Examining Breeding Bird Diets to Improve Avian

Home , Abacion, Abacionidae, Bahama oriole, Bridled titmouse, Eastern bluebird, Eastern towhee

EXAMINING BREEDING BIRD DIETS TO IMPROVE AVIAN

CONSERVATION EFFORTS

Ashley C. Kennedy

A dissertation submitted to the Faculty of the University of Delaware in partial fulfillment of the requirements for the degree of Doctor of Philosophy in Entomology and Wildlife Ecology

Summer 2019

EXAMINING BREEDING BIRD DIETS TO IMPROVE AVIAN

CONSERVATION EFFORTS

Ashley C. Kennedy

Approved: ______Jacob L. Bowman, Ph.D. Chair of the Department of Entomology and Wildlife Ecology

Approved: ______Mark W. Rieger, Ph.D. Dean of the College of Agriculture and Natural Resources

Approved: ______Douglas J. Doren, Ph.D. Interim Vice Provost for Graduate and Professional Education and Dean of the Graduate College

I certify that I have read this dissertation and that in my opinion it meets the academic and professional standard required by the University as a dissertation for the degree of Doctor of Philosophy.

Signed: ______Douglas W. Tallamy, Ph.D. Professor in charge of dissertation

Signed: ______Charles R. Bartlett, Ph.D. Member of dissertation committee

Signed: ______Jeffrey J. Buler, Ph.D. Member of dissertation committee

Signed: ______Ian Stewart, Ph.D. Member of dissertation committee

ACKNOWLEDGMENTS

First and foremost, I would like to thank Daniel Hildreth, whose generosity made this project possible. I thank my advisor, Doug Tallamy, whose guidance was invaluable to me in every aspect of this project. I am also indebted to my graduate committee members, Charles Bartlett, Jeff Buler, and Ian Stewart, for their support and expertise. Additionally, my colleagues Desiree Narango and Adam Mitchell provided vital collaboration and counsel that greatly expedited my progress on this project.

I am indebted to Kevin McGraw for conducting carotenoid analyses and to

Tyler Hagerty, Adam Mitchell, Douglas Tallamy, and Kimberley Shropshire for collecting specimens. I am grateful to Nate Shampine and the Mt. Cuba Natural Lands team for allowing me to conduct field work at a beautiful site, to Justin Bredlau and

Jessica Bray for helping me to create an award-winning video on this research, and to

Mike Vella and Frontier Scientific for supplying thousands of caterpillars. I thank

Charles Bartlett, Anthony Deczynski, Derek Hennen, Matt Bertone, Hal White, Adam

Mitchell, and others who helped identify countless arthropods from photos and Patrick

Carney, Emily Baisden, and Ian Stewart for identifying birds. I am indebted to Lee

Coats for his enduring support and patience while I prioritized this project above all else.

I would especially like to thank the veritable army of community scientists, over twelve hundred strong, who supplied me with photos of birds eating insects. This project would not have been possible without their talent as photographers and willingness to share their beautiful photos.

This research was made possible through the University of Delaware

Department of Entomology and Wildlife Ecology and the University of Delaware

Graduate and Professional Education Summer Doctoral Fellowship.

DEDICATION

To my husband, Lee Coats, who works tirelessly to make the world a better place for birds and bugs.

TABLE OF CONTENTS

LIST OF TABLES ...... ix LIST OF FIGURES ...... x ABSTRACT ...... xi

Chapter

1 DIET OF EASTERN BLUEBIRDS IN DELAWARE ...... 1

1.1 Introduction ...... 1 1.2 Background Information ...... 3 1.3 Objectives ...... 14 1.4 Materials and Methods ...... 14 1.5 Results ...... 18 1.6 Discussion ...... 25 1.7 Conclusions ...... 34

2 ASSESSMENT OF EASTERN BLUEBIRD PREY PREFERENCES ...... 36

2.1 Introduction ...... 36 2.2 Materials and Methods ...... 37 2.3 Results ...... 40 2.4 Discussion ...... 42

3 NORTH AMERICAN BREEDING BIRD FOOD WEBS ...... 45

3.1 Introduction ...... 45 3.2 Materials and Methods ...... 46 3.3 Results ...... 49 3.4 Discussion ...... 66

4 ANALYSIS OF CAROTENOID CONTENT IN ARTHROPODS ...... 72

4.1 Introduction ...... 72 4.2 Materials and Methods ...... 78 4.3 Results ...... 79 4.4 Discussion ...... 83

CONCLUSIONS ...... 86

REFERENCES ...... 88

vii

Appendix

A PAIRED STIMULUS PREFERENCE ASSESSMENT RESULTS ...... 107 B BIRD SPECIES INCLUDED IN THE “WHAT DO BIRDS EAT?” COMMUNITY SCIENCE PHOTO DATABASE ...... 116 C CAROTENOID LEVELS IN INVERTEBRATE TAXA ...... 125

viii

LIST OF TABLES

Table 1 Contingency table of frequencies of different taxa of Eastern Bluebird prey (annual variation), with percent contributions to chi-square ...... 24

Table 2 Contingency table of frequencies of different taxa of Eastern Bluebird prey (seasonal variation), with percent contributions to chi-square ...... 25

Table 3 Composition of arthropod taxa in North American breeding bird diets, based on crowd-sourced photos from community scientists ...... 63

Table 4 Contingency table of frequencies of different taxa of Eastern Bluebird prey (crowd-sourced photos versus camera trap data), with percent contributions to chi-square ...... 65

LIST OF FIGURES

Figure 1 GoPro camera stationed at Eastern Bluebird nest box ...... 17

Figure 2 Paired Stimulus Preference Assessment example. Male bluebird selecting his first choice of 12 prey items (6 waxworms and 6 cabbage loopers) ...... 39

Figure 3 Composition of arthropod taxa in North American breeding bird diets, based on crowd-sourced photos from community scientists. Arthropod orders listed phylogenetically...... 57

Figure 4 Regions of United States and Canada used for geographic comparisons ...... 58

Figure 5 Arthropods in breeding Eastern Bluebird diet ...... 65

Figure 6 Total carotenoid content in examined arthropod taxa; letters denote groups that are similar based on post-hoc comparisons ...... 80

Figure 7 Invertebrate prey prevalence in breeding bird diets compared to total carotenoid content ...... 82

ABSTRACT

Improving our understanding of birds' diets is vital to avian conservation efforts. Once we know which arthropod groups are most important to birds and why, we will be better prepared to manage landscapes to facilitate bird conservation by planting the host plants those arthropods need for their survival and reproduction. Four projects were conducted to investigate the arthropod composition of bird diets. Over three breeding seasons, cameras were stationed at Eastern Bluebird (Sialia sialis) nest boxes in Delaware to record photographs of bluebirds bringing food to their nestlings.

Thirty-eight bluebird broods were monitored from hatching until fledging; identification of over 7,000 arthropod prey from photos taken at the nests indicate that the most common prey taxa are Lepidoptera, Orthoptera, and Araneae. Prey choice tests using 24 bluebird pairs were then conducted to assess bluebirds’ insect prey preferences, indicating that waxworm caterpillars are preferred over mealworms, crickets, cabbage looper caterpillars, and stink bugs. Additionally, a community science project was launched to solicit contributions of photos of North American birds eating arthropod prey. Approximately 6,500 photos of bird-arthropod interactions, representing about 320 North American bird species, were contributed by community scientists and the arthropod prey were identified to lowest possible taxonomic level. Having determined which arthropod groups are the best-represented and most preferred in birds' diets, the next step was to identify what makes those groups important to birds. Levels of carotenoids (lutein, zeaxanthin, beta-

cryptoxanthin, beta-carotene, and alpha-carotene) were quantified and compared across insect groups. Carotenoids play an important role in boosting the immune system, promoting healthy development, and in determining birds' plumage coloration, important in mate selection. Carotenoid analyses revealed that caterpillars

(Lepidoptera) have higher levels of carotenoids than other examined invertebrate groups (Hemiptera, Coleoptera, Hymenoptera: Apocrita, and Araneae). Birds' preferences for certain arthropod groups could be influenced by carotenoid content.

The results of this research suggest that managing landscapes in ways that promote the abundance of green, hairless caterpillars (e.g., Geometridae and Noctuidae) should improve resources required by breeding North American birds.

xii

Chapter 1

DIET OF EASTERN BLUEBIRDS IN DELAWARE

1.1 Introduction More than one-third (432 species) of all bird species that breed in North

America are currently at risk of extinction (North American Bird Conservation

Initiative 2016). Even many species generally considered “common” are showing an unprecedented decline in numbers. The major driver of this decline is believed to be habitat loss and degradation, although outdoor cats and collisions with windows, cell towers, motor vehicles, and power lines play a role as well (North American Bird

Conservation Initiative 2014). Evidence is mounting, however, that access to adequate nutrition is an important and oft-overlooked factor in bird conservation. Numerous recent studies (e.g., Sánchez-Bayo and Wyckhuys 2019, van Strien et al. 2019) suggest that arthropods, a major food resource for birds, are undergoing a sharp decline, and that such declines can reduce breeding bird success (Narango et al. 2018).

Two recent studies in Europe (Gregory et al. 2014, Hallmann et al. 2017) indicate that widespread pesticide use is partly to blame for birds’ declines, as it reduces insect populations that birds need for food. Fitzgerald et al. (2014) suggest that prey availability limits northern Chimney Swift (Chaetura pelagica) populations.

English et al.’s (2018) results from stable isotope analyses of museum specimens of

Eastern Whip-poor-wills (Caprimulgus vociferus) further support the hypothesis that

insectivorous bird populations are declining due to declining availability of prey. Their study found that nitrogen isotope ratios declined in whip-poor-will tissues over 130 years, while they remained relatively stable in insect tissues, indicating that the birds increasingly fed on lower trophic-level prey as higher trophic-level insects declined.

A potential avenue for improving avian conservation efforts is to enhance existing bird habitat by encouraging the growth, survival, and reproduction of the arthropod species on which birds rely for food. Insects and spiders serve as an essential food source for the vast majority of passerine birds, particularly while breeding (Peterson 1980). The volume of insects consumed by birds each year is considerable. Nyffeler et al. (2018) estimate that globally birds consume 400-500 million metric tons of insects each year. Even birds that are described as primarily feeding on seeds and fruits rely on insect protein during the breeding season and will change their foraging patterns dramatically during that time (Judd 1901). Although this heavy reliance on insects in avian diets has long been acknowledged, many details about the taxonomic identity of birds’ insect prey remains unknown. Most ornithological references provide only generalized summaries of which arthropods are consumed by birds (e.g., “caterpillars”, “beetles”), rather than species-specific or even family-level identification of prey. Without such knowledge, experts are limited in their ability to manage landscapes effectively for the production of insects critical to avian conservation. To restore viable bird habitats, we need to know which insect species birds eat, because many insects have specific host plant needs. Most insects are herbivorous and many herbivorous insects have a restricted host plant range,

feeding on only one host plant lineage (Futuyma and Gould 1979, Bernays and

Graham 1988, Forister et al. 2015). Once we understand which insects are most important in bird diets, we can establish the host plants of those insects. This project takes the first step toward providing landscaping recommendations that promote the growth and survival of birds.

1.2 Background Information Past research on bird-insect food webs

The sum total of knowledge on avian food webs gleaned from past studies remains both limited in its scope and scattered across many resources, with species records only rarely consolidated, but some clear trends are apparent in the literature.

One well-established principle is that nestling diet differs distinctly from the adult diet.

Judd (1901) compiled extensive gut dissection and direct observation records to compare various North American nestling birds’ diets with those of adults. He found that the percentage of plant matter in the nestling diet is typically much lower than in adults, while the percentage of insects and other arthropods is higher. For example, berries made up 70% of the diet of adult American Robins (Turdus migratorius), but only 7% of the nestling diet. Similarly, adult sparrows (Passerellidae) were found to be roughly two-thirds granivorous, while the nestlings were exclusively insectivorous.

More recently, Burger et al. (1999) found that California Gnatcatcher (Polioptila californica) adults provisioned their young with a higher proportion of crickets, grasshoppers, and spiders than the adults consumed themselves.

Past studies indicate that even birds regarded as frugivorous, granivorous, or nectarivorous include arthropods in their diet. Polis (1991) reports that while 62% of birds in the Coachella Desert primarily prey on arthropods, an additional 26% use them as secondary prey. West (1973) found that American Tree Sparrows (Spizella arborea) are typically granivorous, but consume more insect matter when insects are abundant during early to mid-summer.

Numerous studies indicate that Lepidoptera, and especially caterpillars, are an important food group for many bird species. Banko et al. (2015) report that moth caterpillars are the dominant prey in the diets of ten of eleven Hawaiian forest bird species. Meunier and Bedard (1983) determined that larval Lepidoptera and Symphyta are the most abundant prey types in the diet of Savannah Sparrow (Passerculus sandwichensis) nestlings. Rodenhouse and Holmes (1992) observed that Lepidoptera made up 58% of the diet of Black-throated Blue Warblers (Setophaga caerulescens).

Stomach content analysis of White-eyed Vireos (Vireo griseus) indicates that

Lepidoptera comprise 46% of the animal food in their diets, 93% of which is from larvae (Nolan and Wooldridge 1962). More than half (54%) of Black-capped

Chickadees’ (Poecile atricapillus) prey items recorded by Kluyver (1961) were caterpillars. Sample et al. (1993) report that several North American passerine species have a caterpillar-dominated diet in early spring, and also note that species not usually associated with caterpillars, such as flycatchers, will prey on them when they are available. In shifting from Lepidoptera to other food groups (i.e., in a setting where pesticide application has reduced the caterpillar population density), birds have to

consume greater amounts of food and expend more energy in searching for food to get the same nutritional value they would have derived from Lepidoptera (Sample et al.

1993). Nagy and Smith (1997) hypothesized that Hooded Warblers (Setophaga citrina) must expand their foraging range or reduce overall food intake in response to a reduction of available Lepidoptera in the environment. Even small leaf-mining caterpillars have value as prey; Connor et al. (1999) suggest that chickadees and titmice (Paridae) are pre-adapted to forage for them.

Past studies in other geographic regions may serve as a useful comparison for

North American species. Grim (2006) determined that Reed Warblers (Acrocephalus scirpaceus) in the Czech Republic prey largely on nonbiting midges (Diptera:

Chironomidae), aphids (Hemiptera: Aphididae), and hoverflies (Diptera: Syrphidae).

Royama’s 1970 study of Great Tits (Parus major) in England and Japan indicates that geometrid caterpillars may be critical prey early in the breeding season, while noctuids predominate in the diet slightly later, before giving way to tortricid pupae. Szentkiralyi and Kristin (2002) found that the foraging mode of songbirds affected the proportion of neuropteroid groups in their diet; foliage gleaners prey more on Chrysopidae, whereas bark foragers prey more on Hemerobiidae and generalist feeders are more likely to prey upon Raphidiidae.

What makes arthropods attractive to birds?

Characteristics of arthropod prey items that could play an important role in nestling survival include total quantity, nutritional value, and moisture content

(Razeng and Watson 2015). Within a given taxon, nutritional content may vary by life cycle stage, sex, season of collection, and diet. According to Bukkens (1997), the protein, iron, and calcium content of insects is comparable to that of pork and beef, and their fiber content is similar to that found in grains. Barker et al. (1998) determined that the five insect taxa they investigated contained enough copper, iron, magnesium, phosphorus, and zinc to meet birds’ requirements, based on known required levels for domestic bird species. Finke (2002) reports that most insects are a good source of selenium as well, but both of these authors note that insects are low in calcium. Razeng and Watson (2015) found that the arthropod groups preyed upon with high frequency (Lepidoptera, Coleoptera, Orthoptera, Hemiptera, and Araneae) contain more macronutrients (fat and protein) and micronutrients (trace elements such as potassium, calcium, magnesium, phosphorus, and zinc) than groups preyed upon less frequently, such as Diptera, Hymenoptera, and Odonata. Spiders (Araneae) have significantly more crude protein and higher levels of micronutrients than other examined groups, and true bugs (Hemiptera) have the highest crude fat content.

Spiders are high in moisture content, which could be an important consideration for birds that derive their water from their food. Ants (Formicidae) stood out as being low in both fat and protein content but were still frequently preyed-upon by some insectivorous birds, perhaps because they are ubiquitous in the environment year- round. Razeng and Watson’s study took place in Australia, but their results partially replicate similar work completed in Kansas by Robel et al. (1995), who independently determined that Hemiptera had the highest fat composition and spiders had the highest

crude protein composition. Kaspari and Joern (1993) found that several grassland bird species avoid small insect prey and prefer intermediate-sized prey, while preference for large insects is directly correlated with bird size; they hypothesized that small insects are avoided because they are harder to find or because of low digestibility/higher chitin content. Numerous bird species have been observed removing the heads or other highly chitinous parts of insects before eating them or feeding them to nestlings.

The importance of Lepidoptera, and especially caterpillars, in avian diets has been noted by numerous authors. Redford and Dorea (1984) assert that low chitin and high fat content and digestibility make Lepidoptera higher-quality prey compared to most other arthropod groups, and adult and larval Lepidoptera are richer in carotenoids than other examined insect groups (Eeva et al. 2010). Of the invertebrate groups sampled by Robel et al. (1995), Lepidoptera had the highest calcium composition.

Razeng and Watson (2015) found that Lepidoptera had the highest potassium content of the 11 arthropod groups they examined. Barker et al. (1998) reported that waxworms (Galleria mellonella) are rich in vitamin E compared to other examined taxa (mealworms (Tenebrio molitor and Zophobas morio), fruit flies (Drosophila melanogaster), house crickets (Acheta domesticus), and earthworms (Lumbricus terrestris)), and Finke (2002) reported that waxworms have higher fat content (60%) than other commercially raised insects, specifically crickets, mealworms, and silkworms (Bombyx mori), although they are deficient in sodium and manganese and have low levels of vitamins A and B. Finke additionally noted that silkworms, another

lepidopteran species, contain high quantities of vitamin A, and female adult gypsy moths (Lymantria dispar) are composed of 80% protein.

Historic methodology

Previous studies have assessed bird dietary choices through a variety of methods such as direct observation, neck ligatures, fecal examination, stomach pumping, gut dissection, and stable isotope analysis (Moreby and Stoate 2000).

Although these methods yield useful data, they have certain limitations. Direct observation (i.e., with binoculars or with aid from a blind, as recorded by Kluyver

(1961) or through “observational tubes” as reported by Baldwin and Kendeigh (1927)) usually only allows for class- or order-level identification of prey, depending on the expertise of the observer; for example, in observations of the House Wren

(Troglodytes aedon), Baldwin and Kendeigh (1927) recorded prey as “fly”, “spider”,

“larva”, and “insect”. When more specific identification is possible, the identification is often deemed tentative (e.g., Nolan and Wooldridge (1962) report a White-eyed

Vireo in the field preying on an “apparent” Pearl Crescent butterfly, Phyciodes tharos). Similarly, in fecal examinations, arthropod prey items are usually only identifiable to order or family (e.g., Calver and Wooller 1982), although Burger et al.

(1999) identified California Gnatcatcher prey items to genus or species.

The ligature method consists of constricting the neck of a nestling with a wire, thread, or band, applying pressure on the proventriculus to prevent swallowing

(Mellott and Woods 1993). Food parcels collected by the neck collar/ligature method

tend to be high-quality and easily identified, although there is a possibility that smaller prey items may pass through the ligature (Johnson et al. 1980, Moreby and Stoate

2000). Neck ligatures can only remain in place for a short time, up to 60 minutes, and food parcels must be removed every 20 minutes (Moreby and Stoate 2000, Grim

2006), making this method particularly labor-intensive as well as intrusive and potentially harmful to the birds. Johnson et al. (1980) determined that food samples collected during a one-hour ligation study with Gray Catbirds (Dumetella carolinensis) and Brown Thrashers (Toxostoma rufum) did not accurately reflect the birds’ diets because the ligatures imposed behavioral changes (e.g., nestlings with ligatures dispelled food from their mouths and gaped less widely than nestlings without ligatures, parent birds may remove food parcels from nestlings’ mouths if they are not swallowed immediately, and some individuals are highly sensitive to disturbance and may not resume feeding activities for up to an hour after human visitation). Kluyver et al. (1961) observed that Black-capped Chickadee nestlings with neck ligatures would not gape at all. In worst-case scenarios, neck collars cause nestling death through strangulation, with pipe cleaner ligatures considered about twice as deadly as electrical cable-tie ligatures (Johnson et al. 1980, Mellott and

Woods 1993).

Fecal samples usually contain a greater diversity of insect prey items than ligature samples because they comprise the remains of several forays, not just one food parcel, and also provide the benefit of being relatively easy to collect without placing undue stress on the avian subjects (Ralph et al. 1985). Fecal analysis, however,

often overlooks soft-bodied and easily digestible prey (e.g., caterpillars, Hemiptera, and Diptera), whose remains may not be easily identifiable or quantifiable, so there is an inherent bias toward hard-bodied taxa (Johnson et al. 1980, Moreby and Stoate

2000). It may also underestimate particular prey taxa if parents remove prey heads prior to provisioning the nestlings. Similarly, gut dissection samples may be incompletely identified due to digestive processes, and this method has the obvious drawback of necessitating the death of the study subject, rendering it infeasible for species of conservation concern or for long-term studies on any bird (Johnson et al.

1980). The use of emetics to cause birds to regurgitate poses similar problems: regurgitated prey items are difficult to identify, and the emetics are stressful and potentially lethal to birds (Ralph et al. 1985). Molecular scatology, or DNA barcoding of fecal samples, can provide species-specific information about birds’ prey, but

Jedlicka et al. (2017) note that primer bias should be considered, as it may lead to underestimation of some taxa. This method is also costly and labor-intensive as it requires collecting fecal material, ideally fresh samples for best results, and requires highly specialized equipment and expertise.

Improvements in camera technology have paved the way toward an alternative method that is far less intrusive and labor-intensive, while still providing unambiguous records of birds’ food choices. Photography has been used in this capacity as early as

1959 (Royama 1959) and has become far more affordable and efficient since then.

Kleintjes and Dahlsten (1992) found that photography was a more effective technique than fecal and gut analysis in determining the diet of cavity-nesting parid nestlings,

with photos yielding more quantifiable and taxonomically-precise data. The authors noted that photographs convey information about prey size and frequency of nest visits over a specific time period, details not attainable via fecal sac or gut dissection analyses. Royama (1970) was able to identify a high proportion of insect prey from bird photographs; to reduce the risk of error, photographs were examined multiple times, insects in the photos were compared with field-collected specimens in a reference collection, and context cues such as the time of appearance and available host plants were taken into consideration. Camera trap studies are minimally invasive as they do not require direct handling of the study organism. Richardson et al. (2009) found that having cameras present at nests did not attract predators and in fact seemed to deter them, perhaps because of predators’ neophobic tendencies; they report that rodents, birds of prey, canids, and corvids are averse to cameras. O’Brien and

Kinnaird (2008) assert that camera trapping is well-suited for shy, rare, or nocturnal species as well as species strongly influenced by human presence, and argue that this method has been under-utilized in past avian studies, noting recent technological advances such as reduced camera size and improved battery life. Gaglio et al. (2017) used digital photography to examine Greater Crested Tern (Thalasseus bergii) diet and asserted that photo-sampling is non-invasive, user-friendly, and allows for accurate prey identification.

Study Organism

Bluebirds were selected as the focal species for this study because they are relatively undisturbed by human visitation to the nest and their nests are easily located, as they readily occupy man-made nest boxes (Hatch and Parlanti 2009). Eastern

Bluebirds are thrushes (Turdidae) that range from Nicaragua north to Canada and as far west as Manitoba and Sonora. Although the International Union for Conservation of

Nature designates their conservation status “least concern” (IUCN 2019), their population may have declined by as much as 90% over the past century due to anthropogenic causes such as habitat loss, competition for nest sites with introduced bird species, and pesticide use (Zeleny 1977). Much of the available data on bluebird populations is thanks to the North American Breeding Bird Survey (BBS) launched in

1966. After a period of decline in the 1970s, their population rose in the 1980s to levels observed in 1966, the first year of the BBS (Sauer and Droege 1990). More recent BBS data indicate that populations remained stable across the U.S. between 2005-2015, but increased in the mid-Atlantic and particularly in Delaware during that time (Sauer et al.

2017).

Bluebirds are secondary cavity nesters (i.e, they do not excavate their own nest holes; LeClerc et al. 2005). They typically occupy holes excavated by woodpeckers or created by the breaking off of branches, but also utilize man-made nest boxes. Cornell et al. (2011) demonstrated that they enjoy higher reproductive success in suburban golf courses compared to other disturbed habitat such as college campuses, agricultural land, and cemeteries. Although golf courses have high levels of human activity and pesticide use, they may allow bluebirds to forage efficiently due to better

visibility in areas with short grass; Pinkowski (1977) noted the importance of sparse vegetative cover in bluebird foraging.

Bluebirds perch on branches, posts, and other vantage points that allow them to look over open ground to visually hunt arthropods (Pinkowski 1977, Cornell et al.

2011). They utilize a variety of methods to capture their prey, such as the drop- foraging technique, aerial flycatching, and gleaning, i.e., removing prey from vegetation. The drop-foraging technique is the most commonly utilized method, making up more than three-quarters of observed prey captures, and consists of searching the ground from a perch and then dropping to the ground to seize prey.

Incidence of drop-foraging behavior decreases over the breeding season, however, as the vegetation grows taller (Pinkowski 1977). Puckett (2009) found that most foraging activity of Eastern Bluebirds in agricultural fields in Nebraska occurs within 50 meters of the forest edge, perhaps because the woody edge provides protective cover, a windbreak to facilitate catching aerial insects, and overall higher invertebrate diversity than is typically encountered in crop fields.

Eastern Bluebirds can produce up to 3 broods per breeding season, although two is typical in Delaware, and each brood typically has 3-5 eggs that are white to pale blue in coloration. The incubation period, which begins when the last egg is laid, typically lasts about two weeks and tends to be longer for spring broods than for summer broods (Gowaty and Plissner 2015). The nestling period (the interval from hatching until fledging) averages 17-18 days (Cornell et al. 2011). Males and females both work to provision nestlings with prey. Nestlings as young as one day old exhibit

begging posture: bills open, necks outstretched (Gowaty and Plissner 2015). Predator guards such as metal stovepipe or cone baffles demonstrably increase nestling survival rate by effectively limiting access by raccoons (Procyon lotor), snakes, southern flying squirrels (Glaucomys volans), and other common predators (Cornell et al. 2011).

1.3 Objectives My aim was to collect detailed data on Eastern Bluebird (Sialia sialis; hereafter “bluebird”) diets in Delaware via camera-trapping. A comprehensive summary of bluebird prey will highlight the arthropod taxa that are most essential to a declining North American insectivorous bird species, better informing future conservation practices.

Specific project goals were 1) to photograph bluebird prey items brought to the nest over the entire nestling period to provide an accurate summary of nestling bluebird diets, 2) to identify the majority of prey items to the ordinal level or below, and 3) to record both first and second broods and to repeat the study for three years to allow for assessment of seasonal and annual variation in diet.

1.4 Materials and Methods In order to investigate Eastern Bluebird diet during the breeding season, I mounted cameras on the roofs of nest boxes at Mt. Cuba Center in Hockessin, New

Castle County, Delaware to provide a photographic record of adult bluebirds provisioning their nestlings with insects and other prey items. I identified the prey items from the photos to the lowest possible taxonomic rank, with assistance from

several other insect taxonomists, using references such as Johnson and Triplehorn

(2005) and Wagner (2005). I performed a chi-squared test to compare the arthropod composition of the diet across the three years of the study, and between the first and second broods to assess seasonal variation in diet.

Eastern Bluebirds are a uniquely well-suited research organism because they frequently nest in man-made nest boxes and acclimate easily to occasional human visitation (Hatch and Parlanti 2009). They also have a tendency to alight on the roof of the nest box (if the roof is flat or gently sloping; they are less prone to alight on steeply sloped roofs; personal observation) before entering the nest hole, which facilitates photo capture of any prey items they deliver to the nestlings.

Originally, I included House Wrens (Troglodytes aedon) as an additional study species, but their rapid movement, smaller average prey size, and disinclination to land on the roof with prey rendered many of the resulting photos too blurry and indistinct to facilitate prey identification. Moreover, they occupied too few nest boxes on the Mt.

Cuba property to make useful comparisons with bluebirds. I added the House Wren photos with identifiable prey to the community science database described in Chapter

Study Site and Nest Boxes

Mt. Cuba Center is renowned as a botanic garden specializing in native plants, located in the Piedmont region of Delaware. The gardens are surrounded by over

1,000 acres of natural lands, including both forest habitat and open fields. The fields

are mown twice a year and managed by a natural lands team with habitat enhancement projects and invasive species removal. Approximately 70 bluebird nest boxes are installed in the natural lands and reliably occupied each year by bluebirds, Tree

Swallows (Tachycineta bicolor), and occasionally by House Wrens. These boxes follow the pattern recommended by the Cornell Lab of Ornithology Nest Watch program: 9” deep, 5 ½” wide, and 5 ½” long, with an entrance hole 2 ¼” high and 1

3/8” wide. Next boxes are mounted on 4-by-4 posts with the nest height between 4-6’.

They are protected by conical plastic predator guards or “collars” attached to the pole underneath the nest box. A team of 2 volunteers monitored the bluebird boxes weekly during the breeding season (April-August) each year to record the number of eggs, nestlings, and fledglings. These volunteers removed the nests from the boxes after each brood fledged, a practice often done in an effort to reduce ectoparasitism rates, although Mason (1944) suggests that removing nests may actually increase ectoparasitism rates, as it removes the natural enemies that keep ectoparasites in check and Davis et al. (1994) demonstrated that bluebirds prefer nesting in boxes with old nesting material left intact.

Cameras

I deployed twelve GoPro HERO 3+ cameras and one GoPro HERO Original camera as camera traps at Mt. Cuba. Although not camera traps in the traditional sense

(i.e., they are not motion- or light-activated), these models can be set to take photos on a time-lapse. I used the 1-second time lapse setting on the twelve GoPro HERO 3+

cameras and the half-second time lapse setting on the

GoPro HERO Original, which does not have an option for

1-second intervals. I chose these cameras in lieu of

traditional trail cameras due to their affordability, but like

trail cameras, they have the benefit of being

waterproof/weatherproof and are capable of withstanding

temperatures up to 125°F. An additional benefit of GoPro

cameras is their small size, allowing the cameras to be

stationed on the tops of the 4-by-4 posts to which the Figure 1. GoPro camera stationed at Eastern Bluebird bluebird boxes were attached, using a flat 4” x 4” plastic nest box. mount (Fig. 1). Without exception, the bluebirds quickly

acclimated to the presence of the cameras and resumed their usual behaviors (e.g.,

foraging) within minutes of camera set-up. I placed the cameras at occupied nest

boxes each morning during the breeding season between 6:00-9:00 a.m. Battery life

typically lasted between 3-4 hours (x̅ = 3.4 hours). Often, I replaced the first camera

with a second one after the battery died, between 10:00 a.m.-1:00 p.m., to capture

several more hours of feeding events. Although the cameras did not capture every

feeding event during the nestling period, setting up the cameras early in the morning

ensured that the busiest part of the bluebirds’ day in terms of provisioning was

recorded; the average number of feedings is higher in the morning than in the

afternoon (Gowaty and Plissner 2015).

1.5 Results Over three field seasons, I monitored 38 bluebird broods from the time the eggs hatched until the young fledged: 12 in 2015, 16 in 2016, and 10 in 2017. The camera traps took a total of 9,680,940 photos, recording approximately 8,200 feeding events (i.e., an adult bluebird returning to the nest box holding a prey item in its bill).

On average, one feeding event occurred every 19 minutes of recording. I reviewed the photos and identified approximately 93% of prey items to ordinal level or below. Male bluebirds took on a slightly higher share of the provisioning burden than females did, capturing 57% of the prey items provisioned to nestlings.

Lepidoptera made up the single most important prey group, comprising 41% of the diet. Caterpillars, a designation that usually refers to the larvae of moths and butterflies (Lepidoptera) but is here extended to include larvae of sawflies

(Hymenoptera: Symphyta) as well due to their morphological and behavioral similarity to Lepidoptera, comprised 92% of prey items designated “Lepidoptera,” greatly surpassing adult moths and butterflies. Within the larval Lepidoptera, most prey items were smooth, green caterpillars as opposed to darker caterpillars with dense hairs or spines; the most commonly observed taxa included Noctuidae, Geometridae,

Papilionidae, and Sphingidae. Most common adult Lepidoptera belonged to Erebidae,

Sphingidae, Nymphalidae, and Papilionidae.

The second most important taxonomic group in the bluebirds’ diet was

Orthoptera, including crickets (Gryllidae), grasshoppers (Acrididae), katydids

(Tettigoniidae), mole crickets (Gryllotalpidae), leaf-rolling crickets (Gryllacrididae),

and camel crickets (Rhaphidophoridae). This group constituted 26% of the overall diet. Within Orthoptera, grasshoppers were the dominant taxon, making up 35.5% of the total orthopteran prey, closely followed by crickets (33%). Katydids constituted

27% of the orthopteran prey, with mole crickets comprising 2.5% and camel crickets and leaf-rolling crickets comprising about 1% each.

The third most heavily predated group was Araneae, making up 19% of the overall diet. The bluebirds did not specialize on a particular family within the Araneae but instead foraged frequently on wolf spiders (Lycosidae), crab spiders (Thomisidae), jumping spiders (Salticidae), and orb weavers (Araneidae).

The fourth most commonly observed prey item in the bluebirds’ diet, and the only substantial non-arthropod group, was earthworms (Megadrilacea), making up 5% of the overall diet. Earthworms were consumed more in 2016 than in the other years;

51% of total earthworm consumption occurred in that year, and earthworms were

6.4% of the overall diet that year compared to 1.6-5.1% in other years. Earthworms were not usually identified below the ordinal level, but in some photos, the clitellum appeared much paler than the rest of the body, indicating that they belong to the genus

Amynthas. This genus is native to Asia and is considered invasive in the United States

(Görres and Melnichuk 2012).

Beetles (Coleoptera), in both larval and adult forms, constituted about 3% of the observed prey items in this study. The most frequently taken beetle groups included click beetles (Elateridae), carrion beetles (Silphidae), and scarab beetles

(Scarabaeidae). Rove beetles (Staphylinidae), soldier beetles (Cantharidae), blister

beetles (Meloidae), ground beetles (Carabidae), and fireflies (Lampyridae) were observed less frequently among the coleopteran prey.

True flies (Diptera) represented about 1% of the bluebirds’ diet. Within this group, the most frequently observed prey were crane flies (Tipulidae), making up 76% of the total dipteran prey. Horse flies (Tabanidae) and robber flies (Asilidae) were occasionally predated as well. Diptera made up a higher proportion of the diet in 2017 than expected, and a lower proportion than expected in 2015 and 2016.

Plant matter, mostly berries, made up about 1% of the bluebirds’ diet. Specific items in this group included white mulberries (Morus alba), blueberries (Vaccinium), black cherries (Prunus serotina), and black gum drupes (Nyssa sylvatica).

The following arthropod taxa were present in the photos of the bluebirds’ prey items, but each represents less than 1% of the overall diet for the breeding season: mayflies (Ephemeroptera), dragonflies and damselflies (Odonata), praying mantises

(Mantodea: Mantidae), true bugs (Hemiptera), dobsonflies (Megaloptera), ants and wasps (Hymenoptera: Apocrita), daddy longlegs (Opiliones), millipedes (Diplopoda), centipedes (Chilopoda), earwigs (Dermaptera), and woodlice (Isopoda). It is important to note that the proportion of hymenopterans in the diet is likely much higher than 1%, but as noted above, larval sawflies (Symphyta) were included with lepidopterans because these two groups were often indistinguishable, depending on the angle, lighting, and general quality of the photo, and because they occupy the same trophic guild. The most commonly observed prey items within the Apocrita were ants

(Formicidae), usually alates, with only occasional predations on wasps (e.g., Vespidae,

Pompilidae).

Odonate prey items, although infrequent (i.e., 10 items total), included both adults and nymphs. On 25 July 2017, two female bluebirds returned to their nests with dragonfly nymphs (Aeshnidae: Epiaeschna heros). Each female captured two nymphs for a total of four immature odonate prey. The first female caught the two nymphs eight minutes apart; the second captured her prey twenty-minute minutes apart. An additional 6 odonate prey items (two of which were identified as adult black- shouldered spinylegs; Gomphidae: Dromogomphus spinosus) were also documented in this study. Prior authors (e.g., Kennedy 1950) report finding adult dragonflies in examined bluebird stomach contents, but do not report nymphs; this is apparently a novel observation. The females that captured odonate nymphs lived in nest boxes within foraging distance (<75 meters) of either Red Clay Creek or a small pond.

Bluebirds were not previously known to forage on immature odonates (Kennedy et al.

2019).

Within the Hemiptera, the most commonly observed prey items were stink bugs (Pentatomidae), which made up half of the observed prey items in this group and mostly consisted of the invasive brown marmorated stink bug (Halyomorpha halys) with occasional inclusion of the native green stink bug (Acrosternum (Chinavia) hilare). Cicadas (Cicadidae) made up roughly one-quarter of hemipteran prey, and occasional leaf-footed bugs (Coreidae) and assassin bugs (Reduviidae) were predated as well.

Slugs and land snails (Gastropoda) were rarely consumed, accounting for only

12 prey items in total. This group represents the only non-arthropod invertebrate taxon aside from earthworms (Megadrilacea) in the bluebirds’ diet. These prey items were not identified below ordinal level; however, the snails’ shells were heliciform

(conical-depressed) and at least superficially resembled those of snails in the families

Zonitidae, Discidae, and Polygiridae.

Eight instances of predation on vertebrates were observed over the course of this study. No mammalian or avian prey were observed, but one brown snake (Storeria dekayi) and seven frogs were brought to the nest by four individual bluebirds. The frogs were not identified to species due to poor photo quality, but belonged to the family Ranidae, and may have been pickerel frogs (Lithobates palustris; Nazdrowicz, pers. comm.).

Although the same major prey groups were consistently taken over the study period, there was some annual variation in the bluebirds’ diet (X2 = 287, df = 36, p <

0.01; Table 1). Fewer spiders were taken in 2015 than expected. Fewer flies were taken in 2015 and 2016, but more in 2017, than expected. Fewer earthworms were taken in 2015, but more in 2016, than expected. More Lepidoptera were taken in 2015 than expected. More Orthoptera were taken in 2016, but fewer in 2017, than expected.

Orthoptera remained the second most common prey group each year, but the most heavily predated family within the order Orthoptera changed from year to year: in

2015, more katydids (Tettigoniidae) were consumed, compared to more grasshoppers

(Acrididae) in 2016 and more crickets (Gryllidae) in 2017.

The composition of prey varied seasonally, i.e., when first broods (i.e., those with nestlings reared in April-mid-June) are compared with second broods (those with nestlings reared in late-June-August) (X2 = 436.19, df = 18, p < 0.01; Table 2). Most earthworms, flies, and spiders were consumed by the first broods, and all praying mantis (Mantodea), vertebrate, and odonate prey were consumed only by the second broods. The proportions of Lepidoptera and Orthoptera in the diet rose each year with the second brood, sometimes dramatically; e.g., in 2016, Orthoptera made up 24% of the diet of the first broods, but 44% of the diet of the second broods. The latter part of the 2016 season marked the only time that caterpillars were not the dominant prey group, as they were eclipsed at that time by Orthoptera; Lepidoptera made up 30% of the diet compared to Orthoptera at 44%.

Table 1. Contingency table of frequencies of different taxa of Eastern Bluebird prey (annual variation), with percent contributions to chi-square.

2015 2016 2017

% % % Obser Observe Expect Prey Taxon Expected Contributi Expected Contribut Observed Contribu ved d ed on ion tion Lepidoptera 638 530 7.7 1058 1136 1.9 1259 1290 0.3 Orthoptera 327 326 <0.1 818 699 7.1 673 793 6.4 Araneae 194 244 3.6 517 523 <0.1 649 593 1.8 Megadrilacea 20 61 9.7 175 131 5.0 147 149 <0.1 Coleoptera 31 39 0.6 78 84 0.2 110 96 0.8 Diptera 4 17 3.6 12 37 6.0 81 42 12.3 Diplopoda 11 8 0.3 9 18 1.6 27 20 0.7 Chilopoda 3 4 <0.1 2 8 1.6 16 9 1.8 Anura & 0 1 0.5 0 3 1.1 8 4 2.0 Squamata Gastropoda 3 2 0.1 0 5 1.6 9 5 0.9 Hemiptera 4 6 0.2 4 12 1.8 23 14 2.3 Hymenoptera 3 7 0.8 10 15 0.6 26 17 1.7 Mantodea 13 13 <0.1 20 27 0.6 37 31 0.5 Odonata 0 1 0.5 0 3 1.1 8 4 2.0 Plants 19 13 1.1 28 27 <0.1 24 31 0.6 Opiliones 5 1 5.0 0 2 0.1 1 3 0.4 Isopoda 0 1 0.3 2 2 <0.1 3 2 0.1 Neuroptera 0 0 <0.1 0 0 0.1 1 0 0.3 Ephemeroptera 0 0 <0.1 0 0 0.1 1 0 0.3

Table 2. Contingency table of frequencies of different taxa of Eastern Bluebird prey (seasonal variation), with percent contributions to chi-square.

Brood 1 Brood 2

% % Prey Taxon Observed Expected Observed Expected Contribution Contribution Lepidoptera 1418 1487 0.7 1521 1452 0.8 Orthoptera 784 915 4.3 1024 893 4.4 Araneae 793 676 4.6 544 660 4.7 Megadrilacea 281 173 15.5 61 169 15.8 Coleoptera 122 96 1.7 67 93 1.7 Diptera 80 48 5.1 14 46 5.2 Diplopoda 14 20 0.4 26 20 0.5 Chilopoda 2 10 1.5 18 10 1.5 Anura & 6 4 0.2 2 4 0.2 Squamata Gastropoda 1 4 0.4 6 4 0.4 Hemiptera 14 13 <0.1 12 13 <0.1 Hymenoptera 18 18 <0.1 17 17 <0.1 Mantodea 0 34 7.9 68 34 8.1 Odonata 3 5 0.2 7 5 0.2 Plants 5 35 6.0 65 35 6.1 Opiliones 0 3 0.7 6 3 0.7 Isopoda 2 3 <0.1 3 3 <0.1 Neuroptera 0 1 0.1 1 1 0.1 Ephemeroptera 1 1 0.1 0 1 0.1

1.6 Discussion The proportion of the nestling diet comprising Lepidoptera clearly indicates that it is the most important arthropod taxon to breeding bluebirds. This observation has implications for land management because the majority of Lepidoptera are host plant specialists. Whereas some phytophagous insects are generalists that can survive and reproduce on a variety of host plants, about 90% of caterpillars are oligophagous or monophagous, having a much more restricted host range (Futuyma and Gould

1979, Bernays and Graham 1988, Forister et al. 2015). To support caterpillars and in

turn support bluebirds, it is necessary to promote the planting of native plants, which produce higher diversity and biomass of Lepidoptera than non-native plants do

(Tallamy and Shropshire 2009, Burghardt et al. 2010, Narango et al. 2017, Richard et al. 2018).

It is presumed that birds can more easily find earthworms in times of heavier precipitation because earthworms typically surface after rainfall, for reasons that are not fully understood (Porter 2011). There was a moderate but not significant correlation between monthly total precipitation and percentage of earthworms in the bluebird diet (r = 0.46, df = 10, p = 0.13). Interestingly, 2016, the year with the greatest earthworm consumption, was the driest year of the study with 52.7 cm total rainfall between April-August, compared to 57.9-58.6 cm for that same period in other years, but most earthworm predation occurred in May of that year, which was a wetter than average month with 18.5 cm rainfall compared to 6.1-14.9 cm in other years.

June 2015, however, was also an unusually wet month with 31.8 cm of rainfall and only saw one earthworm predation event, so total precipitation does not provide a complete explanation for earthworm predation.

Although it is not unusual to observe changes in the arthropod composition of the diet over the breeding season, based on the seasonal availability of various food sources, I did not expect to see the percentage of spiders decline between the first and second broods. This finding is in contrast to findings by Arnold et al. (2010) which indicated that spiders increased in the blue tit (Cyanistes caeruleus) diet over the breeding season.

It is unclear whether the vertebrate prey items (frogs and snake) were successfully ingested by the bluebird nestlings. Other authors (e.g., Greer 2000,

Braman and Pogue 2005, Baxter et al. 2006, Stanback and Mercadante 2009) reported finding dead vertebrates in active bluebird boxes, indicating that they were delivered by the adult bluebirds, but were not consumed by the young. However, Beal (1915) reported bones of frogs and lizards in bluebird gut content analyses, and Bay and

Carter (1997) described bluebirds successfully provisioning their nestlings with ground skinks, resulting in at least partial ingestion. The Mt. Cuba volunteers who monitored the nest boxes did not observe any dead frogs or snakes in the nests, which lends support to the idea that they were consumed. In the instance of the brown snake, which was a small juvenile, it is possible that the adult bluebird mistook it for a large earthworm. The Amynthas earthworms that the bluebirds frequently preyed upon are known by the common names “snake worm” and “crazy snake worm” due to their large size and snake-like behavior (i.e., slithering and jumping movement; Görres and

Melnichuk 2012). This was the first recorded instance of a bluebird preying on a brown snake (Kennedy, 2019).

The sex difference observed in provisioning rates is consistent with earlier studies. Gowaty and Plissner (2015) note that male bluebirds in higher latitudes provision the nestlings more frequently than females do when females are brooding young, which typically occurs from hatching until the nestlings are about 5 days old.

During this period, females are compelled to divide their time between brooding and foraging, while males can focus on searching for prey.

Some bluebird pairs varied substantially from the overall trends. For example, one bluebird pair in 2017 preyed heavily on crane flies (Tipulidae), accounting for

83% of the total crane fly consumption (59 of 71 feeding events) observed in this study and 21.5% of the total prey items recorded for that particular brood. This particular pair lived in a nest box that was within foraging distance (<75 meters) of

Red Clay Creek. Crane flies typically require an aquatic habitat for the larval stage.

Many other bluebird pairs, however, also lived within foraging distance of the creek or a pond and did not forage for crane flies.

The cameras did not capture every feeding event, as they did not run from dawn to dusk, but instead from early morning until late morning or early afternoon, so prey captured at dawn, late in the afternoon, or in the evening were not recorded.

Cameras set up at dawn or in the evening resulted in photos too dark to allow for prey identification due to low ambient light. In addition, Jedlicka et al. (2017) found that

Western Bluebirds (Sialia mexicana) in California fed on ectoparasitic bird blowflies within the nest box; if Eastern Bluebirds exhibit a similar behavior, this interaction could not have been captured on camera. Of the prey items captured on camera, the subset that I could not identify was biased towards smaller insects, as the bird’s bill obscured more of the body.

Generally, bluebirds appear to selectively forage for species that rely on crypsis/camouflage rather than chemical defenses. Many of the nest boxes included in this study were located in meadows with abundant milkweed, but milkweed specialists such as monarch butterflies (Danaus plexippus), milkweed tussock moths (Euchaetes

egle), milkweed beetles (Tetraopes tetrophthalmus), dogbane beetles (Chrysochus auratus), and milkweed bugs (Oncopeltus fasciatus) were not observed among the birds’ prey items, despite being abundant in the environment. Milkweed specialists sequester cardiac glycosides from their host plant, rendering themselves toxic or unpalatable to most predators. Similarly, although one bluebird male arrived at the nest box with a net-winged beetle (Calopteron discrepans) in June 2017, he dropped and subsequently ignored the prey item rather than ingesting it or delivering it to his nestlings. Net-winged beetles, which are marked by aposematic orange and black stripes, are protected by pyrazines and lycidic acid (Eisner et al. 2005).

Within the Myriapoda, the bluebirds appeared to avoid larger, more toxic millipedes (e.g., cherry millipedes) and instead preyed on centipedes in the order

Lithobiomorpha and the genus Scolopocryptops and millipedes in the families

Parajulidae and Abacionidae. It is worthy of note, however, that millipedes in the genus Abacion, which the bluebirds preyed on occasionally, are known to have foul- smelling chemical defenses (Hennen, pers. comm.).

Among the lepidopteran adult prey, most prey items were drab moths rather than aposematic, toxic species, with notable exceptions. Several species of tiger moths in the genus Apantesis were preyed upon by roughly a dozen individual bluebirds over the course of the study. These species are known to sequester toxic secondary metabolites from host plants, and their aposematic coloration advertises their supposed unpalatability to predators (Conner 2009). These colorful moths were the exception rather than the rule; even brightly-colored palatable species, such as the Eastern tiger

swallowtail (Papilio glaucus) were only rarely among the birds’ prey. Among the larval lepidopteran prey, the same rule applied: most caterpillars photographed in this study were smooth, green caterpillars that lacked chemical or physical defenses (e.g.,

Geometridae and Noctuidae). An exception is papilionid caterpillars, which brandish a defensive organ called an osmeterium to emit terpenes when threatened, but this is consistent with Jaervi et al. (1981) and Leslie and Berenbaum (1990), who note that the osmeterium is ineffective against birds. Other exceptions include variegated fritillary caterpillars (Euptoieta claudia), which have six rows of spines, and Eastern tent caterpillars (Malacosoma americanum), which are densely covered in hairs.

Eastern tent caterpillars were preyed upon frequently and yet did not appear to be a preferred food: the birds seldom foraged for them on the ground or gleaned them from vegetation, but instead ate them after the caterpillars had climbed to the nest box roofs of their own volition (or, perhaps, under the influence of a behavior-altering baculovirus; Hoover et al. 2011), and even then, the birds often ignored them for some period before ingesting them.

Occasionally, bluebird juveniles (identified by pale spotting in the plumage of their backs and chests) would alight on the roofs of the nest boxes. Presumably these were individuals from the first brood of the season returning to the nest boxes where they were reared, but this is speculative, as individual identification was not possible.

These juveniles occasionally gaped at the adult bluebirds for food, unsuccessfully, and foraged for food for themselves with some success. The diet of fledglings, based on the limited sample (n = 50 prey) seen in these photos, appears similar to the nestling

diet: 56% Lepidoptera, 22% Araneae, and 20% Orthoptera. As far as the photos indicated, these individuals did not help to rear the second brood, and appeared to be a nuisance to the parents, who typically chased them away. This is consistent with earlier anecdotal reports of juveniles hindering rather than helping adults (Becker

1944).

Prey type and prey size did not appear to vary with age of nestlings; this is consistent with past observations from bluebirds in Tennessee (Pitts 1978). Chinese praying mantises (Tenodera sinensis) and fork-tailed bush katydids (Scudderia furcata) were among the largest prey items procured by the bluebirds, and the bluebirds frequently provisioned them to nestlings that were only 2-3 days old and continued to procure them with the same frequency throughout the nestling period. It is possible that the parents disarticulated larger prey items once inside the nest box to make ingestion easier, but at the time the parents entered the nest, all prey items were intact. Inside-the-nest-box footage from Pennsylvania shows that bluebird nestlings are able to consume prey that is “nearly the same size as them” without the prey being broken down into smaller pieces (Williams 2018). In general, the bluebirds appeared to forage for large insects, although it is possible that they also preyed upon smaller ones and ingested them rather than delivering them to the nestlings, or regurgitated them to the nestlings as Wheelock (1904) reports occurring in Western Bluebirds.

Optimal foraging theory postulates that animals maximize fitness by choosing foraging strategies that offer the most energy for the lowest cost (Pyke et al. 1977). In

practice, birds provisioning their nestlings with food should selectively choose larger prey and ignore or immediately ingest smaller prey.

In addition to the nutritive value of prey, overall abundance, and size, prey mobility (ease of capture) could be important factors in bluebird foraging choices.

Caterpillars, which accounted for about 92% of prey designated as Lepidoptera, are sedentary and easier to catch than mobile adults. Similarly, the most common flies in the bluebirds’ diet were crane flies (Nematocera: Tipulidae), which fly slowly compared to flies in the suborder Brachycera (e.g., horse flies, house flies) and spend much of their adult lives hanging motionless from vegetation. Brachycera were far more uncommon in the birds’ diets. Adult dragonflies, which are among the fastest insects, were only taken rarely, and appeared to be teneral, i.e., recently eclosed and thus weak fliers. Other insects noted for their capable flight and speed, such as hover flies (Syrphidae) and hawk moths (Sphingidae), were similarly rarely or never observed, except in the flightless larval stage. This is consistent with results from

Burger et al. (1999), who found that California Gnatcatchers eat sessile arthropods more than would be expected based on availability in the environment.

Incidental Records

The camera traps recorded other types of behaviors besides foraging, and other species beyond the target species of the study. Most photos with bluebirds as the subjects showed the bluebirds perched on the nest box roofs, sunning and/or surveying their surroundings, and occasionally appearing to sing or vocalize. Bluebird adults

frequently defended their nest boxes from Tree Swallows and rarely from other birds as well, and on some occasions dive-bombed the human intruder setting up the camera at the nest. Bluebird grooming behaviors, such as preening or scratching themselves with their toes, were also recorded.

Other bird species that periodically landed on the roofs of the nest boxes included American Crows (Corvus brachyrhynchos), American Goldfinches (Spinus tristis), American Robins (Turdus migratorius), Baltimore Orioles (Icterus galbula),

Barn Swallows (Hirundo rustica), Blue Grosbeaks (Passerina caerulea), Blue Jays

(Cyanocitta cristata), Brown-headed Cowbirds (Molothrus ater), Carolina Chickadees

(Poecile carolinensis), Chipping Sparrows (Spizella passerina), Downy Woodpeckers

(Picoides pubescens), Eastern Kingbirds (Tyrannus tyrannus), Eastern Phoebes

(Sayornis phoebe), Eastern Towhees (Pipilo erythrophthalmus), Eastern Wood-

Pewees (Contopus virens), European Starlings (Sturnus vulgaris), Gray Catbirds

(Dumetella carolinensis), House Finches (Haemorhous mexicanus), House Sparrows

(Passer domesticus), House Wrens (Troglodytes aedon), Mourning Doves (Zenaida macroura), Northern Cardinals (Cardinalis cardinalis), Northern Flickers (Colaptes auratus), Northern Mockingbirds (Mimus polyglottos), Red-winged Blackbirds

(Agelaius phoeniceus), Song Sparrows (Melospiza melodia), Tree Swallows

(Tachycineta bicolor), and White-breasted Nuthatches (Sitta carolinensis). Usually, these birds simply perched on the nest box roof for a moment before flying on; occasionally, they (specifically, two Eastern Phoebes, an Eastern Wood-pewee, an

Eastern Kingbird, and a Red-winged Blackbird) stayed long enough to catch and eat

an insect prey item. One image captured a Red-tailed Hawk (Buteo jamaicensis) flying by at very low altitude (~2 meters), and Canada Geese (Branta canadensis) were not uncommonly sighted foraging on the ground in the background of the photos. Other non-avian vertebrate species that were sighted in the background of the photos include snapping turtles (Chelydra serpentina), red foxes (Vulpes vulpes), coyotes (Canis latrans), groundhogs (Marmota monax), Eastern cottontails (Sylvilagus floridanus), white-tailed deer (Odocoileus virginianus), as well as humans and domestic dogs. At some nest boxes, the cameras also recorded other indicators of human presence such as cars, trucks, tractors, buses, bicycles, and trains. These incidental captures indicate that camera trapping can provide a useful passive method of conducting animal population surveys.

1.7 Conclusions This study collected an in-depth record of the diet of breeding Eastern Bluebird during three consecutive field seasons, providing the most comprehensive examination of bluebird diet recorded to date, with both a larger prey sample size and higher rate of prey identification than past studies. This study demonstrates that camera trapping is a minimally invasive yet effective technique to study bird diets, a consideration that is becoming increasingly important as bird populations continue to decline and more invasive methods become increasingly difficult to justify. In accordance with past studies, the results indicate that Lepidoptera is the most important food group for

breeding bluebirds, highlighting the importance of native plants that support higher lepidopteran diversity and biomass than alien plants do.

Chapter 2

ASSESSMENT OF EASTERN BLUEBIRD PREY PREFERENCE

2.1 Introduction The field project described in Chapter 1 provided the most comprehensive summary of Eastern Bluebird diets completed to date. It yielded substantial evidence that bluebirds prey on caterpillars more than any other food during the breeding season, while Orthoptera and Araneae, respectively, are the second and third most heavily depredated prey taxa. Despite the fact that the adult bluebirds provisioned their nestlings with caterpillars more than any other food, this does not in itself indicate an innate preference for caterpillars over other prey types. It is possible that bluebirds simply take whichever arthropods are most abundant or accessible to them in the environment. To manage landscapes effectively for avian conservation, it is crucial that we understand not only which insects birds eat, but which insects they prefer. This knowledge would enable landowners and property managers to plant the host plants that are necessary to support the most important insect taxa in breeding bird food webs.

Past studies indicate that dietary discrimination on several bases exists in multiple bird species. Senar et al. (2010) found that Great Tits prefer carotenoid- enriched mealworms over control prey, demonstrating a specific appetite (i.e.,

preference) for carotenoids. Similarly, Murphy and King (1987) demonstrated that molting white-crowned sparrows (Zonotrichia leucophrys) have a specific appetite for sulfur amino acids. Sherry and McDade (1982) found that White-fronted Nunbirds

(Monasa morphoeus) reject various insect prey based on size, hardness, and palatability. Rechten et al. (1983) found that Great Tits follow the predictions of optimal foraging theory more closely when they are hungry versus when they are satiated. Muller et al. (2006) demonstrated that Black-capped Chickadees prefer caterpillars that fed on leaves with lower levels of phenolic glycosides over those with higher levels.

To elucidate if birds’ prey selection represents active choice reflecting an innate preference, a field manipulation called a Paired Stimulus Preference

Assessment or “versus” test (Tobie et al. 2015) was conducted to provide adult bluebirds with different arthropod prey choices. Cameras recorded the sequence in which the bluebirds selected their prey from the evenly-sized, equally abundant choices available.

2.2 Materials and Methods Ten pairs of bluebirds at Mt. Cuba Center (Hockessin, New Castle County,

Delaware) were tested in 2017 and 14 pairs were tested in 2018. A bluebird male- female pair was considered a single unit for the purpose of this experiment, given that they frequently forage simultaneously and work in tandem to feed their nestlings.

Five insect taxa were selected for this experiment based on their availability for purchase or capture in large quantities. Greater waxworms (Lepidoptera: Pyralidae:

Galleria mellonella), Jamaican field crickets (Orthoptera: Gryllidae: Gryllus assimilis), and mealworms (Coleoptera: Tenebrionidae: Tenebrio molitor) were purchased from various pet stores in Newark and Wilmington, Delaware. Cabbage loopers (Lepidoptera: Noctuidae: Trichoplusia ni) were purchased from Frontier

Scientific Services, Inc., in Newark, Delaware. Brown marmorated stink bugs

(Hemiptera: Pentatomidae: Halyomorpha halys) were collected in personal dwellings in Pennsylvania and Delaware. Brown marmorated stink bugs were not used in this experiment during the first year (2017) but were added to the other four prey items in

2018. The insects were kept frozen and then transported to the field in a cooler packed with ice packs to preserve the freshness of the specimens.

A Paired Stimulus Preference Assessment or “versus” test (Tobie et al. 2015) was used to assess which prey types were favored. In most trials, two taxa were simultaneously made available to the bluebirds by placing 6 specimens of each (12 total specimens) on the roofs of the active nest boxes. Another treatment entailed placing 3 specimens of all taxa on the roofs simultaneously for a total of 12 or 15 specimens (15 if brown marmorated stink bugs were included; 2018 only). A GoPro

Hero 3+ camera on a 1-second time-lapse setting was stationed at the nest box to record the sequence in which the bluebirds selected the prey items, either for immediate ingestion or to provision the nestlings inside the nest box. The insects were placed in pairs or groups consisting of one specimen of each taxon, approximately

matched for size so that size could be eliminated as a potential confounding variable

(Fig. 2).

Figure 2. Paired Stimulus Preference Assessment example. Male bluebird selecting his first choice of 12 prey items (6 waxworms and 6 cabbage loopers).

Several different parameters of the Paired Stimulus Preference Assessment were employed to measure preference. In “first choice” analyses, a taxon/food type was considered preferred above the other if the bluebirds selected it first. In Paired

Stimulus Preference Assessment trials, the first choice is considered a reflection of attractiveness (Tobie et al. 2015). The number of times each prey type was selected as a first choice was tallied for each bluebird pair and the resulting tally used to rank the prey items as highest preferred, moderately preferred, or lowest preferred. The second parameter used was the ratio of the first prey type to the second prey type (number of individual specimens consumed). The third parameter examined was the preference ratio, or the amount of each prey type consumed divided by the total amount of food available.

There are some drawbacks inherent in the Paired Stimulus Preference

Assessment. For example, it can only demonstrate the attractiveness of the offered prey items in a relative, not absolute, sense. Additionally, there is no control for how different types of prey might influence each other’s palatability. Nonetheless, it is the most common type of test used in pet food palatability studies (Tobie et al. 2015), an application that has obvious parallels to this study and is a reasonable first step toward understanding food preferences in a field-based study.

2.3 Results One bluebird pair of the 24 tested did not eat any of the insect prey items made available to them, which reduced the sample size to n = 23. A total of 270 trials were performed, with an average of 11 trials per bluebird pair; see Appendix A for complete list of trial results. Nearly all prey items made available to the bluebirds were consumed, which rendered the first choice analyses more informative than the other examined parameters of the Paired Stimulus Preference Assessment. First choice analysis provides a measure of which prey types are more attractive because only the first prey item taken in each trial is considered, rather than the overall volume of insects consumed. In contrast, the other two parameters examined were the ratio of prey type 1 to prey type 2 and the preference ratio (the amount of each prey type consumed divided by the total amount of food available), which both rely on measures of the quantity of consumed prey. In the event that all available prey are consumed,

these parameters do not yield statistically significant differences. For this reason, the following results pertain only to the first choice analyses.

Greater waxworms were the most preferred prey item of the five taxa included in this experiment. They were the highest preferred item or among the highest preferred items in 15 of 23 bluebird pairs (62.5%) and were preferred in 65% of trials in which they were included as a prey item. Mealworms were the highest preferred items, or among the highest preferred items, in 7 of 23 pairs of bluebirds (30.4%).

Crickets emerged as a taxon of medium preference, as they were among the highest preferred items in 6 of 23 bluebird pairs (26.1%). Cabbage loopers were among the highest preferred items in only one bluebird pair (4.4%). Brown marmorated stink bugs clearly emerged as the least attractive food item of the five taxa presented to the bluebirds. They were not among the highest preferred items in any trials, and were among the least preferred prey items for 11 of 12 pairs (91.7%) that were exposed to them.

The final preference ranking of the included insect taxa from most to least preferred, based on first choice analysis, was greater waxworms, mealworms,

Jamaican field crickets, and cabbage loopers in 2017. In 2018, with the addition of a fifth prey type, the ranking was largely the same as in 2017, with the new prey item indicated as the least-preferred. The preference ranking from most to least preferred in

2018 was greater waxworms, mealworms, Jamaican field crickets, cabbage loopers, and brown marmorated stink bugs.

2.4 Discussion This project provides evidence that Eastern Bluebirds will actively select certain types of prey when presented with a choice between different species of equally abundant, similarly-sized prey. The majority of tested bluebird pairs selected greater waxworms before selecting alternative prey options, as opposed to selecting prey randomly, as would be expected if the choice were governed solely by prey abundance.

The bluebirds demonstrably preferred greater waxworms over the other taxa included in this experiment. Waxworms do not closely resemble any arthropod prey that the bluebirds typically encounter in their natural day-to-day foraging as they are native to Eurasia and are nest parasites of bee colonies, a setting that keeps them well- protected from avian predators. This suggests that bluebirds are not averse to trying novel foods. Brown marmorated stink bugs, in contrast, are a species the bluebirds would frequently be exposed to in the wild, as they are commonly sighted at Mt. Cuba

Center (although this species is not native to Delaware, they have been present in New

Castle County since at least 2005; Cutting 2012). Nonetheless, they were the least- favored prey item in this experiment. This is likely due to the stink bugs’ aldehydic secretions that make them taste as well as smell repugnant to predators (Noge et al.

2012).

Past studies provide evidence for both neophobic and neophilic foraging tendencies in birds. This can be assessed at the specific or the individual level; for example, Greenberg (1983) found that Chestnut-sided Warblers (Setophaga petechial)

are more hesitant to try novel foods than are Bay-breasted Warblers (Setophaga castanea), while Boogert et al. (2006) demonstrated that individual European Starlings within the same social groups varied in their neophobic foraging tendencies. Given the broad popularity of waxworms across subjects in this study, and the unpopularity of stink bugs, I suggest that bluebirds as a species are on the neophilic end of the spectrum with regard to foraging behavior. Alternatively, bluebirds may have a general preference for caterpillars as a group, with no importance attached to species- level prey identity.

Although bluebirds do not naturally forage for waxworms, waxworms are caterpillars (Lepidoptera), which as a whole is the most dominant food group in the bluebirds’ diet, and a group noted to be both highly nutritious as well as highly digestible (Redford and Dorea 1984). Interestingly, the bluebirds did not prefer cabbage loopers, the other lepidopteran species included in this experiment. This may be due to the high moisture content in this species. Although moisture content would likely be considered an asset in a living caterpillar, in a dead one it contributes to a more rapid decomposition. The cabbage loopers, if not eaten soon after placement on the nest box roofs, tended to become discolored more quickly and distinctly than the other, drier prey options, particularly on hot, sunny days that expedited the decomposition process.

This study lends further support to the hypothesis that foraging decisions are not guided by prey abundance. Prey choice could be guided instead by inherent characteristics related to prey nutritional value (profitability) or by the birds’ past

experience (e.g., formation of a search image). Royama (1970) introduced the profitability hypothesis, which proposes that birds choose prey to maximize caloric intake while minimizing energy expenditure. Tinbergen (1960) showed that birds capture a disproportionately high number of prey relative to the prey population density, suggesting that birds forage with a specific search image developed after repeated exposure to a particular prey type. Based on these prior studies and the results of this experiment, prey abundance is not the most important factor governing birds’ foraging choices.

Chapter 3

NORTH AMERICAN BREEDING BIRD FOOD WEBS

3.1 Introduction The most recent State of the Birds report indicates that 37% of North American bird species are in need of urgent conservation action (North American Bird

Conservation Initiative, 2016). The report also designated an additional 49% of species as warranting “moderate” conservation concern, leaving only 14% to be ranked of

“low” conservation concern. Data from long-term Breeding Bird Surveys indicate that the number of birds in North America has declined by more than a billion in just forty years (Blancher et al. 2013). These alarming figures highlight the need for swift and decisive action on avian conservation.

Major drivers of bird declines include the loss and degradation of both breeding and non-breeding habitat for multiple reasons, including development for housing, industry or agriculture, pollution and the spread of alien plants. Pimentel et al. (2005) estimate that roughly 25,000 non-native plant species have been introduced to the

United States, while Qian and Ricklefs (2006) claim that over 3,300 of them have become invasive. Invasive plants make up an estimated 1/3 of total plant biomass in most ecosystems. Nelson et al. (2017) reviewed 128 studies to assess the impacts of invasive plant species on North American birds and found that avian species richness decreased with plant invasions in 41% of tests. Non-native plants degrade habitats by

competing with native plants and by reducing insect diversity and biomass because they do not present herbivorous insects with the same nutritional quantity and quality as native plants (Narango et al. 2017). Insect declines have been documented around the globe (e.g., Hallmann et al. 2017, van Strien et al. 2019) and cited as a possible driver of declines in insectivorous birds (Gregory et al. 2014).

Because 96% of North American terrestrial bird species rear their young on insects and other arthropods (Peterson 1980), we need to understand which arthropods are the most essential in bird diets, particularly during the breeding season, so that we can prioritize planting those species’ host plants to restore viable bird habitats.

I sought to expand our knowledge of bird-arthropod food webs in North

America by inviting community scientists (formerly known as “citizen scientists”) to share photos of North American birds eating arthropods. Photography provides the advantage of being a minimally invasive method to investigate birds’ diets, compared to past methods such as gut dissection and neck ligation (see Chapter 1 for more discussion). I used these photographs to quantify the proportions of the various arthropod taxa that comprised the diets of different bird families. The project was focused on breeding birds because insects dominate the diet of both breeding adults and their nestlings (Judd 1901), although I also received and examined photos of birds with arthropod prey during the non-breeding season.

3.2 Materials and Methods D.W. Tallamy launched a website in June 2014 to solicit photographs of birds eating or carrying insects or other arthropod prey to nestlings. This user-friendly

website had the easily memorable URL of www.whatdobirdseat.com and invited bird enthusiasts, nature photographers, and the general public to submit such photographs along with supporting information about when and where they were taken. There were entry fields for the photographer’s name, email address, the date the photograph was taken, the nearest city or town, state/province, bird species (if known), and additional comments (optional). The home page contained a link to a page explaining the background behind the project so users/contributors were aware of why photographs were being requested and how they would be used.

Approximately a year after the website was published (August 2015), I launched a Facebook page to raise awareness of the project and crowd-source additional photographs. The Facebook page (www.Facebook.com/WhatDoBirdsEat) was designed to complement the website as well as reach a different audience. Many photographers preferred sharing their photos with the online community of the Facebook site as this allowed them to receive feedback and engage with like-minded members. Others preferred to keep their photos private by submitting them directly to the website. I shared the website and Facebook page widely using a variety of social media outlets

(e.g., Facebook pages of state or national birding and nature groups, Twitter, and iNaturalist), advertising them in person through more than three dozen presentations, mostly to regional birdwatching clubs, and by distributing business cards at nature centers, wildlife stores, conferences, and other venues likely visited by people interested in birds or photography. In summer 2018, along with two collaborators from Virginia

Commonwealth University, I created a three-minute video summarizing the importance

of arthropods in birds’ diets and posted it on social media to further advertise the project. It amassed more than 50,000 views in the first three months it was live.

I reviewed new submissions periodically and identified the arthropod prey to the lowest possible taxonomic level, typically their order or family. I made identifications using comprehensive references such as Johnson and Triplehorn (2005) and Wagner

(2005). However, because the geographic scope of submissions and taxonomic diversity of the pictured prey items was so broad, I invited several arthropod taxonomists from different regions in the United States who specialize in different taxa to share their expertise in insect identification. Usually, the person who submitted the photo identified the bird to species, although I corroborated the identification using a field guide or with help from bird experts in the UD Department of Entomology and Wildlife Ecology and the Delaware Nature Society. I categorized the bird in each photograph as breeding (i.e., probably carrying prey to its young) or non-breeding (i.e., foraging for itself). I assumed birds were breeding if the date and location of each photograph was consistent with the timing of that species’ breeding season in that area, or if the observer’s comments or bird’s behavior suggested or confirmed breeding (i.e., the bird was photographed at or near a nest).

Larval Symphyta (sawflies) proved very difficult to distinguish from larval

Lepidoptera (caterpillars) and so I grouped these two taxa together for the analysis. This meant that sawflies were excluded from the Hymenoptera category, which became restricted to the Apocrita (wasps, bees, and ants). I counted multiple photos documenting the same prey item (i.e., taken at the same time in the same location) as single feeding events. I disregarded photos with mealworms (Tenebrio spp.) as these

prey had been provisioned by the photographer and are not naturally encountered in

North America.

All breeding bird data were pooled and then grouped into 8 regions to allow geographic comparisons. These regions were the Northeast (i.e., Canada’s easternmost provinces, New England, and south to New Jersey), Mid-Atlantic (Pennsylvania south to Virginia and west to West Virginia), Southeast (Tennessee, North Carolina,

Arkansas, and all states to the south of those), Midwest (states adjacent to the

Mississippi River, from Missouri and Kentucky northward to Ontario, plus Indiana,

Ohio, and Michigan), West (Great Plains and the Rocky Mountains, northward to

Manitoba and Saskatchewan), Southwest (Mexico, Texas, New Mexico, and Arizona),

Pacific (California and Nevada only), and Pacific Northwest (Oregon, Washington,

Idaho, north to Alaska, Yukon Territory, British Columbia, and Alberta) (Fig. 4).

3.3 Results Community scientists contributed photos representing approximately 6,500 instances of birds preying on insects and other arthropods. These photos included 323

North American bird species, every state in the U.S., and almost every Mexican state and Canadian province (see Appendix B for a complete list of species). More than 1,200 community scientists submitted photographs. Most participants submitted only one photo, while some submitted over one hundred photos. The states from which the most photographs were contributed were Virginia, Florida, California, Pennsylvania,

Maryland, New York, and Texas. Most photos were taken in the past 10 years, and nearly all were taken in the past 20 years.

I assumed that the birds in most of the photos, especially most of those depicting passerines, were breeding birds that were carrying prey to provision their young. This assumption is based on knowledge of bird eating behavior; birds provisioning their nestlings hold the prey item while en route to the nest. In contrast, birds that are feeding themselves typically eat the prey item immediately (as there is little reason to wait) and thus the window of opportunity to photograph them is much smaller (personal observation). The photos spanned a wide range in quality and consequently in their usefulness, from those too blurry or distant to facilitate any identification of prey, to those allowing prey identification to the species level. Most (87%) of the contributed photos were deemed useful, i.e., they depicted a North American bird eating arthropod prey that could be identified to the ordinal level or below. Of 5,660 prey items identified to ordinal level, 31% were additionally identified to family, 9% to genus, and

6% to species. Photos taken outside of North America or featuring a non-arthropod prey item were not used. Most bird species were only represented by one or a few photos while some were represented by hundreds (see Appendix B to see most frequently photographed species). Thus, I grouped photos of all species within the same bird family for analyses. I tallied photos depicting predation on an ootheca or other type of egg case conservatively, i.e., representing one prey item.

Breeding Birds

Lepidoptera made up the largest arthropod prey group for 15 of the 20 examined families of breeding birds, and comprised the majority of arthropod prey in seven of those groups; they also made up one of the top three prey taxa in three additional

families of breeding birds (Fig. 3). More than a third (36%) of all recorded bird- arthropod interactions involved lepidopteran prey, and 85% of those lepidopteran prey were in the larval stage.

The arthropod diet of breeding woodpeckers (Picidae) comprised mostly

Hymenoptera (21%), Coleoptera (21%), Lepidoptera (20%), and Hemiptera (10%), based on 152 photos. Nearly all the hymenopteran prey consisted of ants (Formicidae), and most beetles were in the larval form.

Cuckoos (Cuculidae) preyed heavily on Lepidoptera (59% of total arthropod diet), followed by Orthoptera (23%), Odonata (4%), and Hemiptera (4%), based on 73 photos. There was substantial variation between species in this group, as would be expected based on variation in habitat types; for example, Orthoptera made up 65% of the diet of Greater Roadrunners (Geococcyx californianus), a ground-dwelling bird of the arid southwestern U.S., while caterpillars made up a higher proportion of the diet of the tree-dwelling Mangrove Cuckoos (Coccyzus minor), which live in the mangrove swamps of Florida.

Breeding hummingbirds (Trochilidae) fed mainly on Diptera (92%), including flies caught in spider webs, as well as the occasional spider or bee, based on 24 photos.

Within the flycatchers (Tyrannidae), the major arthropod groups were

Lepidoptera (23%), Odonata (19%), Orthoptera (15%), Diptera (10%), Hymenoptera

(10%), and Coleoptera (9%), based on 438 photos, of which 117 depicted Eastern

Phoebes (Sayornis phoebe). Two photos depicting species within the closely-related

Tityridae were included in this grouping.

Shrikes (Laniidae) fed principally on Orthoptera (40%), Coleoptera (32%), and

Lepidoptera (11%), based on 85 photos. These photos included many in which the bird itself was not shown, but the prey had been impaled on a thorn or nail in the characteristic manner associated with this family.

Within the vireos (Vireonidae), the major arthropod food groups were

Lepidoptera (64%), Orthoptera (7%), Hemiptera (7%), and Araneae (6%), based on 162 photos. Lepidopteran families of particular importance to this group include Noctuidae,

Erebidae, Notodontidae, Lasiocampidae, and Papilionidae.

Jays and crows (Corvidae) fed mainly on Coleoptera (26%), Hymenoptera

(22%), Lepidoptera (19%), and Orthoptera (15%), based on 27 photos.

The arthropod diet of breeding swallows (Hirundinidae) comprised mainly

Odonata (37%), Hymenoptera (16%), Diptera (16%), Isoptera (9%), and Hemiptera

(7%), based on 142 photos.

The arthropod diet of breeding chickadees and titmice (Paridae) heavily favored

Lepidoptera (75%), Araneae (15%) and Hemiptera (3%), based on 243 photos. Roughly

150 contributed photos in this group depicted Carolina Chickadees (Poecile carolinensis). Verdins (Auriparus flaviceps) were included in this grouping, although they belong to the closely-related family Remizidae, as they are the only remizids in

North America and did not constitute a large enough data set to analyze separately.

Bushtits (Aegithalidae), nuthatches (Sittidae) and treecreepers (Certhiidae), combined here due to phylogenetic and ecological similarity, had a diet consisting mainly of Lepidoptera (52%), Araneae (16%), Hemiptera (5%), Blattodea (5%), and

Coleoptera (5%), based on 134 photos. Most photos in this group depicted Brown- headed Nuthatches (Sitta pusilla).

Wrens (Troglodytidae) fed mainly on Lepidoptera (35%), Araneae (26%),

Orthoptera (14%), and Opiliones (9%), based on 459 photos. Most (360) photos in this category depicted House Wrens, one of the most frequently included species in this study.

Gnatcatchers’ (Polioptilidae) arthropod prey consisted mainly of Lepidoptera

(43%), Araneae (33%), Diptera (10%), Hymenoptera (3%), and Odonata (3%), based on

72 photos.

The arthropod groups most heavily preyed upon by kinglets (Regulidae) included Hemiptera (36%), Lepidoptera (25%), Diptera (18%), and Araneae (11%), based on 28 photos.

Thrushes (Turdidae) fed heavily on Lepidoptera (45%), followed by Orthoptera

(19%), Araneae (13%), and Coleoptera (11%), based on 856 photos. Most of the contributed photos in this group depicted Eastern Bluebirds, the most frequently included species in this study.

Mimids (Mimidae) preyed most heavily on Lepidoptera (28%), Orthoptera

(19%), Coleoptera (19%), and Hymenoptera (8%), based on 139 photos.

European Starlings (Sturnus vulgaris), as the only sturnid species in North

America, were not grouped with any other species. Their arthropod diet comprised mainly Lepidoptera (45%), Coleoptera (21%), Orthoptera (18%), and Araneae (12%), based on 33 photos.

Cedar Waxwings (Bombycilla cedrorum), the only bombycillid species included in the photo database, were featured in photos documenting 13 arthropod prey items, including 5 Diptera, 2 Hymenoptera, 2 Orthoptera: Acrididae, 2 Odonata, one

Lepidoptera, and one Hemiptera: Cicadidae.

Finches (Fringillidae) were among the least-represented groups included in the study, with only 11 photos with identifiable arthropod prey. These included a fall webworm caterpillar (Hyphantria cunea), another caterpillar, six box elder bugs (Boisea trivittatus), a cicada (Neotibicen sp.), a psyllid, and a wasp. This paucity of arthropod prey photos is unsurprising considering that this group contains some of the most strictly granivorous species. Nonetheless, these photos indicate that even the most granivorous birds will turn to insects for diet supplementation during the breeding season.

Warblers (Parulidae) principally fed on Lepidoptera (51%), Araneae (16%),

Diptera (10%), and Hemiptera (5%), based on 1042 photos. Noctuidae and Geometridae appear to be particularly important lepidopteran families in warbler diets.

Sparrows (Passerellidae) fed most on Lepidoptera (62%), Orthoptera (12%),

Diptera (8%), and Hemiptera (5%), based on 547 photos. House Sparrows (Passeridae) were also included in this grouping due to ecological similarity; as the only passerids in

North America, they did not constitute a large enough data set to analyze separately.

The main arthropod prey of cardinals and allies (Cardinalidae) consisted of

Lepidoptera (37%), Orthoptera (20%), Hymenoptera (17%), Coleoptera (7%),

Hemiptera (5%), and Mantodea (5%), based on 190 photos. This group exhibited a great deal of interspecific variation in diets; for example, the most abundant arthropod prey

was Orthoptera in Dickcissels (80%), caterpillars in Northern Cardinals (55%), and wasps and bees in Summer Tanagers (69%).

Blackbirds, orioles, and allies (Icteridae) fed mainly on Lepidoptera (38%),

Odonata (15%), Orthoptera (13%), Diptera (12%), and Araneae (7%), based on 420 photos. Yellow-breasted Chats (Icteria virens) were included in this grouping, although they belong to the monotypic family Icteriidae, because there were not enough photos to analyze them separately, but the relative proportions of the major arthropod prey types do not change if this taxon is removed.

Picidae, n = 152 Cuculidae, n = 73

59% 21% 18% 21% 10% 23% 5% 4% 5% 2% 2% 3% 4% 1% 1% 4% 1% 1% 1% 1%

Trochilidae, n = 24 Tyrannidae, n = 438 92%

23% 19% 15% 9% 10% 10% 5% 6% 4% 4% 1% 0% 5% 0% 0% 0% 0% 0% 0% Laniidae, n = 85 Vireonidae, n = 162

40% 64% 32%

11% 6% 4% 4% 7% 7% 6% 0% 0% 2% 0% 3% 0% 1% 4% 3% 4%

Corvidae, n = 27 Hirundinidae, n = 142

26% 37% 22% 19% 15% 16% 16% 7% 4% 4% 7% 5% 6% 0% 0% 0% 0% 0% 0% 0%

Paridae, n = 243 Aegithalidae & allies, n = 134

75% 52%

15% 16% 0% 3% 0% 0% 3% 2% 1% 0% 0% 4% 0% 5% 5% 5% 3% 5%

Troglodytidae, n = 459 Polioptilidae, n = 72 35%

26% 43% 33% 14%

10% 3% 3% 4% 1% 2% 3% 4% 2% 1% 3% 0% 0% 0% 0% Turdidae, n = 856 Regulidae, n = 28 36% 45% 25% 18% 11% 19% 11% 13% 4% 4% 3% 0% 0% 0% 0% 2% <1% <1% 2% 2%

Mimidae, n = 139 28% Sturnidae, n = 33 45% 19% 19%

21% 8% 18% 5% 12% 3% 3% 4% 4% 0% 3% 0% 0% 0% 0% 0% Parulidae, n = 1042 Passerellidae, n = 547 51%

62%

16% 10% 12% 4% 5% 8% 3% <1% <1% 2% 2% 2% 5% 3% 3% 3% <1% 0% Cardinalidae, n = 190 Icteridae, n = 420 38% 37%

20% 17% 15% 13% 11% 5% 5% 7% 7% 3% 0% 2% 3% 2% 0% 2% 3% 1%

Figure 3. Composition of arthropod taxa in North American breeding bird diets, based on crowd-sourced photos from community scientists. Arthropod orders listed phylogenetically.

Figure 4. Regions of United States and Canada used for geographic comparisons.

Geographic patterns emerged when all breeding bird data were pooled.

Lepidoptera was the dominant arthropod prey taxon for breeding birds in all 8 regions.

Lepidoptera peaked at 59% of the diet in the Northeast, decreasing along the Atlantic seaboard to 42% in the Mid-Atlantic and 37% in the Southeast. A similar north-south gradient was observed in western North America; Lepidoptera declined slightly from

35% in the Pacific Northwest to 30% in both the Pacific and Southwest. In the middle of the continent, it fell from 43% in the Midwest to 28% in the West.

As Lepidoptera declined along a north-south gradient, Coleoptera and

Orthoptera rose. Beetles made up only 2% of the arthropod diet in the Northeast, but

8% in the Mid-Atlantic and 9% in the Southeast. Orthoptera rose from 3% of the diet in the Northeast to 11% in the Mid-Atlantic and 14% in the Southeast. Beetles comprised only 1% of the diet in the Pacific Northwest but climbed to 9% in both the Pacific and the Southwest. Orthoptera peaked at 20% of the arthropod diet in the Southwest.

Diptera peaked at 17% of the diet in the West and reached a low of 3% in the

Southwest. Less variation was observed in the frequency of Araneae, which peaked at

12% of the arthropod diet in the Mid-Atlantic and was lowest in the Pacific Northwest and in the West at 6%. Hemiptera consistently made up only a small proportion of the diet, from 2% in the Northeast and West to a high of 8% in the Southwest.

For three species (Eastern Bluebirds, House Wrens, and Prothonotary Warblers) more than 200 photos were submitted, enough to analyze regional trends and differences in diet. Some of the same patterns observed in the pooled breeding bird data were seen in these species. For example, Lepidoptera made up 59% of the arthropod diet in bluebirds in the Northeast, 39% in the Mid-Atlantic, and 26% in the Southeast, while Orthoptera and Coleoptera rose along the same gradient; farther west,

Lepidoptera made up 48% of the diet in the West but only 40% in Texas. Orthoptera also increased along the north-south gradient in House Wrens and Prothonotary

Warblers. Lepidoptera, however, peaked in House Wrens at 41% of the diet in the Mid-

Atlantic, compared to 28% in the Northeast and 25% in the Southeast, and peaked at

57% of the Prothonotary Warbler diet in the Southeast, compared to 46% in the Mid-

Atlantic and 25% in the Midwest.

Non-breeding birds

Photos of raptors, owls, wading birds, and various other bird groups with arthropod prey were frequently submitted. In the majority of these photos, in contrast to the passerines and other groups described above, the birds were eating prey directly, not carrying the prey to provision their young. Although the focus of this study is breeding birds’ diets, a generalized summary of the arthropod prey in these other groups is provided below.

Five photos with ducks and allies (Anseriformes) were submitted, showing a

Wood Duck (Aix sponsa) with dragonfly prey, a White-winged Scoter (Melanitta deglandi) with a crayfish, and three Hooded Mergansers (Lophodytes cucullatus) with crayfish.

One photo of a Northern Bobwhite (Colinus virginianus) with a grasshopper

(Orthoptera: Acrididae) was submitted, the only galliform (quails and allies) represented in the photo database.

Eight photos of grebes (Podicepiformes) were submitted, mostly showing

Decapoda as prey, but also one adult moth (Lepidoptera), one fly (Diptera), and one dragonfly (Odonata).

Eleven photos of cranes and rails (Gruiformes) with arthropod prey were submitted. Observed prey included three scarab beetle larvae (Scarabaeidae), one grasshopper, one adult moth, one caterpillar (Erebidae), a green darner dragonfly (Anax junius), and several unidentified dragonflies.

Plovers, sandpipers, and allies (Charadriiformes) fed mainly on Diptera (48%),

Decapoda (36%), and Odonata (7%), based on 84 photos. Several species in this group were only observed feeding on decapods (e.g., crabs, crayfish) as opposed to insects or other arthropods.

Three photos of Common Loons (Gavia immer) with crayfish prey (Decapoda) were submitted; these were the only contributed photos depicting birds in the order

Gaviiformes.

The arthropod diet of herons, ibises, and allies (Pelecaniformes) comprised mainly Decapoda (44%), Odonata (31%), and Hemiptera: Belostomatidae (9%), based on 85 photos. Although crustaceans predictably made up the largest arthropod food group, every bird species included in this group was observed feeding on insects at least once.

The arthropod diet of birds of prey (Accipitridae) consisted mainly of

Hemiptera: Cicadidae (37%), Orthoptera (23%), Coleoptera (17%), and Odonata (11%), based on 35 photos.

Owls (Strigidae) fed upon Lepidoptera (33%), Coleoptera (27%), Decapoda

(18%), and Orthoptera (12%), based on 33 photos. All recorded lepidopteran prey were caterpillars, not adult moths.

Falcons (Falconidae) fed mainly on Orthoptera (45%), Odonata (34%),

Lepidoptera (8%), and Mantodea (8%), based on 66 photos. Nearly all the photos in this group featured American Kestrels (Falco sparverius).

Photos showing six non-breeding trogons (Trogonidae) feeding on arthropods were submitted, showing two praying mantises, a katydid (Tettigoniidae), a grasshopper

(Acrididae), a caterpillar, and an adult moth (Sphingidae) as prey.

Two photos of Belted Kingfishers (Megaceryle alcyon) showed them eating crayfish (Decapoda) as well as indeterminate flying insects that were caught in a spider web.

Table 3. Composition of arthropod taxa in North American breeding bird diets, based on crowd-sourced photos from community scientists.

Lepid Orthopter Coleop Hemipter Bird Taxon Araneae Odonata Diptera Other optera a tera a Picidae 31 3 (2%) 7 (5%) 32 3 (2%) 6 (4%) 15 (10%) 55 n = 152 (20%) (21%) (36%) Cuculidae 43 17 (23%) 1 (1%) 1 (1%) 3 (4%) 1 (1%) 3 (4%) 4 (5%) n = 73 (59%) Trochilidae 0 (0%) 0 (0%) 1 (4%) 0 (0%) 0 (0%) 22 (92%) 0 (0%) 1 (4%) n = 24 Tyrannidae 100 63 (15%) 28 (6%) 41 81 (19%) 43 (10%) 20 (5%) 60 n = 438 (23%) (9%) (14%) Laniidae 9 34 (40%) 3 (4%) 27 5 (6%) 0 (0%) 2 (2%) 5 (6%) n = 85 (11%) (32%) Vireonidae 104 11 (7%) 10 (6%) 7 (4%) 4 (3t%) 7 (4%) 12 (7%) 7 (4%) n = 162 (64%) Corvidae 5 4 (15%) 2 (7%) 7 0 (0%) 1 (4%) 0 (0%) 8 (30%) n = 27 (19%) (26%) Hirundinidae 8 (6%) 1 (<1%) 0 (0%) 7 (5%) 52 (37%) 23 (16%) 10 (7%) 41 n = 142 (30%) Paridae 181 6 (3%) 36 (15%) 5 (2%) 0 (0%) 2 (<1%) 8 (3%) 5 (2%) n = 243 (75%) Aegithalidae 69 5 (4%) 21 (16%) 6 (5%) 1 (<1%) 6 (5%) 7 (5%) 19 and allies (52%) (14%) n = 134 Troglodytidae 162 62 (14%) 118 (26%) 13 2 (<1%) 20 (4%) 14 (3%) 68 n = 459 (35%) (3%) (15%) Polioptilidae 31 3 (4%) 24 (33%) 1 (1%) 2 (3%) 7 (10%) 2 (3%) 2 (3%) n = 72 (43%) Regulidae 7 1 (4%) 3 (11%) 0 (0%) 0 (0%) 5 (18%) 10 (36%) 2 (7%) n = 28 (25%) Turdidae 388 164 (19%) 108 (13%) 90 16 (2%) 19 (2%) 24 (3%) 47 (6%) n = 856 (45%) (11%) Mimidae 39 27 (19%) 5 (4%) 26 4 (3%) 7 (5%) 5 (4%) 26 n = 139 (28%) (19%) (18%) Sturnidae 15 6 (18%) 4 (12%) 7 0 (0%) 0 (0%) 1 (3%) 0 (0%) n = 33 (45%) (21%) Parulidae 535 39 (4%) 170 (16%) 19 30 (3%) 103 (10%) 47 (5%) 99 (9%) n = 1042 (51%) (2%) Passerellidae 340 66 (12%) 18 (3%) 16 8 (2%) 42 (8%) 29 (5%) 28 (5%) n = 547 (62%) (3%) Cardinalidae 70 37 (20%) 6 (3%) 13 5 (3%) 4 (2%) 9 (5%) 46 n = 190 (37%) (7%) (24%) Icteridae 158 53 (13%) 31 (7%) 13 63 (15%) 44 (11%) 9 (2%) 49 n = 420 (38%) (3%) (12%)

As a means of verifying the efficacy of this community science project’s methodology, the subset of photos showing Eastern Bluebirds was compared closely with the photos of Eastern Bluebirds from the field study described above in Chapter 1.

The photos from the bluebird field study are considered unbiased with regard to prey type as they were taken by camera traps rather than human photographers; human photographers could be more inclined to capture photos featuring large, colorful, or otherwise charismatic prey than smaller, more drab prey, while the camera traps continuously took photos, capturing images of all prey brought to the nest while the batteries lasted. An important difference between these two data sets is that the photographers in the community science project were asked to submit only photos of birds eating arthropods, while the camera traps captured other prey items, such as earthworms, gastropods, and berries. Although there were differences between the two data sets (X2= 212.15, df = 16, p < 0.01; Table 4), the top three taxa in both datasets differed very little in their relative frequency and comprised 80-90% of total invertebrates in the diet. In both data sets, caterpillars emerged as the dominant prey group, followed by orthopterans, spiders, and beetles, in the same order of frequency and in similar proportions (Fig. 5). Coleoptera, Hemiptera, and Odonata were more prevalent in the community science photos than the camera trap photos, accounting for most of the differences between these two data sets (Table 4).

Table 4. Contingency table of frequencies of different taxa of Eastern Bluebird prey (crowd-sourced photos versus camera trap data), with percent contributions to chi-square.

Community Science Data Camera Trap Data

% % Order of Prey Observed Expected Observed Expected Contribution Contribution Lepidoptera 192 211 0.8 2955 2936 <0.1 Orthoptera 120 130 0.4 1818 1808 <0.1 Araneae 70 96 3.3 1360 1334 0.2 Coleoptera 50 18 27.6 219 251 2.0 Diptera 7 7 0 97 97 0 Hemiptera 17 3 28.7 31 45 2.1 Mantodea 2 5 0.8 70 67 0.1 Odonata 7 1 14.7 10 16 1.1 Chilopoda 3 2 0.6 21 22 <0.1 Diplopoda 1 3 0.7 47 45 <0.1 Hymenoptera 7 3 2.4 39 43 0.2 Isopoda 1 1 0.4 5 6 <0.1 Isoptera 1 0 6.3 0 1 0.5 Opiliones 0 0 0.2 6 6 <0.1 Blattodea 1 0 6.3 0 1 0.5 Neuroptera 0 0 <0.1 1 1 <0.1 Ephemeroptera 0 0 <0.1 1 1 <0.1

Figure 5. Arthropods in breeding Eastern Bluebird diets. Left: EABL diets in Delaware based on camera trap data, n = 7,173 prey. Right: EABL diets based on community science data, n = 523 prey. For the purposes of this comparison, non-arthropod taxa were excluded from the camera trap data. 65

3.4 Discussion As seen in the Eastern Bluebird project described in Chapter 1, this project yields strong evidence that Lepidoptera is the most important food source for many breeding birds. Given that the majority of caterpillars are host specialists that can only feed on a limited range of host plants (Futuyma and Gould 1979, Bernays and Graham

1988, Forister et al. 2015), these findings have important ramifications concerning land use. As a result of the ongoing evolutionary arms race between plants and herbivores, many phytophagous insects have adapted to circumvent the chemical defenses of their host plants, becoming increasingly specialized to those hosts and unable to survive on other plants (Ehrlich and Raven 1964). Although some insect herbivores are generalists

(e.g., most Orthoptera), fewer than 10% of all insect herbivores feed on plants in more than three plant families (Bernays and Graham 1988). Non-native plants do not produce as much herbivorous insect biomass as native plants do (Tallamy et al. 2010, Richard et al. 2018), so in order to conserve the single most important arthropod group for breeding birds, it is critical to support the use of native plants in both managed and natural landscapes. Based on the findings of this study, planting a wide variety of native plants is a recommended course of action for public and private property managers.

The geographic differences in the composition of bird diets merit further investigation. The higher proportion of Lepidoptera in the diet in more northern latitudes could be linked to mass emergences of species such as the winter moth

(Operophtera brumata) and the forest tent caterpillar (Malacosoma disstria), which

reach outbreak proportions in the Northeast (Roland and Embree 1995, Cooke and

Lorenzetti 2006).

I measured arthropod prey by their abundance in contributed photos; the rankings of prey types would likely be slightly different if prey could be measured by biomass rather than abundance. Larger-bodied taxa such as praying mantises

(Mantodea) would rise in importance while Diptera and Hemiptera would decline in importance, as many of the recorded insects in these groups were small-bodied (e.g., midges, aphids). The rankings of other groups, such as Lepidoptera and Coleoptera, would likely remain relatively stable, as these diverse groups include species spanning a wide range in body size, from diminutive inchworms and lady beetles to the much- larger Luna moth caterpillars and cerambycid beetle larvae.

The crowd-sourcing community science methodology appears to be an effective method for collecting data across a wide geographic range and many species. The proportions of different arthropod taxa observed in the Eastern Bluebird diet from contributed photos and from the camera trap data (Chapter 1) were strikingly similar

(Fig. 5). This indicates that photos taken by community scientists can provide an accurate overview of birds’ diets, given a data set of at least several hundred photos.

The differences between the data sets (i.e., the higher frequency of Hemiptera,

Coleoptera, and Odonata in the crowd-sourced photos relative to the camera trap photos) could be due to geographic variation in arthropod abundance. While the camera trap data were restricted to Delaware, the crowd-sourced data came from across the eastern half of North America. Human photographer bias could play a role as well; e.g.,

large taxa such as many dragonfly and beetle species may attract more attention as they are easier to see and arguably more charismatic.

Photography has become a more accessible hobby in recent decades as cameras have become more affordable, and average photo quality has improved with advanced technology, but the number of photos of birds with identifiable prey taken prior to 2000 is limited. Thus, this methodology is not best-suited for tracking changes in breeding bird diet over the past century, but would be appropriate for tracking future changes in diet.

Occasionally, users submitted photos of “turned tables” bird-arthropod interactions, i.e., arthropods preying on birds. Although these photos were not specifically sought, they provided an interesting complement to the data set on birds eating insects. In each of these photos, the prey species was the Ruby-throated

Hummingbird, Archilochus colubris, which weighs only 2-6 grams and is 7-9 centimeters long. The predator species included a dragonhunter dragonfly, Hagenius brevistylus (Odonata: Gomphidae), a yellow garden spider, Argiope aurantia (Araneae:

Araneidae), and several Chinese mantids, Tenodera sinensis (Mantodea: Mantidae). In the case of the dragonhunter, the photographer commented that he intervened to free the hummingbird, so it is uncertain whether or not the dragonfly would have successfully killed or ingested it. According to Garrison et al. (2006), dragonhunters are 7-9 centimeters long, the same as the Ruby-throated Hummingbird, and as their name suggests, they are specialists that typically feed on other dragonflies. The yellow garden spider wrapped its hummingbird prey in a silk cocoon and scalped it before feeding;

McCormick and Polis (1981) report that this species is known to feed on hummingbirds,

skinks, and snakes. Several additional photos of small birds (e.g., gnatcatchers, flycatchers) caught in spider webs were submitted, but in these instances, it was unclear if the spiders preyed upon them. In the photos of praying mantids preying on hummingbirds, user commentary suggested that the mantids (which can reach lengths of over 11 centimeters and weigh up to 7 grams) waited at hummingbird feeders to ambush their prey and were able to kill and feed on them successfully. Nyffeler et al.

(2017) provide evidence that this is not uncommon.

As seen in the Eastern Bluebird field study in Chapter 1, other bird species generally, but not always, appeared to avoid species with aposematic coloration and chemical defenses. Exceptions include Mountain Bluebirds (Sialia currucoides) in

Alberta that forage frequently on Apantesis tiger moths, just as Eastern Bluebirds in

Delaware do (see Chapter 1). A Common Grackle (Quiscalus quiscula) in Florida in

2012, a Dark-billed Cuckoo (Coccyzus melacoryphus), in Florida in 2019, and a Black

Phoebe (Sayornis nigricans) in California in 2018 consumed Gulf fritillary butterflies

(Nymphalidae: Agraulis vanillae) despite the latter’s orange coloration, sequestered alkaloids, and odorous ester defenses. A Merlin (Falco columbarius) in New York in

2015 captured a monarch butterfly (Nymphalidae: Danaus plexippus), with its talons, but subsequently released it instead of ingesting it. Similarly, an American Kestrel in

Texas in 2018 caught a monarch butterfly, took a bite, and then released it, according to the photographer’s observations. An Eastern Bluebird in Virginia, however, ingested a monarch caterpillar, apparently undeterred by its aposematic coloration and sequestration of cardenolides. A flock of Evening Grosbeaks (Coccothraustes vespertinus) in Utah in 2014 consumed box elder bugs (Hemiptera: Boisea trivittatus)

despite the bugs’ foul-tasting volatile chemicals (specifically, monoterpene hydrocarbons; Palazzo and Setzer 2009) and aposematic coloration. A Warbling Vireo

(Vireo gilvus) in Virginia in 2012 fed on a crowned slug moth caterpillar (Isa textula), a species defended by painful urticating hairs. Scarlet Tanagers (Piranga olivacea),

Summer Tanagers (Piranga rubra), and Western Tanagers (Piranga ludoviciana) may be particularly well-adapted for preying on wasps and bees, even those that are noted for having potent venom and aggressive stinging behavior. These tanagers were recorded consuming bald-faced hornets (Dolichovespula maculata), yellowjackets in the genus Vespula, honey bees (Apis mellifera), and northern paper wasps (Polistes fuscatus).

Many of the contributed photos demonstrate that birds eat invasive insect species, however, I consider the prevalence of invasive insects among submitted photos too low to suggest that birds specialize on them or prey upon them heavily enough to exercise population control. Observed invasive insect species included gypsy moth

(Lymantria dispar), brown marmorated stink bugs (Halyomorpha halys), Chinese praying mantises (Tenodera sinensis), European praying mantises (Mantis religiosa),

Japanese beetles (Popillia japonica), Oriental beetles (Anomala orientalis), European honey bees (Apis mellifera), European hornets (Vespa crabro), and Asian lady beetles

(Harmonia axyridis). The relative scarcity of these species in submitted photos lends support to the widely held view that vertebrate predators do not make successful biological control agents (Wodzicki 1981, Howarth 1991).

The community science approach of this study allowed for data collection across an enormous geographic area and phylogenetic diversity of birds that

likely would not have been possible using more traditional (i.e., field biology) methods.

The same technique could be applied to other regions and other study organisms. Web- sourced images are becomingly increased recognized as valuable data sets for ornithological research (e.g., Naude et al. 2019); community science social networks such as iNaturalist will likely continue to streamline the process of data collection, making it increasingly easier to aggregate data from thousands of individual users. The data gleaned from crowdsourced photographs of birds with prey could potentially provide a more accurate and up-to-date reference of bird diets than is available for many species in the historic literature and paves the way for future research to assess if breeding bird diets have changed or will change over time. Moreover, this study demonstrates that community science can be effectively applied to complex problems across broad spatial scales.

Chapter 4

ANALYSIS OF CAROTENOID CONTENT IN ARTHROPODS

4.1 Introduction Having established that breeding birds forage more heavily on certain arthropod groups than others (see Chapter 1 and Chapter 3 for more detail), and having demonstrated that birds exercise preferences for certain insect taxa rather than preying on insects that are most abundant (see Chapter 2), the next step was to investigate why some arthropod taxa are favored over others. Past authors (e.g.,

Barker et al. 1998, Sillanpää et al. 2008, Razeng and Watson 2015) have suggested that prey size, prey mobility, moisture content, and nutritional content are important factors to consider. Macronutrients (fats, proteins) and micronutrients (trace elements) in many arthropod taxa have been measured in past studies (e.g., Bukkens 1997, Finke

2002). However, a nutritional component of arthropod prey that merits further investigation is the quantity of various carotenoids.

Carotenoids are fat-soluble pigments composed of hydrogen and carbon. They play important roles in animal coloration, immune function, color vision, and DNA repair (Biard et al. 2006, Sillanpää et al. 2008). They are also essential nutrients in animals’ diets, but vertebrates lack the ability to biosynthesize them. Birds must obtain carotenoids either directly from plants, from arthropods that feed upon plants, or

(rarely) from insects (e.g., aphids; Moran and Jarvik 2010) that biosynthesize carotenoids directly. The 750-plus carotenoids that have been described to date are broadly classified as either carotenes (e.g., beta-carotene) or xanthophylls (e.g., lutein; reviewed by Svensson and Wong 2010).

Numerous studies (e.g., Brush 1990, Gray 1996) have shed light on the importance of carotenoid pigments in avian coloration. Carotenoid pigments produce many of the brilliant red, orange, and yellow hues in birds’ plumage, and are often misconstrued as the primary or sole mechanism by which those hues could arise, but research has shown that the relationship between pigments and resulting hues is complex. McGraw et al. (2004) demonstrated that while yellow feathers from

American Goldfinches are rich in carotenoids, yellow and red feathers from Eastern

Bluebirds, Barn Swallows, King Penguins, Macaroni Penguins, and domestic chickens lack carotenoids and were instead rich in eumelanins and phaeomelanins. Pteridine pigments, red hemoglobin, and psittacofulvins can also produce red and yellow coloration (reviewed by McGraw et al. 2005). While many authors (e.g., Brush 1990,

Gray 1996) report that other colors are typically produced by different pigments (e.g., melanins produce brown, black, gray, and dull red; porphyrins produce brown, blue, and green) or structurally (white, blue, and iridescent), carotenoids can, in fact, help to produce purple, green, and blue hues when complexed with proteins to form carotenoproteins (Ong and Tee 1992), further adding to pigment complexity.

Perez-Rodriguez and Vinuela (2008) suggest that carotenoid-based secondary sexual traits may signal birds’ foraging abilities, a factor in mate value, as carotenoid-

rich foods may be limited in the environment; indeed, past work has shown that intraspecific differences in plumage coloration are due to diet, not genetics (Slagsvold and Lifjeld 1985). More generally, coloration helps to advertise male birds’ overall health to prospective mates and thus plays a critical role in reproductive success

(McGraw and Ardia 2003). Carotenoids also play a role in the coloration of nestlings’ gapes (i.e., mouth and flange; Hunt et al. 2003), which has implications for nestling fitness as it could influence parental provisioning rates. It is important to note that even birds that lack carotenoid pigmentation in their plumage rely heavily on carotenoids for a variety of physiological functions and sequester carotenoids elsewhere in the body (e.g., circulating in the plasma). Even vultures, which are notably drab in coloration and feed on carotenoid-poor carrion, must acquire carotenoids and are hypothesized to do so via consuming plant matter directly or indirectly through carcass viscera (Blanco et al. 2013). Senar et al. (2010) demonstrated that Great Tits selectively forage on insects that have been enhanced with carotenoids over control insects.

Bright coloration in birds provides what can be called an “honest signal” or

“honest indicator” of a bird’s physical condition (Perez-Rodriguez and Vinuela 2008), as carotenoids have antioxidant and immunoregulatory properties; all else being equal, a bird that appears healthy and bright is likely healthier than its duller conspecifics.

Carotenoids prevent the formation of radicals and quench molecules of singlet oxygen

(reviewed by Svensson and Wong 2010). Findings by McGraw and Ardia (2003) suggest that carotenoid pigments directly boost the immune system. In their study,

male zebra finches whose diets were supplemented with additional carotenoid pigments showed increased immune response compared to controls. Carotenoids also perform anti-cancer activities and stimulate antibacterial abilities in white blood cells

(Chew 1993). Hamilton and Zuk (1982) and Lozano (1994) suggest that carotenoid- dependent signals (i.e., brightly-colored sexual ornaments) may be honest signals of parasite load.

Carotenoids contribute additional positive health impacts. They function as precursors to vitamin A, important in vision. Biard et al. (2006) found that increased carotenoid intake resulted in higher body mass in blue tit and great tit nestlings; body mass at fledging is directly correlated with both immediate post-fledging survival and overwinter survival (Tinbergen and Boerlijst 1990).

Carotenoids are important to arthropods for some of the same reasons they are important to vertebrates. Studies suggest that carotenoids are essential to insect vision and play a role in their growth and development as well (Feltwell et al. 1974). They may additionally aid in camouflage or sexual signaling, as they influence coloration

(Eichenseer et al. 2002). Feltwell et al. (1974) suggest that carotenoids may protect insects from damaging radiation. Sillanpää et al. (2008) note that carotenoids, as antioxidants, protect insects from oxidative stress, and also provide some antipredator defense via aposematism. It has been suggested that carotenoids contribute to chemical defenses in aposematic insects by enhancing the taste and odor of deterrent compounds; however, results from Feltwell et al. (1974) did not confirm this association. Eichenseer et al. (2002) demonstrated that corn earworms (Lepidoptera:

Noctuidae: Helicoverpa zea) that fed upon greater quantities of tomato plants had higher carotenoid levels than individuals that fed upon smaller quantities. Their study also found that carotenoids are unevenly distributed and sequestered in different tissues (e.g., highest levels in testes, lowest levels in integument), suggesting as-yet unexplored physiological functions.

Previous studies have suggested that not all insects are equal in terms of carotenoid content. Feltwell et al. (1974) report that pupae have higher carotenoid levels than adults of the same species, and larvae, in turn, have higher levels than pupae do. These authors also noted that Lepidoptera sequester and store carotenoids more than Coleoptera and Orthoptera do. Arnold et al. (2010) showed that concentrations of some carotenoids (zeaxanthin, alpha-tocopherol) vary seasonally in geometrid caterpillars, while others (lutein, beta-carotene) remain stable. Work by

Eeva et al. (2010) demonstrated that mean concentrations of lutein, beta-carotene, and total carotenoids were highest in Lepidoptera (larvae and adults) and lowest in ants and roaches, with intermediate levels found in beetles, spiders, and sawfly larvae.

Arnold et al. (2010) also found that caterpillars’ carotenoid content exceeded that of spiders.

Carotenoids typically make their way through avian food webs along a plant- insect-bird chain. Sillanpää et al. (2008) found that abundance of caterpillars was an important predictor of carotenoid pigment content in avian tissue. Eeva et al. (1998) found that plumage color in Great Tits was directly correlated with abundance of green larvae (herbivorous caterpillars and larval sawflies), the primary component of

the nestling diet. Bird species whose diets consist of more green larvae obtain more carotenoids compared to birds whose diets have a smaller proportion of lepidopteran larvae (Eeva et al. 2010). The carotenoid profiles of birds’ prey differ from the birds’ own plasma carotenoid profiles, as birds absorb different carotenoids disproportionately. Lutein is readily absorbed and is the dominant carotenoid in birds’ plasma (Eeva et al. 2010). Senar et al. (2010) found that P. major both in captivity and in the wild preferentially fed on lutein-enhanced mealworms, as opposed to control mealworms, demonstrating a specific appetite for carotenoids. This finding illustrates that the nutritional importance of carotenoids is on par with that of other nutrients, such as sodium and calcium, and that birds can discriminate among prey based on prey carotenoid content.

I sought to assess the carotenoid concentrations in a wide variety of invertebrate taxa which have been recorded as avian prey, many of which had not previously been investigated. I predicted that the same patterns in carotenoid content in arthropod taxa collected in Europe (Eeva et al. 2010) would be found in those same groups collected in North America, e.g., higher levels in Lepidoptera than in beetles, spiders, and sawflies. I also predicted that the invertebrate taxa most frequently depredated by birds, as per results in Chapters 2 and 3, such as Lepidoptera and

Orthoptera would have higher carotenoid content than groups that are less frequently depredated, such as Apocrita, Dermaptera, and Opiliones. These heavily-depredated groups are mostly herbivorous, whereas less-frequently depredated groups include a higher percentage of detritivores and predators.

4.2 Materials and Methods Several methods were employed to collect a diversity of insects and other invertebrate prey items of birds. These methods include sweep-netting vegetation, often in combination with use of an aspirator, light trapping using a mercury vapor lamp, hand collecting, digging in soil and leaf litter, and vacuum sampling. The majority of specimens were collected in the Newark, Delaware vicinity. Three species, purchased from pet stores or a biological supply company, were commercially-raised, reared on an artificial diet. In total, 129 specimens representing 63 unique taxa were included in analyses.

Samples were placed live into a -80°C freezer and kept in the dark to prevent degradation. Subsequently, they were removed and identified to lowest possible taxonomic level, weighed, packaged separately in plastic microvials, and shipped overnight on dry ice to the McGraw lab at Arizona State University. At the McGraw lab, samples were freeze-dried, ground into powder, extracted with acetone and injected into the high-performance liquid chromatography (HPLC) system for separation, identification, and quantification of the following carotenoids: lutein, zeaxanthin, beta-cryptoxanthin, beta-carotene, and alpha-carotene.

I performed a Kruskal-Wallace Rank Sum test to compare mean total carotenoid content of arthropod orders for orders with more than 2 samples, and a

Games-Howell post-hoc test to compare pairwise differences among orders. I performed a correlation analysis to determine if a significant relationship exists

between the average carotenoid content of each invertebrate order and the frequency with which that order is depredated by breeding birds (see Chapter 3).

4.3 Results Carotenoid levels of invertebrates representing thirteen major taxonomic groupings (Orthoptera, Mantodea, Dermaptera, Hemiptera, Coleoptera, Lepidoptera,

Hymenoptera: Symphyta, Hymenoptera: Apocrita, Diptera, Araneae, Opiliones,

Diplopoda, and Annelida: Megadrilacea) were quantified. Five main carotenoids were detected across the samples: lutein, zeaxanthin, beta-cryptoxanthin, beta-carotene, and alpha-carotene, plus an unidentified xanthophyll in roughly half of the samples and an unidentified ketocarotenoid in one sample. Mean total carotenoid content differed significantly among taxa (X2 = 40.3, df = 6, p < 0.01). The mean total carotenoid content of Lepidoptera was higher than that of Coleoptera, Apocrita, Araneae, and

Hemiptera.

No other significant differences were found among taxa. Sawfly larvae

(Symphyta) appear to have the highest mean total carotenoid content, but more samples are needed for this to be supported statistically. For species with duplicate samples (i.e., multiple individuals of the same species), within-species variation was generally low. Variation within orders appeared to be much higher, e.g., Orthoptera ranged from a low of 4.2 microgram/gram dry weight to a high of 196.7 μg/g d.w., and

Lepidoptera ranged from 3.9-160.9 μg/g d.w. Carotenoid content appears to be much

higher in larval Lepidoptera (x̄ = 81.1 μg/g d.w.) than in adults (x̄ = 34.8 μg/g d.w.), but I did not test for differences.

Figure 6. Total carotenoid content in examined arthropod taxa; letters denote groups that are similar based on post-hoc comparisons.

Lutein made up approximately 37% of total carotenoid content among all pooled samples, while beta-carotene made up ~20%, zeaxanthin ~15%, beta- cryptoxanthin ~9%, and alpha-carotene ~7%. Lutein was highest in Symphyta and

Lepidoptera, followed by Orthoptera, with much lower levels in all other taxa.

Zeaxanthin was highest in Symphyta and Orthoptera. Beta-cryptoxanthin was generally low across all samples, but with highest levels in Symphyta and Diptera.

Beta-carotene levels were highest in Orthoptera, Symphyta, and Lepidoptera, respectively. Alpha-carotene levels were highest (although relatively low overall) in

Orthoptera, Symphyta, Diptera, and Lepidoptera, in that order. The unidentified xanthophyll was substantially higher in Symphyta than any other group. Crane flies

(Tipulidae) were found to have 25.9 microgram/gram d.w. of an unknown ketocarotenoid, which was absent in all other samples. The table in Appendix C gives the total carotenoid levels and individual carotenoid levels for all invertebrate taxa.

Insects reared on an artificial diet in captivity had lower carotenoid content than wild-caught insects. The mean total carotenoid content in greater waxworms was

0.77 microgram/gram d.w. and for cabbage looper caterpillars it was 0.57 μg/g d.w., compared to an average of 65.8 μg/g d.w. in wild-caught caterpillars. For Jamaican field crickets, it was 2.23 μg/g d.w., compared to a mean of 92.48 μg/g d.w. in wild- caught crickets. Carotenoid content in captive-reared insects was not included in the overall levels given for those taxa.

Carotenoid concentrations in beetles varied greatly. The mean concentration in herbivorous June beetles (Phyllophaga sp.) was much lower than in the predatory ground beetle (Carabidae) and the nectarivorous goldenrod soldier beetle

(Chauliognathus pensylvanicus). Carotenoid content was lowest in the nectarivorous net-winged beetle (Calopteron discrepans).

There is a significant correlation (r = 0.75, df = 10, p < 0.01) between the mean total carotenoid content in invertebrate taxa and the frequency with which birds include them in nestling diets (Fig. 7; see Chapter 3). Lepidopteran caterpillars and sawfly caterpillars (collectively termed green larvae) were the dominant arthropod group in breeding bird prey, followed by orthopterans. These groups were also richest in total carotenoid content. Groups that are relatively underrepresented in or completely absent from the bluebirds’ diet, such as earwigs, true bugs, millipedes, wasps, and harvestmen, in contrast, are marked by a substantially lower overall carotenoid content.

Figure 7. Invertebrate prey prevalence in breeding bird diets compared to total carotenoid content. r = 0.75, df = 10, p < 0.01.

4.4 Discussion The finding that the frequency with which birds provision their nestlings with arthropod groups is correlated with arthropod carotenoid content supports the hypothesis that carotenoids are essential components of bird diets. This is consistent with earlier results (Senar et al. 2010) which found that birds demonstrate a specific appetite (i.e., preference) for carotenoids. Given the numerous health benefits of carotenoids (e.g., Tinbergen and Boerlijst 1990, Biard et al. 2006), it follows that birds need a carotenoid-rich diet, particularly during early growth and development.

The results of this study closely mirror those observed in the earlier study conducted in Europe (Eeva et al. 2010), although total carotenoid content in larval

Lepidoptera was roughly equivalent to Symphyta in this study, rather than much higher. This similarity in the carotenoid levels of Symphyta and Lepidoptera is expected given their close ecological and phenological similarity, i.e., both are herbivorous in diet and most active at the same time of year (spring and summer). This study used the most current and accepted chemical analysis techniques, investigated a higher number of invertebrate taxa and higher number of individual samples, and relied on expert identification of the arthropod prey, with lepidopteran caterpillars and sawfly caterpillars identified to the species level. Eeva et al. (2010) used more generalized taxonomic designations, e.g., they lumped Diptera, Hymenoptera,

Isopoda, Myriapoda, and Gastropoda into one group (“other invertebrates”), whereas this study examined each taxon on an individual basis to allow for finer-scale analyses of their carotenoid concentrations.

The concentrations of total carotenoids observed within each invertebrate group are generally consistent with what is known about their diets. Carotenoids are synthesized by plants, but not by animals (except in rare cases); animals that feed upon plants would be expected to have higher concentrations of carotenoids than animals that prey upon other animals. As predicted, carotenoid content was higher in herbivorous taxa than in detritivorous and predatory taxa. Sawfly caterpillars and lepidopteran caterpillars, the richest in carotenoid content, are recognized as voracious consumers of leaves. The wild-caught crickets, grasshoppers, and katydids were high in carotenoid content as well, reflecting their mostly herbivorous diet.

At the other end of the spectrum, with the lowest total carotenoid concentrations, earthworms and millipedes are epigean detritivores, feeding on decomposing organic matter at the soil-litter interface. Earwigs, which are opportunistic omnivores with a diverse diet, had a moderate total carotenoid concentration. Predatory taxa, i.e., spiders and praying mantises, were also predictably low in carotenoid content (12.1 μg/g d.w. and 5.8 μg/g d.w., respectively). These taxa tend to be generalists, feeding on a variety of invertebrate prey containing varying carotenoid concentrations.

Within the Hemiptera, Cicadidae was lowest in overall carotenoid content

(<0.1 microgram/gram d.w.). As xylem feeders, cicadas would be expected to be nutritionally poor; xylem fluid is known to be particularly low in nutritional content

(Novotny and Wilson 1997). Whereas xylem and phloem are vascular and aid in transport, parenchyma cells are used in nutrient storage and are rich in sugars, making

them more nutritionally rich to insect herbivores. Squash bugs and stink bugs are parenchyma cell feeders and had higher carotenoid content than cicadas.

This study demonstrates that carotenoid content varies widely across different arthropod groups. Breeding birds appear to prey more frequently on arthropod groups with higher average total carotenoid content, perhaps to take advantage of the numerous health impacts that carotenoids offer. It’s apparent that this subject merits further investigation. Future research could include sampling a wider variety of arthropods, perhaps including Odonata, Blattodea, and other groups that were not included in this study, and include more individual samples for each group to increase the power of the statistical tests used.

CONCLUSIONS

The four projects described above significantly expand upon existing knowledge of bird diets. The field project described in Chapter 1 demonstrated that

Lepidoptera, especially in the larval stage, are the most important prey taxa for breeding Eastern Bluebirds in Delaware. The community science project described in

Chapter 3 further demonstrates that Lepidoptera (again, mainly caterpillars) are the most important food group for most terrestrial North American bird families during the breeding season. The prey choice experiments described in Chapter 2 show that foraging birds select prey based on inherent preferences as opposed to the prey’s relative abundance in the environment. Lastly, the carotenoid measurements and statistical analysis in Chapter 4 show a strong relationship between the total carotenoid content of prey groups and those groups’ importance in bird diets.

These results provide important general guidelines for how landscapes can be managed to promote breeding birds. Many studies (e.g., Tallamy and Shropshire 2009,

Burghardt et al. 2010, Narango et al. 2017, Richard et al. 2018) have shown that native plants, on average, support significantly higher species richness and biomass of

Lepidoptera than do non-native plants. Accordingly, minimizing the use of introduced ornamental plants and reducing the load of invasive plant species in natural areas should be important goals for all land managers. It is equally important, however, to

recognize that all native plants do not support Lepidoptera equally; in fact, native plants differ by orders of magnitude in the number of lepidopteran species they support (Tallamy and Shropshire 2009). For example, oaks (Quercus) support 557 species of Lepidoptera in the mid-Atlantic region, whereas tulip poplars

(Liriodendron) support only 21 species and yellowwood (Cladrastris) support none.

Thus, prioritizing the plants that support the most lepidopteran biodiversity is predicted to significantly elevate the carrying capacity of local landscapes for breeding birds. The National Wildlife Federation has launched a web tool

(www.nwf.org/NativePlantFinder/) designed to allow homeowners, land managers, and restoration ecologists in every county in the U.S. to identify the plant genera most likely to produce Lepidoptera for breeding birds.

The recognition of Lepidoptera’s unparalleled importance as a food source for breeding birds should direct conservation attention to the importance of native plants.

The results from these projects highlight an important and currently underutilized avenue for bird conservation efforts that can be applied at any spatial scale. Property owners and land managers can help to reverse bird declines by prioritizing native plant species in natural areas as well as on residential and corporate landscapes.

Understanding the importance of caterpillars in avian food webs gives us a tangible conservation action we can immediately adopt to promote breeding birds.

REFERENCES

Arnold, K.E., Ramsay, S.L., Henderson, L., and Larcombe, S.D. 2010. Seasonal

variation in diet quality: antioxidants, invertebrates, and blue tits Cyanistes

caeruleus. Biological Journal of the Linnean Society 99: 708-717.

Baldwin, S.P., and Kendeigh, S.C. 1927. Attentiveness and inattentiveness in the

nesting behavior of the House Wren. The Auk 44(2): 206-216.

Banko, P., Peck, R., and Leonard, D. 2015. Richness, diversity, and similarity of

arthropod prey consumed by a community of Hawaiian forest birds. Hawai'i

Cooperative Studies Unit Technical Report HCSU-066, University of Hawaii,

Hilo, HI, USA.

Barker, D., Fitzpatrick, M.P., and Dierenfeld, E.S. 1998. Nutrient composition of

selected whole invertebrates. Zoo Biology 17: 123-134.

Baxter, S.D.V., Baxter, R.J., and Risch, T.S. 2006. An unusual prey item found in

an Eastern Bluebird nest. Journal of the Arkansas Academy of Science 60

(article 25) 168.

Bay, M.D. and Carter, W.A. 1997. Use of ground skinks (Scincella lateralis) as food

for nestling Eastern Bluebirds (Sialia sialis) in Oklahoma. Bulletin of the

Texas Ornithological Society 30:23-25.

Beal, F.E.L. 1915. Food of the robins and bluebirds of the United States. U.S.

Department of Agriculture Bulletin 171.

Becker, P.A. 1944. One season of bluebirds. Flicker 16: 62-64.

Bernays, E., and Graham, M. 1988. On the evolution of host specificity in

phytophagous arthropods. Ecology 69(4): 886-892.

Biard, C., Surai, P.F., and Moller, A.P. 2006. Carotenoid availability in diet and

phenotype of blue and great tit nestlings. The Journal of Experimental Biology

209: 1004-1015.

Blancher, P.J., Rosenberg, K.V., Panjabi, A.O., Altman, B., Couturier, A.R.,

Thogmartin, W.E. and the Partners in Flight Science Committee. 2013.

Handbook to the Partners in Flight Population Estimates Database, Version

2.0. PIF Technical Series No 6. http://www.partnersinflight.org/pubs/ts/

Blanco, G., Hornero-Mendez, D., Lambertucci, S.A., Bautista, L.M., Wiemeyer,

G., Sanchez-Zapata, J.A., Garrido-Fernandez, J., Hiraldo, F., and

Donazar, J.A. 2013. Need and seek for dietary micronutrients: Endogenous

regulation, external signaling and food sources of carotenoids in New World

vultures. PLoS ONE 8(6): e65562.

Boogert, N.J., Reader, S.M., and Laland, K.N. 2006. The relation between social

rank, neophobia, and individual learning in starlings. 72(6): 1229-1239.

Braman, S.C., and Pogue, D.W. 2005. Eastern Bluebird provisions nestlings with

flat-headed snake. The Wilson Bulletin 117(1): 100-101.

Brush, A. H. 1990. Metabolism of carotenoid pigments in birds. The FASEB Journal

4(12): 2969-2977.

Bukkens, S.G.F. 1997. The nutritional value of edible insects. Ecology of Food and

Nutrition 36: 287-319.

Burger, J.C., Patten, M.A., Rotenberry, J.T., and Redak, R.A. 1999. Foraging

ecology of the California gnatcatcher deduced from fecal samples. Oecologia

120: 304-310.

Burghardt, K.T., Tallamy, D.W., Philips, C., and Shropshire, K.J. 2010. Non-

native plants reduce abundance, richness, and host specialization in

lepidopteran communities. Ecosphere 1(5): 1-22.

Calver, M.C., and Wooller, R.D. 1982. A technique for assessing the taxa, length,

dry weight and energy content of the arthropod prey of birds. Australian

Wildlife Research 9(2): 293-301.

Chew, B. P. 1993. Role of carotenoids in the immune response. Journal of Dairy

Science 76(9): 2804-2811.

Conner, W.E. 2009. Tiger moths and woolly bears: behavior, ecology, and evolution

of the Arctiidae. Oxford University Press, Oxford and New York.

Connor, E.F., Yoder, J.M., and May, J.A. 1999. Density-related predation by the

Carolina Chickadee, Poecile carolinensis, on the leaf-mining moth, Cameraria

hamadryadella at three spatial scales. Oikos 87(1): 105-112.

Cooke, B.J., and Lorenzetti, F. 2006. The dynamics of forest tent caterpillar

outbreaks in Quebec, Canada. Forest Ecology and Management 226: 110-121.

Cornell, K.L., Kight, C.R., Burdge, R.B., Gunderson, A.R., Hubbard, J.K.,

Jackson, A.K., LeClerc, J.E., Pitts, M.L., Swaddle, J.P., and Cristol, D.A.

2011. Reproductive success of Eastern Bluebirds on suburban golf courses.

The Auk 128(3): 577-586.

Cutting, B., Dieckhoff, C., and Hoelmer, K. (2012). Biological control of the Brown

Marmorated Stink Bug: Prospects and Procedures [PowerPoint slides].

Retrieved from

https://delawareinvasives.net/yahoo_site_admin/assets/docs/B_Cutting_BMSB

_biocontrol.36163617.pdf.

Davis, W.H., Kalisz, P.J., and Wells, R.J. 1994. Eastern bluebirds prefer boxes

containing old nests. Journal of Field Ornithology 65: 250-253.

Eeva, T., Helle, S., Salminen, J-P., and Hakkarainen, H. 2010. Carotenoid

composition of invertebrates consumed by two insectivorous bird species.

Journal of Chemical Ecology 36: 608-613.

Eeva, T., Lehikoinen, E., and Rönkä, M. 1998. Air pollution fades the plumage of

the Great Tit. Functional Ecology 12(4): 607-612.

Ehrlich, P.R., and Raven, P.H. 1964. Butterflies and plants: a study in coevolution.

Evolution 18: 586-608.

Eichenseer, H., Murphy, J. B., and Felton, G.W. 2002. Sequestration of host plant

carotenoids in the larval tissues of Helicoverpa zea. Journal of Insect

Physiology 48.3: 311-318.

Eisner, T., Eisner, M., and Siegler, M. 2005. Secret Weapons: Defenses of Insects,

Spiders, Scorpions, and Other Many-Legged Creatures. Harvard University

Press. Cambridge, Massachusetts. 384 pp.

English, P.A., Green, D.J., and Nocera, J.J. 2018. Stable isotopes from museum

specimens may provide evidence of long-term change in the trophic ecology of

a migratory aerial insectivore. Frontiers in Ecology and Evolution 6:14.

Feltwell, J., and Rothschild, M. 1974. Carotenoids in thirty-eight species of

Lepidoptera. Journal of Zoology 174: 441-465.

Finke, M.D. 2002. Complete nutrient composition of commercially raised

invertebrates used as food for insectivores. Zoo Biology 21: 269-285.

Fitzgerald, T.M., van Stam, E., Nocera, J.J., and Badzinski, D.S. 2014. Loss of

nesting sites is not a primary factor limiting northern Chimney Swift

populations. Population Ecology 56(3): 507-512.

Forister, M.L., Novotny, V., Panorska, A.K., Baje, L., Basset, Y., Butterill, P.T.,

and 32 coauthors. 2015. The global distribution of diet breadth in insect

herbivores. Proceedings of the National Academy of Sciences 112(2): 442-447.

Futuyma, D.J., and Gould, F. 1979. Associations of plants and insects in a deciduous

forest. Ecological Monographs 49: 33-50.

Gaglio, D., Cook, T.R., Connan, M., Ryan, P.G., and Sherley, R.B. 2017. Dietary

studies in birds: testing a non-invasive method using digital photography in

seabirds. Methods in Ecology and Evolution 8: 214-222.

Garrison, R.W., von Ellenrieder, N., and Louton, J.A. 2006. Dragonfly Genera of

the New World: An Illustrated and Annotated Key to the Anisoptera. The

Johns Hopkins University Press, Baltimore and London.

Görres, J.H., and Melnichuk, R.D.S. 2012. Asian Invasive Earthworms of the Genus

Amynthas Kinberg in Vermont. Northeastern Naturalist 19(2): 313-322

Gowaty, P.A., and Plissner, J.H. 2015. “Eastern Bluebird (Sialia sialis).” The Birds

of North America, edited by Paul G. Rodewald. Ithaca: Cornell Lab of

Ornithology. Retrieved from the Birds of North

America: https://birdsna.org/Species-Account/bna/species/easblu

Gray, D. A. 1996. Carotenoids and sexual dichromatism in North American passerine

birds. American Naturalist 148(3): 453-480.

Greenberg, R. 1983. The role of neophobia in determining the degree of foraging

specialization in some migrant warblers. The American Naturalist 122(4): 444-

453.

Greer, G. 2000. Eastern Bluebird brings ring-necked snake to nestlings. Oriole 65: 11.

Gregory, R., Duffy, J.P., Stott, I., Voříšek, P., and Gaston, K.J. 2014. Common

European birds are declining rapidly while less abundant species’ numbers are

rising. Ecology Letters 18(1): 28-36.

Grim, T. 2006. An exceptionally high diversity of hoverflies (Syrphidae) in the food

of the Reed Warbler (Acrocephalus scirpaceus). Biologia 61(2): 235-239.

Hallmann, C.A., Sorg, M., Jongejans, E., Siepel, H., Hofland, N., Schwan, H., W.

Stenmans, A. Müller, H. Sumser, T. Hörren, D. Goulson and de Kroon, H.

2017. More than 75 percent decline over 27 years in total flying insect biomass

in protected areas. PLoS ONE 12(10): e0185809.h

Hamilton, W.D., and Zuk, M. 1982. Heritable true fitness and bright birds: a role for

parasites? Science 218: 384-387.

Hatch, M.I., and Parlanti, K.M. 2009. Do songbirds reduce provisioning rates in

response to a human visit? Journal of the Pennsylvania Academy of Sciences

83(2/3): 77-81.

Hennen, D. Personal communication, April 7, 2018.

Hoover, K., Grove, M., Gardner, M., Hughes, D.P., McNeil, J., and Slavicek, J.

2011. A gene for an extended phenotype. Science 333(6048): 1401.

Howarth, F.G. 1991. Environmental impacts of classical biological control. Annual

Review of Entomology 36: 485-509.

Hunt, S., Kilner, R., Langmore, N. E., and Bennett, A. T. D. 2003. Conspicuous,

ultraviolet-rich mouth colours in begging chicks. Proceedings of the Royal

Society B, Biological Sciences (Supplement) 270: S25-S28.

International Union for Conservation of Nature. 2019. The IUCN Red List of

Threatened Species. Version 2019-1. http://www.iucnredlist.org. Downloaded

on 21 March 2019.

Jaervi, T., Sillen-Tullberg, B., and Wiklung, C. 1981. The cost of being aposematic:

An experimental study of predation on larvae of Papilio machaon by the great

tit Parus major. Oikos 36: 267-272.

Jedlicka, J.A., Vo, A.-T. E., and Almeida, R.P.P. 2017. Molecular scatology and

high-throughput sequencing reveal predominately herbivorous insects in the

diets of adult and nestling Western Bluebirds (Sialia mexicana) in California

vineyards. The Auk 134: 116-127.

Johnson, E.J., Best, L.B., and Heagy, P.A. 1980. Food sampling biases associated

with the “Ligature Method”. The Condor 82(2): 186-192.

Johnson, N.F., and Triplehorn, C.A. 2005. Borror and Delong’s Introduction to the

Study of Insects, 7th edition. Thompson-Brooks Cole, Belmont, California.

Judd, S.D. 1901. The food of nestling birds. Pp. 411-436. In: Yearbook of the

Department of Agriculture 1900. Government Printing Office, Washington,

D.C. 888 pp.

Kaspari, M., and Joern, A. 1993. Prey choice by three insectivorous grassland birds:

Reevaluating opportunism. Oikos 68(3): 414-430.

Kennedy, A.C. 2019. Storeria dekayi (Dekay’s Brown snake) Predation.

Herpetological Review 50(2): 404-405.

Kennedy, A.C., White, III, H.B., and Tallamy, D.W. 2019. Predation of dragonfly

nymphs by passerines. Northeastern Naturalist 26(3): 21-26.

Kennedy, C.H. 1950. The relation of American dragonfly-eating birds to their prey.

Ecological Monographs 20(2): 103-142.

Kleintjes, P.K., and Dahlsten, D.L. 1992. A comparison of three techniques for

analyzing the arthropod diet of Plain Titmouse and Chestnut-backed Chickadee

nestlings. Journal of Field Ornithology 63(3): 276-285.

Kluyver, H.N. 1961. Food consumption in relation to habitat in breeding chickadees.

The Auk 78(4): 532-550.

LeClerc, J.E., Che, J.P.K., Swaddle, J.P., and Cristol, D.A. 2005. Reproductive

success and developmental stability of Eastern Bluebirds on golf courses:

Evidence that golf courses can be productive. Wildlife Society Bulletin 33(2):

483-493.

Leslie, A.J., and Berenbaum, M.R. 1990. Role of the osmeterial gland in swallowtail

larvae (Papilionidae) in defense against an avian predator. Journal of the

Lepidopterists’ Society 44(4): 245-251.

Lozano, G.A. 1994. Carotenoids, parasites, and sexual selection. Oikos 70:309–311.

Mason, E.A. 1944. Parasitism by Protocalliphora and management of cavity-nesting

birds. Journal of Wildlife Management 8: 232-237.

McCormick, S. and Polis, G.A. 1981. Arthropods that prey on invertebrates.

Biological Review 57: 29-58.

McGraw, K. J., and Ardia, D. R. 2003. Carotenoids, immunocompetence, and the

information content of sexual colors: an experimental test. American Naturalist

162(6): 704-712.

McGraw, K.J., Hudon, J., Hill, G.E., and Parker, R.S. 2005. A simple and

inexpensive chemical test for behavioral ecologists to determine the presence

of carotenoid pigments in animal tissue. Behavioral Ecology and Sociobiology

57: 391-397.

McGraw, K.J., Wakamatus, K., Ito, S., Nolan, P.M., Jouventin, P., Dobson, F.S.,

Austic, R.E., Safran, R.J., Siefferman, L.M., Hill, G.E., and Parker, R.S.

2004. You can’t judge a pigment by its color: Carotenoid and melanin content

of yellow and brown feathers in swallows, bluebirds, penguins, and domestic

chickens. The Condor 106: 390-395.

Mellott, R.S., and Woods, P.E. 1993. An improved ligature technique for dietary

sampling in nestling birds. Journal of Field Ornithology 64(2): 205-210.

Meunier, M., and Bedard, J. 1983. Nestling foods of the savannah sparrow.

Canadian Journal of Zoology 62: 23-27.

Moran, N.A., and Jarvik, T. 2010. Lateral transfer of genes from fungi underlies

carotenoid production in aphids. Science 328(5978): 624-627.

Moreby, S. J. and Stoate, C. 2000. A quantitative comparison of neck-collar and

faecal analysis to determine passerine nestling diet. Bird Study 47: 320-331.

Muller, M.S., McWilliams, S.R., Podlesak, D., Donaldson, J.R., Bothwell, H.M.,

and Lindroth, R.L. 2006. Tri-trophic effects of plant defenses: chickadees

consume caterpillars based on host leaf chemistry. Oikos 114: 507-517.

Murphy, M.E., and King, J.R. 1987. Dietary discrimination by molting White-

Crowned Sparrows given diets differing only in sulfur amino acid

concentration. Physiological Zoology 60(2): 279-289.

Nagy, L.R., and Smith, K.G. 1997. Effects of insecticide-induced reduction in

lepidopteran larvae on reproductive success of Hooded Warblers. The Auk

114(4): 619-627.

Narango, D.L., Tallamy, D.W., and Marra, P.P. 2017. Native plants improve

breeding and foraging habitat for an insectivorous bird. Biological

Conservation 213: 42-50.

Narango, D.L., Tallamy, D.W., and Marra, P.P. 2018. Nonnative plants reduce

population growth of an insectivorous bird. Proceedings of the National

Academy of Sciences 115(45): 11549-11554.

Naude, V.N., Smyth, L., Wiedeman, E., Krochuk, B.A., and Amar, A. 2019. Using

web-sourced photography to explore the diet of a declining African raptor, the

Martial Eagle (Polemaetus bellicosus). The Condor 121: 1-9.

Nazdrowicz, N. Personal communication, October 18, 2018.

Nelson, S.B., Coon, J.J., Duchardt, C.J., Fischer, J.D., Halsey, S.J., Kranz, A.J.,

Parker, C.M., Schneider, S.C., Swartz, T.M., and Miller, J.R. 2017.

Patterns and mechanisms of invasive plant impacts on North American birds: a

systematic review. Biological Invasions 19(5): 1547-1563.

Noge, K., Prudic, K.L., and Becerra, J.X. 2012. Defensive roles of (E)-2-alkenals

and related compounds in heteroptera. Journal of Chemical Ecology 38: 1050–

1056.

Nolan, Jr., V., and Wooldridge, D.P. 1962. Food habits and feeding behavior of the

White-Eyed Vireo. The Wilson Bulletin 74(1): 68-73.

North American Bird Conservation Initiative. 2014. The State of the Birds 2014

Report. U.S. Department of Interior, Washington, D.C. 16 pages.

North American Bird Conservation Initiative. 2016. The State of North America’s

Birds 2016. Environment and Climate Change Canada: Ottawa, Ontario. 8

pages.

Novotny, V., and Wilson, M.R. 1997. Why are there no small species among xylem-

sucking insects? Evolutionary Ecology 11(4): 419-437.

Nyffeler, M., Maxwell, M.R., and Remsen, Jr., J.V. 2017. Bird Predation by

Praying Mantises: A Global Perspective. The Wilson Journal of Ornithology

129(2): 331-344.

Nyffeler, M., Şekercioğlu, Ç.H., and Whelan, C.J. 2018. Insectivorous birds

consume an estimated 400-500 million tons of prey annually. The Science of

Nature 105: 47.

O’Brien, T.G., and Kinnaird, M.F. 2008. A picture is worth a thousand words: the

application of camera trapping to the study of birds. Bird Conservation

International 18: 144-162.

Ong, A.S.H., and Tee, E.S. 1992. Natural sources of carotenoids in plants and oils.

Pp. 142-167. In: Packer, L. (ed.). Carotenoids: Part A. Chemistry, Separation,

Quantitation, and Antioxidation, vol. 213. Academic Press, London. 538 pp.

Palazzo, M.C., and Setzer, W.N. 2009. Monoterpene hydrocarbons may serve as

antipredation defensive compounds in Boisea trivitatta, the boxelder bug.

Natural Product Communications 4(4): 457-459.

100

Perez-Rodriguez, L., and Vinuela, J. 2008. Carotenoid-based bill and eye ring

coloration as honest signals of condition: an experimental test in the red-legged

partridge (Alectoris rufa). Naturwissenschaften 95: 821-830.

Peterson, R.T. 1980. A Field Guide to the Birds: A Completely New Guide to All the

Birds of Eastern and Central North America (The Peterson field guide series).

Houghton Mifflin. Boston, Massachusetts.

Pimentel, D., Zuniga, R., and Morrison, D. 2005. Update on the environmental and

economic costs associated with alien-invasive species in the United States.

Ecological Economics 52: 273-288.

Pinkowski, B.C. (1977). Foraging behavior of the eastern bluebird. Wilson Bulletin

89: 404-414.

Pitts, T. D. 1978. Foods of eastern bluebird nestlings in northwest Tennessee. Journal

of the Tennessee Academy of Science 53: 136-139.

Polis, G. 1991. Complex trophic interactions in deserts: an empirical critique of food-

web theory. The American Naturalist 138(1):123-155.

Porter, C. 2011. “Why do earthworms surface after rain?” Scientific American.

https://www.scientificamerican.com/article/why-earthworms-surface-after-

rain/ Accessed 7 January 2019.

101

Puckett, H.L., Brandle, J.R., Johnson, R.J., and Blankenship, E.E. 2009. Avian

foraging patterns in crop field edges adjacent to woody habitat. Agriculture,

Ecosystems and Environment 131: 9-15.

Pyke, G.H., Pulliam, H.R., and Charnov, E.L. 1977. Optimal foraging: A selective

review of theory and tests. The Quarterly Review of Biology 52(2): 137-154.

Qian, H., and Ricklefs, R.E. 2006. The role of exotic species in homogenizing the

North American flora. Ecology Letters 9: 1293-1298.

Ralph, C.P., Nagata, S.E., and Ralph, C.J. 1985. Analysis of droppings to describe

diets of small birds. Journal of Field Ornithology 56(2): 165-174.

Razeng, E. and Watson, D. M. 2015. Nutritional composition of the preferred prey

of insectivorous birds: popularity reflects quality. Journal of Avian Biology 45:

001-008.

Rechten, C., Avery, M., and Stevens, A. 1983. Optimal prey selection: Why do

Great Tits show partial preferences? Animal Behavior 31: 576-484.

Redford, K.H., and Dorea, J.G. 1984. The nutritional value of invertebrates with

emphasis on ants and termites as food for mammals. Journal of Zoology 203:

385-395.

Richard, M., Tallamy, D.W., and Mitchell, A. 2018. Introduced plants reduce

species interactions. Biological Invasions 21: 983-992.

102

Richardson, T.W., Gardali, T., and Jenkins, S. H. 2009. Review and meta-analysis

of camera effects on avian nest success. Journal of Wildlife Management 73:

287-293.

Robel, R.J., Press, B.M., Henning, B.L., Johnson, K.W., Blocker, H.D., and

Kemp, K.E. 1995. Nutrient and energetic characteristics of sweepnet-collected

invertebrates. Journal of Field Ornithology 66(1): 44-53.

Rodenhouse, N.L., and Holmes, R.T. 1992. Results of experimental and natural food

reductions for breeding Black-throated Blue Warblers. Ecology 73(1): 357-

372.

Roland, J., and Embree, D.G. 1995. Biological control of the winter moth. Annual

Review of Entomology 40: 475-492.

Royama, T. 1959. A device of an auto-cinematic food-recorder. Tori 15: 172-176.

Royama, T. 1970. Factors governing the hunting behaviour and selection of food by

the Great Tit (Parus major L.). Journal of Animal Ecology 39(3): 619-668.

Sample, B.E., Cooper, R.J., and Whitmore, R.C. 1993. Dietary shifts among

songbirds from a diflubenzuron-treated forest. The Condor 95(3): 616-624.

Sánchez-Bayo, F., and Wyckhuys, K.A.G. 2019. Worldwide decline of the

entomofauna: A review of its drivers. Biological Conservation 232: 8-27.

Sauer, J.R., Niven, D.K., Hines, J.E., Ziolkowski, Jr, D.J., Pardieck, K.L., Fallon,

J.E., and Link, W.A. 2017. The North American Breeding Bird Survey,

103

Results and Analysis 1966 - 2015. Version 2.07.2017 USGS Patuxent Wildlife

Research Center, Laurel, MD.

Senar, J.C., Møller, A.P., Ruiz, I., Negro, J.J., Broggi, J., and Hohtola, E. 2010.

Specific appetite for carotenoids in a colorful bird. PLoS ONE 5(5): 1-4.

Sherry, T.W., and McDade, L.A. 1982. Prey selection and handling in two

neotropical hover-gleaning birds. Ecology 63(4): 1016-1028.

Sillanpää, S., Salminen, J-P., Lehikoinen, E., Toivonen, E., and Eeva, T. 2008.

Carotenoids in a food chain along a pollution gradient. Science of the Total

Environment 406(1-2): 247-255.

Slagsvold, T., and Lifjeld, J.T. 1985. Variation in plumage colour of the Great Tit

Parus major in relation to habitat, season, and food. Journal of Zoology 206:

321-328.

Stanback, M.T. and Mercadante, A.N. 2009. Eastern Bluebirds provision nestlings

with snakes. Journal of the North Carolina Academy of Science 125(1): 36-37.

Svensson, P.A., and Wong, B.B.M. 2010. Carotenoid-based signals in behavioural

ecology: a review. Behaviour 148(2): 131-189.

Szentkiralyi, F. and Kristin, A. 2002. Lacewings and snakeflies (Neuroptera,

Raphidioptera) as prey for bird nestlings in Slovakian forest habitats. Acta

Zoologica Academiae Scientiarum Hungaricae 48(2): 329-340.

104

Tallamy, D., Ballard, M., and D’Amico, V. 2010. Can alien plants support generalist

insect herbivores? Biological Invasions 12: 2285-2292.

Tallamy, D.W., and Shropshire, K.J. 2009. Ranking Lepidopteran use of native

versus introduced plants. Conservation Biology 23: 941-947.

Tinbergen, J.M. and Boerlijst, M.C. 1990. Nestling weight and survival in

individual great tits (Parus major). Journal of Animal Ecology 59(3): 1113-

1127.

Tinbergen, L. 1960. The natural control of insects in pine woods. I. Factors

influencing the intensity of predation in song birds. Archives Néerlandaises de

Zoologie 13: 265-343.

Tobie, C., Peron, F., and Larose, C. 2015. Assessing food preferences in dogs and

cats: A review of the current methods. Animals 5(1): 126-137. van Strien, A.J., van Swaay, C.A.M., van Strien-van Liempt, W.T.F.H., Poot,

M.J.M., and WallisDeVries, M.F. 2019. Over a century of data reveal more

than 80% decline in butterflies in the Netherlands. Biological Conservation

234: 116-122.

Wagner, D.L. 2005. Caterpillars of Eastern North America. Princeton University

Press. Princeton, New Jersey. 512 pp.

West, G.C. 1973. Foods eaten by tree sparrows in relation to availability during

summer in northern Manitoba. Arctic 26: 7-21.

105

Wheelock, I.G. 1904. Birds of California. A.C. McClurg and Company, Chicago,

Illinois.

Williams, D. (2018 January 24). The Secret Lives of Bluebirds. Retrieved from:

https://extension.psu.edu/the-secret-life-of-bluebirds

Wodzicki, K. 1981. Some nature conservation problems in the South Pacific.

Biological Conservation 21: 5-18.

Zeleny, L. 1977. Song of hope for the bluebird. National Geographic 151: 854-865.

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Appendix A

PAIRED STIMULUS PREFERENCE ASSESSMENT RESULTS

A: Cabbage loopers B: Waxworms C: Mealworms D: Crickets E: Brown marmorated stink bugs (2018 only)

Bold indicates first choice in item selection and higher preference in preference ratio.

2017 Box Tria Item Ratio of Preference Ratio # l # Selection prey 1: prey 2 61 1 A D 1:3 A: 0.08 D: 0.25 61 2 B D 3:4 B: 0.25 D: 0.33 61 3 B C 6:6 B: 0.5 C: 0.5 61 4 A B 6:6 A: 0.5 B: 0.5 61 5 A C 5:5 A: 0.42 C: 0.42 61 6 C D 2:3 C: 0.17 D: 0.25 61 7 A B C D 2:2:3:3 A: 0.17 B: 0.17 C: 0.25 D: 0.25 61 8 C D 6:6 C: 0.5 D: 0.5 61 9 C D 6:6 C: 0.5 D: 0.5 61 10 A D 6:6 A: 0.5 D: 0.5 61 11 A B C D 2:3:3:3 A: 0.17 B: 0.25 C: 0.25 D: 0.25 62 1 B C 6:6 B: 0.5 C: 0.5 62 2 A D 4:5 A: 0.33 D: 0.42 62 3 A B 4:6 A: 0.33 B: 0.5 62 4 C D 6:6 C: 0.5 D: 0.5 62 5 A C 6:6 A: 0.5 C: 0.5 62 6 B D 6:6 B: 0.5 D: 0.5 62 7 A B 6:6 A: 0.5 B: 0.5

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62 8 A B C D 3:2:3:3 A: 0.25 B: 0.17 C: 0.25 D: 0.25 62 9 A D 5:4 A: 0.42 D: 0.33 62 10 B C 6:6 B: 0.5 C: 0.5 62 11 A C 5:6 A: 0.42 C: 0.5 62 12 A B C D 2:3:3:3 A: 0.17 B: 0.25 C: 0.25 D: 0.25 62 13 C D 6:6 C: 0.5 D: 0.5 62 14 A B C D 1:3:3:3 A: 0.08 B: 0.25 C: 0.25 D: 0.25 62 15 B D 5:6 B: 0.42 D: 0.5 62 16 B C 6:6 B: 0.5 C: 0.5 62 17 C D 5:6 C: 0.42 D: 0.5 66 1 C D 1:2 C: 0.08 D: 0.17 66 2 A C 2:1 A: 0.17 C: 0.08 66 3 A B 6:6 A: 0.5 B: 0.5 66 4 A B C D 3:3:2:3 A: 0.25 B: 0.25 C: 0.17 D: 0.25 66 5 A D 6:6 A: 0.5 D: 0.5 66 6 B C 5:6 B: 0.42 C: 0.5 66 7 B D 6:6 B: 0.5 D: 0.5 66 8 A B C D 2:1:3:2 A: 0.17 B: 0.08 C: 0.25 D: 0.17 66 9 A C 5:6 A: 0.42 C: 0.5 66 10 B D 5:5 B: 0.42 D: 0.42 66 11 A B 6:6 A: 0.5 B: 0.5 66 12 A C 6:6 A: 0.5 C: 0.5 66 13 B C 6:6 B: 0.5 C: 0.5 66 14 A B 6:6 A: 0.5 B: 0.5 66 15 A D 6:6 A: 0.5 D: 0.5 66 16 B D 6:6 B: 0.5 D: 0.5 66 17 C D 6:6 C: 0.5 D: 0.5 66 18 A B C D 3:3:3:3 A: 0.25 B: 0.25 C: 0.25 D: 0.25 66 19 A B 6:6 A: 0.5 B: 0.5 72 1 B C 1:3 B: 0.08 C: 0.25 72 2 A B C D 3:2:3:1 A: 0.25 B: 0.17 C: 0.25 D: 0.08 72 3 C D 6:6 C: 0.5 D: 0.5 72 4 B D 6:6 B: 0.5 D: 0.5 72 5 A C 6:6 A: 0.5 C: 0.5 72 6 B C 6:6 B: 0.5 C: 0.5 72 7 A D 6:6 A: 0.5 D: 0.5 72 8 A B 6:6 A: 0.5 B: 0.5 72 9 B C 5:6 B: 0.42 C: 0.5 72 10 A D 5:6 A: 0.42 D: 0.5 72 11 A C 5:6 A: 0.42 C: 0.5 72 12 A B 5:6 A: 0.42 B: 0.5

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72 13 B C 6:6 B: 0.5 C: 0.5 72 14 A C 4:6 A: 0.33 C: 0.5 77 1 A B 6:5 A: 0.5 B: 0.42 77 2 A C 1:6 A: 0.08 C: 0.5 77 3 C D 5:5 C: 0.42 D: 0.42 77 4 A D 6:5 A: 0.5 D: 0.42 77 5 B C 6:6 B: 0.5 C: 0.5 77 6 A C 5:5 A: 0.42 C: 0.42 77 7 B C 6:6 B: 0.5 C: 0.5 77 8 A B C D 3:3:3:3 A: 0.25 B: 0.25 C: 0.25 D: 0.25 77 9 A B C D 2:3:2:3 A: 0.17 B: 0.25 C: 0.17 D: 0.25 77 10 A C 6:6 A: 0.5 C: 0.5 77 11 A D 6:6 A: 0.5 D: 0.5 77 12 B C 6:6 B: 0.5 C: 0.5 77 13 B D 6:6 B: 0.5 D: 0.5 77 14 A B C D 3:3:3:1 A: 0.25 B: 0.25 C: 0.25 D: 0.08 77 15 C D 6:6 C: 0.5 D: 0.5 77 16 C D 6:4 C: 0.5 D: 0.33 77 17 B D 6:6 B: 0.5 D: 0.5 77 18 B C 6:6 B: 0.5 C: 0.5 79 1 B C 5:6 B: 0.42 C: 0.5 79 2 A C 5:6 A: 0.42 C: 0.5 79 3 A B 6:5 A: 0.5 B: 0.42 79 4 B D 6:6 B: 0.5 D: 0.5 79 5 A B C D 2:3:3:2 A: 0.17 B: 0.25 C: 0.25 D: 0.17 79 6 A D 5:6 A: 0.42 D: 0.5 79 7 C D 6:5 C: 0.5 D: 0.42 79 8 A B 6:6 A: 0.5 B: 0.5 79 9 A C 6:6 A: 0.5 C: 0.5 79 10 A B C D 2:3:3:2 A: 0.17 B: 0.25 C: 0.25 D: 0.17 79 11 A D 4:6 A: 0.33 D: 0.5 79 12 C D 6:6 C: 0.5 D: 0.5 79 13 B D 6:6 B: 0.5 D: 0.5 79 14 B C 6:6 B: 0.5 C: 0.5 79 15 A B C D 3:3:3:3 A: 0.25 B: 0.25 C: 0.25 D: 0.25 79 16 A B 6:6 A: 0.5 B: 0.5 79 17 C D 6:5 C: 0.5 D: 0.42 79 18 A D 6:6 A: 0.5 D: 0.5 79 19 A C 6:6 A: 0.5 C: 0.5 79 20 B D 6:5 B: 0.5 D: 0.42 79 21 A D 5:6 A: 0.42 D: 0.5

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80 1 A B C D 3:3:3:3 A: 0.25 B: 0.25 C: 0.25 D: 0.25 80 2 B D 5:4 B: 0.42 D: 0.33 80 3 A D 5:5 A: 0.42 D: 0.42 80 4 B C 3:2 B: 0.25 C: 0.17 80 5 C D 3:6 C: 0.25 D: 0.5 80 6 A C 5:5 A: 0.42 C: 0.42 80 7 A B 6:6 A: 0.5 B: 0.5 80 8 B C 3:4 B: 0.25 C: 0.33 80 9 C D 6:4 C: 0.5 D: 0.33 80 10 B D 6:5 B: 0.5 D: 0.42 80 11 A C 6:5 A: 0.5 C: 0.42 83 1 A B 6:6 A: 0.5 B: 0.5 83 2 A D 6:6 A: 0.5 D: 0.5 83 3 B C 6:6 B: 0.5 C: 0.5 83 4 C D 6:5 C: 0.5 D: 0.42 83 5 B D 6:6 B: 0.5 D: 0.5 83 6 A B C D 3:3:3:3 A: 0.25 B: 0.25 C: 0.25 D: 0.25 83 7 A C 4:5 A: 0.33 C: 0.42 83 8 A B 6:6 A: 0.5 B: 0.5 83 9 A D 6:6 A: 0.5 D: 0.5 83 10 B D 6:6 B: 0.5 D: 0.5 83 11 A B C D 3:3:3:3 A: 0.25 B: 0.25 C: 0.25 D: 0.25 83 12 A C 6:6 A: 0.5 C: 0.5 83 13 A D 6:6 A: 0.5 D: 0.5 83 14 B D 6:6 A: 0.5 D: 0.5 83 15 C D 6:6 C: 0.5 D: 0.5 83 16 A C 6:6 A: 0.5 C: 0.5 83 17 A D 6:6 A: 0.5 D: 0.5 85 1 A D 6:6 A: 0.5 D: 0.5 85 2 B D 6:6 A: 0.5 D: 0.5 85 3 A B C D 3:3:3:3 A: 0.25 B: 0.25 C: 0.25 D: 0.25 85 4 A C 6:6 A: 0.5 C: 0.5 85 5 B C 5:6 B: 0.42 C: 0.5 85 6 A B 5:6 A: 0.42 B: 0.5 85 7 C D 6:6 C: 0.5 D: 0.5 85 8 B C 6:6 B: 0.5 C: 0.5 85 9 B D 6:6 B: 0.5 D: 0.5 85 10 A B C D 3:3:3:3 A: 0.25 B: 0.25 C: 0.25 D: 0.25 85-2 1 A C 3:4 A: 0.25 C: 0.33 85-2 2 A B 6:6 A: 0.5 B: 0.5 85-2 3 C D 6:6 C: 0.5 D: 0.5

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85-2 4 A B C D 3:3:2:3 A: 0.25 B: 0.25 C: 0.17 D: 0.25 85-2 5 A D 6:6 A: 0.5 D: 0.5 85-2 6 C D 6:6 C: 0.5 D: 0.5 85-2 7 B C 6:6 B: 0.5 C: 0.5 85-2 8 A D 5:6 A: 0.42 D: 0.5 85-2 9 A C 5:6 A: 0.42 C: 0.5 85-2 10 B D 6:5 B: 0.5 D: 0.42 85-2 11 C D 6:6 C: 0.5 D: 0.5 85-2 12 A B 6:6 A: 0.5 B: 0.5 85-2 13 A B C D 3:3:3:3 A: 0.25 B: 0.25 C: 0.25 D: 0.25 85-2 14 B C 6:6 B: 0.5 C: 0.5 85-2 15 B C 6:5 B: 0.5 C: 0.42 85-2 16 B D 6:6 B: 0.5 D: 0.5 85-2 17 A B C D 3:3:3:3 A: 0.25 B: 0.25 C: 0.25 D: 0.25 155 trials, n = 10 bluebird pairs

# of times offered: A: 87 B: 87 C: 93 D: 89

# of times preferred (based on 1st choice): A: 7 (8.0%) B: 57 (65.5%) C: 57 (61.3%) D: 34 (38.2%)

Based on first choice, the order of preference is waxworms > mealworms > crickets > cabbage loopers.

2018 Box Trial Item Ratio of Preference Ratio # # Selection prey 1: prey 2 46 1 B C 4:4 B: 0.33 C: 0.33 46 2 A C 6:6 A: 0.5 C: 0.5 58 1 B C 6:6 B: 0.5 C: 0.5 58 2 A E 5:3 A: 0.42 E: 0.25 58 3 A B C D E 0:3:2:1:2 A: 0 B: 0.2 C: 0.13 D: 0.07 E: 0.13 58 4 A B 5:6 A: 0.42 B: 0.5

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58 5 A D 2:4 A: 0.17 D: 0.33 58 6 C E 6:5 C: 0.5 E: 0.42 59 1 D E 2:0 D: 0.17 E: 0 59 2 A B 1:6 A: 0.08 B: 0.5 59 3 C D 6:6 C: 0.5 D: 0.5 59 4 A B 5:6 A: 0.42 B: 0.5 59 5 A C 5:6 A: 0.42 C: 0.5 59 6 B D 6:6 B: 0.5 D: 0.5 59 7 A B 6:6 A: 0.5 B: 0.5 59 8 A B C D E 3:3:3:3:3 A: 0.2 B: 0.2 C: 0.2 D: 0.2 E: 0.2 59 9 A E 6:5 A: 0.5 B: 0.42 59 10 B C 1:1 B: 0.08 B: 0.08 66 1 B E 6:5 B: 0.5 E: 0.42 66 2 A B C D E 3:3:3:3:3 A: 0.2 B: 0.2 C: 0.2 D: 0.2 E: 0.2 66 3 B C 6:6 B: 0.5 C: 0.5 66 4 A C 6:6 A: 0.5 C: 0.5 66 5 B D 6:6 B: 0.5 D: 0.5 66 6 B C 6:6 B: 0.5 C: 0.5 66 7 B C 6:6 B: 0.5 C: 0.5 66 8 A D 6:6 A: 0.5 D: 0.5 66 9 C D 6:6 C: 0.5 D: 0.5 66 10 A B 5:6 A: 0.42 B: 0.5 66 11 C D 6:6 C: 0.5 D: 0.5 69 1 A C 4:3 A: 0.33 C: 0.25 69 2 B E 1:0 B: 0.08 E: 0 69 3 A D 6:5 A: 0.5 D: 0.42 69 4 A D 6:6 A: 0.5 D: 0.5 69 5 B C 6:6 B: 0.5 C: 0.5 69 6 C E 5:5 C: 0.42 E: 0.42 69 7 A E 6:6 A: 0.5 E: 0.5 69 8 C D 6:6 C: 0.5 D: 0.5 69 9 A B C D E 3:3:3:3:2 A: 0.2 B: 0.2 C: 0.2 D: 0.2 E: 0.13 69 10 A B 5:6 A: 0.42 B: 0.5 69 11 B D 5:6 B: 0.42 D: 0.5 69 12 A C 5:4 A: 0.42 C: 0.33 69 13 D E 6:6 D: 0.5 E: 0.5 72 1 B C 6:4 B: 0.5 C: 0.33 72 2 C D 6:6 C: 0.5 D: 0.5 72 3 A D 6:6 A: 0.5 D: 0.5 72 4 D E 6:6 D: 0.5 E: 0.5

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72 5 B C 6:6 B: 0.5 C: 0.5 72 6 A B C D E 3:3:3:3:3 A: 0.2 B: 0.2 C: 0.2 D: 0.2 E: 0.2 72 7 B D 5:5 B: 0.42 D: 0.42 72 8 B E 6:5 B: 0.5 E: 0.42 72 9 B D 6:6 B: 0.5 D: 0.5 72 10 A B 6:6 A: 0.5 B: 0.5 72 11 A E 6:5 A: 0.5 E: 0.42 72 12 C E 6:6 C: 0.5 E: 0.5 72-2 1 A E 6:3 A: 0.5 E: 0.25 72-2 2 B C 6:6 B: 0.5 C: 0.5 72-2 3 A B 5:6 A: 0.42 B: 0.5 72-2 4 D E 5:6 D: 0.42 E: 0.5 72-2 5 A B 6:6 A: 0.5 B: 0.5 72-2 6 C D 6:5 C: 0.5 D: 0.42 72-2 7 A B C D 3:3:3:3 A: 0.25 B: 0.25 C: 0.25 D: 0.25 72-2 8 B C 6:6 B: 0.5 C: 0.5 72-2 9 A D 6:6 A: 0.5 D: 0.5 73 1 C D 5:6 C: 0.42 D: 0.5 73 2 C E 6:6 C: 0.5 E: 0.5 73 3 B D 6:6 B: 0.5 D: 0.5 73 4 B C 6:5 B: 0.5 C: 0.42 73 5 A B 6:6 A: 0.5 B: 0.5 73 6 A B C D E 3:3:3:3:3 A: 0.2 B: 0.2 C: 0.2 D: 0.2 E: 0.2 73 7 D E 6:5 D: 0.5 E: 0.42 73 8 A B 6:6 A: 0.5 B: 0.5 73 9 A C 6:6 A: 0.5 C: 0.5 73 10 A E 6:3 A: 0.5 E: 0.25 73 11 B E 6:3 B: 0.5 E: 0.25 73-2 1 B E 6:5 B: 0.5 E: 0.42 73-2 2 A C 6:6 A: 0.5 C: 0.5 73-2 3 C D 5:6 C: 0.42 D: 0.5 73-2 4 A D 3:2 A: 0.25 D: 0.17 73-2 5 A E* 0:0 A: 0 E: 0 73-2 6 A B C D E 2:3:3:3:2 A: 0.13 B: 0.2 C: 0.2 D: 0.2 E: 0.13 73-2 7 C E 6:5 C: 0.5 E: 0.42 75 1 B C 6:2 B: 0.5 C: 0.17 75 2 A B 5:6 A: 0.42 B: 0.5 75 3 B D 5:4 B: 0.42 D: 0.33 75 4 A E 6:3 A: 0.5 E: 0.25 75 5 D E 6:3 D: 0.5 E: 0.25 75 6 A D 6:4 A: 0.5 D: 0.33

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80 1 A B* 0:0 A: 0 B: 0 80 2 A D 1:3 A: 0.08 D: 0.25 80 3 A E 4:2 A: 0.33 E: 0.17 80 4 B C 4:3 B: 0.33 C: 0.25 80 5 A B C D E 3:3:3:3:2 A: 0.2 B: 0.2 C: 0.2 D: 0.2 E: 0.13 80 6 C E 6:6 C: 0.5 E: 0.5 80 7 A C 6:6 A: 0.5 C: 0.5 80 8 B E 6:5 B: 0.5 E: 0.42 80 9 C D 6:6 C: 0.5 D: 0.5 80 10 B D 6:6 B: 0.5 D: 0.5 80 11 A D 6:6 A: 0.5 D: 0.5 80 12 D E 6:5 D: 0.5 E: 0.42 80 13 C D 6:6 C: 0.5 D: 0.5 80-2 1 D E 5:4 D: 0.42 E: 0.33 80-2 2 C D 6:6 C: 0.5 D: 0.5 80-2 3 A D 2:2 A: 0.17 D: 0.17 80-2 4 D E 5:1 A: 0.42 E: 0.08 80-2 5 A C 6:6 A: 0.5 C: 0.5 80-2 6 B E 4:1 B: 0.33 E: 0.08 80-2 7 A E 6:1 A: 0.5 E: 0.08 80-2 8 A B 6:6 A: 0.5 B: 0.5 80-2 9 A B C D 3:3:3:3 A: 0.25 B: 0.25 C: 0.25 D: 0.25 80-2 10 C E 6:4 C: 0.5 E: 0.33 80-2 11 B D 6:6 B: 0.5 D: 0.5 80-2 12 A E 4:4 A: 0.33 E: 0.33 84 1 B D 6:5 B: 0.5 D: 0.42 84 2 A C 6:6 A: 0.5 C: 0.5 84 3 A B 6:6 A: 0.5 B: 0.5 84 4 B E 6:6 B: 0.5 E: 0.5 84 5 A E 6:6 A: 0.5 E: 0.5 84 6 B C 6:6 B: 0.5 C: 0.5 * indicates birds did not eat any available prey items

118 trials, n = 13 bluebird pairs

# of times offered: A: 58 B: 57 C: 53 D: 51 E: 44

114

# of times preferred (based on 1st choice): A: 16 (27.6%) B: 41 (71.9%) C: 29 (54.7%) D: 28 (54.9%) E: 1 (2.3%)

Based on first choice, the order of preference is waxworms > crickets > mealworms > cabbage loopers > stink bugs.

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Appendix B

BIRD SPECIES INCLUDED IN THE “WHAT DO BIRDS EAT?” COMMUNITY SCIENCE PHOTO DATABASE

Taxonomic groupings follow designations provided by the American Ornithological Society.

* denotes more than 50 prey records ** denotes more than 100 prey records

Ducks, Geese, and Waterfowl (Anseriformes) 1. Wood Duck (WODU), Aix sponsa 2. White-winged Scoter (WWSC), Melanitta fusca 3. Hooded Merganser (HOME), Lophodytes cucullatus Quails and Allies (Galliformes) 4. Northern Bobwhite (NOBO), Colinus virginianus Grebes (Podicipediformes) 5. Least Grebe (LEGR), Tachybaptus dominicus 6. Pied-billed Grebe (PBGR), Podilymbus podiceps Cuckoos (Cuculiformes) 7. Common Cuckoo (COCU), Cuculus canorus 8. Dark-billed Cuckoo (DBCU), Coccyzus melacoryphus 9. Yellow-billed Cuckoo (YBCU), Coccyzus americanus 10. Mangrove Cuckoo (MACU), Coccyzus minor 11. Black-billed Cuckoo (BBCU), Coccyzus erythropthalmus 12. Greater Roadrunner (GRRO), Geococcyx californianus 13. Groove-billed Ani (GBAN), Crotophaga sulcirostris Swifts and Hummingbirds (Apodiformes) 14. Ruby-throated Hummingbird (RTHU), Archilochus colubris 15. Black-chinned Hummingbird (BCHU), Archilochus alexandri 16. Anna’s Hummingbird (ANHU), Calypte anna 17. Rufous Hummingbird (RUHU), Selasphorus rufus 18. Mangrove Hummingbird (MAHU), Amazilia boucardi Cranes and Rails (Gruiformes) 19. Ridgway’s Rail (RIRA), Rallus obsoletus 20. Sora (SORA), Porzana carolina 21. Purple Gallinule (PUGA), Porphyrio martinicus 22. Sandhill Crane (SACR), Antigone canadensis 23. Whooping Crane (WHCR), Grus americana Plovers, Sandpipers, and Allies (Charadriiformes) 24. Black-necked Stilt (BNST), Himantopus mexicanus 25. Black Oystercatcher (BLOY), Haematopus bachmani

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26. Black-bellied Plover (BBPL), Pluvialis squatarola 27. Wilson’s Plover (WIPL), Charadrius wilsonia 28. Semipalmated Plover (SEPL), Charadrius semipalmatus 29. Killdeer (KILL), Charadrius vociferous 30. Whimbrel (WHIM), Numenius phaeopus 31. Long-billed Curlew (LBCU), Numenius americanus 32. Ruddy Turnstone (RUTU), Arenaria interpres 33. Red Knot (REKN), Calidris canutus 34. Sanderling (SAND), Calidris alba 35. Buff-breasted Sandpiper (BBSA), Calidris subruficollis 36. Wilson’s Snipe (WISN), Gallinago delicata 37. Spotted Sandpiper (SPSA), Actitis macularius 38. Solitary Sandpiper (SOSA), Tringa solitaria 39. Lesser Yellowlegs (LEYE), Tringa flavipes 40. Willet (WILL), Tringa semipalmata 41. Franklin’s Gull (FRGU), Leucophaeus pipixcan 42. Ring-billed Gull (RBGU), Larus delawarensis 43. Western Gull (WEGU), Larus occidentalis 44. Yellow-footed Gull (YFGU), Larus livens 45. California Gull (CAGU), Larus californicus 46. Herring Gull (HERG), Larus argentatus 47. Great Black-backed Gull (GBBG), Larus marinus 48. Whiskered Tern (WHST), Chlidonias hybrida Loons (Gaviiformes) 49. Common Loon (COLO), Gavia immer Herons, Ibises, and Allies (Pelecaniformes) 50. American Bittern (AMBI), Botaurus lentiginosus 51. Least Bittern (LEBI), Ixobychus exilis 52. Great Blue Heron (GBHE), Ardea herodias 53. Great Egret (GREG), Ardea alba 54. Snowy Egret (SNEG), Egretta thula 55. Little Blue Heron (LBHE), Egretta caerulea 56. Cattle Egret (CAEG), Bubulcus ibis 57. Green Heron (GRHE), Butorides virescens 58. Yellow-crowned Night Heron (YCNH), Nyctanassa violacea 59. White Ibis (WHIB), Eudocimus albus 60. Glossy Ibis (GLIB), Plegadis falcinellus Birds of Prey (Accipitriformes) 61. Swallow-tailed Kite (STKI), Elanoides forficatus 62. Mississippi Kite (MIKI), Ictinia mississippiensis 63. Common Black Hawk (COBH), Buteogallus anthracinus 64. Red-shouldered (RSHA), Buteo lineatus 65. Red-tailed Hawk (RTHA), Buteo jamaicensis

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Owls (Strigiformes) 66. Eastern Screech Owl (ESOW), Megascops asio 67. Western Screech Owl (WESO), Megascops kennicottii 68. Elf Owl (ELOW), Micrathene whitneyi 69. Burrowing Owl (BUOW), Athene cunicularia 70. Barred Owl (BADO), Strix varia Trogons (Trogoniformes) 71. Black-throated Trogon (BTTR), Trogon rufus 72. Elegant Trogon (ELTR), Trogon elegans Kingfishers (Coraciiformes) 73. Belted Kingfisher (BEKI), Megaceryle alcyon Woodpeckers (Piciformes) 74. Collared Aracari (COAR), Pteroglossus torquatus 75. Red-headed Woodpecker (RHWO), Melanerpes erythrocephalus 76. Acorn Woodpecker (ACWO), Melanerpes formicivorus 77. Gila Woodpecker (GIWO), Melanerpes uropygialis 78. Hoffmann’s Woodpecker (HOWO), Melanerpes hoffmannii 79. Red-bellied Woodpecker (RBWO), Melanerpes carolinus 80. Williamson’s Sapsucker (WISA), Sphyrapicus thyroideus 81. Yellow-bellied Sapsucker (YBSA), Sphyrapicus varius 82. Red-naped Sapsucker (RNSA), Sphyrapicus nuchalis 83. Red-breasted Sapsucker (RBSA), Sphyrapicus ruber 84. *Downy Woodpecker (DOWO), Picoides pubescens 85. Nuttall’s Woodpecker (NUWO), Picoides nuttallii 86. Ladder-backed Woodpecker (LBWO), Dryobates scalaris 87. Hairy Woodpecker (HAWO), Picoides villosus 88. Red-cockaded Woodpecker (RCWO), Picoides borealis 89. American three-toed Woodpecker (ATTW), Picoides dorsalis 90. Northern Flicker (NOFL), Colaptes auratus 91. Pileated Woodpecker (PIWO), Dryocopus pileatus Falcons (Falconiformes) 92. Crested Caracara (CRCA), Caracara cheriway 93. *American Kestrel (AMKE), Falco sparverius 94. Peregrine Falcon (PEFA), Falco peregrinus 95. Merlin (MERL), Falco columbarius Perching Birds (Passeriformes) Tityras and Allies (Tityridae) 96. Masked Tityra (MATI), Tityra semifasciata 97. Gray-collared Becard (GCBE), Pachyramphus major Tyrant Flycatchers (Tyrannidae) 98. Slaty-capped Flycatcher (SLCF), Leptopogon superciliaris 99. Northern Beardless-Tyrannulet (NOBT), Camptostoma imberbe 100. Dusky-capped Flycatcher (DCFL), Myiarchus tuberculifer

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101. Ash-throated Flycatcher (ATFL), Myiarchus cinerascens 102. *Great Crested Flycatcher (GCFL), Myiarchus crinitus 103. La Sagra’s Flycatcher (LSFL), Myiarchus sagrae 104. Great Kiskadee (GKIS), Pitangus sulphuratus 105. Boat-billed Flycatcher (BOBF), Megarynchus pitangua 106. Tropical Kingbird (TRKI), Tyrannus melancholicus 107. Couch’s Kingbird (COKI), Tyrannus couchii 108. Cassin’s Kingbird (CAKI), Tyrannus vociferans 109. Western Kingbird (WEKI), Tyrannus verticalis 110. *Eastern Kingbird (EAKI), Tyrannus tyrannus 111. Gray Kingbird (GRAK), Tyrannus dominicensis 112. Scissor-tailed Flycatcher (STFL), Tyrannus forficatus 113. Olive-sided Flycatcher (OSFL), Contopus cooperi 114. Greater Pewee (GRPE), Contopus pertinax 115. Western Wood-pewee (WEWP), Contopus sordidulus 116. Eastern Wood-pewee (EAWP), Contopus virens 117. Acadian Flycatcher (ACFL), Empidonax virescens 118. Alder Flycatcher (ALFL), Empidonax alnorum 119. Willow Flycatcher (WIFL), Empidonax traillii 120. Least Flycatcher (LEFL), Empidonax minimus 121. Gray Flycatcher (GRFL), Empidonax wrightii 122. Pacific-slope Flycatcher (PSFL), Empidonax difficilis 123. Cordilleran Flycatcher (COFL), Empidonax occidentalis 124. Black Phoebe (BLPH), Sayornis nigricans 125. **Eastern Phoebe (EAPH), Sayornis phoebe 126. Say’s Phoebe (SAPH), Sayornis saya 127. Vermilion Flycatcher (VEFL), Pyrocephalus rubinus Shrikes (Laniidae) 128. *Loggerhead Shrike (LOSH), Lanius ludovicianus 129. Northern Shrike (NSHR), Lanius excubitor Vireos (Vireonidae) 130. *White-eyed Vireo (WEVI), Vireo griseus 131. Cuban Vireo (CUVI), Vireo gundlachii 132. Bell’s Vireo (BEVI), Vireo bellii 133. Gray Vireo (GRVI), Vireo vicinior 134. Hutton’s Vireo (HUVI), Vireo huttoni 135. Yellow-throated Vireo (YTVI), Vireo flavifrons 136. Cassin’s Vireo (CAVI), Vireo cassinii 137. Blue-headed Vireo (BHVI), Vireo solitarius 138. Plumbeous Vireo (PLVI), Vireo plumbeus 139. Philadelphia Vireo (PHVI), Vireo philadelphicus 140. Warbling Vireo (WAVI), Vireo gilvus 141. Red-eyed Vireo (REVI), Vireo oliveaceus

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Jays and Crows (Corvidae) 142. Canada Jay (CAJA), Perisoreus canadensis 143. Steller’s Jay (STJA), Cyanocitta stelleri 144. Blue Jay (BLJA), Cyanocitta cristata 145. Florida Scrub-jay (FLSJ), Aphelocoma coerulescens 146. California Scrub-jay (CASJ), Aphelocoma californica 147. Clark’s Nutcracker (CLNU), Nucifraga columbiana 148. American Crow (AMCR), Corvus brachyrhynchos 149. Common Raven (CORA), Corvus cryptoleucus Larks (Alaudidae) 150. Horned Lark (HOLA), Eremophila alpestris Swallows (Hirundinidae) 151. *Purple Martin (PUMA), Progne subis 152. *Tree Swallow (TRES), Tachycineta bicolor 153. Violet-green Swallow (VGSW), Tachycineta thalassina 154. Northern Rough-winged Swallow (NRSW), Stelgidopteryx serripennis 155. Cliff Swallow (CLSW), Petrochelidon pyrrhonota 156. Barn Swallow (BARS), Hirundo rustica Chickadees and Titmice (Paridae) 157. **Carolina Chickadee (CACH), Poecile carolinensis 158. *Black-capped Chickadee (BCCH), Poecile atricapillus 159. Mountain Chickadee (MOCH), Poecile gambeli 160. Chestnut-backed Chickadee (CBCH), Poecile rufescens 161. Bridled Titmouse (BRTI), Baeolophus wollweberi 162. Oak Titmouse (OATI), Baeolophus inornatus 163. Tufted Titmouse (TUTI), Baeolophus bicolor 164. Black-crested Titmouse (BCTI), Baeolophus atricristatus Penduline Tits (Remizidae) 165. Verdin (VERD), Auriparus flaviceps Bushtits (Aegithalidae) 166. Bushtit (BUSH), Psaltriparus minimus Nuthatches (Sittidae) 167. Red-breasted Nuthatch (RBNU), Sitta canadensis 168. White-breasted Nuthatch (WBNU), Sitta carolinensis 169. Pygmy Nuthatch (PYNU), Sitta pygmaea 170. **Brown-headed Nuthatch (BHNU), Sitta pusilla Treecreepers (Certhiidae) 171. Brown Creeper (BRCR), Certhia americana Wrens (Troglodytidae) 172. Rock Wren (ROWR), Salpinctes obsoletus 173. **House Wren (HOWR), Troglodytes aedon 174. Winter Wren (WIWR), Troglodytes hiemalis

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175. Marsh Wren (MAWR), Cistothorus palustris 176. *Carolina Wren (CARW), Thryothorus ludovicianus 177. Bewick’s Wren (BEWR), Thryomanes bewickii 178. Sedge Wren (SEWR), Cistothorus platensis 179. Cactus Wren (CACW), Campylorhynchus brunneicapillus Gnatcatchers (Polioptilidae) 180. *Blue-gray Gnatcatcher (BGGN), Polioptila caerulea 181. California Gnatcatcher (CAGN), Polioptila californica 182. Black-tailed Gnatcatcher (BTGN), Polioptila melanura Dippers (Cinclidae) 183. American Dipper (AMDI), Cinclus mexicanus Kinglets (Regulidae) 184. Golden-crowned Kinglet (GCKI), Regulus satrapa 185. Ruby-crowned Kinglet (RCKI), Regulus calendula Old World Warblers (Sylviidae) 186. Wrentit (WREN), Chamaea fasciata Old World Flycatchers (Muscicapidae) 187. Bluethroat (BLUE), Luscinia svecica 188. White-rumped Shama (WRSH), Copsychus malabaricus 189. Northern Wheatear (NOWH), Oenanthe oenanthe Thrushes (Turdidae) 190. **Eastern Bluebird (EABL), Sialia sialis 191. *Western Bluebird (WEBL), Sialia mexicana 192. *Mountain Bluebird (MOBL), Sialia currucoides 193. Townsend’s Solitaire (TOSO), Myadestes townsendi 194. Veery (VEER), Catharus fuscescens 195. Bicknell’s Thrush (BITH), Catharus bicknelli 196. Swainson’s Thrush (SWTH), Catharus ustulatus 197. Hermit Thrush (HETH), Catharus guttatus 198. Wood Thrush (WOTH), Hylocichla mustelina 199. **American Robin (AMRO), Turdus migratorius 200. Varied Thrush (VATH), Ixoreus naevius Mockingbirds, Thrashers, and Allies (Mimidae) 201. *Gray Catbird (GRCA), Dumetella carolinensis 202. Curve-billed Thrasher (CBTH), Toxostoma curvirostre 203. Brown Thrasher (BRTH), Toxostoma rufum 204. Long-billed Thrasher (LBTH), Toxostoma longirostre 205. California Thrasher (CATH), Toxostoma redivivum 206. Sage Thrasher (SATH), Oreoscoptes montanus 207. Tropical Mockingbird (TRMO), Mimus gilvus 208. *Northern Mockingbird (NOMO), Mimus polyglottos Starlings and allies (Sturnidae) 209. European Starling (EUST), Sturnus vulgaris

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Waxwings (Bombycillidae) 210. Cedar Waxwing (CEWA), Bombycilla cedrorum Silky-Flycatchers (Ptiliogonatidae) 211. Phainopepla (PHAI), Phainopepla nitens Old World Sparrows (Passeridae) 212. House Sparrow (HOSP), Passer domesticus Pipits (Motacillidae) 213. American Pipit (AMPI), Anthus rubescens Finches and allies (Fringillidae) 214. Evening Grosbeak (EVGR), Coccothraustes vespertinus 215. House Finch (HOFI), Haemorhous mexicanus 216. Lesser Goldfinch (LEGO), Spinus psaltria 217. American Goldfinch (AMGO), Spinus tristis New World Warblers (Parulidae) 218. Ovenbird (OVEN), Seiurus aurocapilla 219. Worm-eating Warbler (WEWA), Helmitheros vermivorum 220. Louisiana Waterthrush (LOWA), Parkesia motacilla 221. Northern Waterthrush (NOWA), Parkesia noveboracensis 222. Golden-winged Warbler (GWWA), Vermivora chrysoptera 223. Blue-winged Warbler (BWWA), Vermivora cyanoptera 224. *Black-and-white Warbler (BAWW), Mniotilta varia 225. **Prothonotary Warbler (PROW), Protonotaria citrea 226. Tennessee Warbler (TEWA), Oreothlypis peregrine 227. Orange-crowned Warbler (OCWA), Oreothlypis celata 228. Lucy’s Warbler (LUWA), Oreothlypis luciae 229. Nashville Warbler (NAWA), Oreothlypis ruficapilla 230. Mourning Warbler (MOWA), Geothlypis philadelphia 231. Kentucky Warbler (KEWA), Geothlypis formosa 232. *Common Yellowthroat (COYE), Geothlypis trichas 233. Hooded Warbler (HOWA), Setophaga citrina 234. American Redstart (AMRE), Setophaga ruticilla 235. Kirtland’s Warbler (KIWA), Setophaga kirtlandii 236. Cape May Warbler (CMWA), Setophaga tigrina 237. Cerulean Warbler (CERW), Setophaga cerulea 238. Northern Parula (NOPA), Setophaga americana 239. Magnolia Warbler (MAWA), Setophaga magnolia 240. Bay-breasted Warbler (BBWA), Setophaga castanea 241. Blackburnian Warbler (BLBW), Setophaga fusca 242. *Yellow Warbler (YEWA), Setophaga petechial 243. Chestnut-sided Warbler (CSWA), Setophaga petechial 244. Blackpoll Warbler (BLPW), Setophaga striata 245. **Black-throated Blue Warbler (BTBW), Setophaga caerulescens

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246. Palm Warbler (PAWA), Setophaga palmarum 247. Pine Warbler (PIWA), Setophaga pinus 248. *Yellow-rumped Warbler (YRWA), Setophaga coronata 249. Yellow-throated Warbler (YTWA), Setophaga dominica 250. Prairie Warbler (PRAW), Setophaga discolor 251. Black-throated Gray Warbler (BTYW), Setophaga nigrescens 252. Townsend’s Warbler (TOWA), Setophaga townsendi 253. Golden-cheeked Warbler (GCWA), Setophaga chrysoparia 254. Black-throated Green Warbler (BTNW), Setophaga virens 255. Canada Warbler (CAWA), Cardellina canadensis 256. Wilson’s Warbler (WIWA), Cardellina pusilla 257. Red-faced Warbler (RFWA), Cardellina rubrifrons 258. Painted Redstart (PARE), Myioborus pictus New World Sparrows and Allies (Passerellidae) 259. Olive Sparrow (OLSP), Arremonops rufivirgatus 260. Spotted Towhee (SPTO), Pipilo maculatus 261. Eastern Towhee (EATO), Pipilo erythrophthalmus 262. Rufous-crowned Sparrow (RCSP), Aimophila ruficeps 263. Canyon Towhee (CANT), Melozone fusca 264. California Towhee (CALT), Melozone crissalis 265. Abert’s Towhee (ABTO), Melozone aberti 266. Botteri’s Sparrow (BOSP), Peucaea botterii 267. Bachman’s Sparrow (BACS), Peucaea aestivalis 268. Chipping Sparrow (CHSP), Spizella passerina 269. Clay-colored Sparrow (CCSP), Spizella pallida 270. Brewer’s Sparrow (BRSP), Spizella breweri 271. Field Sparrow (FISP), Spizella pusilla 272. Vesper Sparrow (VESP), Pooecetes gramineus 273. Lark Sparrow (LASP), Chondestes grammacus 274. Black-throated Sparrow (BTSP), Amphispiza bilineata 275. Sagebrush Sparrow (SABS), Artemisiospiza nevadensis 276. Lark Bunting (LARB), Calamospiza melanocorys 277. Savannah Sparrow (SAVS), Passerculus sandwichensis 278. Grasshopper Sparrow (GRSP), Ammosdramus savannarum 279. Henslow’s Sparrow (HESP), Centronyx henslowii 280. Saltmarsh Sparrow (SALS), Ammospiza caudacuta 281. Fox Sparrow (FOSP), Passerella iliaca 282. *Song Sparrow (SOSP), Melospiza melodia 283. Lincoln’s Sparrow (LISP), Melospiza lincolnii 284. Swamp Sparrow (SWSP), Melospiza georgiana 285. White-throated Sparrow (WTSP), Zonotrichia albicolis 286. White-crowned Sparrow (WCSP), Zonotrichia leucophrys 287. Golden-crowned Sparrow (GCSP), Zonotrichia atricapilla

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288. **Dark-eyed Junco (DEJU), Junco hyemalis 289. Yellow-eyed Junco (YEJU), Junco phaeonotus Cardinals, Grosbeaks, and Allies (Cardinalidae) 290. Hepatic Tanager (HETA), Piranga flava 291. Summer Tanager (SUTA), Piranga rubra 292. Scarlet Tanager (SCTA), Piranga olivacea 293. Western Tanager (WETA), Piranga ludoviciana 294. Red-crowned Ant Tanager (RCAT), Habia rubica 295. *Northern Cardinal (NOCA), Cardinalis cardinalis 296. Pyrrhuloxia (PYRR), Cardinalis sinuatus 297. Rose-breasted Grosbeak (RBGR), Pheucticus ludovicianus 298. Black-headed Grosbeak (BHGR), Pheucticus melanocephalus 299. Blue Grosbeak (BLGR), Passerina caerulea 300. Lazuli Bunting (LABU), Passerina amoena 301. Indigo Bunting (INBU), Passerina cyanea 302. Varied Bunting (VABU), Passerina versicolor 303. Painted Bunting (PABU), Passerina ciris 304. Dickcissel (DICK), Spiza americana Icteriidae 305. Yellow-breasted Chat (YBCH), Icteria virens Blackbirds and Allies (Icteridae) 306. Bobolink (BOBO), Dolichonyx oryzivorus 307. Eastern Meadowlark (EAME), Sturnella magna 308. Western Meadowlark (WEME), Sturnella neglecta 309. Bahama Oriole (BAHO), Icterus northropi 310. Orchard Oriole (OROR), Icterus spurius 311. Hooded Oriole (HOOR), Icterus cucullatus 312. Bullock’s Oriole (BUOR), Icterus bullockii 313. Baltimore Oriole (BAOR), Icterus galbula 314. **Red-winged Blackbird (RWBL), Agelaius phoeniceus 315. Tricolored Blackbird (TRBL), Agelaius tricolor 316. Brown-headed Cowbird (BHCO), Molothrus ater 317. Melodious Blackbird (MEBL), Dives dives 318. Rusty Blackbird (RUBL), Euphagus carolinus 319. Brewer’s Blackbird (BRBL), Euphagus cyanocephalus 320. *Common Grackle (COGR), Quiscalus quiscula 321. Boat-tailed Grackle (BTGR), Quiscalus major 322. Great-tailed Grackle (GTGR), Quiscalus mexicanus 323. Yellow-headed Blackbird (YHBL), Xanthocephalus xanthocephalus

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Appendix C

CAROTENOID LEVELS IN INVERTEBRATE TAXA

Carotenoid Concentrations in Invertebrate Samples All values in microgram/gram dry weight. * denotes captive-reared taxa. ** denotes presence of unknown ketocarotenoid.

Sampl Higher Lower Taxon Lutein Zeaxa Beta- Beta- Alpha- Xanth Total e # Taxon nthin cryptox carotene carotene ophyll anthin 25A- Orthoptera Acrididae 17 19.47 6.97 0.00 19.72 11.09 0 57.26 25B- Orthoptera Acrididae 17 10.96 3.12 0.00 18.52 4.80 0 37.41 1A-18 Orthoptera Gryllidae 93.85 31.34 0.19 63.41 6.92 1.02 196.73 1B-18 Orthoptera Gryllidae 1.86 0.19 0.09 1.73 0.29 0.03 4.18 1C-18 Orthoptera Gryllidae 31.69 13.03 0.28 25.09 2.72 3.73 76.53 35-17 Orthoptera Gryllidae: Gryllus 8.91 3.15 2.19 15.44 2.75 0 32.44 2A- Orthoptera Gryllidae: 18* Gryllus assimilis 2.36 0.78 0.05 1.25 0.19 0.59 5.21 2B- Orthoptera Gryllidae: 18* Gryllus assimilis 0.11 0.04 0.00 0.45 0.02 0.04 0.65 2C- Orthoptera Gryllidae: 18* Gryllus assimilis 0.46 0.09 0.00 0.22 0.03 0.03 0.84 3A-18 Orthoptera Tettigoniidae: Conocephalus 11.81 4.75 2.76 0.45 0.06 0.02 19.85 3B-18 Orthoptera Tettigoniidae: Conocephalus 10.22 5.54 3.06 0.80 0.03 0.96 20.61 4-18 Orthoptera Tettigoniidae: Microcentrum 4.74 2.28 15.18 2.51 0.14 0.38 25.23 13-17 Orthoptera Tettigoniidae: Orchelimum vulgare 13.46 4.60 4.19 3.52 3.11 0 28.88 6-18 Mantodea Mantidae: Tenodera sinensis 2.29 0.58 0.26 1.50 0.77 0.36 5.75 17-17 Dermaptera Forficulidae: Forficula 5.06 3.19 2.22 2.46 2.14 0 15.07 6A-17 Hemiptera Coreidae: Anasa 9.15 2.64 2.38 2.80 2.58 0 19.54 6B-17 Hemiptera Coreidae: Anasa 7.12 3.86 3.53 4.74 3.67 0 22.93 6C-17 Hemiptera Coreidae: Anasa 9.53 4.32 0.00 6.36 4.12 3.38 27.72 2A-17 Hemiptera Pentatomidae: Halyomorpha halys 2.55 2.80 2.42 2.42 0.00 0 10.19 2B-17 Hemiptera Pentatomidae: Halyomorpha halys 2.16 2.17 2.15 0.00 0.00 0 6.48

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2C-17 Hemiptera Pentatomidae: Halyomorpha halys 3.03 2.41 2.08 2.08 2.07 0 11.68 2D-17 Hemiptera Pentatomidae: Halyomorpha halys 2.46 2.13 2.08 0.00 0.00 0 6.67 2E-17 Hemiptera Pentatomidae: Halyomorpha halys 2.20 2.21 2.08 2.07 0.00 0 8.57 5-18 Hemiptera Cicadidae: Neotibicen tibicen 0.00 0.00 0.07 0.00 0.00 0.00 0.07 3-17 Coleoptera Carabidae 2.98 2.91 3.21 7.01 2.94 0 19.05 24A- Coleoptera Cerambycidae 17 2.47 2.46 0.00 2.46 0.00 0 7.39 24B- Coleoptera Cerambycidae 17 2.57 2.56 0.00 2.58 0.00 0 7.71 24C- Coleoptera Cerambycidae 17 2.07 2.05 2.05 2.04 0.00 0 8.21 24D- Coleoptera Cerambycidae 17 2.22 2.23 0.00 2.25 0.00 0 6.69 24E- Coleoptera Cerambycidae 17 3.03 3.02 0.00 3.00 0.00 0 9.06 4A-17 Coleoptera Cantharidae: Chauliognathus pennsylvanicus 2.59 2.50 2.56 2.78 2.54 2.65 15.61 4B-17 Coleoptera Cantharidae: Chauliognathus pennsylvanicus 2.89 2.86 3.03 3.82 2.95 3.38 18.92 9-18 Coleoptera Elateridae: Limonius 0.19 0.00 0.18 0.16 0.00 0.05 0.58 7-18 Coleoptera Lycidae: Calopteron discrepans 0.00 0.00 2.85 0.00 0.00 0.00 2.85 8A-18 Coleoptera Scarabaeidae: Phyllophaga 0.18 0.04 0.09 0.25 0.03 0.10 0.68 8B-18 Coleoptera Scarabaeidae: Phyllophaga 0.50 0.09 0.27 1.00 0.05 0.33 2.25 8C-18 Coleoptera Scarabaeidae: Phyllophaga 0.19 0.03 0.11 0.66 0.09 0.46 1.53 8D-18 Coleoptera Scarabaeidae: Phyllophaga 0.47 0.04 0.17 1.38 0.15 0.20 2.41 8E-18 Coleoptera Scarabaeidae: Phyllophaga 0.14 0.03 0.07 0.33 0.02 0.02 0.61 1A-17 Lepidoptera Pieridae: (larval) Pieris rapae 71.13 7.74 0.00 18.10 5.64 0 102.62 1B-17 Lepidoptera Pieridae: (larval) Pieris rapae 102.14 6.87 0.00 12.30 4.55 0 125.87 20-17 Lepidoptera Sphingidae: (larval) Eumorpha pandorus 16.95 6.24 0.00 4.21 3.12 0 30.53 21-17 Lepidoptera Sphingidae: (larval) Darapsa myron 14.36 2.74 1.90 2.36 1.86 0 23.21 11-18 Lepidoptera Sphingidae: (larval) Manduca sexta 20.47 0.83 0.00 7.01 0.31 0.00 28.62 17A- Lepidoptera Saturniidae: 18 (larval) Automeris io 43.98 1.81 0.03 5.44 0.36 2.68 54.30

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17B- Lepidoptera Saturniidae: 18 (larval) Automeris io 85.56 4.05 0.00 25.24 2.59 6.77 124.22 28B- Lepidoptera Lasiocampidae: 17 (larval) Malacosoma americanum 57.83 7.34 3.60 18.32 6.18 4.61 97.87 28C- Lepidoptera Lasiocampidae: 17 (larval) Malacosoma americanum 133.01 11.56 2.90 61.75 9.52 3.91 222.65 28D- Lepidoptera Lasiocampidae: 17 (larval) Malacosoma americanum 69.77 8.42 2.01 22.02 4.21 2.42 108.85 15A- Lepidoptera Lasiocampidae: 17 (larval) Malacosoma disstria 19.40 4.13 4.07 5.11 2.75 2.73 38.17 15B- Lepidoptera Lasiocampidae: 17 (larval) Malacosoma disstria 21.73 5.44 6.01 5.31 2.89 2.79 44.18 15C- Lepidoptera Lasiocampidae: 17 (larval) Malacosoma disstria 25.73 5.29 7.10 5.29 3.50 3.41 50.33 15D- Lepidoptera Lasiocampidae: 17 (larval) Malacosoma disstria 12.07 3.60 4.41 3.12 2.57 2.63 28.40 15E- Lepidoptera Lasiocampidae: 17 (larval) Malacosoma disstria 10.19 3.40 3.18 2.94 2.38 2.33 24.43 5A-17 Lepidoptera Erebidae: (larval) Euchaetes egle 97.01 11.70 3.84 41.55 7.38 4.74 166.21 5B-17 Lepidoptera Erebidae: (larval) Euchaetes egle 30.22 8.75 2.51 8.53 2.99 0 53.00 5C-17 Lepidoptera Erebidae: (larval) Euchaetes egle 49.92 10.16 2.48 12.54 3.55 0 78.63 26A- Lepidoptera Erebidae: 17 (larval) Pyrrharctia Isabella 30.50 5.26 0.00 3.98 3.31 0 43.06 26B- Lepidoptera Erebidae: 17 (larval) Pyrrharctia Isabella 5.18 2.57 0.00 2.40 2.37 2.39 14.91 26C- Lepidoptera Erebidae: 17 (larval) Pyrrharctia Isabella 26.53 3.89 0.00 3.53 2.89 0 36.84 26D- Lepidoptera Erebidae: 17 (larval) Pyrrharctia Isabella 24.53 5.47 0.00 10.17 3.93 0 44.11 20-18 Lepidoptera Erebidae: (larval) Hyphantria cunea 34.36 1.53 0.00 3.62 0.32 0.57 40.41 33-17 Lepidoptera Erebidae: (adult) Lascoria ambigualis 16.75 3.45 0.00 3.28 2.29 2.36 28.12 12-18 Lepidoptera Erebidae: (adult) Lophocampa caryae 11.76 0.30 0.11 3.67 0.46 1.32 17.62 13-18 Lepidoptera Erebidae: (adult) Hypercompe scribonia 6.64 0.24 0.01 0.11 0.00 0.01 7.00

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14-18 Lepidoptera Erebidae: (adult) Halysidota harrisii 3.09 0.06 0.06 0.43 0.13 0.11 3.87 11A- Lepidoptera Noctuidae 17 (larval) 8.63 4.55 3.40 13.74 12.56 0 42.89 11B- Lepidoptera Noctuidae 17 (larval) 9.17 6.19 5.75 17.77 15.23 0 54.11 10A- Lepidoptera Noctuidae: 18* (larval) Trichoplusia ni 0.27 0.18 0.06 0.00 0.00 0.00 0.51 10B- Lepidoptera Noctuidae: 18* (larval) Trichoplusia ni 0.36 0.18 0.06 0.00 0.00 0.00 0.59 10C- Lepidoptera Noctuidae: 18* (larval) Trichoplusia ni 0.20 0.16 0.04 0.00 0.00 0.00 0.40 10D- Lepidoptera Noctuidae: 18 (larval)* Trichoplusia ni 0.54 0.21 0.06 0.00 0.00 0.00 0.81 19-17 Lepidoptera Noctuidae: (larval) Acronicta americana 27.79 2.26 1.79 1.97 1.76 0 35.58 16-17 Lepidoptera Noctuidae: (larval) Simyra insularis 53.62 4.56 0.00 9.40 2.56 0 70.14 16-18 Lepidoptera Noctuidae: (adult) Cucullia asteroides 3.97 0.23 0.00 1.21 0.42 0.00 5.82 21-18 Lepidoptera Noctuidae: (larval) Leuconycta diphteroides 21.15 1.34 0.10 1.61 0.36 0.00 24.56 22A- Lepidoptera Notodontidae: 17 (larval) Datana ministra 33.47 3.35 50.59 27.40 3.55 18.53 136.89 22B- Lepidoptera Notodontidae: 17 (larval) Datana ministra 21.53 3.92 51.72 34.56 3.48 20.54 135.75 22C- Lepidoptera Notodontidae: 17 (larval) Datana ministra 35.69 6.78 61.76 23.18 2.85 15.74 146.00 18-17 Lepidoptera Notodontidae: (larval) Schizura unicornis 17.59 6.12 1.32 1.78 1.38 1.37 29.55 18-18 Lepidoptera Notodontidae: (adult) Datana ministra 10.16 3.27 13.67 14.91 1.59 1.63 45.24 7A-17 Lepidoptera Crambidae: (larval) Evergestis rimosalis 52.16 5.49 2.42 6.72 3.58 0 70.37 7B-17 Lepidoptera Crambidae: (larval) Evergestis rimosalis 106.25 11.73 0.00 17.37 6.43 0 141.78 7C-17 Lepidoptera Crambidae: (larval) Evergestis rimosalis 97.77 9.23 0.00 9.99 4.20 0 121.20 7D-17 Lepidoptera Crambidae: (larval) Evergestis rimosalis 63.16 6.57 0.00 4.55 2.73 0 77.02 7E-17 Lepidoptera Crambidae: (larval) Evergestis rimosalis 89.97 9.78 0.00 7.06 3.63 0 110.44 9A-17 Lepidoptera Pyralidae: (larval) Omphalocera munroei 110.04 21.93 0.00 12.81 3.86 9.42 158.08

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9B-17 Lepidoptera Pyralidae: (larval) Omphalocera munroei 84.50 31.35 0.00 12.53 3.80 10.03 142.21 9C-17 Lepidoptera Pyralidae: (larval) Omphalocera munroei 101.61 29.12 0.00 25.18 5.63 20.03 181.57 19A- Lepidoptera Pyralidae: 18* (larval) Galleria mellonella 0.72 0.22 0.00 0.02 0.00 0.00 0.97 19B- Lepidoptera Pyralidae: 18* (larval) Galleria mellonella 0.63 0.19 0.00 0.05 0.00 0.00 0.87 19C- Lepidoptera Pyralidae: 18* (larval) Galleria mellonella 0.34 0.12 0.01 0.00 0.00 0.00 0.47 15-18 Lepidoptera Pyralidae: (adult) Pococera asperatella 19.40 1.14 0.03 5.74 0.49 0.23 27.03 23A- Hymenoptera Tenthredinidae: 17 Macremphytus tarsatus 14.03 6.88 0.00 5.94 2.71 5.54 35.08 23B- Hymenoptera Tenthredinidae: 17 Macremphytus tarsatus 42.71 10.04 0.00 27.24 5.34 29.09 114.41 23C- Hymenoptera Tenthredinidae: 17 Macremphytus tarsatus 14.28 3.40 0.00 6.77 2.18 6.57 33.20 23D- Hymenoptera Tenthredinidae: 17 Macremphytus tarsatus 83.88 39.73 3.96 50.39 9.72 51.86 239.53 22-18 Hymenoptera Argidae: Arge quidia 22.31 14.80 0.48 12.36 2.08 16.62 68.65 10A- Hymenoptera Pamphilidae: 17 Neurotoma fasciata 31.58 13.15 9.44 4.58 2.50 0 61.25 10- Hymenoptera Pamphilidae: 17B Neurotoma fasciata 38.67 17.35 16.25 8.97 3.40 0 84.63 10C- Hymenoptera Pamphilidae: 17 Neurotoma fasciata 45.54 21.83 12.15 8.23 4.54 4.34 96.62 12A- Hymenoptera Vespidae: 17 Vespa crabro 2.32 2.16 2.42 7.21 2.32 0 16.43 12B- Hymenoptera Vespidae: 17 Vespa crabro 1.43 1.40 1.50 1.92 1.39 0 7.64 12C- Hymenoptera Vespidae: 17 Vespa crabro 0.00 1.96 2.12 2.61 2.03 0 8.72 12D- Hymenoptera Vespidae: 17 Vespa crabro 1.95 1.95 2.22 2.72 2.02 0 10.86 12E- Hymenoptera Vespidae: 17 Vespa crabro 2.17 2.17 2.41 3.39 2.23 0 12.38 14-17 Diptera Tipulidae 4.00 4.00 8.64 10.33 4.37 5.98 63.21** 34-17 Diptera Stratiomyidae 3.68 4.93 0.00 2.41 2.16 0 13.18 23A- Araneae 18 1.30 0.78 0.56 0.11 0.19 0.53 3.47 23B- Araneae 18 7.32 1.19 0.89 2.30 0.83 5.04 17.56

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8A-17 Araneae 2.89 2.35 2.39 2.60 2.33 2.37 14.93 8B-17 Araneae 2.54 2.23 2.45 2.45 2.22 2.34 14.23 8C-17 Araneae 3.95 2.31 2.75 3.02 2.20 2.36 16.59 8D-17 Araneae 4.43 2.30 2.49 2.71 2.10 2.20 16.23 8E-17 Araneae 2.84 2.22 2.28 2.24 2.15 2.20 13.94 31-17 Opiliones Sclerosomatidae 2.49 2.42 2.42 2.43 0.00 0 9.76 24-18 Diplopoda Abacionidae 1.83 0.15 0.12 0.45 0.28 0.03 2.87 25-18 Megadrilacea Megascolecidae 0.61 0.12 0.07 0.78 0.88 0.16 2.62

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