ORNITOLOGIA NEOTROPICAL 23: 529–544, 2012 © The Neotropical Ornithological Society

MORPHOLOGICAL AND FORAGING BEHAVIORAL DIFFERENCES BETWEEN SEXES OF THE MAGELLANIC ( MAGELLANICUS)

Laura Chazarreta1, Valeria Ojeda1, & Martjan Lammertink2,3

1Departamentos de Ecología y de Zoología, Universidad Nacional del Comahue-INIBIOMA, Quintral 1250, (8400) Bariloche, Argentina. E-mail: [email protected] 2CICyTTP-CONICET, Matteri y España s/n, (3105) Diamante, Entre Ríos, Argentina. 3Cornell Lab of Ornithology, 159 Sapsucker Woods Road, Ithaca, NY 14850, USA.

Resumen. – Diferencias morfológicas y de comportamiento alimentario entre sexos del Carpintero Gigante (Campephilus magellanicus). – La divergencia ecológica producto de diferencias morfológicas y comportamentales junto con la dominancia social, promueve la separación de nichos entre sexos en aves. La ausencia de competidores favorecería estas diferencias intersexuales. El Carpintero Gigante (Campephilus magellanicus) es el único pícido de gran tamaño en los bosques de de la , sin competidores. Una investigación preliminar documentó diferencias mor- fológicas entre sexos y postuló la existencia de diferencias en el comportamiento alimentario, correla- cionadas con ese dimorfismo. Nuestros objetivos fueron analizar las diferencias morfológicas e investigar si existen diferencias intersexuales en el comportamiento alimentario. Obtuvimos datos mor- fológicos de colecciones de museos y registros comportamentales de poblaciones de Patagonia Argen- tina. Estimamos amplitud y solapamiento de nichos en variables de alimentación. Los machos fueron más grandes y tu-vieron picos 12,4% más largos que las hembras. Ambos sexos se alimentaron princi- palmente sobre árboles vivos, pero los machos usaron sustratos más grandes (troncos) que las hem- bras y alturas intermedias (5–10 m), mientras que las hembras usaron sustratos más pequeños (ramas) dentro de la copa, a mayor altura (> 15 m). La tasa de captura de presas fue similar entre sexos (0,28 presas/min), pero los machos capturaron presas más grandes (larvas xilófagas) que las hembras (pre- sas superficiales). Registramos dominancia social de los machos. Según el análisis de amplitud de nicho, las hembras fueron más generalistas que los machos en el uso de microhábitats y en la posición del cuerpo mientras se alimentaban. El dimorfismo sexual en tamaño corporal y largo del pico fue acorde a la especialización por sustratos en los sexos, lo cual fue probablemente reforzado por la dominancia de los machos. La falta de competencia interespecífica en este bioma contribuiría a la diferenciación observada entre los sexos.

Abstract. – Ecological differentiation arising from morphological and behavioral differences, together with social dominance, is known to promote niche differentiation between sexes in . The absence of competing would favor intersexual differences. The (Campephilus magellanicus) is the only large woodpecker in the southern beech Nothofagus forests of Patagonia, with no competitors. Sexual divergence in morphology had been documented by preliminary research, and differences in foraging behavior were proposed as a correlate. Our aims are to analyze intersexual diver- gence in morphology and to investigate whether the behavioral differences exist. We obtained morpho- logical data from ornithological collections and foraging records from populations from Argentine Patagonia. We estimated foraging niche breadth and the overlap of foraging variables. Adult males were larger and had bills 12.4% longer than those of females. Both sexes foraged mostly on living trees, but males foraged on larger substrates (trunks) at intermediate heights (5–10 m), while females foraged

529 CHAZARRETA ET AL. higher within the crown (> 15 m) on smaller substrates (branches). The rate of captured prey was similar between sexes (0.28 prey/min), but males consumed larger prey (wood-boring larvae) than females (near-surface prey). Social dominance by males was recorded. Based on analysis of niche breadth, females were more generalist than males in microhabitat use and body posture when foraging. Sexual dimorphism in body and bill size seems to be in line with specialization in the use of different substrates between the sexes, which is probably reinforced by male dominance. Lack of interspecific competition in this biome probably contributed to the differentiation observed between sexes. Accepted 23 December 2012.

Key words: Magellanic Woodpecker, Campephilus magellanicus, Austral Temperate Forest, insular biome, niche breadth, sexual dimorphism.

INTRODUCTION (Picidae) are often sexually dimorphic in and morphology, and Sexual dimorphism in size and morphology thus, are an interesting group for studying dif- is widespread among (Hedrick & ferences in foraging behaviors between male Témeles 1989) and has traditionally been and female (Catry et al. 2005). In particular, related to sexual selection, especially in sexual differences in bill size have been species with a polygamous mating system related to differences in feeding behavior, (Amadon 1959, Selander 1972). Nevertheless, explored , and consumed items the evolutionary origin of sexual dimorphism (Selander 1966, Aulén & Lundberg 1991). has multiple pathways (Hedrick & Témeles The southern beech (Nothofagus) temperate 1989), and there are many cases where differ- forests covering southern and Argen- ent size and morphology between males and tina (35°S–56°S), comprise a narrow strip ca. females can be related to ecological causes 2000 km long and up to 120 km wide that (Slatkin 1984, Shine 1989), as in Green Wood- evolved in isolation from other South Ameri- hoopoes (Phoeniculus purpureus, Radford & can forests, constituting a island with Plessis 2003), Darwin’s finches (Grant 1986), high levels of endemism (Vuilleumier 1985, and (Daphoenositta chrysoptera) Armesto et al. 1996). In the interior of Nothof- and (Climacteridae) (Noske agus forests, only two woodpecker species 1986). occur, the small (Venilior- Segregation between sexes in morphologi- nis lignarius, ~ 16 cm, 35–38 g) and the very cal traits is thought to alleviate intersexual large Magellanic Woodpecker (Campephilus competition (Selander 1966, Ruckstuhl & magellanicus, ~ 40 cm, 276–363 g) (Short Clutton-Brock 2005). The absence of com- 1982). In this particular setting, the Magel- peting species would favor a larger niche lanic Woodpecker has no potential ecological width of a species, leading to greater struc- competitor and therefore would show a broad tural dimorphism and the subdivision woodpecker niche (Short 1970a). Pioneering between sexes of the foraging niche (Selander research conducted by Short (1970a) revealed 1966, Shine 1989). Social dominance, where a noticeable sexual dimorphism in bill size the dominant sex (usually male) excludes the (males larger than females), which he pro- subordinate from favored patches or sub- posed would correlate to differences in feed- strates, explains sexual niche segregation in ing behavior and explored habitat, but this several cases (Hogstad 1978, Morse 1980, remained untested. Our aims are to analyze Peters & Grubb 1983, Matthysen et al. 1991, sexual dimorphism in morphology of Magel- Osiejuk 1994, Ruckstuhl 2007). lanic Woodpeckers and to explore sex-specific

530 DIFFERENTIATION BETWEEN SEXES OF MAGELLANIC WOODPECKERS foraging behavior and feeding habitats of this ing Baldwin et al. (1931) guidelines. We only species. used adult specimens as determined from plumage patterns (Ojeda 2004), museum METHODS labels, and size (Short 1970a). We collected the following variables from each skin: wing Study area. Study sites (n = 8) were located and tail length, culmen cord (bill length), and within the Lanín (39°35’–41°19’S) and tarsus, toe (third), and claw (third) length. Nahuel Huapi National Parks (71°17’– Some skins were damaged so we were unable 71°36’W), north and south of Bariloche city, to collect all measurements from those speci- in northern Argentine Patagonia. The climate mens (n = 7). We took most measurements to in the region is characterized by a relatively the nearest 0.01 mm when using calipers, and long winter with rain and snow and by dry to the nearest 1 mm using a ruler for wings summers, with mean monthly winter (June– and tail. August) temperatures of 2°–3°C, and summer Nearly all specimen measurements (98%) (December–March) temperatures of 12°– were taken by one of us (LC) and the remain- 14°C (data from Bariloche Airport, 41°09’S, der was taken by museum curators instructed 71°10’W). by LC. Although skin dimensions vary with Subalpine forests between 1100–1700 m specimen age, preparation technique, and a.s.l. are composed of pure stands of the storage conditions (Bortolotti 1984), we con- deciduous lenga . Our field sidered this variation a random effect in our sites were old-growth lenga stands over 1000 data set. ha each, which were contiguous with other Nothofagus stands. Lenga forest was selected Foraging behavior. We conducted fieldwork dur- because of the great extent of this forest type ing three consecutive years from early spring in the study area and its mostly open under- to late summer (September–April, 2008– story that allows following woodpeckers for 2010). Most behavioral data (85% of observa- monitoring their behavior. tion hours) were obtained from a population of eight pairs and family groups (Challhuaco Species. Magellanic Woodpeckers show a site, 15 km southeast of Bariloche) banded noticeable sexual plumage dimorphism, which during a long-term study of the species facilitates field studies involving sex recogni- (Ojeda 2004, Chazarreta et al. 2011). Thus, tion. They reproduce in monogamous pairs foraging data were mostly based on color- and live in stable family groups consisting of ringed males and females of known age and 2–5 individuals, with offspring delaying dis- reproductive status. Additionally, we collected persal for up to four years (Chazarreta et al. similar data on adult (according to both plum- 2011). Family groups move in relatively lim- age and behavior) unringed birds located at ited areas of forest (ca. 100 ha) all year round, other lenga forest sites. At these sites, when- and members of a group keep in close prox- ever two or more unringed adult birds of the imity (Ojeda 2004). same sex were encountered, they were studied only if they were separated by more than 3 Morphology. We measured morphology from km, representing different territorial birds. specimens held in 19 ornithological collec- We studied foraging behavior by following tions (see Acknowledgments) in order to focal individuals under continued sampling of explore differences between sexes. Fifty-nine variable periods (Martin & Bateson 2008). We males and 64 females were measured follow- conducted observations during all daytime

531 CHAZARRETA ET AL. hours (approximately from 08:00–20:00 h, ing the substrate with lateral head movements = GMT-0300) and only when birds were in order to find prey. Surface (pick- actively foraging. To minimize the effect of ing prey off the surface) was not considered weather, we did not work under conditions of as a tactic itself because it was rarely heavy rain, snow or hard wind. observed. Most near-surface prey occurred A territory was searched systematically under the first layer of bark. Scanning tends until we encountered a woodpecker family. to be a dynamic technique: the birds climb on We then followed in turns, one of its mem- a stem or branch after and before using bers randomly selected, for as long as it another foraging technique, usually upward, remained in sight, and recorded a continuous and alternate soft pecking, listening and account of its movements, foraging tech- movement hops. During a sequence, we also niques, and other behaviors by dictating them recorded behaviors beyond specific foraging into a tape recorder, writing field notes, and and searching techniques, which were catego- using a stopwatch to record time. Distances rized as: 5) food handling: when the focal bird between members of a pair were taken into handled prey for itself or its offspring; 6) account and visually estimated. Behavior dur- movement: when changing location within ing the first 30 s after detection was excluded substrate or among substrates; and 7) other (Morrison 1984). In the banded population, behaviors, which were recorded as detailed as the same individual was not observed more possible (preening, resting, vocalizing, etc.). than once a day to increase sample indepen- Body position while foraging was also dence. To obtain detailed observations we recorded, distinguishing between semi-hori- used 10 x 40 binoculars. Usually, we could zontal with head up, semi-horizontal with approach woodpeckers closely (~ 10 m) with- head down, and vertical with head up. Type of out apparent disturbance. Most observations captured prey were assigned to broad catego- were of adult individuals that occurred in ries: wood-boring larvae; near-surface prey family groups or pairs, but six observations (mainly arachnids, adult or pupae), and were of solitary males. We never met solitary indeterminate, when we were unable to rec- females during the study. ognize a prey (usually because of their small For each adult bird we recorded: sex, for- size). We also recorded all agonistic interac- aging and searching technique, and microhab- tions involving focal birds: interferences (a itat (portions of the trees) using variables dominant bird flies towards a subordinate and similar to those considered in other studies of makes it fly to another location), and chases foraging behavior of woodpeckers (Selander on trunks or in flight. 1966, Jackson 1970, Kilham 1972, Askins 1983, Pasinelli & Hegelbach 1997, Stenberg & Foraging substrates. We defined “snag” as a Hogstad 2004, Newell et al. 2009). We defined standing dead tree with or without branches, searching/foraging techniques as: 1) excavat- “stump” as a dead tree < 3 m high, and ing: subcambial excavation, digging deep (> 2 “coarse woody debris” as downed wood. For- cm) holes; 2) debarking: striking the bill aging substrate diameters were estimated rela- against the substrate to remove some of the tive to the focal bird’s back width (folded exterior (bark, wood, lichens), or digging wings), which is around 75 mm in Magellanic superficially; 3) probing: inserting the bill or Woodpeckers. We estimated foraging heights tongue into cracks or crevices, or into excava- in two ways: 1) relative to the tree height, in tions created by excavating, or picking insects three categories (lower, mid, and higher third off the bark surface; and 4) scanning: explor- of the tree), and 2) absolute foraging height

532 DIFFERENTIATION BETWEEN SEXES OF MAGELLANIC WOODPECKERS above ground, in four classes (0–5 m, 5.1–10 added up the total minutes of the observation m, 10.1–15 m, > 15 m). The absolute height sessions (for each individual), and then esti- was estimated using an electronic clinometer. mated a single overall proportion of the vari- Additional features recorded at foraging loca- ous foraging variables. tion were: bark/ no bark, branch joint or To assess whether one of the sexes was trunk fork, and woodpecker-excavated pits more efficient than the other in capturing (foraging holes). prey, we compared the success rates for each individual as the number of captured prey per Data analyses. With the morphological vari- minute and per number of used substrates, ables recorded for skins, we explored differ- using the unpaired Wilcoxon signed rank test ences between sexes using generalized for independent data. linear models (GLM) with logistic link We analyzed differences in foraging function and binomial error structure (Craw- behavior between sexes by conducting a Prin- ley 2007). We checked for multi-colinearity, cipal Component Analysis (PCA) to collapse a transformed the variables as needed, and set of variables into a reduced number of new ran models with all variables. We fitted axes. All components with eigenvalues > 1 several models using different combinations were retained for subsequent analyses. To bet- of the variables as predictors, including their ter understand the foraging behavior relation- interactions. Fitted models were compared ships between sexes, we calculated niche and hierarchically ordered using the Akaikes overlap and breadth values. Foraging niche Information Criterion (AIC) (Akaike 1973, breadth was calculated for each individual Richards 2005), choosing the model with with a standardized version of Levins’ index the lowest AIC value. Models were simplified (Hulbert 1978): by removing non-significant interaction 2 terms first and then, non-significant predic- (1/ pi ) − 1 B = ∑ tors to generate the minimal adequate model (n −1) (Crawley 2007). The proportion of time spent by individu- For each variable, niche breadth (B) was als at each variable state was used in the analy- calculated separately. The proportion of for- ses. We arcsine √χ-transformed data to meet aging time an individual spends foraging at normality for the analyses. To circumvent a resource state i is pi, and n is the total number unit-sum constraint, variables with two or of resource states for the variable under con- more states were reduced by excluding at least sideration. Values range from one (for equal one state (the one that had the lowest values use of all resource states) to zero, for special- in most individuals) (Aebischer et al. 1993). ization on one resource state. To evaluate if For these analyses we only included states one of the sexes was more stereotyped than strictly referring to foraging techniques (prob- the other, we performed comparisons ing, excavating, debarking, and scanning). We between sexes for foraging diversity, using the assumed no effect of the year and/or month unpaired Wilcoxon signed rank test for inde- on the foraging behavior and pooled data for pendent data. The degree of niche overlap analyses. To reduce bias that multiple records was determined using Schoener’s index may create (Morrison 1984) each individual (Schoener 1968): was treated as a sample unit when determin- ing proportions and sample sizes for statistical 1 C = 1 − | p − p | tests (Airola & Barrett 1985). Therefore, we mf 2 ∑ mi fi

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The index was used as an indicator of the 73.3 min (1.5–94.5 min) for males and 92.0 amount of overlap between males and min (1.8–107.5 min) for females. Fifty-eight females in the use of resource states for a par- percent of males were observed for 5–30 min ticular variable. Values range from zero (no and the rest (42%) for more than 30 min. overlap in resource use) to one (complete Fifty seven of the females were observed for overlap), and pmi and pfi are the mean propor- 5–30 min and 43% for more than 30 min. tion of foraging time that males and females, Living trees were used by both sexes respectively, spent at resource state i (differ- much more (> 90% of foraging time) than ence between sexes at each state are any other substrate type; hence, comparisons summed). regarding microhabitat use were made only We performed all statistical analyses using considering those substrates. As an exception, R statistical software version 2.11.1 (R Devel- successful captured prey comparisons opment Core Team, R Foundation for Statis- included observations from all substrates. tical Computing, Vienna, Austria, www.R- According to the PCA, the first compo- project.org). PCA was conducted with the nent was linked with dimensions (size and package FactoMineR v1.10 (Lê et al. 2008) in height) of the microhabitat, while the second R. We tested normality and homocedasticity component was related to foraging tech- using residual plots and used parametric tests niques and qualitative features at the foraging unless the data distributions violated the locations (Table 2). Males were associated assumptions. All tests were two tailed; values with large values of the first and second com- of P < 0.05 were considered significant. We ponents (R2 = 0.4 and 0.2, respectively, both report median and range, and also means ± components P < 0.001, Fig. 1), while females

SE. did the opposite (t50 = 5.2, P < 0.001; t50 = - 2.9, P = 0.005, PC1 and PC2, respectively). RESULTS Males foraged mostly on trunks and at lower heights than females. Females foraged Morphology. Males were larger than females in on smaller substrates, which occurred higher wing and tail, indicating that males were larger in the trees (Fig. 2, Table 2). These correlated overall. However, the dimension that best dif- features of the foraging substrates resulted in ferentiated the sexes was the bill length (cul- a vertical separation of the sexes, with females men cord length in Table 1). The models foraging in the higher third (crown) more including bill length showed the highest parsi- than in the mid and lower thirds of living mony ranks according to AIC scores. The trees. The highest (terminal) parts of trees selected model included as predictors the cul- were not used as much as other tree portions men cord, wing, tail, and claw length. Parame- by either of the sexes. ter estimates for the best model are shown in Males were more associated with foraging Table 1. locations characterized by the presence of holes than females. Females foraged in both Foraging behavior. Members of the pair nearly microhabitats with and without bark, but always foraged in close proximity (0–50 m) locations covered by bark were the most com- and therefore it was possible to estimate the mon situation (Table 2). Closeness to limb distance between the focal bird and its mate. joint or trunk fork had no association with The total time of observations was 25 h for the foraging location of Magellanic Wood- 31 males and 22 h for 21 females, spread in peckers. Because both sexes generally foraged 164 sequences; median time per sequence was on living trees, the use of dead wood as forag-

534 DIFFERENTIATION BETWEEN SEXES OF MAGELLANIC WOODPECKERS value of the P

1.2 2.2 6.0 2.3 5.0 12.4 in relation to that for that to relation in % Difference % s = 0.09 = 0.08 P < 0.001* < 0.001* = P P P - - 0.10 ± 0.06, 0.10 ± Estimated coefficient Estimated -0.06 ± 0.03, 0.54 ± 0.12, 0.54 ± 0.49, 1.59 ± Range 151–190 198.0–222.5 43.40–56.00 25.53–41.40 22.73–34.48 16.88–21.18 n 64 64 63 64 63 63 Females gellanic Woodpeckers. Estimated standard coefficients, error, and gellanic Woodpeckers. 24.9 ± 2.68 Mean ±SE 48.75 ± 0.39 34.26 ± 0.37 19.29 ± 0.10 174.70 ± 1.09 174.70 ± 4.79 202.70 ± Range 144.50–196 198.50–229 48.50–63.94 29.17–42.84 21.00–36.15 19.00–21.93 n 59 59 59 59 58 58 Males d significantd differences shown. (*) are Mean ± SE Mean ± 54.81 ± 0.45 36.33 ± 0.41 25.47 ± 2.56 20.25 ± 0.09 176.80 ± 1.30 176.80 ± 6.18 205.80 ± Tail Wing Culmen Cord Tarsus Toe (third) (third) Claw 1. Morphometric measurements (mm) of adult male and female Ma female and male adult of (mm) measurements 1. Morphometric TABLE sexe the between values mean in difference the as expressed is difference Thepercentage given. are model best the of variables an (n), size sample ± SE, Means females.

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TABLE 2. Components extracted by PCA from 18 both sexes was debarking (Fig. 3). Females foraging variables and constructed for 31 males were more mobile than males during foraging and 21 females Magellanic Woodpeckers. Variables sequences and this was also reflected by their were significant P < 0.001 in their correlations and more intensive use of the scanning technique loadings = |0.45| were used for interpretation (Table 2), alternated with debarking. A higher (Aspey & Blankenship 1977). investment of time in movements between substrates by females could be attributed to Component their tendency to explore small branches in PC 1 PC 2 the crown. Body positions adopted by Specific location females were distributed among semi-hori- Trunk -0.76 0.34 zontal (both types: with head down and with Substrate condition head up) and vertical, while males foraged in a Live - 0.36 vertical position most of the time (Fig. 3). Relative height Foraging success rate, measured as: 1) the Mid -0.70 -0.37 number of prey obtained per minute and 2) Higher 0.77 0.39 per number of used substrates, was almost Foraging height equal for males and females (median: 0.07, 5.1–10 m -0.60 -0.34 10.1–15 m 0.36 - range: 0–0.28 prey/min., Z = 268.0, P = 0.28; > 15 m 0.42 0.44 median: 0.47 range: 0–5 prey/substrate, Z = Substrate diameter 304.0, P = 0.7, respectively). In contrast, > 30 cm -0.67 - when comparing the type of prey, males cap- 10–15 cm 0.69 - tured more larvae than females (unpaired Wil- < 10 cm 0.36 - coxon signed rank test P = 0.007, Fig. 4). Feature of foraging location However, we found no differences between Bark - -0.52 sexes for near-surface or indeterminate prey Hole - 0.75 (unpaired Wilcoxon signed rank test, P > 0.05 Foraging techniques for both comparisons). For males, 82% per- Excavating 0.35 0.50 cent of the successful prey capture events (n Debarking - 0.32 Probing - 0.60 = 106) occurred after applying the probing Scanning - -0.42 technique, and 14% after debarking. Females Body position captured prey by probing in 73% of recorded Semi-horizontal head-up 0.44 -0.29 events (n = 108), and by debarking in 25% of Vertical -0.41 0.36 the records. These techniques were usually Eigenvalue 3.9 2.8 alternated with excavating (especially by Explained variance (%) 23 16 males) or scanning (especially by females). Cumulative % 23 39 Niche breadth and overlap. Divergences between ing substrate is explained by females using sexes in foraging behaviors were related to dead branches, usually with no bark (Fig. 2). location within substrate, substrate diameter, The use of foraging locations with holes and relative height (Table 3), in accordance by males relates to their foraging techniques. with the previous results (Fig. 2). Females Males regularly foraged at pits previously showed greater flexibility in body position on excavated, and at crevices or natural holes the foraging substrate (P = 0.002), explained (Table 2) using excavating and probing tactics. by their use of horizontal and vertical pos- The most common foraging technique for tures.

536 DIFFERENTIATION BETWEEN SEXES OF MAGELLANIC WOODPECKERS

FIG. 1. PCA based on the Magellanic Woodpecker foraging behavior and substrate use variables. PC1 is mainly represented by the specific location within the foraging substrate (trunk vs branch), foraging height (relative and absolute), and substrate diameter (i.e., greater than 30 cm or between 10–15 cm); while PC2 is depicted primarily by the feature of the foraging location (with or without bark). Empty squared symbols represent barycentres (means) of samples’ placement within the sex categories, with 95% confidence levels within a category given by ellipses.

Social dominance. Sixteen events of displace- smaller niches: differences in resource use ment between adults were recorded (44% of occurred in microhabitat (parts of trees), prey the agonistic interactions among family mem- type, and foraging behavior. The differential bers), all of which corresponded to males dis- utilization of microhabitats and behaviors was placing their mates from tree trunks. accompanied by significant morphological Displacement by females corresponded to differences, with males being larger and adults chasing away their offspring (same or having larger bills. Our observations of male opposite sex, n = 5). Two immature floater dominance support the notion of a possible females were also recorded displacing unre- complementary role of interference as a lated immature individuals. Adult males were mechanism to maintain the resource special- also seen displacing their offspring: immature ization, and the foraging niche partitioning birds of the same (n = 11) or different (n = 4) found between the sexes. sex. According to how the woodpecker species exploit resources, they evolved in different DISCUSSION ways. The most common pattern is that males are usually larger than females in several Adult male and female Magellanic Woodpeck- morphological variables (Short 1982), hence ers forage in close proximity and use living allowing sex-specific differences in resource lenga trees. Despite this overlap in foraging utilization, with females normally foraging habitat, our data reveal that sexes partition on smaller substrates (e.g., spp., their shared main substrates (live trees) into Melanerpes spp., Short 1970b; Crimson-crested

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FIG. 2. Proportion of time invested by males and females of the Magellanic Woodpecker at different for- aging substrates and characteristics of these foraging substrates: A) type of foraging substrates, B) tree sec- tion, C) specific substrate condition, D) characteristic of the foraging location, E) and F) foraging location height, and G) width of the specific substrate. Means and SE are shown.

538 DIFFERENTIATION BETWEEN SEXES OF MAGELLANIC WOODPECKERS

FIG. 3. Proportion of time invested by males and females of the Magellanic Woodpecker in different foraging behaviors (A), and foraging posture within the substrate (B). Means and SE are shown.

Woodpecker, Campephilus melanoleucos, Kilham populations of the same species (Selander 1972; Great Spotted Woodpecker, Dendrocopos 1966). major, Osiejuk 1994; White-backed Wood- The apparently longstanding existence of pecker, D. leucotos, Stenberg & Hogstad the Magellanic Woodpecker without competi- 2004). tors in an isolated biome (Vuilleumier 1985) Intersexual differences in morphology are may explain its degree of sexual dimorphism. more pronounced in insular woodpeckers In support of this, Short (1970a) noted that than in mainland forms of the same or related the overlap in culmen length between the genera because of a reduced interspecific sexes is smaller in the Magellanic Woodpecker competitive environment on islands (Selander (18%) than in the Ivory-billed Woodpecker 1966, Bennett & Owens 2002). In most (Campephilus principalis) (36%) that coexisted woodpeckers, sexual dimorphism in bill with potential competitors. Thus, the dimor- length does not exceed 10%, but in insular phism in bill length between males and species, the bill of the male is, on average, females of the Magellanic Woodpecker is in markedly larger than that of the female (e.g., accordance with its possibly broadened 27% in the Hispaniola Woodpecker, Melaner- “niche” (sensu Short 1970a) in the absence of pes striatus, Selander 1966). Magellanic Wood- competitors. In parallel, we found that Magel- peckers that occur in an insular-like environ- lanic Woodpecker males also consumed larger ment show a degree of sexual bill dimorphism prey from living trunks with thicker bark, (12.4%) that is intermediate between truly compared to small prey obtained on dead or insular and continental species. This degree of living branches by females. This is in agree- sexual dimorphism resembles populations of ment with the specialization hypothesis as a Gila (Melanerpes uropygialis) and Ladder-backed mechanism for resource optimization in this (Picoides scalaris) Woodpeckers occurring at the species, found both in other woodpeckers southern end of the peninsula of Baja Califor- (Kilham 1972, Short 1982, Aulén & Lundberg nia, which apparently are more dimorphic in 1991) and in other bird species (Payne 1984, bill dimensions than are mainland continental Winkler & Leisler 1985, Témeles et al. 2010).

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FIG. 4. Proportion of prey type captured by male and female Magellanic Woodpeckers. Means and SE are shown. Male and female sample sizes refer to the amount of individuals observed consuming prey. Prey item sample size: 47 wood-boring larvae, 21 near-surface, and 38 indeterminate for males; 26 wood-boring larvae, 32 near-surface, and 50 indeterminate for females. Different lowercase letters indicate statistical sig- nificance (P < 0.05) between sexes.

Although males and females overlapped used the debarking technique, males exca- in their niche breadth, the intensity of use of vated deep holes more intensively than different substrate categories varied between females. Other studies concerning foraging sexes of the Magellanic Woodpecker. Males techniques of woodpeckers often found that and females were separated primarily by for- males excavate foraging holes significantly aging location and secondarily by foraging more than females. For example, this was behaviors. The most important microhabitat observed for Melanerpes spp. (Selander 1966, intersexual segregation was the differentiation Wallace 1974), Hairy Woodpecker (Picoides vil- in trunk (mid and low parts of trees) and losus, Kilham 1965), Arizona Woodpecker crown (highest tree portion). The scarce use (Picodes arizonae, Ligon 1968), White-backed of the terminal parts of crowns possibly acts Woodpecker (Aulén & Lundberg 1991, Sten- as an anti-predator strategy from known berg & Hogstad 2004), and Great Slaty predators, such as Buteo spp. or Chilean Hawk Woodpecker ( pulverulentus, Lam- ( chilensis) (McBride 2000, Chazarreta mertink 2004). Vergara & Schlatter (2004) et al. 2011). described the main foraging technique of Concerning the niche breadth in behav- Magellanic Woodpeckers in pure and mixed iors, males were more stereotyped than lenga forests further south in Patagonia females in the body position on substrates, (54°S) as the excavating of holes into hard- spending much of their time at vertical posi- wood followed by debarking, but differences tions. Flexibility in body posture may repre- regarding foraging behavior between sexes sent adaptations to the different subniches were not assessed. Discrepancies with our used by female Magellanic Woodpeckers. study (where debarking was most frequent Although both males and females mostly technique) may be due to observations biased

540 DIFFERENTIATION BETWEEN SEXES OF MAGELLANIC WOODPECKERS

TABLE 3. Foraging niche dimensions for male (n = 31) and female (n = 21) Magellanic Woodpeckers. Z-values are from unpaired Wilcoxon signed rank test. Significant differences are given (*P < 0.05).

Foraging category Niche breadth Niche overlap Male Female Z Median Range Median Range Substrate type 0.00 0.0–0.19 0.00 0.0–0.49 376.5 0.95 Specific location 0.27 0.0–0.5 0.28 0.0–0.52 364.5 0.67 Substrate condition 0.01 0.0–1.0 0.40 0.0–1.0 416.5 1.0 Substrate diameter 0.18 0.0–0.74 0.34 0.0–0.91 419.5 0.57 Relative height 0.32 0.0–0.97 0.22 0.0–0.89 246.5 0.72 Height above ground 0.43 0.0–0.91 0.32 0.0–0.95 317.0 0.81 State of foraging location 0.29 0.0–0.71 0.44 0.0–0.92 397.5 0.80 Foraging technique 0.53 0.19–0.87 0.52 0.19–0.76 311.5 0.90 Body posture 0.01 0.0–0.4 0.13 0.0–0.47 489.0* 0.89 over one of the sexes (males) in the former different food resources by each sex of the study and/or due to different classification of Magellanic Woodpecker. A causal relationship behaviors. between these two fields of sexual divergence Agonistic interactions observed for is among the most difficult hypotheses to test Magellanic Woodpeckers suggest interference in biology (cause-effect). Now, with both the competition with dominance by males over morphological and behavioral divergence pat- females. Social dominance where the male terns confirmed and quantified, it would be excludes females from favored areas or worth designing experimental research resources has been proposed as a factor relat- addressing the most recognized theories of ing to sexual dimorphism and differentiation intraspecific niche differentiation, like past or in several woodpecker species (Ligon 1968, present intraspecific competition, and isolated Hogstad 1978, Peters & Grubb 1983, Matthy- evolution (or innate behavioral preference) sen et al. 1991, Osiejuk 1994). Although we (Slatkin 1984, Shine 1989). found no difference between sexes in prey capture rates, we recorded more deep big ACKNOWLEDGMENTS wood-boring larvae obtained through excavat- ing for males and more near-surface arthro- The following museums allowed access to pods for females. This suggests males may their collections: Museo Argentino de Cien- obtain more energy gain per consumed item, cias Naturales, Buenos Aires; Museo del Lago and thus an advantage of social dominance. Gutierrez, S. C. de Bariloche; Museo de Cien- Interestingly, the same pattern was described cias Naturales de La Plata; Museo de la Pa- for the size/type of prey carried by each sex tagonia, S. C. de Bariloche; Museo Ornito- to active nests during the rearing period lógico de la Patagonia, El Bolsón; Instituto (Ojeda & Chazarreta 2006), when the adapta- CRICyT, Mendoza; Instituto Miguel Lillio, S. tive value of acquiring larger prey becomes a M. de Tucumán; Museo Nacional de Historia benefit for the offspring survival. Natural de Chile, Santiago; Collections of Acting together, morphology and micro- Cornell University, Ithaca; American Museum habitat divergence may explain acquisition of of Natural History, New York; Carnegie

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Museum of Natural History, Pittsburgh; Nat- Amadon, D. 1959. The significance of sexual dif- ural History Museum of Los Angeles County; ferences in size among birds. Proc. Am. Phil. Michigan State University Museum, Lansing; Soc. 103: 531–536. Museum of Zoology, University of Michigan, Armesto, J. J., P. León-Lobos, M. T. K. Arroyo. Ann Arbor; Museum of Vertebrate Zoology, 1996. Los bosques templados del sur de Chile y Argentina: una isla biogeográfica. Pp. 23–28 in Berkeley; National Museum of Natural His- Armesto, J. J., C. Villagrán, & M. T. K. Arroyo tory, Washington, D.C.; Peabody Museum of (eds). Ecología de los bosques nativos de Chile. Natural History, New Haven; Western Foun- Editorial Universitaria, Santiago, Chile. dation of Vertebrate Zoology, Camarillo; and Askins, R. A. 1983. Foraging ecology of temper- Royal Ontario Museum, Toronto. ate–zone and tropical woodpeckers. Ecology We are indebted to many people who 64: 945–956. contributed to this study. The Diversidad- Aspey, W. P., & J. E. Blankenship. 1977. Neumeyer Refuge group helped with field and snails statistical tales: application of multi- logistics. IDEA Wild, Birders’ Exchange, variate analysis to diverse ethological data. Pp. Vuilleumier Fund for Research on Neotropi- 75–120 in Hazlett, B. A. (ed.). Quantitative cal Birds, Manomet-K.S. Anderson Award methods in the study of behavior. Aca- demic Press, New York, New York, USA. and Grant-In-Aid of Research from the Aulén, G., & A. Lundberg. 1991. Sexual dimor- National Academy of Sciences, administered phism and patterns of territory use by the by Sigma Xi, and The Scientific Research White–backed Woodpecker Dendrocopus leucotos. Society (USA) donated equipment fundamen- Ornis Scand. 22: 60–64. tal to this research. The morphological mea- Baldwin, S. P., H. C. Oberholser, & L. G. Worley. surements were completed thanks to the 1931. Measurements of birds. Sci. Publ. Cleve- financial support from the American Museum land Mus. Nat. Hist. 2: 1–165. of Natural History and the Cornell Lab of Bennett, P. M., & I. P. F. Owens. 2002. Evolution- Laboratory. This manuscript was greatly ary ecology of birds. Oxford Univ. Press, improved by comments of the editor and Oxford, UK. anonymous reviewers. Our study complies Bortolotti, G. R. 1984. Sexual size dimorphism and age–related size variation in Bald Eagles. J. with the current laws of Argentina and was Wildl. Managem. 48: 72–81. conducted under permits from the Adminis- Catry, P., R. A. Phillips, J. P. Croxall, K. E. Ruck- tración de Parques Nacionales. shuhl, & P. Neuhaus. 2005. Sexual segregation in birds: patterns, processes and implications REFERENCES for conservation. Pp. 351–378 in Ruckstuhl, K. E., & P. Neuhaus (eds). Sexual segregation in Aebischer, N. J., P. A. Robertson, & R. E. Ken- vertebrates: ecology of the two sexes. Cam- ward. 1993. Compositional analysis of habitat bridge Univ. Press, Cambridge, UK. use from animal radio-tracking data. Ecology Chazarreta, L., V. S. Ojeda, & A. Trejo. 2011. Divi- 74: 1313–1325. sion of labour in parental care in the Magellanic Airola, D. A., & R. H. Barrett. 1985. Foraging and Woodpecker Campephilus magellanicus. J. Orni- habitat relationships of -gleaning birds in thol. 152: 231–242. a Sierra Nevada mixed-conifer forest. Condor Crawley, M. J. 2007. The R Book. John Wiley and 87: 205–216. Sons, Chichester, UK. Akaike, H. 1973. Information theory as an exten- Grant, P. R. 1986. Ecology and evolution of Dar- sion of the maximum likelihood principle. Pp. win’s Finches. Princeton Univ. Press, Princeton, 267–281 in Petrov, B. N., & F. Csaki (eds). 2nd New Jersey, USA. International Symposium on Information The- Hedrick, A. V., & E. J. Témeles. 1989. The evolu- ory. Akademiai Kiado, Budapest, Hungary. tion of sexual dimorphism in animals: hypothe-

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