Selection for Sexual Bill Dimorphism in Ibises: an Evaluation of Hypotheses

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Selection for Sexual Bill Dimorphism in Ibises: an Evaluation of Hypotheses Selection for Sexual Bill Dimorphism in Ibises: An Evaluation of Hypotheses GREGORY A. BABBITT1 AND PETER C. FREDERICK2 1Center of Evolutionary Functional Genomics, The Biodesign Institute, Arizona State University, Tempe, AZ 85287-5001 Corresponding author. Internet: [email protected] 2Department of Wildlife Ecology and Conservation, University of Florida, Gainesville, FL 32605 Abstract.—Male Scarlet Ibises (Eudocimus ruber) and White Ibises (Eudocimus albus) have bills that are on average 22% longer than females, yet only half of this difference can be attributed to body-size differences. In this work it is suggested that the sexual dimorphism in bill length and bill shape is based in large part upon the role of bill length in determining the outcome of male bill-sparring contests. Sexual differences in bill morphology and behav- ior were investigated in a captive flock of 350 Scarlet Ibises. In 29 instances of males sparring with males in contests prior to breeding and in 11 instances of nest take-over during breeding, no significant differences in age, body size, or body condition between winning and losing males were found. However, males winning bill-sparring contests and nest take-overs had significantly longer bills than losing males. Longer billed males also bred significantly ear- lier than shorter billed males in captivity. Sexual differences in the relationship between bill curvature, bill chord and bill length suggest that male Scarlet and White Ibises are under selection for increased bill length. In addition, among 16 of 23 ibis species for which information was available, sexual dimorphism in bill length was positively as- sociated with colonial nesting but was not associated with group foraging. This result supports the theory that close proximity during nesting is one feature that may facilitate bill sparring between males, resulting in selection for longer bills. Received 19 July 2006, accepted 18 December 2006. Key words.—sexual dimorphism, bill length, sexual selection, bill sparring, male-male competition. Waterbirds 30(2): 199-206, 2007 In sexual contests over mating opportu- evolved between the sexes (Selander 1966; nities, success is often dependent upon rela- Aulen and Lundberg 1991). Lauro and Nol tive rather than absolute trait size. This often (1995) offer three non-exclusive hypotheses leads to evolutionary escalation in size of to explain sexual dimorphism in bill mor- body, weapons or displays (Andersson 1994). phology in birds. Sexual dimorphism in bill Therefore, when sexual selection is present, length may have arisen to reduce sexual small relative differences among males be- competition over limited resources (usually come very important in driving evolution of food), to increase the partitioning of repro- size dimorphism. This often affects the distri- ductive roles, or may have resulted from sex- bution of the relative sizes of traits among a ual selection and male-male competition. population. Green (2000) demonstrates that Empirical studies have suggested that bill dimorphism often exhibits positive al- niche divergence in feeding habits is not a lometry when caused by sexual rather than factor in bill dimorphism in gulls (Ingolfsson natural selection (i.e., relatively larger traits 1969), Greater Sheathbill (Chionis alba) in larger individuals). (Shaw 1986) or other Charadrii (Szekely et al. The degree of sexual dimorphism in bill 2000). However, Radford and Du Plessis length in birds often exceeds sexual dimor- (2004) conclude that ecological niche diver- phism in body size (Coulter 1986; Bond et al. gence, not sexual selection, is responsible for 1991; Lauro and Nol 1995), and is probably maintaining a 36% longer bill in the male influenced by multiple selective forces sur- Green Woodhoopoe (Phoeniculus purpureus). rounding feeding and fighting. Among spe- This suggests that there is no single reason for cies, sexual dimorphism of the bill is often bill dimorphism in different groups of birds. pronounced in situations where inter-specif- As a group, ibises (subfamily Threskion- ic competition is reduced and niche breadth ithinae 23 species, 14 genera) differ widely is wide, or where niche partitioning has with respect to social feeding and mainte- 199 200 WATERBIRDS nance of breeding territory. They also exhibit maintaining sexual dimorphism in bill a wide range of sexual dimorphism in both length in colonial ibises by testing the pre- body and relative bill size. Approximately half dictions of these hypotheses. First, we de- of these species exhibit almost no sexual di- scribe sexual variation in bill and body size morphism. The colonially nesting White/ and shape in a group of 454 captive Scarlet Scarlet Ibis (genus Eudocimus) demonstrate Ibis (Eudocimus ruber). Second, we evaluate the most pronounced sexual dimorphism. the hypothesis that bill length affects the out- Male Scarlet Ibises (Eudocimus ruber) have bills come of male contests by analyzing bill spar- that are on average 22% longer than those of ring behavior, timing of nesting and instanc- females (Hancock et al. 1992). Yet only about es of nest piracy or take-over among captive half of this inter-sexual difference in bills is male Scarlet Ibises of known body size, body represented in tarsal length and therefore, condition, bill characteristics and age. sexual bill dimorphism does not seem to be at- Third, we present interspecific comparisons tributable to a body size scaling effect alone. of sexual dimorphism in bill length and inci- In White Ibises (Eudocimus albus), sexual dence of both colonial nesting and group size dimorphism in the body and bill has foraging in 16 species of ibises. been attributed to both natural and sexual selection. Kushlan (1977) proposed that METHODS larger male White Ibises were better able to defend the nest from conspecifics or preda- Study Area tors than smaller males and were also able to Morphometric and behavioral studies were conduct- dominate extra-pair females in mating inter- ed during February-June of 1998 and 1999 with a cap- actions. However, later research showed that tive flock of 454 full-flighted Scarlet Ibises held in a 3,085 m2 aviary at a large theme park (Disney World, Or- male extra-pair mating success was not based lando, Florida). All individuals older than one year of on the ability of males to dominate females age (≈90%) were identifiable by numbered and colored (Frederick 1987). Bildstein (1987) suggest- leg bands easily visible with binoculars. The aviary con- tained mature trees allowing the ibises to nest roughly ed that differences in body and bill size in 15-20 m above the ground. All interspecific compari- White Ibises may reduce inter-sexual compe- sons were based upon measurements and descriptions tition over food, lead to increased clutch size in Hancock et al. (1992). in females, or be a sexually selected trait. Sex Determination Previous hypotheses explaining bill di- The study included 114 Scarlet Ibises whose sex had morphism in ibises have assumed foraging been determined through observations of copulation niche separation is selectively favored by position, and whose eggs also later hatched during the greater inter-sexual competition in socially 1999 nesting season. A canonical discriminant function analysis was conducted on the rest of the aviary based foraging species like the White Ibis (Bild- upon mass, tarsometatarsus length, straight bill length stein 1987, 1993). Alternatively, if sexual dif- (bill chord), curved bill length (bill length), bill depth ferences in bill length have evolved at least and wing chord and then compared the accuracy of these assignments with the behaviorally derived sex as- partly in response to nest defense against signments. By using only those birds whose eggs hatched, conspecifics, we might predict that longer- any male-male single sex pairs were probably eliminated billed males would be more likely to win ag- from the sample. Female-female pairs were not as easily controlled for in this manner since extra-pair copulation gressive contests at nests than shorter-billed did occur in the aviary. Twenty four percent of all copu- males. Additionally, if nest sites or mates are lation occurred outside of established social pairs, as may limiting and long bills confer dominance, be typical in a non-captive situation (Frederick 1987). then longer-billed males would be more like- Morphometrics ly to nest and might also be expected to nest earlier in the season. And unlike niche sepa- In February and March of 1998 and 1999, 378 adults were weighed and measured. Measurements included ration, male competition and sex role parti- log body mass, tarsometatarsus length, curved bill length tioning could create a trend among ibis spe- (from distal edge of skin on forehead along the top of cies where sexual bill dimorphism is associat- the upper mandible to the bill tip), bill chord (straight measure of mandible joint to bill tip), bill depth (at top ed with sociality. In this study, we investigate of the nares) and curved wing chord (1999 only). Mea- the role of potential selection pressures in surement error estimated from a subsample of 144 birds BILL DIMORPHISM IN IBISES 201 was 3.8% log mass, 1.7% bill chord, 1.8% bill length, cies were computed for which data were available. 3.7% bill depth, and 7.5% tarsal length (wing chord is Species were classified as colonial, loosely colonial unknown). The components of sexual size and shape (breeding both solitarily or in small groups), or strictly variation were separated using a correlation-based prin- solitary breeders. The degree of sexual bill dimorphism cipal components analysis (PCA) (Manly 1994). Size and relative to overall size dimorphism in a given species was shape variation were also analyzed in a similar fashion calculated by dividing the average male to female bill within both sexes to compare the degree of male and fe- length ratio by the average male to female wing length male variation in morphology. Body condition index was ratio.
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