Enhanced Berm Habitats Increases the Abundance of Natural Enemies of Insect Pests and Pollinators in the Holland Marsh, Ontario

ENHANCED BERM HABITATS INCREASES THE ABUNDANCE OF NATURAL ENEMIES OF INSECT PESTS AND POLLINATORS IN THE HOLLAND MARSH, ONTARIO

Dillon Brian Muldoon

A Thesis presented to The University of Guelph

In partial fulfilment of requirements for the degree of Master of Science in Environmental Sciences

Guelph, Ontario, Canada

ENHANCED BERM HABITATS INCREASES THE ABUNDANCE OF NATURAL ENEMIES OF INSECT PESTS AND POLLINATORS IN THE HOLLAND MARSH, ONTARIO

Dillon Brian Muldoon Advisors: University of Guelph, 2020 Dr. C. Scott-Dupree Dr. M.R. McDonald

The Holland Marsh (HM), Ontario, is an agroecosystem with a primary focus on carrot and onion production. It contains negligible uncultivated habitat to support beneficial insect populations. Upgrades to the HM drainage system have provided an opportunity to investigate how enhancements to canal berms can affect natural enemies of insect pest populations and pollinators. Five berm sites were established, each with three treatments: (1) unmanaged control; (2) a floral enhancement; and (3) a floral + shrub enhancement. These sites were monitored over two years using both active and passive trapping. Enhanced berm sites did not offer refugia for primary insect pests, and positively affected the abundance of some natural enemies and insect pollinator groups.

Future research should examine: the efficacy of natural enemies in reducing primary insect pest population; and, the relative floral attractiveness of planted floral treatments to bee species to better understand how management strategies can support threatened non-Apis bees.

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ACKNOWLEDGEMENTS I want to express my gratitude to my co-advisors, Drs. Cynthia Scott-Dupree and

Mary-Ruth McDonald, who gave me the opportunity to do my MSc under their guidance.

Thank you both for your advice, support, the many opportunities to travel to and present at scientific conferences, and your backing of my outreach event efforts. I am also grateful to my committee members Drs. Tara Garipey and Lora Morandin for their advice, guidance and support throughout my research journey. To Drs. Andrew Frewin,

Gard Otis, and Angela Gradish for your consultation on statistics and methodology.

I would like to thank the funding agencies: Ontario Agri-Food Innovation, Bayer

CropScience, Syngenta Canada Inc., Bradford Co-op Storage Ltd., Fresh Vegetable

Growers of Ontario, and Pollinator Partnership, to whom without your assistance this project would not have been made possible.

For the invaluable assistance over the past two years on this project from the installation and maintenance of the berm sites, to your support of berm day, technical advice and everything in between, I would like to thank Kevin Vander Kooi, Laura

Riches, Zach Telfer, Tyler Blauel, Shawn Janse, and the rest of the Muck Crop

Research Station staff.

This project would not have been possible without the assistance and cooperation of several people. I would first like to thank my student field/lab assistants

Claire Penstone, Brooke Freestone, Kaitlyn Raine, and Gavin Hossack for their hard work, and dedication to this project. I would like to thank the municipalities of Bradford

West Gwillimbury, and King Township, the county of Simcoe, and the Lake Simcoe

Regional Conservation Authority, especially Avia Eek for their support of this project.

Thank you to Dr. Paul Hoekstra, for assistance in procuring native wildflower seed mix for our outreach day.

To my lab mates, colleagues and friends in the Scott-Dupree, Hallett labs and around the university, thank you for your friendship and support in the ups and downs of this journey. A big thank you to Erika DeBrouwer for being one of the first friends I made in Guelph, you were always there when I needed someone to talk to and showed me the ropes at the Ranch. I would particularly like to thank my MSc partner in crime

Alexandra Stinson-Dacey for always being there with a joke and a smile to keep me going.

I want to especially thank Dr. Angela Gradish for her mentorship and support throughout my thesis. Angela, I am incredibly grateful for everything that you have done for me. You were always there to offer advice, assistance and support during my project through the good times and the bad ones. I will be forever indebted to you for your faith in me and everything that you helped me with. Thank you for being a friend!

To my family, Keegan Muldoon, Mercedes Mueller, Brigid and John Witzke and baby Henry thank you for always being there to listen and provide encouragement to keep me pushing forward.

To my good friend Emma Somerville, wow, who would have thought after meeting in the third year of undergrad we would both be finishing our masters now? I cannot thank you enough for being there for me through the ups and downs. From our late night facetimes to helping me at Bug Day you have always been there with your smile and encouraging words of wisdom. I am looking forward to what comes next and

I’m grateful that wherever it takes us both we will always have each other’s back. To my partner, Nick, thank you for patience with me, my stress and my moods during this final crunch, looking forward to what the future holds.

Finally, a tremendous thank you to my parents, Jackie and Joe for supporting me and my goals. Mom and Dad, I cannot express how lucky I am to have such supportive and loving parents, who offer unwavering encouragement. I am eternally grateful for everything you do for me and the opportunities that you have given me. Without your love, guidance, support and encouragement I would not be the person I am today.

TABLE OF CONTENTS

Abstract ...... ii

Acknowledgements ...... iii

Table of Contents ...... vi

List of Tables ...... ix

List of Figures ...... xi

List of Abbreviations ...... xv

CHAPTER 1 ...... 1

LITERATURE REVIEW ...... 1

1.0 Introduction ...... 1

1.1 Enhancements of Uncultivated Habitat ...... 4

1.2 Conservation Biological Control ...... 8

1.3 Primary Insect Pests and Natural Enemy Interactions at the Holland Marsh ...... 9

1.3.1 Insect Pests of the Holland Marsh ...... 9

1.3.2 Natural Enemies of the Holland Marsh Pests ...... 14

1.4 Pollinator Conservation ...... 19

1.4.1 Bees ...... 21

1.4.2 Other Pollinators ...... 23

1.4.3 Monarch Butterflies ...... 24

1.5 Summary and Objectives ...... 26

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CHAPTER 2 ...... 28

SUPPORTING CONSERVATION BIOLOGICAL CONTROL IN THE HOLLAND MARSH, ONTARIO ...... 28

2.0 Abstract ...... 28

2.1 Introduction ...... 28

2.2 Materials and Methods ...... 33

2.2.1 Berm Site Enhancements ...... 33

2.2.2 Berm Survey ...... 37

2.2.3 Commercial Field Survey ...... 45

2.2.4 Parasitoid Collection – Carrot Root Sections ...... 46

2.3 Statistical Analysis ...... 48

2.4 Results ...... 49

2.4.1 Berm Survey ...... 49

2.4.2 Commercial Field Survey ...... 68

2.4.3 Parasitoid Collection – Carrot Root Sections ...... 72

2.5 Discussion ...... 73

CHAPTER 3 ...... 84

SUPPORTING POLLINATOR CONSERVATION IN THE HOLLAND MARSH, ONTARIO ...... 84

3.0 Abstract ...... 84

3.1 Introduction ...... 85

3.2 Materials and Methods ...... 90

3.2.1 Berm Site Enhancement ...... 90

3.3 Statistical Analysis ...... 95

3.4 Results ...... 97

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3.5 Discussion ...... 113

CHAPTER 4 ...... 122

GENERAL CONCLUSION ...... 122

References ...... 127

Appendices ...... 143

Appendix A: Randomly assigned berm treatments from left to right when viewed head on from the road at each site...... 143

Appendix B: Random site visitation schedule from 1 May to 19 September 2018...... 143

Appendix C: Random site visitation schedule from 1 May to 3 September 2019...... 144

Appendix D: Type III Test of Fixed Effects Table ...... 144

Appendix E: Newspaper clippings from the Bradford Today about the canal berms in the Holland Marsh, Ontario...... 147

LIST OF TABLES

Table 2.1: List of Carabidae taxa and number of individuals captured in berm site treatments at the Holland Marsh, Ontario from 1 May to 3 September, 2018. Dominant species are in bold...... 59

Table 2.2: List of Carabidae taxa and number of individuals captured in berm site treatments at the Holland Marsh, Ontario from 1 May to 3 September, 2019. Dominant species are in bold ...... 60

Table 2.7: Number of taxa, total abundance, and Simpson’s Diversity Index for commercial carrot fields at the Holland Marsh, Ontario from 31 May to 26 September, 2018...... 70

Table 2.8: Number of taxa, total abundance, and Simpson’s Diversity Index for commercial carrot fields at the Holland Marsh, Ontario from 6 June to 29 August, 2019...... 71

Table 3.1: Area in hectares, of land use classes from the centroid of each canal berm site, at a radius of 750 m in the Holland Marsh, Ontario...... 97

Table 3.2: Area in hectares, of land use classes from the centroid of each canal berm site, at a radius of 2000 m in the Holland Marsh, Ontario...... 98

Table 3.3: Observed bloom period from floral species planted in canal berm enhancements, from July to September 2018, and May to August, 2019 in the Holland Marsh, Ontario...... 104

Table 3.4: Observed bloom period from floral species present in canal berm seed banks, from July to September 2018, and May to August, 2019 in the Holland Marsh, Ontario...... 105

Table 3.5: List of insect pollinator taxa and number of individuals captured by aspiration in berm site treatments at the Holland Marsh, Ontario from 10 July to 19 September, 2018...... 109

LIST OF FIGURES

Figure 1.1: Map showing the location of the Holland Marsh, Ontario...... 3

Figure 1.2: (A) Injury caused by carrot weevil (Listonotus oregonensis) larvae in carrot roots - large tunnels in the top third of the root; (B) injury caused by carrot rust fly (Psila rosae) larvae in carrot root – small tunnels toward the bottom of the root...... 12

Figure 2.1: Map of the location of the Muck Crop Research Station (MCRS) [red star] and the five replicate berm sites [yellow dots] established between 2017 and 2018 at the Holland Marsh, Ontario...... 34

Figure 2.2: Diagram of generalized berm site enhancements, with site and treatment dimensions and planting arrangements...... 36

Figure 2.3: (A) Diagram of a Vernon pitfall trap; (B) A Vernon pitfall trap placed in the ground in a treatment at a Holland Marsh canal berm site...... 38

Figure 2.4: (A) An open Boivin trap with carrot root; (B) A closed Boivin trap in a carrot field. (Photo Credit: D. Van Dyk)...... 40

Figure 2.5: (A) An orange-yellow sticky trap used to monitor CRF; (B) A yellow sticky trap used to monitor OM and parasitoid wasp...... 42

Figure 2.6: Diagram of both trap placement within berm sites in 2018. The traps were placed in all treatments but have been spread out for easier visualization...... 43

Figure 2.7: Diagram of both trap placement within berm sites in 2019. The traps were placed in all treatments but have been spread out for easier visualization...... 44

Figure 2.8: Map showing the location of the Muck Crop Research Station (MCRS) [red star] and the eight commercial carrot fields surveyed in 2018 (A-D) [yellow] and 2019 (E-H) [blue] at the Holland Marsh, Ontario...... 45

Figure 2.9: Carrot root sections placed in a carrot field to monitor carrot weevil oviposition and egg parasitism. (Photo credit: Z. Telfer)...... 47

Figure 2.10: (A) Carrot root sections collected from carrot fields at the Holland Marsh were placed in modified Ziploc containers; (B) Insect rearing cages with carrot root section and yellow sticky card traps...... 48

Figure 2.11: Mean(±SE) abundance of Carabidae, beneficial predator, trapped per week over the season in Vernon pitfall traps from 1 May to 3 September 2018 at the Holland Marsh, Ontario. Significant differences among treatments are indicated by different letters according to Tukey’s HSD (α=0.05)...... 51

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Figure 2.12: Mean(±SE) abundance of Carabidae, beneficial predator, trapped per week in Vernon pitfall traps from 1 May to 3 September 2018 at the Holland Marsh, Ontario. Significant differences among treatments within weeks are indicated by different letters according to Tukey’s HSD (α=0.05). No significant difference found among treatments within groups are indicated by *ns (α=0.05)...... 52

Figure 2.13: Mean(±SE) abundance of Carabidae, beneficial predator, trapped per week over the season in Vernon pitfall traps from 1 May to 3 September 2019 at the Holland Marsh, Ontario. Significant differences among treatments are indicated by different letters according to Tukey’s HSD (α=0.05)...... 53

Figure 2.14: Mean(±SE) abundance of Carabidae, beneficial predator, trapped per week in Vernon pitfall traps from 1 May to 3 September 2019 at the Holland Marsh, Ontario. Significant differences among treatments within weeks are indicated by different letters according to Tukey’s HSD (α=0.05). No significant difference found among treatments within groups are indicated by *ns (α=0.05)...... 54

Figure 2.15: Mean(±SE) abundance of Staphylinidae, beneficial predator, trapped per week over the season in Vernon pitfall traps from 1 May to 3 September 2019. No significant difference was found among any of the treatments (α=0.05)...... 55

Figure 2.16: Mean(±SE) abundance of Staphylinidae, beneficial predator, trapped per week in Vernon pitfall traps from 1 May to 3 September 2019 at the Holland Marsh, Ontario. No significant difference was found among any of the treatments (α=0.05). ... 56

Figure 2.17: Rarefaction curves for three berm treatments (Control, Floral and Floral + Shrub) surveyed with Vernon pitfall traps for Carabidae predators of insect pests of marsh crops at the Holland Marsh, Ontario, 2018...... 62

Figure 2.18: Rarefaction curves for three berm treatments (Control, Floral and Floral+Shrub) surveyed with Vernon pitfall traps for Carabidae predators of insect pests of marsh crops at the Holland Marsh, Ontario, 2019...... 63

Figure 2.19: Mean(±SE) abundance of aster leafhopper, primary insect pest, trapped per sweep from 25 June to 27 August 2018. Significant differences among treatments within weeks are indicated by different letters according to Tukey’s HSD (α=0.05)...... 65

Figure 2.20: Mean(±SE) abundance of onion maggot (OM) adults, primary insect pest, trapped per sweep from 3 July to 29 August 2019. Significant differences among treatments within weeks are indicated by different letters according to Tukey’s HSD (α=0.05)...... 66

Figure 2.21: Mean(±SE) abundance of tarnished plant bug (TPB), primary insect pest, trapped per sweep from 9 June to 29 August 2019. No significant difference was found among any of the treatments (α=0.05)...... 67

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Figure 2.22: Mean(±SE) abundance of Mymaridae, beneficial parasitoids, trapped per week on yellow sticky traps from 14 May to 3 September, 2019. No significant difference was found among any of the treatments (α=0.05)...... 68

Figure 2.23: Rarefaction curves for four commercial carrot fields surveyed with Vernon pitfall traps for Carabidae, predators of insect pests of marsh crops at the Holland Marsh, Ontario, 2018...... 71

Figure 2.24: Rarefaction curves for four commercial carrot fields surveyed with Vernon pitfall traps for Carabidae, predators of insect pests of marsh crops at the Holland Marsh, Ontario, 2019...... 72

Figure 2.25: Carrot weevil oviposition scars and parasitoid emergence from carrot root sections collected from the MCRS at the Holland Marsh, Ontario from 10 June to 13 August, 2019...... 73

Figure 3.1: Grower fields in the Holland Marsh, Ontario. (Photo credit: Higheye)...... 89

Figure 3.2: Buffer with 750 m a radius from the centroid of each canal berm site at the Holland Marsh, Ontario. Land use data has been clipped to these buffers and separated into three land classes...... 99

Figure 3.3: Buffer with 2000 m a radius from the centroid of each canal berm site at the Holland Marsh, Ontario. Land use data has been clipped to these buffers and separated into three land classes...... 100

Figure 3.4: NMDS ordinal depicts the relationship of blooming floral community composition among canal berm sites and treatments, from 10 July to 19 September, 2018...... 102

Figure 3.5: NMDS ordinal depicts the relationship of blooming floral community composition among canal berm sites and treatments, from 6 June to 29 August, 2019...... 103

Figure 3.6: Mean(±SE) abundance of honey bees, bumblebees, solitary bees, and hoverflies, observed from 10 July to 19 September, 2018. No significant difference was found among any of the treatments within groups (α=0.05)...... 108

Figure 3.7: A bipartite pollinator network displaying pollinator group (left) interactions with specific floral species (right) in the Holland Marsh, Ontario from 10 July to 19 September, 2019. Line width is relative to the number of observations of the interactions between pollinator groups and floral species...... 110

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Figure 3.8: Mean(±SE) abundance of honey bees, bumblebees, solitary bees, and hoverflies, collected by sweep netting from 6 June to 29 August, 2019. Significant differences among treatments within groups are indicated by different letters according to Tukey’s HSD (α=0.05). No significant difference found among treatments within groups are indicated by *ns (α=0.05)...... 113

LIST OF ABBREVIATIONS

HM – Holland Marsh

MCRS – Muck Crops Research Station (University of Guelph)

SI – sustainable intensification

CBC – conservation biological control

CW – carrot weevil(s), Listonotus oregonenesis

CRF – carrot rust fly(ies), Psila rosae

OM – onion maggot(s), Delia antiqua

ALH – aster leafhopper(s), Macrosteles quadrilineatus

TPB – tarnish plant bug(s), Lygus lineolaris

OPHAP – Ontario Pollinator Health Action Plan

IPM – integrated pest management cv. – cultivar

ETOH – ethanol

CRS – carrot root section(s)

GLMM – generalized linear mixed model

GIS – Geographic information system

NMDA – non-metric multidimensional scaling

CHAPTER 1

LITERATURE REVIEW

1.0 Introduction

Current agricultural production methods must be adapted in order to provide a

resilient and sustainable food system that meets the requirements of a growing

population and environmental and economical sustainability. Production methods

continue to integrate technological advances (Mulla 2013, Hamel and Saindon

2017), ecosystem services (Thies and Tscharntke 1999, Gardiner et al. 2009,

Tscharntke et al. 2012, Morandin et al. 2014, Zalucki et al. 2015), and economics

(Naranjo et al. 2015) to create a more resilient and profitable production system.

One sustainable approach is to utilize uncultivated habitat to provide ecosystem

services to cultivated crop land. The objective is to maintain yields and reduce inputs

(Petit and Usher 1998, Öckinger and Smith 2007, Letourneau et al. 2011).

Landscapes where intensive agricultural is practiced, such as the Holland Marsh

(HM) in southern Ontario, could benefit from the utilization and management of

uncultivated habitat, to enhance sustainable vegetable production in this unique

agroecosystem.

1.0.1 Holland Marsh

The HM (Figure 1) is a mixed-use wetland of approximately 7400 ha, located 50

km north of Toronto, Ontario. Intensive agricultural production takes place in

approximately 60% of the total wetland area (Classens 2016). The cultivated land is

approximately 3000 ha and comprised of some of the most fertile organic black soil

in Canada, known as muck soil (Bartman et al. 2007). Muck soil is defined as a 1

sequence of more than three layers of undifferentiated types of organic material that is comprised of >30% organic matter by weight, with a humic texture and a pH of 5.6

– 7.4 (CanSIS 2013). Carrots and onions are the primary crops grown in the HM and are produced on 70-80% of the total cultivated area. However, 60 other crops including celery, leafy greens, and several Asian vegetables are also grown in the area (Bartman et al. 2007). The region accounts for more than 60% of the province’s total carrot (approximately 150,000 metric tonnes) and onion (approximately 100,000 metric tonnes) production (AAFC 2017, 2018). This agroecosystem is economically important to the province and generates over $1B CAD annually from the sale of crops that are produced there. Producers rely on a network of berms, canals, and pump houses to keep the cultivated land drained, and viable for production (Bartman et al. 2007).

The draining of the HM began in 1925, with a canal and berm system that spanned 28 km. The system has two main canal areas (north and south), both having associated berms and pumping stations. There are 228 km of drains in the system that divert the Schomberg branch of the Holland River around the drained marshland (Bartman et al. 2007). The HM Drainage System Canal Improvement

Project began in 2010 and was completed in 2016. This project was designed to improve safety and efficiency of the canal/berm system, through the expansion of 10 km of berms, and the relocation and clearing/dredging of 19 km of canals (Holland

Marsh Drainage System 2018). These improvements to the canal drainage system were the first since the 1950s and have aided in keeping the land drained for crop

production. Apart from canal berms, there is little to no uncultivated habitat in the HM

(e.g., hedgerows) to support ecosystem services provided by beneficial insects (e.g., pollinators and natural enemies). The improvements and expansion of the berms provided the opportunity to add plants to support ecosystem services offered by beneficial insects, contributing to the long-term sustainability of this unique agroecosystem.

Figure 1.1: Map showing the location of the Holland Marsh, Ontario. 3

1.1 Enhancements of Uncultivated Habitat

Over the past century, the agricultural landscape has expanded and become

more intensive and simplified (Foley et al. 2005, Bianchi et al. 2006). Intensively

managed cropping systems can produce massive amounts of food, but this has

occurred at the cost of diminishing other ecosystems that surround the agricultural

landscape (Foley et al. 2005) with reduced non-crop habitat and increased habitat

fragmentation within these landscapes (Bianchi et al. 2006).

Moving forward, agroecosystems will need to be more sustainable in providing

positive impacts to the environment, economy, and social capital; the three pillars of

sustainability (Van Cauwenbergh et al. 2007). One-way agroecosystems can

achieve positive environmental impacts is through sustainable intensification (SI).

Pretty and Bharucha (2014) defined SI as the ways in which the agricultural yields

are increased without: (1) having an adverse effect on the surrounding environment;

or, (2) the conversion of non-crop habitat to agricultural land. Current views on

creating sustainable agroecosystems suggest that there is importance to both the

enhancement and conservation of non-crop habitats, for the diversity and ecosystem

services they provide to the agricultural landscape.

The enhancement of uncultivated habitat involves the manipulation and alteration

of areas surrounding an agroecosystem to improve the availability of resources

required by beneficial insects for optimal or increased performance (Altieri and

Letourneau 1982, Landis et al. 2000). These changes should enhance the

reproduction, survival, longevity, and efficiency of beneficial insects (Letourneau and 4

Altieri 1999, Eilenberg et al. 2001). Both active and passive restoration has been shown to increase both biodiversity and ecosystem services in a wide range of ecosystems throughout the world (Benayas et al. 2009). In an intensive agroecosystem, the restoration and enhancement of uncultivated habitats has been shown to support natural enemies (Morandin et al. 2014, Blaauw and Isaacs 2015,

Sorribas et al. 2016, Garratt et al. 2017) and pollinators (Wratten et al. 2012,

Morandin and Kremen 2013, Garratt et al. 2017) which help provide ecosystem service to adjacent crops.

The actions of active restoration or enhancement to an ecosystem cannot be implemented without incurring a financial cost, and therefore, to increase its adoption and implementation will require financial incentives (Benayas et al. 2009).

Cost-benefit analyses allow practitioners to analyze both the ecological and economic pathways to maximize the return on investment (Goldstein et al. 2008).

Morandin et al. (2016) looked at the cost-benefit analysis of the restoration of hedgerows in intensive agricultural landscapes and found that over time small-scale restoration to uncultivated habitat can be profitable. With an investment of $4000

USD for the restoration of a 300m hedgerow, the model determined that it would take anywhere from five to sixteen years for a grower to break even, depending on factors such as the crop rotation and availability of financial incentives through governmental funding (Morandin et al. 2016).

In Ontario, there are government assistance programs for restoration and enhancement of non-crop habitat including tax credits and grants, such as, The 5

Great Lakes Agricultural Stewardship Initiative. This grant program offers producers cost-sharing incentives for several best management practices for their agroecosystem. In addition to governmental initiatives, several non-governmental organizations (NGOs) offer grants to improve non-crop habitat in agroecosystems including Pollinator Partnership, Farms at Work, and Alternative Land Use Services

(ALUS) Canada. Local conservation authorities also offer grants and cost-sharing initiatives to improve habitat and riparian areas in agroecosystems. These incentives aim to restore, enhance, and increase non-crop habitats that in turn provide benefits and services to both natural and agroecosystems. Improvement to non-crop habitats, which include berms, hedgerows, and riparian zones in proximity to agroecosystems offer several ecosystem services. These are not only limited to increasing beneficial insect such as natural enemies and pollinators, but can also offer reduced nutrient loading to streams, increase of soil carbon sequestration, erosion control, and wind breaks in the agroecosystems (Clerici et al. 2014).

The completion of the HM Drainage System Canal Improvement Project in 2016 increased the area of non-crop habitat within the HM. These berm improvements provide an opportunity to increase and enhance biodiversity within the ecosystem and the ecosystem services, such as, natural biological controls, habitat, and support for other insect populations.

Although little work has been published on the pest problems associated with agroecosystem revitalization, for producers it is often one of the first questions posed. Liere et al. (2017) investigated the interactions of biodiversity conservation, 6

agroecology, and ecosystem services and emphasized the importance of careful consideration about the type of enhancements used in agroecosystems as they may provide refugia for insect pests. In California, research on native plant hedgerows has shown that enhancements did not increase insect pests and improved the ratio of beneficial insects to insect pests (Morandin et al. 2014). Insect pests were lower in native hedgerow enhancements than in weedy field edges (Morandin et al. 2014).

The current belief that non-crop habitats harbour pest populations is strong amongst growers and it can be difficult to sway their opinions without concrete evidence within their agroecosystem on a large scale (Kleijn et al. 2018, Griffiths et al. 2008).

Although research has demonstrated that the enhancement of non-crop habitat can increase beneficial insects without increasing insect pests, growers have a right to be cautious about the implementation of enhancements to land surrounding their agroecosystems. Caution must be taken in the selection of plants used in enhancements, and local work is needed to inform best management practices for the creation of non-crop habitat. Researchers have an important job to assess both the benefits and possible detriments that could arise from non-crop habitat enhancement. With increased research and understanding of the complex interactions in a region between crop and non-crop habitats we can offer growers targeted recommendations based on best management practices that would increase the ecosystem services provided while decreasing possible refugia for pest populations in a particular region.

1.2 Conservation Biological Control

Conservation biological control (CBC) is the protection of natural enemies

against adverse effects such as pesticides, incompatible cultural practices, and

improving their efficiency by providing resources (Eilenberg et al. 2001). The use of

CBC relies on the practitioners’ in-depth understanding of the life history of natural

enemies and the complex communities in which they reside within the

agroecosystem (Jonsson et al. 2008). Many predators and parasitoids provide

essential ecosystem services in terms of controlling pest populations in an

agroecosystem like the HM. In turn, the abundance and diversity of these natural

enemies can be influenced by surrounding non-crop habitat in agroecosystems

(Gardiner et al. 2009, Bertrand et al. 2016). The conservation, enhancement, and

management of non-crop habitats aim to support natural enemies by offering refuge

and sources of forage at different life stages.

Research on CBC is extremely important, as each agroecosystem is different in

terms of crop production practices, location, landscape complexity, and associated

pests and natural enemies. As such, understanding the ecology of a given

agroecosystem can dictate what possible enhancements can provide the ecosystem

services required by a specific producer and result in a positive outcome. Gardiner

et al. (2009) studied CBC of Coccinellidae in soybean production systems in north-

central US and determined that landscapes with more abundant grasslands and

forest surrounding cultivated fields resulted in a greater abundance of Coccinellidae

and increased suppression of an aphid pest - Aphis glycines. Research by Ramsden

et al. (2015), on winter wheat fields in the UK, determined that diverse non-crop

habitats that included floral resources, provided important forage that increased the

rate of parasitism by parasitoids and the abundance of predators. The use of CBC is

not limited to field crops, studies in both citrus fruit tree production (Sorribas et al.

2016) and vegetable production (Morandin et al. 2014, Letourneau et al. 2015) have

shown that the management of non-crop habitat surrounding agricultural systems

plays an important role for both the abundance and diversity of natural enemies.

Research and reviews on improving CBC have looked at the effects that landscape

complexity, scale, management, structure, and functions of non-crop habitats have

on natural enemy complexes (Bianchi et al. 2006, Griffiths et al. 2008, Holland et al.

2016). The complex interactions between natural enemy and insect pest

communities may result in different recommendations to improve CBC based on the

agroecosystem. This research indicates the importance of understanding how CBC

can best service the type of agroecosystem being studied and how little is known

about the natural enemy – insect pest complex interactions.

1.3 Primary Insect Pests and Natural Enemy Interactions at the Holland Marsh

1.3.1 Insect Pests of the Holland Marsh

Carrot Weevil

Carrot weevil (CW), Listronotus oregonensis (Le Conte) (Coleoptera:

Cuculionidae) was first detected in Apiaceae species in Ohio and Illinois (Chandler

1926, Harris 1926, Pepper and Hagmann 1938) during the 1920s. Currently, CW is

present across northeastern North America (Telfer et al. 2018, Justus and Long

2019) and in Canada has caused field damage that exceeds 40% of total carrot field

yield (Boivin 1985, Telfer et al. 2018). The damage to carrots is visible in the upper

third of the root and is caused by CW larval feeding (Boyce 1927, Boivin 1988). The

tunneling damage caused by CW larva is distinct in that the tunnels are large and

extend downward from the carrot crown (Fig 2.1a). Carrot weevil causes direct yield

loss to the harvestable portion of the crop and an increased economic burden for

carrot grading. Until recently, CW was considered a univoltine pest (Stevenson and

Boivin 1990), but research provides strong evidence of a second generation of CW

(Stevenson 1977, Boivin 2013, Telfer et al. 2018).

Carrot Rust Fly

Carrot rust fly (CRF), Pslia rosae (Fab.) (Diptera: Psilidae) is native to Europe

and was introduced to North America in 1885. The larval stage of the CRF causes

damage to carrots when they enter the taproot to feed on the cortex tissue resulting

in rust coloured mines/tunnels as a result of frass deposition (Capinera 2001). The

mines of CRF are thin and tunneling typically moves horizontally across the carrot

root (Fig 2.1b) and are generally seen lower on the carrot (Jones 1979), making the

injury caused by CRF distinct to that caused by CW. Carrot rust fly is a multivoltine

pest in Ontario with two complete generations and the possibility of a third

incomplete generation depending on weather (Stevenson 1983, Boivin 1987). Mines

made by CRF reduce marketable yields and can make grading carrots a time-

consuming process. If too many carrots are affected, the packaging plant may reject

a whole field. Damage caused by CRF can be highly variable from year to year and

within a field. Losses to carrot crops have been reported to be between 30-60% in the UK (Dufault and Coaker 1987) and as much as 100% damage to crops in

Quebec (Lemay 2017). Research by Telfer et al. (2018) at the HM, indicated in the

2015 and 2016 field seasons pest pressure for CRF was low with the highest injury rating being 2.0% (±0.9) in 2015 and no injury being found in 2016.

Onion Maggot

Onion maggot (OM), Delia antiqua (Meigen) (Diptera: Anthomyiidae) is an

economically important insect pest of onion (Allium cepa L.) crops throughout its

growing regions in the northern hemisphere. The pest was introduced to North

America in the 19th century (Lossjes 1976) and has since spread throughout the

continent becoming a primary pest of onion in Canada, especially those grown on

muck soil (Perron 1972, McDonald et al. 2002). Onion maggot is multivoltine having

three generations per year; onions are most susceptible to injury by the first

generation, when OM larvae injure seedlings, which can result in stand loss. The

second and third generation larvae do not kill plants, but bulb injury makes onions

unmarketable and can lead to secondary infections by fungi or bacteria (Lossjes

1976, Whitfield et al. 1985, Brewster 1994, McDonald et al. 2002).

Aster Leafhopper

Aster leafhopper (ALH), Macrosteles quadrilineatus (Forbes) (Hemiptera:

Cicadellidae) are a vector of aster yellows disease (Macrosteles phytoplasma),

which can cause extensive damage in HM grown vegetables including lettuce,

celery, and carrots (Chaput and Sears 1998, Goodwin et al. 1999). Aster

leafhoppers have three to five generations in southern Ontario. Adult ALH cannot

overwinter in the Great Lakes region but can overwinter as eggs in the leaf tissue of

plants (Hagel and Landis 1967, Goodwin et al. 1999). Long distance spread of ALH

from the southern US can happen in some years and these populations often have a

higher percentage infected with the aster yellows pathogen (Chaput and Sears

1998, Goodwin et al. 1999). Research by Beanland et al. (2000) found that ALH

infected by the aster yellows pathogen lived longer and laid more eggs than ALH

who were not infected. Aster yellows disease outbreaks in the HM have caused 15-

50% losses to lettuce, due to crop damage such as chlorosis, stunting, and

branching (Chaput and Sears 1998,).

Tarnished Plant Bug

Tarnished plant bug (TPB), Lygus lineolaris (Palisot de Beauvois) (Hemiptera:

Miridae) is a pest of celery, lettuce, and other brassicas grown in the HM (Young

1986). Tarnished plant bugs have three to five complete generations in Ontario per

year. Early damage symptoms in celery can appear as yellowing or wilted leaves;

this is usually followed by a secondary bacterial infection causing large necrotic

lesions and rot (Chaput and Uyenaka 1998). Feeding by TPB in lettuce can reduce

the marketability and result in predisposition to secondary bacterial infections.

Feeding is primarily found on the midribs of leaves (Chaput and Uyenaka 1998).

1.3.2 Natural Enemies of the Holland Marsh Pests

The use of natural enemies of Marsh pests through CBC could be helpful in

reducing and/or maintaining pest numbers at low levels in the HM agroecosystem.

Most of the important insect pests including CW, CRF, and OM live the majority of

their lifecycle in close proximity to the soil, which provides opportunities for predation

from natural enemies. Several predators and parasitoids have been identified as

natural enemies of primary insect pests in the HM agroecosystem, although more

research is needed to improve our understanding of these natural enemy - insect

pest complexes.

Predators

Ground beetles (Coleoptera: Carabidae) are generalist predators that prey on

CW (Baines et al. 1990, Zhao et al. 1990), CRF (Wright et al. 1947, Burn 1982), and

OM (Tomlin et al. 1985, Grafius and Warner 1989). These ground beetle predators

have a cosmopolitan distribution and exhibit species diversity in both size and

feeding patterns, which makes them ideal natural enemies to study in conjunction

with CBC.

Field collections by Baines et al. (1990) and Zhao et al. (1990) from Ste. Clotilde,

Quebec determined that there were many predator species present during CW

oviposition in muck soil agroecosystems including Pterostichus melanarius (Illiger),

Poecilus lucublandus (Say), Bembidion quadrimaculatum oppositum (Say), Clivina

fossor L.), and Anisodactylus sanctaecrucis (Fabricius). Laboratory feeding trials

concluded that P. melanarius consumed the greatest number of CW at the larval and

pupal stages. It was also observed that B. quadrimaculatum oppositum would not

prey on CW eggs that were laid on carrot plant foliage (Zhao et al. 1990).

Choice and no-choice food bioassays were conducted for the five common

species of carabids found in muck soil using CW egg, fourth instar larvae, pupae,

and adults (Baines et al. 1990). In no-choice tests, all species consumed egg, fourth

instar larvae and pupae; P. melanarius was the only species that consumed adult

CW. In no-choice tests, the smaller carabids (C. fossor and B. quadrimaculatum

oppositum) were the best egg predators, consuming significantly more CW eggs

then the other three species, and all five carabid species tested were efficient

predators of fourth instar larvae and pupae, consuming between 80 – 98% consumption (Baines et al. 1990). In choice tests, B. quadrimaculatum oppositum and A. sanctaecrucis preferred CW pupae, and P. lucublandus preferred fourth instar larvae (Baines et al. 1990). The researchers also observed in voracity tests that P. melanarius and P. lucublandus consumed three times more when presented their preferred CW life stage than B. quadrimaculatum oppositum and A. sanctaecrucis (Baines et al. 1990).

In comparison, is it believed there are 60 to 100 species of Carabidae that prey on CRF in the UK (Burn 1980). The main egg predators are B. quadrimaculatum oppositum and Trechus quadrustriatus (Shrank). However, Burn (1982, 1984) suggested that egg predation was unlikely to play a significant role in mitigation of

CRF populations. Over 20 species of Carabidae are believed to prey on the OM including: B. quadrimaculatum oppositum which prefers OM eggs, and first instar larvae (Grafius and Warner 1989), P. lucublandus, Agonum muelleri (Herbst),

Bembidion tetracolum (Say), Bembidion oblongum (Serville), and Trechus incurvus

(Say) which consumed both the egg and larval stages (Tomlin et al. 1985).

Lemay et al. (2018) measured the abundance and diversity of ground-dwelling beetles in the HM in 2015 and 2016. They showed that even under the intensive agricultural practices found in the HM, there is an established predator population within the agroecosystem. Currently the effectiveness of ground beetle predators on reducing HM insect pest populations is unknown, and more work is needed to determine if they are negatively affecting these pests in field realistic settings.

Within muck soil, agricultural production areas, such as the HM, there are many

generalist predators that could predate on CW, CRF, OM, ALH, and TPB. These

potential predators include true bugs (Hemiptera: Anthocoridae, Anthomyiidae,

Reduvidae, and Nabidae), beetles (Coleoptera: Coccinellidae and Staphylinidae),

lacewings (Neuroptera: Chrysopidae) (Chaput 1996), and spiders (Araneae) (Pluess

et al. 2010). In the HM agroecosystem these predators have not been well studied.

More research is needed to gather information on how to conserve these predators

in the agroecosystem and how they benefit the production of HM crops as a result of

pest mitigation.

Parasitoids

In Ontario there are two known species of parasitoid wasps which parasitize CW

- Anaphes listronoti (Huber) and Anaphes victus (Huber) (Hymenoptera: Mymaridae)

(Cormier et al. 1996). In Ontario and Quebec, A. listronoti can be found in regions

where muck soils are common, whereas A. victus was only present in the HM

(Cormier et al. 1996). Anaphes listronoti is an egg parasitoid of CW, which produces

four to six generations during the CW oviposition period. The field rate parasitism of

CW eggs can reach 50-90% during higher egg density of 1-2 CW eggs per plant

(Collins and Grafius 1986 a & b, Boivin 1993). In the HM agroecosystem, both

species of Anaphes complete one to three generations before CW oviposition begins

as they emerge before the pest (Cormier et al. 1996). Little research has been

conducted on the assessment of parasitism rates by these two Anaphes species in

the HM since the mid-1990s. In 2015 and 2016, Telfer (2017) conducted a study in

the HM involving placement of carrot roots inoculated with CW eggs in the field but was only able to rear out three A. listronoti in the two seasons of the study.

Research needs to continue to determine if these parasitoids play a role in the regulation of CW populations. If CW parasitoids do play a meaningful role in population control, research should focus on how to increase and conserve CW parasitoids populations in the HM.

Two parasitoids of CRF - Dacnusa gracilis (Nees) (Hymenoptera: Braconidae) and Loxotropa tritoma (Thomson) (Hymenoptera: Proctotrupoidea) were released into both the HM and Quebec carrot growing areas of Canada between 1949 and

1953 (Wright et al.1947; Maybee 1954). Dacnusa gracilis is the more important of the two species as it has higher parasitism rates (Wright and Ashby 1947). However,

D. gracilis does not emerge from the CRF larvae until after it has finished feeding on the root and therefore does not prevent crop injury. Neither of the parasitoids were able to establish in Canada and the reasons for this failure are not known (McLeod

1962). The failure of augmentative biocontrol in field scenarios has been linked to simplified landscapes (Perez-Alvarez et al. 2019), this suggests that the creation of enhanced non-crop habitat for CBC would not only support existing natural enemy populations but could also make augmentative biocontrol practices more successful by increasing landscape complexity.

In laboratory studies, Aphaereta pallipe (Say) (Hymenoptera: Bravonidae) parasitize all larval instar stages of the OM (Salkeld 1959). Field research found seven parasitoids on OM and two of these caused useful levels of mortality: A.

pallipe and Aleochara bilineata (Gravenhorst) (Coleoptera: Staphylinidae) with

parasitism rates of 17.0 and 20.7%, respectively (Tomlin et al. 1985).

Research by Lemay et al. (2018) and Cormier et al. (1996) have shown that

there are natural enemies within the intensively cultivated agricultural fields of the

HM. Enhancing additional habitat, such as the berms surrounding these agricultural

fields, could provide refuge and forage to the natural enemy populations found in the

cultivated areas. Supporting these natural enemy populations could in turn offer

increased control of primary pest populations at the HM.

1.4 Pollinator Conservation

Pollination occurs when pollen grains from male anthers of a flower are

transferred to the female stigma; as a result, fertilized flowers produce seeds. Most

flowers rely on a vector to move pollen grains from anther to stigma. These vectors

are either abiotic (i.e., wind or water) or biotic (i.e., insects, birds, bats or other

animals) (Dafni 1992). Insect pollinators play an important role in the production of

food including fruits, vegetables and some field crops (Klein et al. 2007).

Research by Gallai et al. (2009) estimates the total economic value for pollination

worldwide in 2005 was $231B CAD, which represented 9.5% of agricultural

production for human consumption. In Ontario, both wild and managed pollinators

combined contribute $992M CAD annually to the economy (OMAFRA 2016). There

is no generally accepted economic valuation formula to determine the value of

pollination services to crops (Allsopp et al. 2008, Hein 2009, Winfree et al. 2011),

and therefore some valuations can be misleading. Winfree et al. (2011) proposed a

new method of valuing pollination services in agriculture which: (1) removed the costs of inputs; (2) valued only the pollination required by the crop; and (3) valued the pollinating taxa separately, resulting in a more accurate value of pollination services. Although the economic valuation of pollination as an ecosystem services is complex, understanding the economic values of these services is important to conserve, support, and maintain pollinator habitat in an agroecosystem.

The decline of insect pollinator populations including honey bees and some non-

Apis bees have been well documented worldwide (Ghazoul 2005, Biesmeijer et al.

2006, Williams and Osborne 2009, Potts et al. 2010a, 2010b, Cameron et al. 2011,

Colla et al. 2012, Bartomeus et al. 2013, Burkle et al. 2013). There are several potential drivers of global pollinator declines, but the human impact of habitat alterations is one of the most detrimental, especially in extremely disturbed landscapes with little natural area (Winfree et al. 2009, Potts et al. 2010a, 2010b).

The Ontario government has created the Ontario’s Pollinator Health Action Plan

(OPHAP), with goals of improving habitats, reducing pesticide exposure, improving public engagement, and increasing research on both managed and wild pollinators in Ontario (OMAFRA 2016). Although pollination services are not required for crops produced in the HM, the recent completion of the Holland Marsh Drainage System

Canal Improvement Project in 2016 has resulted in an increased area of uncultivated habitat. This increased habitat has allowed growers and conservation authorities to continue their land stewardship practices through the planting of different floral resources, which can provide refuge and forage for pollinators and helps to reduce

habitat fragmentation in this agroecosystem. Pollinators play a vital role in both

natural and agricultural ecosystems, providing services that either directly or

indirectly affect the food production systems in Ontario.

1.4.1 Bees

Apis mellifera

Apis mellifera L. (Hymenoptera: Apidae), the European honey bee, is an

important commercial pollinator in the Americas and agricultural commodity both in

Ontario and around the world. In Ontario, managed honey bees are used to pollinate

a wide range of crops including apples, apricots, squash, canola and melons

(OMAFRA 2016). In 2016, the OPHAP identified several stressors that have affected

honey bee populations in Ontario, including a lack of genetic diversity, pest and

disease pressure, reduced and fragmented habitat, climate change, and pesticide

exposure. Although pollination is not required for crops grown in the HM,

enhancements to non-crop habitat (e.g., canal berms) could reduce habitat

fragmentation in this intensively cultivated agroecosystem and providing much

needed foraging sites for honey bees.

Non-Apis Bees

Non-Apis bees are any other wild or managed bee that is not a honey bee, this

includes native bees. Non-Apis bees species play a vital role in the pollination of

crops in Ontario including: alfalfa leafcutting bee (Megachile rotundata (Fabricius)

(Hymenoptera: Megachilidae)) which pollinate alfalfa (Lerer et al. 1982), the

common eastern bumble bee (Bombus impatiens (Cresson)(Hymenoptera: Apidae))

used mainly in greenhouse pollination of tomatoes and peppers (Velthuis and Van

Doorn 2006), and the blue orchard bee (Osmia lignaria (Say)(Hymenoptera:

Megachilidae) used to pollinator orchard crops like apples and pears (Bosch and

Kemp 2000). Wild non-Apis bees play an important role in pollination and are more effective pollinators than honey bees in many cropping systems globally (Garibaldi et al 2013).

Research has shown the importance of non-Apis bees and their contribution to pollination in both natural ecosystems and agroecosystems. Kremen et al. (2002) concluded that native bees in intensive agroecosystems, given the right conditions, were able to offer pollination services that equaled those of A. mellifera. This emphasizes the importance of keeping diverse non-crop ecosystems, which support pollination services of non-Apis bees. Garibaldi et al. (2013) found that wild bees pollinate crops more effectively than A. mellifera, finding that honey bees supplement the work of wild bees and that integration of both Apis and non-Apis bees for pollination could increase fruit set. These studies show the important role non-Apis bees play in agroecosystem and suggest that the conservation and enhancement of non-crop habitat is important to increase wild bee populations.

Most of these non-Apis bees are facing the same environmental stressors as honey bees - climate change, habitat loss, and pesticide exposure. They also are affected by the competition for limited floral resources (Paini 2004, Wojcik et al.

2018). The OPHAP report states that Ontario is Canada’s hotspot for non-Apis bee diversity with 420 of the 855 native bee species in Canada recorded in the province

(OMAFRA 2016). Non-Apis bees serve an important role in the pollination of both

natural ecosystems and agroecosystems. Global declines in honey bee and some

non-Apis bee populations have been documented (Biesmeijer et al. 2006, Potts et

al. 2010a, 2010b, Cameron et al. 2011, Colla et al. 2012, Bartomeus et al. 2013,

Burkle et al. 2013), and as a result it is important to promote and support pollinator

conservation especially within or in close proximity to agroecosystems.

The literature on pollinator conservation in agroecosystems has shown the

importance of diversifying the landscape and the benefits that enhanced non-crop

habitat offer to pollinator populations and crop production. Morandin and Kremen

(2013) determined that managed floral hedgerows (enhanced with native floral

plantings) in proximity to agroecosystems increased the abundance of native

pollinators species by seven times compared to unmanaged hedgerows. Another

study found that hedgerows with a high diversity of woody species supported twice

as many bumblebees (Garratt et al. 2017). It is important to know the outcomes that

are trying to be achieved from the enhancement of non-crop habitat, such as,

preferred pollinator taxa and their life history, so that informed decisions can be

made when the enhancements are being planned.

1.4.2 Other Pollinators

Diptera

Until recently non-bee pollinators (e.g., Diptera) were not extensively studied by

scientists as an important provider of ecosystem services to agroecosystems. With

identified bee declines in many countries, researchers have begun to recognize their

significance (Rader et al. 2015). Hoverflies (Syrphidae) are important pollinators for

agricultural systems because they have different resource needs and dispersal

methods compared to non-Apis bees (Jauker et al. 2009, Rader et al. 2015).

Hoverflies play an important role in pollination services for agroecosystems that may

be unsuitable for bee species (Jauker et al. 2009). Hoverfly adults feed mainly on

pollen and nectar and are a vector for plant pollination. Orford et al. (2015)

investigated the importance of other Diptera, not in the family Syrphidae, as

pollinators in agroecosystems. When comparing syrphids to non-syrphid Diptera

pollinators there was no difference between the pollen loads carried, and non-

syrphid Diptera accounted for more flower visits (Orford et al. 2015). It is important to

investigate the abundance and diversity of potential Dipteran pollinators at the HM.

1.4.3 Monarch Butterflies

The monarch butterfly (Danaus plexippus L.; Lepidoptera: Nymphalidae) is

currently listed as a species of conservational concern in Ontario. Its range spans

from Central America to southern Canada (MNRF 2014). Government agencies

have noted that this species could become threatened or endangered due to

different biological characteristics or identified threats (MNRF 2014). The monarch

butterfly is one of the most well-known lepidopteran species, based on its legendary

and complex long-distance migration over three countries (Flockhart et al. 2013).

The larval stages of the monarch butterfly are obligated on milkweed (Asclepias

sp.) as a host and the adult butterflies prefers it for oviposition over other related

plants like dog-strangler vine (Vincetoxicum rossicum (Kleopow)) (Mattila and Otis 24

2003). Pleasants and Oberhauser (2013) suggested that the decrease in milkweed resulting from the increase use of glyphosate in agroecosystems in North America has negatively affected monarch populations. A more in-depth model found that both climate change and milkweed loss were significant factors that influenced population size of the monarch butterfly in NA (Thogmartin et al. 2017).

Inamine et al. (2016) suggest that the lack of milkweed in the agricultural environment is unlikely to be the cause of monarch declines. Their work takes aim at the lack of nectar resources due to habitat degradation and fragmentation for migrating monarchs. They also suggest that the destruction of overwintering habitat in central Mexico from the logging industry has also contributed to population declines. Thus, conservation efforts need to focus on all phases of the monarch’s migration. Providing areas which offer milkweed host plants and forage such as milkweed and other nectar plants, and refuge within agroecosystems like the HM, will reduce fragmentation and could offer relief for these species of concern.

The completion of the Holland Marsh Drainage System Canal Improvement

Project in 2016 has offered incredible opportunity for land stewardship within the HM agroecosystem. The creation of pollinator habitat within agroecosystems can offer several other benefits to surrounding ecosystems. Enhanced pollinator habitat can also contribute to biodiversity, more natural enemies of insect pests, and the protection of soil and water quality. Increased floral diversity within an intensively cropped agroecosystem also provides an aesthetic element, which can be pleasing to the eye (Wratten et al. 2012). 25

1.5 Summary and Objectives

The overarching goal of this research is to document how enhancements to

surrounding uncultivated habitat can affect beneficial insect populations, which could

enhance ecosystem services, and contribute to sustainable food production. This

project looks at the impact of enhancements to uncultivated habitat on the

abundance and diversity of pollinators and natural enemies of insect pests in the

Holland Marsh, Ontario. If enhancements increase beneficial insects, this may

indicate that ecosystem services like greater pest control and pollination could be

enhanced by habitat alterations.

Chapter 2 of thesis [Supporting Conservation Biological Control in the Holland

Marsh, Ontario] has three main research objectives and focuses on the HM: (1)

compare the diversity and abundance of natural enemies of CW and CRF in different

mixed floral plantings on canal berms; (2) determine the seasonal population trends

of CW, CRF, OM, ALH, and TPB in mixed floral plantings on canal berms; and (3)

assess the abundance and diversity of Carabidae in commercial carrot fields. This

will determine the role of CBC in intensively cultivated muck soil vegetable

production systems.

Chapter 3 [Supporting Pollinator Conservation in the Holland Marsh, Ontario]

focuses on insect pollinators in the different floral planting on the canal berms of the

HM to: (1) compare the diversity and abundance of these pollinators; and (2)

determine the standardized specialization index of the different flowers (naturally

occurring vs planted agricultural pollinator mix) to their insect pollinators.

Finally, in chapter 4 a summary and general discussion of the key findings of this research is provided together with suggest lines of inquiry for future research on this topic.

CHAPTER 2

SUPPORTING CONSERVATION BIOLOGICAL CONTROL IN THE HOLLAND MARSH, ONTARIO

2.0 Abstract

Natural enemies such as predatory beetles and parasitoid wasps can provide

vital pest control services to agroecosystems. Few integrated pest management

programs look at pest management through a landscape lens or try to incorporate

the use of conservation biological control (CBC) into their management programs.

The enhancement of uncultivated landscapes surrounding agroecosystems can

support the diverse natural enemy groups through an increase of floral resources

such as pollen and nectar and the creation of microclimates. There are several

known natural enemies of the primary insect pests of the Holland Marsh (HM),

including Carabidae and Mymaridae species. In this study, the natural enemy

communities were studied in three berm treatments: (1) unmanaged control; (2) a

floral enhancement; and (3) a floral + shrub enhancement, at five sites over two

years. All known Carabidae predators of carrot weevil were found on berm sites. The

mean abundance of Carabidae captured per week was significantly higher in both

the floral and floral + shrub treatments. Future research should examine the efficacy

of natural enemies supported in uncultivated enhancements at reducing primary

insect pest populations in the HM.

2.1 Introduction

The expansion and intensification of agriculture has been widely recognized as

one of the most significant anthropogenic alterations of the global landscape. The 28

revolution of agriculture in mid-20th century with its technological advancements and economic incentives drove increased agricultural production and intensification that has shaped today’s homogenous farm landscape (Matson et al. 1997, Berton et al.

2003, Foley et al. 2005, Bianchi et al. 2006). The advancements from this revolution successfully fed the world’s growing population, but at a cost to diversity and the natural ecosystem (Tilman 1998). As our global population continues to grow to a projected 9 to 10 billion, with growing competition for resources to produce food, we will require a revolution that reduces the impact of our agricultural system on the environment (Godfray et al. 2010). Moving forward we cannot rely on the finite solutions of the past, such as increasing production land. We need to utilize new solutions like sustainable intensifications (SI) which aim to increase agricultural yields without converting more land into agricultural use or having adverse effects on the environment (Pretty and Bharucha 2014). The use of SI within an agricultural system aims to support diversity by protecting current non-crop habitat. These non- crop habitats have an ability to provide ecosystems services to the surrounding agroecosystem.

Non-crop habitat is any natural or semi-natural area that is located within or surrounding an agroecosystem. The enhancement of non-crop habitat consists of any anthropogenic alteration of these natural or semi-natural areas with the aim to improve the ecosystem services they provide. Non-crop habitats support several ecosystem services in agroecosystems including increase in soil carbon sequestration, wind breaks, erosion control, reduced nutrient loading of waterbodies,

and support for beneficial insects (Clerici et al. 2014). Throughout different geographical locations and cropping systems, landscapes with high proportions of non-crop habitat increase landscape complexity which is associated with an increased abundance and diversity of natural enemies in agroecosystems (Bianchi et al 2006, Chaplin-Kramer et al. 2011). The enhancement of non-crop habitat can be achieved through the addition of perennial vegetation such as grasses, flowering plants, shrubs and/or trees. The enhancement of habitat does not necessarily reduce yields, as enhancements take little to no land away from crop production and utilize land, which is not suitable for agricultural production (Morandin et al. 2014).

The simplification of agroecosystems has had a negative effect on pest control, and the restoration and enhancement of non-crop habitat is seen as a fundamental first step to support pest control services from natural enemies (Rusch et al 2016).

The aim of conservation biological control (CBC) is to maximize pest control services through several practices including the creation or enhancement of habitat to support indigenous natural enemies (Fiedler et al. 2008, Chaplin-Kramer and

Kremen 2012). Natural enemies such as parasitoids and predators provide natural pest control services to agroecosystems. The greater abundance and diversity of these natural enemies have been associated with surrounding non-crop habitat in agroecosystems (Gardiner et al. 2009, Chaplin-Kramer et al. 2012, Bertrand et al.

2016). A meta-analysis by Chaplin-Kramer et al. (2011) found that natural enemies were positively affected by greater landscape complexity. Several studies have shown that the enhancement of non-crop habitat surrounding an agroecosystem can

support the greater abundance and diversity of natural enemies in field crop production (Gardiner et al. 2009, Ramsden et al. 2015), vegetable production

(Morandin et al. 2014, Letourneau et al. 2015), citrus tree production (Sorribas et al.

2016), and blueberry production (Blaauw and Isaacs 2015). These non-crop habitats can support natural enemies by providing alternative food resources, overwintering sites, and areas for reproduction (Knapp and Řezáč 2015).

The HM is a mixed-use wetland located 50 km north of Toronto, Ontario. The cultivated land is comprised of fertile organic black muck soil, with approximately

3000 ha used for intensive vegetable production (Bartman et al. 2007). Muck soil is defined as a sequence of more than three layers of undifferentiated types of organic material that is comprised of >30% organic matter by weight, it has a humic texture and a pH of 5.6 – 7.4 (CanSIS 2013). Over 60 different crops are grown in the HM including carrots, onions, celery, beets, Asian vegetables, and leafy greens. Around

70-80% of the total cultivated area is devoted to the production of the two primary crops, carrots and onion (Bartman et al. 2007, Lemay 2017). The agroecosystem generates over $1B CAD annually from the sale of crops and is the largest producer of carrots and onions in Ontario (Bartman et al. 2007). There are five primary insect pests: (1) carrot weevil (CW), Listronotus oregonensis (Le Conte) (Coleoptera:

Cuculionidae); (2) Carrot rust fly (CRF), Pslia rosae (Fab.) (Diptera: Psilidae); (3)

Onion maggot (OM), Delia antiqua (Meigen) (Diptera: Anthomyiidae); (4) Aster leafhopper (ALH), Macrosteles quadrilineatus (Forbes) (Hemiptera: Cicadellidae) and; (5) Tarnished plant bug (TPB), Lygus lineolaris (Palisot de Beauvois)

(Hemiptera: Miridae), which are of concern to producers in the HM as they can cause significant crop losses if not controlled.

The HM producers rely on a drainage network consisting of berms, canals, and pump houses to keep the intensively cultivated land drained for production (Bartman et al. 2007). Apart from canal berms, there is little to no non-crop habitat (e.g. hedgerows) at the HM to support natural enemies. At the completion of the HM

Drainage System Canal Improvement Project in July 2016, 19 km of canals were dredged, and 10 km of berms were expanded to improve safety and efficiency of the drainage network. After construction, the canal berms were planted with grasses and some trees and shrubs to reduce erosion and are predominantly naturalized and unmanaged, although some have grass that is mowed regularly. The canal drainage restoration project has offered an opportunity to engage in CBC through canal berm enhancement. These canal berms offer a potential refuge for predators like ground beetles (Carabidae) and parasitoids like fairy wasps (Mymaridae) that are known natural enemies of primary insect pests at the HM and have been found through previous surveys (Cormier et al. 1996, Lemay et al. 2018).

This study assessed the abundance and diversity of Carabidae in four different commercial carrot fields over two seasons in the HM. It examined the primary insect pests and the abundance and diversity of many of the known natural enemies in two mixed floral and shrub enhancements and in an unmanaged control with existing seed bank, at five sites over two seasons. Three main questions are asked: (1) Do enhanced mixed floral, and floral and shrub plantings on canal berms in the HM

increase natural enemy abundance and diversity when compared to the unmanaged

control on canal berms?; (2) Do enhanced mixed floral, and floral and shrub

plantings on canal berms in the HM provide more suitable refuge for populations of

CW, CRF, OM, ALH, and TPB, when compared to the unmanaged control on canal

berms?; and (3) What is the abundance and diversity of Carabidae in commercial

carrot fields in the HM?

2.2 Materials and Methods

2.2.1 Berm Site Enhancements

In 2017, four replicate berm sites were established throughout the HM with the

cooperation of growers, landowners, and the local municipalities, the Town of

Bradford West Gwillimbury and Township of King. In 2018, a fifth replicate berm site

was established (Figure 2.1). Berm sites were chosen to best represent the HM in its

entirety based on the available land provided. Once berm sites were selected each

site was prepared in an identical manner.

Figure 2.1: Map of the location of the Muck Crop Research Station (MCRS) [red star] and the five replicate berm sites [yellow dots] established between 2017 and 2018 at the Holland Marsh, Ontario.

Each berm site consisted of three treatments, which were assigned a random

position at each site. The three treatments were: (1) unmanaged control - consisting

of grasses that were planted on the berms after re-construction to reduce erosion,

and wildflowers present in the existing seed bank; (2) managed floral enhancement -

consisting of butterfly milkweed (Asclepias tuberosa L.) planted as plugs, a modified

Syngenta Operation Pollinator seed mix containing 20% coated wildcat DC red clover (Trifolium prattense L.), 20% yellow blossom sweet clover (Melilotus officinalis

(L.) Pall.), 10% coated alsike clover (Trifolium hybridum L.), 10% timothy (Phleum pretense L.), 20% coated bruce birds-foot trefoil (Lotus corniculatus L.), 20% common tansy (Tanacetum vulgare L.) and wildflowers present in the existing seed bank; and, (3) managed floral and shrub enhancement – a combination of the modified Syngenta Operation Pollinator seed mix, wildflowers present in the existing seed bank, butterfly milkweed and two herbaceous shrubs species – one cultivar of red currant (Ribes rubrum L.) cv. Red Lake and two cultivars of haskap (Lonicera caerulea L.) cv. Borealis Honeyberry and Polar Jewel Honeyberry. Two cultivars of the haskap shrubs were used to help ensure adequate pollination.

The berm sites were established in 2017, a year before the assessments began.

Each berm site was first measured and staked out at the four corners to establish sites that were 24.4 m long (along the road) and 6.11 m wide (road to canal).

Individual treatment plots were staked out within each site as 6.1 m by 3.05 m with

1.53 m between treatment plots and surrounding vegetation. Treatments were assigned randomly from left to right facing the canal using a random number generator (Appendix A). Berm treatments marked out as unmanaged control were left as is; enhanced berm treatments underwent further site preparation. The area of

1.53 m surrounding and separating each treatment at each site received the same site preparation. Site preparation consisted of mowing down the area and removing

vegetative residues. A burn-down application of the herbicide Round-Up (R/T 540

Liquid Herbicide [glyphosate]) at the label rate of 1.5 L/ha was applied to all mowed

areas to help reduce plant competition before the vegetative enhancements were

planted. The enhanced berm sites were scarified with a field cultivator, large stones

were removed, and approximately 2 cm of topsoil was added to ensure an adequate

seedbed. The Syngenta Operation Pollinator seed mix was seeded with a broadcast

spreader at a rate of 12.5 kg/ha and raked so that seeds were slightly imbedded in

the soil. Nine Butterfly milkweed plants in seedling plugs were planted at enhanced

berm sites arranged in a three by three grid in both the floral and floral + shrub

treatment. In the floral + shrub enhancements one cultivar of red currant shrubs was

planted in a row of five in the center, and two cultivars of haskap shrubs were

planted in two rows of three along the edges of each treatment (Figure 2.2).

Figure 2.2: Diagram of generalized berm site enhancements, with site and treatment dimensions and planting arrangements.

2.2.2 Berm Survey

Pitfall trap samples

Pitfall traps were used to measure the presence of predatory arthropods that

reside or crawl close to the surface of the ground (Martin 1977). One pair of pitfalls

consisting of a 148 mL (5 oz) specimen container (Globe Scientific, Inc., Mahwah

NJ) nested inside a Vernon pitfall trap (Fig. 2.3) was placed in each treatment.

Vernon pitfall traps were used to protect traps from bycatch of unwanted animals,

and rain. The paired traps were placed along the diagonal transect in each treatment

~2.27 m in from the corner of the treatment and ~2.27 m between each individual

trap. All specimen containers were filled with ~130 mL of 70% ethanol (ETOH)

solution that was diluted with tap water from a 95% ETOH (Fisher Scientific Inc.)

solution. All Vernon pitfall traps were placed in the ground so that the top rim was

level with the soil surface (Figure 2.3). In 2018 and 2019, the contents of the traps

were collected weekly from 1 May to 3 September.

Figure 2.3: (A) Diagram of a Vernon pitfall trap; (B) A Vernon pitfall trap placed in the ground in a treatment at a Holland Marsh canal berm site.

The insects in the pitfall traps were collected using a series of sieves, decreasing

from 8 mm to 400 µm. Any soil that had fallen into the Vernon pitfall traps was

sieved away and remaining arthropods were placed in 148 mL specimen containers

containing 95% ETOH solution and placed in cold storage (5±1°C 30-40% RH) until

identification could take place. Carabidae were identified to lowest taxonomic level

using the nomenclature of Bousquet (2010). Staphylinidae were confirmed to

subfamily and all were grouped together. Identification of Staphylinidae to genus and

species level can be challenging, especially for the genus Aleochara, as there is a

lack of adequate keys for identification (Klimaszewski 1984). Currently the keys for

staphylinid groups are under-illustrated and cover large geographic areas making

them difficult to use (Brunke et al. 2011). In 2019, the most commonly retrieved

Staphylinidae was confirmed to be in the subfamily of Aleocharinae using Brunke et 38

al. (2011). The lowest taxonomic level and abundance of each taxon, and date were

recorded for every location. Voucher specimens were submitted to the University of

Guelph Insect Collection.

Sweep netting samples

Sweep netting samples were taken weekly from 1 May to 3 September in both

years. In 2018, a sweep sample consisted of 5, 180° sweeps with a 38 cm diameter

net. One sweep sample was taken per treatment along two diagonal transects from

corner to corner at each berm site. In 2019, a sweep sample consisted of 15, figure-

eight sweeps with a 38 cm diameter net along one of three parallel transects. The

three parallel transects were flagged out one to three, with one being closest to the

road at each site. Each transect was 5 m in length, and were 0.5 m from the

treatment edge, with 1 m between each transect. Transects were walked in a

random order at each treatment and surveyors were randomly assigned to a

treatment at each berm site (Appendix F).

After each sweep, sweep nets were flipped to trap captures and the end of the

net was put into a kill jar until the insects were dead. Kill jars were made from 29 cm

by 20 cm by 15.5 cm lunch coolers containing an acetone-soaked paper towel. The

insects and vegetation in the nets were transferred from the net to a 500 mL deli

container and labeled with the corresponding treatment and transect number. At the

end of the field day, containers were put into a freezer for later processing. Insects

were identified that were of economic importance to the crops grown in the HM

region. Identification was to species or higher taxonomic levels.

Boivin traps for carrot weevil

The Boivin trap (Boivin 1985) was used to capture adult CW. It consists of a

series of wooden slats held together by bolts, with space cut out in the center to fit a

carrot root (Figure 2.4). The traps attract adult CW due to the volatiles from the

carrot root and the CW stay in the traps because of the dark narrow shelter spaces

between the wood slats. In both 2018 and 2019, Boivin traps were placed in the

center of each treatment site ~3.05 m in from the width and ~1.52 m in from the

length. These traps were monitored weekly, adult CW were counted and carrot roots

changed.

Figure 2.4: (A) An open Boivin trap with carrot root; (B) A closed Boivin trap in a carrot field. (Photo Credit: D. Van Dyk).

Sticky card trap samples

Orange-yellow sticky traps were used to monitor adult CRF in all treatments at

each berm site. Brunel et al. (1969) concluded that the colour orange-yellow, similar

to “buttercup yellow”, (RHS colour chart yellow-orange group 15B or #ffb61f) was most attractive to adult CRF. Orange-yellow coloured waxed cardboard milk cartons

(Evergreen Packing Canada Ltd., Montreal, QC) were cut into 11 by 14 cm double- sided traps and a thin layer ~ 0.5 mm of Tangle-Trap (TangleFoot, Maryville, OH) was applied to each side. A wooden stake was placed in the center of each treatment ~3.05 m in from the width and ~1.52 m in from the length, orange-yellow sticky card traps were attached using a binder clip 10 cm above the canopy (Figure

2.5 A) following MCRS IPM program protocol (Chaput 1993). Traps were collected weekly from 1 May to 3 September; the cards were individually wrapped in plastic wrap, labeled, and placed in a freezer for later processing and identification.

In 2019, yellow sticky traps were added and used to monitor adult OM and parasitoid wasps (Mymaridae) in all treatments at each berm site. Yellow milk cartons (Evergreen Packing Canada Ltd. Montreal, QC), 22 by 14 cm were used as double-sided card traps and a thin layer ~ 0.5 mm of TangleFoot was applied to each side. An aluminum metal stake with a height of ~1 m was placed in the center of each treatment ~3.05 m in from the width and ~1.52 m in from the length, yellow sticky card traps were attached to the metal stake by threading the bent stake through holes punched in the top margin of each cards (Figure 2.5 B). Traps were collected weekly from 14 May to 3 September, individually wrapped in plastic wrap, labeled, and placed in a freezer for later processing and identification.

Figure 2.5: (A) An orange-yellow sticky trap used to monitor CRF; (B) A yellow sticky trap used to monitor OM and parasitoid wasp.

Monitoring in 2018

In 2018, four berm sites (Site 1-4) were monitored weekly from 1 May to 3

September. Sites were visited in a random order each week, a schedule for site

visitation (Appendix B) was created using a random number generator. Active

(sweep netting) and passive trapping (Vernon pitfall traps, orange-yellow sticky

cards for CRF, and Boivin traps for CW) were used to assess arthropod

communities (Figure 2.6). Insects were retrieved from all traps and sorted into either

natural enemies or insect pest groups. The insect pest group was sorted into primary

insect pests of HM crops: CW, CRF, ALH, OM, and TPB as described above. The

natural enemy group was sorted into ground beetles (Carabidae), a known predator

of the primary insect pests in the HM.

Figure 2.6: Diagram of both trap placement within berm sites in 2018. The traps were placed in all treatments but have been spread out for easier visualization.

2019 monitoring

In 2019, five berm sites were monitored weekly, four berm sites (Site 1, and 3-5)

from 1 May to 2 September, and one berm site (Site 2) from 1 May to 18 June (due

to a miscommunication between landowners and researchers resulting in the site

being mowed in mid-June). Sites were visited in a random order each week,

following a schedule (Appendix C) created using a random number generator. Active

and passive traps were used as described above, with the addition of yellow sticky

traps for OM (Figure 2.7). Insects were sorted as described above but the natural

enemy group was sorted as ground beetles (Carabidae), rove beetles

(Staphyliniade), and parasitoids – parasitic wasps (Mymaridae). 43

Figure 2.7: Diagram of both trap placement within berm sites in 2019. The traps were placed in all treatments but have been spread out for easier visualization.

Commercial Field Sites

In 2018 and 2019, four commercial carrot fields were selected in each year to be

sampled for ground dwelling natural enemies (Figure 2.8). The location of these

sites were chosen from fields that participated in the MCRS IPM program, and

based on the proximity to fields that had high pest pressure in the previous year, and

located to represent each region (North, South, East, West areas) of the HM. Fields

chosen in 2018 were not seeded in carrots in 2019 due to normal crop rotation

followed by commercial growers in the HM, so different fields had to be used in

2019.

2.2.3 Commercial Field Survey

Trapping methods were adapted from Lemay et al. (2018) in which two pairs of

pitfall traps, as described above for the berm sites, were placed in each field. There

were four traps per commercial carrot field (n=4). The paired traps were placed at

opposite ends of the fields ~5 m in from the edges of the field and ~30 m between

the separate pairs. The individual traps within each pair were placed between the

hilled carrots ~2 m from one another.

The contents of the traps were collected weekly from 30 May to 26 September, in

2018 and from 6 June to 29 August in 2019. Occasionally, traps were not collected

due to pesticide applications (fields B, C, D on 7 June, field D on 14 June, field D on

14 July, field B on 7 August, and field B and D on 28 August in 2018; field G on 13

June, field F and G on 27 June, field E on 18 July, and field G on 22 August in

2019). In those instances, the contents of the traps were collected the following

week.

The insects in the traps were collected by sieving the soil using a series of sieves

decreasing from 8 mm to 400 µm mesh size. Remaining arthropods were placed in

148 mL specimen containers containing 95% ETOH solution and placed in cold

storage (5°C 30-40% RH) until identification could take place. Carabidae were

identified to lowest taxonomic level using the nomenclature of Bousquet (2010).

Lowest taxonomic level and abundance of each taxon, and date were recorded for

every location.

2.2.4 Parasitoid Collection – Carrot Root Sections

Carrot root sections (CRS) are an alternative way to monitor CW oviposition and

egg parasitoids. These were used in 2019. Four groups of five CRS, ≥60 mm long

by 35-45 mm diameter were placed along transects throughout ranges and field

edges at the MCRS following Stevenson (1985) (Figure 2.9). The CRS were

collected and replaced every 3-4 days from 10 June to 13 August. After each

collection, CRS were brought back to the University of Guelph and number of CW

oviposition cavities present in each CRS were counted using a compound

microscope (OptiTech Scientific Instruments, Pickering, ON) at 10x magnification.

Figure 2.9: Carrot root sections placed in a carrot field to monitor carrot weevil oviposition and egg parasitism. (Photo credit: Z. Telfer).

The CRS were then sprayed with a 10% bleach (Clorox Original, The Clorox

Company) and water solution, and put into a 15.6 cm2 by 5.7 cm deep Ziploc

container with two ~2.5 cm holes cut on 2 sides and covered with thrips mesh

(Figure 2.10 A). These containers were labeled with the date the CRS were

collected and assessed, sealed with a lid and placed in a growth room at 27±1°C,

60% RH and a 16:8 light:dark photoperiod for seven days. At seven days, lids were

removed, and the containers were place in a 24.5 cm3 insect rearing cage

(BugDorm) with 650 µm mesh for another 14 days (Figure 2.10 B). On day 7, a 15 x

10 cm yellow sticky card (Bioquip) was hung inside the Bugdorm cage with a twist-

tie to trap the Mymaridae egg parasitoids that hatched from the CRS. The

Mymaridae were removed and assessed on day 21. The CRS and container were

sprayed every two days with a 10% solution of bleach and water to reduce mold

growth.

2.3 Statistical Analysis

The same approach was used for analysis of the abundance of Carabidae, and

Staphylinidae collected from pitfall traps in the berm treatment, and the abundance

of Mymaridae. The data were analyzed using a generalized linear mixed model

(GLMM) with a negative binomial distribution in PROC GLIMMIX with treatment and

week as the fixed and berm site as the random factor, using SAS University Edition

9.4 (SAS Institute Inc., Carry, NC, USA). An α=0.05 was used in all analyses. Means

separation was done using Tukey’s HSD post hoc test when a significant difference

was identified. To assess the diversity of Carabidae from pitfall traps, in both the

commercial fields and canal berms, Simpson’s Diversity Index and Rarefaction

curves for each treatment were calculated using the package vegan (version 2.5-6)

in R, version 3.5.2 (The R Foundation, Vienna, Austria). In 2019 site 2 was dropped

from the statistical analysis as the site had been accidently mowed. To compare the

sweep net samples, richness, abundance, and Simpson’s Diversity among

treatments over the growing season a (GLMM) with a gaussian distribution in PROC

GLIMMIX with treatment as the fixed and berm site as the random factor SAS

University Edition 9.4 (SAS Institute Inc., Carry, NC, USA). No statistical analysis

was carried out on the parasitoid collections as these assessments were not

replicated.

2.4 Results

2.4.1 Berm Survey

Pitfall trap samples

In 2018, a total of 2366 individual Carabidae were collected from Vernon pitfall

traps in berm treatments at the HM. There was a significant difference in temporal

variation among weeks (F16,185=1.73; p=0.0436). There was a significant difference

among treatments in the abundance of Carabidae collected per week over the 49

season (F2,185=21.19; p=<0.0001). Both the floral and the floral + shrub treatments had significantly more Carabidae collected per week over the season 14.9 (±1.05) and 12 (±0.89), respectively, compared to the control 8 (±1.13), the floral treatment had significantly more Carabidae collected per week over the season, compared to the floral + shrub treatment (Figure 2.11). There was a significant difference among treatments in the abundance of Carabidae collected from Vernon pitfall traps per week on 5 June (F2,5=9.40; p=0.0220) and 21 June (F2,9=6.73; p=0.0163). On 5 June there was significantly more Carabidae collected in the floral than in the control treatment, but the floral + shrub treatment was no different from the control or floral

(Figure 2.12). On 21 June there was significantly more Carabidae collected in the floral than in the control treatment, but the floral + shrub treatment was no different from the control or floral (Figure 2.12).

Control Floral Floral + Shrub 18 A 16 14 B

Carabidae Carabidae 12 10 C 8 6 4 2

per week over the season the over week per 0 Mean abundance of of abundance Mean Berm Treatment

40.0 *ns Control 35.0 Floral 30.0 Floral + Shrub *ns Carabidae *ns 25.0 *ns *ns *ns *ns *ns *ns A *ns 20.0 *ns*ns *ns *ns *ns

15.0 AB 10.0 A B

5.0 AB Mean abundance of of abundance Mean B 0.0

Date (2018)

In 2019, a total of 2798 individual Carabidae were collected from Vernon pitfall

traps in berm treatments at the HM. There was a significant difference in temporal

variation among weeks (F17,177=15.37; p=<0.0001). There was also a significant

difference among treatments in the abundance of Carabidae collected per week in

Vernon pitfall traps over the season (F2,164=30.05; p=<0.0001). Both the floral and

the floral + shrub treatments had significantly more Carabidae collected per week

over the season 13.8 (±1.46) and 13.5 (±1.69), respectively, when compared to the

control 7.5 (±0.92) (Figure 2.13). There was a significant difference among

treatments in the abundance of Carabidae collected from Vernon pitfall traps per

week on 4 June (F2,6=8.46; p=0.0179), 11 June (F2,6=9.52; p=0.0137) and 18 June

(F2,6=5.45; p=0.0447) . On 4 June there was significantly more Carabidae collected

in the floral and the floral + shrub than in the control treatment (Figure 2.14). On 11

June there was significantly more Carabidae collected in the floral and the floral +

shrub than in the control treatment (Figure 2.14). On 18 June there was significantly

more Carabidae collected in the floral + shrub than in the control treatment, but the

floral treatment was no different from the control or floral + shrub (Figure 2.14).

Control Floral 18 Floral + Shrub A A 16 14 12 10 B 8 6

per week over the season the over week per 4

Mean abundance of Carabidae Carabidae of abundance Mean 2 0 Berm Treatment

55.0 Control 50.0 45.0 *ns Floral Floral + Shrub 40.0 *ns A 35.0 A AB 30.0 A *ns 25.0 *ns A A *ns 20.0 B *ns *ns *ns *ns *ns 15.0 *ns *ns *ns *ns 10.0 *ns B B Mean abundance of Carabidae Carabidae of abundance Mean 5.0 0.0

Date (2019)

In 2019, a total of 4793 individual Staphylinidae were collected from Vernon

pitfall traps in berm treatments. There was a significant difference in temporal

variation among weeks (F17,193=5.10; p=<0.0001). There was no significant

difference among treatments in the abundance of Staphylinidae collected per week

over the season in Vernon pitfall traps (F2,193=2.39; p=0.0940). The control, floral,

and the floral + shrub treatments had a mean abundance of 24.7 (±3.70), 18.3

(±2.36) and 19.36 (±2.44), respectively, of Staphylinidae trapped per week (Figure

2.15). There was no significant difference among treatments within weeks of the

abundance of Staphylinidae collected per week in Vernon pitfall traps (Figure 2.16)

Control

A Floral 30 28 Floral + Shrub 26 24 A 22 A

20 Staphylinidae Staphylinidae 18 16 14 12 10 8

per week over the season the over week per 6 4 Mean abundance of of abundance Mean 2 0 Berm Treatment

120.0 Control 100.0 Floral 80.0 Floral + Shrub 60.0

40.0

20.0 Staphylinidae Staphylinidae

Mean abundance of of abundance Mean 0.0

Date (2019) Figure 2.16: Mean(±SE) abundance of Staphylinidae, beneficial predator, trapped per week in Vernon pitfall traps from 1 May to 3 September 2019 at the Holland Marsh, Ontario. No significant difference was found among any of the treatments (α=0.05).

The Carabidae (2366 individuals) collected from the berms in 2018 represented

32 different Carabidae taxa (Table 2.1). Dominant taxa which cumulatively

represented >80% of the abundance of Carabidae collected from Vernon pitfall

traps, and therefore considered dominant taxa. Dominant taxa are identified for each

treatment: Control: (Harpalus sp. (33.2%), Poecilus sp. (19.3%), Pterostichus sp.

(17.6%), Agonum cupripenne (5.7%), and Chaelinus sp. (5.1%)); Floral: (Poecilus

sp. (23.7%), Harpalus sp. (21.6%), Amara sp. (15.6%), Chaelinus sp. (11.6%),

Harpalus affinis (6.3%), and Harpalus pensylvanicus (3.3%)); Floral + Shrub:

(Poecilus sp. (27.6%), Harpalus sp. (25.2%), Chaelinus sp. (12.5%), Notiobia sp.

(5.3%), Amara sp. (5.2%), and Harpalus affinis (5.2)).

In 2019, a total of 2798 individual Carabidae were collected representing 24 different Carabidae taxa from the berm treatments (Table 2.2). Dominant taxa which cumulatively represented >80% of the abundance of Carabidae collected from

Vernon pitfall traps, and therefore considered dominant taxa. Dominant taxa are identified for each treatment: Control: (Poecilus sp. (46.3%), Harpalus sp. (21.3%),

Harpalus affinis (8.0%), and Pterostichus.sp (5.5)); Floral: (Poecilus sp. (49.3%),

Harpalus sp (21.6%) Agonum cupripenne (7.8%), and Harpalus pensylvanicus

(4.5%)); Floral + Shrub: (Poecilus sp. (47.3%), Harpalus sp. (18.2%), Agonum cupripenne (10.8%), Harpalus pensylvanicus (3.3%), Chlaenius sp. (3.1%), and

Harpalus affinis (3.0%)).

Rarefaction curves from both 2018 (Figure 2.17) and 2019 (Figure 2.18) show the difference both in richness and abundance of Carabidade among treatments in both years. The rarefaction curves did not converge and do not reach a plateau which indicates that an insufficient sampling effort occurred to determine the entire richness of berm treatments.

In 2018, there was a significant difference in the mean number of taxa among treatments (F2,6=6.53; p=0.0.0312). There were significantly more taxa found in the floral treatments compared to the control (Table 2.3). There were no significant differences among treatments for the mean abundance (F2,6=1.80; p=0.2446) or the mean Simpson’s diversity index (F2,6=2.78; p=0.1398) (Table 2.3).

In 2019, there was a significant difference in the mean abundance of Carabidae among treatments (F2,6=7.45; p=0.0237). There was significantly greater mean

abundance of Carabidae in both the floral and floral + shrub treatments compared to the control (Table 2.4). There were no significant differences among treatments for the mean number of taxa (F2,6=4.66; p=0.0601) or the mean Simpson’s diversity index (F2,6=1.25; p=0.3528) (Table 2.4).

Table 2.1: List of Carabidae taxa and number of individuals captured in berm site treatments at the Holland Marsh, Ontario from 1 May to 3 September, 2018. Dominant species are in bold. Berm Treatment Control Floral Floral + Shrub Taxa Total % Abund. Total % Abund. Total % Abund. Abax parallelepipedus 0 0.0 1 0.1 0 0.0 Agonum cupripenne 31 5.7 21 2.1 12 1.5 Amara hyperborea 0 0.0 3 0.3 0 0.0 Amara sp. 4 0.7 158 15.6 42 5.2 Amphasia sp. 1 0.2 0 0.0 0 0.0 Anisodactylus sp. 23 4.2 19 1.9 12 1.5 Bembidion quadrimaculatum 1 0.2 9 0.9 18 2.2 Bembidion sp. 5 0.9 10 1.0 10 1.2 Brachinus sp. 0 0.0 1 0.1 0 0.0 Carabus sp. 1 0.2 4 0.4 4 0.5 Chaelinus sericeus 1 0.2 8 0.8 4 0.5 Chaelinus sp. 28 5.1 117 11.6 101 12.5 Cicindela sexguttata 0 0.0 1 0.1 0 0.0 Diplocheila sp. 12 2.2 4 0.4 2 0.2 Gastrelarius sp. 1 0.2 2 0.2 0 0.0 Harpalus affinis 9 1.7 64 6.3 42 5.2 Harpalus pensylvanicus 17 3.1 33 3.3 35 4.3 Harpalus sp. 181 33.2 218 21.6 204 25.2 Lachnocrepis parallela 0 0.0 1 0.1 0 0.0 Lebia atriventris 1 0.2 0 0.0 0 0.0 Notiobia nitidipemmis 0 0.0 1 0.1 0 0.0 Notiobia sp. 4 0.7 24 2.4 43 5.3 Paranchusaltipes sp. 0 0.0 1 0.1 0 0.0 Platynus sp. 0 0.0 1 0.1 2 0.2 Poecilus sp. 105 19.3 239 23.7 224 27.6 Pterostichus melanarius 4 0.7 19 1.9 6 0.7 Pterostichus sp. 96 17.6 18 1.8 39 4.8 Scarites subterraneus 1 0.2 1 0.1 0 0.0 Stenolophus sp. 1 0.2 1 0.1 0 0.0 Stenolophus comma 0 0.0 10 1.0 8 1.0 Stereocerus sp. 0 0.0 1 0.1 0 0.0 Carabidae (DAMAGED)a 18 3.3 20 2.0 3 0.4 a Damaged specimen could only be identified to family

Table 2.2: List of Carabidae taxa and number of individuals captured in berm site treatments at the Holland Marsh, Ontario from 1 May to 3 September, 2019. Dominant species are in bold Berm Treatment Control Floral Floral + Shrub Taxa Total % Abund. Total % Abund. Total % Abund. Agonum cupripenne 12 2.0 87 7.8 117 10.8 Amara sp. 1 0.2 16 1.4 11 1.0 Anisodactylus sanctaecrucis 1 0.2 7 0.6 1 0.1 Bembidion quadrimaculatum 1 0.2 6 0.5 2 0.2 Bembidion sp. 5 0.8 6 0.5 12 1.1 Bachinus sp. 0 0.0 0 0.0 1 0.1 Carabus sp. 3 0.5 3 0.3 5 0.5 Chlaenius sericeus 2 0.3 2 0.2 2 0.2 Chlaenius sp. 2 0.3 24 2.2 34 3.1 Cicindela sexguttat 0 0.0 0 0.0 1 0.1 Cicindela sp. 0 0.0 2 0.2 0 0.0 Clivina fossor 0 0.0 1 0.1 0 0.0 Diplocheila sp. 10 1.7 1 0.1 7 0.6 Gastrellarius sp. 0 0.0 1 0.1 0 0.0 Harpalus affinis 48 8.0 35 3.1 33 3.0 Harpalus pensylvanicus 27 4.5 50 4.5 36 3.3 Harpalus sp. 128 21.3 240 21.6 198 18.2 Notiobia sp. 12 2.0 6 0.5 12 1.1 Poecilus sp. 278 46.3 548 49.3 514 47.3 Pterostichus brevicornis 12 2.0 9 0.8 9 0.8 Pterostichus melanarius 5 0.8 11 1.0 15 1.4 Pterostichus.sp 33 5.5 26 2.3 28 2.6 Scarites.subterraneus 3 0.5 1 0.1 0 0.0 Stenolophus.comma 0 0.0 4 0.4 0 0.0 Carabidae (DAMAGED)a 17 2.8 26 2.3 48 4.4 a Damaged specimen could only be identified to family

Table 2.3: The mean(±SE) number of Carabidae specimens collected, number of taxa represented, and Simpson’s Diversity Index at the 3 canal berm treatments at the Holland Marsh, Ontario from 1 May to 3 September, 2018. Berm Treatment No. of Taxa b Abundance a Simpson’s Index a Control 13.3 (±1.03) a 138.3 (±61.88) ns 0.79 (±0.03) ns Floral 18.3 (±1.11) b 255.5 (±25.63) 0.74 (±0.02) Shrub 15.0 (±0.82) ab 270.0 (±36.18) 0.80 (±0.01) a Numbers in columns with followed by the same letter are not significant different according to Tukey’s HSD (α=0.05). b Numbers in columns with followed by ns indicate there is no significant difference found among any treatments (α=0.05).

Table 2.4: The mean(±SE) number of Carabidae specimens collected, number of taxa represented, and Simpson’s Diversity Index at the 3 canal berm treatments at the Holland Marsh, Ontario from 1 May to 3 September, 2019. Berm Treatment No. of Taxa a Abundance b Simpson’s Index a Control 10.5 (±0.96) ns 141.0 (±62.03) b 0.73 (±0.04) ns Floral 14.8 (±0.85) 252.5 (±69.04) a 0.65 (±0.06) Shrub 14.0 (±1.29) 252.3 (±88.08) a 0.69 (±0.04) a Numbers in columns with followed by ns indicate there is no significant difference found among any treatments (α=0.05). b Numbers in columns with followed by the same letter are not significant different according to Tukey’s HSD (α=0.05).

Sweep netting samples for insect pests

In 2018, there were no OM found in any sweep netting samples in treatments at

any of the berm sites surveyed in the HM. There was a total of two TPB found in

sweep netting samples (one in floral + shrub on 1 May and one in control on 21

June) in berm treatments surveyed. ALH was first detected at berm treatment in late-

June, peaked in mid-July, and dropped in late-July. There was a significant

difference in temporal variation among weeks for ALH (F9,104=22.22; p=<0.0001). 63

There was a significant difference among treatments in the abundance of ALH collected from sweep netting on 16 July (F2,6=9.00; p=0.0156). There was significantly more ALH collected in the control than in the floral treatment, but the floral + shrub treatment was no different from the control or floral (Figure 2.19), however the numbers were very low in all treatments.

In 2019, there was a total of two ALH found in sweep netting samples (two in floral on 20 August) in berm treatments surveyed. OM was first detected in berm treatments at the beginning of July and varied weekly until the end of August. There was a significant difference in temporal variation among weeks for OM (F7,83=10.10; p=<0.0001). There was a significant difference among treatments in the abundance of OM collected from sweep netting on 3 July (F2,6=6.00; p=0.0370) and 9 July

(F2,6=1.29; p=0.0063). On 3 July there was significantly more OM collected in the control than in the floral treatment, but the floral + shrub treatment was no different from the control or floral (Figure 2.20). On 9 July there was significantly more OM collected in the floral + shrub than in the control and floral treatments (Figure 2.20).

TPB was first detected in berm treatments at the beginning of July and varied weekly until the end of August (Figure 2.21). There was no significant difference in temporal variation among weeks for OM (F6,73=0.44; p=0.8473). No significant difference was found among berm treatments for the mean TPB collected per sweep per week

(F2,73=0.62; p=0.5410).

Control 0.5 Floral 0.45 0.4 Floral + Shrub 0.35 A 0.3 0.25 AB 0.2 0.15 B

0.1 Leafhopper per sweep per Leafhopper

Mean abundance of Aster Aster of abundance Mean 0.05 0

Date (2018)

Control 0.4 Floral 0.35 0.3 A A Floral + Shrub 0.25 0.2 AB 0.15 0.1

per sweep per B B 0.05

0 B Mean abundance of Onion Maggot Maggot Onion of abundance Mean Date (2019)

Control Floral 0.7 Floral + Shrub 0.6 0.5 0.4

0.3 per Sweep per

0.2

Tarnished Plant Bug Plant Tarnished Mean abundance of of abundance Mean 0.1 0

Date (2019)

Boivin trap samples

In both 2018 and 2019, no CW were found in Boivin traps in any treatment at any

of the berm treatments surveyed at the HM.

Sticky card trap samples

In both 2018 and 2019, no CRF were found on orange-yellow sticky card traps in

any treatment at any of the berm sites surveyed in the HM. In 2019, with the addition

of yellow sticky card traps, no OM were found in any treatment at any berm site. In

2019, a total of 537 individual Mymaridae were trapped on yellow sticky card traps in

berm treatments. There was no significant difference found in the abundance of 67

these parasitoids trapped per week among any of the treatments (F2,165=0.01;

p=0.9941). The control, floral, and the floral + shrub treatments had a mean

abundance of 13.3 (±3.47), 12.8 (±3.38) and 12.3 (±4.01) Mymaridae trapped per

week, respectively (Figure 2.22).

18.0 Control 16.0 14.0 Floral 12.0 Floral + Shrub 10.0 8.0

6.0 Mymaridae 4.0 Mean abundance of of abundance Mean 2.0 0.0

Data (2019)

2.4.2 Commercial Field Survey

In 2018, a total of 656 individual Carabidae were collected representing 15

different taxa in four commercial carrot fields (Table 2.5). In 2019, 14 taxa were

identified in the four commercial carrot fields with a total abundance of 298

individuals (Table 2.6). Rarefaction curves from both 2018 (Figure 2.23) and 2019

(Figure 2.24) showed that there was a large variability in both richness and

abundance of Carabidade among fields in both years. The rarefaction curves

indicate that an insufficient sampling effort occurred to determine Carabidade

richness in commercial carrot field sites. The Simpson’s diversity index differed

among commercial fields in both 2018 (Table 2.7) and 2019 (Table 2.8).

Table 2.5: List of Carabidae taxa and number of individuals captured in 4 commercial carrot fields (A,B,C and D) at the Holland Marsh, Ontario from 31 May to 26 September, 2018. Dominant species are in bold. Number of Individuals Collected Taxa Field A Field B Field C Field D Total % Abund. Agonum cupripenne 1 0 0 0 1 0.2 Amara sp. 16 10 8 3 37 5.6 Anisodactylus sp. 50 5 30 1 86 13.1 Bembidion quadrimaculatum 0 10 33 11 54 8.2 Bembidion sp. 1 3 3 138 145 22.1 Clivina fossor 0 2 0 3 5 0.8 Harpalus affinis 3 1 1 1 6 0.9 Harpalus pensylvanicus 1 0 0 3 4 0.6 Harpalus sp. 2 0 1 0 3 0.5 Poecilus chalcites 1 0 0 0 1 0.2 Poecilus lucublandus 2 0 3 0 5 0.8 Pterostichus melanarius 67 18 30 30 145 22.1 Pterostichus sp. 0 2 2 0 4 0.6 Stenolophus comma 18 11 33 5 67 10.2 Caradidae (DAMAGED) 66 10 10 7 93 14.2

Table 2.6: List of Carabidae taxa and number of individuals captured in 4 commercial carrot fields (E,F,G and H) at the Holland Marsh, Ontario from 6 June to 29 August, 2019. Dominant species are in bold. Number of Individuals Collected Taxa Field E Field F Field G Field H Total % Abund. Amara sp. 37 1 7 1 46 15.4 Anisodactylus sp. 95 3 1 0 99 33.2 Bembidion quadrimaculatum 1 0 0 0 1 0.3 Bembidion sp. 0 0 0 1 1 0.3 Clivina fossor 0 5 1 4 10 3.4 Harpalus affinis 2 1 0 1 4 1.3 Harpalus sp. 1 4 0 3 8 2.7 Poecilus chalcites 9 1 0 0 10 3.4 Poecilus lucublandus 2 0 0 0 2 0.7 Pterostichus melanarius 18 4 4 46 72 24.2 Pterostichus sp. 5 2 1 5 13 4.4 Stenolophus comma 7 5 0 7 19 6.4 Stenolophus sp. 4 1 0 0 5 1.7 Carabidae (DAMAGED) 7 0 1 0 8 2.7

Table 2.7: Number of taxa, total abundance, and Simpson’s Diversity Index for commercial carrot fields at the Holland Marsh, Ontario from 31 May to 26 September, 2018. Location 2018 No. of Taxa Abundance Simpson's Index Field A 12 228 0.77 Field B 10 72 0.85 Field C 11 154 0.82 Field D 10 202 0.51 Commercial Field Total 15 656 0.84

Table 2.8: Number of taxa, total abundance, and Simpson’s Diversity Index for commercial carrot fields at the Holland Marsh, Ontario from 6 June to 29 August, 2019.

Location 2019 No. of Taxa Abundance Simpson's Index Field E 12 188 0.69 Field F 10 27 0.86 Field G 6 15 0.69 Field H 8 68 0.52 Commercial Field Total 14 298 0.80

Figure 2.23: Rarefaction curves for four commercial carrot fields surveyed with Vernon pitfall traps for Carabidae, predators of insect pests of marsh crops at the Holland Marsh, Ontario, 2018.

Figure 2.24: Rarefaction curves for four commercial carrot fields surveyed with Vernon pitfall traps for Carabidae, predators of insect pests of marsh crops at the Holland Marsh, Ontario, 2019.

2.4.3 Parasitoid Collection – Carrot Root Sections

In 2019, a total of 14 parasitoids were produced from 596 CW oviposition pits

assessed on CRS collected from the MCRS at the HM. All emerged parasitoids

collected were from CRS placed in the field from 14 June to 18 June 2019 (Figure

2.25). All emerged parasitoids were identified as Anaphes sp. (Hymenoptera:

Mymaridae).

140 120 100 80 60 40 20 0

CW Oviposition Scars Parasitoid Emergence

Figure 2.25: Carrot weevil oviposition scars and parasitoid emergence from carrot root sections collected from the MCRS at the Holland Marsh, Ontario from 10 June to 13 August, 2019.

2.5 Discussion

Few studies to date have evaluated the diversity and abundance of natural

enemies or economically important insect pests in non-crop habitat in proximity to

commercially cultivated fields at the HM. However, a few studies have focused on

the survey of ground-dwelling beetles in the HM in both cultivated carrot (Lemay et

al. 2018) and onion (Tomlin et al. 1985) fields. This study was conducted to further

our understanding of how canal berm enhancements would affect natural enemy,

and primary insect pest population, to increase our understanding of CBC in the

agroecosystem of the HM.

This study demonstrated that the small-scale enhancement of non-crop habitat through the establishment of mixed floral and floral + shrub plantings, can positively affect the abundance and richness of natural enemy groups in areas adjacent to fields with commercially cultivated crops. The results show that there were greater abundance and richness of Carabidae in enhanced berm habitat, which supports established patterns that more complex agroecosystem support a greater abundance and diversity of natural enemies compared to simple agroecosystems

(Thomas et al. 1991, Lee et al. 2001, Blaauw and Isaacs 2015). In both years of the berm survey, known predators of carrot pests where found in the non-crop berm treatments at the HM. Pterostichus melanarius, the only known predator of CW adults, had almost double the abundance in floral and floral + shrub enhancements compared to the control. Other known predators of the larvae and egg stages of CW and CRF were also present at the berm treatments including Poecilus lucublandus,

Bembidion quadrimaculatum oppositum, Clivina fossor, and Anisodactylus sanctaecrucis. This study found no difference among treatments in the abundance of Staphylinidae, although other research has shown that mixed floral plantings can increase Staphylinidae assemblage in agroecosystems, specifically that more predators and fungivores occur in mixed floral plantings while more parasitoids occur in cultivated fields (Twardowski et al. 2019). Further identification to a lower taxonomic resolution would be beneficial for determining if the mixed floral planting increased known Staphylinidae predators or parasitoid of HM insect pests.

Contrary to our expectations, there was not a greater abundance of Mymaridae parasitoids in the enhanced berm treatments. Many parasitoid adults rely on alternative floral resources, mainly nectar and pollen, as sources of carbohydrates and protein, respectively (Landis et al. 2000). The addition of non-crop floral resources can benefit parasitoids by increasing their fecundity and longevity (Lee and Heimpel 2008, Géneau et al. 2012). The increase of floral resources in simplified agroecosystems increased parasitoid abundance in several studies

(Winkler et al. 2009, Morandin et al. 2014, Blaauw and Isaacs 2015). Although the present study found no difference in abundance of Mymaridae among berm treatments, the focus was on very specific taxa of a parasitoid that is a known CW egg parasitoid within the genus Anaphes (Cormier et al. 1996). Little is known about how enhanced floral resources could affect Mymaridae and the known CW parasitoids within it. More research is needed on floral resource requirements of

Anaphes spp. It can be a challenge to tell the difference among floral enhancements in close proximity as parasitoids are highly mobile and may be benefiting from enhancements and then moving elsewhere to rest or oviposit. A broader taxonomic resolution of all parasitoid wasps collected in this study might trend more along the lines of previous studies.

Little work has been conducted on the two known CW egg parasitoids Anaphes listronoti (Huber) and Anaphes victus (Huber) in the last 25 years. The taxa are under-studied, and little is known of their ecology, life history, and alternative host species. Research by Telfer (2017) that monitored parasitoids of CW eggs using

carrots baited with CW eggs was relatively unsuccessful, as only three parasitized

CW eggs successfully produced parasitoids over two seasons. Previous research also concluded that although the use of egg-baited carrots was adequate for determining the presence of Anaphes spp. and the timing of parasitism, it was not adequate for estimating the percentage of parasitism (Cormier et al. 1996). In 2019,

CRS were used instead of baited carrots, allowing CW adults to oviposit as they would in field grown carrots (i.e., near the crown at the soil surface). To reduce egg manipulation that could potentially damage parasitized eggs, only oviposition pits were counted, and parasitoids were left to develop inside CRS. Fourteen parasitoids were found, all identified as A. listronoti. The use of this less invasive method for rearing out parasitoids may yield more reliable data in determining rates of parasitism in the field.

Growers are understandably concerned about a potential increase of insect pests in enhancements to uncultivated habitat close to cultivated fields. This study showed that the three non-crop berm treatments did not provide refuge for economically important insect pests. Neither, CW nor CRF was found in any berm treatment at any of the five berm sites. The berm enhancements used in this study do not provide refuge for these primary insect pests of carrots. OM were only found in one year through sweep netting and the numbers captured remained low. In both years TPB and ALH were present at berm treatments but the numbers captured remained low. It was difficult to determine and compare if populations passed an economic threshold for the application of insecticides as action thresholds for these

pests are usually indicated by the number of pests per plant as indicated for TPB in celery (Chaput 1993, Chaput and Uyenaka 1998) or through the use of other indices that require plant counts, such as the aster yellows index for ALH (Chaput 1993,

Chaput and Sears 1998). When comparing pest populations captured on the berms to those captured through the IPM scouting programs, in both years the number of pests captured at the berm sites was lower than those captured in IPM scouting on the actual crops (Telfer and McDonald 2018, Blauel and McDonald 2019). This study has demonstrated that the restoration of berms with floral and floral + shrub enhancements do not offer refuge to economically important insect pests of crops at the HM.

There was substantial variation of abundance, richness, and diversity of

Carabidae in commercial carrot fields in both 2018 and 2019. The study found known predators Poecilus lucublandus, Bembidion quadrimaculatum oppositum,

Clivina fossor, and Anisodactylus sanctaecrucis of both CW and CRF were similar to that found in a survey by Lemay et al. (2018). The commercial carrot field with the lowest abundance of Carabidae in 2018 was extremely weedy and had an infestation of quack grass. Vegetation density has been shown to bias pitfall trap captures, and thus a high density of weeds could reduce or bias the abundance of carabids trapped in fields (Thomas et al. 2006). In 2019, three of the four surveyed commercial carrot fields had very low abundance of Carabidae. Visual observation of these fields indicated that these growers utilized between row tillage to reduce weed pressure more so than the commercial field with a higher abundance. Some

research has been conducted on the effects of cultivation on Carabidae assemblages in agroecosystems with mixed results. In a review of carabid beetles in sustainable agriculture by Kromp (1999) they found that carabids can be negatively affected by deep tillage and enhanced in a conservation tillage system. Research by

Cárcamo et al. (1995) found that reduced tillage did not change species composition or activity; however, the ways species reacted to tillage were different. There are several reasons why Carabidae assemblage could be affected in commercial carrot fields, from agronomic practices like tillage and weed control, to surrounding landscape composition. The present study did not assess the agronomic practices within, or the landscape composition around, the commercial fields surveyed, but future studies should take these into account. Long term, continuous data collection in the same commercial fields, regardless of crop type would offer insight into how agronomic practices and surrounding landscape composition affect Carabidae assemblages.

Although we have found that enhanced floral and floral + shrub berm treatments can benefit some groups of natural enemies, it is not clear what effects, if any, the enhancements had on the control of the primary pest populations at the HM. The use of CBC within an IPM program is often overlooked and the actual impact of the method is under studied. When agronomists think of pest management, it is often seen through a finite field scale lens, but the processes that determine natural enemy abundance and pest control take place at a large landscape scale (Thies and

Tscharntke 1999, Gardiner et al. 2009, Chaplin-Kramer et al. 2011). A study of how

the larger landscape influences an IPM program’s pest numbers and crop damage would require additional experiments. These experiments would not only look at how natural enemies and pest populations are influenced by landscape enhancements to non-crop habitat, but also how these landscape enhancements influence pest control in adjacent fields. To understand the effects that canal berm enhancements might have on insect pest control, the study protocol would have to be modified, so that a single berm treatment would be paired with an adjacent cultivated field.

Additional trapping methods would need to be incorporated, such as: (1) the use of mark-recapture experiments to understand predator movement (Thomas et al.

2006); (2) sweep netting along transects from the field edge into the field and egg baited parasitoid traps similar to Morandin et al. (2014) to understand the movement of parasitoids; (3) the use of molecular techniques to analyze the gut content of known predators to understand their predation rate of known primary insect pests; and (4) sampling primary crops along transects from field edge into the field to assess for crop damage by primary insect pests.

The current research had some limitations. One limitation was an insufficient sampling effort indicated by rarefaction curves that have not fully converged for either the berm treatments or the commercial fields. This means that the entire species richness at the sites were not captured. The use of split plot sampling and the addition of more sites, along with a further refinement of taxonomic identification could result in more robust sampling.

Another concern of this study and others is the use of pitfall traps for ecological studies. Pitfall traps are known to bias samples towards Carabidae with larger body mass (Spence and Niemelä 1994, Hancock and Legg 2012). Arguments that species richness can be confidently assessed with data, which have been pooled over the growing season has been widely debated (Baars 1979, Standen 2000,

Ward et al. 2001, Knapp and Růžička 2012). In short, pitfall traps are cheap, easy to use, and widely used in ecological studies (Thomas et al. 2006). This study acknowledges the shortcomings of pitfall traps, but this type of trapping method was justifiable in meeting the goals of this study. This study focused primarily on known natural enemies of primary HM pests, such as Carabidae and Mymaridae. This choice limited the capture and identification of other important natural enemy groups such as Coccinellidae, Syrphidae larva, and other generalist natural enemies. There was no assessment of all captured generalist natural enemies that could help control insect pest populations in the HM.

Another limitation was the establishment of the milkweed and shrubs in the enhanced areas. The milkweed that was planted failed to establish fully at most berm sites even though watered and tended to regularly. The slow growth and small stature of the milkweed compared to other plants within the enhancements may explain why it failed to establish. The shrubs that were planted in the floral + shrub treatments were chosen to add levels of foliage, which would create different microclimates, and flowers to attract and support general beneficial insects and pollinators. The planted floral mixtures over grew the relatively young shrubs which

meant that there were only small differences between the floral, and floral + shrub treatments. With time, the shrubs should mature, grow and provide different vegetative heights and levels to the enhancement. Longitudinal studies on the enhancement of non-crop habitat over several season would allow for the differences between these two treatments to be more defined.

This study used small size of berm treatments in the replications, which was ideal for investigating how enhancements could benefit natural enemy groups in non-crop habitat, but to assess further the impacts of berm enhancements at a landscape scale the size and separations of treatments, will have to increase.

This project could take several future directions. The first would be to grow the project to assess the impact of berm enhancements at a landscape scale, and to determine the effects on pest control and natural enemy complexes through the assessment of adjacent fields. Another direction would be to investigate different seed mixes, which contain plant seeds that are native to the region. This current project used a modified older (~$4225 CAD per ha) floral seed mix from Syngenta which contained mostly naturalized legumes, including red and yellow clover and common tansy. These are non-native species, which compete with native wildflowers in non-crop enhancements. Assessing how native seed mixes influence natural enemy assemblages could make for more ecological friendly enhancements and seed mixes that may be more aesthetically pleasing to community stakeholders.

One of the biggest issues arising from this project was the social perspective on the aesthetic appearance of the berms. Concerns from stakeholders about the

weedy and unkept look of the canal berms surrounding the HM was evident from articles in the local paper (Appendix E), and complaints to local municipalities This issue has brought several interesting questions and possible directions for future study. One of the biggest requests received from surrounding community stakeholders was to mow down the unsightly berms. This would allow us to ask additional questions, such as how do different mowing regimes affect the assemblage of natural enemies and pests on uncultivated canal berms? The concerns raised have also led to questions about the mobilization, transfer of knowledge, public engagement on diversity, and how more complex agroecosystems can be beneficial to both the agricultural landscape and the natural ecosystem.

There are several directions this current research could take and not all of them being in the purely scientific, projects focused on sustainability in the agroecosystem can be seen through several lens such as economic, social, and cultural perspectives and it is important not to silo them off into specific streams.

This study investigated the potential of small-scale enhancements to non-crop habitat (canal berms) in an intensive agroecosystem, and demonstrated that there was a potential increase in natural enemy complexes without providing refuge to primary insect pests of the HM. Further assessment and experimentation at these berm sites, and their influence on pest management in the HM, should be conducted in 2020 and onwards. The collections from the past two years have shown that berm enhancements had a positive impact on the abundance of some natural enemy

groups, specifically Carabidae predators potentially enhancing ecosystem services that they provide. If these treatments continue to support natural enemies, without providing refuge for or increasing populations of primary insect pest of the HM, they could contribute to ensuring the long-term sustainability of this specialized agroecosystem.

CHAPTER 3

SUPPORTING POLLINATOR CONSERVATION IN THE HOLLAND MARSH, ONTARIO

3.0 Abstract

Insect pollinators such as honey bees, bumble bees, solitary bees, and hover

flies can provide vital ecosystem services to both the natural ecosystem and

agroecosystems. The enhancement of uncultivated landscape surrounding or within

agroecosystems can support insect pollinators with the addition of floral resources

such as pollen and nectar, and the creation of suitable refuge and nesting habitat.

Even though pollination is not required to produce the primary crops in the Holland

Marsh, the addition of these enhancements could help reduce landscape

fragmentation and promote pollinator conservation in this intensive agroecosystem.

Insect pollinator communities were studied in three berm treatments: (1) unmanaged

control; (2) a floral enhancement; and (3) a floral + shrub enhancement at five sites

over two years. Honey bees, bumblebees, solitary bees, and hover flies were found

on all berm site treatments. The mean abundance of solitary bees was higher in the

floral + shrub enhancement compared to the control in 2019, but no differences were

found in the abundance of any other bees. Future research should look at relative

floral attractiveness and population changes resulting from floral enhancements to

bee pollinators at a species level to better understand how management strategies

can support bees and other pollinators, including threatened species.

3.1 Introduction

Pollination in flowering plants occurs when pollen from male anthers are

transferred to the female stigma, which allows for the fertilization of the plant to

produce fruit and seed. Insect pollinators are important in both natural ecosystems

for wild plants and agroecosystems for cultivated crops (Stanley and Stout 2014).

The valuation of pollination worldwide in 2005 was estimated at $231B CAD (Gallai

et al. 2009). Wild and managed pollinators combined contribute an estimated $992M

CAD annually to the Ontario economy (OMAFRA 2016). Although understanding the

economic valuation of pollination as an ecosystem service is complex, it is important

to conserve, support, and maintain pollinator habitat for insect pollinators in

agroecosystems.

Insect pollinators provide essential ecosystem services worldwide as primary

animal pollinators to both wild plants and agricultural crops. Pollination in agriculture

across the world has relied mainly on managed honey bees (Apis Mellifera L.)

(Hymenoptera: Apidae). These are considered one of the most economically

important insect pollinators for food crops that require insect-mediated pollen

transfer (Allen-Wardell et al. 1998, Delaplane and Mayer 2000, Klein et al. 2007).

Although the honey bee is an effective pollinator for many crops, there are risks to

relying on a single managed pollinator, especially as colony numbers continue to

decline in both North America and Europe due to multiple drivers (Potts et al. 2010a,

2010b). As such, growers and scientists are now recognizing the important role of

non-Apis bees and other insects such as flies as pollinators in agroecosystems.

Non-Apis bees include any other wild or managed bee that is not a honey bee, this includes native bees. Several studies have shown that when there are adequate natural or uncultivated areas of habitat within an agroecosystem (Morandin et al.

2007, Garibaldi et al. 2011) non-Apis bees are as effective as honey bees, or more so, for some crop pollination (Kremen et al. 2002, Klein et al. 2007, Breeze et al.

2011, Garibaldi et al. 2013, Klatt et al. 2014). Numerous studies have shown the important role non-bee pollinators from the family Diptera play in agroecosystems that are unsuitable for, or have experienced declines of, bee species (Jauker et al.

2009, Orford et al. 2015, Rader et al. 2015).

In recent years, the decline of insect pollinator populations including honey bees and some non-Apis bees have been well documented throughout the world

(Ghazoul 2005, Biesmeijer et al. 2006, Williams and Osborne 2009, Potts et al.

2010a, 2010b, Cameron et al. 2011, Colla et al. 2012, Bartomeus et al. 2013, Burkle et al. 2013). Potential drivers of global pollinator declines include; pesticide application and environmental pollution; changes in resource diversity; alien species; pathogen spread; climate change; and land-use changes (Potts et al. 2010a,

2010b). For insect pollinators, rarely a single environmental driver affects their diversity and abundance, but instead multiple interacting drivers can explain ongoing declines (Potts et al. 2010a, 2010b). A meta-analysis of the anthropogenic impact on bee abundance and diversity found habitat alterations to be the most detrimental, especially in extremely disturbed landscapes with little natural area (Winfree et al.

2009).

Anthropogenic impacts and transformation of landscapes have reduced unmodified natural habitat around the globe (Foley et al. 2005). These transformations can be seen extensively in today’s modern agricultural landscapes, which over the past century have become more simplified and intensive (Foley et al.

2005, Bianchi et al. 2006). Due to increased landscape fragmentation, the lack of ecosystem diversity and uncultivated habitat in these intensive agroecosystems, marginal non-crop habitat has become especially important for the conservation of insect pollinators (Kremen et al. 2002, Westphal et al. 2003, Kremen et al. 2007,

Lentini et al. 2012, Dicks et al. 2013). Enhancement and restoration of marginal uncultivated habitat in intensive agroecosystems offers the potential to provide needed floral resources and refuge habitat to insect pollinators in fragmented landscapes with poor resource diversity.

Insect pollinators have diverse life histories which require various floral and nesting resources. Pollinator communities require landscapes with diverse floral characteristics, floral resource availability throughout the seasons, and nesting substrates to sustain their populations. It is important to understand the phenological differences among the floral resources already present and the ones being planted and how they can contribute to pollination as an ecosystem service (Kremen et al.

2007). When adding floral resources to the landscape it is important that they have a wide range of morphological traits such as flower size, shape, colour, and nectar.

Providing diverse morphological traits in floral plantings is important to support different insect pollinators, such as different bees that vary in size and tongue length.

The enhancement of uncultivated areas should aim to increase diversity; this can be done through manipulation, alteration, or restoration of uncultivated areas in proximity to agroecosystems. The purpose of enhancements is to ensure adequate resource availability for the optimal or increased performance of beneficial insects such as pollinators (Altieri and Letourneau 1982, Landis et al. 2000). In intensive agroecosystems, the enhancement of uncultivated habitat with different vegetative forb and shrub plants have been shown to support insect pollinators (Wratten et al.

2012, Morandin and Kremen 2013, Blaauw and Isaacs 2014, Garratt et al. 2017) which can provide ecosystem services to adjacent fields.

The Holland Marsh is a mixed-use wetland located 50 km north of Toronto,

Ontario. Approximately 3000 ha is comprised of a fertile organic black muck soil, which is cultivated for intensive vegetable production (Bartman et al. 2007). Muck soil is defined as a sequence of more than three layers of undifferentiated types of organic material that is comprised of >30% organic matter by weight, it has a humic texture and a pH of 5.6 – 7.4 (CanSIS 2013). Over 60 different crops are grown in the HM including carrots, onions, beets, celery, Asian vegetables, leafy green, green onion, leeks, and other herbs. The sale of crops from the HM agroecosystem generates over $1B CAN annually to the Ontario economy (Bartman et al. 2007).

Around 70-80% of the total cultivated land is devoted to the production of the two primary crops, onions and carrots (Bartman et al. 2007). These two primary crops are biennials that are produced as annuals and grown primarily for their edible roots, or bulbs. Therefore, the plants do not reach the flowering stage before they are

harvested and do not require pollination. Due to the unique agroecosystem, the HM

has a very intensive cultivated area where grower fields are side-by-side with little to

no uncultivated habitat surrounding them (Figure 3.1).

Figure 3.1: Grower fields in the Holland Marsh, Ontario. (Photo credit: Higheye).

Producers in the HM rely on a drainage network consisting of berms, canals, and

pump houses to keep the intensively cultivated areas drained for production

(Bartman et al. 2007). Apart from canal berms, there is little to no uncultivated

habitat (e.g. hedgerows) at the HM to support insect pollinators.

The HM Drainage System Canal Improvement Project was completed in July

2016. Nineteen km of canals were dredged, and 10 km of berms were expanded to

improve community road safety and efficiency of the drainage network. Canal berms

were planted with grasses and some trees and shrubs after construction of the

berms to reduce erosion. The berms are predominantly naturalized and unmanaged,

although some private areas have grass that is mowed regularly. The canal drainage

restoration project has offered an opportunity to engage in pollinator conservation

through enhancement of the canal berms with beneficial plants. These canal berms

offer a potential to provide forage, refuge, and nesting habitat for insect pollinators

like bees and hover flies.

This study assessed the abundance of four groups of insect pollinators: (1)

managed honey bees; (2) bumble bees; (3) solitary bees; and, (4) hover flies, in two

mixed floral and floral + shrub enhancements and in an unmanaged control with

existing seed bank, at five canal berm sites over two seasons. Two main questions

are asked: (1) Do enhanced mixed floral and floral + shrub plantings on canal berms

in the HM have greater numbers of insect pollinators compared to the unmanaged

control sites on the berms; and, (2) What is the value of planted and naturally

occurring floral species to different pollinator species, their interaction networks, and

the standardized specialization on canal berms?

3.2 Materials and Methods

3.2.1 Berm Site Enhancement

Berm site enhancements for this study were those that were described in

Chapter 2 [Supporting conservation biological control in the Holland Marsh, Ontario]

in section 2.2.1 [Berm Site Enhancements]. Five replicate berm sites were

established throughout the HM with the cooperation of growers, landowners, and the

local municipalities, the Town of Bradford West Gwillimbury and Township of King

(Figure 2.1). Each berm site had three treatments: (1) unmanaged control -

consisting of grasses that were planted on the berms, and wildflowers present in the

existing seed bank; (2) managed floral enhancement – consisting of butterfly 90

milkweed, a modified Syngenta Operation Pollinator seed mix (floral constitution and

proportions in chapter 2 section 2.2.1), and wildflowers present in the existing seed

bank; and, (3) managed floral + shrub enhancement – consisting of the modified

Syngenta Operation Pollinator seed mix, wildflower present in the existing seed

bank, butterfly milkweed and two herbaceous shrubs species – red currant and

haskap (cultivar information in chapter 2 section 2.2.1). The modified Syngenta

Operation Pollinator seed mix was chosen because it contains different plants that

provide bloom over the period of May to September, and as perennials continue to

bloom throughout the season over many years. The modification to the mix was the

addition of common tansy, a late season blooming plant (July-October). The shrubs

chosen were haskap, which is an early blooming plant that flowers from the

beginning of May into early June; and red currants that bloom late May to mid-June.

These choices were made to ensure that there would be forage for pollinators

available from early May to October. The butterfly milkweed was planted to provide

additional floral and oviposition resources for the at-risk monarch butterfly.

Site dimensions, treatment location, preparation, and planting arrangements

were identical to those described in chapter 2 section 2.2.1 (Figure 2.2).

Characterization of Landscape

To investigate the difference in landscape composition surrounding berm

enhancements, landscape variation was quantified in geographical information

system (GIS) based on the percentage of different land cover classes surrounding

berm sites. Land cover layers for the Lake Simcoe Region were obtained from Land

Information Ontario via the Ontario Geospatial Data Exchange (Data: LAKE

SIMCOE WATERSHEAD LAND COVER 2011, LSRCA 2011). These data was used

to calculate land cover percentage for three classes: (1) agricultural land (intensive

agriculture and non-intensive agriculture); (2) natural/semi-natural land (natural

heritage feature and manicured open spaces); and, (3) rural/urban land (commercial,

estate residential, golf course, industrial, institutional, road, rural development,

urban). ArcGIS 10.5 was used to create buffers around the centroid of each site, and

the “Calculate Area” tool determined the proportion of agricultural land, natural/semi-

natural land, and rural/urban land within each buffer using the Lake Simcoe

Watershed land cover data. The characterization of land cover was conducted at

750 m the maximum foraging distance for most non-Apis bees (Osborne et al. 1999,

Gathmann and Tscharntke 2002, Zurbuchen et al. 2010) and 2000 m the mean

foraging range for honey bees (Beekman and Ratnieks 2000).

Floral Assessment

The assessment for blooming floral communities was conducted visually for each

treatment at canal berm sites. Each surveyor would walk through a treatment plot to

record the species of all visible blooming plants and assign a percentage cover of

that blooming floral species out of the total treatment area. If a floral species was

unknown, a cutting of that plant species was taken for later identification and was

labeled with a unique identification. Surveyors were trained each growing season on

the visual assessment protocol and identification of the agricultural pollinator mixture

plants and commonly occurring wildflowers. In 2018, blooming floral community

composition were assessed at four berm sites (Site 1-4) weekly from 10 July to 19

September. In 2019, blooming floral community composition were assessed at four

berm sites (Site 1 and 3-5) weekly from 6 June to 29 August. Sites were visited in a

random order each week, following a planned schedule for site visitation in 2018

(Appendix B) and 2019 (Appendix C).

Pollinator Monitoring

In 2018, four berm sites (Site 1-4) were monitored weekly from 10 July to 19

September for insect pollinators. Sites were visited in a random order each week, a

schedule for site visitation (Appendix B). Methods were adapted from Morandin and

Kremen (2013), sampling was only conducted on days when the temperature was at

least 15°C, winds were below 3.0 m/s, and when cloud conditions were bright

overcast (even haze/clouds but sun and/or shadows are visible) to clear (clouds

rarely/never cover sun) for the entire sampling time.

Observational Assessment of Insect Pollinators

Observational assessments of insect pollinators occurred weekly throughout the

season. After floral assessments were completed, surveyors would complete a 15-

minute insect observation period to record flower visiting. Surveyors would walk

throughout the assigned berm treatment assigned using an “S” pattern end to end

until the 15-minute time period had elapsed. The observer would record the type of

insect pollinators that encountered the reproductive parts of blooming flowers.

Aspiration of Insect Pollinators

Insect pollinators were collected by aspiration weekly throughout the season.

After the floral assessment and observation period were completed, surveyors would

complete a 15-minute flower visiting insects aspiration period. Surveyors would walk

throughout the assigned berm treatment assigned using an “S” pattern end to end

until the 15-min time period had elapsed. The surveyor would aspirate any insect

pollinators, with the exclusion of honey bees and bumblebee queens, that

encountered the reproductive parts of recorded blooming flowers. Aspirated insect

pollinators were then exhaled into 500 mL clear plastic deli containers. The deli

containers were labeled with the site, and treatment, taken back to MCRS and

placed in the freezer (-18°C±2) to freeze-kill the insects. Insects were returned to the

University of Guelph and identified to family.

In 2019, four berm sites (Site 1 and 3-5) were monitored weekly from 6 June to

29 August for insect pollinators. Sites were visited in a random order each week, a

schedule for site visitation (Appendix C). The same sampling criteria for weather that

was used in 2018 was applied in 2019 although the sampling methods were altered

from observational and aspiration to sweep netting. The sampling method was

modified to simplify the collection of data.

Sweep Netting

Sweep netting samples for insect pollinators occurred weekly over the sampling

period. A sweep sample consisted of 15 figure-eight sweeps with a 38 cm diameter

net along one of three parallel transects. The three parallel transects were flagged

out one to three, with one being closest to the road at each site. Each transect was 5

m in length, and were 0.5 m from the treatment edge, with 1 m between each

transect (Figure 2.7). Transects were walked in a random order at each treatment

and surveyors were randomly assigned to a treatment at each berm site. After each

sweep, sweep nets were flipped to trap captures and the end of the net was put into

a kill jar until the insects were dead. Kill jars were made from 29 cm by 20 cm by

15.5 cm lunch coolers with an acetone-soaked paper towel. The insects and

vegetation in the nets were transferred from the net to a 500 mL deli container and

labeled with the corresponding treatment and transect number. At the end of the

field day, containers were put into a freezer for later processing. Collected insects

were identified to the insect pollinator groups of honey bee, bumblebee, solitary bee,

or hover fly.

3.3 Statistical Analysis

The composition of the blooming floral community was compared among

treatments at berm sites using a non-metric multidimensional scaling (NMDS). The

percent coverage of each floral species was averaged across each treatment at

each site for both 2018 and the 2019. The similarity among treatments was

quantified using the zero-adjusted Bray-Curtis coefficient, accounting for

heteroscedasticity when multiple zeros are present for many species. The matrix

developed was used to create the NMDS ordination, in which treatments are ranked

on their similarities. On the ordination space, floral communities which are similar fall

closer together, and the distance between the treatments increases as treatments

become dissimilar in composition. A PERMANOVA was done to test for differences between groups using 999 permutations with the Bray-Curtis method. Assumptions of homogeneity of multivariate dispersion were met. All statistical analysis was preformed using the package vegan (version 2.5-6) in R, version 3.5.2 (The R

Foundation, Vienna, Austria).

The abundance of honey bees, bumblebees, solitary bees, and hover flies that were observed in 2018 and solitary bees and hover flies that were collected through sweep netting in 2019, were analyzed with a generalized linear mixed model

(GLMM) using a negative binomial distribution in PROC GLIMMIX with treatment as the fixed and berm site as the random factor. In 2019, honey bees and bumblebees were analyzed with a Possion distribution. In both years, SAS University Edition 9.4

(SAS Institute Inc., Carry, NC, USA) was used to analyze the GLMMs. An α=0.05 was used in all analyses. Means separation was done using Tukey’s HSD post-hoc test when a significant difference was identified.

From the 2018 pollinator observational assessment the standardized specialization (d’ prime index) was calculated for each plant species, for both planted and naturally occurring flowers on canal berms, and each pollinator group.

This index ranges from 0, the pollinator group having no specialization, to 1, a group being a perfect specialist. This analysis was performed with dfun, using the package bipartite (version 2.15) in R, version 3.5.2 (The R Foundation, Vienna, Austria). A bipartite pollinator network was produced displaying pollinator group interactions

with specific floral species. No statistical analysis was carried out on the

characterization of land cover.

3.4 Results

Characterization of Landscape

At a 750 m radius surrounding canal berm site centroid points, approximately

two-thirds of the sites had at least half of this area identified as agricultural land, with

a range of 45% to 65%. At this radius, natural areas were variable with some sites

having as little as one-quarter of the area and others having more than half of the

area surrounding the site as natural/semi-natural lands, with a range of 26% to 53%.

Rural/urban land at this radius was always below 20% (Table 3.1 and Figure 3.2).

At a 2000 m radius surrounding canal berm site centroid points, every site had

more than half of the area as agricultural land, with a range of 56% to 75%. At this

radius almost all the sites had below one-quarter of the area as natural/semi-natural

land. Rural/urban land at this radius was always below 15% (Table 3.2 and Figure

3.3)

Table 3.1: Area in hectares, of land use classes from the centroid of each canal berm site, at a radius of 750 m in the Holland Marsh, Ontario. Land Use Class Site 1a Site 2a Site 3a Site 4a Site 5a Agricultural Land 115 80 102 86 99 Natural/semi-natural Land 47 93 61 64 48 Rural/urban Land 15 4 14 27 30 a – Area of each land use class is measured in hectares.

Table 3.2: Area in hectares, of land use classes from the centroid of each canal berm site, at a radius of 2000 m in the Holland Marsh, Ontario. Land Use Class Site 1a Site 2a Site 3a Site 4a Site 5a Agricultural Land 862 709 909 947 917 Natural/semi-natural Land 202 473 275 215 163 Rural/urban Land 191 73 71 93 176 a – Area of each land use class is measured in hectares.

Figure 3.2: Buffer with 750 m a radius from the centroid of each canal berm site at the Holland Marsh, Ontario. Land use data has been clipped to these buffers and separated into three land classes.

Figure 3.3: Buffer with 2000 m a radius from the centroid of each canal berm site at the Holland Marsh, Ontario. Land use data has been clipped to these buffers and separated into three land classes.

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Floral Assessment

In 2018, the NMDS analyses showed there were significant differences in

blooming floral community composition among treatments (F2,9=1.959; p=0.035).

(two-dimensional stress 1.7). Both the floral and the floral + shrub were grouped

closer together and were more like each other than the control treatment (Figure

3.4).

In 2019, the NMDS analyses showed no significant differences (F2,9=1.0157;

p=0.422) in blooming floral community composition among treatments (two-

dimensional stress 1.5). Blooming floral composition among treatment and sites

were more similar to each other this year. In site four, the floral treatment, was

similar to the control treatment, and in site one, the floral was similar to the floral +

shrub treatment (Figure 3.5).

The observed floral blooming period for species that were planted as part of

berm enhancements are shown in Table 3.3, and the naturally occurring species

from the existing seed bank are shown in Table 3.4, for the months of July to

September for 2018 and June to August for 2019. The agricultural pollinator mix and

shrubs had a blooming period that covers from May into September.

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Figure 3.4: NMDS ordinal depicts the relationship of blooming floral community composition among canal berm sites and treatments, from 10 July to 19 September, 2018.

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Figure 3.5: NMDS ordinal depicts the relationship of blooming floral community composition among canal berm sites and treatments, from 6 June to 29 August, 2019.

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Table 3.3: Observed bloom period from floral species planted in canal berm enhancements, from July to September 2018, and May to August, 2019 in the Holland Marsh, Ontario. Observed Bloom Observed Bloom Period 2018 Period 2019 Common Name Scientific Name July August Sept. May June July August

Agricultural Alsike Clover Trifolium hybridum X X X X X

Pollinator Mix Birds-foot Trefoil Lotus corniculatus X X X X X X

Common Tansy Tanacetum vulgare X X X X X

Red Clover Trifolium pratense X X X X X X

Sweet Yellow Clover Melilotus officinalis X X X X X X

Planted Shrubs Red Currant Ribes rubrum X X

Haskap Lonicera caerulea X X

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Table 3.4: Observed bloom period from floral species present in canal berm seed banks, from July to September 2018, and May to August, 2019 in the Holland Marsh, Ontario. Observed Bloom Observed Bloom Period 2018 Period 2019 Common Name Scientific Name July August Sept. May June July August

Flowers Present Aster Aster amellus X in Seed Bed Borage Echium vulgare X X X X X X

Canadian Goldenrod Solidago canadensis X X X

Chicory Cichorium intybus X X X X X

Crown Vetch Securigera varia X X X X

Dandelion Taraxacum officinale X X X

Daisy Bellis perennis X X X X

Evening Primrose Oenothera biennis X X X X

Field Thistle Cirsium discolor X X X X X

Flat Top Goldenrod Euthamia graminifolia X X X

Flea Bane Erigeron annuus X X X X X X

Hairy Vetch Vicia villosa X X X X X X

Medick Medicago sp. X X X X X

Mother Wort Leonurus cardiaca X X

Mustard Sinapis arvensis X X X X X

Queen Anne's Lace Daucus carota X X X X X

Sow Thistle Sonchus sp. X X X X X

Shepherd's Purse Capsella bursa-pastoris X X

St John's Wort Hypericum perforatum X X

Sweet White Clover Melilotus albus X X X X X X

Wild Lettuce Lactuca virosa X X X X

Yarrow Achillea millefolium X X

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Insect Pollinator Monitoring in 2018

A total of 229 individual honey bees were observed during pollinator observation

periods in berm treatments. There was no significant difference found in the

abundance of honey bees observed over the season among any of the treatments

(F2,117=2.14; p=0.1221). The control, floral, and the floral + shrub treatments had a

mean abundance of 13.8 (±3.92), 18.2 (±4.42) and 27.8 (±10.28) honey bees

observed per treatment, respectively (Figure 3.6).

A total of 443 individual bumblebees were observed during pollinator observation

periods in berm treatments. There was no significant difference found in the

abundance of bumblebees observed over the season among any of the treatments

(F2,115=0.98; p=0.3794). The control, floral, and the floral + shrub treatments had a

mean abundance of 42 (±9.95), 39.2 (±4.48) and 33.2 (±8.06) bumblebees observed

per treatment, respectively (Figure 3.6).

A total of 207 individual solitary bees were observed during pollinator observation

periods in berm treatments. There was no significant difference found in the

abundance of solitary bees observed over the season among any of the treatments

(F2,114=0.32; p=0.7249). The control, floral, and the floral + shrub treatments had a

mean abundance of 19.3 (±5.57), 16 (±1.38) and 16.6 (±3.57) solitary bees

observed per treatment, respectively (Figure 3.6).

A total of 279 individual hover flies were observed during pollinator observation

periods in berm treatments. There was no significant difference found in the

abundance of hover flies observed over the season among any of the treatments

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(F2,113=0.79; p=0.4559). The control, floral, and the floral + shrub treatments had a mean abundance of 25.5 (±2.47), 24.4 (±2.06) and 19.8 (±6.18) hover flies observed per treatment, respectively (Figure 3.6).

In the control treatment > 60% of the taxa collected during aspiration periods were bumblebees, and > 30% of the taxa collected were solitary bees (Table 3.5). In the floral treatment, bumblebees and solitary bees were approximately 30% of the taxa collected each, and hover flies were approximately 40% (Table 3.5). In floral + shrub treatments, hover flies, bumblebees, and solitary bees accounted for 37%,

35% and 28% of the taxa collected, respectively. Monarch butterflies were observed flying around berm sites in 2018.

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60 Control Floral 50 Floral + Shrub

20 Mean Abundance Mean

0 Honey Bee Bumblebee Solitary Bee Hover Fly 2018

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Table 3.5: List of insect pollinator taxa and number of individuals captured by aspiration in berm site treatments at the Holland Marsh, Ontario from 10 July to 19 September, 2018. Family Genus Species Control Floral Floral + Shrub Syrphidae 0 54 56 Andrenidae 1 0 0 Apidae 2 2 3 Bombus bimaculatus 12 8 10 Bombus impatiens 73 29 35 Bombus pensylvanicus 0 0 2 Bombus perplexus 3 0 3 Bombus rufocinctus 1 4 2 Ceratina 5 0 2 Colletidae 1 1 2 Hylaeus 1 0 0 Halictidae 28 28 29 Halictus 1 1 0 Lasioglossum 1 6 1 Megachilidae 11 6 3 Megachile rotundata 0 0 2

Standardized specialization indexes (d’ prime index) were calculated for each

pollinator group, honey bees (0.33) were the most specialized insect pollinator for

the floral species present on canal berms in 2018. Solitary bees (0.21), hover flies

(0.20), and bumblebees (0.19) were similarly specialized for the floral species

present on canal berm in 2018. Sweet white clover (0.34), hairy vetch (0.22), sow

thistle (0.21) had the most specialized visit from insect pollinators (Figure 3.7).

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Insect Pollinator Monitoring in 2019

A total of 247 individual honey bees were collected using sweep netting in berm

treatments. There was no significant difference found in the abundance of honey

bees collected in sweep nets over the season among any of the treatments

(F2,1=16.26; p=0.1727). The control, floral, and the floral + shrub treatments had a

mean abundance of 31.3 (±23.4), 11.4 (±5.53) and 19 (±5.63) honey bees collected

per treatment, respectively (Figure 3.8).

A total of 30 individual bumblebees were collected using sweep netting in berm

treatments. There was no significant difference found in the abundance bumblebees

collected in sweep nets over the season among any of the treatments (F2,1=3.20;

p=0.3677). The control, floral, and the floral + shrub treatments had a mean

abundance of 2.5 (±1.85), 3.2 (±1.22) and 1.2 (±0) bumblebees collected per

treatment, respectively (Figure 3.8).

A total of 267 individual solitary bees were collected using sweep netting in berm

treatments. There was a significant difference among treatments in the abundance

of solitary bees collected over the season through sweep netting (F2,117=4.50;

p=0.0131). There were significantly more solitary bees collected in the floral + shrub

than in the control treatment, but the floral treatment was no different from the

control or floral + shrub. The control, floral, and floral + shrub treatments had a mean

abundance of 12.8 (±4.33), 17.4 (±7.73) and 30.2 (±11.18) solitary bees collected

per treatment, respectively (Figure 3.8).

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A total of 866 individual hover flies were collected using sweep netting in berm treatments. There was no significant difference found in the abundance of hover flies collected in sweep nets over the season among any of the treatments (F2,117=0.17; p=0.8468). The control, floral, and floral + shrub treatments had a mean abundance of 63.3 (±19.52), 80.2 (±19.48) and 69.4 (±22.6) hover flies collected per treatment, respectively (Figure 3.8). Monarch butterflies were observed flying around berm sites and larvae were found on butterfly milkweed at berm site five in 2019.

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Control 110 Floral *ns 100 Floral + Shrub 90 80 70 60 50 *ns A 40

Mean Abundance Mean 30 AB 20 B 10 *ns 0 Honey Bee Bumblebee Solitary Bee Hover Fly 2019

3.5 Discussion

Many factors such as, increases in global food demand, has resulted in the

intensification of agroecosystems (Godfrey et al. 2010). Restoring or enhancing

uncultivated marginal lands in intensive agroecosystems to support the biodiversity

and ecosystem services provided by beneficial insects is important to ensure long-

term sustainability of agriculture (Bommarco et al. 2012, Tscharntke et al. 2012,

Pretty and Bharucha 2014). No studies to date have evaluated the abundance of

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insect pollinators in non-crop habitat surrounding the intensive agroecosystem of the

HM. This study was conducted to document how canal berm enhancements affect insect pollinator communities, and to provide information to improve pollinator conservation in and around the agroecosystem of the HM.

This study suggests that the enhancement of uncultivated marginal lands through the establishment of mixed floral and floral + shrub plantings, could play a role that positively affects the abundance of some insect pollinator groups in areas adjacent to intensively cultivated fields. The greater number of solitary bees in the floral + shrub enhancement support established patterns that the addition of floral resources to marginal uncultivated lands surrounding agroecosystems support a greater abundance of some non-Apis bees (Lentini et al. 2012, Morandin and Kremen 2013,

Blaauw and Isaacs 2014).

The lack of difference in honey bees, bumblebees, hoverflies, and solitary bees in some years was somewhat expected because of the proximity of treatments and age of enhancements. Our sampling method show the use of floral resources among treatments rather than differences in populations from enhancements as the study organisms are highly mobile. Non-Apis bee populations take time to establish and can change year to year based partly on the availability of floral resources in previous years (Williams et al. 2001, Blaauw and Isaacs 2014). The floral enhancements on canal berm sites were established in 2017 and 2018, making these the first and second years of pollinator observation and collection from these enhanced sites. It can take three to five years for wildflower planting on 114

enhancements to become established (May et al. 2017, Neal 2019). The changes in non-Apis bee populations may not be detected in short-term studies (Venturini et al.

2017). The current setup of this study can only show the differences in usage and pollinator supports of floral resources, even over multiple years of establishment, but these enhancements can potentially lend to greater populations over time if the supporting resources lead to greater reproduction.

The numbers in each insect pollinator groups differed between the two years.

This difference was likely due to differences in both the collection method and reporting period between the two years. In 2018, observational and aspiration collections reported over a total of 30 min time period was used to determine the abundance of insect pollinators, while in 2019 insects were collected by sweep netting along transects. Using the observational and aspiration methods can be biased towards larger bodied insect pollinators like bumblebees because they are easier to see than smaller solitary bees and hover flies. The recording of pollinators and blooming floral resources did differ over the two years. The 10 weeks in 2018 occurred from the second week in July until the third week in September, whereas the 10 weeks in 2019 occurred from June until the end of August. The difference in the collection periods for pollinator was due to refined methodology and an effort to increase efficiency of time management for assessments. The air temperature in

May (15.8°C), 2018 was above average when compare to the previous 10-year average (13.9°C). In 2019, the air temperature in May (11.4°C) was below average when compared to the previous 10-year average (14.3°C). The air temperatures

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from June until September were either average or above average when compared to the previous 10-year average. The differences in weather at the beginning of the season might have played a role in the slower start for flowers and therefore, abundance of pollinators in 2019.

In 2018, there was a significant difference in blooming floral community composition among treatments, the floral and floral + shrub treatments were more similar to each other than to the control treatments. Contrary to our expectations, there was no difference in blooming floral community composition among treatments in 2019; the control, floral and floral + shrub communities were similar to each other.

Floral observations indicated that control treatments became more contaminated with species from the agricultural pollinator mix in 2019 when compared to 2018.

There was 9.5 times more sweet yellow clover and 2 times more red clover and alsike clover at control sites in 2019 than in 2018. This suggests that treatment spacing of plants and mobility of pollinators might be an important aspect to consider when designing studies that look at the differences in insect pollinator and floral communities due to spill-over between treatments. It was impressive to see the number of naturally occurring flowers present in both the control and enhancement treatments. Understanding the current seed bank of naturally occurring flowers could aid in the choices of additional floral resources in future enhancements.

The assessment of the standardized specialization index, which mainly reflects reciprocal specialization (Blüthgen et al. 2008) shows that the four groups of insect pollinators were generally flexible in floral preference when assessed at this high 116

level. Research has shown that flower visitation for species of insect pollinators, even those thought of as generalists, display species specialization (Fründ et al.

2010). Within the larger groups of bumblebees, solitary bees and hover flies there could be species that are more specialized. Refining the taxonomic scale would indicate if certain insect pollinator species are more specialized on a floral species and could help improve seed choices in planting for pollinator conservation.

Observations from the bipartite pollinator network can also be used to increase our understanding of preferred floral resources for insect pollinator groups. Using this information, we could make recommendation for floral species choices for future seed mix combinations based on the insect pollinator groups we are hoping to support.

Landscape characterization by land class showed that at both the 750 m and

2000 m scale berm sites were surrounded by at least 50% agricultural land. Rural and urban landscapes were always under 20% of land coverage at both the 750 m and 2000 m scales. Natural and semi-natural land was always under 25% land coverage at the 2000 m scale, and was more variable at 750 m, from approximately

25% to 50% land coverage. This natural and semi-natural land coverage offers the best opportunity to participate in pollinator conservation through the floral enhancement of these areas. The addition of floral resources at these different landscape scales can reduce landscape fragmentation and support both managed honey bees (Decourtye et al.2010) and non-Apis bees (Nicholls and Altieri 2013,

Kennedy et al. 2013).

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This study has shown that canal berm enhancements can support some insect pollinator groups. Insect pollinators as an ecosystem service provider is often not of any consequence to growers in the HM, as there is little, to no need, for use of pollination in the crops they cultivate. As such, pollinator conservation is not always at the forefront when conversations take place on how best to maintain uncultivated marginal lands surrounding their businesses. Although we have found that enhanced floral and floral + shrub berm treatments can benefit one group of insect pollinators, there is always concern from growers about the possible impact of pest species finding refuge in these uncultivated areas. In the previous chapter, we showed that the enhancement of canal berms does not support primary insect pest populations of crops grown at the HM. Engaging and sharing this information with growers, could help improve acceptance of adding floral resources to uncultivated canal berms, as they can be beneficial for the ecosystem by supporting pollinator conservation.

These ‘working lands’ are key areas for the preservation of declining beneficial insects including threatened and endangered species (Kremen and Merenlender

2018). Research has shown that there is a difference between the delivery and management of pollination service to an agroecosystem and pollinator conservation

(Kleijn et al. 2015, Senapathi et al. 2015). Because this agroecosystem does not require pollination services, it offered the opportunity to focus merely on aspects of preserving pollinator diversity and the conservation of threatened non-Apis pollinators.

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The current research had some limitations. One limitation was the proximity of berm treatments to each other at the berm sites when assessing highly mobile organisms such as most pollinators. This made it difficult to differentiate between insect pollinator communities as most non-Apis bees have a maximum foraging distance of 750 m (Osborne et al. 1999, Gathmann and Tscharntke 2002,

Zurbuchen et al. 2010) and, as such, were not independent communities among treatments. In terms of the floral communities, plants established in the enhancement plots also started to appear more frequently in the control plots, especially in year two of the study. Moving control sites at least 1 km away from enhanced treatment sites would allow independent communities non-Apis bee to be assessed and quantified.

Another limitation was the taxonomic resolution; insect pollinators were grouped into four main types of insect pollinators of honey bees, bumblebees, solitary bees, and hoverflies. Increasing taxonomic resolution to the genus or species level and relating them to the floral species they were visiting would provide more details on which species specialized on which flowers and could be useful if looking to improve floral mixes for the conservation of threatened non-Apis bee species.

Another issue was the establishment of the agricultural pollinator mix, the milkweed and shrubs in the enhanced areas. At enhancement sites, sweet yellow clover became an issue, it grew as tall as 1.82 m at some sites. This made it difficult for other plants, especially the milkweed and shrubs, to establish due to their slow growth, small stature, and need for sun. Another issue in year one, the sweet yellow 119

clover established itself as the most dominant floral, and then it went to seed in early to mid-July leaving very little abundance of other floral resources at enhanced sites.

With time, the shrubs should mature, grow and provide different vegetative heights and levels to the enhancement. Site maintenance such as prescribed burns or mow downs is need every 4-5 years to encourage regrowth (May et al. 2017, Neal 2019).

Longitudinal studies on the enhancement of non-crop habitat over several seasons would allow for the differences between these two treatments to be more defined.

This project could take several future directions. One issue arising from this project was the societal perspective on the aesthetic appearance of the berms.

Community stakeholder concerns about the weedy and unkept appearance of the canal berms surrounding the HM was evident from articles in the local paper

(Appendix E) and complaints to local municipalities. Requests for all the canal berms to be mown have been made and discussed at local municipal council meetings.

Understanding how different mowing regimes of uncultivated canal berm affect insect pollinator diversity and abundance when compared planted floral enhancements is important.

Another direction this project could take is to determine what native wildflower could be planted in enhance the conservation of threatened pollinator species, along with the economic cost of different native wildflower seed mixes. Researchers could then assess how these native seed mixes influence insect pollinator assemblages and could make for more ecological friendly enhancements, seed mixes that may be

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more aesthetically pleasing to community stakeholders and help conserve threatened pollinator species.

This study investigated the potential of small-scale enhancements to non-crop habitat (canal berms) in an intensive agroecosystem, and demonstrated that there was an increase in support to solitary bees in one year in the HM. Further assessment and experimentation at these berm sites, and their influence on pollinator conservation in the HM agroecosystem, should be conducted in 2020 and onwards. If these treatments continue to support insect pollinators, they could contribute to ensuring the long-term sustainability through pollinator support and conservation within an intensive agroecosystem.

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CHAPTER 4

GENERAL CONCLUSION

No studies to date have evaluated the role that non-crop habitat (canal berms) could play for supporting beneficial insects and the long-term sustainability of agriculture in the Holland Marsh (HM). However, a few studies have focused on natural enemy assemblages within cultivated areas of the HM (Tomlin et al. 1985, Lemay et al.

2018). Research from other types of agroecosystems have shown that by enhancing habitat at a landscape scale for both pest management (Thies and Tscharntke 1999,

Gardiner et al. 2009, Chaplin-Kramer et al. 2011) and pollinator conservation

(Bommarco et al. 2012, Tscharntke et al. 2012, Pretty and Bharucha 2014) the ecosystem and the agroecosystem can benefit in the long-term. This study was conducted to determine the role that current, and enhanced, canal berms play on the populations of natural enemies, insect pollinators, and primary insect pests, which can result in enhanced conservation biological control (CBC) if greater populations of beneficial insects are found in berm habitat and pollinator conservation in the agroecosystem of the HM.

This study demonstrated that the small-scale enhancement of non-crop habitat through the establishment of mixed floral and floral + shrub plantings can positively affect the abundance and richness of Carabidae in areas adjacent to fields with commercially cultivated crops. Supporting these natural enemies could in turn have a positive effect on the biological control of primary insect pests in cultivated fields but further research is needed. This study has also shown that the canal berm enhancements provided more floral support for solitary bees. Insect pollination is not 122

needed for the primary crops grown at the HM and as such, pollinator conservation may be a less relevant consideration for growers, but important for general support of pollinators, many of which are declining due to habitat loss.

Although this study found that enhanced floral and floral + shrub berm treatments can benefit some groups of insect pollinators and some groups of natural enemies, there is always concern from growers about the possible impact of pest species finding refugia in these uncultivated areas. Data from both years show that the enhancement of canal berms does not support populations of the primary insect pests of crops grown in the HM, which would be of concern for growers. Sharing this information with growers could help improve acceptance of adding floral resources to canal berms surrounding the HM.

The study indicates that known predators of primary insect pests are present in the commercially cultivated areas of the HM. There was substantial variation of abundance, richness and diversity of Carabidae in commercial carrot fields in both

2018 and 2019. Using longitudinal continuous data collection in the same commercial fields, regardless of crop type, would offer insight into how agronomic practices and surrounding landscape composition affect natural enemy assemblages.

Anaphes spp. are a known but an under-studied parasitoid of CW eggs. In 2019, they were measured using a modified technique of carrot root sections instead of egg-baited carrots. The use of this less invasive method for rearing out parasitoids may yield more reliable data in determining rates of parasitism in the field. Gaining

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more information about alternative host species, the ecological niche of Anaphes spp., and more accurate sampling methods to determine parasitism rates, could shed light on the role they play in controlling CW populations in the HM.

There are several future directions this current research could take, not all of them specific to scientific work. Projects focused on sustainability in the agroecosystem can be seen through several lenses such as, economic, social, and cultural perspectives and it is important not to silo these lenses into specific streams.

Future work should incorporate several disciplines so that well-rounded conclusions, which incorporate both science and the humanities can become more accessible to policymakers and the public.

Although it was found that enhanced floral and floral + shrub berm treatments can benefit some groups of natural enemies, it is not clear what effects, if any, the enhancements had on the control of the primary pest populations in commercial cultivated fields at the HM. A study of how larger landscapes can influence an IPM program, pest numbers, and crop damage would be the next step to build on the information gathered from this study. This further research would aim to understand the effects that canal berm enhancements might have on insect pest control.

One issue arising from this project was the societal perspective on the aesthetic appearance of the berms. Community stakeholders were concerned about the weedy and unkept appearance of the canal berms surrounding the HM. Requests for all the canal berms to be mown were made and discussed at the local municipal level. The concerns raised have led to questions about the mobilization, transfer of

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knowledge and public engagement on landscape diversity and how increasing landscape complexity in agroecosystems can be beneficial to both the agroecosystem and the natural ecosystem. Grower and public outreach, sharing the research in accessible manner and having an open dialog with community stake holders, are all important for conducting applied research in agroecology.

This study demonstrates that floral and floral + shrub berm enhancements can help support some groups of natural enemies, which in turn may improve the biological control of primary insect pests at the HM. The results also show that berm enhancements do not provide refugia for primary insect pests, so currently there is little concern about a potential negative impact of canal berm enhancements on commercially cultivated crops at the HM. The flowers on the canal berms provided additional floral resources for insect pollinators, and the enhanced flower planting increased the number of solitary bees in one year.

This research is a starting point to identify how the uncultivated land can be modified to benefit both the agroecosystem and the natural ecosystem. The vegetative enhancements at the berm sites have provided opportunities for both growers and the public to observe land stewardship, sustainable pest management, and pollinator conservation in an intensively cultivated agroecosystem. Further assessment and experimentation at these berm sites, and their influence on pest management and pollinator conservation in the HM, should be conducted in 2020 and onwards. Collections from the past two years have shown that berm enhancements had a positive impact on the abundance of some natural enemy 125

groups, specifically Carabidae predators, as well as insect pollinators, specifically solitary bees, and the ecosystem services that they may provide. If these treatments continue to support natural enemies and insect pollinators, without providing refuge for or increasing populations of primary insect pests of the HM, they could contribute to ensuring the long-term sustainability of this specialized agroecosystem.

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APPENDICES

Appendix A: Randomly assigned berm treatments from left to right when viewed head on from the road at each site.

Berm Site Treatment Left Treatment Center Treatment Right 1 Control Shrub Floral 2 Floral Control Shrub 3 Shrub Floral Control 4 Shrub Control Floral 5 Control Shrub Floral

Appendix B: Random site visitation schedule from 1 May to 19 September 2018.

Month Week of the Site 1 Site 2 Site 3 Site 4 Site 5 May 1 4 2 5 3 1 May 7 4 2 1 5 3 May 14 2 5 4 1 3 May 21 4 3 2 5 1 May 28 1 2 4 3 5 June 4 2 4 1 5 3 June 11 4 2 3 1 5 June 18 5 1 4 2 3 June 25 4 5 3 2 1 July 2 2 3 4 1 5 July 9 3 2 5 4 1 July 16 4 2 3 1 5 July 23 4 5 1 2 3 July 30 2 5 3 4 1 August 6 5 3 2 4 1 August 13 1 2 3 4 5 August 20 1 2 4 3 5 August 27 5 4 1 3 2 September 3 3 1 4 2 5 September 10 3 2 5 4 1 September 17 3 2 1 5 4

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Appendix C: Random site visitation schedule from 1 May to 3 September 2019.

Month Week of the Site 1 Site 2 Site 3 Site 4 Site 5 May 1 4 5 1 2 3 May 7 2 5 3 4 1 May 14 5 3 2 4 1 May 21 1 2 3 4 5 May 28 1 2 4 3 5 June 4 5 4 1 3 2 June 11 3 1 4 2 5 June 18 3 2 5 4 1 June 25 4 5 3 2 1 July 2 3 2 4 1 5 July 9 3 2 5 1 4 July 16 1 5 2 4 3 July 23 4 3 5 2 1 July 30 2 5 1 3 4 August 6 1 4 2 5 3 August 13 4 2 1 3 5 August 20 5 3 1 4 2 August 27 3 5 4 1 2 September 3 3 1 4 2 5

Appendix D: Type III Test of Fixed Effects Table

Figure/Table Description Type III Test of Fixed Effects Table

Figure 2.11 Carabidae/week 2018

Figure 2.12 Carabidae/week 2019

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Figure 2.13 Staphyliniade/week 2019

Table 2.3 No. Taxa 2018

Table 2.3 Abundance 2018

Table 2.3 SDI 2018

Table 2.4 No. Taxa 2019

Table 2.4 Abundance 2019

Table 2.4 SDI 2019

Figure 2.16 ALH/week 2018

Figure 2.17 OM/week 2019

Figure 2.18 TPB/week 2019

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Figure 2.19 Mymaridae/week 2019

Figure 3.6 HB/season 2018

Figure 3.6 BB/season 2018

Figure 3.6 SB/season 2018

Figure 3.6 HF/season 2018

Figure 3.7 HB/season 2019

Figure 3.7 BB/season 2019

Figure 3.7 SB/season 2019

Figure 3.7 HF/season 2019

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Appendix E: Newspaper clippings from the Bradford Today about the canal berms in the Holland Marsh, Ontario.

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