UNIVERSITY OF CALIFORNIA, SAN DIEGO

Phainopepla nestlings adjust begging behaviors to different male and female parental provisioning rules

A thesis submitted in partial satisfaction of the requirements for the Master of Science degree

in

Biology

by

Jeanne Marie Messier

Committee in charge:

Professor Sandra L. Vehrencamp, Chair Professor David S. Woodruff Professor Joshua R. Kohn Professor Trevor D. Price

2000

The Thesis of Jeanne Marie Messier is approved, and it is acceptable in quality and form for publication on microfilm and electronically:

______

______

______

______Chair

University of California, San Diego

2000

iii

DEDICATION

This Thesis is dedicated to Anne and John Messier, in memory of their daughter Jeanne.

iv

TABLE OF CONTENTS

Signature page...... iii

Dedication...... iv

Table of Contents...... v

List of Figures...... vi

List of Tables...... vii

Preface...... viii

Acknowledgements...... x

Vita...... xi

Abstract...... xii

Introduction...... 1

Methods...... 5

Results...... 13

Discussion...... 28

References...... 34

v

LIST OF FIGURES

Figure 1. Provisioning and begging variables in subsequent parental visits...... 10

Figure 2. Feeding rates and weight gain for deprived nestlings and nestmates...... 16

Figure 3. Food allocation to deprived nestling versus its previous weight loss...... 17

Figure 4. Changes in begging behaviors between control and experimental sessions for deprived and non-deprived nestlings in male- and female-tended nests...... 23

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LIST OF TABLES

Table 1. Parental provisioning rates in control and experimental sessions...... 19

Table 2. Results of multiple linear regression analyses on parental allocation of feeds as a function of nestling begging behaviors...... 21

Table 3. Summary of primary nestling begging behaviors and cues used by parents to allocate food in each nest...... 26

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PREFACE

Jeanne Messier’s plan for her PhD dissertation research was to investigate the honesty of parent-offspring communication system in two avian species: one species with a small clutch of synchronously hatching chicks, which was predicted to exhibit honest signaling of chick hunger and reliable responsiveness by the parents; and another species with a larger clutch of asynchronously hatching chicks, which was predicted to exhibit some competition among the chicks, possible deceitful signaling of hunger, and parental discounting of chick begging signals. She selected the phainopepla and the robin, respectively. These species had open-cup nests for ease of videotaping, sexually dichromatic adults for distinguishing male and female parents, and non-overlapping breeding seasons. In 1993, her first full field with the early-breeding phainopepla,

Jeanne succeeded in conducting nestling removal and replacement studies at 8 nests.

Back in the lab, she trained an undergraduate assistant to score the nestling and parental behaviors in recorded videos, then headed up to northern California to work on the robins. Toward the end of the season she was stricken by a hantavirus infection, and was airlifted to a hospital in Reno where she fought for her life. Tragically, she lost.

As her advisor, I endeavored to complete the analysis of the phainopepla data.

The undergraduate student finished the video data extraction, and I ran the statistical analyses that Jeanne and I had planned, wrote a manuscript draft, and submitted it for publication to a behavior journal. Unfortunately, the manuscript was rejected because of the small sample size. The research project clearly would have benefitted from one more field season. Nevertheless, some highly interesting and statistically significant patterns emerged. She would have been among the first to show parental sex differences

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in provisioning responses to nestlings, and furthermore to show that nestlings learn and adapt their begging behaviors to these sex-specific parental characteristics. Given

Jeanne’s well-designed study and skill in executing the field experiments, coupled with her outstanding performance on her earlier qualifying exam, the committee agrees that

Jeanne Messier is fully deserving of a posthumous Master of Science in Biology degree.

The committee verifies the academic integrity of this thesis submission, which is based on the submitted manuscript.

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ACKNOWLEDGEMENTS

We thank Erin Muntean for assistance in the field, Danton Kono and Catherine deRivera for assistance with the video analysis, and Professor Robert Schwager

(Cornell University) for statistical advice. Professors Arnon Lotem, Jonathan Wright, and Rebecca Kilner provided stimulating discussions, reviews of manuscript drafts, and access to unpublished manuscripts. The field research was supported by the Los

Angeles Audubon Society, Sigma Xi, the UC Natural Reserve System, and training grant support to JMM from the UCSD Biology department.

x

VITA

1988 BA, Biology, Cornell University

1990-1993 PhD Candidate, Biology, UC San Diego

2000 MS, Biology, UC San Diego

WORK EXPERIENCE

1988-1990 Research Assistant, Harvard Medical School

PUBLICATIONS

Shaw LM, Messier JM, Mercurio AM. 1990. The activation dependent adhesion of macrophages to laminin involves cytoskeletal anchoring and phosphorylation of the alpha-6-beta-1-integrin. Journal of Cell Biology 110:2167-2174.

Woo HJ, Shaw LM, Messier JM, Mercurio AM. 1990. The major non-integrin laminin binding protein of macrophages is identical to carbohydrate binding protein-35 (MAC-2). Journal of Biological Chemistry 265:7097-7099.

Messier JM, Shaw LM, Chafel M, Matsudaira P, Mercurio AM. 1993. Fimbrin localized to an insoluble cytoskeletal fraction is constitutively phosphorylated on its headpiece domain in adherent macrophages. Cell Motility and the Cytoskeleton 25:223-233.

Morin PA, Messier JM, Woodruff DS. 1994. DNA extraction, amplification, and direct sequencing from hornbill feathers. Journal of the Science Society of Thailand 20:31-41.

FIELDS OF STUDY

Behavioral ecology, animal communication, ornithology

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ABSTRACT OF THE THESIS

Phainopepla nestlings adjust begging behaviors to different male and female parental provisioning rules

by

Jeanne Marie Messier

Master of Science in Biology

University of California, San Diego, 2000

Professor Sandra L. Vehrencamp, Chair

We studied the nestling begging behaviors and parental provisioning responses of the phainopepla (Phainopepla nitens), a sexually dichromatic silky flycatcher native to Mexico and the southwestern United States deserts. Because of its small clutch size

(usually two eggs) and synchronous hatching strategy, we predicted that size-based nestling competitive interactions and brood reduction strategies would be absent, so that parental food allocation would accurately reflect nestling need. At eight nests we temporarily removed one nestling to deprive it of food, and video-taped the nestling and

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adult behaviors after the nestling was returned to the nest. Both male and female parents preferentially allocated food to the hungry nestling, but used different provisioning strategies and nestling cues to achieve this result. Males increased their visit rate and food load and used begging start order and initial beak height, as well as beg duration and intensity, as cues to allocate food. By contrast, females only increased food load and allocated resources to the nestling that begged more intensely. Most of our study nests were attended by only one parent. Hungry nestlings in male and female nests used different begging strategies associated with the cues employed by the parent

(start/height in male nests, beg intensity in female nests). Nestlings appear to learn which begging signal components are most likely to generate food rewards. We suggest that conditioned learning could be a common mechanism by which nestlings adjust their begging behavior to their need, but would lead to an honest parent-offspring signaling system only when conflicts of interest between sender and receiver are absent and competing senders experience similar conditioning regimes.

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INTRODUCTION

Begging signals by needy individuals toward potential donors have been a prime focus of theoretical models of signal honesty, because beggars are likely to benefit by exaggerating their need at the expense of donors (Maynard Smith 1991; Godfray 1991,

1995; Johnstone and Grafen 1992; Johnstone 1997, 1999). Nestling birds have been the empirical study system of choice, and the current view is that nestling begging signals are not always honest indicators of their need (Kilner and Johnstone 1997). An honest parent-offspring food solicitation signaling system can be demonstrated by first showing that one or more components of nestling begging behavior increase monotonically with increasing nestling need, and then demonstrating that parents use these cues or signals to preferentially deliver food to the neediest nestlings. The net result is a positive correlation between nestling need and rate of food received, which is a key prediction of the models for an evolutionarily stable strategy (Godfray 1995,

Johnstone 1997). Many careful studies of avian begging behavior have demonstrated the first stage of the signaling relationship, a positive correlation between nestling need and begging intensity, but some have failed to show the second stage, a positive association between begging intensity and provisioning rate (reviewed in Kilner and

Johnstone 1997, Budden and Wright 2000).

Conflicts of interest between parents and offspring and among offspring are responsible for degraded correlations at both stages. A reduced correlation between need and solicitation intensity can be caused by competition among siblings in a nest if less hungry nestlings escalate their begging intensity in the presence of a very hungry sibling (Smith and Montgomerie 1991, Godfray 1995, Price and Ydenberg 1995, Price

1 2 et al. 1996). Severely underfed nestlings may be too weak to signal their need accurately with vigorous and costly begging signals, resulting in a non-monotonic relationship between need and solicitation intensity. Complex interactions between nestling size (long-term need) and hunger (short-term need) could even lead to a negative relationship between need and solicitation intensity (Lotem 1998a,b). Another factor potentially confounding the need – signal intensity relationship is conditioned learning of begging responses by nestlings, which can produce individual variation in begging behaviors for a given level of need (Stamps et al. 1989, Kedar et al. 2000).

The most important cause of degraded correlations between signal intensity and parental provisioning rate is probably hatching asynchrony. Hatching asynchrony in species with large clutch sizes serves to heighten the effects of sibling competition by increasing the size differential among siblings. Larger nestlings can more effectively position themselves in the path of the arriving parent to monopolize feeding opportunities (McRae et al. 1993, Kilner 1995, Cotton et al. 1999, Ostreiher 2001).

Hungry but small nestlings therefore may not be able to obtain the food they need despite begging at high intensity. In some species, parents may intentionally feed larger nestlings more, especially as a brood-reduction mechanism when food supplies are low

(Kacelnik et al. 1995, Lotem 1998c, Krebs and Magrath 1999, Bu 1999). Another factor that may determine the correlation between signal intensity and resource delivery is the manner of feeding nestlings, which affects the ability of parents to assess nestling signals accurately. Single-load feeders usually make frequent and quick visits to the nest and may use immediately available information to decide which mouth to fill, whereas multiple-load regurgitation feeders spend more time at the nest, feed most or

3 all nestlings in a single visit, and have the opportunity to assess more subtle but reliable signals (Kilner and Davies 1998). Finally, male and female parents may employ different provisioning rules, permitting nestlings to adjust their behavior to divergent food delivery patterns, or making it difficult to discern the correlation between begging intensity and parental feeding responses in monomorphic species (Gottlander 1987,

Stamps et al. 1989, Slagsvold 1997, Kölliker et al. 1998, Krebs et al. 1999, Krebs and

Magrath 1999).

This study examines the nestling begging behavior and parental feeding responses of the phainopepla, Phainopepla nitens, an unusual passerine with a small clutch size, synchronous hatching, and a multiple-load regurgitation style of nestling feeding. Because of these life-history features, we predicted that competitive nestling interactions would be minimal and that parents would be able to assess nestling need accurately. In addition, adults are sexually dichromatic in plumage, allowing me to evaluate any sex-based differences in parental provisioning behavior. We manipulated nestling need by randomly removing one nestling for a period of time to increase the difference in hunger levels between the chicks. We then replaced it in the nest while monitoring its behavior, the behavior of its nestmate, and the parental provisioning responses. In this paper we first ask whether the hungrier nestling obtains more feedings, and whether male and female parents differ in their responses to the change in nestling need. We then attempt to identify which nestling behaviors affect the allocation of food to the two nestlings (i.e., the second-stage correlation between signals and provisioning rate). Lastly, we examine the first-stage correlation between nestling need and signals by asking which behaviors differ between the hungry and satiated

4 nestling relative to their behaviors in the pre-manipulation control period. If we find that the removed nestling is fed preferentially, and that the signals it uses when hungry are the same ones the parents use to preferentially allocate food to it, then the signaling system is basically honest.

METHODS

Study species

The phainopepla is a small (24 g) silky flycatcher that overwinters and attempts a first brood in the desert scrub and mesquite habitat of the southwestern United States and Mexico before migrating north to coastal woodland habitat for a second breeding attempt. In the desert sites, two, rarely three, eggs are laid one day apart, with the young hatching within a day of each other (Walsberg 1977). The nestlings are provisioned by one or both parents, who collect mistletoe berries and insects and deliver these in a series of regurgitations to all nestlings during each provisioning visit. The first few regurgitations (hereafter called feeds) tend to contain more insects and are therefore more protein-rich than the subsequent feeds. Nest predation appears to be high: eggs disappeared from five of 16 nests, and nestlings from three.

Experimental methods and video analysis

Eight phainopepla nests, each with a brood size of two, were studied from April

8 to April 21, 1993 at Deep Canyon Reserve near Palm Desert, Riverside County, CA.

Experiments were conducted when the nestlings were 5 to 16 days old. For identification purposes, nestlings were banded and their heads were marked using non- toxic acrylic paint. We mounted 8mm video cameras on nearby trees at positions slightly higher than the nest to record behaviors of nestlings and parents; the cameras did not seem to disturb the parents. Each experiment consisted of three parts: a 1-hr video-taped control session used to establish baseline begging and feeding rates; a 1- to

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2-hr removal period during which one randomly chosen nestling was removed from the nest, kept warm, and deprived of food; and a 45- to 90-min video-taped experimental session after the removed nestling was returned to the nest. Removed nestlings were returned to the precise location in the nest from which they had been taken. Both nestlings (removed and nestmate) were weighed after each part of the experiment, and once a day for several days before and after the experiment. Removed nestlings lost from 0 to 2 g during the removal period, but gained most of this weight back by the end of the experimental period. Our protocol was approved by the animal care committees at the University of California’s San Diego and Santa Barbara campuses.

Observers analyzed the video tapes without the knowledge of which nestling had been food-deprived. For each parental visit, we noted the time of the visit, parent sex, number of feedings to each nestling, and the amount of time the parent spent at the nest before starting to feed, while feeding nestlings, and after feeding nestlings. The total visit duration was segregated into feeding time, brooding time, and “other” time

(mostly standing at the side of the nest). We were careful to note “fakes” (where the parent starts to feed a nestling but withdraws its beak before food is delivered) and

“switches” (a fake followed by feeding the other nestling). Feeding rates were calculated by multiplying the number of visits per hour by the number of feeds per visit, yielding a measure of feeds per hour. We computed visit rate by multiplying the time lapse from the first to the last visit of a session by the number of visits minus one. This procedure removed differential lag time effects of human disturbance from the handling of nestlings and camera, as well as any effects of provisioning just one nestling in the removal period on the initial parental responses during the experimental session. The

7 percentage of feeds to each nestling was computed as the number of feeds to a nestling during a visit divided by the total number of feeds in that visit. The fraction of first feeds given to each nestling was calculated for each session. Finally, we also scored fecal sac removals and time spent brooding; the latter always occurred at the end of a feeding visit.

Using the method of Redondo and Castro (1992), begging intensity was divided into ranked categories based on body posture. Nestlings that did not raise their heads at all received a score of 0. Nestlings begging with a partially open beak, a horizontally oriented beak, or relaxed neck received a score of 1. Lack of body shaking while begging also received a score of 1. Begging with an open beak oriented toward the parent's beak and at least a partially extended neck while shaking was scored as 2. A score of 3 was assigned to a fully extended neck and open beak with some tarsal extension while shaking, and a score of 4 required full extension of the neck and tarsus accompanied by shaking and wing flapping. Observers recorded the duration of each level of begging intensity for each nestling, starting with the nestling opening its beak and ending with the first of: closing its beak for more than two seconds, returning to a resting position for the remainder of the visit, or parental departure. A nestling typically switched between different begging intensity ranks during a parental visit. Each begging intensity level was multiplied by its duration. For each visit, these products were summed and then divided by the total begging duration to calculate an average begging intensity.

Several other begging behaviors were quantified as well. Using the same criteria as Smith and Montgomerie (1991), start of begging, height of beak extension,

8 parent-nestling beak distance and parent-nestling body proximity all were measured when the nestlings first responded to parental arrival. Different nest angles and camera placements required ranking these latter four components of begging. Ranks were given with 2 being earlier, higher, or closer, and 1 being later, lower or more distant.

Since start rank and initial height rank were often correlated, we combined them into a single measure, start+height, by adding the ranks. Similarly, we additively combined body and beak proximity into a single measure of proximity. In addition, we noted as present or absent several other parameters possibly reflecting hunger or motivation, such as begging before the parent landed, begging within one second of parental arrival, full extension of the neck, and begging throughout the entire parental visit. Phainopepla nestlings occasionally did not swallow the food their parents placed in their mouths, perhaps because they continued begging too vigorously. Such failure to swallow was also tabulated.

Statistical analyses

Most analyses consisted of two-way ANOVAs executed on the general linear model (GLM) platform of JMP 3.2.1 statistical software. Factors included treatment

(two fixed levels: control and experimental session) and either nestling (two fixed levels: removed nestling and nestmate) or sex of the parent (two fixed levels: male and female) depending on the question. The appropriate treatment*nestling or treatment*sex interaction term was also included. We controlled for possible mean differences among nests by adding nest ID (nested within parent sex in models containing this main effect) as a fixed factor in the model. Variables were transformed

9 as necessary to achieve approximately normal frequency distributions for all parametric analyses. However, to illustrate the absolute values of dependent variables and the differences among treatment, parent sex, and nestling groups, tables and graphs show the mean values of the untransformed and uncorrected variables.

To maximize the power of our analyses, we made the assumption that each parental visit within a session was an independent event. We justify this procedure with two types of evidence. First, we looked for significant meaningful within-session variation and association between nestling and parental behaviors. We examined the partial correlation between each parental behavior and each of the four nestling behavior components (beg duration, beg intensity, start+height, and proximity) while controlling for session using GLM analyses. Every one of the parental behaviors was significantly correlated with at least one nestling behavior. For example, total feeds per visit, time per feed, feed duration, and time to the next visit were correlated with begging duration, and the number and percent of feeds to each nestling as well as the non-feed, non-brood time per visit were correlated with begging intensity (all P < 0.003, less than the Bonferroni-corrected P of 0.013 with four tests per variable). Figure 1 demonstrates visually how both parental and nestling behaviors change during the experimental session as the parents detect the hungry nestling and as the removed

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Figure 1. Means of some provisioning and begging variables for the control session (gray bar) and the first eight experimental session parental visits (white bars). A. Total number of regurgitations per visit. B. Number of feeds to the food-deprived nestling. C. Begging duration of the food-deprived nestling. N = 8 nests.

11 nestling presumably becomes satiated with time.

Second, we examined each parental and nestling variable for autocorrelation at a lag of 1 (again correcting for session in the GLM). Only one variable, nestling proximity to the parent, showed evidence of autocorrelation (P = 0.005); the remaining variables shows no evidence of autocorrelation (all P > 0.1) and thus were independent of values in the prior visit.

In preliminary analyses of the changes in provisioning and begging behaviors during the course of each experiment, we noticed that the rates of all non-ranked variables were high during the first part of the experimental period but dropped off part way through the period. This implied that the needs of the initially hungry nestling were satisfied part way into the experimental session. Since we were specifically interested in the magnitude of parental and nestling behaviors in the presence of a hungry nestling, we sought a quantitative method for deciding which of the later parental visits to exclude from the analyses. We chose the chronological clustering algorithm of Legendre et al. (1985), which is designed to identify discontinuities in a multivariate time series. Using three of the non-ranked parental and nestling variables, we first computed a matrix of Mahalanobis distances between each of the first eight visits of the experimental sessions (data from all 8 nests included). This distance matrix was then converted to a similarity matrix and submitted to the Chrono routine of the R

Package (Legendre et al. 1991), which clusters the visits with a temporal contiguity constraint. Each clustering step is subjected to a permutation test before the fusion of two visits (adjacent in time) is authorized. We obtained the same outcome using different variables, criterion levels, and number of iterations (see Results). Basic

12 statistics were run on Statview 5.0. Significant tests are those with P-values < 0.05, or the Bonferroni-corrected values where multiple tests are conducted. Nearly significant relationships are those with 0.05 < P < 0.08. The main text, graphs, and tables give means ± standard errors.

RESULTS

General patterns

Phainopepla parents visited nests at an average interval of 5.6 min (±0.43, range

0.1 to 23.5 min) and delivered an average of 4.6 food loads (± 0.30, range 1 to 17) to the two nestlings per visit. They spent a total of 71.5 sec at the nest during each visit

(±13.2, range 1 to 686 sec). An average of 12.7 sec of this time was spent feeding nestlings (±1.02, range 0-44 sec), and the duration of feeding was strongly correlated with the number of regurgitations (Pearson r = 0.881, n = 114, P < 0.0001). The remaining time was spent standing on the side of the nest, removing fecal sacs, and/or brooding.

Using data from control periods only (n = 48), we looked for any correlations of the begging factors and provisioning variables with nestling age and time of day that might confound the analyses, and also verified that none of these correlations was affected by parent sex. Younger nestlings were brooded more than older nestlings (age versus brood time, r = –0.627, P < 0.0001). Time per feeding decreased with age (r =

–0.305, P = 0.035) but no other provisioning rate or nestling begging behavior variables were significantly correlated with age. Time of day (from 0730 to 1000) was significantly positively correlated with non-feed-non-brood time (r = 0.448, P = 0.001), time per feeding (r = 0.285, P = 0.049) and begging duration (r = 0.334, n = 96, P =

0.001). Parent sex was not associated with age or time (n = 8, P >0.4). Although none of these relationships represent important confounding effects, we nevertheless controlled for all time and age trends, along with any other nest differences, by

13 14 including nest ID in the statistical models.

At the nest with 5-day-old nestlings, both parents attended the nest, although the female made nearly twice as many visits as the male. At the nests with older nestlings, however, only one parent attended the nest for the entire observation period (control and experimental sessions); the female was the provisioning parent at four of these nests while the male provisioned at three nests. The biparental nest was categorized as a female-attended nest for all nest- and session-based analyses involving parent sex.

Since the adults were not banded, we were not able to determine the whereabouts of the missing parent. Walsberg (1977) noted that male phainopeplas sometimes defend two territories, and both males and females sometimes abandon their mates and either move to another territory or leave the area altogether, presumably migrating to the northern breeding area in coastal woodland habitat.

Preferential provisioning of the hungry nestling

Phainopepla parents increased their feeding rate in response to the presence of the hungry nestling, but the effect waned after the first four visits. Figure 1 shows the mean values of several parental and nestling behaviors for the control session and each of the first eight experimental session visits. The elevated response levels during the first four visits for these and all other behaviors clearly returned to control levels by the fifth and subsequent visits, suggesting that the hungry nestling's needs were satisfied at this point. We statistically verified this discontinuity in behaviors between visits 4 and

5 using the chronological clustering algorithm described in the methods section.

Therefore, the following analyses on provisioning rates and nestling behaviors involve

15 comparisons between the entire control session visits and only the first four experimental visits. Parents increased their feeding rate to the hungry nestling while maintaining the same feeding rate to the nestmate (Figure 2a). This increase was achieved by the combined effects of increases in visit rate, the number of feeds per visit

(in the second through fourth visits), and the proportion of feedings given to the hungry nestling. Moreover, the hungry nestling received 72% of the nutrient-rich first feeds, compared to 50% of first feeds received during the control period. As a result, the hungry nestling, which lost an average of 1.69 g during the removal period, gained an average of 1.41 g during the experimental period (Figure 2b). Finally, the feeding response of the parent was sensitive to the level of nestling need; the percentage of feedings allocated to the hungry nestling during the first four experimental visits was significantly correlated with the weight loss of the hungry nestling during the removal period (Spearman rank correlation, rs = 0.881, n = 8, P = 0.014; Figure 3).

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Figure 2. Comparison of feeding rates and weight gain between the control and experimental sessions for the deprived nestling (black circles) and the non-deprived nestmate (white circles). Means ± SE are shown. See text for statistical analysis results.

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Figure 3. Proportion of regurgitations allocated to the removed nestling during the first four experimental visits is greater for nestlings that lost more weight during the removal period. Male-tended nests are indicated with squares, female nests with circles, and bisexual nests with a star.

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Male and female provisioning responses

Although both male and female parents preferentially allocated feedings to the hungry nestling, males increased their overall feeding rate to the nest more than females did (Table 1). Males increased both their visit rate and their feeds per visit during the experimental session, whereas females increased only feeds per visit. Females not only brooded the young more often than males, but also spent more non-feeding and non- brooding time (i.e., “other” time) at the nest (Table 1). Females reduced their pre- and post-feeding time at the nest during the experimental session relative to the control session to meet the increased nestling demand. While feeding nestlings, females took significantly more time than males to accomplish each regurgitation. The net result of these sex-based differences was that males were more effective in meeting the deprived nestling's needs. Removed nestlings in male-tended nests gained more weight during the experimental session than the removed nestlings in female-tended nests (2.08 versus

1.00 g, respectively, t = 2.54, n = 8, P = 0.044).

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5

S * T F=3.22 F=4.07 F=0.39 F=0.35 F=0.95 F=0.37 P=0.098 P=0.067 P=0.53 P=0.559 P=0.334 P=0.544

ANOVA F=3.61 F=1.33 F=4.52 F=4.60 F=0.27 F=3.32 P=0.082 P=0.271 P=0.036 P=0.870 P=0.073 P=0.037 Treatment

Sex F=5.12 F=4.45 F=0.09 F=0.10 F=6.08 P=0.057 P=0.761 P=0.756 F=10.01 P=0.043 P=0.016 P=0.002

Exp. 65.1 ± 7.5 65.1 ± 37.7 ± 5.4 37.7 ± 6.9 58.9 ± 2.8 11.6 ± 3.6 20.3 ± 96.8 ± 36.9 96.8 ± 0.87 6.83 ± 0.21 2.16 ± 7.10 ± 1.59 7.10 ± 0.68 5.70 ± 0.71 3.39 ± 15.03 ± 3.83 15.03 ±

parental sex interaction effect (T * S). Significant results are are results effect* S). (T Significant sex interaction parental

Treatment 0.20 Control 9.8 ± 1.6 9.8 ± 43.3 ± 4.6 43.3 ± 5.8 36.2 ± 7.8 46.2 ± 4.3 49.3 ± 8.93 ± 0.90 8.93 ± 2.39 8.76 ± 0.91 4.99 ± 0.53 4.51 ± 1.90 ± 0.33 3.24 ± 12.7 41.5 ±

n (3, 3) (3, 3) (5, 5) (5, 5) (C,E) (15, 12) (15, 12) (15, 12) (15, 12) (33, 20) (33, 20) (33, 20) (33, 20) based analyses, nest ID nested within sex was also included as a factor (results not not (results factor as a sex wasincluded also within ID nest nested analyses, based -

Male Male Male Male Male Male Parent Female Female Female Female Female Female

Provisioning Variable Feeds/hr Visits/hr Feeds/visit fed to % removed per Time (sec) Feeding “Other” (sec) time

Table 1. Parental provisioning rates (means ± SE) in the control and experimental sessions,of results and ANOVA showing experimental and control the SE) in ± (means rates provisioning 1. Parental Table * treatment effects the and sex main parental and treatment font. visit bold For in the highlighted shown).

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Parental responses to nestling behaviors

To determine which nestling behaviors parents used to preferentially allocate food to a hungry nestling, we ran separate analyses for males and females. The two key parental food allocation variables, % feeds to the removed nestling and number of first feeds to the removed nestling, served as dependent variables. Independent variables include start+height, proximity, and the differences between the two nestling’s beg duration and beg intensity (i.e., relative beg duration and relative beg intensity). We initially included nest ID as a factor in the model, but the presence of this variable did not affect the results so we removed it and performed a standard multiple regression.

This procedure allows us to report the beta coefficients for each variable, which provides an indication of the direction and relative magnitude of the partial correlation between each independent variable and the dependent variable. The results are summarized in Table 2. Males and females attended to somewhat different nestling behaviors to allocate feedings. Both sexes allocated more feedings to the nestling with the higher begging intensity. Begging intensity was the only nestling behavior used by females to allocate food. Males, on the other hand, also used beg duration to allocate feeds, and they showed a very strong preference for feeding the nestling with the higher start-height score first. Neither males nor females appeared to use proximity as a cue for allocating feeds.

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Table 2. Multiple linear regression analyses to determine the role of the four nestling begging behaviors (independent variables, first column) on parental allocation of feeds (% feeds and fed first, dependent variables) to the removed nestling. All control and experimental visits were included in the analyses. Relative beg duration is the difference in beg duration between the removed and nestmate nestlings during a visit, and relative beg intensity is the analogous difference between beg intensities. Males (n = 56) and females (n = 62) analyzed separately. Significant relationships are highlighted in bold font.

% feeds to removed Fed first nestling MALES beta t P beta t P

Relative beg duration +0.296 2.288 0.026 +0.197 1.532 0.132

Relative beg intensity +0.293 2.291 0.026 +0.033 0.260 0.796

Start+height rank +0.171 1.205 0.234 +0.411 2.916 0.005

Proximity rank –0.068 0.509 0.613 –0.091 0.682 0.498

Whole model (R2, F, P) 0.217 3.533 0.013 0.225 3.708 0.010

FEMALES

Relative beg duration +0.092 0.663 0.510 +0.066 0.470 0.640

Relative beg intensity +0.296 2.071 0.043 +0.060 0.418 0.678

Start+height rank –0.017 0.123 0.903 +0.237 1.669 0.101

Proximity rank –0.008 0.060 0.953 +0.089 0.642 0.523

Whole model (R2, F, P) 0.115 1.852 0.132 0.112 1.801 0.141

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Changes in nestling behavior associated with food deprivation

To determine which behaviors nestlings varied when hungry to signal increased need to parents, we first ran two-way ANOVAs on the pooled male and female nests with each of the four nestling behavior variables (beg duration, average beg intensity, start+height, and proximity) as the dependent variable. Factors in the model included treatment, nestling, nestling*treatment interaction, and nest ID. Analyses used all control session visits and the first four experimental session visits (see methods section). A significant change in behavior by the removed nestling during the experimental session is expected to generate a significant interaction term. To our surprise, no interaction term was significant for any of the variables (all P > 0.1).

However, we did find highly significant nest differences for both beg duration and beg intensity (no such nest differences are possible for the two ranked variables). This finding implied that some other confounding factor was strongly affecting begging behaviors differentially in each nest; parent sex was an obvious possibility.

We therefore conducted the same analyses as before, but separately for male and female nests. A two-way ANOVA was also run on each behavior using removed nestlings only, with sex, treatment, sex*treatment interaction, and nest ID factors, to evaluate the difference between male and female responses. Figure 4 summarizes the significant effects in all of these analyses. Nestlings in male and female nests used different behaviors to signal their hunger. Hungry nestlings in female nests increased their beg intensity slightly, and although the interaction term was not significant, there was a significant difference between the begging intensity of removed and nestmate

23

Figure 4. Changes in begging behaviors between the control and experimental sessions (first four visits) for the deprived nestling (black) and its nestmate (gray) in male-tended and female-tended nests. P-values for the significant factors in two-way ANOVAs are shown. Horizontal bars indicate treatment differences, vertical bars indicate nestling differences, crossed dashed lines show significant nestling *treatment interactions, and double-headed arrows indicate sex differences. A. beg duration, B. average beg intensity, C. start+height, and D. proximity to the parent.

24

nestlings using only experimental visits (paired t-test, t = 2.55, df = 31, P = 0.016).

Nestlings in female nests begged with higher intensity under all conditions than did nestlings in male nests. By contrast, hungry nestlings in male nests increased their begging start+height.

In both male and female nests there was a significant main effect of treatment on beg duration, with both the hungry nestling and the nestmate begging longer in the experimental period. This result raises the possibility that the satiated nestmate escalated its own begging behavior in response to the presence of its strongly begging hungry nestmate. On the other hand, beg duration was very strongly correlated with the duration of the parental visit (brood time excluded, r = 0.675, P < 0.0001), so beg duration could be affected by the presence of the parent rather than the begging of the other nestling. Nestlings tended to beg at some level as long as a parent was standing at the side of the nest. The significantly longer beg duration in female compared to male nests is almost certainly due to the longer visit duration of female parents. We evaluated the correlation between nestmate beg duration and removed nestling beg duration, controlling for parental visit duration (excluding incubation time) as well as nest and treatment effects. Both parental visit duration (F = 22.27, n = 114, P < 0.0001) and removed nestling beg duration (F = 220.3, P < 0.0001) had highly significant independent effects on nestmate beg duration. Thus nestlings do modify each other’s begging duration. We looked for equivalent effects of the beg intensity of the removed nestling on the beg intensity of the nestmate, controlling for nest and treatment, and found a strong but non-significant positive trend (F = 3.09, P = 0.082).

25

Finally, proximity to the parent showed a curious interaction between nestling and parent sex. Removed nestlings were closer to the parent in male nests and farther from the parent in female nests, but this pattern was identical in the control sessions as well. It would not have been possible for the parent to know which nestling we would remove, and respond differentially to it during the control period. Recall that this variable exhibited significant autocorrelation within sessions. Parents tended to arrive on the same side of the nest for several successive visits, then arrive from a different side, presumably based on where they had been foraging between visits. Phainopepla nestlings lean toward the parent when begging, but they do not jostle for positions close to the parent. Parents also do not show any tendency to preferentially feed chicks that are closer to or farther away from them (see analysis in prior section). We believe this result is an unfortunate bias in the position of the removed nestling in the three male nests relative to the preferred arrival location of the parent.

Table 3 shows a summary of the key behaviors used by nestlings and parents, broken down by individual nest. The third column gives the most significant, or strongest, behavior used by the removed nestling in the experimental session compared to the control session, extracted from the analyses of Figure 4. If a second behavior was also significant and positively associated with experimental session, it is also indicated.

The fourth and fifth columns show the strongest correlates of two parental allocation variables, % fed to the removed nestling and removed nestling fed first. For % fed removed, nestlings and parents employed the same first or second most important behaviors in 8 out of 9 cases (sign test, P = 0.039). The equivalent analysis for removed fed first was not as strong (7 out of 9, P = 0.180) because females were less

26

Table 3. A summary of the most significant behavior(s) used by the removed nestlings in the experimental versus control sessions in each nest, and of the most significant behavior(s) used by the parent to allocate food to the removed nestling. If nestlings or parents used two different behaviors, both behaviors are shown in order of importance. Results are shown for the two measures of parental response, % fed removed and removed nestling fed first. Nests are grouped by parental sex. Nest D was attended by both the male and female parent, and parental allocation correlations are shown separately for each one. Dur = beg duration, Int = beg intensity, StHt = Start+height, Prox = proximity to parent.

Parental behavior(s)

Nestling Nest Parent % fed removed Removed fed first behavior(s)

C Male StHt, Int Dur, StHt Prox, StHt

G Male Int, StHt Int StHt

H Male Dur Dur Dur

D Male StHt, Dur Dur Dur, StHt

D Female StHt, Dur Int, Dur StHt

A Female Int, Dur Int Int

B Female Int Int Dur

E Female Int, Dur Int, Dur Dur

F Female StHt Prox Prox

27

likely to feed the quickest nestling first. One nest (F), the outlier in Figure 3, showed no strong nestling or parental behaviors; this nestling lost very little weight during removal and was not preferentially fed by the (female) parent. In conclusion, male and female parents used different begging behaviors as cues for allocating food to nestlings, and hungry nestlings in male and female nests emphasized those begging components to which the parent was most responsive, i.e. start+height in male nests and begging intensity in female nests.

DISCUSSION

Phainopeplas possess an honest system of signaling nestling need to parents, probably facilitated by a small clutch size, a synchronous hatching strategy that equalizes nestmate competitive ability, and a multiple-load regurgitation style of nestling provisioning. In these field-based food-deprivation experiments, parents quickly detected the hungry nestling when it was returned to the nest and preferentially fed it during the first four parental visits. Preferential food allocation to the deprived nestling increased with the degree of food deprivation. Removed nestlings regained almost all of the weight they had lost during the removal period by the end of the experimental session. These results are very similar to those found for pigeons

(Columba livia), which also possess a 2-egg clutch, synchronous hatching, and regurgitation feeding style (Mondloch 1995).

We discovered that male and female parents responded in slightly different ways to the presence of a hungry nestling. Males nearly doubled their visit rate, whereas females did not increase visit rate relative to the control period. Both sexes increased the number of regurgitations per visit and the proportion of feeds to the hungry nestling to a similar degree. However, they used different cues from the nestlings to allocate feeds. Males responded primarily to begging start order+height, whereas females responded to begging intensity. Because of the unusual habit of one or the other parent deserting its mate in this species, older nestlings are often fed exclusively by either the male or female parent. The most striking finding was that nestlings emphasized different components of begging behavior depending on the tending parent’s sex, and when hungry increased that component of begging to which the parent was most likely

28 29 to respond. This result implies that nestlings learn and adjust their begging behavior according to their past experience of those signal components that elicit rewards.

Remarkably, the signaling system remains honest despite the clear role of learning.

An alternative hypothesis for the similar overall ability of both male and female parents to selectively provision the hungry nestling, despite the apparently different nestling cues, is that parents used another signal component that we did not measure to assess true nestling need. Mouth color flush, for example, is known to vary with hunger level in some other regurgitation feeders and is used as a cue to allocate feedings in canaries (Kilner 1997, Kilner and Davies 1998). The color flush could be a physiologically constrained index signal of recent feeding activity (A. Lotem, pers. comm.). However, gape color appears to be a useful and honest indicator of need only in very young chicks and is unlikely to have played a role in this study involving older chicks (Kilner, pers. comm.). Nevertheless, parents could be using other unmeasured cues.

Several studies have uncovered differential provisioning rules for male and female parents. In species with asynchronous hatching, males and females often show different preferences for large and small nestlings (e.g., budgerigars (Melopsittacus undulatus, Stamps et al. 1985), crimson rosellas (Platycercus elegans, Krebs et al.

1999), great tits (Parus major, Bengtsson and Ryden 1981), tree swallows (Tachycineta bicolor, Leonard and Horn 1996), and pied flycatchers (Ficedula hypoleuca, Gottlander

1987), but see Smiseth et al. (1998) for an exception in the bluethroat (Luscinia svecica)). In most studies that manipulated nestling hunger or begging stimulus levels, both sexes tended to increase their provisioning rate to a similar degree (e.g., pied

30 flycatchers (Gottlander 1987), red-winged blackbirds (Agelaius phoeniceus,

Whittingham and Robertson 1993, Burford et al. 1998), yellow-headed blackbirds

(Xanthocephalus xanthocephalus, Price 1998), canaries (Serinus canarius, Kilner 1995) and starlings (Sturnus vulgaris, Kacelnik et al. 1995). However, a few studies have carefully examined the begging signal components used by male and female parents to allocate food among nestlings varying in hunger levels (Budden and Wright 2000).

Detailed studies of two psittacine species have shown that males pay attention to begging intensity signals indicating short-term nestling need while females generally ignore begging signals and preferentially provision smaller nestlings (Stamps et al.

1985, 1987, 1989; Krebs and Magrath 1999). A recent study on canaries showed that males allocated food based primarily on nestling height while females allocated food based on both height and hunger-based differences in begging display intensity (Kilner

2002), results quite similar to those described here in the phainopepla.

What drives these differences in male and female provisioning rules? The studies mentioned above found that males allocate feedings according to quickly- assessable nestling cues such as proximity, height, and begging rate, whereas females take more time while feeding and provision according to more difficult-to-assess cues

(Budden and Wright 2000). Our results are consistent with this pattern, and we suggest a proximate explanation. Male phainopeplas possess reserve energy for functions such as territory defense, and respond to an increase in nestling need with a larger increase in expensive parental investment than females do, i.e., by increasing their visit rate. Their use of the more quickly assessable nestling cues, begging start rank and initial beak height, may be a consequence of the time constraints males are under to fit rapid

31 feedings within other duties such as territory defense. Females, who have produced a clutch of eggs and performed most of the incubation, may be operating at their upper physiological limit during the control periods and are unable to increase visit rate further during brief periods of increased nestling need. Females also spend more time standing at the nest and brooding, enabling them to assess more subtle nestling cues such as begging intensity. Despite their more careful attention to details, the female strategy was less effective in meeting the hungry nestling's needs than the more energetically costly male strategy.

There is growing evidence that nestling birds use conditioned learning to adjust their begging strategies when soliciting food from their parents. Stamps et al. (1989) first proposed learning as an explanation for the higher begging intensity of female nestlings in the budgerigar. Male parents in this species preferentially feed female offspring and use begging intensity as a cue for allocating food, whereas female parents ignore begging and preferentially feed small nestlings. Conditioned learning was suggested as an explanation for the higher begging rates of smaller nestlings in barn swallows (Hirundo rustica, Lotem 1998a,b) and starlings (Cotton et al. 1999). Either small nestlings learn that they must beg at higher rates than their larger nestmates in order to be noticed and fed at all, or large nestlings learn that reduced begging suffices to elicit food rewards. Learned responses were clearly responsible for nest-positioning strategies in nestling great tits (Kölliker et al. 1998). In this species, male and female parents consistently approach the nest from different locations and tend to feed the closest nestling. Females provision at higher rates than males, so hungrier nestlings position themselves on the female-arrival side of the nest. Recently, experimental

32 evidence for learning of nestling begging behaviors has been demonstrated in house sparrows (Passer domesticus) by Kedar et al. (2000). They found that hand-fed nestlings rewarded for high or low begging intensities quickly shifted their average begging level in the expected direction. Our study not only provides more evidence for learning by nestlings, but also extends the role of learning to the development of alternative begging signal components. Demonstration of this effect was only made possible by the unusual uni-parental social system of the phainopepla, which provided consistently different reward environments in male-and female-tended nests.

Learning by nestlings did not disrupt the correlation between need and resources obtained, and in fact learning by both parent and offspring may have fine-tuned the accuracy of the signaling system and provisioning rules. In asynchronously hatching species such as starlings, on the other hand, learning by nestlings generated the positive correlation between (size-based) need and begging intensity, but parents did not preferentially feed more vigorously begging nestlings. Parental strategies clearly differ among species. Learning may be a ubiquitous mechanism by which nestlings adjust their begging and other behaviors to those that provide rewards, but may only lead to an honest signaling system when the conditions for an ESS are met. Learning has been shown to be an effective mechanism for reaching the ESS (Harley 1981). Phainopeplas may meet enough of the ESS conditions to fit the Godfray (1995) model (e.g., only two young differing in cryptic need, parents strive to raise both of them), whereas asynchronous species do not meet the model's assumptions (e.g., facultative brood reduction, allocation of food based on non-cryptic nestling attributes).

Another view, not incompatible with the one above, is that the level of honesty

33 in a signaling system depends on the initial accuracy of the sender's encoding rule

(association between context and signal given) and on the net payoffs to sender and receiver of alternative receiver decisions (Bradbury and Vehrencamp 2000). When sender and receiver have conflicting interests (i.e., disagree about the optimal receiver response in some contexts) the sender's encoding rule will end up being less accurate than when they have concordant interests. Asynchronous hatching not only generates competitive strategies and counterstrategies among nestmates, which reduce the initial accuracy of sender encoding, but also results in conflicts of interest between parents and some of the young when food supplies are low. A partially accurate signaling system, or no signaling, is likely to result. The facultative nature of brood reduction and the observed changes in parental allocation rules with changes in food availability (Smiseth et al. 1998, Krebs and Magrath 1999, Cotton et al. 1999) could also explain the partial accuracy of some parent-nestling signaling systems.

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