red-winged blackbird aggression but not nest defense ... · !1 1! red-winged blackbird aggression...

Red-winged blackbird aggression but not nest defensesuccess is predicted by exposure to brood parasitism bybrown-headed cowbirdsKen Yasukawa, Josie Lindsey-Robbins, Carol S Henger, Mark E. Hauber

The brown-headed cowbird (Molothrus ater) is an obligate brood parasite known to useover 200 host species. The red-winged blackbird (Agelaius phoeniceus) is a commonlyused accepter host that incubates cowbird eggs and cares for cowbird nestlings andfledglings. This host species, however, may reduce the risk of parasitism with afrontloaded antiparasite strategy in which it attacks parasites that approach active hostnests. To test this frontloaded parasite-defense hypothesis (FPDH), we presentedtaxidermic models of a female northern cardinal (Cardinalis cardinalis), which representsno threat to redwings, a male cowbird, which cannot lay a parasitic egg, and a femalecowbird, together with species- and sex-specific vocalization playbacks for 5 min. Weconducted these presentations at 25 active redwing nests at Newark Road Prairie in south-central Rock County, Wisconsin, USA, where 18% of redwing nests were parasitized bycowbirds in 2015. As predicted by the FPDH, the female cowbird mount elicited the mostaggressive responses and the female cardinal mount the least aggressive, as measured bynumber of times more than one male redwing responded and number of times the malehost attacked the mount, and by Principal Component analyses yielding redwingaggressive behavior and intimidation scores. Contrary to the predictions of FPDH regardingthe success of nest defense behaviors, male redwings responding at naturally parasitizednests were significantly more likely to attack the mount than males with nests that werenot parasitized. We also compared our results with those of a study using the samemethods and conducted in New York State where cowbird parasitism was rare. Wisconsinredwings were more aggressive toward the female cowbird mount than redwings in NewYork State. Red-winged blackbirds appear to frontload their antiparasite defenses and theaggressiveness, but the apparent success of those defenses depends on individual andpopulation-level experience with parasites.

PeerJ PrePrints | https://dx.doi.org/10.7287/peerj.preprints.1274v1 | CC-BY 4.0 Open Access | rec: 31 Jul 2015, publ: 31 Jul 2015

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Red-winged blackbird aggression but not nest defense success is predicted by 1

exposure to brood parasitism by brown-headed cowbirds 2

3

ABSTRACT 4

The brown-headed cowbird (Molothrus ater) is an obligate brood parasite known to use over 200 5

host species. The red-winged blackbird (Agelaius phoeniceus) is a commonly used acceptor host 6

that incubates cowbird eggs and cares for cowbird nestlings and fledglings. This host species, 7

however, may reduce the risk of parasitism with a frontloaded antiparasite strategy in which it 8

attacks parasites that approach active host nests. To test this frontloaded parasite-defense 9

hypothesis (FPDH), we presented taxidermic models of a female northern cardinal (Cardinalis 10

cardinalis), which represents no threat to redwings, a male cowbird, which cannot lay a parasitic 11

egg, and a female cowbird, together with species- and sex-specific vocalization playbacks for 5 12

min. We conducted these presentations at 25 active redwing nests at Newark Road Prairie in 13

south-central Rock County, Wisconsin, USA, where 18% of redwing nests were parasitized by 14

cowbirds in 2015. As predicted by the FPDH, the female cowbird mount elicited the most 15

aggressive responses and the female cardinal mount the least aggressive, as measured by number 16

of times more than one male redwing responded and number of times the male host attacked the 17

mount, and by Principal Component analyses yielding redwing aggressive behavior and 18

intimidation scores. Contrary to the predictions of FPDH regarding the success of nest defense 19

behaviors, male redwings responding at naturally parasitized nests were significantly more likely 20

to attack the mount than males with nests that were not parasitized. We also compared our results 21

with those of a study using the same methods and conducted in New York State where cowbird 22

parasitism was rare. Wisconsin redwings were more aggressive toward the female cowbird 23


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mount than redwings in New York State. Red-winged blackbirds appear to frontload their 24

antiparasite defenses and the aggressiveness, but the apparent success of those defenses depends 25

on individual and population-level experience with parasites. 26

27

Authors 28

Ken Yasukawa1, Josie Lindsey-Robbins1, Carol S. Henger2,3, and Mark E. Hauber2 29

1 Beloit College, Department of Biology, Beloit, WI, USA 30

2 Department of Psychology, Hunter College, and The Graduate Center of the City University of 31

New York, NY, USA 32

3 Department of Biological Sciences, Fordham University, NY, USA 33

34

Corresponding Author 35

Ken Yasukawa, Beloit College, Department of Biology, 700 College Street, Beloit, WI 53511, 36

[email protected] 37

38

39


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INTRODUCTION 40

41

About 1% of bird species are obligate brood parasites, whose reproductive strategy depends 42

exclusively on host species to build nests, incubate eggs, and care for their nestlings and 43

fledglings (Davies, 2010). The interactions of brood parasites and their hosts are a highly studied 44

model system of co-evolution because of the tractability of reciprocal adaptations between hosts 45

and parasites across different evolutionary timescales (Rothstein, 1990). In these model systems, 46

natural selection favors adaptations of the parasite that increase its ability to reproduce, including 47

the ability to locate suitable host nests, place eggs in those nests, and ensure that the host parent 48

will care for the parasitic young (Moskàt, Barta, Hauber & Honza, 2006). However, because of 49

the fitness disadvantages of parasite eggs and nestlings for the host, natural selection also favors 50

adaptations of the host that increase its ability to avoid being parasitized, including placing nests 51

in inaccessible locations (Hauber, 2001; Hoover & Robinson, 2007) or in dense cover (Clotfelter, 52

1998; Hauber & Russo, 2000), abandoning parasitized nests (Graham, 1988; Yasukawa & 53

Werner, 2007), recognizing and ejecting, puncturing, or burying parasite eggs (Graham, 1988; 54

Valera, Hoi & Schleicher, 1997; Lahti, 2006), or directing parental care to their own offspring 55

instead of the foreign chick (Lichtenstein 2001; Peer, Rothstein, Kuehn & Fleischer, 2005). 56

These host adaptations exert selective pressures on the parasites to become better at exploiting 57

their hosts, and the parasite counter-adaptations in turn favor hosts that are even better at 58

avoiding parasitism. This process is described as co-evolutionary arms race in which an 59

adaptation in one species selects for a counter-adaptation in the other (Dawkins & Krebs, 1979). 60

The brown-headed cowbird (Molothrus ater; hereafter “cowbird”) is a generalist obligate 61

brood parasite in that it uses over 200 hosts species to rear its offspring (Friedmann, 1971). To 62


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reproduce successfully, a cowbird must 1) find a suitable host nest, 2) determine that the host is 63

actively laying, 3) evade behavioral host defenses, 4) rapidly lay its egg, 5) remove a host egg, 6) 64

escape undetected. 65

The red-winged blackbird (Agelaius phoeniceus; hereafter “redwing”) is a commonly 66

used host species that accepts and incubates cowbird eggs, and cares for cowbird nestlings and 67

fledglings (Rothstein, 1975a) despite the fitness cost of parasitism (Røskaft, Orians & Beletsky, 68

1990; Clotfelter & Yasukawa, 1999; Hoover, Yasukawa & Hauber, 2006). Because they are so 69

common, redwings may be the host species that produces the greatest number of cowbird 70

fledglings across this parasite’s range (Lowther, 1993). Many authors have asked why redwings 71

do not eject cowbird eggs to prevent the recoverable costs of parasitism (Rothstein, 1975a; 72

Røskaft, Orians & Beletsky, 1990; Clotfelter & Yasukawa, 1999; Henger & Hauber, 2014), and 73

several hypotheses have been proposed to explain this failure to eject cowbird eggs. Specifically, 74

the evolutionary lag hypothesis proposes that redwings have not had enough time to evolve 75

ejection behavior (Ward, Lindholm & Smith, 1996), whereas the evolutionary equilibrium 76

hypothesis suggests that the cost of ejection is too great or the benefit too small to make ejection 77

adaptive (Rohwer, Spaw & Røskaft, 1989; Lorenzana & Sealy, 1999). Alternatively, mechanical 78

or perceptual constraints may prevent egg or chick ejection even if it were evolutionarily 79

advantageous (Rohwer & Spaw, 1988). 80

Rothstein (1970) noted that the most effective antiparasite defense is to avoid being 81

parasitized in the first place, thus one strategy to reduce the cost of cowbird parasitism is for 82

redwings to frontload nest defense against cowbirds (Welbergen & Davies, 2009; Kilner & 83

Langmore, 2011; Feeney, Welbergen & Langmore, 2012; Feeney & Langmore, 2015). One 84

potentially frontloaded defense is to begin incubating eggs prior to clutch completion to limit 85


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cowbird access to the nest (Uyehara & Narins, 1995; Clotfelter & Yasukawa, 1999). Redwings 86

also have a variety of antipredator behaviors (Yasukawa, Whittenberger & Nielsen, 1992; 87

Beletsky 1996), which could be also used to prevent parasite access to the vicinity of their nests 88

(Henger & Hauber, 2014). Alarm calling, mobbing, and physically attacking cowbird intruders, 89

as if nest predators, have all been observed at redwing nests during experiments in which 90

taxidermic mounts of female cowbirds were presented (reviewed by Henger & Hauber 2014). 91

These defenses appear to prevent the cowbird from approaching the nest, laying its egg, and 92

removing a redwing egg. 93

We presented taxidermic mounts of female and male cowbirds as well as a female 94

northern cardinal (Cardinalis cardinalis; hereafter "cardinal") to test the hypothesis that 95

redwings frontload their antiparasite defenses by aggressively preventing female cowbirds from 96

approaching and parasitizing their nests (Feeney, Welbergen & Langmore, 2012; Henger & 97

Hauber, 2014). We used a female cardinal as an experimental control because cardinals co-occur 98

with redwings, are approximately the same size as cowbirds, and are neither brood parasites nor 99

nest predators (Halkin & Linville, 1999). 100

101

Comparison 1 102

The frontloaded parasite-defense hypothesis (FPDH) predicts that the female cowbird mount will 103

elicit the most aggressive host responses because it represents the greatest threat to the fitness of 104

the host, whereas hosts will be least aggressive toward the female cardinal mount because it 105

represents the lowest threat to host fitness (Henger & Hauber, 2014). Responses to the male 106

cowbird should be intermediate because male cowbirds cannot lay parasitic eggs, but they do 107

attract and defend females, and may assist the female in searching for host nests (Strausberger, 108


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1998). 109

110

Comparison 2 111

As with antipredator behavior (Knight & Temple, 1986; Curio, 1993; Martin, 2014), 112

aggressiveness toward a brood parasite may be affected by past experience with brood parasites 113

or parasitism (Robertson & Norman, 1976, 1977). We compared the range and extent of 114

aggressive behaviors exhibited by redwings locally at nests that had been naturally parasitized by 115

cowbirds with those that had not been parasitized to determine whether experience with cowbird 116

parasites influences redwing antiparasite defense. The FPDH predicts a negative relationship 117

between nest defense intensity and parasitism itself, as more aggressive defenders should be 118

more successful at preventing parasitism. 119

120

Comparison 3 121

The intensity of antiparasite defense is also thought to be a positive function of the incidence of 122

population-level risk of parasitism (Rothstein, 1975b; Robertson & Norman, 1976) or the 123

historical duration of parasite-host sympatry (Robertson & Norman, 1977; Freeman, Gori & 124

Rohwer, 1990). However, the FDPH hypothesis specifically predicts that more aggressive 125

responses should yield lower parasitism rates. Accordingly, Freeman, Gori & Rohwer (1990) 126

compared results of 16 studies of cowbird parasitism of redwings and found higher rates of 127

parasitism in locations where cowbirds and redwings have a long history of parasitism than in 128

locations where the two species have only recently come into contact. Robertson & Norman 129

(1977) found that hosts with the longer history of sympatry with cowbirds were more aggressive 130

than hosts that became sympatric more recently. In a test of this directional selection hypothesis, 131


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but contrary to the expectations of FDPH, Robertson & Norman (1977) found a positive 132

correlation across species between aggression toward model cowbirds and rate of parasitism. 133

However, many of these previous studies used different methodologies to assess nest defense by 134

redwings. Here we compared data collected using the same experimental methods regarding the 135

antiparasite aggression of redwings between our Wisconsin study area where parasitism is 136

common (since 1984: 15% of 1942 redwing nests were parasitized by cowbirds, and 18% in 137

2015) and that of redwings in New York State where parasitism is rare (0% in Ithaca, NY 138

between 1997 and 2002, and 8.3% in 2010 for the sites combined from Henger & Hauber, 2014). 139

140

MATERIALS & METHODS 141

142

Study species and location 143

We studied the antiparasitic behavior of redwings defending active nests at Newark Road Prairie 144

in Rock County, Wisconsin, USA (42o32'N, 89o08'W) from April to July 2015. Newark Road 145

Prairie is a 13-ha wet-mesic remnant prairie and sedge meadow habitat that supports about 35 146

redwing territories (Yasukawa, 1989). All male redwings were banded with USGS numbered 147

aluminum bands and unique color combinations of plastic wraparound bands for individual 148

identification (United States Geological Survey permit # 20438). Most females were not banded. 149

We used the behavior of female and male redwings to locate active redwing nests and monitored 150

their contents throughout the study. We compared results from Newark Road Prairie with those 151

gathered at locations in New York and Ithaca, New York, USA by Henger & Hauber (2014). 152

153

Presentation of mounts 154


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We replicated the methods of Henger & Hauber (2014) using their taxidermic mounts (courtesy 155

of Bill Strausberger) and vocalization playback files to perform presentations at redwing nests 156

with eggs. All presentations occurred between 06:00 and 09:00 CDT. We obtained approval for 157

all activities from the Beloit College Institutional Animal Care and Use Committee (Protocol 158

Number 13-001). 159

In each presentation all three models (female cardinal, male cowbird, female cowbird) 160

were used in a random, balanced order. We pushed a metal rod into the ground 1–3 meters from 161

the nest and clamped a dowel, to which the model was attached, to the rod at a height of ~1.5 m. 162

The model was always positioned facing the nest. The playbacks were composed of 10 163

repetitions of 10 s of vocalization followed by 20 s of silence for a total of 5 min to represent a 164

typical singing schedule. A 3rd generation iPod Touch (Apple Inc., Cupertino, California, USA) 165

was connected to an Ecoxgear ECOXBT speaker (Grace Digital Audio, Peterborough, Ontario, 166

Canada) via an auxiliary cable and played back at normal volume. We used one mount per 167

species/sex, and we acknowledge this methodological limitation explicitly. Two exemplars of 168

each species- and sex-specific vocalization were used for the male cowbird, female cowbird, and 169

female cardinal to avoid pseudoreplication concerns (Henger & Hauber, 2014). 170

Successive presentations at each nest were separated by 30–45 min to allow redwings to 171

return to normal behavior (Honza et al., 2006). Although we presented the three mounts at 50 172

nests, because we used up to four nests on a single male's territory, we restricted our analysis to 173

the first set of mount presentations to each of 25 males to avoid pseudoreplication. By limiting 174

analysis to presentations of all three mounts at one nest per male, we also minimized the chances 175

of using a female more than once even though most females were not banded for individual 176

identification. Banded females were never used more than once. 177


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178

Response variables 179

We recorded the same variables as Henger & Hauber (2014: Supplementary Materials S Table 2) 180

on check sheets using zero-one scan sampling every 15 s for 5 min (20 total scan periods in each 181

presentation). To estimate responses to the three mounts, we chose response variables based on 182

the Principal Components analysis of Henger & Hauber (2014: Supplementary Materials S 183

Tables 3-5). We tested the response variables: 1) number of presentations in which > 1 male 184

responded, 2) number of presentations in which > 1 female responded, 3) number of 15-s periods 185

in which the male flew over the mount, 4) number of periods in which the male attacked the 186

mount (in contrast to Henger & Hauber (2014), we combined hovers, dives, and strikes because 187

they were highly correlated), 5) number of periods in which the male was < 3 m from the mount, 188

6) number of periods in which the male was perched and looking at the mount, 7) number of 189

periods in which the male gave "check" vocalizations, 8) number of periods in which the male 190

gave "whistle" vocalizations, 9) number of times the female struck the mount, and 10) number of 191

periods in which the female perched and looked at the mount. 192

Daily nest checks allowed us to determine whether each nest used in our mount 193

presentations was naturally parasitized by cowbirds. This information was used in a comparison 194

of attacks of the female cowbird mount at parasitized and nonparasitized nests to determine 195

whether recent experience with parasites or parasitism affected host behavior. 196

Comparisons of redwing behavior at Newark Road Prairie (Wisconsin) and New York 197

State used the Principal Components analysis of Henger &Hauber (2014), who focused on four 198

Principal Components named "Aggressive Response," Aggressive Male Vocalizations," "Close 199

Male, Female Any Distance," and "Intimidation." We used these same four components to 200


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calculate PC scores for our 25 Wisconsin presentations and 11 New York presentations (Henger 201

& Hauber, 2014). 202

203

Statistical analysis 204

We used JMP version 11.1.1 (SAS Institute, Inc., Cary, NC) to perform all statistical analyses 205

except Friedman's repeated measures 2-factor analysis (via an Excel spreadsheet). All inference 206

tests of single response variables used nonparametric methods because data were not normally 207

distributed. Tests of Principal Component scores used parametric methods because the 208

assumption of normality was met. Statistical significance was accepted at α = 0.05. 209

210

RESULTS 211

212

Comparison 1 213

We presented the three mounts at 25 nests defended by different males. Analysis of single 214

response variables showed that the female cowbird mount elicited the most aggressive responses 215

of redwings and the female cardinal mount the least aggressive responses, in our presentations. 216

Specifically, as shown in Figure 1, the number of times more than one male redwing 217

responded differed significantly among mounts (Log-likelihood G2 = 7.86, P = 0.020), but the 218

responses of female redwings were not significantly different between different stimuli (G2 = 219

0.60, P = 0.74). 220

221


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222

Figure 1 Presentations in which > 1 male and > 1 female red-winged blackbird responded to 223

three mounts Number of presentations with > 1 male redwing responding differed significantly 224

among mounts, but > 1 female redwing did not differ significantly (n = 25 nests for all 225

comparisons). 226

227

Figure 2 shows responses of male redwings to the three mounts. Male attacks differed 228

significantly among mounts (Friedman's repeated measures χr2 = 13.6, n = 25, P = 0.001) and all 229

pairwise comparisons were significant (Wilcoxon matched-pairs P < 0.01). The female cowbird 230

mount was most often attacked, whereas the female cardinal mount was attacked least often. 231

Male redwings perching within 3 m differed significantly among mounts (χr2 = 18.5, n = 25, P < 232

0.001) and male < 3 m for each of the two sexes of the cowbird mounts was significantly 233

different than for the cardinal mount (male cowbird Wilcoxon matched-pairs S = 57.5, n = 25, P 234

= 0.004; female cowbird S = 105.0, n = 25, P < 0.001). Male perching and looking at the mount 235

(PLM) differed significantly among mounts (χr2 = 6.00, n = 25, P = 0.049) and PLM for both 236

cowbird mounts was significantly different than for the cardinal mount (male cowbird Wilcoxon 237

02468

10

Female cardinal

Male cowbird

Female cowbird

# pr

esen

tatio

ns

Mount presented

Males Females


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matched-pairs S = 227.5, n = 25, P = 0.01; female cowbird S = 301.0, n = 25, P < 0.001). Female 238

redwing PLM and attacks did not differ among mounts (Friedman's repeated measures P > 0.05). 239

240

241

Figure 2 Mean (+ SE) male red-winged blackbird responses to three mounts Male redwing 242

attacks, < 3 m, and perching and looking at the mount differed significantly among mounts (* = 243

P < 0.05; ** = P < 0.01), but fly over, check, and whistle were not significantly different. 244

Pairwise comparisons showed that the female cowbird elicited the most aggressive, and the 245

female cardinal the least aggressive responses (n = 25 nests for all comparisons). 246

247

Figure 3 shows redwing responses using the Principal Component scores of Henger & 248

Hauber (2014). Scores differed significantly among mounts for Aggressive Response, Close 249

Male, Female Any Distance, and Intimidation (repeated measures ANOVA, P < 0.001) and for 250

all pairwise comparisons (Tukey HSD, P < 0.05). The female cowbird mount elicited the highest 251

Aggressive Response scores and Close Male, Female Any Distance scores, whereas the female 252

cardinal the lowest scores. Intimidation scores were lowest (more negative) in response to the 253

048

1216

Female cardinal Male cowbird Female cowbird

# of

per

iods

Mount presented

Fly over Attack ** < 3 m **PLM * Check Whistle


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female cowbird mount. The Intimidation score depends primarily on the behaviors hover, dive, 254

and no reaction so that more negative scores represent when redwings are more likely to attack 255

cowbirds than to dive or hover near them (Henger & Hauber, 2014). Aggressive Male 256

Vocalizations scores did not differ significantly among models (F2,48 = 2.13, P = 0.13). 257

258

259

Figure 3 Mean (± SE) Principal Component scores for red-winged blackbirds responding to 260

three mounts PC scores were calculated as in Henger & Hauber (2014). Scores differed 261

significantly among mounts for Aggressive Response, Close Male, Female Any Distance, and 262

Intimidation (* = P < 0.001) and for all pairwise comparisons. Scores for Aggressive Male 263

Vocalizations did not differ significantly among models (n = 25 nests for all comparisons). 264

265

Comparison 2 266

We examined the effect of direct experience with parasites by comparing attacks of the female 267

cowbird mount by males defending naturally parasitized and unparasitized nests. Parasitized 268

-0.40-0.200.000.200.400.600.801.00

Female cardinal

Male cowbird

Female cowbird

PC sc

ore

Mount presented

Aggressive response *

Aggressive male vocalizationsClose male, female any distance *Intimidation *


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males were significantly more likely to attack than unparasitized males (Log-likelihood G1 = 269

3.99, P = 0.046). 270

271

Figure 4 Likelihood of attacking a female cowbird mount and red-winged blackbird 272

parasitism status Males defending naturally parasitized nests (n = 4) were significantly more 273

likely to attack a female cowbird mount than males with unparasitized nests (n= 21). 274

275

Comparison 3 276

We used the Principal Component loading coefficients of Henger & Hauber (2014) to compare 277

responses of New York State and Wisconsin male redwings to the female cowbird mount. Figure 278

5 shows that males in Wisconsin responded significantly more aggressively, as measured by 279

Principal Components Aggressive Response and Intimidation, than males in New York State (t34 280

= 2.16, P = 0.038 and t34 = -2.12, P = 0.042, respectively). PC scores for Aggressive Male 281

Vocalizations and Close Male, Female Any Distance did not differ significantly between 282

locations, however (t34 = 1.29, P = 0.21 and t34 = -1.56, P = 0.13, respectively). 283

0

5

10

15

20

25

Parasitized Not parasitized

# pr

esen

tatio

ns

Parasitism status

Attack No Attack


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284

Figure 4 Mean (± SE) Principal Component scores of red-winged blackbirds in New York 285

State and Wisconsin responding to a female cowbird mount. Aggressive Response and 286

Intimidation PC scores were significantly different for the two locations (* = P < 0.05), but PC 287

scores for Aggressive Male Vocalizations and Close Male, Female Any Distance did not differ 288

significantly between New York (n = 11 nests) and Wisconsin (n = 25 nests). 289

290

DISCUSSION 291

292

Comparison 1 293

Redwings responded most aggressively to the female cowbird mount, were intermediate in 294

aggression toward the male cowbird mount, and were least aggressive toward the female cardinal 295

mount. These results are similar to those of Henger & Hauber (2014), who found that the female 296

cowbird mount consistently elicited the most aggressive response from redwings, and that 297

-0.50

0.00

0.50

1.00

Aggressive Response *

Aggressive Male

Vocalizations

Close Male, Female Any

Distance

Intimidation *

PC sc

ore

Principal component

New York Wisconsin


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responses to male and female cowbird mounts were different in some, but not all, Principal 298

Component scores. Both sets of results support the frontloaded parasite defense hypothesis 299

(FPDH). 300

Differences in response to model presentations of cowbirds versus nonparasites have 301

been found in many previous studies (e.g., Robertson & Norman, 1976; Ortega & Cruz, 1991; 302

Prather, Ortega & Cruz, 1999; Henger & Hauber, 2014), but differences in response to male 303

versus female cowbirds are often not apparent (e.g., Robertson & Norman, 1976; Strausberger & 304

Horning, 1998; Gill, Neudorf & Sealy, 2008). In some cases, however, hosts have been shown to 305

respond differently to male and female cowbirds (e.g., Folkers, 1982; Henger & Hauber, 2014). 306

As a commonly exploited cowbird host, redwings may have evolved the ability to discriminate 307

between and respond differently to male and female cowbirds because they represent different 308

levels to threat to redwing fitness. Unlike many other studies on redwings (reviewed by Henger 309

& Hauber, 2014), our study, identical in methods to Henger & Hauber (2014), used both visual 310

(model) and acoustic (playback) sensory modalities to simulate parasitic (or control) intruders 311

near the redwing nest, perhaps allowing for better discrimination between cowbird sexes and 312

leading to more accurate assessment of the relative threat of parasitism by this host species. 313

314

Comparison 2 315

We found that naturally parasitized male redwings were more aggressive toward the female 316

cowbird mount than unparasitized males. Our results are contrary to the predictions of the FPDH, 317

implying that aggressive nest defense is not an effective antiparasite strategy. In contrast to our 318

results, in his study at the same location in Wisconsin, Clotfelter (1998) found that parasitized 319

and unparasitized redwings did not differ in their aggressiveness toward a female cowbird mount 320


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and Strausberger (2001), working in Northern Illinois, found that more aggressive redwings 321

suffered lower rates of parasitism. The difference between our results and those of the prior study 322

at our Wisconsin site cannot be explained by a difference in parasitism rate; our rate of 18% is 323

very similar to the 20% parasitism during Clotfelter's study. When comparing these three sets of 324

results, it seems clear that the relationship between host antiparasite aggression and parasitism is 325

complex. Perhaps antiparasite aggression is disadvantageous in some circumstances, but 326

occasionally advantageous. Cowbirds were more likely to parasitize more vocally active 327

redwings (Clotfelter, 1998) and willow flycatchers (Empidonax traillii (Uyehara & Narins, 328

1995), as well as more aggressive older song sparrows (Melospiza melodia) (Smith & Arcese, 329

1994), but occasionally the parasites may still be successfully repelled by nest defense of the 330

aggressive hosts (Hauber, 2014) 331

Strausberger (2001) compared upland- and marsh-nesting redwings and found that 332

redwings nesting in dense aggregations in marshes were rarely parasitized and always detected 333

female cowbird mounts near their nests, whereas sparser upland redwing colonies were more 334

frequently parasitized and were less likely to detect the female cowbird mount. In contrast, 335

Freeman, Gori & Rohwer (1990) found no differences between parasitism rates of marsh and 336

upland redwing populations. Our studies all occurred in marsh and water-edge nesting 337

populations of redwings, thus it is unlikely that colony locality explains the intra- and inter-site 338

patterns in our comparisons. 339

Several authors have suggested that antiparasite aggression is only effective in dense host 340

populations (Robertson & Norman, 1977; Freeman, Gori & Rohwer, 1990; Strausberger, 2001) 341

where many pairs of eyes can watch for parasites and many hosts can be recruited to mob the 342

parasite. Model-presentation experiments showed that superb fairy-wrens (Malurus cyaneus) 343


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increase their antiparasite vigilance when the risk of parasitism is high (Feeney & Langmore, 344

2015). In low-density populations where vigilance and mobbing recruitment are limited, 345

however, antiparasite aggression may be a cue that parasites use to find nests (Robertson & 346

Norman, 1977; Smith, Arcese & McLean, 1984) or to assess the quality of potential hosts 347

(Smith, 1981). Further, Welbergen & Davies (2009) suggest that antipredator aggression may not 348

be adaptive in populations with a low risk of parasitism. Although antiparasite aggression thus 349

would be maladaptive in low-density or low-risk populations, the evolution of increased 350

aggressiveness is favored if host fitness is increased even slightly on average by antiparasite 351

defense (Sealy et al., 1998; see also Sih, Bell & Johnson, 2004). 352

Some studies have found that antiparasite defense was associated with nest success 353

(Clark & Robertson, 1979; Folkers & Lowther, 1985; Strausberger, 2001), but others have found 354

the opposite or no association (Seppä, 1969; Robertson & Norman, 1976, 1977; Smith, 1981; 355

Clotfelter, 1998; this study). Welbergen & Davies (2009) found that antiparasite aggression of 356

individual reed warblers (Acrocephalus scirpaceus) was highly repeatable and therefore unlikely 357

to be influenced by previous exposure to a real parasite at their nests, but these authors also 358

found that mobbing propensity was positively associated with parasitism risk. Given this result, 359

we examined the repeatability of redwing antiparasite aggression using 19 males each tested at 360

two different nests and found that male attack was significantly correlated for successive 361

presentations at different nests of the same male (Spearman's ρ = 0.461, n = 19, P = 0.047). This 362

result is consistent with a behavioral syndrome for antiparasite aggression (e.g., Sih, Bell & 363

Johnson, 2004; Avilés, Bootella, Molina-Morales & Martínez, 2014), and is not consistent with a 364

developmental hypothesis that male redwing antipredator aggression depends on direct, past 365

individual experience with cowbirds. Sealy et al. (1998) discussed the methods used in studies of 366


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host-parasite interactions, however, and suggested that the effectiveness of host defense can only 367

be determined when cowbirds come to lay their eggs. 368

369

Comparison 3 370

We found that Wisconsin redwings were more aggressive toward the female cowbird mount than 371

redwings in New York State (also see Armstrong 2002). Our Wisconsin study population (see 372

Schorger, 1937) falls within the traditional (long history) area of redwing-cowbird sympatry 373

(Freeman, Gori & Rohwer, 1990) and our 32-year parasitism rate of 15% is similar to the 374

approximately 22% parasitism for traditional upland habitats of Freeman, Gori & Rohwer 375

(1990). In contrast, parasitism is rare (in most years 0%) in the New York populations (Henger & 376

Hauber, 2014) into which cowbirds have only recently spread (Friedmann, 1929). Several studies 377

have found that hosts with a long history of sympatry with cowbirds are more aggressive toward 378

them (reviewed in Røskaft et al., 2002) and Briskie, Sealy & Hobson (1992) showed that hosts 379

attacked female cowbird mounts more aggressively in sympatric than allopatric populations. 380

Freeman, Gori & Rohwer (1990) also found that host populations only recently sympatric with 381

cowbirds have lower parasitism rates than host populations with a long history of sympatry, so 382

the mechanism that produces this geographic difference is unclear. At this point we suspect that 383

the expression of antiparasite aggression reflects evolutionary, ecological, and developmental 384

processes, rather than direct experience with parasites or parasitism per se during the breeding 385

history of individual hosts. 386

387

CONCLUSIONS 388

389


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Our results support some of the predictions of the hypothesis that redwings frontload their 390

defenses to prevent cowbirds from parasitizing their nests: redwings most aggressively attack 391

female cowbirds that represent the most immediate risk of parasitism. However, aggressive nest 392

defense does not directly translate into lower rates of parasitism at our Wisconsin study site, both 393

at micro- and the macro-scale comparisons. Combating parasitism in the first place may thus be 394

sufficient in redwings and other acceptor host species, making potential advantages of egg 395

ejection too small to favor its evolution. We also attempted to examine the relationship between 396

antiparasite aggression and natural parasitism, but given the high variance in results of multiple 397

studies, we cannot conclude with confidence that our results support the developmental 398

hypothesis that experience with natural parasitism enhances the antipredator aggressiveness of 399

host redwings. Finally, Wisconsin redwings were more aggressive toward the female cowbird 400

mount than New York redwings, but because the two locations differed in parasitism rate and 401

history of interaction (among other things), we cannot determine whether ecological or 402

evolutionary processes were the primary factors affecting the aggressiveness of host responses to 403

parasites. Given the variance in results among studies, a meta-analysis of redwings’ antiparasitic 404

strategies, now including our new data, might be a productive next step of research. 405

406

ACKNOWLEDGEMENTS 407

408

We thank Beloit College and the Department of Biology for allowing us to conduct our research 409

at Newark Road Prairie. We thank Bill Strausberger for kindly loaning to us his mounted 410

stimulus birds. 411

412


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