Demographic and Behavioral Responses of Breeding Birds to Variation in Food Nest Predation and Habitat Structure Across Multiple Spatial Scales

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Demographic and behavioral responses of breeding birds to variation in food nest predation and habitat structure across multiple spatial scales

Anna D. Chalfoun The University of Montana

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Recommended Citation Chalfoun, Anna D., "Demographic and behavioral responses of breeding birds to variation in food nest predation and habitat structure across multiple spatial scales" (2006). Graduate Student Theses, Dissertations, & Professional Papers. 9604. https://scholarworks.umt.edu/etd/9604

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8/98

. VARIATION IN FOOD, NEST PREDATION, AND HABITAT STRUCTURE

ACROSS MULTIPLE SPATIAL SCALES

Anna D. Chalfoun

B.A., Smith College, 1995

M.S., University of Missouri, 2000

Presented in partial fulfillment of the

requirements for the degree of

Doctor of Philosophy

The University of Montana

May, 2006

Approved by:

Dean, Graduate School

(o'l'O C a

Date

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Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Chalfoun, Anna D., Ph.D., May 2006 Fish and Wildlife Biology

Demographic and behavioral responses of breeding birds to variation in food, nest predation, and habitat structure across multiple spatial scales.

Chairperson: Thomas E. Martin

Birds show huge spatial variation in breeding behaviors and demography, from the global scale to the local. Yet the causes of this variation remain poorly understood. We reviewed the literature and document a worldwide pattern that southem-latitude passerine birds show consistently lower nest attentiveness during incubation than related northern species. We experimentally tested the hypothesis that greater food limitation may be responsible for low nest attentiveness in southern birds, by providing supplemental food during incubation to the karoo prinia (Prinia maculosa), a southem-hemisphere species with low attentiveness. Attentiveness was significantly higher in food-supplemented females than controls, but was still substantially below that of other related northern species. We therefore reject the hypothesis that food limitation is the main cause of latitudinal variation in incubation behavior. Habitat selection is another critical behavior with substantial fitness consequences. A main assumption of habitat selection theory has been that habitat preferences are adaptive. Yet, mismatches between habitat preferences and reproductive performance have been prevalent across a wide variety of taxa. We take an integrative and comprehensive approach to the evaluation of habitat selection in a breeding songbird, the Brewer’s sparrow (Spizella breweri), by examining habitat preferences and a suite of fitness components across multiple spatial scales. We show that habitat preferences and resulting fitness consequences vary across spatial scales, and different environmental factors (e.g., food versus nest predation) may be more important at different scales. At the largest scale, birds preferred landscapes with higher shrub cover, which was associated with greater offspring size and the ability of parents to attempt more nests within a season. At the smallest scale, parents chose nest patches containing higher densities of shrubs, which was associated with higher nest success. We experimentally tested two hypotheses (total-foliage and potential-prey-site) for why microhabitat structure influences nest predation rates, and found strong support for the potential-prey- site hypothesis that predators may abandon search efforts sooner in areas where more potential nest sites must be searched prior to finding actual sites. Together, our results demonstrate the utility of conceptually thorough approaches and experimental analyses towards a better understanding of habitat selection and other important behaviors.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Acknowledgements

I am struck with what a humbling and emotional experience it is to think back on

five intense and wonderful years as a Ph.D. student at the University of Montana, and all

the people to whom I am incredibly grateful. From the very beginning, I have been

thankful for the chance to be a part of the ever-talented and supportive group that is the

Martin lab. For this opportunity, and all of his efforts (despite my unintentional

stubbornness) to push me towards doing the best science possible, I will always be

grateful to my advisor, Tom Martin. I doubt that I would have achieved the same level of

intellectual and scientific growth in any other lab. I am also grateful to Tom for the

opportunity to travel to South Africa and conduct research at the international level.

South Africa was the most eye-opening and amazing experience I have ever had.

While Tom has served as my Ph.D. advisor, Vanetta Burton has been my advisor

in so many other ways. I have been so appreciative of Vanetta’s constant expertise and

good humor, and will miss her greatly. Jeanne Franz has also graciously and helpfully

addressed my pesky inquiries regarding bureaucratic procedures. I would also like to

thank Dan Pletscher for his all of his advice, encouragement, and support (including

facilitating additional project funding), and for offering me the unique opportunity to

teach a university course. Along those lines, I would like to express my gratitude to all of

the students I have had, for helping me to leam about the very rewarding process of

teaching and how I can continue to improve.

I am grateful to my committee members, Ray Callaway, Dick Hutto, Scott Mills,

and especially Doug Emlen. You have all impressed and inspired me in different ways,

and I have been truly lucky to have worked with you. Special thanks to the Emlen lab for

iii

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. their recent generosity in assisting with the honing of my defense talk. Also integral in

my development as a scientist have been all of the “Tea” participants, and all those

involved in our weekly evolution and ecology discussions. I will especially miss our

riveting conversations about science over bloody mary’s and kalamari.

My experience as a graduate student has been enhanced by the amazing cohort of

lab-mates and friends with whom I have had the pleasure to study and play. I have

especially enjoyed and benefited from my impromptu ecological discussions in the office

with Dan Barton. I cannot do justice with words for how grateful I have been for the

constant support and companionship of Christine Miller, Rob Fletcher, Karie Decker, T.J.

Fontaine, Bruce Robertson, Olga Helmy, Jedediah Brodie, Anna Noson, and Doug Milek.

Special thanks to T. J. (my partner in crime for five years) and Karie for being such

inspirational and helpful lab-mates and friends, and for facilitating my sanity at my

“home away from home” replete with hockey, wine, and puppies.

Funding for my dissertation work came from an NSF EPSCoR Fellowship, NSF

grants to Tom (South Africa work), the Montana Cooperative Wildlife Research Unit, a

SWG grant through Montana Fish, Wildlife & Parks, the Bureau of Land Management

(Billings Field Office), and the USDA Forest Service (Rocky Mountain Research Station,

Missoula). Many thanks to Jay Parks at the BLM for financial and logistical support, and

to Len Ruggiero, Dean Pearson, and Yvette Ortega of the Forest Service for generously

providing some last minute funding to get me through my final field season.

The vast amount of data collection needed for this project could not have been

achieved without the hard work of many field assistants. Special thanks to Jessica

Bolser, Brandon Breen, Kristen Ellis, Chris Forristal, Caitlin Hill, Kelly Jewell, Kate

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Nittinger, Andrea Saari, Dan Rauch, Darcie Westerman, and especially Cathy Ricketts

for many days traipsing around in 100-degree heat chasing cryptic sparrows and

measuring shrubs. I also had the pleasure of staying on the ranch of the Peterson family

for four summers, and am especially grateful for their kindness, accommodating nature,

and willingness to bail me out when Murphy’s law struck.

Finally, I would like to thank my family for all their support, advice, and love.

My mother, Eileen Chalfoun, has always emphasized the importance of higher education

and the fulfillment that can come from having the strength to take risks and challenge

oneself to the fullest. She has bolstered my confidence and encouraged me when I

needed it the most. I am grateful to Turtle, who has been my faithful companion through

it all. And last but most importantly, I am indebted to my husband, Scott Guenther, who

at various times has served as my field assistant and chief of logistical operations, and in

many ways deserves an honorary doctorate himself. Scott, for your unwavering support,

patience, and tolerance, I dedicate this dissertation to you.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Table of Contents

Abstract ...... ii

Acknowledgements ...... iii

Table of Contents...... vi

List of Tables...... ix

List of Figures...... x

Chapter 1...... 1

Abstract ...... 2

Introduction...... 3

Methods...... 5

Summary of Nest Attentiveness Across Latitudes ...... 5

Food Supplementation Experiment...... 6

Results ...... 9

Summary of Nest Attentiveness Across Latitudes ...... 9

Food Supplementation Experiment...... 9

Discussion...... 10

Acknowledgements ...... 13

Literature Cited ...... 14

Figure Legends ...... 20

Appendix A ...... 26

Chapter 2...... 32

Abstract ...... 33

Introduction...... 34

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Methods 36

Study System ...... 36

Habitat Preferences ...... 38

Fitness Consequences...... 38

Territory Density...... 39

Nest Searching and Monitoring...... 39

Focal-Pair Monitoring...... 40

Egg and Nestling Measurements ...... 40

Habitat Measurement ...... 41

Data Analysis...... 42

Results ...... 44

Discussion...... 46

Acknowledgements ...... 50

Literature Cited ...... 50

Figure Legends ...... 57

Chapter 3...... 64

Abstract ...... 65

Introduction...... 66

Methods...... 68

Observational Data ...... 69

Microhabitat Manipulation Experiment...... 71

Results ...... 72

Total-Foliage Hypothesis...... 72

vii

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Potential-Prey-Site Hypothesis...... 73

Discussion...... 74

Acknowledgements ...... 76

Literature Cited ...... 77

Figure Legends ...... 81

viii

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. List of Tables

Chapter 1

Table 1: Summary of results from studies examining the effect of supplemental

food on passerine nest attentiveness (%)...... 19

Chapter 2

Table 1: Indices used for quantification of habitat preferences and

fitness/demographic consequences of Brewer’s Sparrows at each spatial

scale...... 56

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. List of Figures

Chapter 1

Figure 1: Nest attentiveness (% time spent on the nest) for passerine species with

female-only incubation in north temperate versus tropical/south-

temperate latitudes ...... 21

Figure 2: Nest attentiveness of passerine families found primarily or exclusively

in either northern or southern

latitudes ...... 22

Figure 3: Mean nest attentiveness during early incubation for food-supplemented

versus control nests of the Karoo Prinia,Prinia maculosa...... 23

Figure 4: Mean on-bout and off-bout lengths during early incubation for food-

supplemented versus control nests of the Karoo Prinia...... 24

Figure 5: Hypothesized relationship of food availability and avian nest

attentiveness across species and latitudes ...... 25

Chapter 2

Figure 1: Chronology of Brewer’s sparrow first nest initiations in relation to

breeding densities...... 58

Figure 2: Brewer’s sparrow seasonal reproductive success in relation to breeding

densities...... 59

Figure 3: Landscape-scale daily nest survival probabilities in relation to seasonal

reproductive success estimates ...... 60

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Figure 4: Landscape-scale habitat preferences and associated fitness

consequences of the Brewer’s sparrow in relation to % shrub cover,

shrub density, and potential nest shrub density ...... 61

Figure 5: Territory-scale habitat preferences and seasonal reproductive success of

Brewer’s sparrows in relation to % shrub cover, shrub density, and

potential nest shrub density ...... 62

Figure 6: Brewer’s sparrow patch-scale habitat preferences and nest success in

relation to% shrub cover, shrub density, and potential nest shrub

density ...... 63

Chapter 3

Figure 1: Brewer’s sparrow nest patch choice in relation to the total amount of

foliage and potential nest shrub density within patches ...... 82

Figure 2: Fitness surfaces (probability of nest survival) of Brewer’s sparrows as a

function of the density of total foliage and potential nest shrubs in nest

patches...... 83

Figure 3: Results of a microhabitat manipulation experiment in which the amount

of total foliage and density of potential nest shrubs within Brewer’s

sparrow nest patches were reduced relative to controls...... 84

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. CHAPTER 1

LATITUDINAL VARIATION IN AVIAN INCUBATION ATTENTIVENESS AND A

TEST OF THE FOOD LIMITATION HYPOTHESIS

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. ABSTRACT

Avian incubation attentiveness has important fitness consequences through its

influence on the number and quality of hatched young and energetic costs imposed on

parents. Nest attentiveness is highly variable across species and geographic regions. We

reviewed the literature and show a worldwide pattern that nest attentiveness is generally

lower in southern compared with northem-latitude passerine species. We then

experimentally tested the hypothesis that greater food limitation may be responsible for

low nest attentiveness in southern birds. We used the karoo prinia {Prinia maculosa) in

South Africa, which has very low nest attentiveness (~ 50%) compared with average (~

73%) north-temperate species. We provided supplemental food during early incubation to

experimental females and measured nest attentiveness and on-and off-bout lengths

compared to paired control females. Nest attentiveness was significantly increased at

food-provisioned nests (57% versus 49%). Food-supplemented females spent

significantly less time off the nest than control females, whereas mean on-bout lengths

did not differ. However, mean nest attentiveness of food-provisioned females was still

substantially below attentiveness of other similar bird species worldwide. We suggest that

food can be an important proximate influence on parental care behavior within species,

but the low attentiveness of many southern bird species appears to represent an evolved

trait that is not simply constrained by food.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. INTRODUCTION

The extent of parental care can greatly influence reproductive success and the

quantity and quality of reared young (Clutton-Brock 1991). Yet, parents inevitably face

tradeoffs in terms of how much energy to allocate to their developing young versus their

own condition and longevity (Martin 1987, Clutton-Brock 1991, Martin 2002, Royle et

al. 2004). Species differ in their parental care strategies for resolving these trade-offs

(Clutton-Brock 1991, Martin et al. 2000), but the causes underlying this variation remain

poorly understood.

Parental care strategies include a number of behavioral components, and one that

has important fitness consequences for birds is nest attentiveness (the percentage of time

parents spend on the nest during incubation). Nest attentiveness affects egg temperatures

(White and Kinney 1974, Haftom 1988), which influence the length of the incubation

period (Pricel998, Martin 2002, Martin et al. in review), and thereby the extent to which

young and attending parents are exposed to time-dependent mortality from nest predators

(Magrath 1988, Martin 2002). Such risks suggest that individuals should be under

selection to increase attentiveness in order to minimize the incubation period (Bosque and

Bosque 1995). Yet, even within environments with high nest predation risk, birds display

extensive interspecific variation in nest attentiveness (Martin 2002, Martin et al. in

review). Potential causes underlying variation in nest attentiveness, therefore, remain a

critical question in need of study.

Avian nest attentiveness appears to vary geographically even within a single order

such as Passeriformes (Martin 2002). Phylogenetically matched pairs of species in

several passerine families show lower nest attentiveness at a southem-hemisphere

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. (Argentina) study site compared to a north-temperate (Arizona) site (Martin 2002). Here,

we review existing literature to assess the ubiquity of this pattern and find worldwide

evidence for geographic variation in nest attentiveness (Figure 1). Southern latitude

species consistently show lower attentiveness even when controlling for phylogeny. The

factors responsible for this pattern, however, remain unclear.

One potential cause of this latitudinal pattern might be food limitation. Nest

attentiveness reflects on-bouts to keep eggs warm and temporary off-bouts to forage

because parents must balance their own energetic requirements with the needs of their

developing embryos (reviewed in Deeming 2002; Martin 2002). Energetic expenditures

during incubation are considerable, and can influence future prospects of parents

(Thomson et al. 1998, Visser and Lessells 2001, Tinbergen and Williams 2002). If food

availability is more limited in southern areas, then energetic constraints from greater food

limitation may require more and/or longer off-bouts, potentially explaining lower nest

attentiveness of southern birds.

Some evidence suggests that food may be an important proximate influence on

nest attentiveness (Nilsson and Smith 1988, Smith et al. 1989, Sanz 1996, Eikenaar et al.

2003, Pearse et al. 2004), but the ability of food to explain latitudinal patterns in

attentiveness is unstudied. First, experimental tests of food limits on attentiveness have

not considered latitudinal differences. Indeed, four of six species tested in previous

studies were from north-temperate regions (Table 1). Second, four of six species were

cavity nesters. Cavity nesting species engage in nest guarding in order to protect the

cavity from usurpers, so presence in the nest in response to food does not separate

attentiveness from guarding components. Finally, all but one of the studies were on

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. species with relatively high nest attentiveness (Table 1), which does not address the

question of why southern species have low attentiveness. Thus, experimental studies are

needed on non-cavity-nesting, southern species with low nest attentiveness.

The karoo prinia(Prinia maculosa; Cisticolidae) is a southern species that

provides a good example for experimentally testing the relationship between food

availability and incubation behavior. The karoo prinia is a southern hemisphere warbler

that builds its own nest and has low mean incubation attentiveness (52%, Martin et al. in

review) compared to other passerine species worldwide (Deeming 2002, Martin 2002).

Karoo prinias experience high rates of nest predation (daily nest mortality of 9.3%,

Martin et al. in review) and should be under selection to reduce the length of the

incubation period. We therefore explored the hypothesis that the low attentiveness of

prinias reflected greater food limitation compared with similar northern species.

Specifically, we tested the prediction that if food limitation is responsible for variation in

attentiveness across latitudes, then increasing food availability to this southern species

should increase attentiveness levels to at least the lower limits of related northern species.

METHODS

Summary of Nest Attentiveness Across Latitudes

To assess the generality of latitudinal variation in nest attentiveness, we reviewed

the literature for published estimates of nest attentiveness of passerine birds around the

world. We limited our review to species with female-only incubation so as not to

confound the issue with number of incubating parents. We categorized species as

northern if they breed within north-temperate latitudes, and southern if they breed < 23.5°

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. N latitude, which is the northern demarcation point for the tropics (Tropic of Cancer). We

grouped south-temperate and tropical species together based on evidence that they share

more similar life histories with each other than either do with north-temperate species

(Martin 1996 and references therein). All attentiveness estimates were obtained from

visual observations (either direct or by video recordings). If more than one source

provided an estimate of nest attentiveness for the same species, we averaged estimates.

Species means were averaged within each family for northern versus southern locations

and compared as pairs within families to control for potential phylogenetic effects

(Mpller and Birkhead 1992). For families endemic to either northern or southern

latitudes, and those for which we only had estimates from one latitude class, we

conducted a phylogenetic analysis using independent contrasts (Felsenstein 1985)

through the BRUNCH option of program CAIC (Purvis and Rambaut 1995) for

dichotomous contrasts. The phylogeny for these contrasts was taken from Sibley and

Ahlquist (1990) and is illustrated in Fig. 2. The resulting contrasts were then compared to

0 in a one-sample, one-tailed t-test to determine whether attentiveness was significantly

higher in northern compared with southern families.

Food Supplementation Experiment

We conducted our food manipulation experiment during September to early

November, 2004 at the Koeberg Nature Reserve (33°41’S, 18°27’E) in the Western Cape

Province of South Africa. The region has a Mediterranean climate, consisting of warm,

dry summers (10 - 38 0 C) and cool, wet winters (2 - 25 0 C). The reserve consists of a

mosaic of strandveld succulent karoo, dune thicket and sand plain fynbos vegetation

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. types (Nalwanga et al. 2004a). The karoo prinia is a small (9 g), territorial warbler and a

common resident at this site. Nests are enclosed and dome-shaped, built off the ground in

restio plants (Restionaceae) and various shrub species (Nalwanga et al. 2004b). Only

females incubate the eggs, and mate feeding in this species is minimal. Females must

leave the nest intermittently to forage and meet nutritional requirements.

Prinia nests were located by observing parental behavior during the nest-building

stage (e.g., the male or female carrying nest material). We controlled for any potential

confounding effects of clutch size (Thomson et al.1998, Reid et al. 2002, Tinbergen and

Williams 2002) by pairing nests of the same clutch size when possible and only using

nests containing the modal number of eggs (3 or 4). Moreover, because ambient

temperature may influence incubation rhythms (White and Kinney 1974, Conway and

Martin 2000a, Deeming 2002), we paired nests by initiation date and collected data on

experimental and control nests simultaneously on the same days. For each pair of nests,

we randomly assigned one to the experimental treatment and one as the control. We

performed the experiment during early incubation (2 or 3 days after clutch completion)

for all birds to control for possible stage effects (e.g. Deeming 2002).

Experimental nests received a small, clear plastic cup with mealworms (larvae of

Tenebrio molitor) just below the nest entrance and within 10 cm of the nest. Initial

feeding trials were conducted to determine how many mealworms birds were willing to

consume during the experimental observational period. As a result, approximately 60

mealworms (5-6 g) were placed in each cup. The average daily energy requirement for

birds of similar body size to the karoo prinia is 45 kJ/day (Williams 1993). Mealworms

have an energy content of 11.6 kJ/g and a minimum assimilation efficiency of 0.71 in

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. birds (Bell 1990), so we provided females with 92-110% of their daily energetic

requirements- a major energetic augmentation. Control nests received an empty cup in

the same location. We placed the plastic cup with an equal number of mealworms near

the nest for 6 to 8 hours on the day prior to the actual experimental trial to ensure that

experimental females: (1) were accustomed to the presence of the cup, (2) learned to take

the novel food, and (3) had augmented energy intake prior to measuring incubation

responses. In most cases, females rapidly learned to utilize the additional food. Control

nests were similarly primed, but with an empty cup.

On the day we measured responses, food containers were placed at nests within

one-half hour of sunrise. Data on nest attentiveness for experimental and control nests

were collected by videotaping nests for 6-8 hours beginning when the cups were placed.

We calculated three parameters from the videos: mean incubation on-bout length, mean

off-bout length, and overall percent attentiveness. Mean bout lengths were calculated by

averaging all of the complete on-bouts and off-bouts observed during an entire filming.

Attentiveness was calculated as the total percentage of time the female spent on the nest

incubating during the 6-8 hours, following Martin (2002). Mean bout lengths and percent

attentiveness for experimental versus control nests were compared using paired T-tests.

We arcsine transformed attentiveness data for statistical analysis, but present raw data in

figures for ease of interpretation. Bout length data were not transformed prior to analyses

as they were approximately normally distributed, and Levene tests (Dytham 2003) were

insignificant indicating homogeneity of variances.

In order to examine whether food availability could be responsible for latitudinal

differences in attentiveness, we tested two predictions. First, we examined whether nest

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. attentiveness of food-supplemented karoo prinias increased to at least the lower limits of

attentiveness reported for related species at northern latitudes. Second, we predicted that

southern birds should show a larger increase in nest attentiveness with supplemental food

than similar northern species if food is more limiting in southern latitudes. In order to test

this prediction, we compared the increase in attentiveness obtained in passerine food-

supplementation experiments (Table 1) for northern versus southern locations.

RESULTS

Summary of Nest Attentiveness Across Latitudes

We found a consistent and statistically significant difference (Paired t test: tn =

5.27, P < 0.001) in nest attentiveness across families of passerine birds represented in

both northern and southern latitudes (Figure 1). Almost all families for which we found

nest attentiveness estimates for both northern and southern species showed lower

attentiveness in the south (Figure 1). This pattern was further reflected in families found

primarily or exclusively in either the north or the south (Figure 2). Three contrasts were

obtained between families with purely north or south data (see Figure 2) and these

contrasts also demonstrated that southern families had lower overall attentiveness than

northern (t2 — 6.21, P = 0.01).

Food Supplementation Experiment

We observed a total of 20 karoo prinia nests (10 food-supplemented and 10

control). Incubation attentiveness was significantly higher in experimental than control

nests (tg = 2.31, P < 0.05; Figure 3). The difference in nest attentiveness between

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. treatments was caused by a disparity in the amount of time females spent off the nest.

Mean off-bout length was significantly shorter at experimental nests(tg = -3.34, P <

0.01), whereas mean on-bout length was virtually identical between treatments (tg = 0.18,

P = 0.86) (Figure 4).

Mean attentiveness even for experimental females fed ad libitum (57 % ± 3.5),

however, remained far below unmanipulated estimates of incubation attentiveness for

most other songbird species with female-only incubation (e.g., 73 %, n = 231 species;

Deeming 2002), especially those in the north (Figures 1 and 2). We were unable to locate

published estimates of nest attentiveness for other northern members of the family

Cisticolidae for direct comparison. However, estimates were available for many northern

species of the superfamily Sylvioidea, to which karoo prinias belong (Sibley & Alquist

1990). Mean nest attentiveness for 22 species of northern members of Sylvioidea

averaged 74.8% ± 9.1, well out of the range of attentiveness for food-supplemented

prinias in this study (One-Sample t test: t\ = 7.40, P = 0.04). Moreover, contrary to the

prediction that southern species should respond more strongly to increased food, northern

species actually showed a greater increase in attentiveness with supplemental food than

southern species (One-way ANOVA: Fi = 7.01, P < 0.05; Table 1).

DISCUSSION

Our review demonstrated a worldwide, latitudinal pattern in an important avian

breeding behavior. Passerine incubation attentiveness was consistently lower in southern

latitude species than for their northern counterparts (Figures 1 and 2). Our experimental

test of the hypothesis that food limitation was the basis of this latitudinal pattern yielded

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. an increase in nest attentiveness in a southern species with low attentiveness. This result

corroborates the long-standing view that food can have important proximate effects on

parental behaviors (Lack 1954, Lack 1968, Martin 1987).

Previous food supplementation experiments for incubation behavior in other

species have yielded mixed results. Two studies (Nilsson and Smith 1988, Sanz 1996)

documented a decrease in the incubation period length of blue tits and pied flycatchers,

respectively, suggesting that nest attentiveness was increased, but actual nest

attentiveness was not measured. In studies directly measuring attentiveness, supplemental

food increased attentiveness in five species, and had no effect in two (Table 1). Few

studies had a large increase in attentiveness (Table 1) compared with the variation among

species (Figures 1 and 2).

Although prinias in our study altered their incubation behaviors in response to

supplemental food, incubation attentiveness even for females given access to unlimited

food remained very low relative to attentiveness of other female-only incubators,

especially in the north (Deeming 2002, Martin 2002, Martin et al. in review). The lack of

a larger response is unlikely to be due to a lack of behavioral flexibility of attentiveness

in prinias, as attentiveness was variable among individuals and as high as 74% in one

experimental female. We also observed females loafing and preening at the food cup,

indicating they had free time that could have been allocated to nest attentiveness but was

not. The Australian reed warbler, another southem-hemisphere songbird with similarly

low nest attentiveness (51%, Eikenaar et al. 2003) showed the identical pattern;

attentiveness was significantly increased with supplemental food, but still remained low

(57%). Interestingly, Eikenaar et al. (2003) focused on the significant increase and argued

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. food was an important limit on attentiveness, while overlooking the fact that attentiveness

was extremely low in the broader geographic context that we document.

Several other lines of evidence also suggest that food is not the cause of broad

species differences in attentiveness. First, our comparison of attentiveness responses to

supplemental food in the north versus the south yielded a result opposite to that predicted;

northern species actually showed a greater increase in attentiveness with increased food

than southern species. Food availability is therefore unlikely to be more limited in the

south. Similarly, in a comparative analysis across passerine species, Conway and Martin

(2000b) found no effect of two potential correlates of food limitation (diet and foraging

strategy) on nest attentiveness. Finally, after nearly a century of being introduced to a

novel, food-rich environment (Vancouver, British Columbia) the subtropical crested

mynah (Stumus cristatellus) still exhibits very low (47%) nest attentiveness, typical of

southern species (Johnson and Cowan 1974). The results of our study and others,

therefore, do not support the hypothesis that food limitation is the sole cause of evolved

differences in nest attentiveness between latitudes (Figure 5). Low attentiveness in the

karoo prinia and other species instead appears to be an evolved parental strategy,

independent of food effects.

In conclusion, food may be an important proximate factor affecting the extent of

parental care in birds but only within limits. Food limitation alone cannot explain large-

scale, across-species geographic variation in parental care strategies, and alternative

explanations for this pattern require further examination. Latitudinal variation in

attentiveness is unlikely to be driven by variation in nest predation risk selecting for

shorter developmental periods, as nest predation is variable both within and across

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. latitudes and with no clear north-south gradient (Martin 1996, Martin et al. 2000).

Moreover, many southern species experience very high rates of nest predation, yet

maintain relatively low nest attentiveness. Climatic variation across latitudes may play a

role in the amount of time parents spend on the nest, although temperatures at many

south-temperate sites often approximate those at north-temperate sites during the

breeding season (Martin 2002). One promising alternative explanation for geographic

patterns in nest attentiveness is variation in adult mortality across latitudes (Martin 2002).

According to classic life history theory (e.g. Roff 1992), if southern birds experience

lower adult mortality, they should be less willing to invest as much in nest attentiveness

and other components of current reproduction. Testing for the existence of a trade-off

between adult mortality and nest attentiveness across latitudes is therefore a critical next

step in addressing geographic variation in parental care strategies.

ACKNOWLEDGEMENTS

We are grateful to P. Lloyd, E. Kofoed, and S. Auer for assistance in the field, and

C. M. Lessells and two anonymous reviewers for helpful comments on a previous draft of

this manuscript. This work was supported by U. S. National Science Foundation grants to

T.E.M. (INT-9906030, DEB-9981527).

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. LITERATURE CITED

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Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. White, F. N., and J. L. Kinney. 1974. Avian incubation: interactions among behavior,

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South Africa. Condor 95:115-126.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. This study Eikenaar et al. (2003) Open Cup Mackintosh & Briskie (2004) Cavity Pearse et al. (2004) CavityCavity Smith et al. (1989) Pearse et al. (2004) Nest Type Source Y Enclosed Signif. (%) 19 1 N 8 12 Y 12 Y 8 N Cavity Moreno (1989) 6 Y Enclosed Change (%) 80 86 57 81 10 Y 82 82 49 57 Control (%) Food N 78 N 70 * Latitude: * N = North temperate; S = Tropics or south temperate South IslandRobin S 79 Karoo Prinia S Australian Reed Warbler S 51 Wheatear House Wren N 71 Species Lat.‘ Bewick’s Wren PiedFlycatcher N 70 Table 1. Summaryresults of from studies examining the effect ofsupplemental food on passerinenest attentiveness (%)

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. FIGURE LEGENDS

Figure 1. Paired family means (± SE) of nest attentiveness (% time spent on the nest) for

passerine species with female-only incubation in north temperate (black bars) versus

tropical/south temperate (< 23.5° N; gray bars) latitudes. Species sample sizes are

indicated after the family names. Data were obtained from the literature (Appendix A).

Figure 2. Nest attentiveness of passerine families (± SE) found primarily or exclusively

in either northern (black bars) or southern (< 23.5° N; gray bars) latitudes. Species sample

sizes are indicated after the family names. Data were obtained from the literature

(Appendix A), and phylogenetic relationships from Sibley and Ahlquist (1990).

Figure 3. Mean nest attentiveness (± SE) during early incubation for food-supplemented

versus control nests of the Karoo Prinia,Prinia maculosa, (n = 10 matched pairs) in

South Africa during September - November 2004.

Figure 4. Mean on-bout and off-bout lengths (± SE) during early incubation for food-

supplemented versus control nests of the Karoo Prinia,Prinia maculosa, (n = 10 matched

pairs) in South Africa during September - November 2004.

Figure 5. Hypothesized relationship of food availability and avian nest attentiveness

across species and latitudes. Both northern (black line) and southern (dashed line) species

are expected to show proximate increases in attentiveness in response to increased food

availability, and preliminary data (Table 1) further suggest that northern species show

slightly stronger responses. Food availability alone, however, cannot ultimately explain

why southern species generally show lower nest attentiveness than similar northern

species (gray arrows).

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. without prohibited reproduction Further owner. copyright the of permission with Reproduced Figure 1. Figure Nest Attentiveness (%) South 1 North I 21 Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. without prohibited reproduction Further owner. copyright the of permission with Reproduced

Nest Attentiveness (%) i South i i North 0.65 -i Matiii Control 0.60 -

5? 0.55 OT C/3 c 0.50 CD >

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CO 03 0.40 -

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Figure 3.

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■'tiV.Ui

Off On

Figure 4.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. c 0) > ■+■* M l c 0) 0 Z

Food Availability

Figure 5.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Appendix A. References for summary (shown in Figures 1 and 2) of passerine nest

attentiveness by family in northern versus southern latitudes. Avian families are listed

taxonomic order; references alphabetically.

Family References Tyrannidae 4, 8, 21, 23, 34, 35, 37, 38,40 Pipridae 23,40 Menuridae 20 Ptilonorhynchidae 12, 13 Orthonychidae 14 Paradisaeidae 10, 11 Bombycillidae 18 Nectariniidae 23,44 Sittidae 4, 23, 27 Paridae 4, 17, 23, 24 Hirundinidae 4, 7, 34 Pycnonotidae 23 Troglodytidae 4,21,23,28,34, 35,38,40,41 Cisticolidae 23 Sylviidae 6, 16, 22, 23 Turdidae 4,21,23,25, 33,35,38,40 Mimidae 18, 35 Parulidae 4, 15, 19,21,23,35,36 Thraupidae 23,29,31,32,35,36,37,40,45 Cardinalidae 4,35 Emberizidae 1,3,4,9,21,23,26,35,42,43 Icteridae 4,39 Fringillidae 2,4,23,30,35,37,40

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Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. CHAPTER II

MISMATCHES BETWEEN HABITAT PREFERENCES AND REPRODUCTIVE

PERFORMANCE: TRADE-OFFS AMONG FITNESS COMPONENTS AND

SPATIAL SCALES

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. ABSTRACT

Ecological theory predicts that habitat choices should be adaptive, such that

fitness is higher in preferred habitats. However, studies often report mismatches between

habitat preferences and reproductive outcomes across a wide variety of taxa. We

examined whether the matching of habitat preferences with multiple fitness components

changed with spatial scale (landscape, territory, nest patch) in a breeding songbird, the

Brewer’s sparrow (Spizella breweri). Birds settled earlier and in higher densities in

landscapes with greater shrub cover and height. Yet, nesting success was similar across

landscapes. However, nestling mass and the number of nesting attempts per pair

increased with shrub cover and height, raising the possibility that landscapes were chosen

on the basis of food availability rather than safe nest sites. At the opposite spatial

extreme, nest patches contained greater densities of shrubs and potential nest shrubs than

random patches, and nest success was higher in patches with higher potential nest shrub

densities. Pairs that established territories with higher potential nest shrub densities also

showed greater seasonal reproductive success. Territories were placed in areas with

greater shrub cover, height, density, and density of potential nest shrubs, indicating a

potential strategy to maximize the inclusion of all attributes with potential fitness

consequences at larger and smaller scales. Habitat preferences may therefore reflect the

integration of multiple environmental factors across multiple spatial scales, and

individuals may have more than one option in terms of optimizing fitness via habitat

selection strategies.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. INTRODUCTION

Under natural conditions, habitat preferences are assumed to be shaped by the

fitness outcomes of using particular habitats (Hilden 1965, Orians and Wittenberger

1991, Jaenike and Holt 1991, Martin 1998). However, unambiguous examples of

adaptive habitat preferences are uncommon (Martin 1998, Clark and Shutler 1999,

Misenhelter and Rotenberry 2000, Robertson and Hutto 2006). Actual habitat

preferences and the resulting fitness consequences are often not quantified (Martin 1998,

Clark and Shutler 1999, Garshelis 2000, Jones 2001), and when they are, many results

suggest neutral or even inverse relationships between preferred habitats and indices of

fitness across a wide variety of taxa (e.g., Thompson 1988, Valladares and Lawton 1991,

Misenhelter and Rotenberry 2000, Kolbe and Janzen 2002, but see Martin 1998). Such

results pose a potential paradox: why should animals ever choose habitats that yield

lower fitness?

Habitat choices determine the acquisition of critical resources such as food

(MacArthur et al. 1966, Cody 1974, Willson 1974, Rotenberry and Wiens 1998) and

refugia from predators (Leber 1985, Martin 1988, Soderstrbm 2001, Heithaus and Dill

2002, Eggers et al. 2006), which in turn influence fitness consequences. Different

resource types, however, may influence different fitness components to varying degrees.

In breeding birds, for example, food availability often manifests in terms of the ability of

parents to invest in offspring (e.g., clutch size, clutch mass, offspring size, numbers of

nesting attempts (Martin 1987, Arcese and Smith 1988, Holmes et al. 1992, Bolton et al.

1993, Martin 1995, Nagy and Holmes 2004) whereas nest predation risk influences the

probability of nesting success for each attempt. Because food and nest predation can

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. both affect the overall reproductive output within a season, individuals may adopt

alternative habitat selection strategies to achieve the same net fitness. For example,

individuals that select food-rich habitats may be able to compensate for higher predation

risk via the ability to renest more quickly and more often, and/or by rearing higher quality

young that are more likely to survive to breeding age. Identifying such tradeoffs among

fitness components, however, necessitates the simultaneous examination of multiple

fitness components; an approach that has been extremely rare in studies of habitat

selection.

Selection pressures imposed by food versus predation may also act more strongly

at particular spatial scales (Pribil and Pieman 1997). Food availability often varies across

fairly large spatial scales coincident with climatic and edaphic variation (Orians and

Wittenberger 1991, Rotenberry and Wiens 1991), though food may also vary on finer

scales. Predation risk is often the result of complex interactions between predator

abundance and behavior, availability of alternative prey, and habitat structure, and can

therefore vary significantly both temporally and spatially (Crowder and Cooper 1982,

Salamolard et al. 2000, Weatherhead and Blouin-Demers 2004). Yet, predicting

predator-prey encounter rates may be more feasible at smaller spatial scales where habitat

attributes often proximately influence predator success rates. Accordingly, multiple

spatial scales need to be incorporated into studies of habitat selection (Allan and Starr

1982, Hutto 1985, Wiens 1989, Menge and Olson 1990, Orians and Wittenberger 1991,

Levin 1992, Saab 1999, Clark et al. 1999). Spatial scales should be chosen based on the

biology of focal species, and indices of habitat preference and subsequent fitness

outcomes should be specifically tailored to each spatial scale.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Detailed empirical studies that measure habitat preferences and a suite of fitness

components across multiple spatial scales are therefore needed to more effectively

delineate the potential evolutionary bases of habitat preferences. Such an approach may

also help resolve the apparent paradox between habitat preferences and reproductive

performance. Here, we examine breeding habitat preferences and several demographic

components (fledging success, seasonal reproductive success, clutch size, clutch mass,

nestling mass, and numbers of nesting attempts) of a passerine bird across multiple,

ecologically-relevant spatial scales: the landscape, territory, and nest patch. Specifically,

we test whether tradeoffs among multiple fitness components across spatial scales can

help explain habitat preference-performance mismatches that are often observed when

fitness components and spatial scales are examined in isolation.

METHODS

Study System

Our focal species was the Brewer’s Sparrow(Spizella breweri), a common

inhabitant of North American sagebrush steppe. Brewer’s sparrows are locally abundant

during the breeding season, thereby permitting intensive and replicated data collection.

Shrubsteppe consists of both local and landscape-scale gradients in habitat structure, thus

permitting habitat selection comparisons across spatial scales. Nest predation is the main

cause of reproductive failure in the Brewer’s sparrow, and varies with variation in habitat

structure (Chapter 3). Nest predation therefore imposes strong fitness consequences in

this system, and likely influences habitat choice. Food resources are also known to vary

spatially and temporally in shrubsteppe (Rotenberry and Wiens 1998). Therefore, our

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. study system permitted simultaneous evaluation of multiple fitness components likely to

be influenced by variation in habitat structure.

Data collection took place during May to August of 2003-2005 within public and

private lands in Carbon County, Montana. The predominant overstory plant species in

the study area was big sagebrush {Artemisia tridentata), mixed with greasewood

(Sarcobates vermiculatum) and rabbitbrush {Chrysothamnus spp.). The understory was

sparse due to the dry climate (approximately 20 cm of annual precipitation) and consisted

of various small forbs, native grasses, and cactus. We established eight 25- to 30-ha

study sites separated by at least 1 km within which to conduct analyses. Sites represented

the landscape scale for the purposes of our study, as each encompassed multiple

individual Brewer’s sparrow territories/home ranges. Sites were selected so as to capture

the full range of regional structural variation in sagebrush steppe, and differed in terms of

their overall shrub cover, height and density. Each plot also contained microhabitat

gradients according to localized variation in soil moisture content.

Confirmed nest predators in the study area were the bullsnake {Pituophis

melanoleucus), prairie rattlesnake ( Crotalis viridis), various rodent species, and

loggerhead shrike {Lanius ludovicianus). Other potential nest predators observed

included the black-billed Magpie {Pica hudsonia), pinyon jay {Gymnorhinus

cyanocephalus), common grackle{Quiscalus quiscula), brown-headed cowbird

{Molothrus ater), coyote{Canis latrans) and raccoon {Procyon lotor).

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Habitat Preferences

We used Brewer’s sparrow density as an indicator of habitat preference at the

landscape scale. Density may sometimes be a misleading indicator of actual habitat

preference and/or quality (Van Home 1983), so we also examined densities with respect

to initiation dates (day the first egg was laid) of first nests within each breeding season.

First nest initiation dates should reflect the chronology of settlement and/or the quality of

settling individuals, and therefore provide an additional metric of habitat preference

(Robertson and Hutto 2006). At the territory scale, within each study site we compared

the habitat structure within Brewer’s sparrow territories to that in surrounding unused but

available habitat. Nest patch preferences were similarly measured by comparing

attributes of 5-m nest patches to unused but available patches.

Fitness Consequences

Nesting success was used as a fitness proxy at all spatial scales. We estimated

nest survival at the landscape scale by pooling all nests within each landscape (study site)

during each year and calculating daily nest survival probabilities (Mayfield 1975). We

calculated the seasonal reproductive success (total offspring fledged per year) of pairs of

birds within a subset of territories within each landscape to estimate the relative success

of different territories and landscapes. Finally, we compared the habitat structure of

successful versus depredated nest patches within each landscape.

Within each study site we also collected information on demographic parameters

indicative of parental investment and/or offspring quality including clutch size, clutch

mass, nestling mass, and numbers of nesting attempts.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Territory Density

We mapped male territories during each breeding season in order to compare

Brewer’s Sparrow densities across landscapes. Plots were flagged into 50 x 50 m grids,

and each received 8-10 survey visits every 2 to 5 days from early May to mid-June.

During survey visits, a surveyor slowly walked and mapped observations of male singing

locations, as well as visual observations of birds. Individual survey data from each study

site within each year were transposed onto a single composite map showing the location

and number of individual territories. The total number of territories was divided by the

total study site area to calculate territory density/ha. Territories whose locations were

only partially covered by the study site were counted as one-half of a territory.

Nest Searching and Monitoring

Nests were located within each study site using behavioral observations and

systematic searches. Nests were monitored every other day until completion following

protocols outlined in Martin and Geupel (1993). For each nest, we calculated nest

initiation date, and fate (successful, depredated or mortality due to other causes). Nests

that fledged at least one young were considered successful. Observations of nestlings

within 1-2 days of fledging age, fledglings near the nest or parents with food in the

vicinity of the nest were taken as evidence of a successful nest (Martin 1998). Nests

were considered to have been depredated when nest contents (eggs or nestlings too young

to have fledged) disappeared.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Focal-Pair Monitoring

Each year we randomly selected 5-10 Brewer’s sparrow pairs within each study

site to monitor intensively throughout the entire breeding period. Brewer’s sparrows are

socially monogamous, multi-brooded, and will renest following nest failure. We

therefore attempted to document the fates of every nesting attempt of focal pairs in order

to calculate season-long reproductive success. Focal pairs were dispersed throughout

study plots to obtain variation in territory habitat structure. The male and female of each

focal pair were captured via target-netting at their first nest of the season and given a

unique combination of color bands with which to identify and subsequently monitor

individual birds. We calculated seasonal reproductive success for each pair by tallying

the total number of young successfully fledged from all nesting attempts within a season.

Egg and Nestling Measurements

Clutch size, clutch mass, and nestling size were recorded at all sites. Clutch size

was recorded for nests that we were able to observe at least twice following the laying of

the last egg. Sufficient sample sizes of clutch and nestling mass across all 8 sites were

obtained during 2005 only. Mass measurements were recorded using a portable 0.001-g

sensitivity balance. Egg mass was only recorded for nests with known nest initiation

dates and within 3 days of clutch completion, to limit variation due to egg water loss later

in the incubation period (Martin et al. 2006). Values for all eggs within a clutch were

averaged to record mean clutch masses. Nestling mass was obtained only from nests

with known hatch dates and modal brood sizes (3 or 4) so as to standardize measurements

across nests and locations. Nestlings were always weighed on day 6 of the nestling

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. period (out of approximately 9 days) to reduce force-fledging after handling and control

for stage day.

Habitat Measurement

Brewer’s Sparrows concentrate their activities within the shrub layer, i.e., nesting,

foraging, perching, and singing all take place within or from the tops of shrubs (Wiens et

al. 1987, Rotenberry and Wiens 1989). We therefore identified four main shrub-layer

habitat attributes relevant to the ecology and behavior of Brewer’s sparrows on which to

focus our habitat analyses: percent shrub cover, shrub height, shrub density, and density

of potential nest shrubs. Shrub height, however, was redundant with shrub cover

(Pearson correlation: 0.48,P < 0.001) and showed identical preference/performance

patterns across scales, so we only present data on shrub cover. Designation of potential

nest shrubs was based on two years of prior study in which attributes (height, maximum

crown width, and % live crown) were measured and used to establish criteria for nest

shrubs. Specifically, potentially suitable nest shrubs needed to be between 20 - 175 cm

in height, 30 - 250 cm in width, and with a minimum of 25 % live crown. In addition,

shrubs needed to contain at least one semi-concealed “niche” within its branch structure

that could potentially accommodate a Brewer’s sparrow nest.

Habitat structure was measured within 5 m-radius vegetation plots (Martin et al.

1997). Plots were centered at nests, and at systematically located points throughout each

site (approximately one per ha). Systematic vegetation plots were establisheda priori

using site maps prior to bird arrivals, and so, by chance, some fell within territories and

some outside. Therefore, mean habitat attributes could be compared within versus

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. outside of areas chosen for territories during each year. In 2004 and 2005, two additional

vegetation plots were randomly established within each focal-pair territory, for more

precise quantification of potential differences in vegetation structure among territories

and in relation to reproductive performance.

Each vegetation plot was marked into 4 quadrants using a tent stake and 4

attached 5-m lengths of rope spread in the 4 cardinal directions from plot center. Within

each quadrant, we visually estimated the percent shrub cover, and counted the number of

shrubs in four different size classes (0-20, 20-50, 50-100 and > 100 cm) and the number

of potential Brewer’s sparrow nest shrubs. We also recorded the shrub species and height

of each shrub touching the rope lines. Habitat measurements from the four quadrants at

each plot were averaged. Only shrubs larger than 20 cm in height were included in total

shrub density estimates.

Data Analysis

Three unique sets of preference and fitness metrics were used to assess habitat

relationships of Brewer’s sparrows across the three spatial scales (Table 1). We initially

explored the relationship between Brewer’s sparrow nesting chronology and densities

using ANCOVA with year as an additional factor, in order to determine whether density

was a suitable index of habitat preference at the landscape scale. We specifically

predicted that Brewer’s sparrows should initiate first nests earlier within landscapes with

higher densities. We also tested for density-dependent effects by examining the

relationship between sparrow density and seasonal fecundity (number of offspring

produced per pair) (Fretwell and Lucas 1970).

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Landscape-level analyses of habitat preference and reproductive performance

were conducted using ANCOVA, with year as a factor in both models. Territory density

was the dependent variable in habitat preference models, with percent shrub cover, shrub

density, and potential nest shrub density, respectively, as covariates. Daily nest survival

probability was the dependent variable in models evaluating landscape-level fitness

consequences. We also compared nest survival probabilities with actual seasonal

fecundity estimates from each site and year to assess the efficacy of using Mayfield nest

survival probabilities as an accurate fitness metric.

Territory-level habitat preferences were assessed by comparing means of the three

shrub attributes between territory and non-territory areas using ANCOVA. Year and

study site were included as additional factors. Fitness consequences at the territory scale

were compared to each habitat attribute using ANCOVA with seasonal fecundity as the

dependent variable, and year and study site as additional factors.

Habitat attributes were compared between nest and systematic patches to

document nest patch preferences, and between successful and depredated nests to

examine reproductive success in relation to nest patch choice, using ANOVA. Year and

study site were included as additional factors in all models.

Comparisons of additional demographic components (clutch size, clutch mass,

nestling mass, and numbers of nesting attempts) were conducted only at the landscape

scale. Brewer’s sparrows can forage and obtain resources outside of territory boundaries,

and therefore, landscape-scale analyses of fitness components were most appropriate.

Clutch size and estimates of numbers of nesting attempts were examined with respect to

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. site-level habitat means using ANCOVA, with year as a fixed factor. Clutch and nestling

mass data from 2005 were compared across study sites using linear regression.

RESULTS

Brewer’s sparrow pairs initiated first nests earlier at study sites with higher

breeding densities during all 3 years of the study (date: F li252 = 53.18, P < 0.001; year:

F2,252 = 1-39, P = 0.25), though the relationship was slightly relaxed in 2005 (year x

density: F2,252 = 4.63, P = 0.01) (Figure 1). Moreover, seasonal reproductive success,

while annually variable (year: F2,23 = 5.73, P = 0.01), did not decline with increased

Brewer’s sparrow density (success: F i j23 = 1-57, P = 0.23; year x density: F 2>23 = 1-57, P

= 0.24) (Figure 2). We therefore focused on density as an index of habitat preference in

subsequent landscape-scale analyses.

Mayfield nest survival probabilities were positively correlated with season-long

reproductive success across sites during all years of the study (success: F ]j23 = 7.54, P =

0.01; year: F 2>23 = 0.40 , P = 0.68; success x year: F 2j23 =0.82 , P = 0.46) (Figure 3). The

use of nest survival probabilities as an index of fitness in subsequent landscape-level

analyses therefore seemed justified.

Brewer’s sparrows preferentially settled in landscapes with higher shrub cover

(Fi,23 = 71.77, P < 0.001) and slightly lower shrub density (Fi >23 = 8.84, P = 0.008)

during all 3 years of the study (year: F 2>23 = 0.38, P = 0.69) (Figure 4). Landscape-scale

settlement was unrelated to potential nest shrub densities (Fi >23 = 0.006, P = 0.94; Figure

4). Landscape-scale nest survival showed no relationship with shrub cover (Fi>23 = 0.71,

P = 0.41), density (Fi >23 = 0.10, P = 0.75), or potential nest shrub density (Fii23 = 0.12, P

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. = 0.73) during any year of the study (year: F\z$ = 3.37, P = 0.06) (Figure 4). Seasonal

reproductive success was similarly unrelated to shrub cover (Fii23 = 0.25, P = 0.62),

density (F )i2 3 = 0.10, P = 0.75), or potential nest shrub density (F]i23 = 0.10, P = 0.75),

though reproductive output was higher in 2005 (year: F 2>23 = 5.62, P = 0.01) (Figure 4).

Clutch size varied annually (F2>23 = 42.85, P < 0.001) but not in relation to any of

the habitat attributes (all P values > 0.05). Clutch mass in 2005 was similarly unrelated to

any of the landscape-scale habitat variables (overall model; F7 = 0.45, P = 0.77). The

number of nesting attempts per pair increased with shrub cover (Fi >23 = 8.58, P = 0.009)

but not shrub density (Fi j23 = 1.62, P - 0.22) or potential nest shrub density (Fi j23 =0.53,

P = 0.48) with no year effect (F2i23 = 0.54, P = 0.59) (Figure 4). Nestling mass also

increased with shrub cover (t = 2.69, P = 0.04) but decreased with potential nest shrub

density (t = - 2.75, P = 0.04) (Figure 4).

Brewer’s sparrows selected territories containing greater shrub cover (Fi,623 =

31.98, P < 0.001) and potential nest shrub density (Fi,623 = 13.44, P < 0.001) but not

shrub density (Fi >623 = 2.35, P = 0.13) after accounting for variation across study sites

(F7, 623 = 4.53, P < 0.001) (Figure 5). Patterns were similar across years (year: (F2>623 =

0.10, P = 0.91; year x site: Fu,623 = 0.56, P = 0.90). Seasonal reproductive success was

higher within territories with higher potential nest shrub density (F i^ = 4.17, P = 0.04)

but not shrub cover (F i^ = 0.30, P = 0.59) or density (F^gg = 0.16, P = 0.69) (Figure 5).

Overall territory-level reproductive success was higher in 2005 than 2004 (year: F ]^ =

8.46, P = 0.005).

Shrub cover did not differ between nest and systematic patches (F ij366 = 1-45, P

= 0.23; Figure 6), even after accounting for variation due to year (F2ii366 = 17.42, P <

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 0.001) and study site (F7ii 366 = 15.34, P < 0.001). Shrub cover was also similar between

successful versus depredated nest patches (Fii508 = 0.008, P = 0.93) (Figure 6). Both

shrub density and potential nest shrub density were higher in nest patches compared to

systematic patches, yet nest success was only higher in patches containing greater

potential nest shrub density (Figure 6; Chapter 3).

DISCUSSION

Brewer’s sparrows showed clear habitat preferences within each spatial scale that

we examined, but preferences varied across scale. At the largest scale, Brewer’s

sparrows preferentially settled in landscapes with higher shrub cover and greater shrub

height throughout the duration of the study. At the smallest scale, birds selected nest

patches with higher shrub density and potential nest shrub density. Choices at the

intermediate scale of the territory seemed to reflect a “best of all worlds” scenario in

which all attributes examined (shrub cover, shrub density and potential nest shrub

density) were greater than available, on average, throughout the landscape.

Concordance between habitat preferences and nesting success was especially

evident at the nest patch scale. Successful nest patches clearly contained higher densities

of shrubs that were suitable for nesting. In Chapter 3, we experimentally examine the

potential processes underlying the relationship between potential nest shrub density and

nest predation rates, within the context of the interaction between predator foraging

strategies and microhabitat structure. Potential nest site density also corresponded with

higher seasonal fecundity of Brewer’s sparrow pairs at the territory scale, further

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. emphasizing the importance of this previously largely unrecognized and unappreciated

habitat attribute.

Birds settled earlier and in higher densities in landscapes containing greater

overall shrub cover and taller shrubs. Yet, nesting success and seasonal reproductive

success were not higher in such landscapes. The apparent mismatch between landscape-

scale habitat preferences and reproductive performance in our study is therefore an

intriguing result. The pattern that nesting success was relatively similar across sites

regardless of habitat structure and density is consistent with the predictions of the Ideal

Free Distribution (Fretwell and Lucas 1970). According to the IFD model, individuals

should settle in the highest quality habitats first, but fitness declines as densities increase

in preferred habitats. The end result can therefore be similar reproductive outputs across

sites of varying territory density.

Yet, the Ideal Free Distribution model does not explain why Brewer’s sparrows in

our study preferred landscapes with higher shrub cover. One explanation is because of

benefits accrued through fitness components other than nesting success. Indeed, both

numbers of nesting attempts and offspring size increased with shrub cover. Maximizing

renesting ability may be especially critical when nest predation rates are high, but may

also permit exceptional breeding performance during lower predation periods (Holmes et

al. 1992, Nagy and Holmes 2004, Grzybowski and Pease 2005). Settling in landscapes

that maximize renesting potential should also be beneficial in systems where nest

predation rates are highly temporally and spatially variable, as they are at our sites.

Nestling mass was also significantly greater in landscapes containing higher shrub cover.

Such landscapes may therefore act in a cumulative way to enhance offspring quality via

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. greater overall productivity of the shrub layer and associated insect prey (Rotenberry and

Wiens 1998, Morrison and Bolger 2002). If offspring quality subsequently influences the

lifetime fitness and/of performance of individuals as in other systems (Roff 1992, Sinervo

1990), landscape preferences may reflect selection on offspring quality in addition to

quantity.

Large-scale habitat preferences may also reflect more long-term optima than we

were able to characterize during our study. Conversely, if critical attributes of

shrubsteppe habitats in our study area or surrounding areas have been changed from

historical conditions, populations may not have had enough time to respond and readjust

habitat preferences accordingly. The vast majority of high cover, tall sagebrush areas in

Carbon County have been converted for agriculture and/or altered due to livestock

grazing. Habitat loss may therefore now be concentrating many different organisms

(many of which will depredate nests upon incidental contact) into the remaining high-

cover, tall sage patches. Nest predation rates in these remaining patches may thus be

higher relative to historic levels and represent an ecological trap (Robertson and Hutto

2006).

The mismatches that we document between landscape-scale habitat preferences

and nesting success are unlikely to due to methodological artifact. First, while many

researchers correctly caution that density is not always a suitable indicator of habitat

preference and/or quality (Van Home 1983, Wheatley et al. 2002), Brewer’s sparrow

densities at our study sites were positively correlated with habitat preferences and several

aspects of breeding habitat quality. Birds settled earlier and reared larger offspring in

landscapes with greater shrub cover and height, and territory density was significantly

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. related to the overall number of offspring fledged per unit area. Interestingly, occupancy

patterns also remained consistent among sites across years, a pattern that further suggests

habitat preference and is contrary to previous results in this system (Rotenberry and

Wiens 1980). Controversy has also arisen over whether aggregate estimates of nest

survival such as Mayfield (1975) represent actual seasonal fecundity (Jones et al. 2005).

However, we ensured upfront that our fitness indices accurately reflected fitness

components. Daily Mayfield nest survival probabilities were significantly positively

correlated with seasonal fecundity estimates during all three years of the study.

In conclusion, animal habitat preferences are scale-dependent. Apparent

mismatches between habitat preferences and resulting fitness consequences could

therefore occur when preferences and performance are only examined within a single

spatial scale. Our results are also consistent with the hypothesis that the resources

forming the basis for habitat choice (such as refugia from predators and food availability)

may vary in importance across spatial scales, and may manifest in different (but

potentially equally important) ways in terms of fitness consequences. Our study therefore

emphasizes the utility of integrating multiple spatial scales and resulting fitness

components into studies of habitat selection. Understanding which habitat characteristics

are important across different, ecologically-relevant scales will help elucidate factors

truly underlying habitat choices, and will lead to improved assessment of habitat quality

for the successful maintenance of animal populations.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. ACKNOWLEDGEMENTS

We thank D. Barton, C. Miller, D. Emlen and the Emlen Lab, T. J. Fontaine, K.

Decker, R. Fletcher and C. Ricketts for support and advice, and numerous field assistants

for their hard work in data collection. Special thanks to Jayson Parks for much help and

support. Funding was provided by an NSF EPSCoR Fellowship to ADC, the Bureau of

Land Management (Billings Field Office), a SWG grant through Montana Fish, Wildlife

& Parks, and the U. S. Forest Service (Rocky Mountain Research Station, Missoula).

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Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Table 1. Indices used for quantification of habitat preferences and fitness/demographic

consequences of Brewer’s Sparrows at each spatial scale.

Habitat Preference Indices Fitness Indices

Landscape

Daily nest survival probabilities,

seasonal reproductive success,

Territory density and initiation clutch size, clutch mass, nestling

dates of first nests in relation to mass, numbers of nesting

site-level habitat characteristics attempts/pair

Territory

Habitat attributes of territories

versus non-territory areas Seasonal reproductive success

Nest Patch

Habitat attributes of nest patches

versus systematic points Individual nest fates

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. FIGURE LEGENDS

Figure 1. Chronology of Brewer’s sparrow first nest initiations (Julian date) in relation

to breeding densities during 2003-2005 in Carbon County, MT.

Figure 2. Brewer’s sparrow seasonal reproductive success (total number of offspring

fledged per pair) in relation to breeding densities in Carbon County, MT.

Figure 3. Landscape-scale daily nest survival probabilities in relation to seasonal

reproductive success estimates (number of young fledged/pair) from a sub-set of color-

marked Brewer’s sparrow pairs on each site during 2003-2005 in Carbon County, MT.

Figure 4. Landscape-scale habitat preferences and associated fitness consequences of the

Brewer’s sparrow in Carbon County, MT during 2003-2005 in relation to% shrub cover

(left column), shrub density (center column), and potential nest shrub density (right

column). Rows display density (territories/ha), daily nest survival, seasonal reproductive

success (total offspring fledged/pair), numbers of nesting attempts per pair, and mass of

six-day-old nestlings (2005 only) respectively, from top to bottom. Asterisks in upper

left indicate significance at the P < 0.05 level; double asterisks indicate P < 0.01.

Figure 5. Territory-scale habitat preferences (left column) and seasonal reproductive

success (right column) of Brewer’s sparrows during 2003-2005. Rows display data for %

shrub cover, shrub density, and potential nest shrub density, respectively, from top to

bottom.

Figure 6. Brewer’s sparrow patch-scale habitat preferences (left column) and nest

success (right column) in relation to % shrub cover (top row), shrub density (center row),

and potential nest shrub density (bottom row) during 2003-2005.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 0 § 150 S 148 # - - 2003 O — 2004 : I 1 4 6 2005 142 0 140 o 138 0 5 136 c 134 0 3 132 “ 3 0.0 0.5 1.0 1.5 2.0 2.5 3.0 3.5 Territories/ha

Figure 1.

Seasonal reproductive success 0 2 3 4 5 6 1 i 7 . 05 . 15 . 25 . 3.5 3.0 2.5 2.0 1.5 1.0 0.5 0.0 • ' y j o n‘ •h •h ...... ■ Density (territories/ha) Density o ~i_i _ W - - - .... " " 1 ■ a... . V— ^ — o ■ • .... 2005 2004 2003 O Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. without prohibited reproduction Further owner. copyright the of permission with Reproduced Figure 3. Figure

Seasonal reproductive success 0 2 3 4 5 1 6 7 .0 .2 .4 .6 0.98 0.96 0.94 0.92 0.90

— o ..... ■ • Daily Mayfield nest survival nest Mayfield Daily 2005 2004 2003 60 1.00 • - - 2003 O — 2004 ■ ..... 2005 3.5 _cCO 3.0 ^/5 2.5

~ 2.0

0.5 0.0

1.00

0.98

3 0.94 CO CO 0.92

0.90

CO . i c 1°- o • o_ 8 TS CD Q C/D Q . CO CO 8 o

3.5 ** 3.0 o ■ CO 'cO 2 5 C05 Q 2.0

8.8 ^ 86 g 5 2 ? 8 4 = CO 8.2 CO {2 8 0 CD TO

7.6 7.4 24 26 28 30 32 34 36 38 0.6 0.7 0.8 0.9 1.0 1.1 1.2 0.450.45 0.50 0.50 0.55 0.55 0.60 0.60 0.65 0.65 % shrub cover Shrub density/m2 Potential nest shrubs/m2

Figure 4.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Preference Success 1 — — 2004 O — 2005

810

0 0 j o 26 COCD O O ruQ CD 24 ocns e a c o o o co 22

10 20 30 40 50 % shrub cover 0.55 0 CD O O COO O 0 o c o o « o co 0.45 - a m o o c ra a o c # c r (l ^ ' m m mjtD-fxy-m' "So • 0 —0 • • • • • • • 0 •» «d» CB* 0

0.5 1.0 1.5 2.0 2.5 3.0 0.30 Shrub density/m2

* £ 0.65 o 0 0 0 o o 8 6 o o o * o a o _ co 0.55 U d) o ------~ 1 4 c 03 ot^a-MicxEi • o 0 0.50 ■S 2 • • • H— * c C o o 0 ajc/3 0 • • ••• CD * 0 (13 B 0.45 CO Q. 0.2 0.4 0.6 0.8 1.0 1.2 Territory Non-territory Potential nest shrubs/m2

Figure 5.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Preference Success

n 24 ' i. M Bs

■: < rt*

*■:' **

fl> 1.0 ■ # *j Va^T « vf

CM 0.75 (6 0.70 .Q

*- 0.60 c 0.55 ~ 0.50

Nests Non-nest Successful Depredated

Figure 6.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. CHAPTER III

ADAPTIVE NEST SITE SELECTION: ALTERNATIVE HYPOTHESES AND

EXPERIMENTAL TESTS

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. ABSTRACT

Breeding habitat preferences are assumed to result from natural selection favoring

choice of sites with the greatest potential for reproductive success. Yet, many studies of

reproductive site selection across diverse taxa have reported mismatches between habitat

preferences and reproductive performance. Such mismatches may be explained by

intercorrelated habitat variables that obscure patterns, and/or a lack of understanding of

how important agents of selection interact with habitat attributes. We used observational

data and a habitat manipulation experiment to test two hypotheses for why microhabitat

structure may influence nest site preferences and rates of nest predation (an important

agent of selection) in the Brewer’s sparrow(Spizella breweri). The total-foliage

hypothesis predicts that nest predation will decline in areas of greater overall vegetative

density, whereas the potential-prey-site hypothesis predicts that nest predation should be

lower in areas where predators must search among a greater number of potential nest

sites. Our results show clear support for the potential-prey-site hypothesis, and reject the

total-foliage hypothesis. We show, moreover, that when these two correlated ecological

variables (total foliage and potential prey site density) are included in measures of site-

specific reproductive performance, actual variation in nest site quality matches very

closely with nest site preferences. Developing a better understanding of habitat selection

may therefore require a more explicit understanding of how important processes such as

nest predation are mediated by habitat features.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. INTRODUCTION

Understanding why animals select particular habitats over others is of critical

importance for explaining distributional patterns of organisms and differentiating

between habitats of different value. Under natural conditions, habitat preferences are

assumed to be shaped by fitness outcomes (Jaenike and Holt 1991, Orians and

Wittenberger 1991, Martin 1998). Choice of habitat in which young are reared are

particularly critical, especially for temporarily sessile offspring (Price 1998, Lindstrom

1999, Brown and Shine 2004). The choice of oviposition or nest site, for example, can

determine the probability that enemies such as predators or parasites will discover young

(Thompson and Pellmyr 1991, Martin 1992, 1993, 1998; Clark and Shutler 1999, Kolbe

and Janzen 2002). Such risks should impose strong selection for the evolution and

maintenance of preferences for safer habitats.

Clear examples of adaptive reproductive site preferences, however, are

uncommon (Mayhew 1997, Martin 1998, Clark and Shutler 1999, Misenhelter and

Rotenberry 2000). Many studies have shown neutral or even negative relationships

between preferred habitats and indices of reproductive success across a wide variety of

taxa including insects, reptiles, and birds (Thompson 1988, Holway 1991,Valladares and

Lawton 1991, Filliater et al. 1994, Hoover and Brittingham 1998, Wilson and Cooper

1998, Misenhelter and Rotenberry 2000, Willson and Gende 2000, Kolbe and Janzen

2002, but see Martin 1998).

Apparent mismatches between reproductive site preferences and resulting

reproductive performance may result in some cases due to intercorrelations between

important and unimportant habitat variables. If two habitat variables are correlated, and

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. only one is measured and related to preferences and reproductive performance,

researchers may not correctly identify which habitat attribute actually influences the

fitness consequences of habitat use and habitat choices.

Clarifying which habitat features are likely to be important in terms of fitness

consequences and habitat choices also requires consideration of how important selective

agents such as predators interact with habitat structure. Past research has emphasized the

relationship between habitat structural complexity and predator foraging success,

especially in aquatic systems (e.g., Crowder and Cooper 1982, Warfe and Barmuta 2004).

However, the specific mechanisms for why microhabitat structure influences predator

foraging strategies or success are unclear.

For avian systems, the total amount of vegetation surrounding reproductive sites

is often examined relative to reproductive success (e.g., Holway 1991, Howlett and

Stutchbury 1996, Hoover and Brittingham 1998, Braden 1999), and may be an important

influence on predation risk. However, we need to carefully consider how such habitat

factors may influence processes such as predation. Two specific scenarios could lead to a

relationship between vegetation structure and nest predation risk (Martin and Roper 1988,

Martin 1992, 1993). First, individuals might benefit by selecting habitat patches

containing denser foliage because this better conceals reproductive sites from predators

and/or physically impedes predator search efforts (total-foliage hypothesis). Second,

individuals may benefit by selecting patches containing a greater number of potential

reproductive sites because predators should abandon search efforts sooner where more

unoccupied potential prey sites must be searched before finding occupied sites (potential-

prey-site hypothesis). Yet, these alternative hypotheses of specific habitat factors and

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. their influence on predation risk have rarely been explicitly tested (but see Martin and

Roper 1988, Martin 1998, Liebezeit and George 2002, and Mezquida and Marone 2002).

In this study, we collected observational data on reproductive site choice and

reproductive success across multiple study sites and years, and conducted the first

experimental test designed to differentiate between the total-foliage and potential-prey-

site hypotheses. Specifically, we focused on nest predation rates in relation to

microhabitat structure for a passerine bird.

METHODS

We identified a songbird species that breeds within North American shrubsteppe

habitats, the Brewer’s sparrow (Spizella breweri), as a promising study species with

which to test the two hypotheses. Brewer’s sparrows are locally abundant during the

breeding season, select nest sites across a gradient of microhabitat structure, and nest in

shrubs, which constitute discrete and quantifiable nest sites. Brewer’s sparrow nests are

depredated by a diverse suite of predators, including two species of snakes, rodents,

medium-sized mammals, and corvids (ADC personal observation). Moreover, nest

predation is the primary cause of reproductive failure in this system (Rotenberry and

Wiens 1989).

Data were collected during May-August 2003-2005 on public and private lands

within southern Carbon County, Montana, USA. Eight 30-ha study sites, each separated

by > 1 km, were chosen that represent the full range of structural habitat variation typical

of shrubsteppe systems. Sites were dominated by big sagebrush (Artemisia tridentata),

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. with scattered greasewood (Sarcobatus vermiculatus) and rabbitbrush (Chrysothamnus

spp.).

Observational Data

Nests were located by observing parental behaviors and/or by systematically

searching shrubs within an active territory, and monitored every 2-3 days (Martin and

Geupel 1993). Nests were considered successful if they fledged at least one young, and

depredated if nest contents disappeared earlier than possible fledge dates. Following nest

completion, we measured (1) the total number of shrubs greater than 20 cm in height as a

proxy for the total amount of foliage, and (2) the total number of shrubs in the patch that

could potentially accommodate a Brewer’s sparrow nest (potential prey sites), within a 5

m-radius patch surrounding each nest. The designation of a potential nest shrub was

based on two years of prior study in which attributes (height, crown dimensions, percent

live crown) of 334 shrubs used as nest sites were measured to determine the range of

these attributes for identifying potential nest shrubs. We also estimated the density of

total foliage and potential nest shrubs within 5 m-radius vegetation sampling plots located

systematically throughout all 8 study sites (approximately one sampling plot per ha per

site). Systematic samples were used to determine the distribution of total foliage and

potential nest shrub densities available to the birds on average.

Total foliage and potential nest shrub density were compared between nest versus

systematic patches to document nest patch preferences, and between successful and

depredated nests to examine reproductive success in relation to microhabitat choice,

using ANOVA. Year and study site were included as additional factors in all models.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Year was not significant in any model, and data were pooled across years for subsequent

analysis. Study sites differed in nest site choice analyses, so comparisons of nest site

choice were also made within each plot using t-tests for independent samples, with

critical p-values adjusted for 8 comparisons using a Bonferroni correction.

Measuring the resulting fitness components of phenotypic traits such as

reproductive site choice also affords the opportunity to examine the actual form and

significance of natural selection operating on traits (Lande and Arnold 1983, Schluter

1988, Brodie et al.1995, Martin 1998). We estimated the fitness surfaces for nest

survival relative to total foliage and potential nest shrub density in patches using non-

parametric cubic spline regression (Schluter 1988). Cubic spline regression was applied

to binomial (successful versus depredated) data as in Martin (1998). These analyses

determined the relative intensity of selection via the coefficient of variation in relative

fitness, measured as predicted fitness (Schluter 1988, Brodie et al. 1995). Confidence

limits for splines were estimated by bootstrapping in which the original data were

resampled 200 times (Schluter 1988, Martin 1998). Analyses were conducted using

software provided by D. Schluter. Selection differentials, or the phenotypic response to

selection within a generation, were calculated following Lande and Arnold (1983) and

Schluter (1988). Specifically, we estimated the selection differential, s, as the slope of

the univariate regression of relative fitness on total foliage and potential nest shrub

density, respectively.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Microhabitat Manipulation Experiment

To more conclusively differentiate between the total-foliage and potential-prey-

site hypotheses, we also conducted a microhabitat manipulation experiment. Four

additional study sites were chosen for experimental tests in 2004 and 2005. We grouped

nests into triads and randomly designated one as a control and two as experimental nests.

Nests within each triad were initiated (date first egg laid) within 5 days of one another,

and separated by no more than 500 m to control for potential temporal or spatial effects.

Nest patches initially contained a minimum of 50 potential nest shrubs (approximate

mean for previously measured Brewer’s sparrow nest patches). Manipulation of each

nest occurred early in the incubation period (day 1 to day 6) to ensure adequate exposure

to treatments. During each year, nest triads were replicated 7-10 times within each site.

For the total foliage experimental nest within each triad, we removed 50% of

shrubs > 20 cm in height within the 5 m-radius patch relative to paired control nests using

pruning shears, but only those shrubs deemed unlikely to be used as nest shrubs. At the

potential prey site experimental nest patch, we also removed 50% of shrubs relative to

controls, but only shrubs classified as potential nest shrubs. Within control nest patches,

we counted the total number of shrubs > 20 cm in height and the total number of potential

nest shrubs, and made small clippings of shrub tips to mimic the disturbance and

potential scent of shrub cuttings that occurred at experimental nests. All experimental

treatments were conducted on the same day for each nest within a triad. Manipulations

took 10-20 minutes to complete, and we spent the same amount of time within control

nest patches to account for possible disturbance effects. Each nest was monitored every 2

days to document nest fate.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. For each nest, we calculated the proportion of potential post-treatment survival

days using 11 days for the incubation period and 8 for the nestling period. For example, if

a nest was manipulated on day 2 of the incubation period and it failed on day 4, survival

was 2/17 days, or 0.12. Nests that survived to fledge received a 1.00. Data were arcsine

transformed and survival of experimental nests was compared to control nests within

each year using paired t-tests. Responses were similar across study plots (independent

samples t-tests, all P values > 0.05) so plots were pooled for further analysis.

Under the total-foliage hypothesis, we predicted that both types of experimental

removals would significantly decrease nest survival relative to control nests. Under the

potential-prey-site hypothesis, we predicted that only the removal of potential nest shrubs

would significantly decrease nest survival relative to controls.

RESULTS

Total-Foliage Hypothesis

Birds consistently chose nest patches with more total foliage than available on

average in the landscape (patch type: F yt 1132 = 205.99, P < 0.0001; Figure la). The

amount of total foliage in nest and systematic patches differed among study sites (study

site: F 7j 1132 = 10.97, P < 0.0001) to differing extents (study site x patch type: F iy 1132 =

11.86, P < 0.0001). Nest patches contained a significantly greater amount of total foliage

than systematic patches within 6 of the 8 individual study sites (Figure la).

The amount of total foliage in nest patches did not differ between failed versus

successful nests (nest fate: F i, 457 = 0.12, P = 0.73). Total foliage again differed among

study sites (study site: F 7j 457 = 8.20, P < 0.0001), but the lack of difference in total

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. foliage between successful and failed nests remained consistent across sites (study site x

nest fate: F 7, 457 = 0.52, P = 0.82). Brewer’s sparrows showed no selection for the

amount of total foliage in nest patches(P = 0.68, Figure 2a) as also indicated by a

selection differential, s, of 0.02 ± 0.048 that does not differ from zero.

Observational results were confirmed in microhabitat manipulation experiments.

Experimentally reducing the total amount of foliage in nest patches did not affect rates of

nest predation in 2004 (t = 0.34, P = 0.73) or 2005 (t = 0.12, P = 0.91) (Figure 3).

Potential-Prey-Site Hypothesis

Patches chosen for nesting contained a greater density of potential nest shrubs

than available on average within the landscape (patch type: F 1,1125 = 130.81, P < 0.0001),

though densities varied across study sites (study site: F 7,1125 = 6.61, P < 0.0001) to

differing extents for nest and systematic patches (study site x patch type: F 7,1125 = 5.34, P

< 0.0001) (Figure lb). Nest patches contained a significantly greater density of potential

nest shrubs within 7 of 8 individual study sites (Figure lb).

The density of potential nest shrubs in nest patches was greater at successful than

failed nests (nest fate: F 1 ,4 5 7 = 5.25, P = 0.02; study site x nest fate: F 7 ,4 5 7 = 0.73, P =

0.65). Brewer’s sparrows showed strong directional selection for the density of potential

nest shrubs in nest patches (P = 0.001, Figure 2b.) as further indicated by a large

selection differential, s, of 0.365 ± 0.105.

Finally, experiments again confirmed observational results. Experimental

removal of potential nest shrubs from patches significantly decreased rates of nest

survival in 2004 (t = 2.18, P = 0.04) and 2005 (t = 2.95, P = 0.006) (Figure 3).

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. DISCUSSION

While Brewer’s sparrows in our study preferred nest patches containing both a

significantly greater amount of total foliage and density of potential nest sites than

available on average, only the density of potential nest sites was positively correlated

with nest survival. Notably, cubic spline analysis showed strong directional selection for

nest patches containing greater densities of potential nest shrubs, and no selection

operating on total foliage density. Experimental manipulation of microhabitats further

confirmed the importance of potential nest sites within nest patches to nesting success.

Therefore, our observational and experimental results suggest: (1) that birds in our study

system are exhibiting adaptive nest site selection behaviors at a local scale, (2) support

for the potential-prey-site hypothesis, and (3) rejection of the total-foliage hypothesis.

Many previous studies of nest site selection and reproductive success have

focused on factors related to the total amount of foliage within nest patches (e.g., Holway

1991, Wilson and Cooper 1998, Hoover and Brittingham, Braden 1999, Jones and

Robertson 2001) whereas the concept of potential-prey-site density has rarely been

explicitly investigated (but see Martin and Roper 1988, Martin 1988, 1992, 1993, 1998;

Liebezeit and George 2002, Mezquida and Marone 2002). Several researchers, however,

identified potential-nest-site density in nest patches as a possible post hoc explanation for

habitat-nest success relationships (Holway 1991, Ricketts and Ritchison 2000, Jones and

Robertson 2001, Moorman et al. 2002).

Our study raises an important caveat to future studies designed to assess habitat

preferences and the fitness consequences of habitat use. Total foliage and potential nest

site density were correlated in our study system; more potential nest shrubs in an area

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. were associated with increased total density of vegetation (Pearson r = 0.51, P < 0.0001,

n = 958). Nest patches chosen by birds contained more total foliage than available on

average, and thus, a study that merely looked at habitat choice relative to random would

have concluded that total foliage forms an important basis of habitat preference.

Moreover, if the total amount of foliage within nest patches were the only habitat

attribute identified in advance as potentially important and measured with respect to

nesting success, we would have failed to find the reason for why birds likely choose

patches containing a greater amount of total foliage. Indeed, we would have concluded,

as many previous habitat selection studies have, that preferred habitats were unrelated to

reproductive success. If habitat attributes actually driving habitat choice are not

identified, researchers may incorrectly conclude that habitat preferences are not adaptive,

and/or subsequent habitat priorities may be developed and management actions

implemented that impart neutral or even negative consequences to the target population.

Undoubtedly, the extent to which the total-foliage hypothesis, potential-prey-site

hypothesis or other habitat hypotheses will be supported within any given system will

depend on the nature of the habitat, as well as the composition of the predator assemblage

and the dominant search strategies employed by specific predator types (Martin and Joron

2003). For example, within a desert scrubland dominated by avian nest predators,

Mezquida and Marone (2002) found no support for the potential-prey-site hypothesis,

whereas in a more vegetated forest system dominated by small mammalian predators,

Martin (1988, 1998) found that patches containing a greater number of plant stems of the

type used for nesting significantly decreased rates of nest predation. Further examination

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. of the interactions between predator foraging strategies and reproductive site attributes

would be a fruitful line of research.

In conclusion, our observational and experimental analyses showed strong

support for the potential-prey-site hypothesis for a common bird species in shrubsteppe

habitats, across multiple spatial replicates and several years of study. Interactions

between predator foraging success and habitat structure is therefore more complex than

simple impedance by vegetation. Future tests of the potential-prey-site hypothesis in

other ecological systems will aid in the determination of its ubiquity. Our results further

highlight the utility of experimental manipulations for clearly differentiating between

correlated habitat characteristics and identifying those that are truly important in terms of

fitness consequences.

ACKNOWLEDGEMENTS

We are grateful to J. Bolser, B. Breen, K. Ellis, C. Forristal, C. Hill, K. Jewell, K.

Nittinger, A. Saari, D. Rauch, D. Westerman and especially C. Ricketts, for assistance in

the field. Funding was provided by an NSF EPSCoR (US) fellowship to ADC, the U.S.

Bureau of Land Management, a USFWS State Wildlife Grant through Montana Fish,

Wildlife and Parks, BBIRD, the Montana Cooperative Wildlife Research Unit, and the

USDA Forest Service Rocky Mountain Research Station. Helpful comments on an

earlier version of the manuscript were provided by D. Barton, J. J. Fontaine, and R.

Fletcher.

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Wilson, R. R., and R. J. Cooper. 1998. Acadian Flycatcher nest placement: does

placement influence reproductive success? Condor 100:673-679.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. FIGURE LEGENDS

Figure 1. Brewer’s sparrow nest patch (0.5-m radius) choice in relation to the total

amount of foliage (density of shrubs > 20 cm in height) (a), and potential nest shrub

density (b) within patches during 2003-2005 in Montana, USA. Data are means ± 1 SE.

White bars represent nest patches and gray bars are systematic vegetation plots, within

each of 8 study plots. Asterisks indicate the significance of the patch type comparison

within individual plots, from independent samples t-tests with critical p-values adjusted

for multiple comparisons.

Figure 2. Fitness surfaces (probability of nest survival) of Brewer’s sparrows as a

function of the density of total foliage (a) and potential nest shrubs (b) in nest patches.

Dashed lines indicate ± 1 SE around the predicted probability of nest survival based on

200 bootstrap replicates of the fitness function.

Figure 3. Results of a microhabitat manipulation experiment in which the amount of

total foliage (light gray bars) and density of potential nest shrubs (hatched bars) within

0.5 m-radius Brewer’s sparrow nest patches were reduced relative to controls (white bars;

see text for complete experimental protocol). Data are means of the proportion of post

treatment survival days relative to possible survival days ± 1 SE.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. ** P < 0.001 3 N ests * P < 0.05 i Available

I - 0 . 8 -

3 4 5 6 Study Site

Figure 1.

Pr(nest survival) 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 0.2 1.0 0.3 0.4 0.5 0.6 0.7 0.8 0.9 . 10 . 20 . 30 . 40 4.5 4.0 3.5 3.0 2.5 2.0 1.5 1.0 0.5 . 0.4 0.2 oeta NetSrb/ 2 Shrubs/m est N Potential oa Foliage/m Total 0.6 83 0.8 1.0 1.2 1.4 Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. without prohibited reproduction Further owner. copyright the of permission with Reproduced Figure 3. Figure Proportion post-treatment survival days 0.6 . - 0.7 0.8 . - 0.9 1.0 - IZZZ2 Potential nest sites nest Potential IZZZ2 ] Control Control ] Total foliage foliage Total 2004 84 2005