Journal of Arid Environments 102 (2014) 89e97

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Journal of Arid Environments

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A temperature-based monitoring of nest attendance patterns and disturbance effects during incubation by ground-nesting

F. Mougeot a,b,*, A. BenítezeLópez b, F. Casas a,b, J.T. Garcia b, J. Viñuela b a Estación Experimental de Zonas Áridas (EEZA-CSIC), Carretera de Sacramento s/n, 04120 La Cañada de San Urbano, Almería, Spain b Instituto de Investigación en Recursos Cinegéticos (IREC-CSIC-UCLM-JCCM), Ronda de Toledo s/n, 13005 Ciudad Real, Spain article info abstract

Article history: Sandgrouse are of arid environments adapted to cope with extreme temperature variations. We Received 29 November 2012 used temperature data-loggers to remotely study incubation rhythms by pin-tailed and black-bellied Received in revised form sandgrouse in Spain. In both , mates switched incubation roles twice a day, between 08:00 and 14 June 2013 10:00 and between 19:30 and 21:30, when the nest and ambient temperature were most similar. During Accepted 27 November 2013 mate switches, sandgrouse preferred to risk a cooling rather than a warming of eggs. In the pin-tailed Available online sandgrouse, the timing of morning switches was consistent within-pairs, while the timing of evening switches was more related to sunset time. Absences lasted longer following a disturbance than during a Keywords: Data-logger mate switch. During disturbances, changes in nest temperatures depended on the changes in outside Breeding biology temperature, and negatively correlated with absence duration. Absences following a disturbance were Pin-tailed sandgrouse shorter when the outside temperature was higher. Nesting success was low (19%), with no noticeable alchata effect of data-loggers. Our study highlights some of the constraints that birds breeding in arid envi- Black-bellied sandgrouse ronments, such as sandgrouse, face during incubation. It also stresses out the importance of evaluating Pterocles orientalis the consequences of disturbances during incubation, in particular nest visits. Temperature data-loggers can provide an easy and effective way of monitoring nests, without the need of repeated nest visits. Ó 2013 Elsevier Ltd. All rights reserved.

1. Introduction source of disturbance and a cause of nest failure (Carey, 2011; Götmark, 1992; Ibanez-Alamo et al., 2012; Weidinger, 2006). Knowledge of nest attendance patterns and incubation rhythms When direct observations of nest activity are not feasible or desir- are key to our understanding of adaptations to extreme envi- able, researchers have used alternative means of monitoring nest ronments (Grant, 1982), the demands and energetic costs imposed activity, such as video camera recordings, electronic balances, light- on incubating parents (Reid et al., 2002; Thomson et al., 1998) and sensitive and temperature data-loggers. parental investment strategies and life-history trade-offs (Conway Temperature data-loggers have been successfully used to and Martín, 2000; Wiebe, 2001). It is also relevant to conserva- determine when a bird is on or off the nest (e.g. Arnold et al., 2006; tion and can inform about the timing and causes of breeding fail- Weathers and Sullivan, 1989; Weidinger, 2006) and may be ures, and the potential effects of disturbance by humans (Ibañez- particularly suited for studying incubation rhythms of birds in arid Alamo et al., 2012; Lloyd et al., 2000; Schneider and McWilllams, environments, where thermal conditions are critical. Technological 2007). advances have produced data-loggers that are smaller, more ac- A wide variety of nest monitoring methods have been used in curate and with greater battery and data storage capacities. During avian field studies, depending on the characteristics of the target incubation, data-logger methods generate times series that can be species and monitoring aims. Direct observations of nests are time- used to determine the thermal conditions experienced by incu- consuming and often not feasible or desirable, because the nest bating birds, as well as the occurrence (timing, frequency) and content sometimes cannot be observed from a distance, or because duration of absences from the nest (hereafter off-bouts), by the presence of an observer may alter parental behaviour and be a comparing the nest temperature with the outside temperature. Data-logger methods also allow studying the effects of distur- bances, such as nest visits, as well as the breeding phenology and * Corresponding author. Estación Experimental de Zonas Áridas (EEZA-CSIC), nest survival (Schneider and McWilllams, 2007; Weidinger, 2006). Carretera de Sacramento s/n, La Cañada de San Urbano, 04120 Almería, Spain. fi Tel.: þ34 926 29 54 50. In this study, we used for the rst time temperature data- E-mail address: [email protected] (F. Mougeot). loggers to study the nest attendance patterns and the effects of

0140-1963/$ e see front matter Ó 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.jaridenv.2013.11.010 90 F. Mougeot et al. / Journal of Arid Environments 102 (2014) 89e97 nest visits during incubation by two birds typical of arid environ- in JuneeSeptember by pin-tailed and black-bellied sandgrouse, ments: the pin-tailed sandgrouse (Pterocles alchata, Linnaeus 1766) respectively (De Borbón et al., 1999b; Znari et al., 2008). Nests and the black-bellied sandgrouse (Pterocles orientalis, Linnaeus typically consist of a 10e15 cm wide shallow depression on the 1758) in Spain. Sandgrouse nest on the ground and have to cope ground in an area with no or low vegetation cover, unlined or with a with extreme temperature variations during incubation, which few pieces of dried grass (Fig. 1). makes them of particular interest for studying incubation rhythms. Our specific aims were as follows: 1) to document the range of 2.2. Study areas and field procedures temperatures experienced by incubating birds and their clutch; 2) to determine the timing and duration of off-bouts; 3) to analyse Fieldwork was conducted in MayeAugust 2011 in Spain, in two within- and between-pair variation in the timing and duration of study areas located in Campo de Calatrava, Castilla-La-Mancha, off-bouts (when mates normally switch incubation roles); 4) to Ciudad Real province (Special Protection Area e SPA-157; 38 relate the timings of mate switches to thermal conditions (differ- 540N, 3 550W) and in the Bardenas Reales Biosphere Reserve and ences between the nest and control temperatures); and 5) to Natural Park, Navarra province (42 080N, 1 260W). These areas evaluate the effects of nest visits and other disturbances (which were characterized by agro-steppes (Ciudad Real), and by natural may be by people other than researchers or predators) by deter- steppes and/or ploughed fields or barren areas with low vegetation mining how long a bird takes to resume incubation after a distur- cover (Bardenas Reales). bance and the consequences of absences from the nest, in terms of Sandgrouse nests were located by means of conventional radio- exposure of the clutch to potentially harmful temperatures. We use tracking of birds previously caught and fitted with radio- the information to highlight the benefits and limitations of tem- transmitters (see Benítez-López et al., 2011; Martín et al., 2010a,b perature data-loggers for monitoring nests during incubation, and for details on the capture method and tags), or by systematic to give recommendations for optimizing the breeding monitoring search and field observations of unmarked individuals. When of sandgrouse and other birds living in similar arid environments. breeding was suspected (i.e. when a bird was repeatedly located within the same area, and was observed without its partner indi- 2. Materials and methods cating that its mate may have started incubation), we searched for the nest. To do so, we walked towards its putative location. When an 2.1. Study species observer approaches a nest, incubating sandgrouse typically walk away and take off from a short distance. We land marked the last Sandgrouse (family Pteroclidae) are medium-sized ground- location where the bird was seen and carefully searched around it to nesting steppe-birds that are particularly difficult to observe locate the nest. Each nest position was recorded using a GPS (Gar- because of their cryptic and well camouflaged plumage, discrete min eTrex) to the nearest 3e4 m in to facilitate relocation. behaviour and sensitivity to human disturbance (De Juana, 1997). Sandgrouse are well adapted to cope with and arid envi- 2.3. Temperature recordings ronments (Hinsley, 1992; Johnsgard, 1991; Thomas, 1984; Thomas and Maclean, 1981). These adaptations include a dense plumage We used DS1923 Hygrochron Temperature/Humidity Logger i- and thick feet to increase isolation from extreme thermal condi- Buttons with a 8 kb data-log memory (Maxim/Dallas Semi- tions, heat regulation based on high evaporation rates and peculiar conductor Corp; Fig. 1) for temperature recordings. These data- behaviour such as regular visits to waterholes for drinking and loggers record temperature ranging between 20 C and þ85 C, water transportation to chicks (Hinsley, 1992; Johnsgard, 1991; with an accuracy 0.5 C in the range 10 Ctoþ65 C. Marder et al., 1986; Thomas, 1984; Thomas and Maclean, 1981; For each study nest, we set-up two temperature data-loggers: Thomas and Robin, 1977). one was placed inside the nest, underneath the nest lining mate- The pin-tailed and black-bellied sandgrouse are typical of dry rial and the eggs, and covered by a thin layer of soil so that it could steppes and extensive agricultural habitats (del Hoyo et al., 1997; not be seen by the birds (hereafter nest data-logger), and the other Benítez-López et al., in press). Both species have a “Least Concern” one was placed at c.1 m away from the nest, also covered by a thin (LC) conservation status in Europe (BirdLife International, 2004; De layer of soil (hereafter control data-logger). The location of the Juana, 1997) and a “Vulnerable” status in Spain, due to recent control data-logger was chosen to have similar vegetation, shading population declines (Suárez and Herranz, 2004a,b; Suárez et al., conditions and substrate as its corresponding nest data-logger. 2006). Data-loggers were programmed to record temperature every While some aspects of their general ecology have been studied, 5 min during a maximum period of 28 days (the data storage ca- such as their distribution and habitat preferences (Martín et al., pacity of the i-Buttons). This programming ensured covering the 2010a,b; Seoane et al., 2010; Suárez et al., 1997), other aspects, whole incubation period, known to last 20e22 and 26 days in pin- and in particular their breeding biology, are still poorly known (De tailed and black-bellied sandgrouse, respectively (De Borbón et al., Borbón et al., 1999b; De Juana, 1997; Znari et al., 2006). Pin-tailed 1999b; del Hoyo et al., 1997). and black-bellied sandgrouse are socially monogamous, and both Nest monitoring included nest visits (during which we flushed sexes share reproductive duties, mainly to distribute the high de- the incubating bird to check the nest content) and triangulations mands associated with breeding in arid environments (De Juana, (to check for the presence a radio-tagged bird at the nest from a 1997; Johnsgard, 1991). Mates take turns to incubate the clutch distance of 50e100 m, without flushing the incubating bird; and switch incubation roles in the morning and in the evening Table 1). Nests were visited in the morning between 06.40 and (Johnsgard, 1991; Marchant, 1961). The female typically attend the 11.00 or in the afternoon between 18.30 and 21.00, with one nest during the day, and the male attend it from dusk until mid- exception in mid-day (12.25). The repeated absence of a tagged bird morning; during mate switches, the bird leaving the nest typi- from a nest during its normal period of nest attendance would cally first visits a drinking place, and then feeds and rests before indicate that the eggs had either hatched (chicks leave the nest resuming its incubation duty (De Borbón et al., 1999b; De Juana, with their parents after hatching) or that the nest had failed and the 1997). Young leave the nest soon after hatching (De Juana, 1997). parents deserted it. For each nest visit and triangulation, we Breeding takes place from late spring to late summer, depending recorded the day and time of the visit, the presence of an incubating on the latitude, with clutches being usually laid in MayeAugust and bird, as well as the nest content (for nest visits only). At the end of F. Mougeot et al. / Journal of Arid Environments 102 (2014) 89e97 91

Fig. 1. Photos of a radio-tagged male pin-tailed sandgrouse incubating (top), of a typical sandgrouse nest with three eggs (bottom left) and of the i-button data-logger used in this study (bottom right). the nest monitoring period, we retrieved both data-loggers and when the male returns to replace the female; (De Borbón et al., downloaded the temperature recordings using the Eclo Express- 1999b); (3) a nest disturbance (other than a nest visit or a Thermo software 2007 (www.eclo.pt/expressthermo). triangulation), when the off-bout occurred at a time when we did not visit a nest and when mates do not normally switch incu- 2.4. Analyses of temperature recordings bation roles (i.e. between 1200 and 1700). For some analyses, we only considered two classes of events, and regrouped the nest “ ” Off-bouts were identified by comparing the control and nest visit and other disturbance events into a disturbance event, as “ ” temperatures. Because nest temperature is much more stable than opposed to a mate switch event. ambient temperatures during incubation (Fig. 2a), off-bouts are On some days, temperature recordings showed no visible off- characterized by a sudden change in nest temperature relative to bouts. In such cases, we assumed that a normal mate switch took control data-loggers, which can be easily detected (Fig. 2b). During place, but was too brief to be noticed by a change in nest temper- an off-bout, the nest temperature drops or increases when the ature (it lasted less than 5 min). In such cases, we cannot determine control temperature is lower or higher than the nest temperature, the timing of the mate switch (or the temperature ranges associ- respectively (Fig. 2b). For each identified off-bout, we recorded the ated with it), but we assigned these off-bouts a duration of 5 min following: 1) the nest (pair) identity, 2) the date, 3) the time of the (the maximum possible undetected absence), to avoid a possible off-bout onset (to the nearest 5-min), 4) the duration of the off-bout bias in our estimation of nest absences during mate switches. (in min), 5) the nest and the control temperature at the beginning In order to investigate the associations between sunrise/sunset of the off-bout; and 6) the nest and the control temperature at the times and the timing of morning and evening mate switches, we end of the off-bout. We also calculated the changes (difference) in obtained data on sunset/sunrise times for each day of monitoring in both the nest temperature and the control temperature between each study area from the Astronomical Applications Department, the start and the end of the off-bout (DNTemp and DCTemp for nest U.S. Naval Observatory (www.usno.navy.mil). Times are given as þ and control, respectively). Recordings around hatching were local times (GMT 1). excluded because incubation behaviour becomes irregular after the first egg hatched (Fig. 2c). 2.5. Sample sizes for analyses We classified each off-bout a posteriori into the following three event categories: (1) a nest visit event, when its timing We monitored with data-loggers a total of 14 pin-tailed sand- coincided with one of our visits to that particular nest (none of grouse nests (11 in Ciudad Real and 3 in Bardenas Reales) and one the 16 triangulations made to check for the presence of a tagged black-bellied sandgrouse nest (in Bardenas Reales). Out of 11 pin- bird at a nest resulted in an off-bout); (2) a mate switch event, tailed sandgrouse nests monitored in Ciudad Real, only 7 gave when the off-bout occurred at a time when mates normally useful temperature recording data for analyses (the others failed switch incubation roles, i.e. between 0600 and 1200: when the too soon after set-up). We thus had useful temperature recordings female returns to replace the male, or between 1700 and 2200, from 10 pin-tailed sandgrouse nests and one black-bellied 92 F. Mougeot et al. / Journal of Arid Environments 102 (2014) 89e97

Table 1 Summary data for the sandgrouse nests used in the temperature-based monitoring study.

Species Monitoring start Monitoring end Days incubated Nest visitsa Triang.b Fate

P. alchata 03/06 at 1830 16/06 at 1930 11 4 0 Failed 14/6/2011 at 0934. Eggs predated P. alchata 13/06 at 1050 20/06 at 2100 7 3 0 Failed 20/06/2011 at 2100. Empty nest P. alchata 13/07 at 2100 18/07 at 1330 4 1 1 Failed 17/7/2011 at 0929. Eggs predated P. alchata 14/07 at 1815 19/07 at 1800 6 1 0 Hatched, after data-logger removal P. alchata 05/07 at 1020 20/07 at 1220 15 3 6 Hatched 19/7/2011 e leave the nest at c.0900 P. alchata 13/07 at 2130 21/07 at 1910 5c 1 3 Failed 19/7/2011 at 0923. Eggs predated P. alchata 17/06 at 0934 21/06 at 1930 2 1 0 Hatched 18/06/2011 e leave nest at c.0800 P. alchata 25/7 at 1800 1/8 at 0800 1 1 0 Failed 27/7/2011 at 0800. Empty nest P. alchata 15/7 at 0800 21/7 at 1200 3 1 0 Failed 17/7/2011 at 2244. Empty nest P. alchata 19/07 at 0900 01/08 at 1915 9d 1 6 Failed 28/7/2011 at 0447. Empty nest P. orientalis 18/7 at 0859 3/8 at 0900 14 1 0 Hatched 31/07/2011 e leave nest at c.1000

a Including the nest visit for data-logger set-up. b During a triangulation, the nest is not visited but the presence of a radio-tagged bird at the nest is confirmed from a distance. c The nest monitoring started when the female had just laid the last egg of a clutch of 3. The nest was not incubated at night (by the male) during the first night (laying being not complete) but the male incubated on the following nights; the female incubated all days. d The nest monitoring started when the female was still laying eggs. The nest was not incubated at night (by the male) during the first 4 nights (the male most likely waited until laying was complete to start), but incubated on the following nights; the female incubated all days.

Nest temperature Off-bouts Control Temperature

60 a

50

40

30 Temperature 20

10 Time

b off-bout 1 off-bout 2 c off-bout 1 off-bout 2 Hatching 60 50

50

40 40

30 Temperature 30 Temperature

20 20

Time Time

Fig. 2. Times series of temperature recordings (in C) of the control (dashed black line) and nest (solid red line) data-loggers obtained (a) during a 15-days monitoring pin-tailed sandgrouse nest; (b) for a particular day showing two off-bouts (absences from the nest, highlighted with vertical grey bars); and (c) for the last two days of nest-attendance, with hatching on the second day. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

sandgrouse nest, covering incubation periods that ranged between sandgrouse nests in Ciudad Real, in which we did not set-up 1 and 15 days (Table 1). We only analysed statistically the data from data-loggers, during the same breeding season (MayeAugust 2011). pin-tailed sandgrouse nests, and report on the data obtained from the black-bellied sandgrouse nest for descriptive and comparative 2.6. Statistics purposes. In order to compare the fate of nests with and without data We analysed the data from the monitored pin-tailed sandgrouse loggers, we also monitored the breeding of another 18 pin-tailed nests using Generalized Linear Mixed Models (GLMM), which F. Mougeot et al. / Journal of Arid Environments 102 (2014) 89e97 93

Nest temperature Control temperature Off-bouts 0,8 a 60 0,7 y

0,6 50 robabilit

0,5 p

40 0,4

Temperature 30 0,3

0,2 20 Off-bout occurrence 0,1

10 0,0 00:00 02:00 04:00 06:00 08:00 10:00 12:00 14:00 16:00 18:00 20:00 22:00 00:00 Time

0,8 b 0,7 y

40 0,6 robabilit

0,5 p

30 0,4

Temperature 0,3

20 0,2 Off-bout occurrence 0,1

10 0,0 00:00 02:00 04:00 06:00 08:00 10:00 12:00 14:00 16:00 18:00 20:00 22:00 00:00 Time

Fig. 3. Mean (SD) daily temperature variations for the control (blue line and bars) and the nest (red line and bars) data-loggers, and mean (SD) probability of off-bout (absence from the nest) occurrence associated with a mate switch (black histograms and bars). (a) Data from 10 pin-tailed sandgrouse nests; (b) data from one black-bellied sandgrouse nest (see Table 1). (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.) included “nest identity” as a random variable (in order to take into between pair variation. Repeatability indicates how strong the in- account that data from the same nest were not independent). dividual consistency in a trait is in the population (the proportion of Dependent variables (time and duration of off-bouts, change in nest behaviour variation explained by the variation among individuals). temperature during off-bouts) were fitted to models using a normal We calculated both “repeatability” and “adjusted repeatability” (i.e. error distribution and an identity link function. repeatability after accounting for other variables such as sunset or We first tested whether the duration of an off-bout differed sunrise time), as the ratio “between-individual variance/residual between daytime periods (morning vs evening) and between event (within-individual) variance” from the null models or the models types (nest visit vs disturbance vs mate switch) using GLMMs that with covariates, respectively (see Nakagawa and Schielzeth, 2010). included these variables and their interaction as explanatory To investigate factors influencing the changes in nest tempera- variables. ture during an off-bout (DNTemp), we used GLMMs that included We estimated the repeatability of the timing and duration of the the type of event (disturbance vs mate switch), duration of the off- off-bouts associated with mate switches by comparing within- and bout, and the change in the control temperature during the off-bout 94 F. Mougeot et al. / Journal of Arid Environments 102 (2014) 89e97

(DCTemp), as well as the interactions between these factors. Initial In the black-bellied sandgrouse, detected mate changes took models also included the factor daytime period, but this variable place between 08:00 and 10:00 and between 20:00 and 21:00 was highly related to DCTemp and not retained in final models. (Fig. 3b). As for the pin-tailed sandgrouse, the timing of mate Finally, we analysed factors modulating off-bout duration using changes occurred at times when the control and nest temperatures GLMMs that included the control temperature at the onset of the were similar (Fig. 3b). off-bout, the type of event, and their interaction. Data are expressed as means SD and tests are two-tailed. We used SAS 9.2 (SAS, 2012) for all analyses. 3.3. Consistency in the timing and duration of mate switches

In the pin-tailed sandgrouse, the timing of morning switches 3. Results was unrelated to sunrise time (F1,37 ¼ 0.27; P ¼ 0.608), while the timing of evening switches positively correlated with sunset time 3.1. Off-bouts characterization and duration (F1,36 ¼ 4.99; P ¼ 0.032). In JuneeJuly, morning mate switches occurred on average 3 h after sunrise, and evening switches 7 min Control temperatures greatly fluctuated daily while nest tem- before sunset. The time at which mate switches occurred in the peratures showed dampened fluctuations when a nest was nor- morning was less variable within-pairs than between pairs and had mally incubated (Fig. 2a,b). When a nest was deserted (either a high repeatability value (R ¼ 0.61). A similarly high repeatability because it hatched or failed), nest and control temperature became value was obtained when including sunrise time as a covariate similar, so the monitoring allowed to determine precisely the (R ¼ 0.63). The time of evening mate switches was also repeatable timing of hatching or breeding failure (Fig. 2c; Table 1). (R ¼ 0.45), but less than that of morning switches. Controlling for For the pin-tailed sandgrouse (n ¼ 10 nests), we identified a sunset time gave a similar repeatability value (R ¼ 0.44). In contrast, total of 97 off-bouts, which lasted on average 30.3 25.3 min the duration of off-bouts was not repeatable (R-values of 0.06 and (range 10e165). Most off-bouts were associated with putative mate 0.24 for morning and evening off-bouts, respectively). switches (n ¼ 71), followed by nest visits (n ¼ 17) and other pu- tative disturbances (n ¼ 9). Off-bouts caused by nest visits lasted on average 46.6 34.1 min 3.4. Off-bouts and changes in nest temperature (range 10e140), and those caused by other disturbances lasted 50.6 46.9 min (range 10e165). Off-bouts associated with mate In the pin-tailed sandgrouse, changes in nest temperature dur- switches lasted on average 23.8 14.2 min (range 10e85, n ¼ 71). ing off-bouts depended on the duration of the absence (F ¼ 5.58; However, if we include mate switches that were too short to result 1,85 P ¼ 0.020) and the change in control temperature (DCTemp) in in an off-bout detectable by a change in nest temperature over a interaction with type of event (DCTemp: F ¼ 32.94; P < 0.001; 5 min period (c.25% of all switches), off-bouts lasted 19.0 14.8 min 1,85 Event: F ¼ 5.58; P ¼ 0.020; DCTemp Event: F ¼ 5.46; (range 5e85; n ¼ 95). 1,85 1,85 P ¼ 0.022). The shorter the absence from the nest, the less the nest Overall, off-bouts associated with disturbance events (nest visits temperature changed during the off-bout (duration effect: and other disturbances combined) were significantly longer than slope se: þ0.023 0.009). In addition, changes in nest tempera- those associated with mate switches (Mixed model: F ¼ 20.84; 1,86 ture were positively correlated with change in control tempera- P < 0.001). In addition, off-bout duration depended on the time tures, with a steeper slope during disturbance events period (morning versus evening) in interaction with the type of (slope se: þ0.426 0.099) as compared with mate switch events event (Time period Event: F ¼ 4.38; P ¼ 0.040). In the morn- 1,84 (slope se: þ0.201 0.056; Fig. 4). ing, off-bouts related to mate switches lasted 26.4 4.2 min (n ¼ 48), and those related to disturbances 59.9 6.2 min (n ¼ 14; Event effect: F ¼ 13.99; P < 0.001). In the evening, off-bouts 1,38 3.5. Modulation of off-bout duration related to mate switches lasted 22.5 4.1 min (n ¼ 47) and those related to disturbances 34.2 7.0 min (n ¼ 12; Event effect: In the pin-tailed sandgrouse, off-bout duration depended on the F ¼ 5.48; P ¼ 0.024). 1,39 type of event, the control temperature at the start of the off-bout For the black-bellied sandgrouse (n ¼ 1 nest), we identified 18 (CTemp), and their interaction (CTemp: F ¼ 21.87; P < 0.001; off-bouts, which lasted on average 31.9 16.8 min (range 10e60). 1,86 Event: F ¼ 23.70; P < 0.001; CTemp Event: F ¼ 13.20; All off-bouts were associated with putative mate switches (the nest 1,86 1,86 P < 0.001; Fig. 5). During mate switch events, off-bout duration was was not visited after data-logger set-up until after the young unrelated to control temperature (F ¼ 1.39; P ¼ 0.242; hatched, and we had no evidence of disturbances during incuba- 1,63 slope se: 0.279 0.236). In contrast, during disturbances, off- tion). If we also consider those mate switches that were too short to bout duration decreased with increasing control temperature result in a detectable off-bout, absences during mate switches were (F ¼ 7.95; P ¼ 0.013; slope se: 2.333 0.828): when a sand- estimated to last 23.0 18.8 min (range 5e60; n ¼ 27). Absences 1,15 grouse was disturbed during high-temperature hours, it returned lasted 26.5 23.12 min (n ¼ 13) and 19.6 13.7 min (n ¼ 14) during more rapidly to its nest to incubate. the morning and evening mate switches, respectively.

3.2. Timing of off-bouts associated with mate switches 3.6. Nest fates

In the pin-tailed sandgrouse, detected mate changes took place The only monitored black-bellied sandgrouse nest successfully between 08:00 and 10:00 and between 19:30 and 21:30 (Fig. 3a). hatched. Out of the 14 pin-tailed sandgrouse nests with tempera- Interestingly, mate switches occurred at a time in the morning ture data-loggers (see Methods and Table 1), 3 (21%) successfully when the control temperature was lower than or nearing the nest hatched and 11 failed. Out of the 18 pin-tailed sandgrouse nests temperature, and in the evening at a time when the control tem- without temperature data-loggers, 3 (17%) successfully hatched perature was similar to or cooler than that of the nest temperature and 15 failed. We therefore had no evidence that nest success rate (Fig. 3a). differed between nests with or without data-loggers. F. Mougeot et al. / Journal of Arid Environments 102 (2014) 89e97 95

Mate change Nest visit / disturbance metabolic demands for clutch formation and egg-water loss (Thomas, 1984). Sandgrouse eggs are also relatively smaller than those of similar-sized species (e.g. Charadriiformes), allowing them 10 to complete their clutch with a low investment of resources (minerals, nutrients and water), which is an advantage in arid and environments (Thomas, 1984). This study is the first, to our knowledge, to use data loggers for studying incubation rhythms by birds in arid environments. In 5 terms of incubation, breeding in arid climates implies that eggs, although protected by parents most of the time, are exposed to large temperature variations, and, in particular, occasionally exposed to very high temperatures. For instance, during the incu- bation of monitored pin-tailed sandgrouse nests, the temperatures 0 recorded at the control data-logger greatly fluctuated, with daily oscillations between a minimum average of c.19 C (between 06:00 and 08:00) and a maximum average of c.55 C (between 14:00 and 17:00; Fig. 3a). In contrast, the temperatures recorded at the nest Change in nest temperature showed dampened oscillations between average temperatures of -5 30 and 39 C(Fig. 3a). Note that these are not directly equivalent to ambient and egg temperatures, respectively, but indicate an average amplitude variation of c.36 C outside the nest, but of only c.9 C at the nest. Incubation by both sexes (by the female during -20-100 10203040the day and by the male at night) therefore prevents an exposition Change in control temperature of eggs to critically high temperatures during daytime, or to an excessive cooling of eggs at night, respectively. Since the eggs are Fig. 4. Relationship between the change in nest temperature during an off-bout and on the ground, soil-surface temperatures are critical for sandgrouse the change in control temperature over the same period according to the type of event nesting success. For example, when temperatures are particularly (mate switches events: white dots; nest visits/other disturbances: black dots). high, incubating (Pterocles namaqua) raise their body, and face the wind to allow a convective cooling of eggs (McLean, 1995). If soil temperatures are too high (>55 C), incu- 4. Discussion bating birds are unable to regulate effectively nest temperature and the embryos do not survive (McLean,1995; Webb, 1987). Deviations 4.1. Sandgrouse incubation rhythms from the normal nest incubation temperatures, if prolonged in time, may provoke egg desiccation and threaten the embryo’s Sandgrouse are particularly well adapted to cope with arid en- viability (McLean, 1995). During some absences from the nest vironments, and with extreme temperature variations (Johnsgard, associated with disturbances, we recorded changes in nest tem- 1991; Thomas, 1984; Thomas and Maclean, 1981). These adapta- peratures of up to 10 C above the normal nest temperatures tions include a specialized reproductive biology, reducing the (Fig. 4). Absences from the nest during incubation, irrespective of their cause, may therefore be critical for nesting success of these Mate change Nest visit / disturbance species. The combination of a nest and control temperature data-logger 140 allowed us to accurately characterize off-bouts in terms of their timing, duration and temperature context (Fig. 2). A limitation, 120 however, is that their cause was not always known (except when we visited nests). Knowing the biology and incubation routines of 100 these sandgrouse species, we could reasonably well characterize off-bouts that were related to mate switches and incubation reliefs. Both the pin-tailed and the black-bellied sandgrouse exhibited 80 similar incubation rhythms and mate switch times (Fig. 3; De Borbón et al., 1999a,b), which normally occurs during cooler 60 hours after dawn and before dusk, as described in other sandgrouse species (De Borbón et al., 1999b; De Juana, 1997). In the pin-tailed 40 Off-bout duration sandgrouse, the timing of morning mate switches was not tightly related to sunrise time (at least in JuneeJuly, during the course of 20 the study) but was repeatable, indicating that each pair had its routine for morning incubation reliefs. In the evening, mate 0 switches correlated with sunset time and appeared more syn- chronous between pairs, possibly because the window of optimal thermal conditions for a mate switch is more constrained than in 15 20 25 30 35 40 45 50 55 the morning. A similar relief pattern was documented in the namaqua sandgrouse, with variation in evening switch times Control temperature related to sunset throughout the breeding season (Lloyd et al., 2001). Longer absences associated with mate switches may thus Fig. 5. Relationship between the duration of an off-bout and the control temperature at the start of the off-bout according to the type of event (mate switches events: white correspond to cases in which male or female leave the nest before dots; nest visits/other disturbances: black dots). the return of its mate, as reported to occur sometimes in the pin- 96 F. Mougeot et al. / Journal of Arid Environments 102 (2014) 89e97 tailed sandgrouse species (De Borbón et al., 1999a; Benítez-López, after abandonment) may not be always possible without checking personal obs.). the nest content after failure. If a failed nest contains un-hatched Interestingly, we found that in both studied species the timing of (cold) eggs, abandonment is likely. Broken eggshells may indicate mate switches occurred when the differences between the nest and , their inspection may precise avian versus pre- control temperatures were typically minimal (Fig. 3). On the one dation, and the timing of nest failure indicate if it was by a diurnal hand, this may reduce our ability to detect such off-bouts using the or nocturnal predator. If a nest is found empty, however, the cause temperature data-loggers (when nest and control temperatures are of failure could be predation or abandonment followed by preda- similar, off-bouts are less noticeable). Indeed, c.25% of mate tion (De Borbón et al., 1999a,b; De Juana, 1997). switches that must have occurred, given the normal incubation Nesting success was overall low in the pin-tailed sandgrouse, routine of sandgrouse, were not detected, either because they were with no evidence that setting up data-loggers at nests affected too short (<5 min), or because they happened precisely at a time success during incubation (21% and 17% of nests with and without when nest and control temperature were identical. On the other temperature data-loggers successfully hatched, respectively), as in hand, this indicates that the timing of these mate switches is other studies (e.g. Cervencl et al., 2011). Similar low nesting success adaptive, in order to maintain the clutch within an optimal tem- has been previously reported for pin-tailed and black-bellied perature range. The changes in nest temperature recorded during sandgrouse (10% and 25%, respectively; De Borbón et al., 1999a,b), the off-bout associated with mate switches were mostly tempera- for namaqua sandgrouse (7e15%; Lloyd et al., 2000) and for yellow- ture decreases (range 0 to 5 C) and very rarely temperature in- throated sandgrouse Pterocles gutturalis (25%; Tarboton et al., 1999). creases (see Fig. 4). This indicates that during a mate switch, Low productivities likely contribute to the vulnerable conservation sandgrouse are more willing to risk a cooling rather than a warming status and population declines observed in some sandgrouse spe- of their clutch. While a cooling of eggs may slow down the em- cies. Predation is considered a main cause of failure (De Borbón bryo’s development, and have consequences in terms of duration of et al., 1999a; Lloyd, 2004; Lloyd et al., 2000; Tarboton et al., incubation, an overheating might be more critical for the embryo’s 1999). However, nest abandonment or predation following distur- viability (Grant, 1982; McLean, 1995; Webb, 1987). bances could also be a significant cause of nesting failure. Sandgrouse are characterized by highly synchronized early Sandgrouse may be particularly sensitive to human distur- morning and late afternoon arrivals to drinking points during bances during incubation. Indeed, we found that the duration of breeding season, a behaviour that has been mainly interpreted as a off-bouts was significantly greater when the cause was a nest visit strategy to reduce predation risk or to reduce evaporative water or disturbance as compared with a mate switch. Sandgrouse also loss and save energy (Ward, 1972; Yosef and Zduniak, 2011). Our avoid leaving the nest unattended during the hottest hours of the data indicate that the timing of incubation reliefs, and therefore for day (De Juana, 1997), when the nest temperature can increase travelling to drinking points is constrained by thermal conditions dramatically, even during a short absence. During a disturbance, we (in order to maximize eggs and small chick survival). We suggest found that the incubating bird returned faster to its nests when the that the limited window of optimal thermal conditions for leaving outside temperature was higher (Fig. 5), most likely to prevent an the nest in order to maximize nesting success should also be overheating of the clutch. Also, when incubating parents are considered when explaining the high synchrony in sandgrouse disturbed and leave the nest, the eggs can be exposed to drinking behaviour. “abnormal” variations in temperature that may reduce egg viability or influence the duration of the incubation period. Prolonged in- 4.2. Sandgrouse nest monitoring: usefulness and limitations of cubation periods imply higher predation risk for both eggs and temperature data-loggers adults, and greater energetic costs associated with incubation (Thomson et al., 1998). Therefore, the need for a nest monitoring in By setting up data-loggers upon a unique nest visit, researchers species of arid climates should be carefully evaluated, and if it is can monitor the nest fate and obtain information on breeding considered necessary, carefully planned and timed. phenology without the need of revisiting it again until after hatching. Successful hatching can be detected from temperature 5. Conclusions recordings (e.g. Fig. 2c; low amplitude nest temperature oscilla- tions occur during hatching), and distinguished from breeding This study highlighted some of the constraints that birds failures (abrupt change in nest temperature that quickly equals the breeding in arid environments, such as sandgrouse, face when control temperature). This may be particularly useful in precocial incubating their clutch. It also highlighted the importance of species because nests are sometimes left empty (without egg shell monitoring the potential impacts of nests visits. For monitoring remains) after successful hatching (De Borbón et al., 1999a,b). If purposes, the timing of nests visits should be carefully planned, laying was not complete upon data-logger set-up, this can also be taking into account the temperature context and the birds’ incu- detected. Sandgrouse attend their nest as soon as the first egg is laid bation rhythms, preferentially using the same time windows that (Johnsgard, 1991), but incubation fully starts only after the last egg the birds prefer for mate switches. The use of temperature data- is laid (De Juana, 1997). The male does not incubate until laying is loggers for monitoring sandgrouse nests has provided novel and complete, but the female does, and stays at the nest during the day, useful information in that respect. We suggest that data-logger protecting the egg from the heat and intense solar radiation methods could allow an effective monitoring of other birds (Herranz and Suárez, 1999; Hinsley and Hockey, 1989; Lloyd et al., breeding in similar arid environmental conditions, without risking 2001). For two study nests (see Table 1), the temperature re- an exposure of the clutch to potentially harmful temperatures. cordings clearly showed that the nest was not being incubated at night (by the male) initially, but was attended (by the female) Acknowledgements during the day, and our nest monitoring (visits) confirmed that in both cases, the data-loggers were set-up before laying was This study was funded by the Spanish “Ministerio de Educacion complete. y Ciencia” (project CGL2008-04282/BOS and intramural GranGanga Temperature data-loggers allow determining precisely when a grant to FM) and the “Comunidad de las Bardenas Reales de Nav- nest fails (Table 1). A limitation, however, is that distinguishing arra” (project UCTR110053). FC was supported by a JAE-Doc grant between causes of failure (abandonment, predation, or a predation (“Junta para la Ampliación de Estudios”, European Social Fund). F. Mougeot et al. / Journal of Arid Environments 102 (2014) 89e97 97

This study also contributes to Steppe-Ahead, a project funded by Lloyd, P., 2004. Variation in nest predation among arid-zone birds. Ostrich 75, 228e the FGCSIC. We thank: Alejandro Urmeneta and Sergio Gonzalez for 235. Lloyd, P., Little, R.M., Crowe, T.M., 2000. Investigator effects on the nesting success their help with the fieldwork and logistics in Bardenas Reales; of arid-zone birds. Journal of Field Ornithology 71, 227e235. María Calero-Riestra for sharing ideas about study design; Julien Lloyd, P., Little, R.M., Crowe, T.M., 2001. The breeding biology of the namaqua e Terraube, Fernando Alda and Xurxo Piñeiro for help with captures; sandgrouse, Pterocles namaqua. Ostrich 72, 169 178. Marchant, S., 1961. Observations on the breeding of the sandgrouse Pterodes alchata and Carlos Martín for comments on an earlier version. Individual and senegallus. 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