An Invasive Paper Wasp, Polistes Dominulus

Home , Apoica pallens, Asian golden weaver, Baya weaver, Belonogaster, Cowbird, European paper wasp

Wasp and Bird Nesting Interactions with special reference to Polistes dominula

Christopher Gene Earley

A Thesis presented to The University of Guelph

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

Guelph, Ontario, Canada

ABSTRACT

WASP AND BIRD NESTING INTERACTIONS

WITH SPECIAL REFERENCE TO POLISTES DOMINULA

Christopher Gene Earley Advisor: University of Guelph, 2013 Professor Gard W. Otis

Polistes dominula and P. fuscatus often nest in bird nest boxes. Potential competition between wasps and birds was studied by removing wasp nests from some boxes. No difference in nesting success of breeding birds was found between boxes with wasp nests and those in which wasp nests were removed. Boxes that never had a wasp nest and boxes from which wasp nests were removed differed greatly in bird occupancy, suggesting that birds detected previous wasp presence.

Some bird species gain protection by nesting near wasp nests. Birds may prefer to nest near wasp species that inflict higher sting pain levels. A rank correlation of data from published studies provided no evidence that pain level influences which wasp nests are most attractive to nesting birds.

A comprehensive table of bird-wasp nesting associations (listing 121 bird species, 28 wasp species and 4 bee species) is included here.

ACKNOWLEDGEMENTS

I would like to thank Dr. Gard W. Otis, my advisor, for all of his support throughout this process. His friendship and instruction is greatly appreciated. I also thank the other members of my committee, Dr. Ryan Norris and Dr. John Wenzel, for their patience as I worked through the part-time aspects of this project. Thanks to Dr. George Gamboa for his help in the initial stages of my research.

None of the field research for this project would have been possible without the help of the many people who assisted with setting up the bird boxes and collecting the data. Thank you to Gustavo Betini, Stephanie Van Ryswyk, Jason Mouland, Joe Crowley, Holly Dodds, Megan

Sellick, Lauren Rae, Ivan Casas and Dr. Ryan Norris. Local bird box monitors David Lamble,

Joe Kral and Bryan Wyatt were incredibly helpful with my project and their support and friendship is gratefully appreciated.

For the sting pain chapter, I thank the wasp researchers who supplied information as well as encouragement and enthusiasm. These include Dr. James Carpenter, Dr. Robert Jeanne, Dr.

Justin Schmidt, Dr. Christopher Starr and Dr. John Wenzel.

I gratefully acknowledge statistical help I received from Lucia Costanzo. As well, thank you to Dr. Shelley Hunt for her encouragement during the final stages of my thesis writing.

Thank you to my examination committee members, Cynthia Scott-Dupree and Ernesto Guzman, for their evaluations and comments during my defense. Dr. Scott-Dupree’s comments on my thesis before the defense were particularly helpful.

Last, but not least, I would like to thank my wife, Dr. Jiffy Gibson, and our children,

Nathan and Skye, for putting up with a grumpy thesis-writer who often took over the whole

iii

dining room table with papers, books and snacks. Your love and support will be cherished forever.

TABLE OF CONTENTS

LIST OF TABLES ...... vii

LIST OF FIGURES ...... viii

ACKNOWLEDGEMENTS ...... iii

CHAPTER 1 GENERAL INTRODUCTION 1.1 Nest-builders ...... 1 1.2 Social wasps and their nests ...... 1 1.3 Birds and their nests ...... 2 1.4 Interactions between nesting wasps and nesting birds ...... 3 1.5 Bird nests near wasp nests ...... 4

CHAPTER 2 AN INVASIVE PAPER WASP, POLISTES DOMINULA, AND ITS EFFECTS ON THE BREEDING SUCCESS OF CAVITY-NESTING BIRDS 2.1 INTRODUCTION ...... 11 2.1.1 Polistes dominula ...... 11 2.1.2 Cavity-nesting birds ...... 13 2.1.3 Competition for cavities ...... 14 2.1.4 Interactions between P. dominula & cavity-nesting birds ...... 15 2.2 MATERIALS AND METHODS ...... 19 2.2.1 Study area and nest boxes ...... 19 2.2.2 Data collection ...... 20 2.2.3 Data analysis ...... 21 2.3 RESULTS AND DISCUSSION ...... 21 2.3.1 Results ...... 21 2.3.2 Use of a box by a wasp and a bird simultaneously ...... 26 2.3.3 Nest box design ...... 27 2.3.4 Conclusion ...... 28

CHAPTER 3 THE INFLUENCE OF WASP STING PAIN LEVEL ON NEST SITE CHOICE BY BIRDS THAT NEST NEAR WASPS 3.1 INTRODUCTION ...... 30 3.1.1 Wasp sting pain level ...... 30 3.1.2 Wasp nest-associating birds ...... 31 3.2 MATERIALS AND METHODS ...... 32 3.3 RESULTS AND DISCUSSION ...... 32

CHAPTER 4 GENERAL DISCUSSION AND CONCLUSION ...... 36

REFERENCES ...... 39

APPENDIX A BIRD-WASP NESTING ASSOCIATIONS ORGANIZED BY BIRD ...... 52

APPENDIX B BIRD-WASP NESTING ASSOCIATIONS ORGANIZED BY WASP ...... 66

LIST OF TABLES

Table 2.1. Nesting attempts in nest boxes by birds (Tree Swallows, Tachycineta bicolor, Eastern

Bluebirds, Sialia sialis and Black-capped Chickadees, Poecile atricapillus) and presence

of Polistes (P. dominula and P. fuscatus) wasp nests in a Guelph, Ontario, Canada study

site ...... 23

Table 2.2. 2 X 2 Contingency Table for Bird Boxes with Wasp Nests (W) and Bird Boxes with

Wasp Nests removed (X) (Fisher’s Exact Test; p=0.26) ...... 23

Table 2.3. 2 X 2 Contingency Table for Wasp Nest Removed (X) boxes and boxes that never

had a wasp nest (Fisher’s Exact test; p=0.01) ...... 24

Table 2.4. 2 X 2 Contingency Table for Bird Boxes with Wasp Nests at some point (both with

wasp nest left intact (W) and with wasp nests removed (X)) and Bird Boxes that never

had a Wasp Nest (Fisher’s Exact Test; p=0.0000004) ...... 25

Table 3.1. Wasp species, Number of bird nests associated with each (Joyce, 1990) and sting pain

levels (Starr, 1985; Schmidt, 1990; Wenzel, unpublished data). Colony size data from

Jeanne (1991) ...... 33

Table 3.2. P and rho values from Spearman Rank Order Correlation showing the relationship

between sting pain level and the number of bird nests near each wasp species’ nests ...... 34

vii

LIST OF FIGURES

Figure 1. A domed bird nest (right) in association with a wasp nest in Northeastern Brazil ...... 6

Figure 2. Polistes dominula ...... 11

Figure 3. Polistes fuscatus ...... 12

Figure 4. Nest box showing triangular opening at the top of one side ...... 20

viii

CHAPTER 1

GENERAL INTRODUCTION

1.1 Nest-builders

While many diverse taxa of animals are able to build structures, three classes are known for the complexity and diversity of their architecture: Arachnida (spiders and mites), Insecta

(insects) and Aves (birds; Hansell 2000). While spiders (order Araneae) build webs primarily as foraging devices (Starr 1991), termites (order Isoptera), ants, bees and wasps (order

Hymenoptera) and birds build nests in which they rear their offspring. These nest-builders are able to manipulate their environment in such a way that their reproductive fitness may increase through the use of a built structure (Hansell 2000).

1.2 Social Wasps and their Nests

For colonial insects such as social wasps, sterile or non-breeding individuals help fertile family members reproduce. The “inclusive fitness” they gain by helping kin allows the non- breeders to have shared genes passed on to future generations (Hamilton 1964 a, b). Individual wasps in a colony interact with one another at their nest which provides the colony with a “stage on which this drama of cooperation and conflict is played” (Starr 1991). And while social wasp species have evolved to utilize over 50 different architectural designs (Wenzel 1991), the primary function of all wasp nests is too contain the brood (immature offspring) so they can be cared for (Jeanne 1977). Each nest is made up of cells where eggs are laid, larvae are fed and pupae reside. Secondary functions of the nest include the following: 1) defense against enemies of the brood; 2) maintenance of favourable physical conditions; 3) serving as the main locus of social interactions; and 4) preservation of the nest’s own structural integrity (Jeanne 1977). The

first of these secondary functions, brood defense, is a spectacular example of how small

invertebrates can be powerful members of their ecosystem. A large number of stinging adults

allows social wasps to defend their nest en masse, even against large vertebrate predators (see

Chapter 3). Even though they are not always successful (Jeanne 1975), the ability to defend their nest against vertebrates is crucial to social wasps because many of the nests are quite

conspicuous and contain quantities of nutritious brood.

1.3 Birds and their Nests

Most bird nests are only used to raise young (Hansell 2000). The nest allows the adults

to brood the eggs at an optimal temperature (Calder and King 1974) and reduce predation of eggs

and young (Hansell 2000). However, after the young leave the nest, many birds do not return,

suggesting that continued use of the nest would increase the risk of ecto-parasites (Moller 1994,

Hansell 2000) and predation. Nest defense of some type by adults will likely decrease risk to the

eggs and young bound to the nest.

Alerstam and Hogstedt (1981) summarized three strategies by which birds defend their

nests from predators: 1) active nest defense; 2) concealment or camouflage; and 3) sheltered

nests. By using active nest defense, large and/or social species can try to stop predators from

getting to eggs or nestlings. These nests tend to be constructed in relatively open sites from

where the parent birds can see approaching predators. Many small birds cannot use this strategy

because they are not powerful enough to stop most nest predators. Sheltered nests, such as those

within cavities, can help protect nesting birds and their broods (see section 2.1.2). Additionally,

by nesting close to more formidable animals, birds can utilize their associates’ defense

mechanisms to help protect their own nests (Haemig 2001; see Appendix A).

1.4 Interactions between Nesting Wasps and Nesting Birds

The shared behaviour of building nests may be one reason that some birds and wasps associate at nesting sites. Both are looking for sites that provide a variety of conditions that may include shelter from the elements, nest attachment site, local nesting materials, camouflage or concealment from potential predators and temperature control (Joyce 1990).

Both birds and wasps may use sites where another species offers protection. For example, in the Neotropics, some wasp species nest in trees occupied by Azteca ants; these ants defend the tree, and consequently the wasps, from army ants (Eciton spp.) which are known to prey upon wasp nests (Jeanne 1991). Some bird species gain protection when their nests are located near Pseudomyrmex ants (Joyce, 1990) or wasps (see Appendix A). Wasp nests sometimes provide attachment points for bird nests. Grimes and Darku (1968) and Weeks (1977) found that many Barn Swallow (Hirundo rustica), Eastern Phoebe (Sayornis phoebe) and White- necked Rockfowl (Picathartes gymnocephalus) nests under concrete bridges and caves were built on the mud nests of sphecid wasps. The established nests of the sphecid wasps allowed the birds to attach their nests where it might not have been otherwise possible. Wasps may also use bird nests as attachment sites. For example, an African Polistes wasp may place its nest at the bottom of colonial White-browed Sparrow-Weaver (Ploceopasser mahali) nests (Keeping, pers. comm. to Hansell 2000). Bologna et al. (2007) have also reported wasps, Belonogaster lateritia

Gerstaecker, building their nests on the bottoms of the colonial nests of the Sociable Weaver,

Philetarius socius, in Namibia. They suggested that this association has benefits to the birds (i.e., the wasps’ presence provides protection) and to the wasps (the wasps being able to prey on flies that are attracted to the birds’ feces).

Birds and wasps may also compete for nesting sites, as may be the case between Polistes

spp. and cavity-nesting birds. Gibo (1980) found that House Wrens apparently compete with

Polistes fuscatus Fabricius for nest sites. Myers (1935) saw an American Kestrel (Falco sparverius, a small falcon that nests in cavities) check an old woodpecker hole in the stump of a palm and fly away. Inside the nest, Myers found a “populous nest” of Polistes canadensis

(Linnaeus).

Many naturalists that monitor bird nest boxes find Polistes dominula (Christ) and P. fuscatus using the boxes. This potential competition for a nest site has received little attention by researchers (Stanback 2009). One part of this thesis explores possible competition for nest boxes by Polistes wasps and cavity-nesting birds.

1.5 Bird Nests near Wasp Nests

Many examples of birds placing their nests near active wasp nests occur throughout the literature (Joyce 1990, Haemig 2001). Birds of at least 9 different orders construct their nests near other “protector” species (Quinn and Ueta 2008). These protector species include (but are not limited to) birds such as falcons (Wiklund 1979, Bogliani et al. 1999, Sergio and Bogliani

2001, Quinn et al. 2003), owls (Summers et al. 1994, Quinn et al 2003, Halme et al. 2004), and gulls (Wheelwright et al. 1997), as well as the social hymenoptera: ants (Grimes 1973, Haemig

1999), wasps and bees (see Appendix A and Appendix B). Additionally, wasps may gain protection themselves by nesting near ants, other wasp species, or other social insects (Starr

1988, Joyce 1990, Jeanne 1991). When examined in detail, these interactions have been shown to usually enhance the breeding success of the protected species. When one or both of the

species are rare, understanding these associations may be important for their conservation

(Haemig 2001).

Gosse (1847) was the first to record a nesting interaction between birds (Yellow-faced

Grassquit, Tiaris olivacea, and Bananaquits, Coereba flaveola) and a wasp (Polistes sp.). Since that time, many observers have noted nesting associations between a variety of wasp and bee species and bird species (Appendix A and Appendix B). Joyce (1990) compiled a list 113 birds species and 19 families that nest in association with colonies of wasps, ants, and bees. I have added to this list (Appendix A) which now includes 121 bird species of 25 families that have been found to have bird-wasp or bird-bee associations. I did not include ants in my research.

Bird names in the list are from Clements (2011). Appendix B reorganizes the data by the wasp/bee species. This includes 28 wasp and 4 bee species.

Most anecdotal observations lack scientific rigour and fail to test whether birds truly choose to nest in proximity to wasps. However, some studies have shown this to be true. Dejean and Fotso (1995) found bird-wasp associations with Polybioides tabidus (Fabricius) and 7 species of birds in Cameroon mango plantations (see Appendix B). They found that trees with wasp nests were 3.3 times more likely to have at least one bird nest in them. They also found a positive correlation between the size of the bird and the distance its nest was from the wasp nest.

This is significant because nesting near an active wasp nest is a risky undertaking and the larger the bird the more likely it would disturb the wasps as it lands on its own nest or any nearby branch. It appears that the wasps gradually become habituated to this movement but the adult birds are still at some risk. For example, Belt (1874 in Myers 1929) found a yellow and brown flycatcher nest beside a wasp nest. He saw the flycatcher dart out of its domed nest and get caught on a nearby thorn. As the bird struggled to free itself, wasps came out of the wasp nest

and attacked the bird, stinging it to death in less than a minute. It is likely that the movement

from the frantic bird was too different from its regular movements and the wasps then perceived

it as a threat (Hindwood 1955).

It is interesting that most birds that nest near wasps build bag-like, domed or roofed nests

(Myers 1929 and 1935, Wunderle and Pollock 1985, Joyce 1990). This likely offers some protection to young and brooding birds from the wasps (Figure 1).

Figure 1. A domed bird nest (right) in association with a wasp nest in Northeastern Brazil.

Photo by Shirley Sekarajasingham.

Considering how many species of birds have been found to nest near wasps, there have been very few experimental or quantitative studies of these interactions. Five studies have looked into the association and found that it lowered the predation of the adult breeding birds and/or their eggs/young (Smith 1968, Robinson 1985, Wunderle and Pollock 1985, Joyce 1990 and 1993, Beier and Tungbani 2006). Smith (1968) studied Chestnut-headed Oropendulas

(Psarocolius wagleri), Crested Oropendulas (Psarocolius decumanus) and Yellow-rumped

Caciques (Cacicus cela) in Panama. Robinson (1985) also studied Yellow-rumped Caciques; he observed wasps (Agelaia flavipennis (Ducke) and Chartergus artifex (Christ)) repel White- fronted Capuchins (Cebus albifrons), Brown Capuchins (Cebus paella) and Squirrel Monkeys

(Saimiri sciureus) in his Peru study site. Only the cacique nests within 0.5 m of the wasp nests received a benefit from being near the wasps.

In a study of Bananaquits (Coereba flaveola), Wunderle and Pollock (1985) showed that the birds have higher nesting success if they nest near a Polybia occidentalis (Olivier) wasp nest.

They determined that some snakes were able to destroy Bananaquit broods that were within 1 m of a wasp nest, possibly because the snake attacked at night and/or moved slowly through the branches.

To study the effects of wasp nests near Rufous-naped Wren (Campylorhynchus rufinucha) nests, Joyce (1993) placed active Polybia rejecta (Fabricius) nests near wren nests that were not associated with a wasp nest. The wrens that subsequently had wasp nests near their own nest had significantly higher fledging success of young than those wrens that had no wasp nest nearby. He attributed this to the deterrence by the wasps of predatory vertebrates, such as

White-faced Monkeys (Cebus capucinus).

Beier and Tungbani (2006) were the first to not only look at the association with respect

to the bird’s reproductive success but also the wasp’s success as well. They found that Red-

cheeked Cordonbleus (Uraeginthus bengalus) in Ghana were twice as likely to fledge young if

their nests were associated with the wasp Ropalidia cincta (Lepeletier) than those without wasps.

Lower predation rates of bird nests near R. cincta nests were the apparent reason for this

difference. The wasps, in contrast, experienced no benefit, making this a commensal association.

One study by Barnard and Markus (1990) showed no benefit to birds nesting near wasps

(Polistes and Ropalidia). They believed that waxbills (specifically Blue-breasted Cordonbleu,

Uraeginthus angolensis, and Melba Finch, Pytilia melba) may use wasp nests as flags, structures that communicate something about their surroundings. Polistes and Ropalidia wasps will not nest in trees with acacia ants (Pseudomyrmex spp.). Ants of this genus are known to swarm over both bird and wasps nests and cause the nest owners to desert. Barnard and Markus (1990) proposed that waxbills use the wasp nests as a sign that ants are not present in a tree. They did not find any difference between survival of waxbill nests associated with wasp nests and those without. However, their data indicate that the waxbills placed their nests an average of 36.9 cm from the wasp nests. It seems unlikely that the finches would place their nests so close to the wasps if they only use the wasp nest as a flag. Beier and Tungbani’s (2006) subsequent study found that another Cordonbleu species does indeed benefit from nesting near wasps (see preceding paragraph).

Birds uncommonly nest inside unoccupied wasp nests. While it is possible that birds use these inactive wasp nests only because the nest provides a cavity site, it is also possible that they benefit from nesting inside a wasp nest because predators may have learned to associate wasp nests (the physical structures) with wasps and consequently avoid them (see Chapter 3). Species

that are known to occasionally nest in abandoned wasp nests include House Wrens (Troglodytes

aedon) (Sanborn 1932) and Carolina Wrens (Thryothorus ludovicianus) (Brooks 1932). The

Violaceous Trogon (Trogon olivaceus) is known to catch wasps, eat them, and usurp the wasp nest for its own nesting activities (Skutch 1942 in Hindwood 1959).

The nesting associations of birds and wasps are extensive and diverse. Most are probably

commensal and a few appear to be parasitic or symbiotic. However, for the vast majority, the

ecology of the relationship remains largely unknown. In Appendix A and Appendix B, I

summarize these nesting associations in hope that this analysis will spark future research into this

fascinating aspect of bird and wasp/bee biology.

Most of the projects that have studied this bird-wasp nesting association phenomenon in depth have concluded that the birds benefit from the relationship (Smith 1968, Robinson 1985,

Wunderle and Pollock 1985, Joyce 1990 and 1993, Beier and Tungbani 2006). The major objective of my research is to have a better understanding of the nesting relationships between birds and wasps. The following are specific objectives:

1. To determine if the presence of Polistes in bird boxes effects the breeding success of

cavity-nesting birds. I hypothesize (HA) that the presence of a Polistes sp. nest has

some effect on the successful breeding of cavity-nesting birds. The null hypothesis is

that the relative proportion of successful bird nesting attempts is the same regardless

of whether a wasp nest is present in the bird box or not.

2. To determine if birds that typically nest in association with wasps do so

preferentially with wasps that have more painful stings. I hypothesize (HA) that birds

will nest more often with wasps that have high sting pain indices. The null

hypothesis is that there is no association between wasp sting pain level and the

frequency at which several bird species construct their nests near wasp nests.

3. To compile a comprehensive list of bird-wasp nesting association observations and

studies in the hopes that it will be useful for future researchers studying this

fascinating aspect of bird and wasp natural history.

CHAPTER 2

AN INVASIVE PAPER WASP, POLISTES DOMINULA, AND ITS EFFECTS ON THE

BREEDING SUCCESS OF CAVITY-NESTING BIRDS.

2.1 INTRODUCTION

2.1.1 Polistes dominula

The European Paper Wasp, Polistes dominula (Vespidae), is a bright yellow and black hymenopteran that is native to Europe, North Africa and Asia (Cervo et al. 2000, Figure 2). This

Figure 2. Polistes dominula. Photo by Glenn Barrett.

species was accidentally introduced to North America in the late 1970’s (Eickwort 1978) and has subsequently become common over a wide area of the continent (Pickett and Wenzel 2000,

Liebert et al. 2006). P. dominula reached southern Ontario in 1997 (Hoebeke and Wheeler

2005) and was found in Guelph in the early 2000’s (Otis pers. comm.1) where it is now

frequently encountered and considered to be an invasive species. Invasive species are defined by

the Government of Canada as “plants, animals, aquatic life and micro-organisms that outcompete

native species when introduced outside of their natural environment and threaten Canada's

Figure 3. Polistes fuscatus. Photo by Chris Earley

1 Dr. Gard Otis, School of Environmental Science, University of Guelph, Ontario, Canada, N1G 2W1, [email protected] 12

ecosystems, economy and society” (Government of Canada, 2009). Many species that are

introduced to new regions either fail to become established or remain at low densities; it is

interesting biologically when an introduced species is able to outcompete a native species that

has adapted to its environment (Allendorf and Lundquist 2003). For example, the native Golden

Paper Wasp (P. fuscatus, Figure 3) has been replaced by P. dominula in parts of its range

(Gamboa et al. 2002; Liebert et al. 2006). Pickett and Wenzel (2000) and Liebert et al. (2006)

have summarized many factors that have contributed to the success of introduced P. dominula.

These include its earlier and higher production of workers; greater nectar storage; higher queen

and worker foraging rates; higher production of gynes and a greater ability to respond to

changing resource abundance. They also suggest that P. dominula may gain fitness advantages

from lower colony failure rates; higher survival of single-foundress queens; higher renesting success after raccoon predation; more efficient foraging; reduced vulnerability to strepsipteran parasites; and decreased predation risk due to aposematic coloration (P. fuscatus is much duller

and less “yellow jacket-like” than P. dominula (Figures 2 and 3).

2.1.2 Cavity-nesting Birds

Four percent of North American bird species nest obligately in cavities and a number of

other bird species occasionally nest in cavities (Newton 1994). Secondary cavity-nesting species, those that usually do not make their own holes, depend on natural cavities and abandoned holes of primary cavity-nesters (predominantly woodpeckers). In Ontario, secondary cavity-nesters include members of many bird families including ducks (Anatidae), owls

(Strigidae), flycatchers (Tyrannidae), swallows (Hirundinidae), wrens (Troglodytidae),

chickadees (Paridae), nuthatches (Sittidae), bluebirds (Turdidae), warblers (Parulidae), starlings

(Sturnidae) and Old World sparrows (Passeridae) (James 1984).

Martin and Li (1992) found that nest success increased in the following order: open-

nesting (birds with “regular” open cup nests) < secondary cavity-nesters < primary cavity- nesters. The fact that secondary cavity-nesters have lower nest success than primary cavity- nesters is especially interesting because they utilize the same sites but in different years. It is possible that because many nest predators, such as squirrels and raccoons, are long-term residents, they may find and remember locations of cavities and may check them regularly for active nests during subsequent bird breeding seasons (Li and Martin 1991).

While secondary cavity-nesting birds obviously save energy and time by using pre- existing cavities made by woodpeckers, they still have some costs associated with their use.

Limited availability of cavities likely means there will be strong competition for these sites (see

Section 2.1.3). While Hansell (2000) stated that there is no cost to the construction of the nest for secondary cavity-nesters, many species such as wrens, chickadees, swallows, warblers and bluebirds still add a nest or extensive nest lining to the inside of the cavity. Another cost to reusing old cavities is the possible presence of blood-sucking nest parasites left in the nest by their previous occupants (Hansell 2000). As well, adult survival is lower for secondary cavity-

nesters, likely due to higher predation levels (Martin and Li 1992). To possibly overcome this,

many secondary cavity-nesters have larger broods than primary cavity-nesters (Martin 1993).

2.1.3 Competition for Cavities

The populations of many species of cavity-nesting birds are limited by the number of nest sites available (Newton 1994, Dobkin et al. 1995; however, see Waters et al. 1990). The limited

resource of cavities can lead to competition with conspecifics, other bird species, mammals and even insects. Some of these competitors are invasive species. In fact, an introduced species’ success may be linked to its ability to usurp nest sites of native species (Lindell 1996).

European Starlings, introduced to North America in 1890, compete directly for nest sites with many different native cavity-nesting birds. These include Purple Martins (Progne subis, Allen and Nice 1952), Red-bellied Woodpeckers (Melanerpes carolina, Kilham 1958, Ingold 1989),

Red-headed Woodpeckers (Melanerpes erythrocephalus, Ingold 1989), Lewis’ Woodpeckers

(Melanerpes lewis, Vierling 1998), Gila Woodpeckers (Melanerpes uropygialis, Kerpez and

Smith 1990), Acorn Woodpeckers (Melanerpes formicivorus, Troetschler 1976), Northern

Flickers (Colaptes auratus, Ingold 1996), American Kestrels (Falco sparverius, Bechard and

Bechard 1996), Wood Ducks (Aix sponsa, McGilvrey and Ulher 1971) and Buffleheads

(Bucephala albeola, Peterson and Gauthier 1985). Another invasive competitor for cavity nests is the introduced House Sparrow (Passer domesticus) which is known to compete with Eastern

Bluebirds (Sialia sialis) (Gowaty 1984, Pogue and Schnell 1994) and Purple Martins (Jackson and Tate 1974) for cavity nests.

2.1.4 Interactions between Polistes dominula and Cavity-nesting Birds.

Polistes dominula builds its nests in a variety of locations such as in hollow ladder rungs, gaps in wooden siding, hollow statuary, hollow railings, barbeques, under house eaves (Earley, pers. obs.) and in human-made bird nest boxes (Morton 2000). This nesting behavior makes the wasp a possible competitor with cavity-nesting birds that utilize nest boxes (Liebert et al. 2006).

A parallel example is the introduced honey bee (Apis mellifera Linnaeus), known to compete with, or at least occupy the nest sites of, many cavity-nesting birds around the world (Ercit and

Otis, unpublished data). These bird species include cockatoos (Western Australia Museum

2012) and Regent Parrots (Polytelis anthopeplus, Oldroyd 1994) in Australia; Wood Ducks (Aix sponsa, Robb 1995), Eastern Screech Owls (Megascops asio) and Great Crested Flycatchers

(Myiarchus crinitus, Twedt 2001) in the United States of America; Scarlet Macaws (Ara macao) in Guatemala (CITES, 2001) and Costa Rica (Vaughan 2003); Puerto Rican Parrots (Amazona vittata) in Puerto Rico (White and Vilella 2004); and Spix’s Macaws (Cyanopsitta spixii) in

Brazil (Caparroz 2001). Both the Spix’s Macaw and the Puerto Rican Parrot are critically endangered and so any nest sites no longer available to the birds due to occupancy by honey bees could be especially detrimental to these species. Honey bees have killed adult breeding female

Echo Parakeets (Psittacula eques) on the nest, and chicks and eggs have died due to the activities of the bees (Mauritian Wildlife Foundation, unpublished data). These endangered parakeets also have to contend with the wasp Polistes olivaceus (DeGeer). These wasps may use nest boxes and natural cavities as hibernacula outside of the Echo Parakeet breeding season.

However, some boxes and cavities that were regular nest sites for certain female Echo Parakeets were not used when the wasps were still present during the bird’s nesting season (Mauritian

Wildlife Foundation, unpublished data).

Feral European races of honey bees (e.g., Apis mellifera ligustica) tend to use large cavities (~40 L in volume, Seeley and Morse 1976) and would compete only with large cavity- nesting birds, but smaller birds in warm climates of the New World and in Africa may be in competition with the African races of honey bee (Apis mellifera scutellata) due this bee’s smaller nest size and ability to use small cavities (approximate mean volume of 25 L, McNally and

Schneider 1992).

Polistes have been using bird nest boxes for decades; McAtee noted their presence in

1929 and 1931. Many naturalists and researchers who monitor nest box lines in North America now complain about the presence of P. dominula in their boxes (Morton 2000, Daniel 2007).

However, even though the presence of wasps is discussed frequently, little research has been done on the real impacts of the wasps on the birds that use nest boxes. Blem and Blem (1991) recorded wasps (they had both paper wasps and sphecid wasps) to be present in 41.8% (1987) and 28.5 % (1988) of their Prothonotary Warbler (Protonaria citrea) nest boxes in Virginia. It is unknown which species of wasps they recorded. They concluded that the wasps and the warblers generally did not compete for nest sites as they chose cavities that were not usually acceptable to the other species (wasps preferred boxes farther from the water, having more ground cover under the box, increased direct sunlight and entrance hole facing south or southeast). The only contests for cavities were in an overlap zone of intermediate conditions. In 1988, three of the 214 boxes contained both active paper wasps and warbler nestlings (73 contained warbler nestlings but no wasps and 58 contained wasps but no warbler nestlings), suggesting that the two species can co- inhabit successfully, albeit rarely. This may not be the case if nest cavities are in short supply, however. Petit (1991) found that Prothonotary Warblers with fewer cavities to choose from were more likely to accept a cowbird as a brood parasite than they would in areas with an abundance of nest sites where they were more likely to abandon parasitized nests. McAtee (1929) also recorded one case of a bird (species not given) and a Polistes wasp sharing a nest box in

Maryland. Of the 99 nest boxes in that study, 40.4% had Polistes nests in them.

Stanback et al. (2009) studied cavity use by the native Golden Paper Wasp, P. fuscatus, and birds. Carolina Chickadees (Poecile carolinensis) and Eastern Bluebirds had similar nest initiation dates as Polistes fuscatus. Stanback et al. found that if both birds and wasps initiated

nest construction in the same box, birds were able to usurp nest boxes from wasps more often than vice versa. As well, wasps were more likely to use nest boxes with large wire mesh over the entrance hole to exclude birds than boxes that either species could utilize, suggesting that birds were the dominant species in this relationship.

Some bird species, especially in tropical areas, place their nests near wasp nests, presumably to get added protection from predators due to the defensive behaviour of the wasps

(see Appendix A). A cavity-nesting bird attempting to use a nest box occupied by a wasp nest could possibly gain protection in this way as well.

In 2006, J. Kral (pers. comm.2) of Guelph, Ontario, Canada, removed over 440 wasp nests (P. dominula and P. fuscatus) from a total of 528 boxes. This high occurrence of wasps could be cause for concern if the wasps are indeed competing with birds for nest sites.

Excluding wasps from nest boxes is very difficult. To discourage the European Starling (Sturnus vulgaris), many nest boxes are now designed with hole sizes too small for the starling to enter but sufficiently large for most native bird species. This would not work for wasps because they are smaller than birds. Currently, many people who maintain and monitor bird boxes remove wasp nests as they find them. However, it is possible that the wasps exclude potential nesting birds between the visits made by box monitors. This may be compounded by the fact that not all boxes are monitored regularly early in the nesting season. If wasps do exclude some birds from nesting in nest boxes, the same process may occur in natural tree cavities. This process could be amplified because a high use of nest boxes or cavities by P. dominula in newly colonized sites could occur very quickly because of the possibility of Polistes selecting sites due to tradition rather than genetic control. Wenzel (1996) showed that gynes of Polistes annularis (Linnaeus)

2 To contact J. Kral, contact Chris Earley, The Arboretum, University of Guelph, Guelph, Ontario, Canada, N1G 2W1, [email protected] 18

chose nest sites similar to those they were raised in, even when their natal nests were removed

from the sites where their mothers constructed them and then put in nearby novel sites. If this

ability to pass down a nest site tradition occurs in other Polistes species such as P. dominula,

then unmonitored nest box lines and areas with many natural cavities and old woodpecker holes

could have high wasp use very quickly.

Because P. dominula and P. fuscatus frequently occupy cavities in the region

surrounding Guelph, Ontario, I hypothesize (HA) that the presence of a Polistes sp. nest has an effect (positive or negative) on the successful breeding of cavity-nesting birds. The null hypothesis is that the relative proportion of successful bird nesting attempts is the same regardless of whether a wasp nest is present in the bird box or not.

2.2 MATERIALS AND METHODS

2.2.1 Study Area and Nest Boxes

The study sites , located within The Arboretum and Turfgrass Institute of the University of Guelph, had a combined area of approximately 300 ha comprised of a variety of habitats including maple-beech forests, old fields, woody plant collections, cut lawns, small ponds, gardens, cropland, agroforestry plots and dogwood-buckthorn scrub. A total of 130 bird nest boxes were erected in open field and cut lawn areas. The boxes were made of 2.2 cm thick pine boards and designed as described by the Golondrinas de Las Americas swallow project

(http://golondrinas.cornell.edu, Figure 4). This design was chosen because of another research

project on Tree Swallows happening at the same site. The entrance hole diameter for these

boxes is 3.8 cm which would allow Tree Swallows (Tachycineta bicolor), Eastern Bluebirds,

Black-capped Chickadees (Poecile atricapillus), House Wrens (Troglodytes aedon) and possibly

Figure 4. Golondrinas of the Americas nest box showing triangular opening at the top of one

side. Photo by Chris Earley.

House Sparrows (Passer domesticus) to enter. The boxes were wired on metal posts driven into

the ground and spaced at least 25 m apart. These bars were coated in mechanic’s grease to

discourage terrestrial predators from climbing them. The height of the nest hole was

approximately 1.5 m from the ground.

2.2.2 Data Collection

Boxes were monitored weekly from early May until mid-July, 2007. Upon finding the first wasp nest in a box, it was marked with a “W” and the wasp nest was left intact. The next

box with a wasp nest in it was marked with an “X” and the wasp nest was removed. As

additional wasps nests were found, they continued to be alternately left intact or removed and

marked accordingly. If wasps renested in “X” boxes they were removed again. The species of

wasp was recorded. For any boxes inhabited by birds, the species and number of eggs and/or

nestlings was recorded. A successful breeding attempt was recorded if at least two eggs were

present. The criterion of two eggs rather than one was adopted as birds may dump an egg in a

box even if they are not actively using that box (Lamble, pers. comm.3).

2.2.3 Data Analysis

Because all of the nest boxes studied were in a relatively small area and in open field habitats, the data were combined into a single analysis. Bird breeding success in boxes with wasp nests vs. boxes with wasp nests removed was analyzed using Fisher’s exact tests.

2.3 RESULTS AND DISCUSSION

2.3.1 Results

I recorded 80 successful nesting attempts by Tree Swallows, Black-capped Chickadees and Eastern Bluebirds. Of these, 4 occurred after June 10, and were excluded from this study as they were thought to be second nesting attempts. Because of the difficulty of seeing into House

Wren nests to check for eggs, 5 boxes in which House Wrens attempted to build a nest before

June 10 were excluded from this analysis. Of the 121 nest boxes remaining, 76 (63%) had a successful bird nesting attempt (e.g. at least 2 eggs) during the study period. Polistes started to construct a nest in 34 of 121 (28%) nest boxes at least once. In 3 cases for “X” nests, the wasp

3 To contact D. Lamble, contact Chris Earley, The Arboretum, University of Guelph, Guelph, Ontario, N1G 2W1, [email protected] 21

queen was not in the box at the time of the wasp nest removal so it was unknown what species the nest belonged to. One box had two wasp nests in it, one of each species. Of the 32 wasp nests that could be identified to species, 28 were P. dominula (88%); the remaining 4 were P. fuscatus.

For the analysis comparing “X” and “W” boxes, four nest boxes found with a new wasp nest on or after June 3 were excluded; I did this because I did not feel that one week was sufficient time for potential breeding birds to find the nest box. Three nest boxes had an active bird nest when a wasp started building in them. The wasp nest was left in one box allowing a P. dominula and a bird (Tree Swallow) to share a box. The Tree Swallows were the first to use the box and the wasp started building during the bird’s egg-laying/incubation stage; they coexisted for at least 22 days. The wasp nest had 34 cells by the time the Tree Swallow’s 4 nestlings were ready to fledge. This and the other 2 boxes where a wasp starting building after the birds did are discussed in Chapter 2.3.2.

Table 2.1 presents an overall summary of the results of this nest box study. In total, there were 73 successful bird nesting attempts. Note that one of 13 “W” nest boxes and three of 9 “X” nest boxes had successful bird nesting attempts.

The data shown in Table 2.2 suggest that there was neither a positive nor negative association of boxes with wasps nests and successful attempts of bird nesting (Fisher’s exact test, p=0.26), and thus the null hypothesis is accepted. In only one W box did the wasp nest disappear and a Tree Swallow usurped the box and successfully nested in it. In this case, there were 3

Table 2.1. Nesting attempts in nest boxes by birds (Tree Swallows, Eastern Bluebirds, and

Black-capped Chickadees, and presence of Polistes dominula and Polistes fuscatus wasp nests in the Guelph, Ontario, Canada study site.

No wasp nest Wasp nest Wasp nest (W) removed (X) Successful bird nesting 69 3 1 attempt* No bird or an 20 6 12 unsuccessful bird nesting attempt Total 89 9 13 *defined as a nest with at least 2 eggs

adult Tree Swallows in the box while the P. dominula wasp nest (but not the queen) was still present. At the next assessment one week later, the wasp nest was gone and a pair of Tree

Swallows were building a nest. It is presumed that the Tree Swallows removed this wasp nest.

Table 2.2: 2 X 2 Contingency Table for Bird Boxes with Wasp Nests (W) and Bird Boxes with

Wasp Nests removed (X) (Fisher’s Exact Test; p=0.26).

Wasp Nest (W) Wasp Nest Removed (X)

Successful Bird Nest 1 3

No Bird Nest or 12 6 Unsuccessful Bird Nest

The results of the W and X study show that P. dominula and P. fuscatus appear not to be competing with cavity-nesting birds for nest sites at my study site, though this may be attributed to my small sample size. It would be interesting to see if this is the case at other sites with higher wasp occurrence. Considering how prevalent P. dominula has become in nest boxes

across many areas of North America, it is surprising that their potential effects on birds have

been given so little study by the scientific community. Possible wasp exclusion of birds from

nest boxes may be especially problematic to rare bird species such as the once vulnerable Eastern

Bluebird and the endangered Prothonotary Warbler (in Canada, COSEWIC 2007).

Sixty-nine of 89 nest boxes that never had a wasp nest built in them had successful bird

nests (Table 2.1). When compared to the 3 of 9 “X” nest boxes that had successful bird nests, my data suggest that the birds in my study avoided nest boxes from which wasp nests were removed (Table 2.3; Fisher’s exact test, p=0.01). When “W” and “X” boxes are combined and compared to the boxes that never had a wasp nest, my data strongly suggests that the birds avoided any box that at some point had a wasp nest in it (Table 2.4; Fisher’s exact test, p=0.0000004).

The difference found in the use of the boxes by birds between boxes that never had wasps and those that had wasp nests that were removed is very interesting. It is possible that some aspect of the boxes was not attractive to birds but was attractive to the wasps, but as the boxes seemed to be in similar habitats and were distributed throughout the study site, this does not seem likely. Nest assessments were done once a week. It is possible that the presence of the

Table 2.3: 2 X 2 Contingency Table for Wasp Nest Removed (X) boxes and boxes that never had a wasp nest (Fisher’s Exact Test; p=0.01).

Never a Wasp Nest Wasp Nest Removed (X)

Successful Bird Nest 69 3

No Bird Nest or 20 6 Unsuccessful Bird Nest

adult wasps and/or their nests between assessments deterred the birds long enough that they did not use the boxes even when the boxes were subsequently free of the wasps.

Table 2.4: 2 X 2 Contingency Table for bird boxes with wasp nests at some point during the study (both with wasp nest left intact (W) and with wasp nests removed (X)) and boxes that never had a wasp nest (Fisher’s Exact Test; p=0.0000004).

Never a Wasp Nest Wasp Nest Removed (X) and

Wasp Nest (W)

Successful Bird Nest 69 4

No Bird Nest or 20 18 Unsuccessful Bird Nest

To test to see if the presence of the wasp nest alone was important in nest box choice by the birds, I started an experiment with old wasp nests. I attached old Polistes wasp nests to the roofs of 42 nest boxes in late April at another study site where P. dominula was still rare (on fenceposts along roads near Fergus, Ontario, ~27 km north of my study site). Every other box in a line received a wasp nest and the other boxes received only the pin and white glue used to attach them to make sure the method of attachment did not influence the birds’ nest box choice.

Unfortunately, most of the pins did not stay in place and they and any attached wasp nests were found on the bottoms of the boxes on the first nest assessment of the season. By then, nesting by the birds had begun and the experiment could not be restarted. It should be noted that some birds built their nest on top of the fallen wasp nests. Repeating this study of how birds might perceive the presence of a wasp nest is warranted.

Birds might be able to detect the previous occupancy of wasps through sensory cues other than vision. For example, birds may be able to smell pheromones or other chemicals that have been left by the wasps. Pheromones are important in social insect communication and some wasps and bees are known to leave a pheromone marker at the entrance to their nests (Butler et al. 1969). As well, wasps may use an ant-repellent substance on the pedicel that holds the nest to the substrate (Jeanne 1970, Gadagkar 1991). If birds can smell any of these chemical marks, they could use the information to discover and avoid a possibly aggressive insect in a newly found nest cavity. While it is known that certain birds such as Turkey Vultures (Cathartes aura), kiwis and procellariiform seabirds (petrels, shearwaters and albatrosses) have a good sense of smell

(Owre and Northington 1961, Wenzel 1971, Nevitt 1999, McShea et al. 2000), most researchers have assumed that other birds do not have a useful sense of smell based on an olfactory bulb size study by Bang and Cobb (1968). However, recent bird olfaction studies have shown that, contrary to previous assumptions, many birds may have a functional sense of smell (Wenzel

2007). As bird olfaction studies continue to shed light on the sensitivity of this avian sense, it may be possible to do a future study on whether or not birds can sense social insect scent markers in nesting cavities.

2.3.2 Use of a box by a wasp and a bird simultaneously

One box had a successful Tree Swallow and P. dominula nest in it at the same time (two other boxes had an active wasp nest and an active bird nest simultaneously but the wasp nests were removed due to being designated as “X” boxes). While rare, this association between a

Polistes wasp and a cavity-nesting bird has been found in other studies as well (McAtee 1929,

Blem and Blem 1991). Because most naturalists who manage bird boxes remove Polistes nests,

it is possible that this association could be more common than we realize. An association where either the bird or the wasp or both gain benefits could develop with the newly arrived P. dominula and cavity-nesting birds.

2.3.3 Nest box design

It is possible that the nest box design for this study was not optimal for wasps, resulting in fewer wasps using the boxes. J. Kral continues to have a much higher incidence of wasps at his site (Kral, pers. comm.), Guelph Lake Conservation Area, which is only 7 km north of my study site. His boxes utilize a more traditional design which has no opening between the roof and the walls. My boxes had a triangular opening under the roof on each side of the box (Figure

4). The length of the vertical side of the triangle was approximately 2.2-3.1 mm. While the difference in numbers of wasps at the Kral site and my site could be attributed to habitat differences (i.e., the plant community composition, proximity to water, amount of surrounding urbanization), the placement of the wasp nests within the boxes suggests otherwise. Out of 27 boxes in my study where the wasp nest placement was recorded, 23 (85%) wasp nests were on the sides of the box and only 4 (15%) were on the roof. In Kral’s boxes, most wasp nests are found hanging from the roof (Kral, pers. comm.). The difference could be due to the protection the wasps receive from the elements in the more enclosed boxes. In these boxes at Kral’s site, the wasps would get protection in any nesting location and but they may choose the roof because it is likely easier for them to build their typically horizontal comb (Reeve 1991). In my boxes with the openings at the tops, the wasps would be exposed to the elements more if they built on the roof than if they built on the sides. P. fuscatus is more likely to build its nest in a warm site as a “passive” temperature regulation strategy (Jones and Oldroyd 2006). P. dominula uses less

protein during its nest construction making the nest less waterproof than other native Polistes

nests; this may be an outcome of P. dominula’s longer association with human civilization in

Europe (Pickett and Wenzel 2000). Having a less waterproof nest may make the building

location of the nest more critical for P. dominula. In my study, the construction of nests on side

walls of the nest box may be another way in which wasps regulate their temperature in these

more open boxes. If wasps avoid boxes of this design, then nest box design could be used to

deter, or at least decrease, the numbers of wasps using boxes intended for birds. If there is no

difference to the birds’ nesting success, using boxes that are less attractive to nesting wasps

might increase the number of boxes available to birds.

It is interesting to note that in subsequent years of 2008 and 2009, there were far fewer

wasps using the nest boxes in my study site compared to the same number or more wasps in

Kral’s study site. These two years were much cooler and wetter than 2007. The decrease in

wasp numbers in my study site could have been due to the more open box design.

As well, the openings at the top of the boxes could allow more frequent positive associations between the birds and wasps. Many wasps were seen using the top openings to exit and enter the nest boxes instead of the main entrance hole; this may decrease the number of direct interactions between birds and wasps in the same box. Box designs could even be modified so that they are taller to allow more space between the wasps using the ceilings of the nest boxes and the birds using the floors.

2.3.4 Conclusion

The fact that bird use of wasp (W) boxes and wasp excluded (X) boxes did not differ but that birds avoided boxes of which wasp nests were removed (X) in comparison to boxes that

never had a wasp nest suggests that there is a subtle interaction between the birds and wasps in nest boxs. Bird box design may contribute to the number of wasps nesting in the boxes. The abundance of wasps in many areas with bird boxes should provide researchers with the opportunity to study these interactions. Unfortunately, most naturalists who monitor bird boxes try to produce as many nestling birds as possible and consequently they are very reluctant to leave wasp nests in some boxes to enable the study of bird-wasp interactions. This is unfortunate as understanding these interactions is important in figuring out ways to protect cavity-nesting birds from potential competition with the invasive species, P. dominula.

CHAPTER 3

THE INFLUENCE OF WASP STING PAIN LEVEL ON NEST SITE CHOICE BY

BIRDS THAT NEST NEAR WASPS

3.1 INTRODUCTION

3.1.1 Wasp Sting Pain Level

While at least some species in over half of all terrestrial invertebrate orders have chemical defensive compounds, only 4 orders, Scorpionida, Lepidoptera, Coleoptera and

Hymenoptera, have a stinging structure (Whitman et al. 1990, Berkov et al. 2008). In some lepidopteran caterpillars, hairs or spines can pierce the predator’s skin to deliver poison

(Whitman et al. 1990). Scorpions have a modified caudal spine and the Cerambycid beetle,

Onychocerus albitarsi Pascoe has a modified terminal antennal segment that functions as a stinger (Berkov et al. 2007).

Many female aculeate Hymenoptera have a modified ovipositor that can inject venom.

The act of being stung by a bee, wasp or ant can cause a startle and/or pain reaction in potential predators that could protect the individual insect or its nest (Schmidt 1990). Even large vertebrates that could potentially destroy the nest structure, brood, eggs and larvae (Judd 1998) can be stopped by the defensive stinging of the nest inhabitants (Jeanne 1977, Schmidt 1990).

Without this venom-assisted defensive strategy, social Hymenoptera would likely not exist because they could not defend their energy-rich nest from vertebrate predators (Schmidt 1990).

Most species of aculeate Hymenoptera have a sting that they use to subdue prey, protect themselves, and/or protect their nests. During nest defense, three aspects influence the ability of

a colony to defend itself (Starr 1985):

1. Number of defenders in the colony;

2. Aggressiveness of the wasps;

3. Sting pain level of each sting.

A sting pain index for Hymenoptera has been developed by Starr and Schmidt (Starr 1985,

Schmidt 1990). It attempts to describe and rank the pain of a sting of approximately 100 species of wasps, ants, and bees, as experienced by humans. Although this index relates to human pain, I assume here that it is likely to be similar to what other vertebrates feel when they are stung.

3.1.2 Wasp Nest-associating Birds

Over one hundred species of birds have been recorded to nest near wasp nests, presumably as a way to gain protection from predators (Joyce 1990; see Appendix A). The few studies that have examined this relationship have shown that the breeding success of the birds was enhanced when their nests are situated near wasp nests (Smith 1968, Robinson 1985,

Wunderle and Pollock 1985, Joyce 1990, Beier and Tungbani 2008, but see Barnard and Markus

1990). In these studies and many other observations (see Appendix A and Appendix B), the birds place their nests near active wasp or bee colonies and are able to build their nests without having the insects chase them away. While the nesting beside certain wasps is likely an instinctive behaviour, it is unknown if there are aspects of the wasps’ defensive strategy that makes them better protective neighbours. Of the three factors mentioned above, only the sting pain level of each sting is known at this time for many of the wasp and bee species. By using the

Starr/Schmidt sting pain index, one can examine the relationship between sting pain level and bird nest placement behavior. I hypothesize (HA) that birds will nest more often with wasps that have high sting pain indices. The null hypothesis is that there is no association between wasp

sting pain level and the frequency at which several bird species construct their nests near wasp

nests.

3.2 MATERIALS AND METHODS

Data for this study were obtained from the literature, as follows: Sting pain level from

Starr (1985) and Schmidt (1990); bird nesting associations from Joyce (1990); wasp colony sizes from Hastings et al. (1998) and Jeanne (1991). Joyce (1990) studied three bird species: Yellow- olive Flycatcher (Tolmomyias sulphurescens), Banded Wren (Thyrothorus pleurostictus) and

Rufous-naped Wren (Campylorhynchus rufinucha) in Costa Rica. A proportion of the nests of each of these species were constructed next to a social wasp nest. Most nests were in ant- acacias.

Spearman’s Rank Order Correlations were conducted to determine the relationship between the sting pain level of a wasp and the number of times birds of each species built their nests beside that wasp species. This was also done for the three bird species combined.

3.3 RESULTS AND DISCUSSION

Data were organized to compare the number of bird nests associated with each sting pain level (Table 3.1). The sting pain level is available for 11 of 12 wasp species. No sting pain level was available for Polistes major Beauvois, so it was not included in the statistical analyses.

There were no significant correlations between sting pain level and the number of nests of each of the three bird species for which data were available (Table 3.2).

Table 3.1. Wasp species, Number of bird nests associated with each (Joyce 1990) and sting pain

levels (Starr 1985, Schmidt 1990, Wenzel, unpublished data). Colony size data from Jeanne

(1991) and Hastings et al. (1998): w – winter, s – summer, ds – dry season, ws – wet season.

Sting Pain Level: 0 is a sting that cannot penetrate the human skin and 4 is the greatest-known sting pain. For comparison purposes, a honey bee is a 2.

Number of Bird Nests

olive naped naped

- -

Sting Pain Level Yellow Flycatcher Banded Wren Rufous Wasp (mean number of adults in colony) Wren Total Polybia diguetana Buysson 0-1 0 1 0 1 Agelaia areata (Say; 5693w, 13570s) 1 3 3 0 6 Polybia occidentalis (Olivier; 37ws, 77ds) 1 2 24 1 27 Mischocyttarus immarginatus Richards 1-2 0 2 0 2 Apoica pallens (Fabricius; 170) 2 1 1 0 2 Brachygastra mellifica (Say; 7951) 2 1 22 0 23 Parachartergus fraternus (Gribodo; 280) 2 22 10 1 33 Polistes instabilis Saussure 2 0 3 0 3 Polybia rejecta (Fabricius; 1877) 2 27 27 41 95 Polistes canadensis (Linnaeus) 2-3 0 2 0 2 Synoeca septentrionalis Richards (275) 3-4 28 11 0 39 Polistes major Beauvois ? 0 1 0 1 Total Nest Numbers 84 106 43 233

Table 3.2. rho and P values from Spearman Rank Order Correlations showing the relationship

between sting pain level and the number of bird nests near each wasp species’ nests.

Bird Species Spearman’s rho Value p-value Yellow-olive 0.27 0.42 Flycatcher Banded Wren 0.19 0.59 Rufous-naped Wren -0.07 0.83 All Species 0.36 0.28

The lack of significance of the correlation analyses suggests that factors other than sting pain level may be involved in nest site selection by birds. Wasp nest size and aggressiveness should be considered. Unfortunately, colony size information was available for only some of the wasp species and aggressiveness levels were unavailable for this analysis. Downhower and

Wilson (1973) noticed a progression of aggressiveness between 5 genera of wasps that katydids associated with. They note that the “majority” of the associations were with Polistes and

Synoeca, both of which are large wasps and have large nests.

In Joyce’s (1990) study, the three bird species primarily nested in ant-acacias (with or without an associated wasp nest). For Yellow-olive Flycatchers, 88% of 344 nests were in ant- acacias and 86% of 561 Banded Wren nests and 93% of 338 Rufous-naped Wren nests were in ant-acacias as well (Joyce, 1990). So, it may not be surprising that Polybia rejecta attracted the most birds because this wasp species usually nests in ant-acacias (Joyce 1990). But, Rufous- naped Wrens almost always nest beside P. rejecta nests when they associate with a wasp species, even though 3 other species (Polybia occidentalis, Brachygastra mellifica (Say) and

Parachartergus fraternus (Gribodo)) are known to nest in ant-acacias as well. In comparison, these 4 wasp species were in the top 5 wasp species that Banded Wrens nested beside. Some

factor appears to be important in why one wren nests primarily beside Polybia rejecta and the other wren nests beside a variety of the wasp species. Banded Wrens also nested beside Synoeca septentrionalis Richards, which was not known to nest in ant-acacias, but it was a favourite nest associate of the Yellow-olive Flycatcher as well. This wasp species appears to have some kind of defensive strategy that is especially attractive to these two species of birds because they will place their nest on a non-ant-acacia tree to be associated with it.

Visibility of the wasp nest to potential predators may be important. Nests that are large, or more conspicuous may make them more visible to vertebrate predators and thus can be avoided. As well, the precise locations of wasp nests may be important to nest site choice by birds (Joyce 1990). For example, it is difficult for most birds to nest near Synoeca septentrionalis nests because of the wasp`s nests being on exposed tree trunks and large branches, but it is still a favourite nest-association species for Yellow-olive Flycatchers and

Banded Wrens.

Hopefully additional data will be forthcoming so that a more comprehensive wasp index incorporating sting pain, colony size, aggressiveness and possibly other factors can be developed and tested.

CHAPTER 4

GENERAL DISCUSSION AND CONCLUSION

Birds and wasps both build nests to raise and protect young. Because both of these taxa may try to build their nests in optimal places for protection from the elements and/or predators, associations between the two may occur. Polistes wasps are known to build their nests in human-made nest boxes put out for cavity-nesting birds. Many populations of secondary cavity- nesting birds are limited by the numbers of cavities available. The invasive European Paper

Wasp, P. dominula, is a recent invader to southern Ontario and has become common in local nest boxes.

I wanted to find out if this species and the native Golden Paper Wasp, P. fuscatus, were competing with birds for nest boxes. In a study site of 130 nest boxes in Guelph, Ontario,

Canada, I recorded the breeding success of cavity-nesting birds in boxes with wasp nests and in boxes where wasp nests were removed. My null hypothesis that the relative proportion of successful bird nesting attempts is the same regardless of whether a wasp nest is present in the bird box or not was accepted. My alternative hypothesis that the prior presence of Polistes sp. nest has some effect on the successful breeding of cavity-nesting birds was rejected. However, when bird breeding success in boxes that never had a wasp nest was compared to bird breeding success in boxes that had wasp nests that were removed, my data suggest that the birds avoided nest boxes from which wasp nests were removed.

It seems that while the wasps were not competing with the birds for nest boxes, the birds were detecting the previous presence of wasp nests and avoiding those boxes. How the birds are

doing this is unknown but the fact that they are avoiding the boxes indicates that wasp presence is important in the use of nesting cavities for birds.

In my study site, the nest boxes were designed with openings at the top of each side of the box. Most of the wasp nests (85%) built in these boxes were on the inside walls of the box.

In Kral’s study site, the boxes had no openings at the top of the box. Most of the wasp nests in these boxes were built on the ceiling of the box. I believe that the lower numbers of wasps found in my study site could be attributed to the box design. Wasps may prefer to build their nests hanging from the horizontal ceiling of the nest box, but in my study site they placed their nests on the vertical walls, thereby reducing exposure to wind and rain that could enter through the openings at the top of the box. If the breeding success of birds is not dependent on whether or not there are openings at the top of the box, nest box design could be used to decrease the number of wasps using nest boxes.

Birds of many species have been known to build their nests near wasp nests that provide protection from predators. Female social wasps are equipped with stingers that can deliver painful stings to potential vertebrate predators. I wanted to explore the role of wasp sting pain level in the choice of nesting sites of three wasp nest-associating bird species. My null hypothesis that there is no association between wasp sting pain level and the frequency at which several bird species construct their nests near wasp nests was accepted. My alternative hypothesis that birds will nest more often with wasps that have high sting pain indices was rejected.

It appears that sting pain level alone is not an important aspect to why birds may nest near certain species of wasps. Other factors such as colony size and aggressiveness level of each

wasp species are likely part of this bird-wasp nesting association complex. As well, nest size, nest placement and nest visibility may be important.

Many observers have noted nesting associations between a variety of wasp and bee species and bird species. I have compiled a list of 121 bird species, 28 wasp and 4 bee species that have been recorded to have some kind of nesting association (Appendix A and Appendix B).

Considering how many species are on this list, it is surprising that only five studies have looked into the wasp/bee-bird association and found that it lowered the predation of the adult breeding birds and/or their eggs/young. It is hoped that by providing this list, more research will be done on this fascinating aspect of bird-insect interactions.

REFERENCES

Alerstam, T. and G. Hogstedt. 1981. Evolution of hole-nesting in birds. Ornis Scandinavica 12: 188-193.

Allen, R.W. and M. M. Nice. 1952. A study of the breeding biology of the Purple Martin (Progne subis). American Midland Naturalist 47: 606-665.

Allendorf, F. W. and L.L. Lundquist. 2003. Introduction: population biology, evolution and control of invasive species. Conservation Biology 17: 24-30.

Arnold, K.A. 1966. The avian genus Thryothorus (Troglodytidae) in Costa Rica: A study in species diversity. PhD thesis. Louisiana State University.

Baker, E.C.S. 1931. Nesting association between birds and wasps, ants, or termites, in the oriental region. Proceeds of the Entomological Society of London 6:34-37.

Baker, E.S.C. 1934. The Nidification of Birds of the Indian Empire. Vol. 3. Taylor and Francis, London.

Bang, B.G. and S. Cobb. 1968. The size of the olfactory bulb in 108 species of birds. The Auk 85: 55-61.

Barnard, H.G. 1911. Field notes from Cape York. Emu 11: 17-32.

Barnard, H.G. 1926. Birds of the Cardwell District. Emu 26: 1-13.

Barnard, P. and M.B. Markus. 1990. Reproductive failure and nest site selection of two estrildid finches in Acacia woodland. Ostrich 61: 117-124.

Bechard, M. J. and J. M. Bechard. 1996. Competition for nest boxes between American Kestrels and European Starlings in an agricultural area of southern Idaho. In Raptors in Human Landscapes: Adaptations to Built and Cultivated Environments. Eds: Bird, D. M., Varland, D. E. and Negro, J. J. Pages 155-162. Academic Press Limited, London.

Beier, P. and A.I. Tungbani. 2006. Nesting with the wasp Ropalidia cincta increases nest success of Red-cheeked Cordonbleu (Uraeginthus bengalus) in Ghana. Auk 123(4): 1022.

Berger, A.J. 1975. The Warbling Silverbill, a new nesting bird in Hawaii. Pacific Science 29:51-54.

Berger, A.J. 1977. The Exotic Birds of Hawaii. Island Heritage Limited, Norfolk Island, Australia.

Berkov, A., N. Rodriguez and P. Centeno. 2008. Convergent evolution in the antennae of a Cerambycid beetle, Onychocerus albitarsis, and the sting of a scorpion. Die Naturwissenschaften 95: 257-261.

Bird Ecology Study Group. 2007. http://www.besgroup.org/2007/06/28/baya-weaver-hornets/

Blem, C.R. and L.B. Blem. 1991. Nest-box selection by Prothonotary Warblers. Journal of Field Ornithology 62: 299-307.

Bogliani, G., F. Sergio and F. Tavecchia. 1999. Woodpigeons nesting in association with Eurasian Hobby falcons: advantages and choice rules. Animal Behavior 57: 125-131.

Bologna, M.A., P. Bombi, M. Pitzalis and S. Turillazzi. 2007. A previously unreported association between a social wasp and a social passerine bird. Tropical Zoology 20: 211- 214.

Brooks, M. 1932. Carolina Wrens roosting in abandoned hornets’ nests. Auk 49: 223-224.

Brown, C.B. 1876. Canoe and Camp Life in British Guiana. Edward Stanford, London.

Butler , C.G., D.J.C. Fletcher and D. Watler. 1969. Nest-entrance marking with pheromones by the honey bee, Apis mellifera, and by a wasp, Vespula vulgaris. Animal Behavior 17:142- 147.

Campbell, A. J. and H.G. Barnard, 1917. Birds of the Rockingham Bay District, North Queensland. Emu 17:21.

Caparroz, R., C.Y. Miyaki, M.I. Bampi and A. Wajntal. 2001. Analysis of the genetic variability in a sample of the remaining group of Spix's Macaw (Cyanopsitta spixii, Psittaciformes: Aves) by DNA fingerprinting. Biological Conservation 99: 307-311.

Cervo, R., F. Zacchi and S. Turillazzi. 2000. Polistes dominulus (Hymenoptera: Vespidae) invading North America: some hypotheses for its rapid spread. Insectes Sociaux 47: 155-157.

Chapin, J.P. 1954. The Birds of the Belgian Congo. Part 4. Bulletin of the American Museum of Natural History, Volume 75B.

Chisholm, A.H. 1952. Bird-insect nesting associations in Australia. Ibis 94:395-405.

Chubb, C. 1916. The Birds of British Guiana, Based on the Collection of Frederick Vavasour McConnell. 2 Volumes. B. Quaritch, London.

CITES, 2001. Convention on International Trade in Endangered Species of Wild Fauna and Flora. Seventeenth meeting of the Animals Committee, Hanoi (Viet Nam), 30 July- 3 August 2001 (http://www.cites.org/eng/com/ac/17/E17-08-1.pdf)

Clements, J. 2011. The Clement’s Checklist of Birds of the World. Cornell University Press, Ithaca, N.Y.

Collias, N.E. and E.C. Collias. 1984. Nest building and bird behavior. Princeton University Press, Princeton.

Contino, F. 1968. Observations on nesting of Sporophilia obscura in association with wasps. Auk 85: 137-138.

Cornwall, E.M. 1910. Notes on the Great-billed Heron (Ardea sumatrana). Emu 9: 138-141.

COSEWIC 2007. COSEWIC Assessment and Update Status Report on the Prothonotary Warbler Protonotaria citrea in Canada. Committee on the Status of Endangered Wildlife in Canada. Ottawa. (www.sararegistry.gc.ca/status/status_e.cfm).

Daniel, B. 2007. Paper wasps and what to do about them. North American Bluebird Society. Spring 2007:16-17, 22.

Dejean, A. and R.C. Fotso. 1995. Nesting associations of small birds and Polybioides tabidus (Vespidae Epiponinae) in southern Cameroon. Ethology, Ecology and Evolution 7: 11- 25.

Dobkin, D.S., A.C. Rich, J.A. Pretare and W.H. Pyle. 1995. Nest-site relationships among cavity-nesting birds of riparian and snowpocket aspen woodlands in the Northeastern Great Basin. Condor 97: 694-707.

Downhower, J.F. and D.E. Wilson. 1973. Wasps as a defense mechanism for katydids. American Midland Naturalist 89: 451-455.

Eickwort, G.C. 1978. Polistes dominulus discovered near Boston. Polistine Information Bulletin Newsletter.

Elgood, J.H. and P. Ward. 1960. The nesting of Heuglin’s Masked Weaver in Nigeria. Ibis 102: 472-473.

Ercit, K. and G. Otis. The birds and the bees: Competition between Honey Bees (Apis mellifera L.) and cavity-nesting birds. Unpublished manuscript.

Feekes, F. 1981. Biology and colonial organization of two sympatric caciques, Cacicus cela and Cacicus h. haemorrhous (Icteridae, Aves) in Suriname. Ardea 69: 83-107.

Fitzgerald, J.W. 1976. Systematics and biogeography of the Tyrannid genus Todirostrum and related genera (Aves). Bulletin of the Museum of Comparative Zoology 147: 436-563.

Fraga, R.M. 1989. Colony size and nest trees of Montezuma Oropendulas in Costa Rica. Journal of Field Ornithology 60: 289-295.

Frohawk, F.W. 1935. Martins and wasps nesting together. Proceeding of the Royal Entomological Society of London 10:77-78.

Gadagkar, R. 1991. Belonogaster, Mischocyttarus, Parapolybia, and Independent-founding Ropalidia. In The Social Biology of Wasps. K.G. Ross and R.W. Matthews, Eds. Pages 149-190. Cornell University Press, Ithaca, N.Y.

Gamboa, G. J., E.I. Greig and M.C. Thom. 2002. The comparative biology of two sympatric paper wasps, the native Polistes fuscatus and the invasive Polistes dominulus (Hymenoptera, Vespidae). Insect Sociaux 49: 45-49.

Gibo, D.L. 1980. Apparent nest site competition between the paper wasp Polistes fuscatus (Hymenoptera: Vespidae) and the house wren. Journal of the New York Entomological Society 88: 143-145.

Goodwin, D. 1982. Estrilid Finches of the World. Cornell University Press, Ithaca, N.Y.

Gosse, P.H. 1847. The Birds of Jamaica. John van Voorst, London.

Government of Canada, 2009. Invasive Species in Canada (http://www.invasivespecies.gc.ca/english/View.asp?x=501). Accessed in 2013.

Gowaty, P.A. 1984. House Sparrows kill Eastern Bluebirds. Journal of Field Ornithology 55: 378-380.

Grant, P.R. 1966. The coexistence of two wren species of the genus Thryothorus. Wilson Bulletin 78: 266-278.

Gray, W.J. 1945. Some notes on the nesting of certain birds in northern Nyasaland. Ostrich 16: 49-54.

Grimes, K and L. Darku. 1968. Some recent breeding records of Picathartes gymnocephalus in Ghana and notes on its distribution in West Africa. Ibis 110: 93-99.

Grimes, L.G. 1973. The breeding of Heuglin’s Masked Weaver and its nesting association with the red weaver ant. Ostrich 44: 170-175.

Gross, A.O. 1958. Life history of the Bananaquit of Tobago Island. Wilson Bulletin 70: 257- 279.

Haemig, P.D. 1999. Predation risk alters interactions among species: competition and facilitation between ants and nesting birds in a boreal forest. Ecology Letters 2: 178-184.

Haemig, P.D. 2001. Symbiotic nesting of birds with formidable animals: a review with applications to biodiversity conservation. Biodiversity Conservation 10: 527-540.

Halme, P., M. Hakkila and E. Koskela. 2004. Do breeding Ural Owls Strix uralensis protect ground nests of birds? An experiment using dummy nests. Wildlife Biology 10: 145- 148.

Hamilton, W.D. 1964a. The genetical evolution of social behavior, I. Journal of Theoretical Biology 7: 1-16.

Hamilton, W.D. 1964b. The genetical evolution of social behavior, II. Journal of Theoretical Biology 7: 17-52.

Hansell, M. H. 2000. Bird Nests and Construction Behaviour. Cambridge University Press, London.

Harrower, D.E. 1935. The habits of passerine birds of Central America with particular reference to their breeding. Ph.D. dissertation. Cornell University.

Hastings, M.D., D.C. Queller, F. Eischen and J.E. Strassmann. 1998. Kin selection, relatedness, and worker control of reproduction in a large-colony epiponine wasp, Brachygastra mellifica. Behavioral Ecology 9: 573-581.

Haverschmidt, F. 1950. The nest and eggs of Tolmomyias poliocephalus. Wilson Bulletin 62: 214-216.

Haverschmidt, F. 1957. Nachbarschaft von Vogelnestern und Wespennestern in Surinam. Journal für Ornithologie 98: 389-396.

Haverschmidt, F. 1968. Birds of Surinam. Oliver and Boyd, Edinburgh.

Haverschmidt, F. 1974. Great Kiskadee nesting in an old woodpecker hole. Auk 91: 639.

Hindwood, K.A. 1955. Bird/wasp nest nesting associations. Emu 55: 263-274.

Hindwood, K.A. 1959. The nesting of birds in the nests of social insects. Emu 59: 1-36.

Hoebeke, E. R. and A.G. Wheeler, Jr. 2005. First records of adventive Hymenoptera (Argidae, Megachilidae, Tenthredinidae and Vespidae) from the Canadian maritimes and the United States. Entomological News 116: 159-166.

Hoesch, W. 1956. Überdas Nisten südwestafrikanischer Vögel unter dem Schultz der Wespe Belonogaster rufipennis. Journal für Ornithologie 97: 341-342.

Ingold, D.J. 1989. Nesting phenology and competition for nest sites among Red-headed and Red-bellied Woodpeckers and European Starlings. Auk 106: 209-217.

Ingold, D. J. 1996. Delayed nesting decreases reproductive success in Northern Flickers: implications for competition with European Starlings. Journal of Field Ornithology 67: 321-326.

Jackson, J.A. and J. Tate Jr. 1974. An analysis of nest box use by Purple Martins, House Sparrows, and Starlings in Eastern North America. Wilson Bulletin 86: 435-449.

James, R.D. 1984. Habitat management guidelines for cavity-nesting birds in Ontario. Ontario Ministry of Natural Resources.

Jeanne, R.L. 1970. Chemical defense of brood by a social wasp. Science 168: 1465-1466.

Jeanne, R.L. 1975. The adaptiveness of social wasp nest architecture. Quarterly Review of Biology 50: 267-287.

Jeanne, 1977. Ultimate factors in social wasp nesting behaviour. Proceedings of the 8th International Congress of the International Union of the Study of Social Insects. Pages 164-168.

Jeanne, 1991. The swarm-founding Polistinae. In The Social Biology of Wasps. K.G. Ross and R.W. Matthews, Eds. Cornell University Press, Ithaca, N.Y. Pages 191-231.

Jones, J.C. and B.P. Oldroyd. 2006. Nest thermoregulation in social insects. Advances in Insect Physiology 33: 153-191.

Joyce, F.J. 1990. Nesting associations of Birds, Ants and Wasps. Ph.D. dissertation. Cornell University.

Joyce, F.J. 1993. Nesting success of Rufous-naped Wrens (Campylorhynchus rufinucha) is greater near wasp nests. Behavioral Ecology and Sociobiology 32: 71-77.

Judd, T.M. 1998. Defensive behavior of colonies of the paper wasp, Polistes fuscatus, against vertebrate predators over the colony cycle. Insectes Sociaux 45: 197-208.

Kalter, L.B. 1932. Carolina Wren roosting in hornet’s nest. Auk 49: 90.

Kerpez, T.A. and N.S. Smith. 1990. Competition between European Starlings and native woodpeckers for nest cavities in Saguaros. Auk 107: 367-375.

Kilham, L. 1958. Pair formation, mutual tapping and nesthole selection of Red-bellied Woodpeckers. Auk 75: 318-325.

Koepcke, M. 1972. Über die Resistenzformen der Vogelnester in einem begrenzten Gebiet de tropischen Regenwaldes in Peru. Journal für Ornithologie 113: 138-160.

Liebert, A.E., G.J. Gamboa, N.E. Stamp, T.R. Curtis, K.M. Monnet, S. Turillazzi and P.T. Starks. 2006. Genetics, behavior and ecology of a paper wasp invasion: Polistes dominulus in North America. Annales Zoologici Fennici 43: 595-624.

Lindell, C. 1996. Patterns of nest usurpation: when should species converge on nest niches? Condor 98: 464-473.

Lynes, H. 1924. On the birds of north and central Darfur, with notes on the West-Central Kordofan and North Nuba provinces of British Sudan. Ibis 11: 399-446 & 648-719.

Mackworth-Praed, C.W. and C.H. Grant, 1960. Birds of Eastern and North Eastern Africa. Vol. 2. Longmans, Green and Company, London.

Marchant, S. 1960. The breeding of some S.W. Ecuadorian birds. Ibis 102: 349-382 & 584-599.

Marshall, A.J. 1933. The Large-billed Warbler. Emu 33: 81-85.

Martin, T.E. 1993. Evolutionary determinants of clutch size in cavity-nesting birds: nest predation or limited breeding opportunities? American Naturalist 142: 937-946.

Martin, T.E. and P. Li. 1992. Life history traits of open- vs. cavity-nesting birds. Ecology 73: 579-592.

McAtee, W. L. 1929. Paper wasps (Polistes) as pests in bird houses. Proceedings of the Entomological Society of Washington 31: 136.

McAtee, W.L. 1931. Paper wasps (Polistes) in bird houses. Proceedings of the Entomological Society of Washington 33: 186.

McComb, W. C. and R.E. Noble. 1982. Invertebrate use of natural tree cavities and vertebrate nest boxes. American Midland Naturalist 107: 163-172.

McCrae, A.W. and J.F. Walsh. 1974. Association between nesting birds and Polistine wasps in North Ghana. Ibis 116: 215-217.

McGilrey, F. B. and F. M. Uhler. 1971. A starling-deterrent Wood Duck nest box. Journal of Wildlife Management 35: 793-797.

McNally, L.C. and S.S. Schneider, 1992. Seasonal cycles of growth, development, and movement of the African honey bee Apis mellifera scutella (Hymenoptera: Apidae) in Botswana, Africa. Insectes Sociaux 39: 167-179.

McShea, W.J., E.G. Reese, T.W. Small and P.J. Weldon. 2000. An experiment on the ability of free-ranging turkey vultures (Cathartes aura) to locate carrion by chemical cues. Chemoecology 10: 49-50. Miller, A.H. 1932. Observations on some breeding birds of El Salvador, Central America. Condor 34: 8-14.

Moller, A.P. 1994. Parasites as an environmental component of reproduction in birds as exemplified by the swallow Hirundo rustica. Ardea 82: 161-172.

Moreau, R.E. 1942. The nesting of African birds in association with other living things. Ibis 84: 240-263.

Moreau, R.E. 1943. Dr. J. G. Myers on migrants and on bird-insect nesting associations. Ibis 85: 97-101.

Morton, E.S. 2000. The European Paper-wasp: A new threat to cavity-nesting birds is coming! Purple Martin Update 9: 12 (purplemartin.org).

Myers, J.G. 1929. The nesting-together of birds, wasps and ants. Proceedings of the Royal Entomological Society of London 4: 80-88.

Myers, J.G. 1935. Nesting associations of birds with social insects. Transactions of the Entomological Society of London 83:11-22.

Nevitt, G. 1999. Foraging by Seabirds on an Olfactory Landscape: The seemingly featureless ocean surface may present olfactory cues that help the wide-ranging petrels and albatrosses pinpoint food sources. American Scientist 87: 46-53.

Newby-Varty, B.V. 1945. Observations made on Umwukwe Ranch, 27 miles north of Banket, S. Rhodesia. Ostrich 16: 218-220.

Newton, I. 1994. The role of nest sites in limiting the numbers of hole-nesting birds: a review. Biological Conservation 70: 265.

O’Donel, H.V. 1934. On the nesting association of an Indian bird, Ploceus megarhynchus, and the jungle bee, Apis indicus. Fabr. Proceedings of the Entomological Society of London 8: 137.

O’Donnell, S. 1993. Interactions of predaceous katydids (Orthoptera: Tettigoniidae) with neotropical social wasps (Hymenoptera: Vespidae): are wasps a defense mechanism or prey? Entomological News 104: 39-42.

Oldroyd, B.P., S.H. Lawler and R.H. Crozier. 1994. Do feral Honey Bees (Apis mellifera) and Regent Parrots (Polytelis anthopeplus) compete for nest sites? Australian Journal of Ecology 19: 444.

Oniki, Y. 1970. Nesting behavior of Reddish Hermits (Phaethornis ruber) and occurrence of wasp cells in nest. Auk 87: 720-728.

Owre, O.T. and P.O. Northington. 1961. Indication of the Sense of Smell in the Turkey Vulture, Cathartes aura (Linnaeus), from Feeding Tests. American Midland Naturalist 66: 200-205.

Peck, M.E. 1910. The effects of natural enemies on the nesting habits of some British Honduras birds. Condor 12: 53-60.

Peterson, B. and G. Gauthier. 1985. Nest site use by cavity-nesting birds of the Cariboo Parkland, British Columbia. Wilson Bulletin 97: 319-331.

Petit, L.J. 1991. Adaptive tolerance with cowbird parasitism by Prothonotary Warblers: a consequence of nest site limitations? Animal Behaviour 41: 425-432.

Pickett, K.M. and J.W. Wenzel. 2000. High productivitiy in haplometrotic colonies of the introduced paper wasp Polistes dominulus (Hymenoptera: Vespidae; Polistinae). Journal of the New York Entomological Society 108: 314-325.

Pizzey, G. and R. Doyle. 1980. A Field Guide to the Birds of Australia. Princeton University Press, Princeton.

Pogue, D.W. and G.D. Schnell. 1994. Habitat characterization of secondary cavity-nesting birds in Oklahoma. Wilson Bulletin 106: 203-226.

Poulton, E.B. 1932. Hive-bees occupying a hole in a chestnut tree in which a Jackdaw was nesting. Proceedings of the Entomological Society of London 6: 82.

Quelch, J.J. 1901. Animal Life in British Guiana. Argosy Publishers Limited, Georgetown.

Quinn, J.L., J. Prop, Y. Kokorev and J.M. Black. 2003. Predator protection of similar habitat selection in Red-breasted Goose nesting associations: extremes along a continuum. Animal Behavior 65:297-307.

Quinn, J.L. and M. Ueta. 2008. Protective nesting associations in birds. Ibis 150: 146-167.

Reeve, H.K. 1991. Polistes. In The Social Biology of Wasps. K.G. Ross and R.W. Matthews, Eds. Cornell University Press, Ithaca, N.Y. Pages 99-148.

Richards, O.W. and M.J. Richards. 1951. Observations on the social wasps of South America (Hymenoptera, Vespidae). Transactions of the Royal Entomological Society of London 102: 1-169.

Robb, J.R. and T.A. Bookhout. 1995. Factors influencing Wood Duck use of natural cavities. Journal of Wildlife Management 59: 372.

Robinson, S.K. 1985. Coloniality in the yellow-rumped cacique as a defense against nest predators. Auk 102: 506-519.

Sanborn, C.C. 1932. A Hornet-Wren nest. Auk 49: 224.

Sedgewick, E.H. 1947. Northern Territory bird notes. Emu 46: 349-378.

Schafer, E. 1952. Querschnitt durch den Parque national de Aragua. . Journal für Ornithologie 93: 343

Schmidt, J.O. 1990. Hymenopteran venoms: striving toward the ultimate defence against vertebrates . In Insect Defences: Adaptive Mechanisms and Strategies of Prey and Predators. D.L. Evans and J.O. Schmidt, Eds. Pages 387-419.

Schmidt, J.O. and R. Hurley. 1995. Selection of nest cavities by Africanized and European Honey Bees. Apidologie 26: 467-475.

Sherry, T.W. 1983. Todirostrum cinereum (Espatulilla Comun, Peclita, Tontilla, Common Tody-flycatcher). In Costa Rican Natural History, D.H. Janzen, Ed University of Chicago Press, Chicago. Pages 608-610.

Short, L.L. 1979. Burdens of the picid hole-nesting habit. Wilson Bulletin 91: 16-28.

Sergio, F. and G. Bogliani. 2001. Nest defense as parental care in the Northern Hobby (Falco subbuteo). Auk 118: 1047-1052.

Sick, H. 1993. Birds in Brazil. Princeton University Press, Princeton.

Skead, C.J. 1967. The sunbirds of southern Africa: also the sugarbirds, the white-eyes and the Spotted Creeper. Trustees of the South Africa Bird Book Fund. Balkema, Cape Town.

Skutch, A.F. 1960. Life histories of Central American birds. II. Pacific Coast Avifauna, No. 34. Cooper Ornithological Society, Berkley.

Skutch, A.F. 1969. Life histories of Central American birds. III. Pacific Coast Avifauna, No. 35. Cooper Ornithological Society, Berkley.

Skutch, A.F. 1972. Studies of Tropical American Birds. Publications of the Nuttall Ornithological Club 10: 1-228. Cambridge, Mass.

Skutch, A.F. 1976. Parent birds and their young. University of Texas Press, Austin, Texas.

Slud, P. 1964. The birds of Costa Rica: distribution and ecology. Bulletin of the American Museum of Natural History. Volume 128. New York.

Smith, N.G. 1968. The advantage of being parasitized. Nature 219: 690-694.

Stanback, M., A. Mercadante, W. Anderson, H. Burke and R. Jameson. 2009. Nest site competition between cavity nesting passerines and golden paper wasps Polistes fuscatus. Journal of Avian Biology 40: 650-652.

Starr, C.K. 1985. A simple pain scale for field comparison of hymenopteran stings. Journal of Entomological Science 20: 225-231.

Starr, C.K. 1988. The nesting association of the social wasps Mischocyttarus immarginatus and Polybia spp. in Costa Rica. Biotropica 20:171-173.

Starr, C. K. 1991. The nest as the locus of social life. In The Social Biology of Wasps. K. G. Ross and R. W. Matthews, eds. Cornell University Press. Ithaca, NY. Pages 520-539.

Stiles, F.G., A.F. Skutch and D. Gardner. 1989. A Guide to the Birds of Costa Rica. Cornell University Press, Ithaca, N.Y.

Summers, R.W., L.G. Underhill, E.E. Syroechkovski Jr, H.G. Lappo, R.P. Pyrs-Jones and V. Karpov. 1994. The breeding biology of Dark-bellied Brent Geese Branta b. bernicla and King Eiders Somateria spectabilis on the northeastern Taimyr Peninsula, especially in relation to Snowy Owl Nyctea scandiaca nests. Wildfowl 45: 110-118.

Sutton, G.M. 1948. The nest and eggs of the White-bellied Wren. Condor 50: 101-112.

Thomas, D.K. 1960. Notes on birds breeding in Tanganyika. Tanganyika Notes and Records 55: 225-243.

Todd, W.E.C. and M.A. Carriker Jr. 1922. The birds of Santa Maria region of Columbia: a study in altitudinal distribution. Annals of Carnegie Museum 14.

Tremoleras, J. 1929. Curiosa nidificacion del Hornero. El Hornero (Buenos Aires) 4: 294-298.

Troetschler, R. G. 1976. Acorn Woodpecker breeding strategy as affected by starling nest-hole competition. Condor 78: 151-165.

Twedt, D.J. and J.L. Henne-Kerr. 2001. Artificial cavities enhance breeding bird densities in managed cottonwood forests. Wildlife Society Bulletin 29: 680-687.

Van Rossem, A. 1914. Notes on the Derby Flycatcher. Condor 16: 11-13.

Vaughan, C., N. Nemeth and L. Marineros. 2003. Ecology and management of natural and artificial Scarlet Macaw (Aro macao) nest cavities in Costa Rica. Ornitologia Neotropical 14: 381-396.

Vierling, K.T. 1998. Interactions between European Starlings and Lewis’ Woodpeckers at nest cavities. Journal of Field Ornithology 69: 376-379.

Waters, J.R., B.R. Noon and J. Verner. 1990. Lack of nest site limitation in a cavity-nesting bird community. Journal of Wildlife Management 54: 239-245.

Wenzel, B.M. 1971. Olfactory sensation in the kiwi and other birds. Annals of the New York Academy of Sciences 188: 183-193.

Wenzel, B.M. 2007. Avian olfaction: then and now. Journal of Ornithology 148: 191-194.

Wenzel, J.W. 1991. Evolution of nest architecture. In The Social Biology of Wasps. K.G. Ross and R.W. Matthews, Eds. Cornell University Press, Ithaca, N.Y. Pages 480-519.

Wenzel, J.W. 1996. Learning, behaviour programs, and higher-level rules in nest construction of Polistes. In Natural History and Evolution of Paper-Wasps. S. Turillazzi and M.J. West-Eberhard, M. J., eds. Oxford University Press, Oxford, England. Pages 58-74.

Weeks, H.P. 1977. Nest reciprocity in Eastern Phoebes and Barn Swallows. Wilson Bulletin 89: 632-635.

Western Australia Museum, 2012. http://museum.wa.gov.au/explore/online- exhibitions/cockatoo-care/feral-bees. Accessed April 25, 2013.

Wetmore, A., R.F. Pasquier and S.L. Olson. 1984. The Birds of the Republic of Panama, Part 4. Passeriformes: Hirundinidae (Swallows) to Fringillidae (Finches). Smithsonian Institution Press, Washington, D.C.

Wheelwright, N.T., J.J. Lawler and J.H. Weinstein. 1997. Nesting selection in Savannah Sparrows: using gulls as scarecrows? Animal Behavior 53: 197-208.

White, H.L. 1922. A collecting trip to Cape York Peninsula. Emu 22: 99-116.

White, T.H. and F.J. Vilella. 2004. Nest management for the Puerto Rican Parrot (Amazona vittata): gaining the technological edge. Ornitologia Neotropical 15: 467.

Whitman, D.W., M.S. Blum and D.W. Alsop. 1990. Allomones: Chemicals for defense. In Insect Defences: Adaptive Mechanisms and Strategies of Prey and Predators. D.L. Evans and J.O. Schmidt, Eds. Pages 289-351.

Wiklund, C.G. 1979. Increased breeding success for Merlins Falco columbarius nesting among colonies of Fieldfares Turdus pilaris. Ibis 121: 109-111.

Winterbottom, J.M. 1939. Miscellaneous notes on some birds of Northern Rhodesia. Ibis 14: 712-734.

Woodall, P.F. 1985. On the life history of the Bronze Manakin. Ostrich 46: 55-86.

Wunderle, J.M. and K.H. Pollock. 1985. A Bananaquit-wasp nesting association and a random choice model. Ornithological Monographs 36: 595-603.

Appendix A. Bird-wasp nesting associations organized by bird.

*Using nest (for breeding and/or roosting) after wasps gone or removed

^Wasp placed nest beside Angola Swallow nest being used by swift

Order FAMILY Bird Taxon Bird Common Name Wasp Taxon Locality Reference Cuculiformes CUCULIDAE (Cuckoos) Crotophaga ani Smooth-billed Ani Polistes sp. Trinidad Williams 1922 (in Myers 1929, 1935) Crotophaga sulcirostris Groove-billed Ani Costa Rica Joyce 1990 Apodiformes APODIDAE (Swifts) Apus caffer White-rumped Swift ^ Kenya Pitman in Moreau 1942 Panyptila cayennensis Lesser Swallow-tailed Swift Polistes sp. South Myers 1935 America Guyana Beebe quoted by Chubb in Myers 1929 Coliiformes COLIIDAE (Mousebirds) Urocolius indicus Red-faced Mousebird West Africa Hoesch 1956 Trogoniformes TROGONIDAE (Trogons) Trogon violaceus Violaceous Trogon * Costa Rica Skutch 1942 in Hindwood 1959

Passeriformes TYRANNIDAE (Tyrant Flycatchers) Camptostoma obsoletum Southern Beardless-tyrant Ecuador Marchant 1960 Hemitriccus rufigularis Buff-throated Tody-tyrant Peru Fitzpatrick, J.W. (pers. comm.) Fluvicola pica Pied Water-Tyrant Polybia rejecta Trinidad, Myers, 1935 Polybia sp. Venezuela Arundinicola leucocephala White-headed Marsh-Tyrant Trinidad Fitzgerald 1938 Pitangus lector Lesser Kiskadee Polybia sp. Brazil Myers 1935 Pitangus sulphuratus Great Kiskadee El Salvador Van Rossem 1914 Polybia sp. South Myers 1935 America Polybia rejecta Trinidad Myers 1935 South Cleare 1923 in America Myers 1929 Myiozetetes similis Social Flycatcher Costa Rica Joyce 1990 El Salvador Van Rossem 1914 Costa Rica Skutch in Hindwood 1955 Myiozetetes grandadensis Gray-capped Flycatcher Costa Rica Skutch 1960, 1972 Legatus leucophaius Piratic Flycatcher Brazil Oniki 1970 Costa Rica Skutch 1960 * Costa Rica Skutch 1942 in Hindwood 1959 Surinam Haverschmidt 1957 Costa Rica, Skutch 1972 Venezuela Tyrannus sp. Kingbird sp. Chartergus sp. Brazil Sick 1993 Tyrannus melancholicus Tropical Kingbird Polistes canadensis Trinidad Williams 1922 53

(Myers, 1929) Todirostrum maculatum Spotted Tody-Flycatcher Surinam Hamerschmidt 1955, 1957 Todirostrum cinereum Common Tody-flycatcher Costa Rica Sherry 1983 Todirostrum nigriceps Black-headed Tody-flycatcher Costa Rica Skutch 1972 Todirostrum chryscrotaphum Yellow-browed Tody-flycatcher Peru Robinson, S.K. (pers comm.) Surinam Haverschmidt 1968 Tolmomyias sp. Trinidad Myers 1935 Rhynchocyclus sp Flatbill sp. Polybia sp. Brazil Myers 1935 Tolmomyias sulphurescens Yellow-olive Flycatcher Costa Rica Slud 1964 Agelaia areata Costa Rica Joyce 1990 Apoica pallens Brachygastra mellifica Parachartergus fraternus Polybia occidentalis Polybia rejecta Synoeca septentrionalis Costa Rica Stiles et al. 1989 Venezuela Schafer 1952 Tolmomyias assimilis Yellow-margined Flycatcher Costa Rica Stiles et al. 1989 Tolmomyias poliocephalus Gray-crowned Flycatcher Surinam Haverschmidt 1950 Belize Peck 1910 Tolmomyias flaviventris Yellow-breasted Flycatcher Colombia Todd and Carriker 1922 Polybia occidentalis Surinam Haverschmidt Polybia sp. 1957, 1974 Synoeca surinama TITYRIDAE (Tityras and allies) Pachyramphus aglaiae Rose-throated Becard El Salvador Van Rossem 1914

Pachyramphus rufus Cinereous Becard Guyana Richards and Richards 1951 Trinidad, Cleare 1923 Brazil Myers 1929, 1935a Pachyramphus cinnamomeus Cinnamon Becard Costa Rica Skutch 1969 Pachyramphus polychopterus White-winged Becard Costa Rica Joyce 1990 Surinam Haverschmidt 1968, 1974 Costa Rica Skutch 1969, 1972 FURNARIIDAE (Ovenbirds and Woodcreepers) Furnarius rufus Rufous Hornero Uruguay Tremoleras 1929 Synallaxis sp. Polybia nigriceps Brazil Myers 1935 Synallaxis cinnamomea Stripe-breasted Spinetail Guyana Chubb 1916 Trinidad Lloyd 1897 (in Myers 1929) Certhiaxis cinnamomea Yellow-chinned Spinetail South Myers 1935 America, Trinidad Phacellodomus rufifrons Rufous-fronted Thornbird Brazil Sick 1993 ACANTHIZIDAE (Thornbills and allies) Gerygone sp. Gerygone sp. Polistes and perhaps Australia Alexander 1931 Ropalidia in Myers 1935 Gerygone chloronota Green-backed Gerygone Australia Sedgewick 1947 Australia Chisholm 1952 Gerygone palpebrosa Fairy Gerygone Australia Chisholm 1952 (and references listed within) Australia Chisholm 1952 Australia Barnard 1911, 1926 Australia Campbell and

Barnard 1917 Australia Alexander in Poulton 1931 Gerygone olivacea White-throated Gerygone Australia (McLennan 1922 in Chisholm 1952) Australia White 1922 Gerygone magnirostris Large-billed Gerygone Australia Chisholm 1952 Australia Cornwall 1910 Australia Marshall 1933 Gerygone fusca Western Gerygone Australia Marshall 1933 Gerygone levigaster Mangrove Gerygone Australia Chisholm 1952 PLATYSTEIRIDAE (Wattle-eyes and Batises) Platysteira cyanea Brown-throated Wattle-eye Polybioides tabidus Cameroon Dejean and Fotso 1995 LANIIDAE (Shrikes) Lanius collaris Common Fiscal Polybioides tabidus Cameroon Dejean and Fotso 1995 CORVIDAE (Crows, Jays and Magpies) Corvus monedula Eurasian Jackdaw Apis mellifera England Poulton 1932 in Myers 1935 HIRUNDINIDAE (Swallows) Tachycineta bicolor Tree Swallow Polistes dominula Canada Earley pers .obs. (Ontario) Hirundo rustica Barn Swallow U.S.A. Joyce 1990 (New York) Hirundo angolensis Angola Swallow Kenya Pitman (in Moreau 1942) Cecropis abyssinica Lesser Striped-Swallow Kenya Pitman (in Moreau 1942) Delichon urbicum Common House-Martin Vespa sylvestris England Frohawk 1935 TROGLODYTIDAE (Wrens) Campylorhynchus sp. Wren sp. Polybia sp. Colombia Myers 1935 56

Campylorhynchus rufinucha Rufous-naped Wren Costa Rica Slud 1964 Parachartergus fraternus Costa Rica Joyce 1990 Polybia occidentalis Polybia rejecta Trigona silvestriana (bee) El Salvador Van Rossem 1914 Campylorhynchus griseus Bicolored Wren Venezuela Austad, S. (pers. comm.) Thryothorus felix Happy Wren Mexico Grant 1966 Thryothorus sinaloa Sinaloa Wren Mexico Grant 1966 Thryothorus pleurostictus Banded Wren Costa Rica Arnold 1966 Costa Rica Skutch 1976 Agelaia areata Costa Rica Joyce 1990 Apis mellifera (bee) Apoica pallens Brachygastra mellifica Mischocyttarus immarginatus Parachartergus fraternus Polistes canadensis Polistes instabilis Polistes major Polybia diguetana Polybia occidentalis Polybia rejecta Synoeca septentrionalis Trigona fuscipennis (bee) Trigona sp. El Salvador Miller 1932 Thryothorus rufalbus Rufous-and-white Wren Costa Rica Alfaro 1929 (in Harrower 1935) Costa Rica Arnold 1966 Costa Rica Pers obs

Thryothorus superciliaris Superciliated Wren Ecuador, Marchant 1960 Peru Thryothorus ludovicianus Carolina Wren * U.S.A. Kalter 1932 (OH) Dolichovespula maculata * U.S.A. Brooks 1932 and (WV) Page in Brooks 1932 U.S.A. McComb and (LA) Noble, 1982 Troglodytes aedon House Wren * U.S.A. (IL) Sanborn 1932 Uropsila leucogastra White-bellied Wren Mexico Sutton 1948 PYCNONOTIDAE (Bulbuls) Pycnonotus barbatus Common Bulbul Polybioides tabidus Cameroon Dejean and Fotso, 1995 TURDIDAE (Thrushes) Turdus? (Planesticus)sp. Thrush sp. South Hindwood 1955 America DICAEIDAE (Flowerpeckers) Dicaeum minullum Plain Flowerpecker India Baker 1931 in Myers 1935 PARULIDAE (New World Warblers) Protonotaria citrea Prothonotary Warbler Polistes sp. U.S.A. Blem and Blem, (VA) 1991 COEREBIDAE (Bananaquit) Coereba flaveola Bananaquit Polybia occidentalis Grenada Wunderle and Pollock 1985 Jamaica Gosse 1847 Trinidad Fitzgerald 1938 Polistes canadensis Venezuela, Myers 1929, Polistes sp. West Indies 1935 Tobago Gross 1958 EMBERIZIDAE (Buntings, Sparrows and allies) Tiaris olivacea Yellow-faced Grassquit Polistes sp. Jamaica Gosse 1847 58

Tiaris obscura Dull-colored Grassquit Polistes canadensis Argentina Contino 1968 Sicalis flaveola Saffron Finch Polistes canadensis Argentina Contino 1968 ICTERIDAE (Troupials and allies) Scaphidura oryzivora Giant Cowbird Protopolybia sp. Panama Smith 1968 Agelaia sp. Trigona sp. (bee) Icterus nigrogularis Yellow Oriole South Hindwood 1955 America Icterus gularis Altamira Oriole El Salvador Van Rossem 1914 Icterus pustulatus Streak-backed Oriole Costa Rica Joyce 1990 El Salvador Van Rossem 1914 Icterus xanthornus common name unknown Polybia sp. Guyana Myers 1929 Synoeca sp. Cacicus haemorrhous Red-rumped Cacique Surinam Feekes 1981 Polistes sp. Northern Myers 1929, Polybia rejecta South 1935 America Guyana Quelch 1901 Surinam Haverschmidt 1968 Cacicus uropygialis Scarlet-rumped Cacique Costa Rica Skutch 1972 Panama Wetmore et al. 1984 Cacicus cela Yellow-rumped Cacique Brazil Oniki 1979 Polybia rejecta Northern Myers 1935 Polistes canadensis South Meliponine bee America Guyana Brown 1876 Guyana Quelch 1901 Panama Wetmore et al. 1984

Agelaia flavipennis Peru Robinson 1968, Chartergus artifex 1985 Peru Koepcke 1972 Surinam Haverschmidt 1968 Surinam Feekes 1981 Apoica pallida South Schultz in Myers America 1935 Protopolybia sp. Panama Smith, 1968 Agelaia sp. Trigona sp. (bee) Psarocolius angustifrons Russet-backed Oropendola Peru Koepcke 1972 Peru Robinson, S.K. (pers. comm..) Psarocolius decumanus Crested Oropendula Peru Smith 1968, Koepcke 1972 Psarocolius wagleri Chestnut- headed Oropendula Protopolybia sp. Panama Smith 1968 Agelaia sp. Trigona sp.(bee) Panama Wetmore et al. Psarocolius montezuma Montezuma Oropendula Costa Rica Fraga 1989 THRAUPIDAE (Tanagers and allies) Tachyphonus rufus White-lined Tanager Wasp or bee Brazil Oniki 1979 Ramphocelus carbo Silver-beaked Tanager Wasp or bee Brazil Oniki 1979 Thraupis episcopus Blue-gray Tanager Trinidad Myers 1935 ESTRILDIDAE (Waxbills and allies) Nigrita canicapilla Gray-headed Negrofinch Polybioides tabidus Cameroon Dejean and Fotso, 1995 Uraeginthus angolensis Blue-breasted Cordonbleu Malawi Gray 1945 Belonogaster griseus Zimbabwe Talent 1937 in Moreau 1942 (and other references listed

within) Zimbabwe Newby-Varty 1945 South Skeed 1975 Africa Polistes sp. South Barnard and Ropalidia sp. Africa Markus 1990 Belonogaster sp. South Kruger 1928 in Africa Myers 1935 Tanzania Arthur Loveridge in Poulton 1929 Belonogaster sp. South Marshall in Africa Poulton 1930 Uraeginthus bengalus Red-cheeked Cordonbleu Africa Goodwin 1982 Ghana McCrae and Walsh 1974 Hawaii Berger 1977 Belonogaster griseus Kenya and Various Uganda references in Moreau 1942 Belonogaster griseus South van Someren in Africa Poulton 1929 Uganda Chapin 1954 Uraeginthus cyanocephalus Blue-capped Cordonbleu Tanzania Thomas 1960 Ropalidia cincta Africa Moreau 1942 South van Someren in Africa Poulton 1929 Tanzania Mackworth- Praed and Grant 1960 Pytilia melba Green-winged Pytilia Polistes sp. South Barnard and Ropalidia sp. Africa Markus 1990 Lagonosticta senegala Red-billed Firefinch East Africa Arthur Loveridge

1923 in Poulton 1929 Belonogaster griseus South van Someren in Wasp sp. Africa Poulton 1929 Ropalidia sp. Africa Moreau 1942 Amandava amandava Red Avadavat India Baker 1931 in Myers 1935 Neochmia temporalis Red-browed Finch Polistes humilis Australia Hindwood 1955 Taeniopygia bichenovii Double-barred Finch Polistes humilis Australia Hindwood 1955 Australia Pizzey and Doyle 1980 Spermestes cucullata Bronze Manakin Africa Goodwin 1982 Ghana Beier and Tungbani, 2006 Zimbabwe Woodall 1985 Ropalidia sp. Tanzania Moreau 1936 Belonogaster griseus Africa van Someren in Poulton 1929 Central Collias and Africa Collias 1984 Ropalidia cincta Ghana McCrae and Walsh 1974 Belonogaster griseus Africa Van Someren in Myers 1935 Africa In Myers 1929 Spermestes bicolor Black-and-white Manakin Africa Van Someren in Myers 1935 Polybioides tabidus Cameroon Dejean and Fotso 1995 Belonogaster griseus Africa Van Someren in Poulton 1929 in Moreau 1942 Euodice cantans African Silverbill Sudan Myers (in

Moreau 1943) Euodice malabarica Indian Silverbill Hawaii Berger 1975, 1977 Lonchura punctulata Nutmeg Manakin Polistes exclamans Hawaii Berger 1975, 1977 Polistes humilis Australia Hindwood 1955 (NSW) NECTARINIIDAE (Sunbirds) Anthreptes longuemarei Western Violet-backed Sunbird Sudan Myers in Moreau 1943 Anthreptes orientalis Kenya Violet-backed Sunbird Ropalidia cincta Tanzania Moreau 1942 Ropalidia nobilis Hedydipna collaris Collared Sunbird Ropalidia sp. and bee Tanzania Moreau 1936 Nigeria Searle 1938 in Moreau 1942 Hedydipna collaris Collared Sunbird Polybioides tabidus Cameroon Dejean and Fotso, 1995 Cyanomitra veroxii Mouse-colored Sunbird Tanzania Pakenham in Moreau 1942 Chalcomitra senegalensis Scarlet-chested Sunbird Africa Skead 1967 Tanzania Moreau 1936, 1942 Zimbabwe Newby-Varty 1945 Cinnyris bifasciatus Purple-banded Sunbird Tanzania Pakenham in Moreau 1943 Cinnyris talatala White-breasted Sunbird Malawi Skead 1967 Cinnyris asiaticus Purple Sunbird India Baker 1931 in Myers 1935 Aethopyga siparaja Eastern Crimson Sunbird bee India Baker 1931 in Myers 1935 PASSERIDAE (Old World Sparrows) Passer eminibey Chestnut Sparrow Sudan Myers in Moreau

1943 PLOCEIDAE (Weavers and Allies) Bubalornis albirostris White-billed Buffalo Weaver West Africa Hoesch 1956 Dinemellia dinemelli White-headed Buffalo Weaver Sudan Myers (Moreau 1943) Sporopipes frontalis Speckle-fronted Weaver Ropalida cincta Ghana Beier sand Tungani 2006 Philetairus socius Social Weaver West Africa Hoesch 1956 Ploceus luteolus Little Weaver Sudan Lynes 1924 Sudan Myers in Moreau 1943 Ploceus ocularis Spectacled Weaver Polybioides tabidus Cameroon Dejean and Fotso 1995 Ploceus intermedius Lesser Masked-Weaver West Africa Hoesch 1956 Ploceus velatus Southern Masked-Weaver Malawi Gray 1945 South Hoesch 1956 Africa Zimbabwe Porter in Moreau 1942 Zambia Winterbottom 1939 Ploceus heuglini Heuglin’s Masked-Weaver Wasps and bees Nigeria Elgood and Ward 1960 Ghana Grimes 1973 Wasps and bees Sudan Myers in Moreau 1943 Ropalidia cincta Ghana, McCrae and Nigeria Walsh 1974 Ploceus cucullatus Village Weaver Nigeria Elgood and Ward 1960 Haiti Myers 1935 Ploceus manyar Streaked Weaver India Baker 1931 Ploceus philippinus Baya Weaver Singapore Hindwood 1955 64

Baya Weaver Vespa affinia Singapore Bird study group 2008 – how do I cite a website? Ploceus hypoxanthus Asian Golden Weaver Burma Baker 1931, 1934 Ploceus megarhynchus Yellow Weaver Apis cerana India O`Donel 1934 Ploceus benghalensis Bengal Weaver Burma Baker 1931

Appendix B. Bird-wasp nesting associations organized by wasp

*Using nest (for breeding and/or roosting) after wasps gone or removed

^Wasp placed nest beside Angola Swallow nest being used by swift

Wasp/Bee Bird Scientific Name Bird Common Name Locality Reference Agelaia sp. Cacicus cela Yellow-rumped Cacique Panama Smith, 1968 Psarocolius wagleri Chestnut- headed Oropendula Panama Smith 1968 Scaphidura oryzivora Giant Cowbird Panama Smith 1968 Agelaia areata (Say) Thryothorus pleurostictus Banded Wren Costa Rica Joyce 1990 Tolmomyias sulphurescens Yellow-olive Flycatcher Costa Rica Joyce 1990 Agelaia flavipennis (Ducke) Cacicus cela Yellow-rumped Cacique Peru Robinson 1968, 1985 Apis cerana Fabricius Ploceus megarhynchus Yellow Weaver India O`Donel 1934 Apis mellifera Linnaeus Corvus monedula Eurasian Jackdaw England Flinthoff, Poulton 1932 in Myers, 1935 Thryothorus pleurostictus Banded Wren Costa Rica Joyce 1990 Apoica pallens (Fabricius) Thryothorus pleurostictus Banded Wren Costa Rica Joyce 1990 Tolmomyias sulphurescens Yellow-olive Flycatcher Costa Rica Joyce 1990 Apoica pallida (Olivier) Cacicus cela Yellow-rumped Cacique South Schultz in Myers 1935 America Belonogaster sp. Uraeginthus angolensis Blue-breasted Cordonbleu South Kruger 1928 in Myers Africa 1935 South Marshall in Poulton 1930 Africa Belonogaster griseus Lagonosticta senegala Red-billed Firefinch South van Someren in Poulton (Fabricius) Africa 1929 Spermestes bicolor Black-and-white Manakin Africa Van Someren in Poulton 1929 in Moreau 1942 Spermestes cucullata Bronze Manakin Africa Van Someren in Myers 1935 Uraeginthus angolensis Blue-breasted Cordonbleu Zimbabwe Talent 1937 in Moreau 1942 (and other

references listed within) Kenya and Various refences in Uganda Moreau 1942 South van Someren in Poulton Africa 1929 Brachygastra mellifica (Say) Thryothorus pleurostictus Banded Wren Costa Rica Joyce 1990 Tolmomyias sulphurescens Yellow-olive Flycatcher Costa Rica Joyce 1990 Chartergus sp. Tyrannus sp. Brazil Sick 1993 Chartergus artifex (Christ) Cacicus cela Yellow-rumped Cacique Peru Robinson 1968, 1985 Dolichovespula maculata Thryothorus ludovicianus Carolina Wren * U.S.A. (W. Brooks 1932 and Page in (Linnaeus) Va.) Brooks 1932 Dolichovespula sylvestris Delichon urbicum Common House-Martin England Frohawk 1935 (Scopoli) Mischocyttarus immarginatus Thryothorus pleurostictus Banded Wren Costa Rica Joyce 1990 Richards Parachartergus fraternus Campylorhynchus rufinucha Rufous-naped Wren Costa Rica Joyce 1990 (Gribodo) Thryothorus pleurostictus Banded Wren Costa Rica Joyce 1990 Tolmomyias sulphurescens Yellow-olive Flycatcher Costa Rica Joyce 1990 Polistes sp. Cacicus haemorrhous Red-rumped Cacique Northern Myers 1929, 1935 South America Coereba flaveola Bananaquit Venezuela, Myers 1929, 1935 West Indies Crotophaga ani Smooth-billed Ani Trinidad Williams 1922 (in Myers 1929, 1935) Gerygone sp. Australia Alexander 1931 in Myers 1935 Panyptila cayennensis Lesser Swallow-tailed Swift South Myers 1935 America Protonotaria citrea Prothonotary Warbler U.S.A. Blem and Blem 1991 (Virginia) Pytilia melba Green-winged Pytilia South Barnard and Markus Africa 1990

Tiaris olivacea Yellow-faced Grassquit Jamaica Gosse 1847 Uraeginthus angolensis Blue-breasted Cordonbleu South Barnard and Markus Africa 1990 Polistes canadensis Cacicus cela Yellow-rumped Cacique Northern Myers 1935 (Linnaeus) South America Coereba flaveola Bananaquit Venezuela, Myers 1929, 1935 West Indies Thryothorus pleurostictus Banded Wren Costa Rica Joyce 1990 Tiaris obscura Dull-colored Grassquit Argentina Contino 1968 Sicalis flaveola Saffron Finch Argentina Contino 1968 Tyrannus melancholicus Tropical Kingbird Trinidad Williams 1922 (Myers, 1929) Polistes dominula (Christ) Tachycineta bicolor Tree Swallow Canada Earley pers .obs. (Ontario) Polistes exclamans Viereck Lonchura punculata Nutmeg Manakin Hawaii Berger 1975, 1977 Polistes humilis (Fabricius) Lonchura punculata Nutmeg Manakin Australia Hindwood 1955 Neochmia temporalis Red-browed Finch Australia Hindwood 1955 Taeniopygia bichenovii Double-barred Finch Australia Hindwood 1955 Polistes instabilis Saussure Thryothorus pleurostictus Banded Wren Costa Rica Joyce 1990 Polistes major Beauvois Thryothorus pleurostictus Banded Wren Costa Rica Joyce 1990 Polybia sp. Campylorhychus sp. Colombia Myers 1935 Fluvicola pica Pied Water-Tyrant Trinidad, Myers 1935 Venezuela Icterus xanthornus common name unknown Guyana Myers 1929 Pitangus lictor Lesser Kiskadee Brazil Myers 1935 Pitangus sulphuratus Great Kiskadee South Myers 1935 America Rhynchocyclus sp. Flatbill sp. Brazil Myers 1935 Tolmomyias flaviventris Yellow-breasted Flycatcher Surinam Haverschmidt, 1957, 1974 Polybia diguetana Buysson Thryothorus pleurostictus Banded Wren Costa Rica Joyce 1990 Polybia occidentalis (Olivier) Campylorhynchus rufinucha Rufous-naped Wren Costa Rica Joyce 1990 68

Coereba flaveola Bananaquit Grenada Wunderle and Pollock 1985 Thryothorus pleurostictus Banded Wren Costa Rica Joyce 1990 Tolmomyias flaviventris Yellow-breasted Flycatcher Surinam Haverschmidt, 1957, 1974 Tolmomyias sulphurescens Yellow-olive Flycatcher Costa Rica Joyce 1990 Polybia nigriceps Zavattari Synallaxis sp. Brazil Myers 1935 Polybia rejecta (Fabricius) Cacicus cela Yellow-rumped Cacique Northern Myers 1935 South America Cacicus haemorrhous Red-rumped Cacique Northern Myers 1929, 1935 South America Campylorhynchus rufinucha Rufous-naped Wren Costa Rica Joyce 1990 Fluvicola pica Pied Water-Tyrant Trinidad, Myers, 1935 Venezuela Pitangus sulphuratus Great Kiskadee Trinidad Myers 1935 Thryothorus pleurostictus Banded Wren Costa Rica Joyce 1990 Tolmomyias sulphurescens Yellow-olive Flycatcher Costa Rica Joyce 1990 Polybioides tabidus Hedydipna collaris Collared Sunbird Cameroon Dejean and Fotso, 1995 (Fabricius) Lanius collaris Common Fiscal Cameroon Dejean and Fotso, 1995 Nigrita canicapilla Gray-headed Negrofinch Cameroon Dejean and Fotso, 1995 Platysteira cyanea Brown-throated Wattle-eye Cameroon Dejean and Fotso, 1995 Ploceus ocularis Spectacled Weaver Cameroon Dejean and Fotso, 1995 Pycnonotus barbatus Common Bulbul Cameroon Dejean and Fotso, 1995 Spermestes bicolor Black-and-white Manakin Cameroon Dejean and Fotso, 1995 Protopolybia sp. Cacicus cela Yellow-rumped Cacique Panama Smith, 1968 Psarocolius wagleri Chestnut- headed Oropendula Panama Smith 1968 Scaphidura oryzivora Giant Cowbird Panama Smith 1968 Ropalidia sp. Hedydipna collaris Collared Sunbird Tanzania Moreau 1936 Lagonosticta senegala Red-billed Firefinch Africa Moreau 1942 Pytilia melba Green-winged Pytilia South Barnard and Markus

Africa 1990 Spermestes cucullata Bronze Manakin Tanzania Moreau 1936 Sporopipes frontalis Speckle-fronted Weaver Ghana Beier sand Tungani, 2006 Uraeginthus angolensis Blue-breasted Cordonbleu South Barnard and Markus Africa 1990 Ropalidia cincta (Lepeletier) Anthreptes orientalis Kenya Violet-backed Sunbird Tanzania Moreau 1942 Ploceus heuglini Heuglin’s Masked-Weaver Ghana, McCrae and Walsh 1974 Nigeria Spermestes cucullata Bronze Manakin Ghana McCrae and Walsh 1974 Uraeginthus cyanocephalus Blue-capped Cordonbleu Africa Moreau 1942 Ropalidia nobilis Anthreptes orientalis Kenya Violet-backed Sunbird Tanzania Moreau 1942 (Gerstaecker) Synoeca sp. Icterus xanthornus common name unknown Guyana Myers 1929 Synoeca septentrionalis Thryothorus pleurostictus Banded Wren Costa Rica Joyce 1990 Richards Tolmomyias sulphurescens Yellow-olive Flycatcher Costa Rica Joyce 1990

Synoeca surinama Linnaeus Tolmomyias flaviventris Yellow-breasted Flycatcher Surinam Haverschmidt, 1957, 1974 Meliponine bee Cacicus cela Yellow-rumped Cacique Northern Myers 1935 South America Trigona sp. (bee) Cacicus cela Yellow-rumped Cacique Panama Smith 1968 Psarocolius wagleri Chestnut- headed Oropendula Panama Smith 1968 Scaphidura oryzivora Giant Cowbird Panama Smith 1968 Thryothorus pleurostictus Banded Wren Costa Rica Joyce 1990 Trigona fuscipennis Friese Thryothorus pleurostictus Banded Wren Costa Rica Joyce 1990 Trigona silvestriana Vachal Campylorhynchus rufinucha Rufous-naped Wren Costa Rica Joyce 1990 Vespa affinis (Linnaeus) Ploceus philippinus Baya Weaver Singapore Bird ecology study group 2007