Ben-Gurion University of the Negev

Jacob Blaustein Institutes for Desert Research

Albert Katz International School for Desert Studies

Foraging ecology, body temperature patterns and space use

characteristics of the Nubian Nightjar, Caprimulgus nubicus, in

Israel

Thesis submitted in partial fulfillment of the requirements for the degree of "Master of

Science"

By: Yoav Perlman

June 2007

Ben-Gurion University of the Negev

Jacob Blaustein Institutes for Desert Research

Albert Katz International School for Desert Studies

Foraging ecology, body temperature patterns and space use

characteristics of the Nubian Nightjar, Caprimulgus nubicus, in

Israel

Thesis submitted in partial fulfillment of the requirements for the degree of "Master of

Science"

By: Yoav Perlman

Under the Supervision of Prof. David Saltz and Prof. Berry Pinshow

Mitrani Department of Desert Ecology, Jacob Blaustein Institutes for Desert

Research, Ben Gurion University of the Negev.

Author’s Signature ...... Date ......

Approved by the Supervisor...... Date ......

Approved by the Director of the School ...... Date ...... 3

Foraging ecology, body temperature patterns and space use characteristics of the

Nubian Nightjar Caprimulgus nubicus in Israel

______

Yoav Perlman

Thesis submitted in partial fulfillment of the requirements for the degree of "Master of

Science"

Albert Katz International School for Desert Studies, Jacob Blaustein Institutes for

Desert Research, Ben-Gurion University of the Negev.

June 2007

ABSTRACT

Nightjars are the only nocturnal, aerial, insectivorous taxon of birds that

locates its prey visually. As such, they are subject to substantial predation risk while

foraging in periods of the night with relatively strong light intensity. Further,

nightjars are small endotherms that often use facultative hypothermia in order to

reduce energy costs during periods of low ambient air temperatures (Ta), or food shortage. The Nubian Nightjar (Caprimulgus nubicus, Lichtenstein, 1823) is a small nightjar (46 - 61 g) that breeds locally in southern Israel and the Israeli population is at serious risk of extinction. The goal of my research was to study the temporal and spatial activity patterns and body temperature variation, and their interactions, in the

Nubian Nightjar, by exploring the direct and indirect effects of several environmental variables on these patterns, including Ta, light intensity and potential prey availability.

From 2004 to 2006, I tracked seven Nubian Nightjars fitted with radio tags for a total

of 73 nights in the Kikar Sdom region of southern Israel. I found that Nubian 4

Nightjars foraged more during periods of the night with stronger light intensity. I also found that they probably trade-off safety with foraging efficiency by using periods with crepuscular sunlight (after dusk and before dawn) on nights with no moon, but avoid foraging at these hours when moonlight is strong. I also found that Nubian

Nightjars forage during periods when noctuid moth activity peaks. Nubian Nightjars use facultative hypothermia regularly, and do so more on cold nights, and on nights when light intensity is low, when foraging opportunities are limited. This is the first reported indication that light intensity might act as a cue for entry into torpor by a bird. Finally, I found that Nubian Nightjars have relatively small home ranges, which include patches of salt marsh which they use almost exclusively for roosting and breeding, and forage mainly in open habitats, including agricultural fields. In designing a conservation scheme for this species in Israel, habitat structure, protection of water sources and light pollution must be taken into account.

ACKNOWLEDGEMENTS

I thank Arnon Tsairi, who first introduced me to the Nubian Nightjars at Ne’ot

Hakikar, motivated me to begin with the research and helped me hugely in the field with his intimate knowledge of the nightjars. I thank both my advisors, Profs. David

Saltz and Berry Pinshow, for their patience and trust during all the stages of this work.

Their valuable suggestions and remarks during the research improved it greatly. I thank Dan Alon, director of the Israeli Ornithological Center for financial support to this project and for use of equipment. I’d like to thank all the people who helped me with the strenuous fieldwork: Yair Dalbar, Zeev Shahar, Gal Abdu, Ido Tsurim,

Michał Wojciechowski, Rami Mizrahi, Dubi Shapiro, Sameh Darawshe, Amir

Balaban, Yoni and Lior Belmaker, Gidon Perlman, and Uri Makover. Amir Balaban 5 helped in filming the nightjar behavior in the field. My thanks go also to Nir Sapir and Ido Tsurim for their help in data analysis. Dr. Amos Bouskila and Haim Berger helped much with the telemetry work and equipment. Special thanks to Michał

Wojciechowski, Shai Daniel, Niv Palgi and Carmi Korine who provided important help with the body temperature work. Thanks to Dr. Andrew McKechnie for granting me permission to use his energetic benefit model. I thank the residents of Neot

Hakikar and Ein Tamar for allowing me access to their fields (and often houses too).

Their hospitality and flexibility permitted this work to be done. Special thanks go to

Ehud Tsairi, resident of Neot Hakikar and father of Arnon, who helped me much with supplying equipment and introducing me to his fellow farmers, and made my work much easier. I thank Harel Ben Shahar of the Nature and Parks Authority for his invaluable support and help to the project. Thanks also the Caracal unit of the Israel

Defense Forces, for permitting my stay in such a sensitive area at night. Thanks to

Ami Maduel from the Jewish National Fund research station at Ein Tamar for the use of the meteorological data he recorded for the Israel Meteorological Service. Special thanks to Vasiliy Kravchenko of Tel Aviv University for sharing his knowledge and data of moth activity, and to Eran Levin for his help with analysis of nightjar pellets.

My M.Sc. studies were supported by a scholarship of the Albert Katz

International School for Desert Studies Foundation. I also received support from the

Ornithological Society of the Middle East (research grant 3/2006) and from the Gidi

Zakkay fund, for which I am most grateful.

Last, and most importantly, I thank my wife Adva for her endless support, during all stages of the research and my dog Leica for her patient company during the long nights in the field. Without their support this research would not have been possible. 6

TABLE OF CONTENTS

Abstract ...... 3

Acknowledgements ...... 4

Table of contents ...... 6

List of tables and figures ...... 7

Introduction ...... 8

Hypotheses and predictions ...... 13

Methods ...... 14

Study site ...... 14

Nightjar activity and body temperature patterns ...... 15

Environmental conditions ...... 17

Data analysis ...... 18

Results ...... 22

General ...... 22

Foraging activity patterns ...... 23

Body temperature patterns ...... 30

Space use characteristics ...... 34

Discussion ...... 39

Foraging activity patterns ...... 39

Body temperature patterns ...... 41

Space use characteristics ...... 47

Conservation implications ...... 47

References ...... 51

Appendix 1: The food of the Nubian Nightjar ...... 57 7

Appendix 2: Moth activity patterns at Neot Hakikar ...... 58

Appendix 3: Aspects in the natural history of the Nubian Nightjar ...... 60

Appendix 4: World distribution and subspecific structure of the Nubian Nightjar .. 61

Hebrew abstract ...... 63

LIST OF TABLES AND FIGURES

Table 1: monitoring periods and biometrics of seven Nubian Nightjars ...... 23

Table 2: The relationship between light intensity and foraging activity ...... 25

Table 3: Goodness of fit of the regression between light intensity and foraging

activity...... 25

Table 4: The relationship between light intensity, Ta and foraging activity ...... 26

Table 5: circadian patterns of foraging activity ...... 29

Table 6: The relationship between Ta, moon phase and the use of torpor ...... 33

Table 7: Kernel home ranges of six Nubian Nightjars ...... 36

Table 8: Habitat selection analysis for six Nubian Nightjars ...... 37

Table 9: Habitat selection of two habitat types by all nightjars ...... 38

Table 10: Systematic composition of 19 Nubian Nightjar pellets ...... 58

Figure 1: The relationship between light intensity and foraging activity (logistic) ....24

Figure 2: The relationship between light intensity and foraging activity ...... 27

Figure 3: The relationship between moon phase and the time of emergence ...... 28

Figure 4: Circadian patterns of foraging activity ...... 29

Figure 5a to 5e: Frequency distribution of Tskin ...... 31

Figure 6: Skin temperature fluctuations of a single Nubian Nightjar, 23 - 24/3/06 ... 32

Figure 7: The relationship between Ta and the use of torpor ...... 34 8

Figure 8: Home range of a Nubian Nightjar ...... 35

Figure 9: Habitat selection by Nubian Nightjars ...... 39

Figure 10a to 10c: Energetic benefits of the use of torpor ...... 46

Figure 11: Spatial distribution of Nubian Nightjar territories ...... 48

Figure 12: Seasonal activity patterns of noctuid moths at Neot Hakikar ...... 60

INTRODUCTION

To maximize fitness, organisms should be active in space and time in a manner that maximizes the difference between the energy intake and the cost of foraging. Nightjars

(Caprimulgiformes) are the only major group of nocturnal aerial insectivores that locate their prey visually. As such, these birds face unique trade-offs while foraging. On the one hand, light intensity varies at night according to both the circadian and lunar cycles. This might affect both the birds' ability to locate prey by sight and the preys’ activity. On the other hand, some true nightjars (Caprimulgidae) are relatively small (body mass ranging between

35 and 70 g - Holyoak, 2001) and, because many nightjar species are dependent on light to actively locate their prey, they are also vulnerable to predators foraging during periods of the night when light intensity is relatively high (Endler, 1991). Therefore, nightjars face a trade- off between foraging successfully and avoiding predation by potential predators such as owls, foxes and cats.

Several temperate and tropical nightjars, such as the Standard-winged Nightjar

Macrodipteryx longipennis, Long-tailed Nightjar Caprimulgus climacurus and Common

Poorwill Phalaenoptilus nuttallii are highly dependent on nocturnal light to hunt, and do so at twilight or when moonlight is strong (Jetz et al., 2003; Brigham and Barclay, 1992). Mills

(1986) showed that the overall activity of several nightjars was positively linked to the lunar cycle. Nightjars that use nocturnal light to locate their prey are sensitive to a wavelength 9

range similar to the human eye, of about 400 to 700 nm. These species manage to locate

flying insects in dim light by concentrating light in the tapetum lucidum tissue in their eyes, by having many elongated rods, and having a high concentration of cones that contain oil droplets (Lythgoe, 1979; Nicol and Arnott, 1974). Other nightjars, such as the Australian

Owlet Nightjar Aegotheles cristatus tend to forage more on dark nights, when predation risk

is lower, but rather than visually locating their prey, they randomly trap it by flying with their

beaks agape (Brigham and Barclay, 1992; Brigham et al., 1999).

Foraging activity has been well studied in many organisms and was found to vary greatly

over spatial and temporal pattern, depending on resource distribution, energetic benefits from

foraging, and predation risk (for review see Stephens and Krebs, 1986). Patterns of spatial

foraging activity may be affected by the distribution of resources, and by the specific

ecological attributes and responses of the organisms other than for foraging (e.g.

reproduction, risk). Temporal foraging activity patterns may be affected by the temporal

distribution of resources, and by other processes, biotic or physical, occurring on different

temporal scales, such as circadian and lunar cycles. Predation risk may affect activity

patterns on both spatial and temporal scales, and has been found to be one of the most

important factors determining foraging activity of various organisms (Brown et al. 1994).

Thus, the effect of nocturnal light intensity on nightjar activity is not straightforward, and

other factors might also influence their foraging decisions. Consequently, to predict the

response of a nightjar species’ foraging activity to nocturnal light intensity, other

environmental variables that might affect foraging activity, such as air temperature and prey

availability, must be taken into account (Brigham et al., 1999).

Because they are small endothermic animals, ambient temperature (Ta) is expected to

have a significant effect on the nightjars' foraging decisions. Endotherms maintain high body

temperatures (Tb) by endogenous heat production. This has significant ecological advantages 10

because it allows activity in variable and often extreme weather conditions (Prizinger et al.,

1991). In contrast, maintaining high Tb continuously is costly in terms of energy. Mammals

and birds have physiological and behavioral adaptations to reduce energy expenses related to

Tb maintenance, especially in periods with low Ta or short food supply. Small mammals and birds with high surface area to volume ratios often use controlled hypothermia in order to save energy when inactive. The use of controlled hypothermia varies greatly among different species, and can also vary within the same species in response to environmental factors

(McKechnie and Lovegrove, 2002). Controlled hypothermia can vary in expression from (1) minor fluctuations, where Tb drops just below the normothermic Tb range where, as part of

the normal diurnal cycle, when Tb declines by 3 to 4 ºC while the animal sleeps to (2) rest- phase hypothermia, with Tb dropping by ~5 ºC, while the animal remains responsive to

external stimuli. Deeper controlled hypothermia includes torpor, in bouts up to 24 h, with Tb

dropping to 17.4 ºC (McKechnie and Lovegrove, 2002), and hibernation, in multi day bouts

with Tb dropping as low as Ta (see Geiser and Ruff (1995) for review). By allowing their Tb

to drop, with the obligate concomitant reduction in metabolic rate associated with a reduction in heart rate and breathing rate, such animals can save over 50% of their daily energy expenses when Ta is low, and thus alter their energy budget substantially (Willis and

Brigham, 2003; Reinertsen, 1996).

Torpor is normally divided into three discrete phases: 1) entry, where metabolic rate and

Tb decrease below normothermic rest-phase levels, 2) maintenance, where Tb either follows

Ta, or is thermogenically regulated, and 3) rewarming, where Tb returns to normothermic

levels by endogenous heat production and/or exogenous heat sources (McKechnie and Wolf,

submitted).

The distinction between torpor and rest-phase hypothermia is subjective. Some

researchers set robust and definite Tb levels beneath which an animal is torpid, for example 11

25 ºC (Prinzinger et al., 1991) or 30ºC (Reinertsen, 1996), and state that torpor and rest-

phase hypothermia are two distinct physiological responses, mainly due to different

behavioral responses to external stimuli. Animals in torpor show no or little response to

stimuli, while animals in rest-phase hypothermia respond strongly to stimuli (Schleucher,

2004). Other researchers propose that both phenomena are a continuum of the same physiological response, and find no clear distinctions between them.

Despite the controversy around the distinction between rest-phase hypothermia and

torpor (Barclay et al., 2001; McKechnie and Lovegrove, 2002; Willis and Brigham, 2003), it

is clear that the energetic benefit of reducing Tb is greater at shallower levels of hypothermia,

i.e., not dropping body temperature too low. The deeper is the hypothermic bout, the lower

are the energy savings because of the high energetic cost of actively rewarming by increased

thermogenesis, rather than passively rewarming, by exposure to solar radiation and

increasing Ta (Willis and Brigham, 2003).

The use of facultative (controlled) hypothermia in birds is widespread, and was reported

in 29 families representing 11 orders (McKechnie and Lovegrove, 2002). Controlled

hypothermia over daily cycles has been described in several caprimulgids: European Nightjar

Caprimulgus europaeus, the North American Whip-Poor-Will Caprimulgus vociferous,

Common Poorwill Phalaenoptilus nuttallii, and Common Nighthawk Choerdeiles minor, and

Australian Owlet-Nightjar Aegotheles cristatus and Tawny Frogmouth Podargus strigoides

of temperate Australia (Peiponen and Bosley, 1964; Brigham, 1992; Brigham et al., 2000;

Fletcher et al., 2004; Körtner et al., 2001; Lane et al., 2004). The Common Poorwill is unique as it is the only avian species known to hibernate, entering multi-day torpor bouts with Tb reduced to 5 ºC for weeks or even months (Jaeger, 1948; Woods and Brigham, 2004).

Several variables were shown to affect the predisposition of endothermic animals to enter

hypothermia, including air temperature, food availability, and the use of controlled 12 hypothermia is usually linked to energy shortages (e.g. McKechnie and Lovegrove, 2002).

The use of hypothermia as a means to save energy by endotherms imposes disadvantages.

First, it reduces vigilance and the ability to avoid threats, and second, elevating Tb back to the level required to be active is energetically expensive. Some birds can use ambient heat sources to passively rewarm to activity-level Tb, but most use metabolically generated heat to warm up after hypothermic bouts (McKechnie and Lovegrove, 2002; Willis and Brigham,

2003).

The Nubian Nightjar (Caprimulgus nubicus, Lichtenstein, 1823) is the smallest nightjar species in Israel, with a body mass of 46 - 61 g (Holyoak, 2001; this study). It is an aerial insectivore, with nocturnal or crepuscular habits. As most other Caprimulgids, it feeds mainly on medium sized moths and other flying insects such as beetles, grasshoppers and mantids, which it catches on the wing (Shirihai, 1996; Cleere, 1999; Jackson, 2000; Holyoak,

2001). A summary of the subspecies of the Nubian Nightjar and notes about its world distribution are in appendix 4.

In Israel, Nubian Nightjars bred until the late 1980’s, locally, but in relatively large numbers, along the Rift Valley from the Bet She’an valley in the north to Eilat in the south.

Breeding was mainly in salt marshes dominated by Tamarix and Suedea bushes, often near natural water sources such as springs and streams in oases.

Since the late 1980’s a sharp decline in numbers of Nubian Nightjars in Israel was noted; only 5-7 pairs were found in national censuses conducted in 2000 and 2003 in the region of

Ne'ot Hakikar, south of the Dead Sea (H. Shirihai, unpublished data). Speculations as to the possible causes for this decline include habitat loss, pesticide use, and road kills. One of the main reasons for the loss of breeding habitat is the recent development in greenhouse agriculture along the rift valley (these cover very large areas that were degraded, replacing the natural vegetation), and the excessive use of the natural water sources for agriculture, 13

eliminating the original freshwater springs in oases (Shirihai, 1996; Alon and Mayrose,

2003). Very little is known about the activity patterns, habitat preference, home range and

other aspects of the life history of Nubian nightjars. As Nubian Nightjars are critically

endangered in Israel, the knowledge I acquired may well become useful in the future, when

deciding on conservation measures for this species.

Hypothesis and predictions

The goal of my research was to study the interactions between temporal and

spatial activity patterns and body temperature variation in the Nubian Nightjar by

exploring the direct and indirect effects of several environmental variables on these

patterns. I hypothesized that the temporal activity patterns of Nubian Nightjars reflect

potential prey availability, nocturnal light intensity, and air temperature (Ta). I further

hypothesized that nightjars will focus their activity towards periods that are warmer, with relatively high night-time light intensity and potential prey abundance, and that

Ta, nocturnal light intensity, and prey availability influence the nightjars’ tendency to

use facultative hypothermia as an energy saving mechanism.

As the Nubian nightjar is a visually orienting predator, it needs a certain minimum level

of nocturnal light in order to locate its prey. Thus, based on my hypotheses, I predicted that

Nubian Nightjars have higher foraging activity during periods when nocturnal light intensity

is higher – at dusk and dawn, and during periods of the night with strong moon light. I also

predicted that potential prey availability affects the foraging activity of the Nightjars.

Medium sized moths, which are the main prey of nightjars, have annual peaks of activity in

spring and autumn, and a daily peak at dusk (Kravchenko, unpublished data; Wolda, 1988;

Intachant et al., 2001; Meyer et al., 2004; see appendix 2). In view of the above, I predicted 14

that Nubian Nightjars would show higher foraging activity when potential prey availability is

high, on a circadian scale at dusk, and on a seasonal scale in spring and summer.

If Nubian Nightjars use facultative hypothermia as an energy-saving mechanism then it

should be affected by Ta. Therefore, I also predicted that in periods when both Ta and prey availability are low, nightjars will use hypothermia when inactive. On a circadian scale, I predicted that nightjars use hypothermia when at rest after the dusk feeding bout ends and before dawn, when Ta is low and potential prey availability decreases. On a seasonal scale, I

predicted that the nightjars use hypothermia in winter and early spring, when Ta is lowest,

and prey availability is also low.

METHODS

Study site

The study was done in the area called Kikar Sdom, south of the Dead Sea (30º57’

N, 35º23’ E), near the settlements of Ne’ot Hakikar and Ein Tamar, at an elevation of

about 350 m below sea level. The climate at Kikar Sdom is hot and dry. Average

annual rainfall is of 40 mm, occurs only during winter, and is highly variable.

Daytime air temperatures are high in summer, often exceeding 40 ºC; winter

minimum nighttime air temperatures are relatively low, often below 10 ºC (Jaffe,

1988).

Until the 1980’s, the whole area was covered by salt marsh, dominated by

Tamarix and Suedea bushes. The shallow underground water table created several

scattered springs and oases producing brackish water that supports marshy habitats.

However, since the 1980’s agricultural development altered the ecosystem structure,

creating a mosaic of agricultural fields, most covered by plastic greenhouses; only

small, isolated patches of natural scrub remaining (Alon and Mayrose, 2003). Some 15 of these patches still hold pairs of Nubian Nightjars. To the east of Ne’ot Hakikar, on the Jordanian side of Wadi Arava, large areas of salt marshes remain uncultivated.

Monitoring nightjar activity and body temperature patterns

I trapped Seven Nubian Nightjars between August 2004 and July 2006 using mist nets, or a hoop net after spotlighting a bird sitting on a gravel road. Each nightjar was fitted with a 0.6 g or 1.5 g temperature-sensitive radio transmitter (Holohil

Systems®, Ontario, Canada), and was banded with a standard Israeli aluminum bird ring. Length of the closed wing (Stiles and Altshuler, 2004) and tail measurements were taken to ± 0.5 mm and body mass measurements were taken to ± 0.5 g (Pesola ® spring balance, model 41000). All transmitters were calibrated in the laboratory to

± 0.1 °C against a mercury-in-glass thermometer with calibration accuracy traceable to the U.S. National Bureau of Standards. The transmitters were placed in an open stainless steel temperature controlled circulator bath (ThermoHaake DC10 and V26,

Karlsruhe, Germany). Transmitter pulse intervals were measured at seven temperatures (20, 25, 30, 35, 40, 45 and 50 °C), and individual regression equations of pulse interval to temperature were calculated.

Transmitters were attached directly to the interscapular skin of the nightjars using

Skinbond® or a cyanoacrylic glue. Before applying the glue, a 2 × 2 cm skin patch in the interscapular region was plucked and cleaned using 65% alcohol in water. The transmitters were attached to the skin, touching no feathers. After the glue dried, which took 10 – 15 minutes, the mantle feathers were reorganized to fully cover the transmitter before the bird was released. The signal of the transmitters could be received from a distance of 100 to 200 m, depending on the height of the bird above 16

the ground. Rapid changes in the intensity of the signal indicated that the bird was in

flight.

The transmitters measured the skin temperature (Tsk) of the nightjars. Tsk is

correlated with Tb, and is a reliable index thereof in birds as the mantle feathers

provide insulation from ambient cooling of the interscapular region for a temperature

range of over 30 ºC (Willis and Brigham, 2003). I did not calibrate Tsk against Tb, as I

could not obtain a permit for this laboratory-based process.

To track the nightjars in the field I used two receivers, an HR2600 Osprey™

VHF receiver (H.A.B.I.T Research® Victoria, Canada) that has a pulse interval data

logger for recording Tsk, and a model R1000 telemetry receiver (Communications

Specialists Inc., Orange, CA). I used a Biotrack® Linflex 3™ flexible 3-element Yagi

antenna for bearing determination, and an omni-directional Biotrack® model LM150

car mounted antenna.

Nightjar activity was recorded from the birds’ emergence at dusk until they flew

to their diurnal roosts at dawn. Location was noted continuously during the whole

night, using standard triangulation techniques if two observers were present, or by

myself, moving fast from one point to another and obtaining quick fixes. Moving

between points took one or two minutes, and I kept bearings on the nightjar while

driving to know whether it moved or not (White and Garrott, 1990). For each

foraging bout, I recorded the central point for the whole bout. Usually the nightjars

stayed within a small area during each foraging bout. During each bout, I observed

the bird and marked the perch where it stayed most time. If the nightjar moved

significantly, I recorded this as another location. Tsk was recorded every 5 to 10 minutes during the night, from ~1 h before sunset to ~1 h after sunrise. Due to 17

technical problems, I obtained partial records of Tsk during the day for only two individuals, in March - April 2005.

While following the nightjars at night, I tried to be as close to them as possible and, if possible, to maintain visual contact in order to record their location to a resolution of few meters, to note their behavior, and to get a reading of Tb (this

required a strong radio signal). On bright, moonlit nights, it was possible to observe

the nightjars’ activity with binoculars (Leica 10 × 42). On darker nights, I used

military night vision goggles (Adi, Israeli Military Industries). To avoid disturbing

the birds, I kept a minimum of 30 m away from them, and always observed them from

within a car, keeping quiet and dark.

For each nightjar location, habitat type, and the nightjar's activity were recorded.

Activities noted were: resting (when the bird was stationary, inside cover); foraging;

and territorial behavior (calls heard and courtship display seen). Foraging bouts were

easily detected from changes in the intensity of the broadcast radio signal; signal

strength rises rapidly as the nightjar sallies from the ground into the air (White and

Garrott, 1990). Each day, I downloaded the temperature data into an IBM®

Thinkpad™ laptop computer using VHFRCV20 software (H.A.B.I.T. research®,

Ontario, Canada). Permits for trapping and radio tagging were obtained from the

Nature and Parks Authority (permit 2005-6 / 22088).

Monitoring environmental conditions

Air temperature measurements were obtained from a meteorological screen of the

Israel Meteorological Service, located 1 km northeast of Ne’ot Hakikar. Air

temperatures were measured every 20 minutes, to ± 0.1°C. During August 2004 –

June 2006, I used data on the phase of the moon as a proxy for the total amount of 18 light experienced by a nightjar during one night, as this measure reflects both the light intensity reflected by the moon and the duration of the moon appearance during the night. I obtained moon phase values and civil dusk and civil dawn times from the Tel

Aviv University Wise Observatory website (http://wise- obs.tau.ac.il/~eran/Wise/wise_calen.html).

During March – May 2006 only, I used an Onset HOBO® Square-Box light intensity data logger (Bourne, MA) that measures illuminance in units of power per area (lux). This measurement reflects the response curve of human eyes, of wavelengths between 400 and 700 nm. As nightjar eyes have a similar response curve to humans at these wavelengths (Holyoak 2001), I used illuminance as a measure of light intensity. The data logger was placed 2 m above the ground near the nightjars’ activity sites, in locations where no objects blocked its view of the sky.

Light intensity was logged every 15 minutes, from before sunset until after the nightjars returned to their diurnal roost site. Due to technical difficulties, I obtained direct light intensity measurements for the two individuals I tracked from March to

May 2006 only.

Data analysis

Foraging activity patterns

I analyzed the relationship between light intensity and foraging activity by two means. The first analysis was based on the light intensity measurements obtained by the Hobo data logger. I used a logistic regression of activity (with the dependent variable being foraging or not foraging) on light intensity. Then, based on the derived logistic equation, I calculated by reverse regression the light intensity at which activity fell below 5%. In order to show the power of the logistic regression model, I 19

used the Hosmer and Lemeshov goodness of fit index. As mentioned above, light

intensity measurements were obtained for two individuals only. I excluded territorial

activities from this analysis.

For the second analysis, I used moon phase as a proxy for light intensity for each

night, using moon phase data for all the nightjars. In this analysis, moon phase

represents an approximate sum of light experienced by nightjars each night, reflecting

both the lunar light intensity itself, which varies through the night, and the amount of

time in which the moon is above the horizon. I created a general linear model, with

which I examined the relationship of moon phase, Ta, and individual variation on

foraging activity levels of each nightjar. In this analysis, one independent variable was the phase of the moon value for each night, i.e., the illuminated portion of the

moon. This variable ranges from 0 (no moon) to 100 (full moon) (Tel Aviv

University Wise Observatory website). The other independent variable was Ta, for

which I used the average Ta of the coldest hour of each night. To test whether

individuals are different in their responses, I used dummy variables (Zar, 1999). I

added the individual as a variable that takes the values 0 or 1 to indicate the absence

of categorical effects that may be expected to bias the outcome. The dependent

variable was the arcsine transformation of the ratio of foraging time to total night

time, from first indication of activity at dusk (calling, movement) to the last indication

of activity at dawn. I further tested the relationship between moon phase (predictor)

and foraging activity (dependent variable) by removing the effect of Ta and individual

variation (dummy variable) and regressed foraging activity to moon phase.

I examined the relationship between moon phase (predictor) and time of

emergence of the nightjars, measured as time between sunset until their first foraging

bout (dependent variable), by regressing moon phase on emergence time. Further, I 20

examined the daily temporal patterns of nightjar foraging by dividing each night into

three parts - the first hour after civil dusk (solar azimuth = -6 º), the night (the period

between one hour after civil dusk and one hour before civil dawn), and the last hour

before civil dawn (solar azimuth = -6 º). The dependent variable was the fraction of

foraging time of the whole period. I used three t-tests for two independent samples to

compare the activity levels between three periods of the night. As the number of

periods is small, and they might not be independent of each other, therefore I used a

Bonferroni correction to adjust the p-values such that α* = α /2n (where n is the number of categories), so the corrected α* = 0.05/6 = 0.008333 and examined whether the derived p-value was still lower than α*.

I further tested the relationship between season and foraging activity by dividing the data into two seasons - spring (March - early May) and summer (June - August)

for four nightjars; one tracked in spring and three in summer. Then, for each nightjar

tracked, I regressed moon phase (predictor) to foraging activity, namely the ratio of

foraging time out of the whole night (dependent variable). Finally I did a t-test, to

compare the intercepts of the above regressions (dependent variable) with season as

independent variable, and weighted the input values using the number of nights I

tracked each nightjar. I then used a t-test to compare the slopes of the above

regressions, with season as independent variable, and weighted the input values using

the number of nights I tracked each nightjar.

Body temperature patterns

Following Barclay et al. (2001), I considered the animals to be torpid if Tsk

dropped 7 °C below the lowest activity Tsk in the dusk foraging bout. In order to examine the relationship among Ta, moon phase and individual variation (predictors) 21

and the use of torpor, I created a multiple regression model. As an index for Ta, I

calculated the average temperature of the coldest hour of the night. In this analysis,

the dependent variable was the arcsine transformation of the proportion of time a nightjar was torpid (as defined above) out of the whole inactivity period of that

specific night.

I further tested the relationship between Ta and the use of torpor, with a Mann-

Whitney U Test. In this analysis, I divided the whole range of Ta measurements

recorded into two groups - low (≤ 15.5 ºC) and high (>15.5 ºC) and used the two

groups as predictors. The dependent variable was, as above, the arcsine

transformation of the proportion of time a nightjar was torpid out of the whole period

at night in which it was inactive.

Space use characteristics

Home ranges of the nightjars were calculated with ArcGIS® software using the

Adaptive Kernel Home range method that describes the use distribution of habitats by

an organism in its home range. This method provides a graphical representation of

how the animal occupies space with isopleths delineating areas in which the animal can be found with a given probability, reflecting the amount of time an animal spends

in each area (Worton, 1989; Seaman and Powell, 1996). To calculate the home range of a nightjar, I used all data points I recorded for it over the whole period I tracked it.

It is worth noting that there is little dependence, if any, between consecutive locations

taken during different foraging bouts, as the nightjars often behaved as central-place

foragers and often returned to their roost sites between switching foraging sites. To

estimate a robust home range, I calculated both 90% and 95% isopleths. The 90%

isopleth gives a good estimate of the home range, with low variance and less 22

statistical bias than the commonly used 95% isopleth (Börger et al. 2006). However,

the 95% isopleth has been commonly used over the last decades for calculating home

ranges and I used this calculation too to allow future comparison with relevant data in

literature.

To examine habitat selection by the nightjars, I first calculated the maximum

home range of the seven birds I tracked using all locations, including extremes and

outliers. I then divided the maximum home ranges into four different habitat types -

salt marsh (for roosting and foraging between the trees and bushes), agricultural

fields, freshwater canals and their banks, and open areas near the edges of the salt

marsh (edge). I did a χ2 test for each nightjar. The observed values were the

proportions of time spent foraging in each habitat type out of the total foraging time I

recorded. For the expected selection, I used the ratio of the area of each habitat type

out of the maximum home range area of each nightjar, multiplied by the total amount

of time spent foraging. To test selection for specific habitat types, I used an

independent sample t-test to compare the average observed and expected values of all

nightjars for each habitat type. Statistical analyses were done with SPSS® 10.0

software. P < 0.05 was chosen as the lowest acceptable level of significance.

RESULTS

General

Between August 2004 and June 2006, I trapped and radio-tagged seven individual Nubian Nightjars (table 1). I tracked each individual from 5 to 15 nights, including only full nights of tracking. Of the seven nightjars I tracked, two were males, two were females, and three could not be identified. Morphological differences between sexes are very slight at most (Cleere, 1999; Holyoak, 2001), but I 23

identified the sex of four birds by their territorial behavior in the field - males were

very vocal, and did courtship displays (see appendix 3). Individuals 2 and 3, and 5

and 6 were pairs occupying the same territories, and were trapped in the same

locations. The other three individuals were trapped in three different locations. All

locations were within a circle of approximately 3 km radius, with some of the

territories being adjacent. All nightjars were released with no apparent harm done

within 30 minutes of being trapped, processed and fitted with radio transmitters.

Table 1: Monitoring periods and biometrics of seven Nubian Nightjars. No. of full

nights stands for the number of nights I tracked an individual and obtained a complete

data set. No. of partial nights stands for nights for which I obtained only partial data.

These nights were excluded from analysis.

Individual Date Sex Length of Body No. of No. of closed mass (g) full nights partial wing nights (mm) 1 August 2004 Unknown 158.5 61 5 2 2 March 2005 Female 149 50 14 4 3 March 2005 Male 156 51 7 3 4 June 2006 Unknown 160 50 10 1 5 March - April Female 153 50 15 0 2006 6 April - May Male 155 48 14 1 2006 7 June 2006 Unknown 154 50 8 0

Foraging activity patterns

Light intensity effects

First, I calculated the light intensity threshold below which the nightjars did

not forage using data from two nightjars that I tracked during March - May 2006, and 24 for which I obtained direct light intensity measurements. For both nightjars, light intensity was significantly and positively correlated with whether they foraged or not

(P = 0.000 and P = 0.012, respectively; Table 2). The Hosmer - Lemeshov goodness of fit index test suggests a significant difference between expected logistic regression curves and the calculated curves (Table 3).

1 y = 1+ e158.8+0.237 x P = 0.000

Figure 1: The relationship between light intensity and foraging activity, with illuminance as an index for light intensity. The black dots note the observed values

(foraging or not foraging) in different levels of illuminance. The black bar represents the logistic regression equation derived from the observed values, predicting probabilities of foraging according to the equation. 25

Table 2: Parameters of the logistic regression used to examine the effect of light intensity on foraging activity in Nubian Nightjars.

Individual df n P 1 1 405 0.000 2 1 160 0.012

Table 3: Goodness of fit for the logistic regression models appearing in table 2 is shown by the Hosmer and Lemeshov goodness of fit index.

Individual Chi-square df P 1 51.01 6 .000 2 57.18 6 .000

For both nightjars, calculation of the illuminance threshold using the derived equation of the logistic regression yielded 0.24 lux.

I created a Multiple Regression model, in order to check the effects of light

2 intensity and Ta on foraging activity. The model itself was highly significant (R =

0.742, sig. = 0.000; table 4). Light intensity was significantly positively correlated with foraging activity, while there was no correlation with Ta.

Table 4: Results of the multiple regression model of foraging activity on light intensity and Ta in Nubian Nightjars. As a proxy for light intensity, I used moon phase. For Ta I used the average Ta of the coldest hour of the night. SS, MS and F are the sum of squares, mean squares and F statistic used for this test.

Source SS df MS F Sig. Corrected 2.845 8 0.356 22.969 0.000 model Intercept 0.127 1 0.127 8.194 0.006 Moon phase 1.393 1 1.393 89.958 0.000 -2 -2 Ta 1.9×e 1 1.9×e 1.227 0.272

When the effect of the other variables was removed, light intensity had a

2 strong correlation with foraging activity (R = 0.611, p = 0.000, see fig. 2), but Ta had no significant correlation with foraging activity, and there were no significant differences between individuals regarding their responses to both other variables.

Figure 2: The relationship between foraging activity index of Nubian Nightjars and effect of light intensity (moon phase). As an index for foraging activity I used the proportion of foraging time out of the whole night. The black line represents the quadratic regression curve which gives the best fit.

The emergence time of nightjars after sunset was positively correlated with moon phase; the more moon light, the later they appeared (ANOVA, df = 1, MS = 680.696,

F = 31.384, R2 = 0.8748, p = 0.000; see fig. 3), and there was no significant difference between individuals in this response. 28

Figure 3: The relation of emergence time after sunset of Nubian nightjars and light intensity index. I used a log transformation of the moon phase as an index for light intensity to get the best fit. The black line represents the linear fit.

Circadian patterns

There was a highly significant difference in levels of activity among the different parts of the night, with the highest activity levels occurring at dusk (Figure

4), the lowest levels during the middle of the night, and medium levels at dawn (Table

5).

Table 5: Circadian patterns of foraging activity in Nubian Nightjars. I divided each night into three periods, and calculated the level of foraging, presented as ratio of foraging out of the total period. t is the t-statistic.

Test pair t df P Dusk - dawn 10.355 6 .000 Dusk - middle 17.33 6 .000 Middle - dawn -9.973 6 .000

1.0

0.8

0.6

0.4 Foraging activity index activity Foraging 0.2

0.0 Dusk Mid Dawn Part of night

Figure 4: Circadian patterns of foraging activity in Nubian Nightjars. Nightjars were significantly more active at dusk and at dawn than in the middle of the night. The black bars indicate the variance above and below the mean.

Seasonal patterns

In order to test for possible differences in foraging activity levels between different seasons, I calculated an average seasonal activity index for each nightjar. I defined two seasons - spring and summer, and divided the data into these two groups, for four nightjars that I tracked in spring, and three that I tracked in summer. I did not find any significant relationship between the season and foraging activity levels.

Body temperature patterns

Nubian Nightjars used nocturnal torpor regularly during March and early

April, when Ta was low at night. All three nightjars tracked during March and early

April used nocturnal torpor on many occasions, with some bouts lasting several hours on dark nights when the nightjars were relatively inactive and when Ta was low

(Figures 5a - 5b, 5d). For instance, during the night of 7-8 March 2006, the nightjar I followed remained torpid for 4 hours and 28 minutes, with its lowest Tsk being 30° C,

11° C below Tsk when active. Another example for the lengthy use of torpor occurred on the night of 23-24 March 2006. On this dark night, the tracked nightjar foraged only after dusk and before dawn, and remained inactive during the rest of the night.

After it became inactive, its Tsk dropped, and it remained torpid for 7 hours and 31 minutes, but the torpor was shallower, with a drop of 8 °C in Tsk. Before dawn, the nightjar raised its Tb and consequently its Tsk, and reached activity Tsk, even though Ta was low at that time. After sunrise, the bird went to roost, and became torpid again, with Tsk dropping to 31°C. When Ta rose later in the morning, Tsk increased as well

(Figure 6). This pattern was consistent; I found that on cold mornings, nightjars often went into torpor after they flew back to their diurnal roosts, and increased their Tsk later in the morning when solar radiation increased. Further, during the few days that 31

I obtained Tsk measurements from nightjars roosting by day, I found no use of torpor, and Tsk remained at normothermic levels. However, the use of torpor differed markedly between individuals, and in summer nightjars never used torpor, even during dark nights (figures 5c and 5e).

Figures 5a to 5e: Frequency distribution of Tsk in Nubian Nightjars. Individuals tracked in early spring (5a and 5d) used torpor regularly, with Tsk dropping to 31 and

30 ºC respectively; individuals tracked later on in the season (5b, 5c and 5e) used torpor less, with Tsk never decreasing below 34 ºC. 32

Figure 6. Skin temperature changes in a single Nubian Nightjar on 23 - 24/3/06. Tsk is the upper dotted line, Ta is the lower one. During this night, the nightjar entered a long torpor bout after foraging at dusk, and remained torpid until before dawn, when it rewarmed and became active again.

To examine the relationship between Ta, moon phase and the use of torpor by

Nubian Nightjars, I did a Multiple Regression test (Table 6). The use of torpor was significantly and negatively correlated with both Ta and moon phase (P = 0.002 and

0.047 respectively), even though one individual out of the seven showed a significantly different response, as it did not use torpor at all, even at low Ta and low moon light.

Table 6: The relationship of the use of torpor by Nubian Nightjars with air temperature (Ta), moon phase and individual variation. For each night, I used the average temperature of the coldest hour of the night, and the log transformation of moon phase to get the best linear fit. MS and F are mean squares and F statistic used for this test.

df MS F Sig. Corrected model 8 0.268 8.322 0.000 Intercept 1 .114 7.360 0.009 Min. Ta 1 .0.410 12.740 0.002 Moon phase 1 .166 3.994 0.047 Individual 6 .127 3.401 .071

To further examine the relationship of Ta alone with the use of torpor, I did a specific test and found that Ta alone had a highly significant relationship with the use of torpor, and nightjars used torpor more often on cold nights (Mann-Whitney U =

89.000, Z = -6.266, P. = 0.000, Figure 7).

Figure 7: The relationship of Ta and the use of torpor in Nubian nightjars. I used the arcsine transformation of the ratio of time the bird was torpid out of the whole resting time of the night as an index for torpidity. I divided the nights to cold (≤ 15 ºC) and warm (> 15 ºC) as a proxy for Ta. Nightjars used torpor significantly more frequently on cold nights. The black bar shows the average use of torpor for each group. Two extreme values are shown for the cold and warm nights each.

Space use characteristics

Home range

I calculated the kernel home range of six nightjars (a representation of one home range is in Figure 8). I excluded the August 2004 bird from the analysis, as I only recorded four nights of data for it. The average home range (90% isopleth) was

7.4 ha (SD = 1.25, n = 6) and 8.43 ha (SD = 1.14, n = 6, 95% isopleth). There was no significant relationship between season and home range size, though home ranges of birds I followed in summer were larger than in spring (Z = -1.852, P = 064; Table 7). 35

Figure 8: 95% isopleth home range of a female Nubian Nightjar at Ne’ot Hakikar during March 2005 (8.4 ha). Each location is marked with a solid yellow circle; the home range is circled with yellow. For each location, use (foraging or roost) and habitat are noted. 36

Table 7: Kernel home ranges of six Nubian Nightjars. For each nightjar, the number

of nights, number of locations and 90% and 95% isopleths are shown.

Individual Period No. No. of locations 90% isopleth 95% of home range (ha) isopleth nights home range (ha) 1 March 14 196 7.8 8.4 2005 2 March- 7 98 6.1 7 April 2005 3 June 2005 10 75 8.8 9.9 4 March - 15 247 7.1 8.2 April 2006 5 April - May 14 222 5.9 7.5 2006 6 June 2006 8 71 8.7 9.6

Habitat selection

Nubian Nightjars roosted only in patches of salt marsh, and their diurnal roost

site selection itself was apparently very conservative; i.e., nightjars tended to roost in

exactly the same spot every day. Two nightjars that I followed, managed to remove

their transmitters before the batteries ran out, and I found the transmitters on the

ground where I flushed each roosting bird. According to the number of fecal pellets

collected, it was clear that each roost had been used for many nights before. The

specific habitat selection of the six nightjars tracked can be seen in Table 8. Five out

of the six nightjars examined showed habitat selection significantly different from the

proportion of each habitat type in their home range. This selection varied amongst

individuals, with several preferences of some individuals contrary to preferences of

other individuals. However, agricultural fields were significantly preferred by all

nightjars, and salt marsh was significantly avoided for foraging by all nightjars (Table

9 and Figure 9). All nightjar territories included some water source, a canal or

marshy area and the birds were often observed foraging near these wet habitats. 37

Table 8: Habitat selection analysis for six Nubian Nightjars. For each nightjar, I

calculated the expected time of foraging by multiplying the proportion of each habitat

type within the individual home range by the total amount of hours the nightjar

foraged during the research period.

Individual Habitat Proportion Observed Expected χ2 P Direction type of habitat hours of hours of of within foraging foraging selection individual home range 1 Salt marsh 0.456 35.18 70.22 10.59 0.014 Avoided

Canal 0.07 10.62 12.32 -

Agriculture 0.32 85.54 49.28 Preferred

Edge 0.144 22.65 22.176 -

2 Salt marsh 0.44 25.31 30.80 8.59 0.035 -

Canal 0.07 0.64 4.90 Avoided

Agriculture 0.36 35.95 25.20 Preferred

Edge 0.13 8.09 9.10 -

3 Salt marsh 0.34 4.30 19.01 9.99 0.019 Avoided

Canal 0.12 0.51 6.72 Avoided

Agriculture 0.45 48.54 25.20 Preferred

Edge 0.09 2.64 5.04 -

Individual Habitat Proportion Observed Expected χ2 P Direction type of habitat hours of hours of of Within foraging foraging selection individual home range 4 Salt marsh 0.38 21.62 62.7 14.82 0.009 Avoided

Canal 0.07 31.26 11.55 Preferred

Agriculture 0.36 101.88 59.4 Preferred

Edge 0.19 10.24 31.35 Avoided

5 Saltmarsh 0.4 16.78 56 6.39 0.094 ns Avoided

Canal 0.1 24.15 14 -

Agriculture 0.39 87.97 54.6 -

Edge 0.11 11.19 15.4 -

6 Saltmarsh 0.36 14.70 23.04 9.34 0.024 -

Canal 0.11 3.5 7.04 -

Agriculture 0.4 45.22 25.6 Preferred

Edge 0.13 0.58 8.32 Avoided

Table 9: Habitat selection between two habitat types by Nubian Nightjars. All six nightjars foraging habitat selection was significantly and positively associated with agricultural fields, and negatively associated with salt marsh. t = t-statistic used in this test.

Habitat type t df P Agriculture 4.917 10 0.001 Salt marsh 3.401 10 0.007 39

Figure 9: Activity time of Nubian nightjars in different habitats. Nubian Nightjars significantly preferred the agricultural fields and avoided the salt marsh for foraging.

Observed selections (the proportion of the amount of time each nightjar spent in the habitat out of the total foraging time) are in dark gray; expected selections (proportion of the habitat type area out of the total home range) are in pale gray. The black diagonal bars show the average selection for all six nightjars for each habitat. All six nightjars positively selected agricultural fields for foraging, and negatively selected salt marsh for foraging.

DISCUSSION

Foraging activity patterns

For caprimulgids, the trade off between safety and foraging is manifested in temporal shifts of activity dictated by light intensity - specifically by avoiding 40 foraging in periods with strong light when prey is abundant but risk is high and dark periods that provide safety but are poor in prey availability (Endler, 1991; Brigham and Barclay, 1992; Jetz et al., 2003). I found evidence for both aspects of this trade- off. First, I found that the foraging activity of Nubian Nightjars is strongly affected by moon light intensity. This is shown by the high positive correlation between moon phase, a general proxy for the sum of moon light experienced by a nightjar each night, and foraging activity (Figure 2). The variation in foraging activity which is similar along the whole range of moon phase suggests that all nightjars I tracked had a similar response to moon phase, and that there is no apparent difference between the different periods of the moon. Further, by directly measuring light intensity during the night, I calculated the illuminance threshold below which nightjars do not normally forage, which is 0.24 lux (figure 1). The poor fit of the logistic regression of foraging activity on illuminance might imply that other variables, possibly Ta and prey availability, might affect this relationship too. Further, there is a clear upper limit of light intensity for foraging, as nightjars do not forage after sunrise or before sunset, perhaps due to high predation risk. This is discussed below too.

Second, Nubian Nightjars apparently rely strongly on crepuscular sunlight for foraging at dusk and dawn, and their foraging activity in the first hour after civil dusk and the last hour before civil dawn is highest, even though moth activity levels are low before dawn. Further, my results support the prediction that the nightjars’ foraging activity is affected by predation risk. This is shown by the late emergence time for their first activity bout at dusk on nights when lunar light intensities are high, and earlier emergence time on dark nights, when lunar light intensities are low (Figure

3), foraging opportunities at night are limited, and in order to obtain sufficient energy from their prey, nightjars need to use the sunlit periods more than on moonlit nights 41 and expose themselves to higher predation risk. However, as mentioned above, foraging does not occur in strong sunlight, only in crepuscular periods and during moonlit periods of the night, in intermediate light levels.

I did not manage to trap nightjars in autumn and winter and fit them with transmitters. Therefore, I could not compare seasonal changes in foraging activity.

However, while attempting to observe and trap nightjars in winter, I noticed that they were present in the area, but were active for very short periods of the night, only at dusk or shortly after. This might be the result of higher Ta after dusk compared to the rest of the night.

My results regarding foraging activity patterns of the Nubian Nightjar fit well with moth activity patterns. This comes in context with an analysis of nightjar fecal pellets I found in diurnal roost sites of two individuals showing that moths comprise some 88% of the Nubian Nightjars’ diet (see appendix 1 for more details). On a circadian cycle, moth activity which is relevant to nightjar foraging activity (when moth flight is low above the ground) peaks about 30 min after sunset, as measured both at Neot Hakikar and Kyrgyzstan (Kravchenko, 1984; Kravchenko, 1986;

Kravchenko, unpublished data), and nightjar foraging activity is highest in this period too. Later on at night, moth activity at low height above the ground usually decreases, and is concentrated higher up (more than tens of meters above the ground,

Kravchenko, 1986), which is much higher than the optimal foraging height of nightjars (Holyoak, 2001; pers. obs.).

On a seasonal cycle, I found high levels of nightjar foraging activity in spring and summer, when moth activity peaks. However, I could not measure the levels of nightjar activity in winter, when I predicted lower foraging activity levels due to lower moth activity (Kravchenko, unpublished data; see Appendix 2). 42

Body temperature patterns

Caprimulgids, as several other taxa of mammals and birds, often use regulated hypothermia to save energy, especially when Ta is low, and/or food is scarce. This type of hypothermia can take the form of a daily cycle, defined as torpor, or multi-day cycles, which is hibernation (i.e. Barclay et al., 2001; McKechnie and Lovegrove,

2002; Willis and Brigham, 2003). The use of torpor in caprumilgids was described mainly for nightjars in temperate zones (i.e. Fletcher et al., 2004; Lane et al., 2004).

I found that Nubian Nightjars use torpor regularly during periods with cold nights, with skin temperature dropping by as much as 11 °C, and torpor bouts of over seven hours. During these cold periods, nightjars often became torpid or used rest- phase hypothermia after they went into their diurnal roost phase, with Tsk decreasing by 5 °C to 8 °C. However, nightjars always increased their Tsk to the normothermic level after short periods of torpor, possibly by using solar radiation as an exogenous heat source for rewarming. I did not record any use of torpor during the day, perhaps as a result of relatively high daytime Ta and normally strong solar radiation during the day, even in early spring. McKechnie and Wolf (submitted) showed that microhabitat selection of a sunny spot versus shaded spot can lead to a significant saving in energy expenditure during diurnal roost, but I could not check whether Nubian Nightjars used passive rewarming after torpid bouts in the early morning.

As in other Caprimulgids, I found that the use of torpor by Nubian Nightjars was significantly correlated with Ta. However, my results do not include the coldest part of the year. In measuring foraging activity levels, I found a significant correlation between nocturnal light intensity and use of torpor as well. From my results, it appears that torpor is not triggered solely by Ta, but also by a potential 43 shortage in prey availability caused by low light intensity levels which alters the birds’ behavior by preventing foraging opportunities.

Energetic benefits of torpor in the Nubian Nightjar

McKechnie and Wolf (submitted) developed a model to calculate the energetic benefits of torpor for endotherms, while taking into account several environmental factors and physiological attributes of the organism. I used this model to calculate the energetic benefit of a Nubian Nightjar for a specific night, 23 - 24/3/06 (Figure 5), in which this nightjar had a long torpor bout and for which the appropriate environmental variables were available.

Torpor metabolic rate (TMR) and resting metabolic rate (RMR) were calculated using values based on several biologically realistic assumptions: 1) that a

Nubian Nightjar of mb = 50 g, goes into torpor for a total duration, DT, of 10 h, divided into DEntry = 3 h, DMaintenance = 5.5 h, and DRewarm = 1.5 h; 2) that the operative environmental temperature (Bakken, 1980), Te = Ta = 15 ºC, which is an average temperature for the torpor period; and 3) that the nightjar roosts on the ground and therefore wind speed is close to zero, and convection is negligible. TNorm (the lowest

Tsk while active) = 40 ºC, TTorp (Tsk while in the observed maintenance phase) = 32 ºC.

Treg (regulated torpor is expected to commence at a slightly lower Ta due to insulation provided by plumage) = 14.8 ºC. C (mass specific heat loss for 50 g bird) = 1.86

J(g⋅h⋅ºC)-1 (Schleucher and Withers, 2001), assuming that heat loss during torpor

(CTorp) equals to heat loss during euthermia (CNorm). s (specific heat of animal tissue)

= 3.43 J(g°⋅C)-1 (Withers, 1992). Basal metabolic rate (BMR) = 558 J⋅h-1, based on the BMR of the Common Poorwill Phalaenoptilus nuttalli, a caprimulgid with a similar mb, which also uses controlled hypothermia regularly (McKechnie and Wolf, 44

2004). I used Q10 (the increase in MR with a temperature change of 10 °C) of 3 that is typical for biological systems, following McKechnie and Wolf (submitted).

Energy expenditure in a euthermic state (Enorm) is based on the calculation of

RMR (equation 1).

−1 −1 (1) RMR = mb × C × ()Tnorm − Ta = 50g ×1.86J (g ⋅ h ⋅°C) × 25°C = 2313.717J ⋅ h

Enorm is calculated by multiplying RMR by total duration of the torpor bout:

−1 (2) Enorm = DT × RMR =10h× 2313.717J ⋅h = 23137.17J

ETorp is the sum of the energy expenditures of all three stages of torpor: entry, maintenance and rewarming.

(3) ETorp = EEntry + Ema int enance + Erewarm

Calculating TMR:

(4) BMR TMR = + C × mb × (Ttorp − 2°C − Ta ) = TNorm −TTorp −2°C ( ) 10 Q10 −1 558J × h −1 = 40°C −(32°C−2°C) + 1.86J (g ⋅ h ⋅ °C) × 50g × ((32°C − 2°C) −15°C) = ( ) 3 10 −1 −1 −1 −1 =186J ⋅ h ⋅ °C + 27.9J (g ⋅ h) =1584.23J ⋅ h

Calculating Eentry:

(5) RMR − TMR E = D (TMR + ) = Entry Entry 2

2313.717Jh −1 −1584.23Jh −1 = 3h(1584.23Jh −1 + ) = 5847J 2

Calculating Emaintenance: −1 (6) EMauntenance = DMa int enance ×TMR = 5.5h ×1584.23J ⋅ h = 8713.265J

Calculating Erewarm: RMR − TMR (7) E = s(T − T )m + D (TMR + ) = rewarm Norm Torp b rewarm 2 = 3.43J ⋅ g −1 ⋅ °C −1 × (40°C − 32°C) × 50g +1.5h × (1584.23J ⋅ h −1 + 2313.717J ⋅ h −1 −1584.23J ⋅ h −1 + ) = 2 = 4295.46J 45

Calculating Etorp:

(8) ETorp = EEntry + Ema int enance + Erewarm = 5847J + 8713.265J + 4295.46J = 18855.73J

Finally, calculating the energetic benefit (EB):

E 18855.27J EB = (1− Torp ) ×100 = (1− ) ×100 = 18.54% ENorm 23137.17J

Thus, the use of the above described torpor bout saved the nightjar about 18% of its energy expenditure for that period. I used the above model to predict the energetic benefits of the use of torpor at different ambient temperatures, and torpor bout durations, which are affected by seasonal and circadian patterns. I found that the expected energetic benefit of the use of torpor decreased as DT decreased, due to the increasing costs of rewarming, and increased as Ttorp decreased. In all cases the energetic benefit increased with Ta until Ta = Ttorp, above which it dropped drastically

(figures 10a to 10c). In other words, in terms of energy alone, it is beneficial to enter torpor as long as Ttorp > Ta.

However, this model gives energetic predictions only on the use of torpor by

Nubian Nightjars, as it does not include several variables that are difficult to assess.

In order to realistically model the benefit of the use of torpor, other variables, such as the cost of the risk of predation, light intensity levels, seasonal prey availability patterns, and breeding cycles should be quantified and used in the model.

My results, along with the model’s predictions, suggest that in the coldest part of the winter, when moth activity is low, the nightjars are active during very short periods of the night, possibly only after dusk when Ta levels are normally the highest of the night, and spend much time in a state of torpor, possibly even during the day when daytime Ta is low too. I predict that even during nights with strong moonlight intensity, the nightjars spend more time torpid and less time foraging than in spring or 46 summer. I hypothesize that the energetic gain from foraging in winter is less than its benefits because of the high metabolic costs of rewarming from torpor to euthermia and the low potential prey availability, and because the perceived cost of predation does not decrease in winter as the nightjars’ potential predators remain active all year round.

Figures 10a to 10c: The relationship between the energetic benefit of the use of torpor and Ta. Figure 10a shows the energetic benefit for bout duration of 10 h, figure

10b shows the energetic benefit for bout duration of 7.5 h, and figure 10c shows the energetic benefit for bout duration of 5 h.

Space use characteristics

The nightjars in my study area preferred foraging in agricultural fields compared to their relative distribution in the total area of their home range. This may 47 be explained by the nightjars’ need for open sky and a clear view to locate flying insects (Holyoak, 2001). On the other hand, nightjars avoided foraging in the salt marsh habitat, perhaps for the same reason - foraging from the ground beneath trees does not allow a clear view of the sky, and prevents successful foraging of flying insects. It is of note that most foraging that did occur in salt marshes took place at the beginning and end of the circadian foraging period, just after emergence at dusk, or just before returning to the diurnal roost at dawn. This is perhaps related to the lower risk of predation between the shelters of bushes in the salt marsh. When sunlight intensity increases, nightjars might become more vulnerable to predation and prefer to forage in sheltered and secluded sites.

No significant selection was found for either habitat, canal and edge, and the time nightjars spent foraging in these habitats was proportional to their availability within the individuals' home range.

Conservation implications

The population of Nubian Nightjars in Israel declined greatly in recent decades, and is threatened. It is regarded as critically endangered. The main cause for this decrease is presumably habitat loss due to agricultural development (Shirihai,

1996; Alon and Mayrose, 2003). During my work in the field, I found 21 territory- holding pairs of Nubian Nightjars (figure 11). This figure might represent an underestimation, as some potential territories were unapproachable, and the true population size might be slightly larger. This is a significant increase compared to the

5 - 7 pairs found by H. Shirihai in 2003, but this is possibly a result of my spending more hours in the field searching for nightjars, rather than a population increase, as 48 the area of salt marsh decreased significantly since 2003 with the expansion of agricultural fields.

Figure 11: Territories of Nubian Nightjars in the Kikar Sdom region. I found 21 territory- holding pairs in the region; each territory is circled in blue. The black line marks the approximate border between Israel and Jordan. The pair marked with a blue arrow held territory in a regenerated area between the two settlements of Neot Hakikar and Ein Tamar.

The salt marsh was cleared in the mid 1990’s, and has regenerated since. 49

From my results, it is evident that the protection of substantial areas of salt marsh habitats in the Kikar Sdom region is important for the survival of the species in Israel. This habitat is used exclusively for breeding and roosting, and its destruction will lead to smaller potential breeding and roosting habitat for the nightjars. Further, the relatively small home ranges of the nightjars mean that even local and small-scale habitat perturbation might lead to disappearance of pairs, and for such a small population a disappearance of even one successful pair might result in a significant risk to the whole population.

It is evident that a full territory should include both patches of salt marsh for breeding and roosting, and other open habitats that are more suitable for foraging, as the nightjars require an open sky for foraging. It appears that they can easily forage in agricultural fields, thus the main problem for their conservation is roosting and breeding habitats, which are exclusively salt marsh, and nearby water sources, which probably have increased local insect density.

Therefore, protecting the open water sources in the Kikar Sdom region is important for the survival of this population. As some nightjar territories were relatively small and isolated within large agricultural areas (size of about 20-30 ha), it is possible that devoting small tracts of land for the regeneration of small patches of salt marsh might create more favorable territories for nightjars.

Another important aspect in the habitat structure of Nubian Nightjars is nocturnal light intensity. I suggest that the nightjars need intermediate levels of nocturnal light intensity, in which they trade-off between foraging efficiency and safety from predators. Nubian

Nightjars were never observed foraging near man-made light sources where the density of moths and other insects is often high (Frank, 1988), even though some nightjar territories in the Neot Hakikar region had man made light sources in them or very near. Thus, it appears that they may be sensitive to ‘light pollution’ caused by high intensity street lights which they might view as high risk of predation areas. Therefore, when designing a conservation 50 plan for the Nubian Nightjar in Israel, it is important that patches of salt marsh with surrounding agricultural fields, which might be occupied by nightjars, will not have any artificial nocturnal light sources in or near them.

As nightjars are highly dependent on noctuid and other small or medium-sized moths for food, there is a great risk to nightjar populations created by the systematic use of pesticides and herbicides that prevent the development of a diverse fauna. The risk for secondary poisoning of Nubian Nightjars through moths seems rather low, as nightjars apparently forage almost exclusively on the wing (Cleere, 1999; Holyoak, 2001). However, the risk of a long-term moth population decline might cause severe damage to the nightjar population too.

Therefore, a reduction in the use of pesticides and herbicides nearby potential nightjar habitats is necessary.

The status of the population in nearby Jordan is unclear. Even though there are only three documented records of Nubian Nightjar in Jordan (Holyoak, 2001), I heard Nubian

Nightjars calling regularly from the Jordanian side of the border, suggesting that there is a healthy population in Jordan, living in the vast saltmarsh that remains in the southern Dead

Sea region. It is probable that there is some interaction between the sub-populations on both sides of the border, creating a larger meta-population, which might explain the survival of such a small population in Kikar Sdom over the last decade or two. A future survey of the

Jordanian population is necessary in order to understand better the whole population dynamics.

REFERENCES

Aebischer, N.J., Robertson, P.A., and Kenward, R.E. (1993). Compositional analysis

of habitat use from animal radio-tracking data. Ecology 74: 1313-1325.

Alon, D., and Mayrose, A. (2003). Avifauna. -In: Dolev, A., and Perevolotzky, A.

(eds.). The Red Book of Vertebrates in Israel. NPA and SPNI publications (in

Hebrew).

Bakken, G.S. (1980). The use of standard operative temperature in the study of

thermal energetics of birds. Physiological Zoology 53: 108-119.

Barclay, R.M.R., Kalcounis, M.C., Crampton, L.H., Stefan, C., Vonhof, M.J., and

Brigham, R.M. (1996). Can external radio transmitters be used to assess body

temperature and torpor in bats? Journal of Mammalogy 77: 1102-1106.

Barclay, R.M.R., Lausen, C.L., and Hollis, L. (2001). What’s hot and what’s not:

defining torpor in free-ranging birds and mammals. Canadian Journal of Zoology

79: 1885-1890.

Börger, L., Franconi, N., De Michele, G., Gantz, A., Meschi, F., Manica, A., Lovari,

S., and Coulson, T. (2006). Effects of sampling regime on the mean and variance

of home range size estimates. Journal of Animal Ecology 75: 1393–1405

Brigham, R.M. (1992). Daily torpor in a free-ranging goatsucker, the Common Poorwill

(Phalaenoptilus nuttallii). Physiological Zoology 65: 457-472.

Brigham, R.M., and Barclay, R.M.R. (1992). Lunar influence on foraging and nesting

activity of common poorwills (Phalaenoptilus nuttallii). The Auk 109: 315-320.

Brigham, R.M., Gutsell, R.C.A., Geiser, F., and Wiacek, R.S. (1999). Foraging Behaviour in

Relation to the Lunar Cycle by Australian Owlet-nightjars Aegotheles cristatus. Emu

99: 253-261. 52

Brigham, R.M., Körtner, G., Maddocks, T.A., and Geiser, F. (2000). Seasonal use of torpor

by free-ranging Australian Owlet-nightjars (Aegotheles cristatus). Physiological and

Biochemical Zoology 73: 613-620.

Brown, J. S., B. P. Kotler and T. J. Valone. 1994. Foraging under predation: a comparison of

energetic and predation costs in communities of Negev and Sonoran Deserts.

Australian Journal of Zoology 42: 435-448.

Cleere, N. (1999). Nubian Nightjar. In: Del Hoyo, J., Elliott, A., and Sargatal, J. (eds.).

Handbook of the Birds of the World. Volume 5: Barn Owls to Hummingbirds. Lynx

Edicions, Barcelona.

Endler, J.A. (1991). Interactions between predator and prey. In: Krebs, J. R. and Davies, N.

B. (eds), Behavioral ecology: an evolutionary approach. Blackwell Scientific

Publications, pp. 169 196.

Fletcher, Q.E., Fisher, R.J., Willis, C.K.R., and Brigham, R.M. (2004). Free-ranging common

nighthawks use torpor. Journal of Thermal Biology 29: 9-14.

Frank, K.D. (1988). Impact of outdoor lighting on moths: an assessment. Journal of the

Lepidopterological Society 42: 63-93.

Geiser, F., and Ruf, T. (1995). Hibernation versus daily torpor in mammals and birds:

physiological variables and classification of torpor patterns. Physiological Zoology 68:

935-966.

Holyoak, D.T. (2001). Nightjars and their Allies. Oxford University Press.

Intachant, J., Holloway, J.D., and Staines, H. (2001). Effects of weather and phenology on

the abundance and diversity of geometrid moths in a natural Malaysian rain forest.

Journal of Tropical Ecology 17: 411-429.

Jackson, H.D. (2000). The food of afrotropical nightjars. Ostrich 71: 408-405.

Jaeger, E. C. (1948). Does the poor-will hibernate? Condor 50: 45-46. 53

Jaffe, S. (1988). Climate of Israel. In: Yom-Tov, Y., and Tchernov, E. (Eds.). The

Zoogeography of Israel. Junk Publishers, Dordrecht, Netherlands.

Jetz, W., Steffen, J., and Linsmair, K.E. (2003). Effects of light and prey availability on

nocturnal, lunar and seasonal activity of tropical nightjars. Oikos 103: 627-639.

Kirwan, G.M. (2004). Remarks on Nubian Nightjar taxonomy. Bulletin of the African Bird

Club 11: 117-125.

Körtner, G., Brigham, R.M., and Geiser, F. (2001). Torpor in free-ranging Tawny

Frogmouths (Podargus strigoides). Physiological and Biochemical Zoology 74: 789-

797.

Kravchenko, V.D. (1984). Behaviour of the cotton bollworm (Heliothis armigera) in natural

conditions. Zoologichesky Zhurnal 63: 682-686 (in Russian).

Kravchenko, V.D. (1986). Duration of night and calling activity of Barathra brassicae L. In:

Animal Chemocommunication. Moscow, pp. 95-97 (in Russian).

Kurta, A. (1986). Factors affecting the resting and postflight body temperature of little brown

bats, Myotis lucifugus. Physiological Zoology 59: 429-438.

Lane, J.E., Brigham, R.M., and Swanson, D.L. (2004). Daily torpor in free-ranging Whip-

Poor-Wills (Caprimulgus vociferous). Physiological and Biochemical Zoology 77: 297-

304.

Lang, A.B., Kalko, E.V.K., Römer, H., Bockholdt, C, and Dechmann, D.K.N. (2006).

Activity levels of bats and katydids in relation to the lunar cycle. Oecologia 146: 659-

666.

Lythgoe, J.N. (1979). The Ecology of Vision. Oxford University Press, Oxford.

McKechnie, E.A., and Lovegrove, B.G. (2002). Avian facultative hypothermic responses: a

review. The Condor 104: 705-724. 54

McKechnie, E.A., and Wolf, B.O. (2004). The allometry of avian basal metabolic rate: good

predictions need good data. Physiological and Biochemical Zoology 77: 502-521.

McKechnie, E.A., and Wolf, B.O. (Submitted). The energetic benefits of torpor in

endotherms: physical, temporal and physiological determinants. Submitted to

Physiological and Biochemical Zoology.

Meyer, C.F.J., Schwartz, C.J., and Fahr, J. (2004). Activity patterns and habitat preference of

insectivorous bats in a West African forest – savanna mosaic. Journal of Tropical

Ecology 20: 397-407.

Mills, A.M. (1986). The influence of moonlight on the behavior of goatsuckers

(Caprimulgidae). The Auk 103: 370-378.

Nicol, J.A.c., and Arnott, H.J. (1974). Tapeta Lucida in the Eyes of Goatsuckers

(Caprimulgidae). Proceedings of the Royal Society of London. Series B, Biological

Sciences 187: 349-352.

Peiponen, V.A., and Bosley, A. (1964). Torpidity in a captive European Nightjar

(Caprimulgus europaeus L.). Ornis Fennica 41: 40-42.

Prinzinger, R., Preßmar, A., and Schleucher, E. (1991). Body temperature in birds.

Comparative Biochemistry and Physiology 99: 499-506.

Reinertsen, R.E. (1996). Physiological and ecological aspects of hypothermia. p. 125-157 in:

Carey, C. (Ed.). Avian Energetics and Nutritional Ecology. Chapman and Hall, New

York.

Seaman, D.E., and Powell, R.A. (1996). An evaluation of the accuracy of kernel density

estimators for home range analysis. Ecology 77: 2075-2085.

Schleucher, E. and Withers, P.C. (2001). Re-evaluation of the allometry of wet thermal

conductance for birds. Comparative Biochemistry and Physiology A 129: 821-827. 55

Schleucher, E. (2004). Torpor in birds: taxonomy, energetics, and ecology. Physiological and

Biochemical Zoology 77: 942-949.

Shirihai, H. (1996). The Birds of Israel. Academic Press, London.

Sierro, A., Arlettaz, R., Naef-Daenzer, B., Strebel, S., and Zbinden, N. (2001). Habitat use

and foraging ecology of the nightjar (Caprimulgus europaeus) in the Swiss Alps:

towards a conservation scheme. Biological conservation 98: 325-331.

Stephens, D.W., and Krebs, J.R. (1986). Foraging theory. Princeton University Press, New

Jersey.

Stiles, F.G., and Altshuler, D.L. (2004). Conflicting terminology for wing measurements in

ornithology and aerodynamics. The Auk 121: 973-976.

White, G.C., and Garrott, R.A. (1990). Analysis of Wildlife Radio-Tracking Data. Academic

Press, San Diego, California.

Whitaker, J.O. (1988). Food habit and analysis of insectivorous bats. Pp. 171-189. In: Kunz,

T.H. (Ed.) Echological and Behavioral Methods for the Study of Bats. Washington,

D.C., Smithsonian Institute.

Wichmann, G. (2004). Habitat use of the nightjar (Caprimulgus europaeus) in an Austrian

pine forest. Journal of Ornithology 145: 69-73.

Willis, C.K.R., and Brigham, R.M. (2003). Defining torpor in free-ranging bats:

experimental evaluation of external temperature-sensitive radiotransmitters and

the concept of active temperature. Journal of Comparative Physiological Biology

173: 379-389.

Wise Observatory (Tel Aviv University) website: http://wise-

obs.tau.ac.il/~eran/Wise/wise_calen.html

Wolda, H. (1988). Insect seasonality: why? Annual Review of Ecology and

Systematics 19: 1-18. 56

Withers, P.C. (1992). Comparative Animal Physiology. Saunders College Publishing,

Fort Worth.

Worton, B. J. (1989). Kernel methods for estimating the utilization distribution in

home range studies. Ecology 70: 164-168.

Woods, C. P. and Brigham, R. M. (2004). The avian enigma: "hibernation" by

common poorwills (Phalaenoptilus nuttalli). - In: Barnes, B. M. and Carey, C.

(eds.), Life in the cold: evolution, mechanisms, adaptation and application. 12th

International Hibernation symposium, pp. 129-138.

Zar, J.H. (1999). Biostatistical analysis. 4th edition. 436-437. Prentice Hall, New

Jersey. 57

APPENDIX 1: The food of the Nubian Nightjar

There are few references regarding the food of the Nubian Nightjar. Jackson

(2000) mentioned stomach analyses of nine nightjars, which contained mostly

Lepidoptera (moths), but also Coleoptera (beetles), Orthoptera (grasshoppers),

Dictyoptera (mantids) and Hemiptera (true bugs). More accurate details were not given. Cleere (1999) and Holyoak (2001) mention moths as being the main food too, but mention also grasshoppers, beetles and mantids.

In August 2004 and March 2005 I located the diurnal roost sites of two individuals that shed their transmitters while the batteries still had power. In both cases I flushed the nightjars from their roost site, and found large numbers of fecal pellets, implying that both nightjars roosted in exactly the same spot day after day for long periods.

I collected 30 pellets from the August 2004 roost site, but only three from the

March 2005 roost site. I analyzed them by soaking the pellets in 65% alcohol in water for a few minutes, examining the composition of the pellets by microscopy, and estimating the biomass of each systematic group. This procedure is commonly used in bat fecal analysis (Whitaker, 1988).

The fecal pellets I examined contained mainly wing scales of noctuid moths, but also other hard parts that allowed identification of several taxa. Moths accounted for 88% of the total biomass on average. Other taxa that were identified were beetles, earwigs (Dermaptera), ants (Hymenoptera), bugs (Heteroptera), and flies (Dipetera).

The former four taxa were never described before in the food of the Nubian Nightjar

(Table 10).

Table 10: Composition of 19 Nubian Nightjar pellets. The composition of each pellet is given for each insect group. UI = unidentified particles. Pellets 1-16 58 belonged to the August 2004 individual. Pellets 17-19 belonged to the March 2005 individual.

Pellet # Lepidoptera ColeopteraDermaptera Other UI Remarks 1 80 0 10 10 0 2 90 0 6 4 0 3 70 20 0 0 10 4 95 0 5 0 0 5 80 20 0 0 0 6 90 0 0 10 0 7 80 0 10 0 10 8 95 0 0 0 5 Large Tamarix flower 9 95 5 0 0 0 10 95 5 0 0 0 11 90 0 10 0 0 12 90 5 5 0 0 Many Coleoptera eggs 13 100 0 0 0 0 14 85 5 10 0 0 15 99 0 0 1 0 16 75 25 0 0 0 17 75 20 0 5 0 18 92 0 0 8 0 19 100 0 0 0 0 Average 88.21 5.53 2.95 2.00 1.32

APPENDIX 2: Moth activity patterns at Neot Hakikar

Medium sized moths are a key component in the diet of nightjars. Thus, understanding the circadian, lunar and annual activity patterns of moths is crucial in predicting the activity patterns of nightjars. Kravchenko (unpublished data) studied activity patterns in Noctuidae moths in the Neot Hakikar region in southern Israel (30º57’ N 35º23’ E) in 2000-2001. He systematically trapped moths using light traps which he placed for one night a month. He found that strong peaks of activity occurred in May - June, and in September – October

(figure 12). In the cold winter months, Noctuidae moth activity was lower, and larger species were more active in these months, probably due to their better ability to generate heat out of flight activity (Wolda, 1988). Furthermore, Kravchenko found a distinct circadian cycle in 59 the activity and mobility of similar taxa in arid Azerbaijan, of a strong peak of mobility about

30 minutes after sunset which usually lasted for about 1 h and was related to the feeding activity of the moths (Kravchenko, 1984; Kravchenko, 1986). Later on at night, another peak of mobility occurred around midnight that was related to mating and reproductive activity.

However, this mobility peak involves flight at altitudes higher than the hunting altitude of nightjars, and may offer fewer foraging opportunities for nightjars. Furthermore, Kravchenko examined the effect of the lunar cycle on moth activity, and found that when strong lunar illumination is available at night, moth activity was lower; however the nocturnal double- peaked patterns were maintained. This effect of lunar illumination on activity and mobility patterns of moths is attributed to higher predation risk on bright nights (Lang et al., 2006).

Figure 12: Seasonal activity patterns of noctuid moths at Neot Hakikar. Moth numbers represent the sum of the monthly totals of both years 2000 and 2001.

APPENDIX 3: Aspects in the natural history of the Nubian Nightjar

During my studies of the Nubian Nightjar, I discovered several aspects that were previously unknown.

Display and courtship behavior

During March - April 2006, while tracking a pair with both birds carrying a radio tag,

I observed display and courtship behavior. This behavior took place during three consecutive nights with maximal nocturnal light intensity, when the moon phase was highest. In this display, both birds flew about 2 m above the ground at a distance of about 1 m between each other, the male leading and the female trailing him. Both birds flew with their wings raised in a shallow V shape. They flew back and forth along a water canal several times, for a distance of about 100 m. Both birds were very vocal during flight. After landing, they faced each other. The male spread his wings and tail on the ground, displayed the white wing and tail patches, and puffed his white throat patches. He called towards the female in, apparently very excited.

The pair repeated this flight together, then landing while calling and then disappeared into the scrub several times, presumably to mate, but I could not see this. A courtship session lasted 1-3 h.

Sex-specific calls

Holyoak (2001) described only one call of the Nubian Nightjar, a hollow, resonant koww koww, and attributed no differences to the sexes. By fitting radio tags to birds, I could relate different calls I heard from pairs to specific birds. I found that the call of the male is higher pitched, while the female gives a lower, hoarser call.

APPENDIX 4: World distribution and subspecific structure of the Nubian

Nightjar

The world distribution of the Nubian Nightjar includes parts of east Africa, south Arabia and the Middle East, and it is normally separated into five subspecies:

Caprimulgus nubicus tamaricis in southern Israel, Jordan and western Arabia; C. n. nubicus in the Rift Valley of S Egypt and C Sudan; C. n. torridus in Djibouti, N

Somalia, C Ethiopia and NW Kenya; C. n. jonesi in Socotra Islands; and C. n. taruensis in S Somalia and S Kenya (Shirihai, 1996; Cleere, 1999; Holyoak, 2001;

Kirwan, 2004). Apart for C. n. tamaricis, all other subspecies are regarded as resident. There is some evidence of C. n. tamaricis performing long distance migration from their breeding grounds in the Middle East and Arabia south to Africa in winter, but these records might be anecdotal at best, and may not represent true migration patterns. It is possible that they resulted from identification mistakes, due to the clinal and slight morphological differences between subspecies, suggested to be a result of localized climatic and soil conditions (Kirwan, 2004). Together with year- round observations of C. n. tamaricis at their breeding grounds (personal observations) it is unclear whether the tamaricis population in Israel performs any migration at all.

שיחור מזון, שינויים בטמפרטורת גוף ודגמי תפוצה מרחביים של התחמס הנובי

Caprimulgus nubicus בישראל

יואב פרלמן

חיבור לשם קבלת תואר מאסטר במדעים (.M.Sc)

ביה"ס הבינלאומי ע"ש אלברט כץ, המכונים ע"ש בלאושטיין לחקר המדבר, אוניברסיטת בן גוריון בנגב

יוני 2007

תקציר

תחמסים הם הקבוצה היחידה של עופות אוכלי חרקים פעילי לילה המאתרים את טרפם בעזרת חוש

הראייה. בשל התלות שלהם בתאורה לציד, הם חושפים את עצמם לטריפה כאשר הם צדים בפרקי זמן

בהם יש עוצמת תאורה חזקה בלילה. בנוסף, תחמסים הם בע"ח אנדותרמיים, ומינים רבים נמצאו

משתמשים בהיפותרמיה מבוקרת על מנת לחסוך באנרגיה בפרקי זמן בהם טמפרטורת האוויר נמוכה או

יש מחסור במזון. התחמס הנובי Caprimulgus nubicus הוא תחמס קטן בעל אוכלוסיה קטנה בישראל

הנמצאת בסכנת הכחדה. מטרת המחקר הייתה להבין את השפעות מספר משתנים סביבתיים, והם

טמפרטורת אוויר, עוצמת תאורה וזמינות מזון פוטנציאלי, על התנהגות שיחור המזון, השימוש

בהיפותרמיה מבוקרת והניצול המרחבי של סביבתם, ועל יחסי הגומלין בין התנהגויות אלה. בין השנים

2004 ל- 2006 לכדתי שבעה תחמסים נוביים באזור כיכר סדום, להם הצמדתי משדרי רדיו זעירים

ועקבתי אחריהם במשך 73 לילות בסה"כ. מצאתי כי התחמסים צדים יותר בפרקי זמן בהם עוצמת האור

בלילה גבוהה יותר. כן מצאתי כי כנראה התחמסים נמצאים במצב של חילופיות בין יעילות הציד בפרקי

זמן מוארים יותר לבין סיכון טריפה גדול יותר בפרקי זמן אלה. מצאתי כי בלילות ללא ירח, התחמסים

ניצלו יותר לציד את שעות הדמדומים, בהן יש מעט קרינת שמש, אך בלילות עם עוצמת תאורת ירח

גבוהה התחמסים נמנעו מלצוד בשעות הדמדומים. מצאתי גם כי התחמסים משתמשים בהיפותרמיה

מבוקרת באופן תדיר, במיוחד בפרקי זמן בהם טמפרטורת האוויר נמוכה, או כאשר עוצמת התאורה

בלילה נמוכה, וההזדמנויות שלהם לציד מוגבלות. יחסי הגומלין הללו בין אקולוגית שיחור מזון לבין

האקולוגיה הטרמלית של ציפורים טרם תוארה. כמו כן מצאתי כי לתחמסים הנוביים אזור מחיה קטנים 63

יחסים, המורכבים מכתמי מלחה, בהם הם משתמשים באופן כמעט בלעדי למנוחה ולדגירה, ומשטחים

פתוחים יותר, כולל שדות חקלאיים, בהם הם צדים. במידה ותיושם תוכנית לשמירה על המין בישראל,

היא צריכה לכלול שמירה על בתי הגידול, על מקורות המים באזור ומניעה של זיהום אור בשטחים

הפתוחים.

שיחור מזון, שינויים בטמפרטורת גוף ודגמי תפוצה מרחביים של התחמס הנובי

Caprimulgus nubicus בישראל

חיבור לשם קבלת תואר מאסטר במדעים (.M.Sc)

אוניברסיטת בן-גוריון בנגב

המכונים ע"ש בלאושטיין לחקר המדבר

ביה"ס הבינלאומי ע"ש אלברט כץ

מאת: יואב פרלמן

מנחים: פרופ' דיוויד זלץ

פרופ' ברי פינשאו

חתימת המחבר ...... תאריך......

חתימת המנחים ...... תאריך ......

...... תאריך ......

חתימת יו"ר ועדת הוראה מחלקתית ...... תאריך ......

אוניברסיטת בן-גוריון בנגב

המכונים ע"ש בלאושטיין לחקר המדבר

ביה"ס הבינלאומי ע"ש אלברט כץ

שיחור מזון, שינויים בטמפרטורת גוף ודגמי תפוצה מרחביים של התחמס הנובי

Caprimulgus nubicus בישראל

חיבור לשם קבלת תואר מאסטר במדעים (.M.Sc)

מאת יואב פרלמן

סיוון תשס"ז יוני 2007