Our results show that timing of management of a cover crop by roller-crimper at specific times in the growing season affects abundance of target predators. Additionally, managing cover crops by a roller-crimper does not negatively impact generalist arthropod predators prior to cash crop planting, and may be a method for terminating cover crops that conserves predators.

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Introduction

In organically managed cropping systems, winter cover cropping provides many benefits to growers compared to fallow, including the potential to attract and retain predatory arthropods in the field prior to planting of the cash crop, which can have strong implications for pest management during the growing season (Carmona and Landis, 1999; Lundgren and Fergen, 2011;

Shearin et al., 2008; Ward et al., 2011). This potential to augment predatory arthropods is dependent on how growers manage cover crops prior to cash crop planting. One management option involves terminating winter cover crops with a roller-crimper (Mirsky et al., 2013). The roller-crimper simultaneously rolls the cover crop to the ground while crimping stems to kill the plant, creating a mulch layer at the soil surface. This mulch provides a complex habitat for ground-dwelling arthropods, including predatory insects and spiders (Mischler et al., 2010a; Nord et al., 2012; Schmidt and Rypstra, 2010). However, management of the cover crops, including species and timing of termination by rolling, may influence the efficacy of cover crops as a resource for predatory arthropods (Mischler et al., 2010a, 2010b; Ward et al., 2011).

Winter cover crops provide many benefits to organic growers, for example, provision and retention of nitrogen, weed suppression, and reduction in the potential for erosion. Increasingly, cover crops are also recognized for their benefit to beneficial arthropods (Blubaugh and Kaplan,

2015; Clark, 2007; Lundgren and Fergen, 2011). In particular, predatory ground-dwelling arthropods, including spiders (Araneae) and Carabidae (Coleoptera), benefit from the additional complexity that winter cover crops provide through the increase in availability of resources compared to fallow ground (Blubaugh and Kaplan, 2015; Rendon et al., 2015; Ward et al., 2011), including additional prey, a stable and favorable microclimate, and refuge from intraguild predators (Birkhofer et al., 2008; Schmidt and Rypstra, 2010; Shearin et al., 2008). For example,

106 in a mark-recapture study to evaluate the potential for cover crops to conserve weed seed predators, as compared to fallow plots, Shearin et al. (2008) recaptured significantly more

Harpalus rufipes DeGeer (Coleoptera: Carabidae) in plots planted in a rotation with the winter cover crops of oat (Avena sativa L.) and pea (Pisum sativum L.) together, followed by hairy vetch

(Vicia villosa Roth) and winter rye (Secale cereale L.) planted together the following year . The higher recaptures in the cover crop treatment were attributed to more favorable conditions for H. rufipes, including higher humidity and lower temperatures than in the fallow treatment (Shearin et al., 2008).

Although winter cover crops and the mulch created by rolling them is beneficial for augmenting predator populations, little is known regarding the effect of cover crop species and the characteristics of the mulch they create. A grass cover crop, for example, will have different characteristics and provide different resources than a legume, both before and after termination, in that the structure of these crops is different, and thus rainfall, sunlight, and wind will all penetrate the mulch differently (Diehl et al., 2012). Too, herbivorous insects may favor one crop over another, thus altering the potential prey resources for predators (Birkhofer et al., 2008). After termination, the rate at which cover crops decompose, a function of the carbon to nitrogen ratio within the crop, the amount of lignin, etc., will dictate the decomposer community, thus affecting the type and availability of prey for predators associated with various cover crops (Gill et al.,

2011; Ruffo and Bollero, 2003).

Cover crop phenology at termination prior to cash crop planting will also affect the local arthropod assemblage. If, for example, a cover crop is allowed to grow for a longer period of time in the spring, it may accumulate more biomass or have a greater availability of floral resources which may affect interactions throughout the arthropod community (Eisenhauer and Reich, 2012;

Mischler et al., 2010b). Too, due to arthropod phenologies, a cover crop terminated later in the spring may serve to attract or conserve a different community of ground-dwelling predators than

107 one terminated earlier. Depending on community composition, this may or may not prove beneficial to predation (Shrestha and Parajulee, 2010). In particular, timing cover crop termination at a point that corresponds with high numbers of predators that contribute to biological control of insect or weed pests may prove beneficial to organic growers.

The use of cover crops in an organic agroecosystem may influence the local assemblage of arthropods, but effects of cover crops on the function of predatory arthropods also warrants further study. Especially in organically managed systems, where growers largely rely on management practices to suppress pests, a robust ground-dwelling predator population is important in helping growers meet their pest control needs (Letourneau and Bothwell, 2008;

Zehnder et al., 2007). Augmenting the predator population through management is beneficial for organic growers, but so too is augmenting the potential for these predators to contribute to biological control (Lundgren and Fergen, 2011). It is thus critical to understand the effect of cover crop management, in particular species and timing of management, on ground-dwelling predatory arthropods and their potential to contribute to biological control. Accordingly, we examined the effects of cover crop management on the ground-dwelling predatory arthropod community and biological control potential in the final year of the mandated three-year transition to organic management in a grain cropping system. We hypothesized that cover crop species, stage (living or rolled), and timing of termination would influence predatory arthropod activity- density and diversity; carabid activity-density and diversity; predatory arthropod community composition; and biological control potential.

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