SHORT COMMUNICATIONS

ORNITOLOGIA NEOTROPICAL 21: 149–154, 2010 © The Neotropical Ornithological Society

NESTING OF THE DOUBLE-STRIPED THICK-KNEE (BURHINUS BISTRIATUS) IN A HOT ENVIRONMENT

Ana I. Pereira1 & Juan A. Amat2

1Universidad de Costa Rica, Sede Guanacaste, Coordinación de Turismo Ecológico, 31-5000 Liberia, Costa Rica. 2Estación Biológica de Doñana, CSIC, calle Américo Vespucio s/n, 41092 Sevilla, Spain. E-mail: [email protected]

Nidificación del Alcaraván (Burhinus bistriatus) en un ambiente caluroso.

Key words: Costa Rica, flushing behavior, Guanacaste, nest crypsis, nesting ecology, thermal environment.

Many shorebirds (Charadrii) nest in sites with 2004a), leaving the eggs exposed to solar radi- no vegetative cover, so that they can quickly ation while the nest in unattended may be detect approaching predators (Maclean 1967, critical for embryos under hot conditions. Koivula & Rönkä 1998, Amat & Masero The thermal environment may affect the dis- 2004a). In these sites, the lack of shade could tance at which the incubating adult flushes lead to heat stress for the incubating from the nest, or the returning time to nest (Grant 1982, Amat & Masero 2004b), and following disturbance, so that will this may be especially critical for nest- remain on the nests longer when approached ing in tropical environments because of by a predator and return to nests faster after a intense solar radiation. This may lead to situa- disturbance at temperatures above 30ºC tions in which the thermal needs of the adults (Maclean 1967, Brown & Brown 2004, Yasué conflict with those of eggs (Carey 2002, Amat & Dearden 2006). Thus, to protect their eggs & Masero 2007). To breed successfully in hot from overheating, incubating adults may environments, adult shorebirds have several expose themselves to greater risks of preda- strategies to protect the eggs from overheat- tion when ambient temperatures are > 30ºC. ing, such as egg-shading or belly-soaking However, short flushing distances of incubat- (Grant 1982, Downs & Ward 1997, Carey ing adults from predators may facilitate nest 2002; Amat & Masero 2004b, 2007). Because finding by predators. To avoid this, shorebirds incubating shorebirds normally depart from may make their nests and eggs cryptic (Sum- nests when predators approach nests (e.g., mers & Hockey 1981, Solís & de Lope 1995). Koivula & Rönkä 1998, Amat & Masero Moreover, diurnal variations in nest/egg

149 PEREIRA & AMAT color appearance due to changes in illumina- We drove along roads and tracks, and tion (see Endler 1991, Endler & Thery 1996) stopped every time we spotted thick-knees or may determine changes in nest crypticity where habitat appeared suitable, in which case throughout the day. This may also affect the we searched using binoculars. Once thick- distance from predators at which incubating knees were located in a site, we found nests adult birds depart from nests during a distur- by observing their behavior with binoculars bance, so that incubating birds may depart at from 50-100 m. Distances of nests to nearest shorter distances from predators during those tree or scrub (> 1 m tall) were estimated by parts of the day when the nest is more cryptic. pacing, and later transformed to the nearest Therefore, decisions of incubating adults metre. We estimated these distances because to depart from nests during a disturbance trees or scrubs provide potential sites for the may depend not only on the thermal risks off-duty adult to remain under shade incurred by embryos when the nests are left (Maclean 1967). All five nests found con- unattended, but also on diurnal changes in tained a single egg, which was measured nest crypticity due to changes in illumination. [maximum length (L) and maximum width As a result, both ambient temperature and (W)] to the nearest 0.1 mm using vernier calli- nest crypsis may determine the flushing pers. Egg volumes (Ve) were estimated accor- 2 behavior of incubating adults. ding to Douglas (1990) as Ve = KvLW , where In this paper we report some breeding Kv corrects for variation in shape and is calcu- strategies of the Double-striped Thick-knee lated as Kv = 0.5236 - [0.5236 × 2(LW)/100]. Burhinus bistriatus in a hot environment. This We also measured the internal diameter of species is restricted to tropical dry regions of nest scrapes to the nearest cm, using a tape. America (Hayman et al. 1986), and at least in To record the flushing distances of incu- Costa Rica, it breeds during the dry season of bating thick-knees, one of us observed the the year (Stiles & Skutch 1989). We present incubating bird through binoculars while the data on diurnal variations in ambient temper- other researcher walked, at constant pace, atures (Ta) beside nests, flushing behavior of directly toward the nest. At the moment at incubating adults in relation to Ta, and diurnal which the incubating bird left the nest the differences in coloration between eggs and first observer started a stopwatch, which was nest sites. Because there are few studies on stopped once the second observer arrived at the nesting biology of the Double-striped the nest. These times were used as surrogates Thick-knee (Freese 1975, Stiles & Skutch of flushing distances. We made three record- 1989) we also present data on nest character- ings for each nest [early morning (up to 1 h istics and eggs size. after sunrise), midday (11:00–13:00 h), and late afternoon (during the last hour before METHODS sunset)]. These recordings were made either on the same day or on two consecutive days, We searched for thick-knee nests in sites up and the order of visits to nests was not time to 30 km around Liberia (Guanacaste Prov- dependent. ince, NW Costa Rica, 10º38’N, 85º26’W) dur- About 5 min after each recording of ing 5–14 February 2008. The site is located in flushing distances, we recorded Ta (to the the Pacific lowlands, and the habitat is charac- nearest 0.1ºC) 5 cm above ground level terized by pastures, stubble fields and patches about 1 m from each nest scrape, using a 20- of tropical dry forest. Along the watercourses gauge copper-constantan probe connected to there is an evergreen, gallery forest. an Omega HH21 microprocessor thermo-

150 SHORT COMMUNICATIONS meter (Omega Engineering, Inc., Stamford, larger ΔE*, the lower is the similarity in color- CT, USA). To avoid egg overheating while ation between two substrates.

Ta was recorded, we shaded the eggs Because the study involved repeated mea- when temperatures could be critical for surements of the same individual nests, differ- embryos. ences in temperatures at nest sites throughout To quantify the coloration of eggs, nest the day were analyzed using repeated mea- scrapes, and nest surroundings we photo- sures ANOVA, while the Student’s paired t- graphed the nests, using a Canon EOS400 test was used to compare flushing distances digital camera equipped with Canon EFS 18- from nests during midday and afternoon. A 55 mm macrozoom lens. From each nest we general linear mixed model (GLMM) took photographs on sunny days at early approach was used to test the effect of time of morning, midday, and late afternoon. Photo- day (three fixed levels: morning, midday, after- graphs were taken directly from above the noon) on color differences (ΔE*) between nests so that the outer edges of the nest filled eggs and either nest scrape or surroundings. the frame. We did not record ultraviolet (UV) Nest identity was included as a random factor reflectance of eggs, which could have affected in the GLMM. Mean values are presented nest detectability, since birds are able to detect with ± 1 SD. wavelengths in the UV spectrum (Bennett & Cuthill 1994). However, eggshells reflect little RESULTS UV (Bakken et al. 1978). We quantified the coloration of eggs, nest Of the five nests found, three were in short scrape, and ground in the immediate sur- grass pastures, one in an opening in woodland roundings of the nests with Photoshop Ele- of Guazuma ulmifolia (Malvaceae), and another ments, version 2.0 (Adobe, San José, in a stubble sugar cane field. Mean values of California, USA). The eyedropper was set at 5 nest and egg dimensions were: 17 ± 3 cm × 5 pixels, and values in the RGB (red, green, (internal diameter of nest scrape), 58.0 ± 1.0 blue) color space were recorded. We took mm (egg length), 41.4 ± 0.8 mm (egg width), readings at spaced points on the images, not- and 50.5 ± 2.5 cm3 (egg volume). The nests ing whether the readings were on eggs, nest were located at 15 ± 15 m from the nearest scrape, or substrate of the nests’ surround- tree or scrub. During daytime, the off-duty ings. Five metric values were obtained for adult was under the shade of the nearest tree each category (egg, nest scrape, and surround- or scrub to the nest on 8 out of 10 visits to ings), which were averaged for each one of nests in midday and afternoon while its mate these categories for each photograph. We was incubating. transformed the RGB color space to the CIE Ambient temperature varied significantly (Commission Internationale d’Eclairage) throughout the three periods of the day. Tem- L*a*b* color space (see Nguyen et al. 2007), perature was higher during midday (39.8 ± where L* defines lightness, a* denotes the 3.75 ºC, n = 5) than during the morning (26.5 red/green value and b* the yellow/blue value ± 1.44 ºC) or afternoon (33.3 ± 2.03 ºC)

(X-Rite 2000). The color transformations (ANOVA for repeated measures, F3,2 = were done using the CIE Color Calculator 1162.8, P < 0.001). (Lindbloom 2009). Color differences (ΔE*) We did not find adults incubating at three between eggs, and either nest scrape or sur- of five nests in the early morning, and for this roundings, were defined by the equation (X- reason we compared flushing times only dur- Rite 2000) ΔE* = (ΔL*2 + Δa*2 +Δb*2)1/2 . The ing midday and late afternoon. Although

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TABLE 1. Differences in coloration (ΔE*) (mean ± 1 SD) between eggs (EG) and both nests (NE) and surroundings (SU) in Double-striped Thick-knee nests (n = 5), during the early morning, midday and late afternoon. Coloration was recorded from digital photographs in the RGB (red, green, blue) color space and then transformed to the Comission International d’Eclairage L*a*b* color space. A generalized linear mixed model was used to test the effect of time of day on color differences (see Methods for further details).

Morning Midday Afternoon F2,8 P ΔE*EG-NE 25.5 ± 13.40 13.4 ± 7.99 27.0 ± 16.71 3.71 0.073 ΔE*EG-SU 35.6 ± 9.41 16.7 ± 7.75 25.4 ± 10.69 8.51 0.010 there was a trend for incubating adults to approach quickly the nest when its mate stops flush at shorter distances from observer dur- incubating, so that the eggs are almost contin- ing midday (14.9 ± 5.60 sec, n = 5) than in the uously attended during stressful conditions. late afternoon (28.9 ± 9.18 sec), the differ- Some nests were found unattended in the ence was not statistically significant (Student’s early morning. This has also been found in paired t-test, t = 2.57, df = 4, P = 0.062). other shorebird species in hot environments

GLMMs indicated that the color differ- when Ta is between 20°C and 30°C (Maclean ences (ΔE*) between eggs and nest scrapes 1967, George Kainady & Al-Dabbagh 1976, did not vary throughout the day (F2, 8 = 3.71, Grant 1982). P = 0.073), although there were color differ- There were diurnal variations in Ta beside ences between eggs and nests surroundings nests, and this may have affected the distance according to time of day (F2, 8 = 8.51, P = at which incubating thick-knees departed 0.010). In this last case, the color differences from predators. Indeed, when we approached between eggs and nest surroundings were less nests, incubating adults took longer to depart obvious during midday than in the other peri- from nests in midday (when Ta was higher) ods (Table 1). than in the late afternoon, although likely due to small sample size the difference in depar- DISCUSSION ture times was marginally non-significant. We found that the difference in coloration Although our sample size was small, some between eggs of the Double-striped Thick- patterns emerged from our results. High knee and their nest scrapes did not vary ambient temperatures (> 35ºC) may limit the throughout the day. The congeneric Stone ability of incubating shorebirds in exposed B. oedicnemus lines the nest scrapes sites to maintain homeostasis. In the case of with materials collected from the surround- the Double-striped Thick-knee, lack of water ings, and this makes the eggs more cryptic bodies near nests may preclude the regulation (Solís & de Lope 1995; see also Mayer et al. of adult body temperature using belly-soaking 2009). It is interesting to note that despite of (Amat & Masero 2009), and would predispose not adding materials to the scrape, there are incubating birds to desert their nests during no diurnal differences in coloration between stressful thermal conditions (Amat & Masero the eggs of the Double-striped Thick-knee 2004b). Therefore, nesting near trees or and their nest scrapes, in spite of diurnal vari- scrubs likely facilitated that the off-duty par- ations in illumination. Nevertheless, differ- ent could stay under shade, and that it may ences in coloration between eggs and nest

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