Wilson Bull., I1 l(3), 1999, pp. 340-345
VISUAL COMMUNICATION AND SEXUAL SELECTION IN A NOCTURNAL BIRD SPECIES, CAPRIMULGUS RUFICOLLIS, A BALANCE BETWEEN CRYPSIS AND CONSPICUOUSNESS
JUAN ARAGONES, 1,2,3LUIS ARIAS DE REYNA, ’ AND PILAR RECUERDA ’
ABSTRACT-Cryptic protective mechanisms and the conspicuousness required to communicate result in a conflict of opposing selection. In the Red-necked Nightjar (Cuprimulgus ru$coZZis) a nocturnal bird, the use of a restricted signaling strategy provides an appropriate balance between these two selection forces. Conspicuous white wing and tail bands may have been favored by sexual selection in this species. We studied the variation of visual signals and found conspicuousness to be closely related to sex and age, being much higher in males and adults. This variation allows an individual to identify the reproductive status of conspecifics, providing sexual selection a basis to select these visual signals in this and other nocturnal bird species. We believe that a relationship between restricted signaling strategy and sexually selected visual signals may occur in nocturnal species that use visual comunication. Received 24 April 1998, accepted 5 Feb. 1999.
Crypsis is one of the more effective anti- visible in some contexts (agonistic, antipred- predator mechanisms (Baker and Parker ator, and sexual displays) when the sender in- 1979). Because it relies on inconspicuousness, tentionally shows its markings to the receiver its use can conflict with the conspicuousness (Bent 1940, Mengel 1972, Bruce 1973, Cramp required for communication. Selection pres- 1985, Fry et al. 1988, Cleere 1998, Aragones sure drives populations to address signals et al, in press). Some caprimulgid species among conspecifics (conspicuousness increas- have been reported to show individual varia- es at close range) and to conceal them from tion in spot size and color (Common Night- predators (inconspicuouness or long range hawk, Chordeiles minor, Selander 1954; Red- crypsis; Butcher and Rohwer 1989). An ap- necked Nightjar, Beven 1973, Soares 1973; propriate balance between crypsis and com- Blackish Nightjar, C. nigrescens, Ingels and munication is achieved by the use of restricted Ribot 1982). This variation in spots suggests signaling, for example, the presence of hidden that signal conspicuousness might vary with conspicuous signals in highly specific body age and sex. zones that are only exhibited in some situa- The objective of this paper is to describe tions (see Butcher and Rohwer 1989). the variation of spots in signal conspicuous- In strictly nocturnal birds, which account ness in the Red-necked Nightjar and to ex- for less than 3% of all bird species (Martin amine whether this variation is related to age 1990), the visual channel is assumed to play and/or sex. We hypothesize that if males, es- an insignificant role in communication com- specially adult males, show greater conspicu- pared to diurnal birds. However, this is only ousness in wing and tail bands, then these an assumption and nocturnal birds may use plumage characters may be sexually selected. visual signals to communicate more widely than is thought. The Red-necked Nightjar (Cu- METHODS primulgus ruficollis) is a nightbird of open and We used data from 170 specimens obtained from semi-open habitats that uses sight to capture bird collections at Estacidn Biologica de Dofiana, flying insects. The plumage of caprimulgids is CSIC (n = 22) and from road casualties (n = 148) in Cdrdoba (southern Spain) during the 1986 to 1994 highly cryptic, but includes white spots on breeding seasons. From this sample we measured the wings, tail, and throat. These markings, be- following variables related to conspicuousness. (1) cause of their anatomical location, are only Band size. The wing-band consisted of 3 to 4 spots and the tail-band of 2 to 3 spots. Using a digital caliper, the longer and shorter axis of each spot was measured 1Dpto. Biologia Animal, Univ. de Cordoba, Avda. (2 0.1 mm) and the area for each was calculated. The San Albert0 Magno, sn. 14004 Cbrdoba, Spain. surface areas of the spots present in the outer primaries 2 Present address: Avda. Cadiz no 5, 14009Cordoba. of the right wing were summed and recorded as wing- Spain. band size and those on right rectrices were summed 1 Corresponding author; E-mail: ba2biani @uco.es and recorded as tail-band size. The area of each spot
340 Aragon& et al. * CRYPSIS AND CONSPICUOUSNESS 341
able for data that are not normally distributed and is more effective than other classifying methods such as discriminant analysis (Press and Wilson 1978; see also Harrell 1986, Schlinger 1990, Fancy et al. 1993). Con- spicuousness data were transformed logarithmically for parametric analysis. All analyses were performed using JMP software (version 2, Macintosh computer).
RESULTS There were significant differences in wing- band size (F = 31.47, df = 3, 90, P < 0.001) and tail-band size (F = 41.61, df = 3, 90, P < 0.001) between sex-age categories. Wing and tail bands were significantly larger in FIG. 1. Wing-band (WBC) and tail-band contrast males than in females and larger in adults rel- (TBC), calculated from color and sharpness values of spots forming the bands (1 = maximum contrast value, ative to young. There was a clear trend for white spot with sharp contrasting edges, 0 = minimum band size to increase in an age-sex sequence, contrast value, dark spots without sharp contrasting both in wing-band (mean young females = edges). 662.3 ? 37.87 SD, n = 29; mean adult fe- males = 803.1 5 52.66, IZ = 15; mean young was indexed by the product of the long and the short males = 986.3 ? 37.24, 12 = 30; mean adult axis. (2) Band contrast. Contrast was measured from males = 1210.5 2 45.61, n = 20) and in tail the color and sharpness of the spots that formed the band (mean young females = 743.4 k 67.06, wing and tail bands. The contrast gradient was estab- n = 29; mean adult females = 1046.4 k lished from a reference series formed by four types of 93.24, IZ = 15; mean young males = 1428.7 spots that were assigned the values 0, 0.33, 0.66 and + 65.93, n = 30; mean adult males = 1852.6 1; where 0 denoted the spot with the darkest colour and least sharp contrasted edges, and 1 that with the -C 80.75, n = 20). Both variables were found lightest color and sharpest edges. A given individual to be positively correlated (r = 0.67, n = 93, can possess spots of different types (depending on col- P < 0.001). or and sharpness variations), so each spot was assigned The multiple logistic regression discrimi- a value, and a mean index was used for the contrast nated between the four age-sex classes in analysis in wing-band contrast and tail-band contrast terms of wing-band or tail-band contrast (Ta- which included all spots of the wing and tail (Fig. 1). (3) Uniformity of color spots within a band. Some in- ble 1). There were significant differences in dividuals showed bands consisting of a single type of sex and age for wing-band contrast (x23 = spot, whereas others had one or two different types; 86.33, P < 0.001, n = 94) and tail-band con- the former were designated “uniform” and the latter trast x23 = 94.21, P < 0.001, n = 94). Males “non-uniform”. (4) Spot number in wing and tail and adults always had the largest contrast in- bands. (5) Band conspicuousness. Band size and con- dex both for wing-band and tail-band (Fig. 2). trast values were first log transformed, normalizing the Sharp edges were detected only in males with data for the application of parametric statistics and used to calculate a conspicuousness index (C) from the wing-band or tail-band contrast index close to following expression: one because only such spots had sharp edge contrasts. Males showed greater uniformity in C = WBS X log(WBCf1) + TBS X log(TBC+l)/ WBS + TBS wing-band contrast than females, and adults were more uniform than young in this respect. where WBS = wing-band size, TBS = tail-band size, All groups showed uniform tail bands (Table WBC = wing-band contrast, and TBC = tail-band contrast. This index varied from 0 to 1, with 1 corre- 2). sponding to maximum conspicuousness. Sex was de- The presence of four spots on the wing is termined by gonadal dissection. Differences in band an exclusive feature of adult males (Table 2); size and conspicuouness were analysed by ANOVA over 45% (n = 16) of adult males have the and the Tukey test, and differences in the number of fourth spot. About 80% of adult males also spots and their uniformity by means of the G-test. Con- tended to possess three caudal spots (n = 28; trast differences were identified by multiple logistic re- gression, which allows one or more categorical vari- Table 2). Additional spots on the tail was not ables (contrast in our case) to be analysed and related significantly different among the other groups to a dependent variable. This method is especially suit- (Table 2). The additional wing spot increased 342 THE WILSON BULLETIN l Vol. III, No. 3, September 1999
TABLE 1. Parameter estimates of logistic functions derived from multiple logistic regression.
Loglstlc function parameters Estimate Wald test P
(Young female vs adult female) Intercept 1 9.47 17.62 the wing-band size of adult males an average of 6% and the tail-band size of adult males an 1 rw. average of 12%. The presence of additional .- spots on wing and tail increased the overall = 0.6 sa band area by 9.6% and presumably increased m .a 0.6 signal conspicuousness. There were signifi- 0 cant differences in conspicuousness (Table 2) L 0.4 with regard to age-sex classes, with greater a conspicuousness in males and adults. 0.2 DISCUSSION We detected a marked trend for signal con- 0 0.1 02 0.3 0.4 0.6 0.6 0.7 0.6 06 1 spicuousness to increase with age and in males which was reflected in an increase of sr .- contrast, number of spots, wing- and tail- = 0.6 bands area, and uniformity of contrast. The a m differences in conspicuousness in wing- and 0.6 II tail-bands were related to the age and sex class 0 L of the individual. Potentially, these signals let 0.4 a conspecifics evaluate one another in aggres- sive or reproductive contexts. Signal conspic- 0.2 uousness seemingly involves little energy ex- penditure but is combined with expensive dis- plays; the combination results in an efficient Tail band contrast signal that conveys a much greater amount of information (Hasson 1991). We found that FIG. 2. Heavy line indicates probability of belong- ing to a sex class as a function of wing-band contrast spot number was related to sex and age, but (WBC) or tail-band contrast (TBC), thin lines indicates Forero and coworkers (1995) found no statis- probability of belonging to an age class. tically significant differences in the average Aragon& et al. l CRYPSIS AND CONSPICUOUSNESS 343 TABLE 2. Frequency distribution of contrast uniformity, additional spots in bands and conspicuousness index for age-sex groups. Female Male Y0ullg Adult Young Adult P Contrast uniformity (n = 94) n = 29 n = 15 n = 30 II = 20 WBC” (G, = 27.29) 37% 66% 66% 95% a WBC = wmg-band contrast, TBC = tail-band contrast. number of spots between groups of the same In the Red-necked Nightjar increased signal species. We believe the addition of new spots conspicuousness may increase the likelihood has a strong biological significance because it of mating (Andersson 1982, Andersson 1992, occurs only in adult males as reported by For- Saetre et al. 1994), and conspicuous males ero and coworkers (1995), but their method, may have a higher mating success (Payne failed to demonstrate a significant difference. 1982, Price 1984, Jkvi et al. 1987, Harvey FIG. 3. For restricted signaling strategy to be effective, conspicuous plumage zones (black and white areas in the drawing) must be concealed by cryptic plumage zones (gray areas in the drawing) while at rest. A hypothetical model based on the genus Cuprimulgus (1) represents the maximum possible conspicuousness for restricted signaling strategy; a larger conspicuous area would defeat the defensive system based on crypsis and hence cancel restricted signaling strategy. The Nacunda Nighthawk (2), the Sand-Colored Nighthawk (3) and the White-Winged Nigthjar (4) use three restricted signaling strategies that are very similar to that of the model, esspecially the Sand-Colored Nighthawk. 344 THE WILSON BULLETIN l Vol. 111, No. 3, September 1999 and Bradbury 1991, Sundberg and Larsson the body (Fig. 3). We subsequently found that 1994). The fact that increased signal conspic- the Nacunda Nighthawk and the White- uousness was associated with adult males sug- Winged Nightjar (Caprimulgus candicans) gests that the signal could be modified by sex- have patterns that closely resemble our model, ual selection (Hoglund 1993). For adult males, and the Sand-colored Nighthawks’ (Chordei- this signal indicates that those individuals les rupestris) visual signals patterns are iden- have survived at least two reproductive sea- tical with that of the model. All three are gre- sons and, therefore, may reflect a high repro- garious South American species of open or ductive quality. In another nocturnal bird spe- semiopen habitats with sexual variations in cies, the Great Snipe (Gallinago media) males wing- and tail-bands (Ffrench 1986, Hilty and have white spots on their tails, and females Brown 1986, Sick 1993). It is interesting to choose the males with the whitest signals note that the Sand-colored Nighthawk and the (Hoglund et al. 1992). This suggests that sig- Yellow-billed Tern (Sterna superciliaris), two nal conspicuousness in nocturnal birds could Amazonic species that use the same fluvial be an effective way of distinguishing between habitat, show almost identical visual signal potential mates. patterns and general appearance (see Sick Our results show that in Red-necked Night- 1993). This convergent evolution stresses the jar both sexes possess ornaments, and that in significance of open and semiopen habitats for both sexes spots tend to increase in conspic- restricted signaling strategy evolution. Such uousness with age. Forero and coworkers habitats are also characterized by other species (1995) claimed that visual signals increased that employ this strategy, Burhinus spp. and only in males. We believe that their results are the Great Snipe (Hayman et al. 1986). We be- due to a less precise method of measuring spot lieve that a relationship between restricted sig- size. naling strategy and sexually selected visual The restricted signaling strategy allows two signals may occur in nocturnal species that scarcely compatible mechanisms to be com- uses visual comunication. bined and might occur in many cryptic species of the genera Burhinus, Charadrius and Gal- ACKNOWLEDGMENTS linago, although this has not yet been inves- Valuable assistance was provided at various stages tigated. For a nocturnal signal, contrast is of this study by many friends. We thank M. C. Casaut, more important than color, as in the capri- A. Leiva, M. A. Nufiez and R. Pulido for help with mulgids and other species that use restricted the collection of traffic casualties, and E M. Coca for help with statistical analysis. We are grateful to M. A. signaling strategy with white spots (i.e., Gal- Nufiez, E M. Coca, R. Reques, S. Carpintero and J. linago media, Hoglund et al. 1992; Burhinus Marfn for practical support, discussion, and comments. spp., Martin 1990, Hayman et al. 1986). Two anonymous referees provided valuable sugges- Therefore, increasing the amount of white col- tions on an early version of this manuscript. or increases contrast and presumably maxi- mizes the signaling ability. Similar trends of LITERATURE CITED increasing conspicuousness with age have ANDERSSON, M. 1982. Female choice selects for ex- been detected in other caprimulgids (Little treme tail lengh in a widowbird. Nature 299:818- Nightjar, C. pan&us heterurus, Schwartz 820. 1968; Chuck-Wills_Widow,’ C. vociferus, ANDERSSON, S. 1992. Female preference for long tails in lekking Jacksons’ Widowbirds: experimental Rohwer 1971; Blackish Nightjar, Ingels and evidence. Anim. Behav. 43:379-388. Ribot 1982; Scrub Nightjar, C. anthonyi, Rob- ARAGON~, J. 1997a. Influencia de la cripsis sobre el bins and Ridgeley 1994; Nacunda Nighthawk, comportamiento de1 Chotacabras pardo, Capri- Podager nacunda, Aragones unpubl. data; mulgus ruficollis. Tesis Doctoral. Univ. de Car- Pauraque, Nyctidromus albicollis, Aragones doba. Cordoba, Spain. 1997a, b). ARAGON~S, J. 1997b. Risk taking and flushing distance: From the distribution of visual signals in a way of parental investment in the Pauraque (Nyctidromus albicollis). Etologia 5:83-90. Red-necked Nightjar (throat, wings, and tail- ARAGONBS, J., L. ARIAS DE REYNA, AND P. RECUERDA. bands), we developed a model plumage pat- 1998. Antipredator strategies and mimicry in Red- tern for a nightjar that represents the optimum/ necked Nightjar Caprimulgus rujicollis. Etologia maximum distribution of conspicuous areas in 6:53-59. Arugon& et al. l CRYPSIS AND CONSPICUOUSNESS 345 BAKER, R. E. AND G. A. PARKER. 1979. The evolution media, prefer males with white tails. Anim. Be- of bird coloration. Phil. Trans. R. 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