Testing an Interference Competition Hypothesis to Explain the Decline of the

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1 Testing an Interference Competition Hypothesis to Explain the Decline of the Convergent Lady Beetle, Hippodamia convergens (Coleoptera: Coccinellidae), in Ohio. THESIS Presented in Partial Fulfillment of the Requirements for the Degree Master of Science in the Graduate School of The Ohio State University By Chelsea Smith Graduate Program in Entomology The Ohio State University 2012 Master's Examination Committee: Mary Gardiner, Adviser John Cardina Daniel A. Herms Andrew Michel

2 Copyrighted by Chelsea Ann Smith 2012

3 Abstract A significant decline in the abundance of the native coccinellid, Hippodamia convergens, coincides with the establishment and population increase of exotic coccinellids in Ohio. This pattern has lead to the hypothesis that intraguild predation by exotic lady beetles explains this decline. Intraguild predation (IGP) is the act of two species, which share a limiting resource, preying on each other. Several laboratory experiments demonstrating the propensity of exotic lady beetles to act as predators of native coccinellid eggs provide support for this hypothesis. The goal of this research was to determine the extent that exotic lady beetles predate on native coccinellid egg masses in the field. Two studies conducted over the course of three field seasons ( ), are presented in Chapters 2 and 3 of this thesis. Chapter 2 examines the extent of predation on coccinellid egg masses, and the role of coccinellids as egg predators. The objectives were to 1) compare the extent of egg predation experienced by three coccinellid species: H. convergens, Coleomegilla maculata, and Harmonia axyridis; 2) examine the levels of egg predation occurring across three habitats; and 3) determine the guild of predators responsible for coccinellid egg predation. To address these objectives, egg predation experiments were conducted in habitats where coccinellids are commonly found foraging: grassland, alfalfa, and ii

4 soybean. Eggs of each focal coccinellid species were placed in the fields for 48 hours. The proportion of eggs remaining was compared among lady beetle species and the habitats. Egg masses from the increasingly-rare native lady beetle, H. convergens, incurred significantly greater predation than eggs from the common exotic lady beetle, H. axyridis. Predation of the egg masses from the three species varied across habitats with the greatest amount of predation occurring in grasslands and the least in the alfalfa. These egg predation experiments provided supporting evidence for the IGP hypothesis. Video surveillance systems were placed in the field and focused on coccinellid egg masses. These preliminary video experiments provided evidence that exotic coccinellids were not common predators of the egg masses. Chapter 3 details video experiments conducted to determine patterns among the guild of predators contributing to coccinellid egg predation. The objectives of this study were to 1) measure the relative abundance and activity density of coccinellid egg predators present within grasslands, alfalfa and soybean fields across Ohio; 2) document the contribution of predator species to native and exotic lady beetle egg predation within each foraging habitat; and 3) determine if the relative abundance of aphids affects the intensity of egg predation experienced by lady beetle egg masses. To address these objectives, video surveillance systems were used to observe predation of H. convergens and H. axyridis egg masses in soybean, alfalfa, and grassland habitats. The relative abundance and activity density of aphids and egg predators was also determined using quadrat sampling, sweep samples, and pitfall traps. From the video observations, the guild of egg predators detected included Stylommatophora, Opiliones, Oniscidea, iii

5 Coccinellidae, Gryllidae, Neuroptera, Tettigoniidae, Acrididae, Formicidae, Nabidae, Thripidae, Syrphidae, Araneae, Staphylinidae, and Diplopoda. This guild varied in diversity across the habitats, with the greatest diversity found within grassland habitats. Redundancy analysis revealed two egg predators that maintained a constant pattern of predation across both 2010 and 2011: Formicidae and Oniscidea. These findings indicate that exotic lady beetles are not a significant predator of native coccinellid egg masses within the systems studied. iv

6 Dedicated to my Mother and Father v

7 Acknowledgments I sincerely thank my adviser, Dr. Mary M. Gardiner, for her guidance, encouragement, and constant support throughout my graduate program. Her dedication and sense of humor gave me the drive to work hard on this research and have fun in the process. I also thank my committee members, Dr. John Cardina, Dr. Daniel Herms and, Dr. Andrew Michel for their invaluable advice, support, and a continued interest in this study. I thank all of the OSU extension educators who took the time to show me field sites for this study. Without their relationships with the growers and land owners, finding suitable field sites would have been incredibly difficult. I am also pleased to thank the grower collaborators and land owners who graciously granted me permission to carry out my study in their fields. I thank the present and past members of the Agriculture Landscape Ecology (ALE) lab, Alfred Alumai, Nita Chavez, Ethan Doherty, Hilary Edgington, Kelsey Greathouse, Scott Harrison, Kara Henn, Bethany Hunt, Kathleen Jackson, Andrea Kautz, Ian McIlvaine, Ben Phillips, Jared Power, Scott Prajzner, Shawn Probst, John Roberts, and Steve Ryan, who provided valuable technical and field support as well as wonderful friendships. I also thank Liz Kolbe who donated her time help me collect samples from my field sites. vi

8 I thank Dr. Matt Grieshop, of Michigan State University, who provided the instructions and advice necessary to construct the surveillance camera systems used in this research. Also, I thank Steve Scott for giving his time and expertise to construct the camera systems. I thank Dr. Steve Naber who answered many questions about statistics. I thank Dr. Luis Cañas, the graduate studies committee chair, for his assistance, advice, and patience as I completed the qualifications necessary for earning a Master s of Science degree though the Department of Entomology. I am also pleased to thank Lori Jones and Brenda Franks for their constant support, assistance, and for answering my various questions about administrative and financial issues. I thank my family who provided unconditional love and support as I accomplished this research, and a very special thanks to my mother, Colleen, and father, Marty, who have always encouraged my education. Thanks are also extended to all of my colleagues who took part in the intellectual conversations during Dollar Beer Wednesdays. This research would not have been possible without funding. Thank you OARDC SEEDS for financial support of this project. vii

9 Vita Berkley High School, MI B.A. Biology, Albion College 2010 to present...graduate Research Associate, Department of Entomology, The Ohio State University Fields of Study Major Field: Entomology viii

10 Table of Contents Abstract... ii Acknowledgments... vi Vita... viii Table of Contents... ix List of Tables... xii List of Figures... xiv Chapter 1: A review of the hypotheses describing mechanisms of native coccinellid decline... 1 Introduction... 1 Research Objectives... 3 Biology and Ecology of Coccinellidae... 5 Biological Control... 6 Establishment of Exotics and the Decline of Native Coccinellids... 7 Interference Competition via Intraguild Predation Conclusions and Implications of Thesis Research ix

11 References Chapter 2: Native coccinellids experience greater egg predation than the common exotic Harmonia axyridis in Ohio croplands and grasslands Abstract Introduction Materials and Methods Results Discussion References Tables Figures Chapter 3: Do the predator guilds attacking coccinellid eggs vary among lady beetle species or across foraging habitats? Abstract Introduction Materials and Methods Results Discussion References x

12 Tables Figures Chapter 4: Conclusions and synthesis References Figure Bibliography xi

13 List of Tables Table 2.1: Coccinellid activity density and diversity. Yellow sticky card trap samples from the week of July 20, Table 2.2: Coccinellid activity density and diversity. Yellow sticky card trap samples from the week of June 8, Table 2.3: Coccinellid activity density and diversity. Yellow sticky card trap samples from the week of July 26, Table 2.4: Coccinellid relative abundance and diversity. Sweep samples from the week of July 20, Table 2.5: Coccinellid relative abundance and diversity, and aphid relative abundance. Sweep samples from the week of June 8, Table 2.6: Coccinellid relative abundance and diversity, and aphid relative abundance. Sweep samples from the week of July 26, Table 2.7: The percent of first attacks carried out by each predator taxa observed during the video experiments...62 Table 3.1: Means ± SEM and percentage of the total coccinellid assemblage collected via sweep sampling Table 3.2: Aphid means ± SEM collected via 0.25m 2 quadrat and sweep sampling xii

14 Table 3.3: Stepwise regression analysis explaining the observed varience in the proportion of eggs remaining xiii

15 List of Figures Figure 2.1: Summary of the egg predation experiments conducted in 2009 and 2010.The proportion of eggs remaining (mean ± SEM) in the Open (predator accessible) treatment after 48 h of exposure in the field Figure 2.2: Pie charts depicting the proportion of first attacks on egg masses carried out by each predator taxa observed during the 2010 video experiments...64 Figure 3.1: Summary of the egg predation experiments conducted in 2011.The proportion of eggs remaining (mean ± SEM) after 24 h of exposure in the field Figure 3.2: Pie charts depicting the proportion of first attacks on egg masses carried out by each predator taxa observed during the 2010 video experiments Figure 3.3: Pie charts depicting the proportion of first attacks on egg masses carried out by each predator taxa observed during the 2011 video experiments Figure 3.4: Pie charts depicting the proportion of secondary attacks on egg masses carried out by each predator taxa observed during the 2010 video experiments xiv

16 Figure 3.5: Pie charts depicting the proportion of secondary attacks on egg masses carried out by each predator taxa observed during the 2011 video experiments Figure 3.6: Mean relative abundance ± SE of the egg predators collected from pitfall traps collected in Figure 3.7: Mean relative abundance ± SE of the egg predators collected from sweep samples collected in Figure 3.8: Biplot depicting redundancy analysis showing associations between predation by common predators of coccinellid egg masses, and the habitat and species of the egg mass, 2010 first attacks Figure 3.9: Biplot depicting redundancy analysis showing associations between predation by common predators of coccinellid egg masses, and the habitat and species of the egg mass, 2011 first attacks Figure 3.10: Biplot depicting redundancy analysis showing associations between predation by common predators of coccinellid egg masses, and the habitat and species of the egg mass, 2010 secondary attacks Figure 3.11: Biplot depicting redundancy analysis showing associations between predation by common predators of coccinellid egg masses, and the habitat and species of the egg mass, 2011 secondary attacks Figure 4.1: Screen shots from a complicated sequence of IGP events that occurred at the same egg mass (H. axyridis) in an alfalfa field during the 2011 video experiments xv

17 Chapter 1: A review of the hypotheses describing mechanisms of native coccinellid decline Introduction Many studies have reported a decline in native lady beetle (Coccinellidae) populations throughout the United States that coincides with the establishment of exotic coccinellid species (Elliott et al. 1996; Colunga-Garcia & Gage 1998; Alyokhin & Sewell 2004; Evans 2004; Harmon et al. 2007). This observation has led to many hypotheses which implicate competition with exotic lady beetles as a mechanism of native lady beetle decline. The interference competition via intraguild predation (IGP) hypothesis suggests that adults and larvae of exotic lady beetles are significant predators of native lady beetle eggs and larvae (Koch 2003; Cottrell 2005). Another proposed hypothesis, exploitative competition, suggests that exotic lady beetles may be impacting native coccinellid populations through competition for shared resources, such as aphids, which displaces native species (Hardin 1960; Evans 2004). A third is the apparent competition hypothesis mediated by a shared parasitoid or disease. This hypothesis proposes that the introduction of the exotic lady beetles caused the density of parasitoids to increase, or introduced new diseases, which attack both native and exotic species, leading to a decline in the abundances of native coccinellids (Holt 1977; Hoogendoorn & Heimpel 2002). It is 1

18 possible that combinations of these hypotheses and/or others could explain the mechanisms for the decline of native lady beetle populations. Currently, we do not fully understand how these competitive interactions may be influencing native coccinellid populations. A main focus of this research was to investigate IGP as a mechanism for native lady beetle decline. Chapter 2 of this thesis examines the role of exotic lady beetles as coccinellid egg predators. Gardiner et al. (2011) had previously determined that a common native coccinellid, Coleomegilla maculata, experiences significant egg predation in soybean fields. A goal of this research was to investigate the prevalence of egg predation experienced by both common and declining native species as well as an exotic lady beetle in crop and non-crop habitats. The premise of these experiments is: if the rare native species (Hippodamia convergens) experiences significantly greater egg predation than the common exotic species (Harmonia axyridis), supporting evidence would be provided for IGP hypothesis. A large body of evidence points towards exotic lady beetles as important intraguild predators of native lady beetle egg masses (Cottrell & Yeargan 1998b; Cottrell 2005; Hautier et al. 2011) however; there has not been an intensive study to directly observe predation events on native and exotic coccinellid egg masses in the field. To observe predation on lady beetle egg masses a video surveillance system was used. The systems were modified from a design that had been used extensively in entomological field studies (Teixeira et al. 2010). Preliminary experiments with the video systems were conducted to determine the guild of predators that attacks coccinellid egg masses, and 2

19 those results are presented in Chapter 2. Chapter 3 discusses video experiments carried out to determine if the common predators observed are associated with native or exotic coccinellid egg masses, as well as if the predator taxa are associated with crop or noncrop habitats. This chapter also discusses the role of within-habitat variables, such as the relative abundance and activity density of egg predators as well as the relative abundance of extraguild prey (aphids), on egg predation. Research Objectives Objective 1: Compare the extent of egg predation experienced by native and exotic lady beetles within crop and non-crop habitats. (Chapter 2) Hypothesis: Predation on egg masses is responsible for the decline of H. convergens. Prediction: Hippodamia convergens will experience a higher amount of egg predation across habitats compared to common native or exotic lady beetle species. Objective 2: Determine the guild of predators that attack native and exotic lady beetle egg masses using video surveillance. (Chapter 2) Hypothesis: Exotic coccinellids are responsible for native lady beetle decline via IGP of native coccinellid egg masses. Prediction: Exotic coccinellids will be the dominant predator observed preying on native and exotic lady beetle egg masses. 3

20 Objective 3: Determine if egg predator taxa exhibit a preference for native or exotic lady beetle eggs. (Chapter 3) Hypothesis: A preference among generalist predators for native over exotic coccinellid eggs has contributed to native coccinellid decline Prediction: A greater number of predator taxa will be associated with native coccinellid eggs than with exotic coccinellid eggs. Objective 4: Examine the influence of aphid abundance, and the abundance and activity density of coccinellid egg predators, on the incidence of egg predation within crop and non-crop habitats. (Chapter 3) Hypothesis 1: The availability of extraguild prey decreases predation on coccinellid egg masses. Prediction: Egg predation intensity will be proportional to aphid abundance. Hypothesis 2: Coccinellid egg masses are predated on by predators that are common within that habitat. Prediction: The relative abundance and activity levels of egg predators that are commonly observed preying on the egg masses will be associated with the prevalence of egg predation that occurs on coccinellid egg masses. 4

21 Biology and Ecology of Coccinellidae Within the lady beetle family Coccinellidae (Coleoptera), there are at least 475 species found throughout the United States and Canada (Gordon 1985), and over 4000 species described worldwide (Hagen 1962). Coccinellidae includes herbivorous, fungivorous, and omnivorous species. Many of the omnivorous species are generalist predators that are considered beneficial insects in agricultural settings (Gordon 1985). Predaceous lady beetles often feed on economically important pests such as Aphidoidea (aphids), Acari (mites), Pseudococcidae (mealybugs), Coccoidea (scales), and immature stages of Lepidoptera (Hagen 1962; Hagen 1968; Gordon 1985; Herren & Neuenschwander 1991; Obrycki & Kring 1998). Omnivorous native coccinellid species found throughout North America include the convergent (Hippodamia convergens Guérin), pink (Coleomegilla maculata De Geer), parenthesis (Hippodamia parenthesis Say), thirteen spotted (Hippodamia tredecimpunctata Linnaeus), twice stabbed (Chilocorus stigma Say), orange spotted (Brachiacantha ursina Fabricius), and polished (Cycloneda munda Say) lady beetles (Gordon 1985). Native coccinellids provide a valuable biological pest control service to crops throughout the United States, including corn (Cottrell & Yeargan 1998a) and soybean (Hagen 1962, Landis et al. 2008), and there have been many efforts to increase the ecological services provided by lady beetles through biological control. 5

22 Biological Control There are three main categories of biological control: importation, augmentation, and conservation. Importation involves the introduction of a non-native species into a region to suppress a non-native pest. Augmentation is the practice of artificially increasing the population of a native biological control agent to suppress a native or nonnative pest. Conservation biological control, unlike importation or augmentation, does not involve the release of natural enemies. Instead, the goal of this practice is to preserve and enhance the environment to benefit existing natural enemy communities (Debach & Rosen 1991). Coccinellids have been used in all three methods of biological control (Obrycki & Kring 1998). As of 1985, 179 lady beetle species had been intentionally introduced into the United States and Canada to suppress pests, and 27 exotic lady beetle species had become established. Out of these 27 established species, 16 of them were introduced intentionally (Gordon 1985). The first coccinellid introduced was the vedalia beetle, Rodolia cardinalis Mulsant, from Australia in The beetle showed successful and almost immediate control of a California citrus pest, cottony-cushion scale (Icerya purchasi Maskell (Margarodidae)), which before the vedalia beetle introduction had been causing devastating damage to citrus groves. After this success, many other exotic coccinellid species were introduced into North America with hopes that they would control other pest species. After initial introductions, very few exotic coccinellids became established or showed signs of successfully controlling the target pest, leading many to question the ability of lady beetles to colonize new habitats (Caltagirone & Doutt 1989). Since then, 6

23 factors have been identified that may have inhibited certain coccinellids from establishing, such as lack of food or overwintering habitat. Other studies have found that exposure to agricultural pesticides may have been another limiting factor (Hoy & Smith 1982). Eventually, established populations of exotic lady beetles were discovered, though often not near release areas. Establishment of Exotics and the Decline of Native Coccinellids Recent population surveys have shown that there are at least four exotic coccinellids that have established populations in the north-central United States, including: the multicolored Asian (Harmonia axyridis), the fourteen-spotted (Propylea quatuordecimpunctata), the seven-spotted (Coccinella septempunctata), and the variegated (Hippodamia variegata) lady beetles. All four of these species have been imported as biological control agents in the United States. Following releases of H. axyridis in 1980 there were no reports that it had become established. It was not until 1988 when established populations of H. axyridis were first detected (Chapin & Brou 1991). It has still not been determined whether or not the establishment of H. axyridis is due to intentional releases (Tedders & Schaefer 1994) or accidental introductions at seaports. Evidence points towards introductions via sea travel since the first established population was discovered in New Orleans, Louisiana (Chapin & Brou 1991; Day et al. 1994). Releases of C. septempunctata occurred over multiple decades starting in 1958, though an established population was not discovered until 1975, and it has been hypothesized that the entry point was the port of New Jersey (Schaefer et al. 1987; Day et 7

24 al. 1994). Releases of H. variegata for use as a biological control agent started in 1986 (Ellis et al. 1999), and no established populations have been documented in the release area. In the late 1980 s, populations of H. variegata were found in eastern Canada, and by 1992 it had spread throughout much of the northeastern United States (Wheeler 1993). Established populations of P. quatuordecimpunctata were first detected in North America in 1968, far from any intentional release sites, and were just recently detected in the north-central United States (Day et al. 1994; Gardiner et al. 2009b). Coinciding with the establishment and population increase of these exotic lady beetles, census surveys documented decreased abundance of some native lady beetle species throughout the United States (Elliott et al. 1996; Ellis et al. 1999; Turnock et al. 2003). There have been many multi-year surveys of coccinellid populations before and during the decline of native lady beetle populations, but it is difficult to determine if the establishment of exotic coccinellids is a significant factor driving native lady beetle decline due to variations within the studies such as sampling methods, locations, field types, and temporal differences. Overall, studies have shown a decrease in the density of native lady beetles, as well as changes in the overall size of the total coccinellid population. As the number of exotic lady beetle species has increased, the proportion of native individuals has decreased. Native coccinellids made up almost 100% of the assemblage in the United States from 1914 to Later, after exotic species became established, sampling between 1987 and 2001 found that native species constituted a significantly lower proportion of the coccinellid community. This suggests that if exotics are responsible for the decline of native lady beetles, either the total impact of all the 8

25 exotic species reached a critical level, or the decline is being caused by the most recently introduced species. It is also clear that both the relative abundance of native coccinellid species and the size of the total coccinellids community were different before, compared to after the establishment of exotic lady beetles in the United States (Harmon et al. 2007). A study conducted over 18 years (13 years before, and 5 years after the establishment of C. septempunctata) in alfalfa, corn, and grain fields in Eastern South Dakota found that the assemblage of the coccinellid community changed as C. septempunctata became established. Native species including Hippodamia tredecimpunctata, Coccinella transversoguttata, and Adalia bipunctata were found to have decreased in abundance after the establishment of C. septempunctata, while the native C. maculata increased in abundance. Even though this appeared to be an interesting and significant trend, native lady beetle populations varied greatly from year to year, leading researchers to conclude that their findings may be a coincidence (Elliott et al. 1996). The relative abundance of coccinellids was also recorded in the Red River Valley of Manitoba from It was found that after the arrival of the exotic lady beetle, C. septempunctata, the relative abundance of H. convergens decreased (Turnock et al. 2003). Additionally, in the northeastern United States the decline of Coccinella novemnotata, which was once common, has been attributed to the establishment and increased population growth of C. septempunctata (Wheeler & Hoebeke 1995). Between 1997 and 2007, only ten specimens of C. novemnotata were collected in North America (Losey et al. 2007). A similar pattern has been documented by Colunga-Garcia and Gage (1998) in Michigan. They reported a decrease in Brachiacantha ursina, Cycloneda 9

26 munda, and Chilocorus stigma abundances after the establishment of H. axyridis. Recent samplings of coccinellid populations in grassland, soybean, and alfalfa fields in Michigan and Ohio have failed to show any signs of H. convergens, which had once been very common in the area (Gardiner et al. 2009a; Gardiner et al. 2010; Gardiner et al. in press). These survey findings have led to multiple hypotheses that attribute competition with exotic coccinellids as a mechanism for native lady beetle decline. The main focus of this thesis is the IGP hypothesis, which proposes that the decline of native coccinellids is due to intraguild predation (IGP). IGP is defined as the act where two species which are potential competitors, kill and eat each other (Polis et al. 1989). It is suspected that exotic lady beetle adults and larvae are attacking and consuming the larvae and eggs of native lady beetles, which is negatively affecting native coccinellid populations (Cottrell 2004, 2005). Interference Competition via Intraguild Predation Intraguild predation may affect the evolutionary potential of a species, as well as its abundance and distribution (Polis et al. 1989; Holt & Polis 1997). In order for IGP to be important for species assemblages, two criteria must be met: IGP should not be random, meaning that the behavior is an attribute of that species, and it is frequently occurring and widespread (Arim & Marquet 2004). There have been multiple laboratory studies conducted to test the IGP hypothesis. Cottrell and Yeargan (1998b) found that H. axyridis larvae preyed upon native C. maculata eggs more frequently than vice versa. Harmonia axyridis was also found to be 10

27 the more aggressive of the two species, and the authors suggested that the establishment of H. axyridis in sweet corn habitats may have a negative effect on populations of C. maculata. Although, C. maculata is a native species, there is no evidence that its populations are currently decreasing. A similar study involving no choice tests was conducted with adult beetles of H. axyridis, C. maculata, and another native species, Olla v-nigrum. The researchers found that H. axyridis eggs were preyed on least often (Cottrell 2005). Another study examined the response of four native species (C. maculata, C. munda, H. convergens, and O. v-nigrum) and one exotic (H. axyridis) to coccinellid eggs of the previously mentioned species. The results again suggested that native eggs are at a higher risk of IGP (Cottrell 2007). Two studies have examined the interactions between larvae of two exotic (H. axyridis and C. septempunctata) and two native (C. transversoguttata and C. convergens) lady beetles. The results of the studies revealed that the two exotic coccinellid larvae have the potential to prey on the native larvae more frequently than vice versa (Snyder et al. 2004; Yasuda et al. 2004). Many researchers have come to the same conclusion that the exotic lady beetles, particularly H. axyridis are aggressive, and mature at a faster rate than the native lady beetles, which may provide them with a competitive advantage (Cottrell & Yeargan 1998b; Cottrell 2005). These laboratory studies suggest potential for IGP to occur between native and exotic lady beetles in the field, but field studies are necessary to further test the IGP hypothesis under more natural conditions. To look for further evidence of exotic lady beetles preying on native lady beetles, gut analyses were conducted on H. axyridis collected from lime trees in Belgium. The 11

28 researchers detected alkaloids from native coccinellids, which provided additional supporting evidence for the IGP hypothesis (Hautier et al. 2011). However, gut analysis was not conducted on native lady beetles, so this study does not provide evidence that the frequency of predation by exotic lady beetles is greater than the frequently of predation by native lady beetles. Other field studies have been conducted to further test the IGP hypothesis. Gardiner et al. (2011) used C. maculata eggs to measure egg predation experienced by native coccinellids in soybean fields in Michigan and Iowa, and found that egg masses of C. maculata experienced significant predation compared to a caged control. From this study it is clear that egg predation does occur on a native coccinellid species in soybean fields, but it was not clear from this study if exotic lady beetles were a significant predator, or if native lady beetle eggs experience greater predation than exotic lady beetle eggs. Conclusions and Implications of Thesis Research Lady beetles provide a valuable biological control service in both agricultural and garden settings, by preying on aphids and other damaging crop pests. Any decrease in the abundance of a generalist predator should cause concern, since this could lead to an increased abundance of pests and pesticide use in crop production (Hagen 1962; Hagen 1968; Gordon 1985; Herren & Neuenschwander 1991; Obrycki & Kring 1998). Exotic lady beetles do provide valuable biological control services, and their establishment was initially seen as a success for biological control. Those views eventually changed as 12

29 scientists began to learn about the interactions occurring with native species, specifically involving H. axyridis and C. septempunctata which are now often considered invasive species (Elliott et al. 1996; Evans et al. 2011). Harmonia axyridis has at times become more of a nuisance than a beneficial insect due to its habit of aggregating in homes to overwinter. It is also considered a pest in the grape industry since it feeds on the fruits in the fall and a single beetle can ruin the taste of a significant portion of wine, which could lead to high economic losses for the wine industry (Koch & Galvan 2008). As generalist predators, coccinellids are important for ecosystem function, as they are often intertwined throughout the food web of a community because they feed on organisms at different trophic levels, including plants (Snyder & Evans 2006). Any alteration to their abundance could affect the abundance of many other organisms in that habitat. Since a changing environment can alter a fauna, the higher the biodiversity, the less impact a change will have. There is a general consensus that a there is a minimum number species required to maintain the function and stability of an ecosystem (Loreau et al. 2001). In addition to the importance of biodiversity, preserving the genetic diversity of a population is important as well. As a population decreases, so does its genetic diversity, and as this occurs, it becomes less likely that the population will adapt to a changing environment. Smaller populations are also sensitive to evolutionary forces such as genetic drift, which could lead to a further loss of genetic diversity (Lacy 1987). Maintaining higher populations of native coccinellids would be important for avoiding these complications caused by a low genetic diversity. 13

30 Even with the problems facing native coccinellid populations throughout the Midwestern United States, there are still no lady beetles on threatened or endangered species lists. Studies dealing with the hypotheses that try to explain the mechanisms behind the decline of native coccinellid populations should continue due to the dangers to both biological control services in agricultural settings, and the drastic changes that could harm the natural habitat of native lady beetles. References Alyokhin A. & Sewell G. (2004). Changes in a lady beetle community following the establishment of three alien species. Biological Invasions, 6, Arim M. & Marquet P.A. (2004). Intraguild predation: a widespread interaction related to species biology. Ecology Letters, 7, Caltagirone L.E. & Doutt R.L. (1989). The history of the vedalia beetle importation to California and its impact on the development of biological control. Annual Review of Entomology, 34, Chapin J.B. & Brou V.A. (1991). Harmonia axyridis (Pallas), the third species of the genus to be found in the United States (Coleoptera: coccinellidae). Proceedings of the Entomological Society of Washington, 93, Colunga-Garcia M. & Gage S.H. (1998). Arrival, extablishment, and habitat use of the multicolored asian lady beetle (Coleoptera: Coccinellidae) in a Michigan landscape. Environmental Entomology, 27, Cottrell T.E. (2004). Suitability of exotic and native lady beetle eggs (Coleoptera : Coccinellidae) for development of lady beetle larvae. Biological Control, 31, Cottrell T.E. (2005). Predation and cannibalism of lady beetle eggs by adult lady beetles. Biological Control, 34,

31 Cottrell T.E. (2007). Predation by adult and larval lady beetles (Coleoptera : Coccinellidae) on initial contact with lady beetle eggs. Environmental Entomology, 36, Cottrell T.E. & Yeargan K.V. (1998a). Effect of pollen on Coleomegilla maculata (Coleoptera: Coccinellidae) population density, predation, and cannibalism in sweet corn. Environmental Entomology, 27, Cottrell T.E. & Yeargan K.V. (1998b). Intraguild predation between an introduced lady beetle, Harmonia axyridis (Coleoptera : Coccinellidae), and a native lady beetle, Coleomegilla maculata (Coleoptera : Coccinellidae). Journal of the Kansas Entomological Society, 71, Day W.H., Prokrym D.R., Ellis D.R. & Chianese R.J. (1994). The known distribution of the predator Propylea quatuordecimpunctata (Coleoptera: Coccinellidae) in the United States, and thoughts on the origin of this species and five other exotic lady beetles in eastern North America. Entomological News, 105, Debach P. & Rosen D. (1991). Biological Control by Natural Enemies. 2 edn. Cambridge University Press, Cambridge. Elliott N., Kieckhefer R. & Kauffman W. (1996). Effects of an invading coccinellid on native coccinellids in an agricultural landscape. Oecologia, 105, Ellis D.R., Prokrym D.R. & Adams R.G. (1999). Exotic lady beetle survey in northeastern United States: Hippodamia variegata and Propylea quatuordecimpunctata (Coleoptera: Coccinellidae). Entomological News, 110, Evans E.W. (2004). Habitat displacement of North American ladybirds by an introduced species. Ecology, 85, Evans E.W., Soares A.O. & Yasuda H. (2011). Invasions by ladybugs, ladybirds, and other predatory beetles. BioControl, 56, Gardiner M.M., Allee L., Brown P., Losey J.E., Roy H. & R. S. (In press). Lessons from lady beetles: accuracy of monitoring data from US and UK citizen science programs. Frontiers in Ecology and the Environment. Gardiner M.M., Landis D.A., Gratton C., Difonzo C.D., O'Neal M., Chacon J., Wayo M.T., Schmidt N., Mueller E. & Heimpel G.E. (2009a). Landscape diversity enhances biological control of an introduced crop pest in the north-central USA. Ecological Applications, 19,

32 Gardiner M.M., Landis D.A., Gratton C., Schmidt N., O'Neal M., Mueller E., Chacon J., Heimpel G.E. & Difonzo C.D. (2009b). Landscape composition influences patterns of native and exotic lady beetle abundance. Diversity and Distributions, 15, Gardiner M. M., Tuell J., Isaacs R., Gibbs J., Ascher J. & Landis D. (2010). Implications of three biofuel crops for beneficial arthropods in agricultural landscapes. BioEnergy Research, 3, Gardiner M.M., O'Neal M.E. & Landis D.A. (2011). Intraguild predation and native lady beetle decline. PLoS One, 6, e Gordon R.D. (1985). The Coccinellidae (Coleoptera) of America north of Mexico. Journal of the New York Entomological Society, 93, Hagen K.S. (1962). Biology and ecology of predaceous Coccinellidae. Annual Review of Entomology, 7, Hagen K.S. (1968). Impact of pathogens, parasites, and predators on aphids. Annual Review of Entomology, 13, Hardin G. (1960). The competitive exclusion principle. Science, 131, Harmon J.P., Stephens E. & Losey J. (2007). The decline of native coccinellids (Coleoptera : Coccinellidae) in the United States and Canada. Journal of Insect Conservation, 11, Hautier L., Martin G.S., Callier P., de Biseau J.C. & Gregoire J.C. (2011). Alkaloids provide evidence of intraguild predation on native coccinellids by Harmonia axyridis in the field. Biological Invasions, 13, Herren H.R. & Neuenschwander P. (1991). Biological control of cassava pests in Africa. Annual Review of Entomology, 36. Holt R.D. (1977). Predation, apparent competition, and the structure of prey communities. Theoretical Population Biology, 12, Holt R.D. & Polis G.A. (1997). A theoretical framework for intraguild predation. American Naturalist, 149, Hoogendoorn M. & Heimpel G.E. (2002). Indirect interactions between an introduced and a native ladybird beetle species mediated by a shared parasitoid. Biological Control, 25,

33 Hoy M.A. & Smith K.B. (1982). Evaluation of Stethorus nigripes (Col.: Coccinellidae) for biological control of spider mites in California almond orchards. Entomophaga, 27, Koch R.L. (2003). The multicolored lady beetle, Harmonia axyridis: A review of its biology, uses in biological control, and non-target impacts. Journal of insect Science, 3, Koch R.L. & Galvan T.L. (2008). Bad side of a good beetle: the North American experience with Harmonia axyridis. BioControl, 53, Lacy R.C. (1987). Loss of genetic diversity from managed populations: Interacting effects of drift, mutation, immigration, selection, and population subdivision. Conservation Biology, 1, Landis D.A., Gardiner M.M., van der Werf W. & Swinton S.M. (2008). Increasing corn for biofuel production reduces biocontrol services in agricultural landscapes. Proceedings of the National Academy of Sciences of the United States of America, 105, Loreau M., Naeem S., Inchausti P., Bengtsson J., Grime J.P., Hector A., Hooper D.U., Huston M.A., Raffaelli D., Schmid B., Tilman D. & Wardle D.A. (2001). Ecology - Biodiversity and ecosystem functioning: Current knowledge and future challenges. Science, 294, Losey J., Perlman J. & Hoebeke E. (2007). Citizen scientist rediscovers rare nine-spotted lady beetle, Coccinella novemnotata, in eastern North America. Journal of Insect Conservation, 11, Obrycki J.J. & Kring T.J. (1998). Predaceous Coccinellidae in biological control. Annual Review of Entomology, 43, Polis G.A., Myers C.A. & Holt R.D. (1989). The ecology and evolution of intraguild predation - potential competitors that eat eachother. Annual Review of Ecology and Systematics, 20, Schaefer P.W., Dysart R.J. & Specht H.B. (1987). North American distribution of Coccinella septempunctata (Coleoptera, coccinellidae) and its mass appearance in coastal Delaware. Environmental Entomology, 16, Snyder W.E., Clevenger G.M. & Eigenbrode S.D. (2004). Intraguild predation and successful invasion by introduced ladybird beetles. Oecologia, 140,

34 Snyder W.E. & Evans E.W. (2006). Ecological effects of invasive arthropod generalist predators. Annu. Rev. Ecol. Evol. Syst., 37, Tedders W.L. & Schaefer P.W. (1994). Release and establishment of Harmonia axyridis (Coleoptera: Coccinellidae) in the Southeastern United States. Entomological News, 105, Teixeira L., Grieshop M. & Gut L. (2010). Effect of pheromone dispenser density on timing and duration of approaches by peachtree borer. Journal of Chemical Ecology, 36, Turnock W., Wise I. & Matheson F. (2003). Abundance of some native coccinellides (Coleoptera: Coccinellidae) before and after the appearance of Coccinella septempunctata. The Canadian Entomologist, 135, Wheeler A.G. (1993). Establishment of Hippodamia variegata and new records of Propylea quatuordecimpunctata (Coleoptera: Coccinellidae) in the eastern United States. Entomological News, 104, Wheeler A.G. & Hoebeke E.R. (1995). Coccinella novemnotata in northeastern North America - historical occurrence and current status (Coleoptera, Coccinellidae). Proceedings of the Entomological Society of Washington, 97, Yasuda H., Evans E.W., Kajita Y., Urakawa K. & Takizawa T. (2004). Asymmetric larval interactions between introduced and indigenous ladybirds in North America. Oecologia, 141,

35 Chapter 2: Native coccinellids experience greater egg predation than the common exotic Harmonia axyridis in Ohio croplands and grasslands. Abstract Several native coccinellid species across North America have experienced significant declines coinciding with the establishment and spread of exotic coccinellids. Intraguild predation (IGP) has been proposed as a possible mechanism to explain these declines; specifically, the introduction of exotic lady beetles has resulted in increased predation of native coccinellid eggs and larvae. The goal of this study was to quantify the extent of egg predation experienced by three coccinellid species, Hippodamia convergens, Harmonia axyridis, and Coleomegilla maculata, in the field and to determine the guild of predators responsible. Egg masses of the three focal species were placed within soybean, alfalfa, and grassland habitats in eight counties across Ohio in 2009 and After 48 hours of exposure, the eggs were collected and the proportion of eggs remaining was calculated. The results showed that the rare native coccinellid eggs incur a greater rate of predation than common exotic or common native coccinellid eggs, with a significantly greater proportion of eggs removed by predators from H. convergens egg masses in grassland and soybean habitats than C. maculata or H. axyridis in June, Hippodamia convergens egg masses again experienced a significantly greater level of 19

36 predation than H. axyridis eggs in soybean fields in July High levels of predation also occurred in the grassland habitat where in 2009 a significantly higher proportion of coccinellid eggs were removed by predators in the grasslands compared to the soybean and alfalfa habitats. In July 2010, C. maculata and H. convergens experienced a higher amount of predation in the grassland habitats than in the alfalfa habitats. These findings provided additional evidence for the IGP hypothesis. However, an assumption of the predation experiments was that coccinellids were attacking the egg masses. Using surveillance camera systems, egg masses of H. convergens and H. axyridis were observed within each focal habitat. A diverse guild of egg predators, which included Stylommatophora, Opiliones, Oniscidea, C. maculata (adult), Gryllidae, Neuroptera (larvae), Tettigoniidae, Acrididae, Formicidae, and Nabidae, attacked the egg masses. Exotic coccinellids were not part of this guild as predicted by previous studies. These findings support the hypothesis that predation on egg masses are a contributor to H. convergens decline; however, results do not point to exotic coccinellids as the cause of the decline of this species. Introduction The introduction and spread of exotic species has ecological and economic impacts worldwide as these organisms alter the composition and function of terrestrial and aquatic communities and ecosystems (Bertness 1984; Vitousek 1990; Gurevitch & Padilla 2004). Declines in some native species have occurred simultaneously with the introduction and spread of invaders, a pattern that implicates exotics as a cause of native 20

37 species decline (Vitousek et al. 1997; Wilcove et al. 1998; Clavero & Garcia-Berthou 2005; Pimentel et al. 2005). The influence that an introduced species has on native populations is often difficult to identify particularly among generalist predators, where both direct and indirect competitive interactions occur within food webs (Bertness 1984; Mack et al. 2000; Snyder & Evans 2006; Crowder & Snyder 2010). Interference competition is a form of direct competition where one species is more aggressive during direct interactions such as fighting or predation (Schoener 1983). Intraguild predation (IGP) is a type of interference competition where two predators within the same feeding guild prey on each other. Mechanisms of indirect competition include exploitive and apparent competition. In exploitative competition, the dominant species maintains a high growth rate when the availability of a limiting resource is insufficient to support the other competing species (Tilman 1982; Bøhn et al. 2008). Apparent competition occurs when two species are attacked by the same predator, parasite or disease, and one species is a preferable prey or host over the other. The dominant species in apparent competition is the prey/host species that maintains the highest density relative to the other prey/host species (Holt et al. 1994). Lady beetles (Coccinellidae) are an excellent model to study the impact of competitive interactions among native and exotic generalist predators because they prey on economically important agricultural pests (Hagen 1962; Hagen 1968; Gordon 1985; Herren & Neuenschwander 1991; Obrycki & Kring 1998). The popularity of releasing exotic coccinellids to enhance biological control was driven in part by the success of the vedalia beetle, Rodolia cardinalis, which was introduced from Australia to California to 21

38 suppress populations of the cottony cushion scale, Icerya purchasi, in 1889 (Caltagirone & Doutt 1989). Since the vedalia beetle success, predaceous lady beetles have been intentionally introduced as biological control agents, joining a diverse guild of native predators. Gordon (1985) reported that at least 179 lady beetle species have been intentionally introduced into the United States and Canada. As of 1985, 27 exotic lady beetle species had become established in North America, although few of these species are common enough to be regularly detected (Harmon et al. 2007). Currently four exotic coccinellid species are established in the north central United States, the multi-colored Asian (Harmonia axyridis Pallas), fourteen-spotted (Propylea quatuordecimpunctata L.), seven-spotted (Coccinella septempunctata L.), and variegated (Hippodamia variegata Goeze) lady beetles. Coinciding with the establishment of these species, several multiyear censuses have documented population declines of native lady beetle species (Wheeler & Hoebeke 1995; Elliott et al. 1996; Colunga-Garcia & Gage 1998; Turnock et al. 2003; Alyokhin & Sewell 2004; Evans 2004; Gardiner et al. 2009; Gardiner et al. 2011). Wheeler and Hoebeke (1995) attributed the decline of the nine spotted lady beetle, Coccinella novemnotata, to an increase of C. septempunctata, in the northeastern United States. Once common, only ten specimens of C. novemnotata were collected in North America between the years of 1997 and 2007 (Losey et al. 2007). A similar pattern was documented in South Dakota by Elliott et al. (1996) who attributed a 20-fold reduction in populations of Coccinella transversoguttata and Adalia bipunctata to the establishment of C. septempunctata. Colunga-Garcia and Gage (1998) also reported a decrease in populations of Brachiacantha ursina, Cycloneda munda, and Chilocorus stigma 22

39 following the establishment of H. axyridis in Michigan. Most recently, Gardiner et al. (2009, 2010, 2011, and in press) failed to detect the previously abundant Hippodamia convergens in soybean, corn, alfalfa, grasslands, or residential gardens (Gardiner et al. 2009; Gardiner et al. 2010; Gardiner et al. 2011; Gardiner et al. in press). These patterns have led to the proposal of several hypotheses implicating the introduction of exotics as the cause of native coccinellid decline. These hypotheses include interference competition via intraguild predation (Koch 2003; Cottrell 2004), exploitative competition for shared prey (Hardin 1960; Evans 2004) and apparent competition via a shared parasitoid (Hoogendoorn & Heimpel 2002). To date, the majority of research examining native coccinellid decline has focused on interference competition, proposing that the observed population decline is the result of IGP on native coccinellid eggs and larvae by exotic coccinellids. This hypothesis is supported by laboratory and field studies which have illustrated the propensity of exotic coccinellids, primarily H. axyridis and C. septempunctata, to act as intraguild predators (Snyder et al. 2004; Cottrell 2005, 2007; Gardiner & Landis 2007). The majority of studies have shown that exotic lady beetles feed on the eggs and larvae of multiple native coccinellid species as well as other predatory insects (Cottrell 2004; Snyder et al. 2004; Cottrell 2005; Sato et al. 2005; Cottrell 2007; Gardiner & Landis 2007). While there is significant evidence from laboratory studies that IGP occurs between native and exotic coccinellids, with exotic lady beetles having the competitive advantage, the actual impact of IGP on native coccinellid reproduction in the field has not been quantified. Field studies provide varied conclusions on the degree of IGP that occurs among native and exotic lady beetles. 23

40 Native coccinellid alkaloids and DNA were detected in % of field-collected H. axyridis in Europe, indicating that this coccinellid acts as an intraguild predator of native lady beetles in the field (Gagnon et al. 2011; Hautier et al. 2011) Although, it is unknown if the level of predation is sufficient to affect native coccinellid populations. Hoogendoorn and Heimpel (2004) found that in field cages, the presence of H. axyridis larvae did not impact the survival or weight gain of C. maculata larvae. These findings suggest that larval interactions between H. axyridis and C. maculata may not have a negative effect on the native coccinellid species. In another study using the same species, Gardiner et al. (2011) found that C. maculata incurs significant egg predation compared to a caged control in soybean fields, indicating that predation on coccinellid eggs does occur in the field. However, the contribution of exotic lady beetles to this predation was not measured. A determination of which animals consume coccinellid eggs, as well as a measure of the prevalence of predation on different coccinellid egg mass species in different habitats was necessary to develop a better understanding of the importance of coccinellid IGP for native lady beetle decline. Our goal was to test the hypothesis that egg predation by exotic coccinellids has contributed to the decline of native lady beetles. Our predictions were that 1) the rare native lady beetle H. convergens would incur greater egg predation than a common native (Coleomegilla maculata) or exotic (Harmonia axyridis) species, and 2) exotic lady beetles would be a dominant coccinellid egg predator. To test our hypothesis we established three research objectives: 1) Compare the extent of egg predation experienced by declining native (H. convergens), common native (C. maculata), and common exotic 24

41 (H. axyridis) coccinellid species; 2) examine the levels of egg predation occurring across coccinellid foraging habitats; and 3) determine the guild of predators responsible for coccinellid egg predation. Materials and Methods Study sites Lady beetle egg predation was measured within nine counties in 2009 and 2010 throughout Ohio: Delaware (2010 only), Fayette, Huron, Knox, Marion (2009 only), Perry, Putnam, Shelby, and Wayne. Within each county three field sites (soybean, alfalfa, and grassland), were selected as focal coccinellid foraging habitats (Evans 2003, 2004; Ohnesorg 2008), each separated by a minimum of four km. The soybean and alfalfa fields were managed by grower collaborators. The grassland habitats consisted of sites planted by landowners as part of the conservation reserve program (USDA 2011). These grasslands contained cool and warm season grasses, native forbs, and agricultural weeds. Within each site four plots were established where data were collected. All plots were a minimum of 30 m from any field edge. Selection of coccinellid species Egg predation on three lady beetle species was examined: H. convergens, C. maculata, and H. axyridis. Hippodamia convergens is a native species that was once common but is now exceedingly rare in Ohio (Gardiner et al. in press). In 2009 egg 25

42 predation was compared between the common native (C. maculata) and exotic (H. axyridis) lady beetles. In 2010, egg predation of H. convergens, C. maculata and H. axyridis were examined. Coccinellid diversity, relative abundance, and activity density sampling The diversity, relative abundance, and activity density of lady beetles present within soybean, alfalfa, and grassland field sites was determined using yellow sticky card traps and sweep sampling. Unbaited yellow sticky card traps (22.86 x cm unfolded) (Pherocon AM, Trécé, Inc. Adair, OK) were attached to step-in fence posts and placed at a height of 0.5 m at each experimental plot. One seven day catch was collected per plot during the egg predation experiments, which are explained below. Four 20-sweep samples were also collected from the fields during the egg predation experiments (one per plot). Two methods were used to survey for lady beetles because each provides different information about the community of coccinellids present in the fields. Sticky cards assess coccinellid activity by trapping individuals that are moving within or among habitats. Sweep samples provide a measure of the relative abundance and diversity of lady beetles engaged in foraging within the habitat (Stephens & Losey 2004; Schmidt et al. 2008). All counts were averaged across plots for each field. Aphid relative abundance sampling The relative abundance of aphids at the sites was estimated using a m quadrat at each plot. The structure of the vegetation differed in each habitat, so different 26

43 methods were used for estimating relative abundance of aphids. In the grassland habitat all the vegetation within the quadrat was inspected for aphids. In alfalfa five stems within the quadrat were cut over a tray to avoid losing the aphids that fell from the stem when disturbed. The aphids from the five stems were counted. In soybean, five whole plants within the quadrat were inspected for aphids. In addition to the quadrat sampling, aphids were counted from the sweep samples that were collected during each egg predation experiment. All aphid counts were averaged across the plots for each field. Insect rearing and egg collection Coleomegilla maculata and H. axyridis adults were collected from overwintering aggregations in Ohio. Hippodamia convergens adults were ordered from a commercial supplier, which collects from overwintering aggregations in California (Rincon-Vitova, Ventura, CA). Adult females were placed into individual plastic vials (8.9 cm deep; 4.5 cm diameter) lined with white paper to act as an egg-laying substrate. The beetles were provided with water, honey, and Helicoverpa zea egg masses every other day. Previous rearing studies have illustrated that H. convergens and H. axyridis will produce the most egg masses when provided with aphids ad libitum (Wipperfurth et al. 1987; Michaud & Qureshi 2006). These species were provided with pea aphid, Acyrthosiphon pisum Harris (Aphididae), green peach aphid Myzus persicae (Sulzer), and soybean aphid, Aphis glycines Matsumura (Aphididae) from laboratory colonies maintained at OSU-OARDC. Egg masses were successfully gathered from C. maculata when fed only honey and H. 27

44 zea egg masses. Eggs deposited onto the paper substrate were counted and stored in a -80 C freezer until enough egg masses were available to conduct the egg predation experiments ( egg masses per species). Measuring predation of frozen egg masses Due to the large quantity of eggs required for the field experiments, they were frozen to prevent degradation and hatching prior to use. To determine if freezing coccinellid eggs affected predation, Gardiner et al. (2011) compared consumption of previously frozen and live C. maculata eggs by four common generalist predators found in coccinellid foraging habitats: C. septempunctata, H. axyridis, H. parenthesis, and Nabis sp. These predators did not have a preference for live or previously frozen coccinellid eggs. In addition to that study, the consumption of previously frozen and live egg masses by Stylommatophora (slugs), Opiliones (harvestmen), Acrididae (short horned grasshoppers) and Tettigoniidae (long horned grasshoppers) was compared. The predators were placed into individual containers (8 cm deep; 11 cm diameter) and provided either a previously frozen or fresh egg mass of H. axyridis or H. convergens. The containers were checked every 30 minutes for four hours, then again at 24 and 48 hours. The proportion of eggs remaining at each time period was determined. Egg predation experimental procedure Egg predation in grassland, alfalfa, and soybean habitats was measured in 2009 and To distinguish egg predation from other forms of damage or loss (desiccation, 28

45 physical dislodgement, etc.), predator accessible (Open) and caged (Exclusion) treatments were compared. The Exclusion treatment consisted of an egg mass enclosed in a 22 mm diameter mesh cage. The Open treatment consisted of an un-caged egg mass. In 2009 the egg predation experiment was conducted once (week of July 20). During this first experiment, egg predation of C. maculata was measured within all 24 field sites (eight of each focal habitat) and predation of H. axyridis was measured within nine sites (one of each focal habitat within Shelby, Wayne, and Perry Co., OH). In 2010 the experiment was conducted twice (weeks of June 8 and July 26). The late spring (week of June 8) experiment was carried out within the perennial alfalfa and grassland habitats. Soybean plants had either recently emerged or had not yet emerged from the ground within our sites so predation in soybean was not examined. In this experiment egg masses of H. axyridis and H. convergens were deployed in all grassland and alfalfa sites and C. maculata in four replicates of each habitat (alfalfa and grassland sites in Knox, Perry, Putnam, and Shelby Co., OH). During the second 2010 experiment (week of July 26) predation was measured in all three focal habitats. Eggs of H. axyridis and H. convergens were deployed in all 24 sites, and C. maculata egg masses in all but one site (alfalfa, Huron Co., OH). To begin each experiment, egg masses deposited onto 1.5 cm 2 paper squares were counted (the number and species of the egg mass was recorded directly on the paper square) and pinned to the vegetation at a height of meters from the soil surface. Two egg masses from each species were present in each plot; one was assigned to the Open treatment and the other to the Exclusion treatment. All treatments remained in the field for 48 hours, after which the egg masses were collected and the remaining 29

46 eggs counted. It was known that predation occurred by the appearance of the paper and the presence of frass surrounding the area where the egg mass had been. By the presence of predator frass within the cage or a hole in the cage mesh, it was determined that predators were able to gain access to a small number of exclusion cages. Data from infiltrated cages were excluded from analysis. The proportion of egg masses remaining for each treatment/species was averaged across plots for each site. Observation of predation events Video systems were used to monitor coccinellid egg masses in the field. Modified from a design by M. Grieshop (Teixeira et al. 2010), each system consisted of a digital video recorder (DVR: model QH25DVR, QSee, Anaheim, CA, USA) and four weather resistant surveillance cameras each with an infrared light for night vision (model QD28414C4 QSee, Anaheim, CA, USA). The system was powered with a deep cycle boat battery (SLI24MDC Xtreme Deep Cycle Marine and Boat, Hartland, WI, USA). Cameras were fitted with aluminum adaptors (Wayne Machine Shop, Wooster, OH, USA) allowing for the attachment of a 10x magnification lens. The cameras were fastened to metal t-posts at a height of meters. A rain guard of white corrugated plastic (30x17cm) was attached above the camera to protect it from precipitation. Video recording experimental procedure Two DVR systems were placed in the field during each experiment (n = 8 cameras). Two egg masses of H. axyridis and H. convergens which had been laid on 30

47 white paper were observed by each DVR system (n = 4 observations per egg mass species, per field). Egg masses were attached to vegetation which was secured to a corrugated plastic stand (5x5 cm) that was anchored to the ground with 12-gauge wire to prevent the egg mass from moving out of the camera shot. The battery powered the system for a range of hours, after which the video was downloaded from the DVR onto a portable hard drive. A total of 128 egg mass observations (66 H. convergens and 62 H. axyridis) were collected; 37 in alfalfa, 63 in grassland, and 28 in soybean. From this video, we determined which animals damaged or consumed the coccinellid egg masses, and only the first attack on each egg mass was recorded. Given the resolution of the video footage, predators were identified to the following taxonomic resolution: Stylommatophora (slugs), Opiliones (harvestmen), Oniscidea (wood louse), C. maculata (adult), Gryllidae (cricket), Neuroptera (lacewing larva), Tettigoniidae (long horned grasshopper), Acrididae (short horned grasshopper), and Formicidae (ant). Data analysis To determine if the relative abundance and activity density of native and exotic coccinellids collected via yellow sticky card traps and sweep sampling varied across habitats for each sampling period (weeks of: July , June , and July ) a generalized linear model with a negative binomial or Poisson distribution was used depending on which distribution best fit the data (PROC GENMOD; SAS Institute, Inc., 2008). A Poisson distribution was the best fit for the mean exotic lady beetles, and mean H. axyridis on yellow sticky card traps from the July 20, 2009 experiment, and 31

48 mean native lady beetles in sweep samples from the June 8, 2010 experiment. The negative binomial distribution best fit the data in all other cases. The response variables for these analyses were mean exotic, native, or H. axyridis per plot, and the predictor variable was habitat. Significant differences in the relative abundance and activity density of Coccinellids between the habitats were detected when P < To determine if the relative abundance of aphids collected via sweep samples varied across habitats a generalized linear model with a negative binomial distribution was used (PROC GENMOD, SAS Institute, Inc., 2008). The June 8, 2010 and July 26, 2010 experiments were each analyzed separately, with a response variable of mean aphids per plot, and the predictor variable being habitat. Significant differences in the relative abundances of aphids between the habitats were detected when P < A mixed effects repeated measures Analysis of Variance model (ANOVA, PROC MIXED, SAS Institute, Inc., 2008) was used to determine if the predators had a preference for previously frozen or fresh egg masses. The response variable in these models was the proportion of eggs remaining, which was arcsine( x) transformed prior to analysis. Separate analyses were conducted for each predator species examined (Stylommatophora, Opiliones, Acrididae, and Tettigoniidae). Fixed factors were egg treatment (fresh or frozen) and time (0.5, 1, 1.5, 2, 2.5, 3, 3.5, 4, 24, or 48 hours) and the interaction term treatment*time was included. Significant differences in the proportion of eggs remaining between the treatments were detected when P < To determine if egg predation varied among lady beetle species or across habitats a mixed effects ANOVA (PROC MIXED, SAS Institute, Inc., 2008) was conducted for 32

49 each of the three experiments (June 20, 2009, June 8, 2010, and June 26, 2010) with fixed effects: treatment (Exclusion and Open), habitat (soybean, alfalfa, and grassland for the July 20, 2009 and July 26, 2010 experiments; alfalfa and grassland for the June 8, 2010 experiment), and egg species (C. maculata and H. axyridis for the July 20, 2009 experiment; C. maculata, H. axyridis and H. convergens for the June 8, 2010 and July 26, 2010 experiments). All possible interaction terms between the fixed effects were included in the model. To meet the assumptions of ANOVA, the response variable, mean proportion of eggs remaining, from all three experiments were arcsine( x) transformed prior to analysis. The differences in the least squares means was used to search for differences between particular Species*Crop combinations Significant differences in the proportion of eggs remaining between the predictor variables were detected when P < The proportions of first attacks by each predator taxa observed from the video experiments were calculated for each Egg species/ Habitat combination. Pie charts were created so predation patterns among predator taxa could be visualized. Results Measuring predation of previously frozen egg masses There was no difference in consumption of live versus previously frozen eggs for any of the four predators examined (Stylommatophora: F 1,138 = 0.06, P = 0.812, Opiliones: F 1,200 = 0.64, P = 0.427, Acrididae: F 1,120 = 0.70, P = 0.403, Tettigoniidae: 33

50 F 1,89 = 0.85, P = 0.359). For Stylommatophora, Acrididae, and Tettigoniidae, egg predation increased over time (Time effect: Stylommatophora: F 9,138 = 13.48, P < 0.001, Opiliones: F 9,200 = 0.42, P = , Acrididae: F 9,120 = 3.84, P < 0.001, Tettigoniidae: F 9,89 = 2.04, P = 0.044). However, there was not a significant treatment*time interaction for any of the predators examined (Stylommatophora: F 9,138 = 0.35, P = 0.957, Opiliones: F 9,200 = 0.06, P = 1.000, Acrididae: F 9,120 = 0.33, P = 0.965, Tettigoniidae: F 9,89 = 0.17, P = 0.997). Coccinellid activity and relative abundance Exotic coccinellids were detected within all habitats during each of the egg predation experiments (Tables ). Harmonia axyridis was the most common exotic lady beetle, followed by P. quatuordecimpunctata, and C. septempunctata. The exotic H. variegata was rare throughout the study, with only one specimen detected in sweep samples from 2009 (Table 2.4). During the week of July 20, 2009 the activity density of exotic lady beetles collected from yellow sticky card traps varied across habitats (χ 2 = 10.68, d.f. = 2, P = 0.005). Exotic lady beetles showed increased activity density in soybean fields compared to grassland (χ 2 = 8.69, d.f. = 1, P = 0.003), and alfalfa fields (χ 2 = 4.76, d.f. = 1, P = 0.029). There was no difference in exotic coccinellid activity among alfalfa and grassland habitats (χ 2 = 0.80, d.f. = 1, P = 0.371). The activity density of the most common exotic coccinellid measured by yellow sticky cards traps, H. axyridis, also varied among habitats (χ 2 = 9.51, d.f. = 2, P = 0.009). The activity of H. axyridis in soybean was greater 34

51 than in grassland habitats (χ 2 = 7.32, d.f. = 1, P = 0.007), but alfalfa fields did not differ from grassland (χ 2 = 0.98, d.f. = 1, P = 0.323) or soybean (χ 2 = 3.73, d.f. = 1, P = 0.054) fields. During the week of June 8, 2010, the activity density of exotic coccinellids measured by yellow sticky card traps was similar between the alfalfa and grassland fields. However, the activity density of H. axyridis was greater in alfalfa fields than in grasslands (χ 2 = 4.87, d.f. = 1, P = 0.027). During the week of July 26, 2010, the activity density of exotic lady beetles was greater in alfalfa fields than in grassland (χ 2 = 5.20, d.f. = 1, P = 0.022) or soybean (χ 2 = 7.15, d.f. = 1, P = 0.008) fields. There was not a significant difference in the activity density of exotic lady beetles between grassland and soybean fields (χ 2 = 0.18, d.f. = 1, P = 0.671). Harmonia axyridis was more commonly found on yellow sticky card traps in alfalfa fields than soybean (χ 2 = 10.35, d.f. = 1, P = 0.001) and grassland habitats (χ 2 = 13.87, d.f. = 1, P < 0.001). During the weeks of July 20, 2009, and June 8, 2010 the relative abundance of exotic coccinellids found in sweep samples did not differ between the focal habitats. Although exotic lady beetle numbers from sweeps samples during the week of July 26, 2010 did vary across habitats (χ 2 = 22.22, d.f. = 2, P < 0.001). A greater relative abundance of exotic coccinellids were found in sweep samples from alfalfa fields than from soybean (χ 2 = 18.58, d.f. = 1, P < 0.001), or grassland (χ 2 = 18.56, d.f. = 1, P < 0.001) habitats. There were no specimens of H. axyridis recovered from sweep samples during the week of July 20, 2009, and the relative abundance of H. axyridis from sweep 35

52 samples did not vary among habitats during the week of June 8, 2010 (χ 2 = 0.50, d.f. = 1, P = 0.479). There was variation in the relative abundance of H. axyridis in sweep samples during the week of July 26, 2010 (χ 2 = 14.85, df = 1, P < 0.001), where there was a greater relative abundance of H. axyridis individuals in alfalfa fields than soybean fields (χ 2 = 17.67, d.f. = 1, P < 0.001), and there were no specimens of H. axyridis collected via sweep samples from grassland fields. Eight native lady beetle taxa were detected throughout the sampling period, these were: Brachiacantha ursina, C. maculata, Cycloneda munda, Hippodamia glacialis, H. parenthesis, Hyperaspis bigeminata, Psyllobora vigintimaculata, and Scymnus sp. (Tables ). The activity density of native lady beetles measured using yellow sticky card traps did not vary across habitats throughout the study. The relative abundance of native lady beetles collected via sweep samples also did not vary across habitats during the weeks of July 20, 2009, and June 8, 2010, but did vary during the week of July 26, 2010 (χ 2 = 3.85, d.f. = 1, P = 0.050). There were fewer native coccinellids in sweep samples from grassland fields compared to alfalfa (χ 2 = 3.90, d.f. = 1, P = 0.048) fields. A premise for the egg predation experiments was that C. maculata is common and H. convergens is rare. No H. convergens were detected during sampling in 2009 or 2010, and C. maculata was among the most common native lady beetles collected during the egg predation experiments particularly during the week of June 8, 2010 where C. maculata made up 12.0% of total coccinellids collected on sticky cards in grassland, and 24.1% in alfalfa (Table 2.1). From sweep samples in 2009, C. maculata made up 12.5%, 36

53 28.6% and 100% (only one specimen was found) in grassland, alfalfa, and soybean fields respectively (Table 2.4). C. maculata also made up 33.3% of the total coccinellid assemblage in grassland and 13.3% in soybean from the week of July 26, 2010 sweep samples (Table 2.6). Relative Abundance of Aphids Quadrat sampling detected 1.94 ± 1.87 aphids per plot (five stems sampled in each plot) in alfalfa during the week of June 8, 2010 and 7.93 ± 1.58 aphids per plot during the week of July 26, No aphids were detected in the grassland habitats via quadrat sampling during the 2010 sampling periods. A low number of aphids (0.063 ± 0.063) were detected per plot in the soybean habitat during the week of July 26, During the week of June 8, 2010 the relative abundance of aphids was greater in sweep samples from alfalfa sites than from grassland (χ 2 = 30.27, d.f. = 1, P < 0.001) sites, with a mean of ± aphids per sweep sample in alfalfa and no aphids recovered from grassland (Table 2.5). During the July 26, 2010 experiment, alfalfa had a greater relative abundance of aphids than both grassland (χ 2 = 55.71, d.f. = 1, P < 0.001) and soybean (χ 2 = 58.53, d.f. = 1, P < 0.001) habitats, with a mean of ± aphids per sweep sample from alfalfa. Sweep samples from grasslands contained a mean of 0.72 ± 0.37 aphids per sweep sample, and there was a mean of 0.19 ± 0.08 aphids per sweep samples from soybean fields (Table 2.6). 37

54 Egg predation experiments During the week of July 20, 2009 the intensity of egg predation experienced by the common native lady beetle, C. maculata was measured within soybean, alfalfa, and grassland sites in eight counties across Ohio. Within a sub-set of these sites (n = 3 of each habitat), the extent of egg predation among lady beetle species was measured by comparing predation of the native C. maculata with the exotic H. axyridis. Both species experienced a similar pattern of egg predation across foraging habitats, with the greatest predation occurring in grassland habitats and least in alfalfa (Fig. 2.1). Coleomegilla maculata experienced significant egg predation within all habitats, whereas H. axyridis eggs were significantly reduced relative to the caged control in soybean and grassland but not in alfalfa fields (Treatment*Habitat interaction F 2,53 = 4.97, P = 0.011). Coleomegilla maculata egg masses experienced significantly greater predation in grassland (39.7% of eggs remaining), than in soybean (69.4% eggs remaining) (t = 3.22 d.f. = 53 P = 0.002) or alfalfa (82.9% eggs remaining) (t = 4.50 d.f. = 53 P < 0.001) habitats. There was no difference in predation on C. maculata egg masses within soybean and alfalfa (t = d.f. = 53 P = 0.207) fields. The exotic H. axyridis experienced greater egg predation in grasslands (49.2% eggs remaining) than alfalfa fields (93.3% eggs remaining) (t = 2.41 d.f. = 53 P = 0.019), and predation of H. axyridis eggs in soybean and grassland fields was equivalent (t = 1.46 d.f. = 53 P = 0.149). Harmonia axyridis egg masses in soybean and alfalfa incurred low levels of predation (82.5% and 93.3% of eggs were remaining in soybean and alfalfa respectively), with no difference in the number of eggs removed by 38

55 predators (t = d.f. = 53 P = 0.275). The level of predation did not differ among egg species in any of the three habitats (Fig. 2.1). In 2010 egg predation of H. convergens, C. maculata, and H. axyridis was compared. During the week of June 8, 2010 the egg predation experiments were conducted in alfalfa and grassland habitats. All three lady beetle species incurred significant egg predation in both habitats, indicated by fewer eggs remaining in the open treatment compared to the exclusion treatment (F 1,68 = 11.6, P < 0.001). In alfalfa, 39.7% of C. maculata, 45.3% of H. axyridis, and 12.0% of H. convergens eggs remained after 48 h. In grassland 36.7% of C. maculata, 62.5% of H. axyridis, and 28.7% of H. convergens eggs were remaining after exposure to predators. The extent of egg predation that occurred among grassland and alfalfa habitats did not differ for any of the three coccinellid species (F 2,68 = 1.76, P = 0.190). However, there were differences in the extent of egg predation experienced among lady beetle species (F 1,68 = 5.86, P = 0.005). Hippodamia convergens egg masses experienced greater predation than H. axyridis in both alfalfa (t = d.f. = 68 P = 0.016) and grassland (t = d.f. = 68 P = 0.007) habitats. There were no significant differences in the extent of predation experienced by C. maculata and the other two focal species in either of the habitats (Fig. 2.1). During the week of July 26, 2010 the frequency of egg predation was measured for all three focal coccinellid species in alfalfa, grassland and soybean habitats. All species sustained significant egg predation within all habitats. The amount of egg predation detected for each species varied among habitats (Treatment*Habitat interaction, F 2,117 = 4.12, P = 0.019). The native H. convergens experienced significantly greater egg 39

56 predation in soybean (t = d.f. = 117 P = 0.002) and grassland (t = 2.65 d.f. = 117 P = 0.009) than in alfalfa habitats. There was no difference in the extent of egg predation experienced by H. convergens among grassland and soybean habitats (t = d.f. = 117 P = 0.625). Predation of H. axyridis eggs was greater in soybean relative to alfalfa (t = d.f. = 117 P = 0.048). In grassland habitats, an average of 58.7% of H. axyridis eggs remained, which was not significantly different than predation on H. axyridis eggs in soybean (54.0% eggs remaining) or alfalfa (77.5% eggs remaining). Predation on C. maculata egg masses in grassland was significantly higher than in alfalfa (t = 1.99 d.f. = 117 P = 0.049). There was no difference in C. maculata egg predation among soybean and grassland (t = 0.83 d.f. = 117 P = 0.409) or soybean and alfalfa (t = d.f. = 117 P = 0.210) fields. Within foraging habitats differences in the extent of egg predation among species were detected. In soybean fields, H. convergens egg masses sustained significantly greater egg predation than H. axyridis egg masses (t = d.f. = 117 P = 0.040). There was no significant difference between the amount of predation experienced by C. maculata and the other two focal species in soybean. In grassland, significantly fewer C. maculata eggs remained relative to H. axyridis (t = 1.98 d.f. = 117 P = 0.050). There was no significant difference between the amount of predation experienced by H. convergens and the other two focal species in grassland. In alfalfa there were no differences in predation on coccinellid eggs between any of the three focal species (Fig. 2.1). 40

57 Video experiments Of 128 egg masses observed, 21, 41, and 16 predation events occurred in alfalfa, grassland, and soybean fields respectively. A diverse community of organisms attacked lady beetle egg masses (Fig. 2.2). The guild of predators attacking lady beetle eggs varied among the foraging habitats examined. In alfalfa, only Stylommatophora and Opiliones were observed attacking egg masses. Opiliones was the dominant predator responsible for 81.1% and 100% of first attacks on H. convergens, and H. axyridis egg masses respectively. In soybean Opiliones, Tettigoniidae, and Acrididae were responsible for first attacks on lady beetle eggs. Opiliones was also the dominant predator in soybean, responsible for 88.9% of first attacks on H. convergens egg masses and 42.9% of first attacks on H. axyridis egg masses. In grassland the guild of egg predators observed was diverse. Stylommatophora was a dominant egg predator in the grassland habitat, responsible for the first attacks on 27.3% of H. convergens and 26.3% of H. axyridis egg masses that experienced predation. Tettigoniidae was also responsible for 27.3% of first attacks on H. convergens, but not for any first attacks on H. axyridis in grassland. There was only one instance of a lady beetle preying on an egg mass, and this was an adult C. maculata, attacking H. axyridis eggs in a grassland site (Table 2.7, Fig 2.2). Discussion Worldwide, native lady beetle species have declined rapidly in recent decades (Roy, 2012). These declines coincide with the introduction, establishment, and spread of exotic coccinellids (Elliott et al. 1996; Colunga-Garcia & Gage 1998; Alyokhin & Sewell 41

58 2004; Evans 2004; Harmon et al. 2007). Within Ohio (Gardiner et al. in press) and Michigan (Gardiner et al. 2009), the once-common native coccinellid, H. convergens has become exceedingly rare. Many factors could be contributing to the decline of this and other native coccinellids, however much of the research conducted to date has focused on potential direct competitive interactions among native and exotic lady beetles (Cottrell & Yeargan 1998; Cottrell 2004; Snyder et al. 2004; Yasuda et al. 2004; Cottrell 2005). Although these studies have confirmed the propensity of coccinellids, predominately H. axyridis, to act as intraguild predators of native lady beetle eggs and larvae, the extent to which rare lady beetles experience egg predation in the field and the guild of predators which contribute to that predation was not known prior to this study. Reduced predation of H. axyridis relative to native species Our findings supported our prediction that H. convergens sustains a greater amount of egg predation relative to H. axyridis in the field. In both the alfalfa and grassland habitats during the week of June 8, 2010, as well in the soybean habitat during the week of July 26, 2010, fewer H. convergens eggs were remaining than H. axyridis eggs. The only instances in which there was not a significant difference in the amount of egg predation incurred among the two species was in alfalfa and grassland during the week of July 26, Our findings did not support the prediction that H. convergens would experience more egg predation than the common native lady beetle, C. maculata because predation between the two species did not differ. 42

59 Laboratory studies have provided similar findings in terms of the patterns of predation observed across the species (Cottrell 2005, 2007). The presence of defensive alkaloids in or on the eggs could explain those differences. Coccinellid eggs may have surface chemicals which signal the toxicity within preventing predation (Hemptinne et al. 2000). Further studies by Kajita et al. (2010) examined variation in quantities of alkaloids in eggs of H. axyridis and C. septempunctata and found that the amount of alkaloids in an egg can vary significantly within the same species, but is correlated with the size of the eggs. High alkaloid eggs have negative effects on lady beetle larvae, particularly when C. septempunctata is fed high alkaloid H. axyridis eggs. Egg predator guilds Unexpectedly, from the video observations, there was a complete absence of IGP involving exotic coccinellid predators within our study sites despite yellow sticky card trap and sweep sample data indicating that exotic coccinellids were traveling through and foraging within all focal habitats during the egg predation experiments. This provides evidence refuting the prediction would be the dominant predator feeding on lady beetle egg masses. There was a single observation of egg predation by a lady beetle, C. maculata (adult) on H. axyridis eggs. Evidence provided by molecular gut analysis studies show that C. maculata consumes exotic lady beetles (Gagnon et al. 2011). However, molecular gut analysis does not provide information on which life stage (egg, larva, pupa, or adult) 43

60 was consumed, and cannibalism cannot be identified, which is an advantage of using video recordings to study egg predation. A diversity of predators consumed the native and exotic lady beetle egg masses. This guild included Stylommatophora, Opiliones, Oniscidea, C. maculata (adult), Gryllidae, Neuroptera (larvae), Tettigoniidae, Acrididae, Formicidae, and Nabidae. Previous studies have provided evidence that a number of these organisms act as predators of other arthropods. Studies using sentinel prey (Lepidoptera larvae) have provided observations of predation by Opiliones, Formicidae, Gryllus pennsylvanicus (field cricket: Gryllidae) and slugs (Stylommatophora) (Brust et al. 1986; Lundgren et al. 2006). Gut content, and fecal matter analysis of Stylommatophora collected from grasslands and forests found small amounts of arthropod prey such as Acari (mites), Collembola, Lumbricina (earthworm) setae, and fragments of larger insects (Pallant 1969, 1972; Jennings & Barkham 1975). Stylommatophora have also been observed to consume aphids, as well as Lepidoptera eggs in a laboratory setting (Fox & Landis 1973). This is the first known study where Stylommatophora have been observed preying on lady beetle egg masses. Formicidae has been observed attacking lady beetle egg masses previous to this study, and they often reduce the viability of coccinellid eggs by physically damaging the eggs, but are not often observed feeding on the contents (Oliver et al. 2008). During video recordings the ants often appeared to disrupt the egg masses rather than consume them. The ants may have carried out this behavior because they were tending aphids within a close vicinity of the egg mass (Majerus et al. 2007). Ant aggression towards 44

61 adult and larvae coccinellids in the vicinity of the aphid colonies being tended has been reported previously (McLain 1980; Vinson & Scarborough 1989; Sloggett & Majerus 2003). Coccinellids may be less likely to oviposit in areas containing high concentrations of ant semiochemical cues (Oliver et al. 2008), possibly due to the aggression of the ants. There are no known previously documented observations of Opiliones preying on coccinellid egg masses. However, it is well known that Opiliones are generalist predators of a diversity of arthropods within fruit, vegetable, field, and forage cropping systems (Newton & Yeargan 2002). Opiliones feeds on a diversity of insect prey including corn earworm (H. zea), imported cabbageworm (Pieris rapae L.), two-spotted spider mite (Tetranychus urticae Koch), Colorado potato beetle (Leptinotarsa decemlineata Say), and several Aphidoidea species (Ashby & Pottinge 1974; Leathwick & Winterbourn 1984; Butcher et al. 1988; Dixon & McKinlay 1989; Newton & Yeargan 2001). Neuroptera larvae, which were observed attacking both native and exotic lady beetle egg masses in the grassland habitat, have already been observed as intraguild predators of Coccinellids (eggs and larvae) in laboratory studies (Lucas et al. 1998; Phoofolo & Obrycki 1998). Egg predation varies across foraging habitats The egg predation experiments conducted during this study illustrated that predation on both native and exotic lady beetle egg masses varies across habitats where lady beetles are commonly found foraging. In 2009, lady beetles experienced the least egg predation in alfalfa fields and the greatest in grasslands. In 2010, the intensity of egg 45

62 predation detected within habitats varied across the season. In early June (week of June 8) equivalent egg predation was detected in alfalfa fields and grasslands. In late July (week of July 26) results were similar to 2009, where coccinellid eggs in the grassland sites experienced the greatest predation and those in alfalfa experienced the least. Lower rates of predation in alfalfa and a greater amount of predation in the grassland habitats may have been a result of the availability of extraguild prey (aphids). The highest amount of aphid prey was detected in the alfalfa habitat while quadrat sampling failed to detect any aphid prey in grassland habitats during the 2010 egg predation experiments which is also the habitat where the most egg predation occurred, although, the lack of aphids recovered may be due to the clumped distribution that aphids can have in these habitats (Cappuccino 1987; Cappuccino 1988). Other studies have shown that the amount of extraguild prey present can affect IGP among generalist predators such as coccinellids, Syrphidae larvae, and Neuroptera larvae (Lucas et al. 1998; Ingels & De Clercq 2011). There is often a trend of decreasing IGP as the abundance of extraguild prey increases (Yasuda et al. 2004; Nóia et al. 2008; Hautier et al. 2011). Although, sometimes this decrease is only evident when there is an exceptionally high aphid density (Lucas et al. 1998). Implications for coccinellid conservation Exotic coccinellids may not be a dominant predator of lady beetle egg masses, but the greater prevalence of egg predation on the native egg masses compared to the exotic 46

63 egg masses implicates egg predation by the observed guild as a possible mechanism of native lady beetle decline. Low-intensity or ley systems such as semi-natural grasslands, where the most egg predation was observed, often have a diverse assemblage of ground-dwelling predators (Lundgren et al. 2006). These habitats are often considered as valuable habitats for coccinellid conservation since many studies have found an abundance of native coccinellids in grassland habitats (Leather et al. 1999; Evans 2000; Werling et al. 2011). However, these findings could have been influenced by the proximity to agricultural fields which could act as a source of native coccinellids (Rand & Louda 2006). The high extraguild prey levels in agricultural fields such as alfalfa may be important for maintaining some native lady beetle populations. Gardiner et al. (2009) found that lowdiversity landscapes composed of a higher proportion of semi-natural grassland and forage habitats, such as alfalfa fields, provided higher abundances of native lady beetles than soybean fields. This study addresses levels of lady beetle egg predation in crop and non-crop habitats, though it does not address the possibility of IGP among coccinellid larvae which may explain the high levels of IGP detected in molecular gut analysis studies (Gagnon et al. 2011; Hautier et al. 2011). Whether or not egg predation is actually a contributor to native lady beetle decline is also not fully understood, though our findings that native coccinellid eggs experience a greater amount of predation than exotic lady beetle eggs do support that hypothesis. Since there are no known measurements of lady beetle egg predation prior to the establishment of exotic lady beetles in the focal habitats used for 47

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72 Tables July Mean ± SE Percent of total Taxa Grassland Alfalfa Soybean P- value Grassland Alfalfa Soybean H. axyridis 0.19 ± ± ± C. septempunctata 0.19 ± ± ± P. quatuordecimpunctata 0.03 ± ± H. parenthesis 0.03 ± C. maculata ± C. munda 0.13 ± B.ursina 0.41 ± H. glacialis 0.03 ± Native Coccinellids 0.59 ± ± Exotic Coccinellids 0.41 ± ± ± All Coccinellids 1.00 ± ± ± Table 2.1: Coccinellid activity density and diversity. Mean ± SEM and percent of the total coccinellid assemblage from yellow sticky card traps placed in grassland, alfalfa, and soybean habitats during the week of July 20, Yellow sticky card traps remained in the field for seven days. P-values < 0.05 signify variation in the activity density of coccinellids across habitats (Generalized linear model, PROC GENMOD; SAS Institute, Inc., 2008). 56

73 June Mean ± SE Percent of total Taxa Grassland Alfalfa P- value Grassland Alfalfa H. axyridis 0.06 ± ± C. septempunctata ± P. quatuordecimpunctata 0.44 ± ± C. maculata 0.09 ± ± C.munda 0.03 ± ± B. ursina 0.13 ± ± Scymnus sp ± ± Native Coccinellids 0.28 ± ± Exotic Coccinellids 0.50 ± ± All Coccinellids 0.78 ± ± Table 2.2: Coccinellid activity density and diversity. Mean ± SEM and percent of the total adult coccinellid assemblage from yellow sticky card traps placed in grassland and alfalfa habitats during the week of June 8, Yellow sticky card traps remained in the field for seven days. P-values < 0.05 signify variation in the activity density of coccinellids across habitats (Generalized linear model, PROC GENMOD; SAS Institute, Inc., 2008). 57

74 July Mean ± SE Percent of total Taxa Grassland Alfalfa Soybean P- value Grassland Alfalfa Soybean H. axyridis 0.28 ± ± ± C. septempunctata 0.03 ± P. quatuordecimpunctata 0.34 ± ± ± Hippodamia parenthesis ± C. maculata ± C. munda 0.03 ± B. ursina 0.09 ± P. vigintimaculata 0.06 ± ± H. bigeminata ± Scymnus sp ± ± ± H. glacialis ± Native Coccinellids 0.22 ± ± ± Exotic Coccinellids 0.66 ± ± ± All Coccinellids 0.88 ± ± ± Table 2.3: Coccinellid activity density and diversity. Mean ± SEM and percent of the total adult coccinellid assemblage from yellow sticky card traps placed in grassland, alfalfa, and soybean habitats during the week of July 26, Yellow sticky card traps remained in the field for seven days. P-values < 0.05 signify variation in the activity density of coccinellids across habitats (Generalized linear model, PROC GENMOD; SAS Institute, Inc., 2008). 58

75 July Mean ± SE Percent of total Taxa Grassland Alfalfa Soybean P- value Grassland Alfalfa Soybean H. axyridis C. septempunctata 0.04 ± ± H. variegata ± H. parenthesis 0.11 ± ± C. maculata 0.04 ± ± ± C. munda 0.07 ± B. ursina 0.04 ± Total Native Coccinellids 0.25 ± ± ± Total Exotic Coccinellids 0.04 ± ± Total Coccinellids 0.29 ± ± ± Table 2.4: Coccinellid relative abundances and diversity. Mean ± SEM and percentage of the total adult coccinellid assemblage during the week of July 20, 2009 collected via sweep sampling in grassland, alfalfa, and soybean habitats. P-values < 0.05 signify variation in the relative abundance of coccinellids across habitats (Generalized linear model, PROC GENMOD; SAS Institute, Inc., 2008). 59

76 June Mean ± SE Percent of total Taxa Grassland Alfalfa P- value Grassland Alfalfa H. axyridis 0.04 ± ± C. septempunctata ± P. quatuordecimpunctata 0.04 ± ± H. parenthesis 0.04 ± C. maculata ± B.ursina ± Total Native Coccinellids 0.04 ± ± Total Exotic Coccinellids 0.08 ± ± Total Coccinellids 0.13 ± ± Aphids ± < Table 2.5: Coccinellid relative abundances and diversity, and aphid relative abundance. Mean ± SEM of adult coccinellids and aphids, and the percentage of the total adult coccinellid assemblage. Samples were collected via sweep sampling during the week of June 8, 2010 in grassland and alfalfa habitats. P-values < 0.05 signify variation in the relative abundance of coccinellids and aphids across habitats (Generalized linear model, PROC GENMOD; SAS Institute, Inc., 2008). 60

77 July Mean ± SE Percent of total Taxa Grassland Alfalfa Soybean P- value Grassland Alfalfa Soybean H. axyridis ± ± 0.07 < P. quatuordecimpunctata 0.09 ± ± H. parenthesis ± C. maculata 0.06 ± ± Scymnus sp ± Total Native Coccinellids 0.09 ± ± Total Exotic Coccinellids 0.09 ± ± ± 0.07 < Total Coccinellids 0.19 ± ± ± 0.07 < Aphids 0.72 ± ± ± 0.08 < Table 2.6: Coccinellid relative abundances and diversity, and aphid relative abundance. Mean ± SEM of adult coccinellids and aphids, and the percentage of the total adult coccinellid assemblage. Samples were collected via sweep sampling during the week of July in grassland, alfalfa, and soybean habitats. P-values < 0.05 signify variation in the relative abundance of coccinellids and aphids across habitats (Generalized linear model, PROC GENMOD; SAS Institute, Inc., 2008). 61

78 Soybean Alfalfa Grassland Egg mass species: H. convergens H. axyridis H. convergens H. axyridis H. convergens H. axyridis Predator Gastropoda (slugs) Opiliones Oniscidea Tettigoniidae Acrididae C. maculata (adult) Gryllidae Neuroptera (larvae) Formicidae Table 2.7: The percent of first attacks carried out by each predator taxa observed during the video experiments. Attacks are separated by habitat and egg mass species. Soybean, H. convergens: n = 9; Soybean, H. axyridis: n = 7; Alfalfa, H. convergens: n = 10; Alfalfa, H. axyridis: n = 11; Grassland, H. convergens: n = 22; Grassland, H. axyridis: n = 1 62

79 Figures Figure 2.1: The proportion of eggs remaining (mean ± SEM) in the Open treatment after 48 h in the field. Figure A (week of July 20, 2009), compares egg predation of C. maculata and H. axyridis in alfalfa, grassland and soybean habitats. Figure B (week of June 8, 2010) illustrates egg predation of C. maculata, H. axyridis, and H. convergens in alfalfa and grassland. Figure C (week of July 26, 2010) shows egg predation of C. maculata, H. axyridis, and H. convergens in alfalfa, grassland, and soybean habitats. Experiments were analyzed separately (ANOVA, p < 0.05). For each experiment, upper case letters indicate significant difference in egg predation for a given species among crops. Lower case letters note a significant difference in egg predation within a crop for different species. 63

80 Figure 2.2: Pie charts depicting the proportions of first attacks on egg masses carried out by each predator taxa observed during the video experiments, separated by habitat and egg mass species. 78 out of the 128 egg masses observed were attacked. 41 out of 66 H. convergens egg masses and 37 out of 62 H. axyridis egg masses experienced predation. 64

81 Chapter 3: Do the predator guilds attacking coccinellid eggs vary among lady beetle species or across foraging habitats? Abstract The incidence of native lady beetle egg predation may affect the size and distribution of their populations. Recently the amount of egg predation sustained by the increasingly rare native, Hippodamia convergens, and the common exotic, Harmonia axyridis lady beetles was measured. Both species experience a significant amount of egg predation in soybean, alfalfa, and grassland habitats. The objectives of this study were to 1) Measure the relative abundance and activity density of coccinellid egg predators present within grassland, alfalfa and soybean fields across Ohio; 2) Document the contribution of predator species to native and exotic lady beetle egg predation within each foraging habitat; and 3) Determine if the relative abundance of aphids affects the intensity of egg predation experienced by lady beetle egg masses. To address these objectives, video surveillance systems were used to directly observe predation of H. convergens and H. axyridis egg masses in soybean, alfalfa, and grassland habitats in eight counties across Ohio. The relative abundance and activity density of aphids and egg predators was also determined using quadrats, sweep samples, and pitfall traps. From the video observations, the guild of egg predators detected included Stylommatophora, Opiliones, Oniscidea, 65

82 Coccinellidae, Gryllidae, Neuroptera, Tettigoniidae, Acrididae, Formicidae, Nabidae, Thripidae, Syrphidae, Araneae, Staphylinidae, and Diplopoda. This predator guild varied in diversity across the habitats, with the greatest diversity found within grassland habitats. Of these predators observed, it was found that Stylommatophora, Oniscidea, Acrididae, and Formicidae had the highest activity density in grassland, while Araneae, Tettigoniidae, and Gryllidae had the highest relative abundances in grassland. Redundancy analysis revealed two primary egg predators that maintained a constant pattern of predation across both 2010 and 2011: Formicidae and Oniscidea. Formicidae was positively correlated with predation on H. axyridis egg masses, while Oniscidea was positively correlated with predation on H. convergens egg masses. There was no correlation between the relative abundances of aphids and prevalence of coccinellid egg predation. These findings have indicated that exotic lady beetles are not a significant predator of native coccinellid egg masses, but that there is a diverse predator guild. The extent of predation in grasslands and lack of predation in alfalfa signifies that alfalfa may be an important habitat for the conservation of native lady beetles. Introduction Several multi-year censuses have illustrated population declines among native lady beetle species coinciding with the establishment of exotic lady beetles (Wheeler & Hoebeke 1995; Elliott et al. 1996; Colunga-Garcia & Gage 1998; Turnock et al. 2003; Alyokhin & Sewell 2004; Evans 2004; Gardiner et al. 2009; Gardiner et al. 2011). Although many factors may have contributed to native coccinellid decline, several studies 66

83 implicate exotic competitors as the primary cause. For example, Wheeler and Hoebeke (1995) attributed the decline of the once-common nine spotted lady beetle, Coccinella novemnotata, to an increase of the exotic Coccinella septempunctata, in the northeastern United States. Just ten specimens of C. novemnotata have been collected in North America over the last ten years (Losey et al. 2007). A 20-fold reduction in populations of Coccinella transversoguttata and Adalia bipunctata was observed in South Dakota by Elliot et al. (1996), who attributed the declines to the establishment of C. septempunctata in the region. Colunga-Garcia and Gage (1998) reported a decrease in native species, Brachiacantha ursina, Cycloneda munda, and Chilocorus stigma abundance following the establishment of Harmonia axyridis in Michigan. More recently, Gardiner et al. (2009, 2011, and in press) surveyed coccinellids in agricultural, residential, and seminatural habitats throughout Michigan and Ohio and failed to detect the previouslyabundant Hippodamia convergens. To date, the majority of research examining native coccinellid decline has focused on the interference competition via intraguild predation (IGP) hypothesis, proposing that observed population declines among native lady beetles is the result of IGP by exotic coccinellids. This hypothesis is supported by several studies conducted in the lab and field, which have illustrated that exotic lady beetles, primarily H. axyridis and C. septempunctata, have a propensity to act as intraguild predators of native lady beetle eggs and larvae (Cottrell 2004; Snyder et al. 2004; Cottrell 2005, 2007; Sato et al. 2005; Gardiner & Landis 2007). Although exotic coccinellids are known to act as intraguild predators, their contributions to IGP in the field has not been extensively studied, with 67

84 only a few studies measuring the impacts of IGP with varied results. Hoogendoorn and Heimpel (2004) observed that the presence of H. axyridis larvae did not impact the survival or weight gain of Coleomegilla maculata larvae in field cages. Gardiner et al. (2011) found that the common native coccinellid, C. maculata, incurred significant egg predation within soybean fields however, the contribution of exotic lady beetles to that predation was not measured. The results of egg predation experiments presented in Chapter 2 add significantly to these studies, providing supporting evidence for the IGP hypothesis as a mechanism to explain the decline of H. convergens, which experienced greater egg predation compared with the common exotic H. axyridis within crop and semi-natural foraging habitats. Additionally, Chapter 2 indicates that a diversity of arthropods, and not exotic coccinellids, consume native and exotic coccinellid egg masses in soybean, alfalfa, and grassland habitats. The guild observed preying on lady beetle egg masses included Stylommatophora (slug), Opiliones (harvestmen), Oniscidea (wood louse), C. maculata (Pink lady beetle, adult), Gryllidae (cricket), Neuroptera larvae (lacewing), Tettigoniidae (long horned grasshopper), Acrididae (short horned grasshopper), Formicidae (ant), and Nabidae (nabid). This community was first identified using video cameras to observe predation events. The use of video is beneficial to the researcher for multiple reasons chief among these is that a large number of predation events can be observed, facilitating analyses of the influences of many environmental variables on predation intensity and predator guild diversity (Frank et al. 2007, Merfield et al. 2004). In addition, video analysis is typically 68

85 less expensive than using methods such as Enzyme-linked immunosorbent assays (ELISA) to determine predation which also has additional limitations such as difficulty quantifying consumption, and recognizing cannibalism (Naranjo & Hagler 2001; Merfield et al. 2004). Building on the research presented in Chapter 2, the goals of this study were to quantify the predator guild attacking native and exotic coccinellid eggs, to determine if predator contributions to egg predation varied across common coccinellid foraging habitats, and to examine if the relative abundance of a predator or the relative abundance of shared prey influenced lady beetle egg predation. To address these goals, the following objectives were completed: 1) Measure the relative abundance and activity density of coccinellid egg predators present within grasslands, alfalfa and soybean fields across Ohio; 2) Document the contribution of predator species to native and exotic lady beetle egg predation within each foraging habitat; and 3) Determine if the relative abundance of aphids affects the intensity of egg predation experienced by lady beetle egg masses. Materials and Methods Study sites Data was collected within eight counties throughout Ohio: Delaware, Fayette, Huron, Knox, Perry, Putnam, Shelby, and Wayne. Within each county a soybean, alfalfa, and grassland site were selected as focal coccinellid foraging habitats (Evans 2003, 2004; 69

86 Ohnesorg 2008), each separated by a minimum of 4.5 km. Grower-collaborators managed the soybean and alfalfa sites, and the grassland habitats consisted of sites planted by landowners as part of the conservation reserve program (USDA 2011). The grasslands contained cool and warm season grasses, native forbs, and agricultural weeds. Within each site four plots were established where data were collected. All plots were a minimum of 30 m from any field edge. Selection of coccinellid species Eggs from two lady beetle species, H. convergens, and H. axyridis, were used in the coccinellid egg predation experiments and video observations. Adult H. axyridis were collected from overwintering aggregations in Ohio, and H. convergens adults were ordered from commercial suppliers, who collect from of overwintering aggregations in California (Gardeningzone.com, Camarillo, CA). Females were placed into individual plastic vials (8.9 cm deep; 4.5 cm diameter), lined with white paper to act as an egglaying substrate. The beetles were provided with water, honey, and Helicoverpa zea egg masses every other day, and aphids were provided ad libitum, which has been shown to increase egg mass production (Wipperfurth et al. 1987; Michaud & Qureshi 2006). The lady beetles were fed with green peach aphid Myzus persicae (Sulzer) reared on bell pepper, zinnia, and broccoli from a laboratory colony maintained at OSU-OARDC. Eggs deposited onto the paper substrate were counted, moved to Petri dishes, and placed in a -80 C freezer to prevent desiccation or hatching until the experiments were conducted. 70

87 Observation of predation events Video systems, modified from a design by M. Grieshop, Michigan State University (Teixeira et al. 2010), were used to monitor coccinellid egg masses in the field. Each system consisted of a DVR (model QH25DVR, QSee, Anaheim, CA, USA) and four weather resistant surveillance cameras each with an infrared light for night vision (model QD28414C4 QSee, Anaheim, CA, USA). A deep cycle boat battery (SLI24MDC Xtreme Deep Cycle Marine and Boat, Hartland, WI, USA) powered the system. The cameras were fitted with aluminum adaptors (Wayne Machine Shop, Wooster, OH, USA) allowing for the attachment of a 10x magnification lens. In the field, the cameras were fastened to metal t-posts at a height of meters. To protect the cameras from precipitation, a rain guard of white corrugated plastic (30 x 17cm) was attached above the camera. Video recording experimental procedure In 2010 two DVR systems were placed in the field (grassland, alfalfa, or soybean) during each experiment (n = 8 cameras). Two laboratory reared egg masses of H. axyridis and H. convergens were observed by each DVR system (n = 4 observations per egg mass species, per field). Eighteen experiments were conducted between June 8 and August 13, nine in grassland, five in alfalfa, and four in soybean. In 2011, one DVR system was placed in the field during each experiment (n = 4 cameras). Two laboratory reared egg masses from each focal species (H. axyridis and H. convergens) were observed by the DVR system (n = 2 observations per egg mass species per site). The 2011 video 71

88 experiments occurred between June 14 and July 26, and thirty-five experiments were conducted, 16 in grassland, 11 in alfalfa, and eight in soybean. At the start of each experiment, the egg masses were attached to vegetation secured to a corrugated plastic stand (5 x 5 cm) which was anchored to the ground with 12-gauge wire to prevent the egg mass from moving out of the camera view. After 24 hours, the systems were removed from the field, the egg masses were collected, and remaining eggs were counted. The video was downloaded from the DVR onto a portable hard drive. The battery powered the systems for hours, though there were cases where the battery lost power after 5 16 hours. In a majority of these cases, no predation occurred on the egg mass and all the eggs were remaining at the time they were collected from the field. In three cases all the eggs were consumed by predators prior to battery loss, allowing data to be collected from the resulting video. In one case, an egg mass was consumed after the battery had run out, resulting in this observation being excluded from analysis in An additional 29 replicates were excluded from analyses due to vegetation blocking the camera view or adverse weather conditions. In 2010 a total of 128 egg masses were observed (66 H. convergens and 62 H. axyridis); 37 in alfalfa, 63 in grassland, and 28 in soybean. In 2011 there were a total of 118 egg mass observations (59 H. convergens and 59 H. axyridis); 36 in alfalfa, 59 in grassland, and 23 in soybean. From the video, the animals that damaged or consumed the egg masses were determined, and each attack was categorized as a first for secondary attack. First attacks were the first predator (primary predator) to attack each egg mass. Secondary attacks (secondary predator) included every predation event on the egg mass following the first attack. All secondary attacks were analyzed 72

89 separately from the first attacks because those predation events took place after the egg mass had been disturbed. Though some of the secondary predators may have been individuals that had initially attacked the egg mass, and were counted as secondary if they left the screen view and then reappeared since it was not known if it was the same individual or not. The video was not clear enough to distinguish how many eggs were removed during each attack. No-camera egg predation experiments During the 2011 video observation experiments, two additional eggs masses of each focal species, H. axyridis and H. convergens, which did not have cameras focused on them, were placed in the field. The egg masses were attached to vegetation and corrugated plastic stands just as the eggs with the cameras were. After 24 hours of exposure in the field, the eggs were collected and counted. The proportion of eggs remaining was calculated for each egg mass, and those proportions were averaged across the plots in the site for each species. The same calculations were conducted for egg masses with cameras. The eggs without the cameras provided additional data on the prevalence of predation in the focal habitats as well as a control to assure that the presence of the cameras did not affect the amount of predation observed. Relative abundance and activity density of coccinellids and egg predators The relative abundance and activity density of coccinellids and egg predators within the sites was determined using sweep sampling and pitfall trapping. Sweep 73

90 samples can provide an accurate measure of the relative abundance and diversity of canopy dwelling arthropods (Stephens & Losey 2004; Schmidt et al. 2008). Four 20- sweep samples, one per plot, were collected from the fields during each video predation experiment. Coccinellids from these samples were identified to the species level. The following taxa were also counted and identified to family, or in the case of spiders to order: Nabidae, Syrphidae, Gryllidae, Tettigoniidae, Acrididae, and Araneae. Pitfall traps consisted of an 11.4 cm diameter, 14 cm deep plastic deli container (Fabri-Kal Corp, Kalamazoo, MI) sunken into the ground with the lip of the container flush with the soil surface. Two types of pitfall traps were used to sample for predators of lady beetle egg masses. The first type of pitfall trap was with filled with 300 ml of Budweiser beer (Anheuser-Busch, St. Louis, MO) to measure slug (Stylommatophora) activity (Hammond et al. 1996; Voss et al. 1998; Peters et al. 2007). These traps remained in the field for 24 hours during each video experiment. After the Stylommatophora were collected from the traps, the deli containers were rinsed with water in the field and filled with 300 ml of soapy water solution, then placed back in the field to sample for additional ground dwelling arthropods. These pitfall traps remained in the field for seven days after each video experiment. While sorting the pitfall samples organisms were identified to family with the exceptions of harvestmen and spiders, which were identified to order. The following taxa were counted: Tettigoniidae, Gryllidae, Acrididae, Araneae, Opiliones, Oniscidea, and Formicidae. Arthropod counts were averaged across plots for each site. Differences in pitfall trap catches reflect variation in the local density and/or activity of the captured arthropods (Southwood & Henderson 74

91 2000). Therefore, we interpret the trap catches as estimating the activity density of captured taxa, which has become standard in studies employing this sampling method to study similar arthropod taxa (Desender & Maelfait 1986; Lee et al. 2001; Hajek et al. 2007; Gardiner et al. 2010). Relative abundance of aphids The relative abundance of aphids was estimated using a m quadrat within each plot. The method of determining the relative abundance of aphids via the quadrats was modified for each habitat because the structure of the vegetation and distribution of aphids varied across the field types. In the grassland habitat all the vegetation within the quadrat was inspected for aphids since their distribution was often patchy. In alfalfa the distribution of aphids was spread more evenly across the field, and five stems within the quadrat were cut over a tray in order to count the aphids that fell from the stem when disturbed. In soybean, five whole plants within the quadrat were inspected for aphids. The total number of aphids counted per plot was recorded. In addition to the quadrat sampling, aphids were counted from the sweep samples that were collected at the start of egg predation video experiments. All aphid counts were averaged across the plots for each field prior to analysis. Data analysis To determine if the prevalence of egg predation varied among habitats or egg species, an Analysis of Variance model (ANOVA) (PROC MIXED, SAS v ) 75

92 was conducted with fixed effects: treatment (Camera and No camera), habitat (grassland, alfalfa, and soybean), and egg species (H. axyridis and H. convergens). Date of collection was included in the analysis as a random variable. Data was collected from habitats across the season, with sites visited once or twice within a year. The random statement: [visit(county*crop)] was included in the analysis of the egg predation experiments. All possible interaction terms between the fixed effects were used. To meet the assumptions of ANOVA, the response variable, mean proportion of eggs remaining was arcsine( ) transformed prior to analysis. The differences in the least squares means was used to search for differences between particular Species*Crop combinations. Significant differences in the proportion of eggs remaining between Habitats or Egg species were detected at P < To determine if the relative abundance or activity density of coccinellids, aphids and possible egg predators collected via sweep samples and pitfall traps in 2011 varied across habitats, a generalized linear model with a negative binomial distribution was used, except in the case of Araneae (sweep samples) and Oniscidea where a Poisson distribution provided a better fit to the data, was conducted with visit(county*crop) as a random variable (PROC GENMOD, SAS v ). Each taxa as well as the different sampling methods were analyzed separately. For the analysis of each taxa, the response variable was mean number of individuals per sweep sample or pitfall trap, and the predictor variable was habitat. The analyses for native lady beetles, coccinellid larvae, and Gryllidae (sweep samples) were run without the habitat variable soybean, since no specimens of those taxa were recovered from sweep samples collected from the soybean 76

93 habitat. Significant differences in the relative abundances and activity densities of predators between the habitats were detected at P < To determine if the relative abundance of aphids correlated with the occurrence of coccinellid egg predation, a linear regression analyses was conducted with the proportion of eggs remaining (arcsine( ) transformed) as the response variable, and the mean aphids per plot as the predictor variable (Minitab v ). A significant correlation among the relative abundance of aphids and prevalence of egg predation were detected at P < Stepwise multiple regression analysis was used to determine if the relative abundance of egg predators explained the prevalence of egg predation. The proportion of eggs remaining (arcsine( ) transformed) was used as a response variable, and the relative abundances (sweep samples) and activity densities (pitfall traps) of the following egg predators were used a predictor variables: Coccinellid larvae (sweeps), Gryllidae (sweeps and pitfall), Tettigoniidae (sweeps and pitfall), Acrididae (sweeps and pitfall), Opiliones (pitfall), Oniscidea (pitfall), Formicidae (pitfall), and Stylommatophora (pitfall, beer) (SAS v ). All variables left in the model are significant at P < To measure the influence of Habitat and Egg species on the predation events observed throughout the video studies, four separate redundancy analyses (RDA) were performed using multivariate software, PC-ORD 6 (McCune & Mefford 2011). The redundancy analyses examined: First attacks 2010, First attacks 2011, Secondary attacks 2010, and Secondary attacks RDA is a constrained ordination technique that 77

94 combines linear regression and principle components analysis (PCA). It is useful for identifying associations between response and explanatory variables when the data set is multivariate (Makarenkov & Legendre 2002; Chapman et al. 2009; Peck 2010). The explanatory variables, Habitat and Egg species, were assigned dummy variables as RDA requires numerical values. The response variables were the proportions of attacks carried out by each predator taxa sample (per egg species/site/visit combination). Proportions were used because the number of egg masses in which predation was observed on was unequal across sites. Egg masses that did not experience predation were removed from the analyses, and egg predators were excluded from analyses when they were present in fewer than three samples. To visualize the trends from the RDA, the response and explanatory variables were plotted on biplots, where proximity indicates the degree of association (Chapman et al. 2009). The different predator taxa, represented by vectors, pointing in the direction of an explanatory variable (Habitat or Egg species), indicate an association between that taxa and the explanatory variable. A positive correlation is shown as a taxa vector roughly pointing in the direction of the explanatory variable(s) that it is associated with. A negative correlation is indicted by a vector pointing away from an explanatory variable. Perpendicular arrows indicate that here is no correlation. The lengths of the taxa vectors indicate the strength of the association. Three randomization tests (999 permutations), which provided P-values, were performed to check the validity of: (1) the linear relationship between the response and explanatory matrices, (2) the first PCA axis, and (3) the association between the first and second set of sample unit ordination scores. 78

95 Low P-values from these three tests indicate that there is a high level of confidence in the predictions which are based on constraining the response data by the chosen explanatory variables (Peck 2010). Results Egg predation experiments The intensity of egg predation experienced by the rare native lady beetle, H. convergens, and the common exotic lady beetle, H. axyridis was measured in both 2010 and 2011 within soybean, alfalfa, and grassland habitats. Results of the 2010 experiment are detailed in Chapter 2. In 2011, there was no difference in predation of H. convergens and H. axyridis egg masses (t = d.f. = 96 P = 0.080) within soybean fields. In the alfalfa fields, H. convergens experienced greater egg predation than H. axyridis (t = d.f. = 96 P = 0.001). Predation also varied across species in the grassland habitat with H. convergens experiencing greater egg predation than H. axyridis (t = d.f. = 96 P < 0.001). Across habitats, H. convergens experienced greater egg predation in grassland than soybean (t = 3.40 d.f. = 55.7 P = 0.001) or alfalfa (t = 3.41 d.f. = 55.7 P = 0.001) habitats; predation did not differ among soybean and alfalfa (t = 0.29 d.f. = 55.7 P = 0.774). Harmonia axyridis egg masses also had a significantly lesser proportion of eggs remaining in grassland compared to the soybean (t = 2.10 d.f. = 55.7 P = 0.040) or alfalfa (t = 3.08 d.f. = 55.7 P = 0.003) habitats. There was no difference in predation on H. axyridis egg masses between the soybean and alfalfa habitats (t = d.f. = 55.7 P = 79

96 0.527) (Fig 3.1). The presence or absence of the video cameras did not affect the mean proportion of eggs remaining (F 1,96 = 1.09 P = 0.299). Coccinellid relative abundance Exotic coccinellids were detected within all focal habitats. Four exotic coccinellid species were found, H. axyridis, C. septempunctata, Hippodamia variegata, and Propylea quatuordecimpunctata. The most abundant exotic lady beetle was P. quatuordecimpunctata, followed by H. axyridis, H. variegata, and C. septempunctata. Native coccinellids were detected in alfalfa and grassland habitats, but not in soybean. Six native lady beetles species were collected, Hippodamia parenthesis, C. maculata, Cycloneda munda, Brachiacantha ursina, Hyperaspis undulata, Psyllobora vigintimaculata, and one additional genus, Scymnus spp. The most abundant native species was C. maculata, followed by H. parenthesis (all specimens were from a single grassland site/visit: Putnam), and Scymnus spp. Cycloneda munda, B. ursina, and H. undulata were rare. Lady beetle larvae were recovered from alfalfa and grassland habitats, but not soybean fields (Table 3.1). The relative abundance of exotic lady beetles did not vary across habitats (F 2,32 = 0.83, P = 0.446). Native lady beetle relative abundance did not differ among the alfalfa and grassland habitats (F 1,25 = 3.38, P = 0.074), and no native lady beetles were recovered from the soybean habitat. Coccinellid larvae relative abundance also did not vary among the alfalfa and grassland habitats (F 1,25 = 2.16, P = 0.154), and no lady beetle larvae were recovered from the soybean sites. 80

97 Relative abundance of aphids Quadrat sampling detected 3.38 ± 2.72 aphids per plot in grassland, 0.94 ± 0.39 aphids per plot in alfalfa, and 0.31 ± 0.31 aphids per plot in the soybean sites. There were 1.86 ± 0.85 aphids per sweep sample in grassland sites, ± 8.23 aphids per sweep sample in alfalfa sites, and 0.13 ± 0.05 aphids per sweep sampling in soybean sites (Table 3.2). The relative abundance of aphids via sweep samples varied across habitats. A greater relative abundance of aphids were in alfalfa than in grassland (t = 5.13, d.f. = 32, P < 0.001) and soybean habitats (t = 5.68, d.f. = 32, P < 0.001). Aphids also had a greater relative abundance in grasslands than soybean fields (t = 2.16, d.f. = 32, P = 0.039). Aphid relative abundance and prevalence of egg predation There was no correlation between the relative abundance of aphids collected in sweep samples and the proportion of coccinellid eggs removed by predators (P = 0.127, R 2 = 0.069). Composition of egg predator guilds Of 128 egg masses observed in 2010, 16, 21, and 41 predation events occurred in soybean, alfalfa, and grassland fields respectively. In 2011, 118 egg masses were observed with, five, 11, and 49 egg masses experiencing predation in soybean, alfalfa, and grassland fields respectively. 81

98 The predators that were observed attacking lady beetle egg masses during the video observation studies in 2010 and 2011 were: Stylommatophora, Opiliones, Oniscidea, C. maculata (adult and larva), H. axyridis (larva), Coccinellid larva (unknown species), Gryllidae, Neuroptera (larva), Tettigoniidae, Acrididae, Formicidae, Nabidae, Unknown Coleoptera, Thripidae, Syrphidae (larva), Diptera (unknown family), Araneae, Staphylinidae, Diplopoda, and an unidentified arthropod taxa. The predator guilds varied among the foraging habitats between the two years. During the 2010 video experiments, Stylommatophora and Opiliones were observed as primary predators on egg masses in alfalfa. Opiliones was the dominant predator responsible for 81.1% and 100% of first attacks on H. convergens, and H. axyridis egg masses respectively. First attacks on egg masses in soybean fields were carried out by Opiliones, Tettigoniidae, and Acrididae. Of these three predators, Opiliones was dominant, being responsible for 88.9% of first attacks on H. convergens egg masses and 42.9% of first attacks on H. axyridis egg masses in soybean. The most diverse guild of primary predators was observed in grassland, and included Stylommatophora, Opiliones, Oniscidea, Tettigoniidae, Acrididae, C. maculata, Gryllidae, Neuroptera, and Formicidae. The dominant primary predator was Stylommatophora, which was responsible for 27.3% and 26.3% of first attacks on H. convergens and H. axyridis respectively. Tettigoniidae carried out 27.3% of the first attacks on H. convergens egg masses but was not observed as a primary predator on H. axyridis egg masses (Fig. 3.2). In 2011 primary predation of coccinellid egg masses in alfalfa was carried out by Syrphidae larvae, C. maculata larvae, and Thripidae. The dominant predator of H. 82

99 convergens and H. axyridis egg masses was C. maculata larvae (50.0% and 60.0% of primary attacks respectively). All of the first attacks in soybean were carried out by Tettigoniidae. Similar to 2010, the guild of primary predators was most diverse in the grassland habitat and included Stylommatophora, Opiliones, Oniscidea, Tettigoniidae, Acrididae, C. maculata (adult), Coccinellidae larvae (unknown species), Gryllidae, Formicidae, Syrphidae (larvae), Araneae, and an unidentified Coleoptera. The dominant primary predator of H. convergens egg masses in grassland was Tettigoniidae (30.8% of first attacks). The dominant primary predator on H. axyridis egg masses in the grassland habitat was Formicidae (32.0% of first attacks) (Fig 3.3). In 2010 secondary predators of coccinellid egg masses in alfalfa included Stylommatophora, Opiliones, and Nabidae. The dominant secondary predator was Opiliones which was responsible for 64.7% of secondary attacks on H. convergens and 94.1% of secondary attacks on H. axyridis. The taxa observed as secondary predators in soybean included Opiliones, Tettigoniidae, Acrididae, Gryllidae, and one unidentified arthropod (video footage did not have the resolution needed for identification). The dominant secondary predator in soybean was Opiliones which was responsible for 90.9% and 44.4% of secondary attacks on H. convergens and H. axyridis egg masses respectively. The taxa that were responsible for secondary attacks in the grassland habitat included Stylommatophora, Opiliones, Oniscidea, Tettigoniidae, C. maculata (adult), Gryllidae, Neuroptera (larvae), and Formicidae. The dominant predators of the H. convergens egg masses were Stylommatophora (26.3% of secondary attacks), Tettigoniidae (21.1% of secondary attacks), and Neuroptera (larvae) (21.1% of secondary 83

100 attacks). The dominant secondary predator of the H. axyridis egg masses in the grassland habitat was Opiliones which was responsible for 31.8% of secondary attacks (Fig 3.4). During the 2011 video experiments secondary attacks on coccinellid egg masses in alfalfa were carried out by Opiliones, C. maculata (larvae), H. axyridis (larvae), Syrphidae (larvae), Thripidae, and Diptera of an unknown family. The dominant predator of H. convergens egg masses in alfalfa was C. maculata larvae (60.0% of secondary attacks), and on H. axyridis egg masses in alfalfa 33.3% of secondary attacks were carried out by Thripidae, while H. axyridis (larvae) and Syrphidae (larvae) each carried out 22.2% of the secondary attacks. The taxa that were responsible for secondary attacks in the grassland habitat included: Stylommatophora, Opiliones, Oniscidea, Tettigoniidae, C. maculata (adult), Gryllidae, Formicidae, Syrphidae (larvae), Staphylinidae, Diplopoda, and Nabidae. The dominant predator on the egg masses was Formicidae which was responsible for 35.7% and 37.5% of secondary attacks on H. convergens and H. axyridis egg masses respectively. There were no secondary attacks in the soybean habitats in 2011, where in three out of the five cases the first attackers consumed the entire egg masses, and in the other two cases no other predators attacked the egg masses (Fig. 3.5). In 2010, observations of lady beetles as first attackers were limited to 5.3% of the total first attacks (one attack) on H. axyridis egg masses in the grassland habitat. In 2011 the proportion of coccinellids as primary predators of the egg masses increased. In alfalfa C. maculata larvae was responsible for a total of six attacks (50.0% and 60.0% of attacks on H. convergens and H. axyridis egg masses respectively) In the grassland habitat, one 84

101 first attack of an H. axyridis egg mass (4.0%) was carried out by a C. maculata adult, and another attack (4.0%) was carried out by a coccinellid larva (species unknown) (figs 3.2 and 3.3). During the 2010 video experiments, C. maculata (adult) was responsible for three (13.6%) secondary attacks on H. axyridis egg masses in the grassland habitat. No additional egg predation by lady beetles was detected. During the 2011 video experiments C. maculata larvae were responsible for three (60%) and one (11.1%) of secondary attacks in alfalfa of H. convergens and H. axyridis egg masses respectively. Two attacks by H. axyridis larvae on H. axyridis egg masses made up 33.3% of the total secondary attacks on H. axyridis egg masses in the alfalfa habitat. In the grassland habitat, adult C. maculata was responsible for one (1.8%) secondary attack on H. axyridis egg masses (figs 3.4 and 3.5) Egg predator activity density and relative abundance The relative abundance and activity density of 2010 egg predators was measured within each habitat in The activity density of Stylommatophora was greater in grassland than in alfalfa (t = d.f. = 32, P = 0.008) but not different from the soybean sites (t = 2.00 d.f. = 32, P = 0.054). There was no difference in the activity density of Stylommatophora between soybean and alfalfa habitats (t = d.f. = 32, P = 0.552) (Fig. 3.6 B). The activity density of Tettigoniidae measured using pitfall traps did not vary across the focal habitats (Fig. 3.6 B). Tettigoniidae relative abundance collected via sweep samples did vary across habitats. Their relative abundance was greater in grassland 85

102 fields than in alfalfa (t = -2.32, d.f. = 32, P = 0.027) and soybean fields (t = 2.06, d.f. = 32, P = 0.048). The relative abundance of Tettigoniidae did not differ between alfalfa and soybean fields (t = -0.04, d.f. = 32, P = 0.964) (Fig. 3.7). Acrididae had a greater activity density in grassland than alfalfa fields (t = -2.23, d.f. = 32, P = 0.033), and the activity density of Acrididae did not differ between soybean and alfalfa (t = -0.42, d.f. = 32, P = 0.677) or grassland (t = 1.59, d.f. = 32, P = 0.122) (Fig. 3.6 B). The relative abundance of Acrididae found via sweep sampling varied across habitats, where fewer individuals were collected in soybean than in both the alfalfa (t = 2.21, d.f. = 32, P = 0.034) and grassland habitats (t = 2.71, d.f. = 32, P = 0.011). There was no difference in the relative abundance of Acrididae between the alfalfa and grassland fields (t = -0.43, d.f. = 32, P = 0.668) (Fig. 3.7). Fewer Gryllidae were recovered from pitfall traps from alfalfa than grassland fields (t = -2.54, d.f. = 32, P = 0.016). There was also no difference in the activity density of Gryllidae between soybean and alfalfa (t = -1.54, d.f. = 32, P = 0.133) or grassland habitats (t = 0.67, d.f. = 32, P = 0.507). (Fig. 3.6 A). Through sweep sampling, the relative abundance of Gryllidae in grassland was greater than in alfalfa habitats (t = -3.89, d.f. = 24, P = 0.001), and there were no Gryllidae recovered from the soybean sites through sweep sampling (Fig 3.7).The activity density of Araneae in grasslands was reduced compared to alfalfa habitats (t = 3.02, d.f. = 32, P = 0.005) (Fig. 3.6 A). There was no difference in the activity density of Araneae between the soybean and alfalfa (t = 0.88, d.f. = 32, P = 0.387) or grassland habitats (t = -1.79, d.f. = 32, P = 0.082). The relative abundance of Araneae via sweep sampling was higher in grassland than in alfalfa (t = -3.68, d.f. = 32, P = 0.001) and soybean habitats (t = 5.22, d.f. = 32, P < 0.001). The 86

103 relative abundance of Araneae was also higher in the alfalfa than in the soybean sites (t = 2.04, d.f. = 32, P = 0.050) (Fig. 3.7). The activity density of Opiliones did not vary across habitats (F 2,32 = 1.21, P = 0.311) via pitfall traps (Fig. 3.6 B). Oniscidea had a higher activity density in the grassland habitats than both soybean (t = 3.85, d.f. = 32, P = 0.001) and alfalfa habitats (t = -4.13, d.f. = 32, P < 0.001). There was no difference in the activity density of Oniscidea between soybean and alfalfa fields (t = 0.10, d.f. = 32, P = 0.921) (Fig. 3.6 A). There were fewer Formicidae in pitfall traps from soybean fields than from alfalfa (t = 3.25, d.f. = 32, P = 0.003) or grassland fields (t = -2.21, d.f. = 32, P = 0.035). The activity density of Formicidae was also greater in grassland than in the alfalfa sites (t = 3.25, d.f. = 32, P = 0.003) (Fig. 3.6 A). Nabidae relative abundance, sampled through sweep samples varied across habitats, there was a greater number of individuals in sweep samples from alfalfa than from soybean (t = 2.39, d.f. = 32, P < 0.023) or grassland habitats (t = 2.34, d.f. = 32, P = 0.026). There was no difference in the relative abundance of Nabidae between the grassland and soybean sites (t = 0.70, d.f. = 32, P = 0.492) (Fig. 3.7). A lesser relative abundance of Syrphidae were collected via sweep sampling from soybean fields than from grassland (t = 2.46, d.f. = 32, P = 0.019) and alfalfa fields (t = 2.34, d.f. = 32, P = 0.025). There was no difference in the relative abundance of syrphidae recovered from alfalfa and grassland fields (t = -0.02, d.f. = 32, P = 0.986) (Fig. 3.7). 87

104 Egg predator activity density and relative abundance, and prevalence of egg predation The stepwise regression showed that together, Formicidae activity density, and Tettigoniidae relative abundance explained 30.0% of the total egg predation variance (Table 3.3). Redundancy analysis of egg predator activity RDA revealed varied patterns of associations among egg predators and the explanatory variables, Habitat and Egg Species, across the two year study (2010 and 2011). The Habitat and Egg Species axes in each biplot explained between % of the total variance of predation events by differing taxa. Significant P-values, < 0.05, listed in the biplot figure legends (Figs. 3.8, 3.9, 3.10, 3.11) indicate that there is a strong confidence in the predictions for the associations shown. In 2010 (Fig. 3.8), examination of primary predation events indicates that attacks by Formicidae and Acrididae have a strong positive association with H. axyridis egg masses and a negative association with H. convergens egg masses. Predation of coccinellid egg masses by Tettigoniidae and Oniscidea have a strong positive association with H. convergens egg masses and a negative association with H. axyridis egg masses. Predation of coccinellid egg masses by Opiliones shows a strong positive correlation with the soybean and alfalfa habitats, and a negative correlation with the grassland habitat. Coccinellid egg predation by Neuroptera larvae and Stylommatophora responded positively to grassland, though the shorter vectors indicate a weak association. 88

105 Primary predation within 2011 showed some similarities to the primary predation measured in 2010 (Fig.3.9). Predation by Formicidae was again positively correlated with H. axyridis egg masses and Oniscidea had a strong positive association with H. convergens egg masses. A weak association of Tettigoniidae with H. convergens was found. The remaining associations observed in 2011 differed from Predation by Opiliones shows a strong positive correlation with H. convergens egg masses in the grassland habitat and a negative correlation with H. axyridis egg masses in alfalfa and soybean habitats. Predation on coccinellid egg masses by Gryllidae also has a positive association with H. convergens egg masses in grasslands, but the association is weaker. Predation by Stylommatophora on coccinellid egg masses has a strong positive correlation with H. axyridis egg masses and a negative association with H. convergens egg masses. Coccinellid egg predation by Tettigoniidae, C. maculata larvae, and Thripidae were positively associated with the alfalfa habitat and negatively associated with the grassland habitat. The 2010 biplot for secondary predator attacks (Fig 3.10) indicates that Oniscidea was highly correlated with H. axyridis eggs in grassland habitats and negatively correlated with H. convergens egg masses in alfalfa and soybean habitats. Predation by Tettigoniidae and Neuroptera on coccinellid egg masses showed a similar, but weaker association to that of Oniscidea. Predation by Stylommatophora appeared to be highly associated with H. convergens egg masses in alfalfa, and predation by Opiliones was positively correlated with soybean and alfalfa habitats and negatively correlated with grassland habitats. Predation on coccinellid egg masses by Gryllidae showed a weak 89

106 positive correlation in the direction of H. axyridis egg masses as well as towards the soybean habitat. The biplot for secondary attacks in 2011 (Fig. 3.11) only includes the alfalfa and grassland habitats, because there were no observations of secondary attacks on coccinellid egg masses in soybean during the 2011 video experiments. The P-values from the randomization tests were not significant (P > 0.05) meaning that there is not a strong confidence in the predictions that are described. Predation by Syrphidae larvae on coccinellid egg masses was positively correlated with the alfalfa habitat and negatively correlated with the grassland habitat. Coccinellid egg predation by Opiliones appears have a strong positive correlation with H. axyridis egg masses and a negative correlation with H. convergens egg masses. Predation by Formicidae on coccinellid egg masses was weakly positively correlated with H. axyridis egg masses in the grassland habitat. Predation on coccinellid egg masses by Gryllidae appears to also be weakly positively associated with the grassland habitat. Coccinellid egg predation by Tettigoniidae and Oniscidea were highly positively correlated with H. convergens egg masses in the grassland habitat. Discussion Native lady beetle decline in North America coincides with the establishment and spread of exotic coccinellid species. Based on those observations, the hypothesis stating that exotic coccinellids are responsible for the decline via IGP has been tested and supported by a number of laboratory studies (Cottrell 2004, 2007, Cottrell & Yeargan 90

107 1998). Open-field egg predation experiments carried out in grassland, alfalfa, and soybean fields found that the rare native lady beetle, H. convergens, tends to experience a greater rate of egg predation then the common exotic, H. axyridis (Chapter 2). During those experiments, early in the season, (week of June ) H. convergens experienced greater egg predation than H. axyridis in both the alfalfa and grassland habitats. Additionally, in late summer (July ) H. convergens egg masses incurred greater egg predation than H. axyridis egg masses in soybean habitats (Chapter 2). In 2011 H. convergens egg masses experienced greater egg predation than H. axyridis egg masses in grassland and alfalfa habitats. The enhanced predation on H. convergens egg masses supports predation on egg masses as a mechanism to explain native lady beetle decline. The role of exotic coccinellids as intraguild egg predators Several studies have documented the propensity of exotic coccinellids to act as intraguild predators of native coccinellids in the laboratory (Cottrell & Yeargan 1998; Cottrell 2004, 2007). In addition, Gagnon et al. (2011) detected native coccinellid DNA within the gut contents of field-collected H. axyridis indicating that this predator does attack native coccienllids under open field conditions. However, interference competition among coccinellids was not responsible for the majority of the egg predation events observed during the experiments conducted for this study. Using video observation, this study found that of the 145 primary predatory attacks observed, 0% and 6.2% were due to exotic and native lady beetles respectively. These included three attacks on native and six attacks of exotic egg masses. Of the

108 secondary predation events observed, 1.0% and 4.1% were due to exotic and native lady beetles respectively. These included three attacks on native and seven attacks on exotic egg masses. No coccinellids were observed attacking egg masses in the soybean habitats. In alfalfa, of the 32 primary predation events observed, 18.8% were carried out by native Coccinellidae and 0% by exotic lady beetles. Three attacks occurred on each, H. convergens and H. axyridis egg masses. In the grassland habitat, of the 92 primary predation events, 3.3% were carried out by native coccinellids and 0% by exotics. All three attacks occurred on H. axyridis egg masses. In alfalfa, of the 48 secondary predation events, 8.3% were by native lady beetles, and 4.2% were by exotic lady beetles. These included three attacks on each of the native and exotic species. These findings suggest that exotic coccinellids may not have a high impact on native coccinellid egg masses refuting the hypothesis that exotic coccinellids are responsible for native lady beetle decline via IGP on egg masses. Hoogendoorn and Heimpel (2004) also suggest that intraguild interactions among coccinellids in the field may have lesser impacts on native populations than predicted by laboratory studies. They found that there were no significant negative effects on the survivability or weight gain of C. maculata when caged on a corn plant along with H. axyridis compared to when C. maculata was placed on a caged corn plant without H. axyridis. Lady beetle egg predator guild The guild of predators observed preying on lady beetle egg masses was diverse and clearly varied across habitats. The most diverse egg predator guild was observed in 92

109 the grassland habitat, with 14 primary predators and 13 secondary predators consuming lady beetle eggs. In alfalfa six primary predators and eight secondary predators were observed. In soybean just three primary predators and five secondary predators were observed. The relative abundance and activity densities of the egg predators most commonly observed preying on egg masses differed among coccinellid foraging habitats. However, the prediction that the abundance and activity levels of egg predators would be associated with the amount of egg predation held true for only two of the egg predator taxa: Formicidae and Tettigoniidae. The activity density of Formicidae and relative abundance of Tettigoniidae were strongly positively correlated with the extent of coccinellid egg predation measured in This study provides the first evidence of Tettigoniidae as a predator of lady beetle egg masses. Tettigoniidae has not been reported as a predator of arthropod egg masses frequently, but has been reported to feed on egg masses the green hairy caterpillar (Rivula atimeta), a pest of rice (Vandenberg, 1992). Formicidae has been reported to attack and reduce the viability of coccinellid eggs (Oliver et al. 2008), which may be a behavior carried out to protect tended aphid colonies (Majerus et al. 2007). Burgio et al. (2008) found ants to be common within cages where predation had occurred on coccinellid egg masses of either H. axyridis or A. bipunctata, which lead the authors to conclude that ants may be important coccinellid egg predators. Aphid tending ants have also been observed to respond aggressively to the presence of adult H. axyridis without physical contact. Although, in the same study the ants were not observed attacking H. 93

110 axyridis larvae unless they came into physical contact with them and attacks on H. axyridis eggs was not examined (Herbert & Horn 2008). Preferences of predators for native or exotic lady beetle eggs Formicidae and Oniscidea were the only egg predator taxa that exhibited consistent preferences as primary predators for H. convergens or H. axyridis eggs across 2010 and This finding provides inconclusive evidence for the hypothesis that a preference among generalist predators for native over exotic coccinellid eggs is contributing to a decline in native lady beetle populations. Formicidae attacks were positively associated with H. axyridis egg masses, and Formicidae was responsible for twice as many H. axyridis attacks than attacks on H. convergens eggs. While, Oniscidea was positively associated with H. convergens egg predation. The only known report of an Isopod (such as Oniscidea) attacking arthropod eggs was reported by Merfield et al. (2004) who observed isopoda consuming blow fly eggs in a video observation study. A preference for a particular egg mass species may be a result of alkaloids present within the eggs. Coccinellids produce species-specific alkaloids (King and Meinwald 1996), and Kajita et al. (2010) tested the effect of alkaloids from H. axyridis eggs on first instar C. septempunctata and found that C. septempunctata dies within three days while being fed H. axyridis alkaloids. The same study also reported that there is a positive linear relationship between egg weight and the amount of alkaloid present. Though, studies investigating the effect of coccinellid alkaloids on generalist predators other than those within the family Coccinellidae are lacking. There is also evidence that Coccinellid eggs 94

111 have surface chemicals which signal the toxicity within, possibly preventing predation (Hemptinne et al. 2000). There were also significant relationships between predator activity and foraging habitat. Predation by Formicidae and Oniscidea was associated with the grassland habitats, and these two predator taxa both had higher activity densities in the grassland habitats than in both the alfalfa and soybean habitats. Therefore, the possibility of egg attack by these generalist predators is likely a function of their density. Beyond Formicidae and Oniscidea, the activity of taxa as predators of H. axyridis verses H. convergens egg masses were not consistent across 2010 and This is not altogether surprising as egg predation by omnivorous arthropods such as Gryllidae, Opiliones, and Stylommatophora are likely influenced by several factors such as temperature, moisture, vegetation structure, and the composition of the habitats bordering the fields. There are no known studies providing observations of Gryllidae, Acrididae, Opiliones, or Stylommatophora attacking coccinellid egg masses. However, some of the egg predators have been observed preying on other arthropods. Brust et al. (1986) used Lepidoptera larvae as sentinel prey to study the guild of predators in corn cropping systems. Among the predators observed attacking tethered lepidopterous larvae were Formicidae and Deroceras laeve (Stylommatophora). Lundgren et al. (2006) conducted fields observations of Lepidoptera larvae in multiple cropping-systems with varied levels of management and input intensities, these included: vegetable (high intensity), cash grain (intermediate intensity), and hay/pasture (low intensity). They found that Opiliones, 95

112 Gryllus pennsylvanicus (Gryllidae) and Slugs (Stylommatophora) acted as predators of the larvae, though they did not mention which were most common in the particular cropping systems. It has been well documented that Opiliones acts as a predator of a diversity of arthropods such as early instar imported cabbageworm (Pieris rapae) (Ashby & Pottinge 1974), eggs and early instar larvae of Colorado potato beetle (Leptinotarsa decemlineata) (Drummond et al. 1990), the two-spotted spider mite (Tetranychus urticae Koch) (Butcher et al. 1988) and, aphids (Leathwick & Winterbourn 1984; Dixon & McKinlay 1989). There is evidence that Stylommatophora can act as a predator of small arthropods, such as, Acari, Collembola, earthworms, various larger insects (Pallant 1969, 1972; Jennings & Barkham 1975), aphids, and Lepidoptera eggs (Fox & Landis 1973). As noted above, some of the egg predators have been observed preying on aphids, meaning that they have shared prey with coccinellids, and predation on coccinellids egg masses by these predators would be a form of IGP. Extraguild prey relative abundance and egg predation Previous studies have shown that IGP interactions can be affected by the abundance of extraguild prey (Lucas et al. 1998; Yasuda et al. 2004; Nóia et al. 2008; Hautier et al. 2011; Ingels & De Clercq 2011). However, the relative abundance of aphids, a prey item for some of the predators collected, was not correlated with the proportion of eggs remaining as had been predicted. The differences in the amount of predation observed across the three habitats may have more to do with the guild of predators within the field than the presence of extraguild prey. There also may have been 96

113 other important prey items or resources lacking from the fields where high levels of predation on coccinellid egg masses was detected. The movement of the predators though the fields would also impact predation as well. If alternative prey was lacking, more stationary arthropods may prey on lady beetle egg masses even if they are not a preferable food item. Implications of findings for coccinellid conservation This study illustrates that coccinellid egg predation is common and a diversity of predators contribute. It is clear that exotic coccinellids are not dominant predators of coccinellid egg masses refuting the hypothesis that predation on native lady beetle eggs by exotic coccinellids is a driving factor for native lady beetle decline. Though the placement of the egg masses within canopy during the experiments may have influenced particular predators and caused them to be observed preying on the egg masses more often. The differences in predation on the rare native, H. convergens egg masses and the common exotic, H. axyridis egg masses provides evidence that egg predation by the observed guild of predators may be an important factor for native lady beetle decline. The patterns of predation observed by the biplots may have been driven by a number of variables other than Egg species and Habitat, such as weather, structure of the surrounding vegetation, and the presence and density of extraguild prey as well as other resources. The landscape surrounding the fields and the habitats bordering the fields could also be an important source for the coccinellid egg predators and may be able to 97

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118 Lundgren J.G., Shaw J.T., Zaborski E.R. & Eastman C.E. (2006). The influence of organic transition systems on beneficial ground-dwelling arthropods and predation of insects and weed seeds. Renew. Agr. Food Syst., 21, Majerus M.E.N., Sloggett J.J., Godeau J.F. & Hemptinne J.L. (2007). Interactions between ants and aphidophagous and coccidophagous ladybirds. Population Ecology, 49, Makarenkov V. & Legendre P. (2002). Nonlinear redundancy analysis and canonical correspondence analysis based on polynomial regression. Ecology, 83, McCune B. & Mefford M.J. (2011). PC-ORD. Multivariate Analysis of Ecological Data. Version 6. In. MjM Software Gleneden Beach, Oregon, U.S.A. Merfield C.N., Wratten S.D. & Navntoft S. (2004). Video analysis of predation by polyphagous invertebrate predators in the laboratory and field. Biological Control, 29, Michaud J.P. & Qureshi J.A. (2006). Reproductive diapause in Hippodamia convergens (Coleoptera : Coccinellidae) and its life history consequences. Biological Control, 39, Minitab Inc. (2010). Mini Tab 16 Statistical Software. Sate College, PA: Minitab, Inc. Naranjo S.E. & Hagler J.R. (2001). Toward the quantification of predation with predator gut immunoassays: A new approach integrating functional response behavior. Biological Control, 20, Nóia M., Borges I. & Soares A.O. (2008). Intraguild predation between the aphidophagous ladybird beetles Harmonia axyridis and Coccinella undecimpunctata (Coleoptera: Coccinellidae): The role of intra and extraguild prey densities. Biological Control, 46, Ohnesorg W.J. (2008). Non-target effects of soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), management in Iowa. In: Entomology. Iowa State University Ames, Iowa. Oliver T.H., Jones I., Cook J.M. & Leather S.R. (2008). Avoidance responses of an aphidophagous ladybird, Adalia bipunctata, to aphid-tending ants. Ecological Entomology, 33,

119 Pallant D. (1969). The food of grey field slug (Agriolimax reticulatus (Müller)) in woodland. J. Anim. Ecol., 38, Pallant D. (1972). The Food of the Grey Field Slug, Agriolimax reticulatus (Müller), on Grassland. J. Anim. Ecol., 41, Peck P.E. (2010). Multivariate Analysis for Community Ecologists: Step-by-step guide using PC-ORD., Gleneden Beach, OR. Peters H.A., Hsu G., Cleland E.E., Chiariello N.R., Mooney H.A. & Field C.B. (2007). Responses of temporal distribution of gastropods to individual and combined effects of elevated CO 2 and N deposition in annual grassland. Acta Oecologica, 31, SAS Institute Inc. (2008). SAS 9.2 Procedures Guide. Cary, NC: SAS Institute Inc. Sato S., Yasuda H. & Evans E.W. (2005). Dropping behaviour of larvae of aphidophagous ladybirds and its effects on incidence of intraguild predation: interactions between the intraguild prey, Adalia bipunctata (L.) and Coccinella septempunctata (L.), and the intraguild predator, Harmonia axyridis Pallas. Ecological Entomology, 30, Schmidt N.P., O'Neal M.E. & Dixon P.M. (2008). Aphidophagous predators in Iowa soybean: A community comparison across multiple years and sampling methods. Annals of the Entomological Society of America, 101, Snyder W.E., Clevenger G.M. & Eigenbrode S.D. (2004). Intraguild predation and successful invasion by introduced ladybird beetles. Oecologia, 140, Southwood R. & Henderson P.A. (1978). Ecological Methods, London. Stephens E.J. & Losey J.E. (2004). Comparison of sticky cards, visual and sweep sampling of Coccinellid populations in alfalfa. Environmental Entomology, 33, Teixeira L., Grieshop M. & Gut L. (2010). Effect of pheromone dispenser density on timing and duration of approaches by peachtree borer. Journal of Chemical Ecology, 36, Turnock W., Wise I. & Matheson F. (2003). Abundance of some native coccinellids (Coleoptera: Coccinellidae) before and after the appearance of Coccinella septempunctata. The Canadian Entomologist, 135, USDA (2011). Conservation Reserve Program. URL 103

120 Voss M.C., Hoppe H.H. & Ulber B. (1998). Estimation of slug activity and slug abundance. Journal of Plant Diseases and Protection, 105, Wheeler A.G. & Hoebeke E.R. (1995). Coccinella novemnotata in northeastern North America - historical occurrence and current status (Coleoptera, Coccinellidae). Proceedings of the Entomological Society of Washington, 97, Wipperfurth T., Hagen K.S. & Mittler T.E. (1987). Egg production by the Coccinellid Hippodamia convergens fed on two morphs of the green peach aphid, Myzus persicae. Entomologia Experimentalis Et Applicata, 44, Yasuda H., Evans E.W., Kajita Y., Urakawa K. & Takizawa T. (2004). Asymmetric larval interactions between introduced and indigenous ladybirds in North America. Oecologia, 141,

121 Tables Taxa Mean ± SE Percentage of total Grassland Alfalfa Soybean Grassland Alfalfa Soybean H. axyridis 0.03 ± ± ± C. septempunctata 0.02 ± ± H. variegata 0.02 ± ± ± P. quatuordecimpunctata 0.13 ± ± ± H. parenthesis 0.38 ± ± C. maculata 0.08 ± ± C. munda 0.02 ± ± B. ursina 0.02 ± ± H. undulata 0.02 ± P. vigintimaculata ± Scymnus sp ± ± Total Native Coccinellids 0.53 ± ± Total Exotic Coccinellids 0.19 ± ± ± Total Coccinellids 0.72 ± ± ± Larvae 0.53 ± ± Table 3.1: Means ± SEM and percentage of the total coccinellid assemblage collected via sweep sampling on the days video systems were set up in the fields. 105

122 Sampling method Mean ± SE Grassland Alfalfa Soybean Sweep sampling 1.86 ± ± ± 0.05 Quadrat sampling 3.38 ± ± ± 0.31 Table 3.2: Aphid means ± SEM collected via 0.25m 2 quadrat and sweep sampling on the days video systems were set up in the fields 106

123 Predator (measurement) C(p) F-value P- value R-sq Total R-sq 1. Formicidae (activity density) Tettigoniidae (abundance) Table: 3.3: Variables included in the model from the stepwise regression analysis. Together these two variables explain 30.0% of the observed varience in the proportion of egg remaining. 107

124 Figures Figure 3.1: The proportion of eggs remaining (mean ± SEM) after 24 h exposure in the field. Figure depicts comparison of predation of H. convergens and H. axyridis in soybean, alfalfa, and grassland habitats. Data were analyzed with ANOVA, P < Upper case letters indicate significant difference in egg predation for a given species among crops. Lower case letters note a significant difference in egg predation within a crop for different species. 108

125 Figure 3.2: Pie charts, First attacks The frequency of first attacks on H. convergens and H. axyridis egg masses by the predators observed with video recordings in soybean, alfalfa, and grassland habitats. 109

126 Figure 3.3: Pie charts, 2011 first attacks. The frequency of first attacks on H. convergens and H. axyridis egg masses by the predators observed with video recordings in soybean, alfalfa, and grassland habitats. 110

127 Figure 3.4: Pie charts, 2010 secondary attacks. The frequency of secondary attacks on H. convergens and H. axyridis egg masses by the predators observed with video recordings in soybean, alfalfa, and grassland habitats. 111

128 Figure: 3.5: Pie charts, 2011 secondary attacks. The frequency of secondary attacks on H. convergens and H. axyridis egg masses by the predators observed with video recordings in soybean, alfalfa, and grassland habitats. There were no second attacks in soybean during the 2011 sampling periods. 112

129 Figure 3.6: Mean relative abundance ± SE of the egg predators collected from pitfall traps. Stylommatophora was sampled with Beer pitfall traps that remained in the field for 24 hours. The remaining taxa were sampled with pitfall traps (filled with soapy water) which remained in the field for seven days. Differences among habitats were measured with a generalized linear model, P <

130 Figure 3.7: Mean relative abundance ± SE of the egg predators collected from sweep samples in the samples were collected on the day the video systems were set up in the fields. Differences among habitats were measured with a generalized linear model, P <

131 Figure 3.8: Biplot, 2010 first attacks: Redundancy analysis biplot depicting associations between predators of coccinellid egg masses (vectors), and habitat (open circles) and egg species (closed circles). Randomization test results: (1) Overall relationship between predictor and response matrices, Ho: no linear relationship between matrices P = (2) Eigenvalues for individual axes P = (3) Correlation between fitted scores and scores in response variable space P =

132 Figure 3.9: Biplot, 2011 First attacks. Redundancy analysis biplot depicting associations between predators of coccinellid egg masses (vectors) and habitat (open circles) and egg species (closed circles). Randomization test results: (1) Overall relationship between predictor and response matrices, Ho: no linear relationship between matrices P = (2) Eigenvalues for individual axes P = (3) Correlation between fitted scores and scores in response variable space P =

133 Figure 3.10: Biplot, 2010 Secondary attacks. Redundancy analysis biplot depicting associations between predators of coccinellid egg masses (vectors) and habitat (open circles) and egg species (closed circles). Randomization test results: (1) Overall relationship between predictor and response matrices, Ho: no linear relationship between matrices P = (2) Eigenvalues for individual axes P = (3) Correlation between fitted scores and scores in response variable space P =

134 Figure 3.11: Biplot, 2011 secondary attacks. Redundancy analysis biplot depicting associations between predators of coccinellid egg masses (vectors) and habitat (open circles) and egg species (closed circles). Randomization test results: (1) Overall relationship between predictor and response matrices, Ho: no linear relationship between matrices P = (2) Eigenvalues for individual axes P = (3) Correlation between fitted scores and scores in response variable space P =

135 Chapter 4: Conclusions and synthesis The drastic decrease of some native coccinellid populations has coincided with the establishment and spread of a number of exotic lady beetle species (Elliott et al. 1996; Colunga-Garcia & Gage 1998; Alyokhin & Sewell 2004; Evans 2004; Harmon et al. 2007). Several hypotheses have been proposed that implicate exotic coccinellids as a cause of the observed declines. The central hypothesis for native lady beetle decline tested through this research was the interference competition via intraguild predation (IGP) hypothesis. This hypothesis states that native lady beetles are in decline because the adults and larvae of exotic coccinellids are preying on the larvae and eggs of native coccinellids (Koch 2003; Cottrell 2005). Two types of experiments to test this central hypothesis were conducted during this study. The egg predation experiments conducted in Chapter 2 quantified the amount of predation that occurs on native and exotic lady beetle egg masses in the field. The prediction tested by the egg predation experiments was that egg masses of the rare H. convergens would experience significantly greater egg predation than the exotic H. axyridis. Based on the results of the egg predation experiments detailed in Chapter 2, the next step was to examine the guild of predators that attack lady beetle egg masses by conducting the video observation experiments. It 119

136 was predicted that exotic coccinellids would be among the dominant predators of lady beetle egg masses. Since egg masses from the native species, H. convergens, experienced greater predation than the eggs from the exotic species, H. axyridis. The experiments provided evidence that egg predation could be responsible for the decline of native lady beetle populations. However, the prediction, based off previous laboratory studies (Cottrell & Yeargan 1998; Cottrell 2005, 2007), that coccinellids are responsible for the majority of predation occurring on the lady beetle egg masses was refuted though the video observation experiments. The results of video experiments, outlined in Chapter 3, revealed an unexpected and diverse guild of predators, many of which had not been previously documented attacking lady beetle egg masses. The occurrence of exotic coccinellids consuming lady beetle egg masses in the three habitats tested (grassland, alfalfa, and soybean) was rare. Exotic lady beetles were not observed attacking native or exotic lady beetle eggs during the first set of video experiments (2010, Chapter 2). During the second year (2011, Chapter 3), just two attacks by exotic coccinellids (H. axyridis larvae) occurred, and these predation events took place on H. axyridis eggs, so they were acts of cannibalism. Although the prediction that exotic lady beetles function as dominant predators of coccinellid egg masses was refuted, H. convergens experienced greater egg predation than H. axyridis. Therefore it is possible that egg predation is playing a role in the decline of this native coccinellid. The organisms within the guild of predators observed from the videos, rather than exotic lady beetles, may be responsible for the declines. Further 120

137 studies are necessary to determine if these predators are influencing the populations of native lady beetles. Other factors could affect the predation of native lady beetle egg masses such as, the alteration to the surrounding landscape, particularly field edges. A previous study has shown that the habitat along the edge of a field affects the amount of predation on coccinellid egg masses within that field. Sites surrounded by semi-natural habitats experience greater egg predation than fields surrounded by other croplands (Gardiner et al. 2011). Other environmental conditions may be affecting the composition of predators present within the field sites as well, which in turn could affect the amount of predation occurring on lady beetle egg masses. Habitat is also plays an important role in lady beetle egg predation. Based on the differences in predation of egg masses across the three foraging habitats tested, the location a lady beetle oviposits within is important. The highest diversity of egg predators was observed in the grassland sites where the highest amount of egg predation also occurred. The lowest level of predation on lady beetle egg masses occurred in alfalfa where not only the predator guild observed was less diverse, but the density of extraguild prey (aphids) was highest. The occurrence of predation on lady beetle egg masses could be affected by both the structure of the surrounding habitat and the presence of extraguild prey. The importance of the habitat structure has been investigated in a prior study where interactions between intraguild predators, H. axyridis and Episyrphus balteatus (Syrphidae), were observed in different arenas. The researchers found that incidences of IGP differed between small Petri dish arenas, and larger more complex potted plant 121

138 arenas (Ingels & De Clercq 2011). More complex habitats may contain refuges that could provide hiding places for intraguild prey, though the refuges would not be of much use for coccinellid egg masses since they cannot move. The presence of extraguild prey has been verified as a factor that affects IGP interactions (Lucas et al. 1998; Cottrell 2005; Nóia et al. 2008; Hautier et al. 2011; Ingels & De Clercq 2011). The listed studies deal mainly with lady beetle IGP interactions, though it is possible that the findings may apply to other arthropod predators as well. Based off of the results of this study, alfalfa could be an important source habitat for native lady beetle populations since their eggs may be less likely to be predated on, and there is often an abundance of extraguild prey available. This research also brought to light the incredible complexity of IGP interactions that can occur in the field. The observations of multiple predators feeding on the same egg mass would be difficult to recreate in laboratory conditions. In addition to having the opportunity to observe primary and secondary attacks on lady beetle egg masses, there were other complex IGP interactions. The events shown in Figure 4.1 illustrate interactions between three different egg predators. The events began with a C. maculata larva attacking a H. axyridis egg mass (Fig. 4.1a). After a period of about five hours, during which the larva had spent feeding on the egg mass and remaining within a close proximity while not feeding, a Syrphidae larva appeared and soon attacked the lady beetle larva (Fig. 4.1b). As the Syrphidae larva continued to feed on the C. maculata larvae an Opiliones approached, took the C. maculata larva, and began to feed on it (Fig. 4.1c). Eventually the Opiliones left the screen shot leaving behind the carcass of the C. maculata larva, which is visible to the right of the egg mass (Fig 4.1d). During these 122

139 events, only 17 of the 33 eggs were removed from the egg mass. The multiple interactions between the predators may have prevented the entire egg mass from being consumed. While this is the most complex sequence of IGP interactions that was observed while reviewing the video, it provides a clear example of a complicated interaction between the egg predators. These interactions may also add sources of error to DNA and alkaloid analyses of predators to detect their prey (Aebi et al. 2011; Gagnon et al. 2011; Hautier et al. 2011). For example, in the case of the syrphid fly larva, since it preyed on a C. maculata larva that had recently preyed on a H. axyridis egg mass, then it would appear that the syrphid fly larvae consumed two coccinellid species when it actually consumed only one. The next critical steps following this research should include further studies on the newly observed egg predators to determine if the patterns of predation hold true. More research on the presence of aphids in the field and the occurrence of intraguild predation would help further the understanding of the effects of extraguild prey on IGP. In addition to these steps, further studies on IGP in alfalfa fields would be beneficial as well. The findings of this study imply that alfalfa may be an important habitat for the conservation of native coccinellids, and an important question to ask may be: why are native coccinellids not currently found in greater abundances in these seemingly important habitats? The decline of multiple native lady beetle species has alarmed scientists and conservationists. The role of coccinellids as generalist predators makes them important for ecosystem function and the control of agricultural pests. This increased knowledge of predation on coccinellid egg masses in semi-natural and 123

140 agricultural habitats will contribute to the future conservation efforts of native coccinellid populations. References Aebi A., Brown P.M.J., De Clercq P., Hautier L., Howe A., Ingels B., Ravn H.P., Sloggett J.J., Zindel R. & Thomas A. (2011). Detecting arthropod intraguild predation in the field. BioControl, 56, Alyokhin A. & Sewell G. (2004). Changes in a lady beetle community following the establishment of three alien species. Biological Invasions, 6, Colunga-Garcia M. & Gage S.H. (1998). Arrival, extablishment, and habitat use of the multicolored Asian lady beetle (Coleoptera: Coccinellidae) in a Michigan landscape. Environmental Entomology, 27, Cottrell T.E. (2005). Predation and cannibalism of lady beetle eggs by adult lady beetles. Biological Control, 34, Cottrell T.E. (2007). Predation by adult and larval lady beetles (Coleoptera : Coccinellidae) on initial contact with lady beetle eggs. Environmental Entomology, 36, Cottrell T.E. & Yeargan K.V. (1998). Intraguild predation between an introduced lady beetle, Harmonia axyridis (Coleoptera : Coccinellidae), and a native lady beetle, Coleomegilla maculata (Coleoptera : Coccinellidae). Journal of the Kansas Entomological Society, 71, Elliott N., Kieckhefer R. & Kauffman W. (1996). Effects of an invading coccinellid on native coccinellids in an agricultural landscape. Oecologia, 105, Evans E.W. (2004). Habitat displacement of North American ladybirds by an introduced species. Ecology, 85, Gagnon A., Heimpel G.E. & Brodeur J. (2011). The ubiquity of intraguild predation among predatory arthropods. PLoS One, 6, e Gardiner M.M., O'Neal M.E. & Landis D.A. (2011). Intraguild predation and native lady beetle decline. PLoS One, 6, e

141 Harmon J.P., Stephens E. & Losey J. (2007). The decline of native coccinellids (Coleoptera : Coccinellidae) in the United States and Canada. Journal of Insect Conservation, 11, Hautier L., Martin G.S., Callier P., de Biseau J.C. & Gregoire J.C. (2011). Alkaloids provide evidence of intraguild predation on native coccinellids by Harmonia axyridis in the field. Biological Invasions, 13, Ingels B. & De Clercq P. (2011). Effect of size, extraguild prey and habitat complexity on intraguild interactions: a case study with the invasive ladybird Harmonia axyridis and the hoverfly Episyrphus balteatus. BioControl, 56, Koch R.L. (2003). The multicolored lady beetle, Harmonia axyridis: A review of its biology, uses in biological control, and non-target impacts. Journal of Insect Science, 3, Lucas E., Coderre D. & Brodeur J. (1998). Intraguild predation among aphid predators: characterization and influence of extraguild prey density. Ecology, 79, Nóia M., Borges I. & Soares A.O. (2008). Intraguild predation between the aphidophagous ladybird beetles Harmonia axyridis and Coccinella undecimpunctata (Coleoptera: Coccinellidae): The role of intra and extraguild prey densities. BioControl, 46,

142 Figure Figure 4.1: Screen shots from a sequence of IGP events occurring at the same egg mass (H. axyridis) in an alfalfa field during the 2011 video experiments. (a) A C. maculata larva can be seen consuming a H. axyridis egg mass. (b) A Syrphidae larva attacks the C. maculata larva. (c) An Opiliones takes the C. maculata larva away from the Syrphidae larva and appears to feed. (d) The Opiliones leaves the screen shot and the carcass of the C. maculata larva is visible directly below the uppermost pushpin visible in the screenshot. 126

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