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Running head: Woodpecker's Cavity Microenvironment

THE WOODPECKER'S CAVITY MICROENVIRONMENT:

ADVANTAGEOUS OR RESTRICTING?

Cynthia Mersten-Katz(1), Anat Barnea(2), Yoram Yom-Tov(1), Amos Ar(1)

1- Department of Zoology, Tel-Aviv University, Tel-Aviv 61391, Israel

2- Department of Natural and Life Sciences, The Open University of Israel

Corresponding author: Anat Barnea, Dept. of Natural and Life Sciences, P.O.Box 808, 108

Ravutski St., The Open University of Israel, Raanana 43107, Israel. Phone number: +972-9-778-

1753; Fax number: +972-9-7780661 Email: anatba@openu.ac.il

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ABSTRACT

We studied the nesting biology of the Syrian woodpecker (Dendrocopos syriacus) in

Israel, with emphasizing its physiological aspects and nest properties. Laying occurred during

April-May. Mean clutch size is 4 (range 3-5). Mean egg mass is 5.4g±0.4SD. Eggs are laid daily.

Incubation starts when the last egg is laid. It lasts 12-13d. Both hatching and fledging spread over

2-3d. Parents share incubation during day but only the male incubates at night. Mean egg

temperature is not significantly different between day and night and averaged 34.2ºC±4.3SD.

Mean egg water loss is 1.4% and 0.5% per day of initial egg mass prior to the onset of incubation

and during incubation, respectively. Extrapolated total water loss of these eggs is 13.1% at the

end of incubation. Mean egg shell water vapor conductance is 2.1mg/(d·Torr), equals to

100mg/(d·kPa). Both parent share feeding equally throughout. Young fledge asynchronously at

the age of 26d, but are fed by their parents outside the nest for another month. Nest bottom gas

compositions initially decrease in O2 by ~1.75% and increase in CO2 by ~1.20%, respectively,

until nestlings are about 15d old. There was little change in nest gas composition until 22d. From

that time on until fledging O2 and CO2 concentrations increase and decrease respectively, due to

nestlings' activity.

Key words

Incubation, fledging, nest gas composition and temperature, egg water loss, nestling growth and

metabolism

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Data on gas composition in cavity nesting birds has been subjected to research in various

species. For example, Birchard et al. (1984) found a reduction in O2 concentration in nest cavities

to 19%, 19.7%, and 17.4% and an increase in CO2 concentration to 1.1%, 1.7% and 3.1% in

Rhinoceros auklet, Burrowing owl and Bank swallow, respectively. Howe et al. (1987) measured

O2 concentrations as low as 18% and CO2 concentration up to 2.6% in the Northern flicker nest

cavities. Ar and Pointkewitz (1992) measured variable O2 and CO2 pressures in occupied nest

chamber of the European bee-eater down to 18.3% and up to 2.0% respectively. All these authors

review previous studies in their articles which show, as expected, low O2 and high CO2

concentrations in the confined environment of hole and borrow nesters.

In a previous study (Ar et al., 2004) we have reviewed some benefits and withdrawals of

living in confined environments in birds and mammals. Based on field measurements of the

physical characteristics of cavities of the Syrian woodpecker (Dendrocopos syriacus) in Israel,

their gas conductance under different environmental conditions (diffusion, wind, heat convection)

and woodpeckers' O2 consumption rate, a model has been proposed. This model predicted that in

most cases, O2 pressure in the cavity does not pose a hypoxic stress to the birds, and a suggestion

was made that the inhabitants of the activity inflict cavity aeration.

Following our model calculations, we hypothesized that O2 and CO2 concentrations in the

nest cavity of the Syrian woodpecker might affect eggs and young hatchlings during incubation

and early stages of development. We further hypothesized that O2 and CO2 concentrations will

increase and decrease respectively and become close to that of free atmosphere later during

nestlings development due to the increased physiological and behavioral activities of the cavity

inhabitants.

In order to test this hypothesis, we measured, in natural woodpeckers cavities, the laying

and incubation behavior, nest and egg temperatures, nest humidity and egg water loss, eggshell

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gas conductance, parental and nestlings behavior and nestlings' growth, nest gas composition, and

attempted to measure O2 consumption and CO2 production rates in the nest cavity.

METHODS

Nest cavity inspection before egg laying. - We used a hand-made periscope constructed

from a polyethylene tube (3cm in diameter, 20cm long), to observe the content of the nest cavity.

To the end of this tube we attached, diagonally, a small mirror with a light bulb connected to a

battery at its base. In order to inspect a cavity we inserted the tube through the nest entrance (top

of cavity), with the mirror facing down and the bulb illuminating the cavity bottom. By looking

through the tube we could inspect the mirror reflection of the cavity bottom.

Access to eggs and nestlings. - Once all eggs had been laid, we created an opening by

drilling out a "door" with a jig-saw in the trunk or the branch containing the nest, close to the

bottom of the nest cavity. The opening was big enough to allow a hand to be inserted and was

drilled on the opposite of the nest entrance, a little higher than the bottom of the cavity. At the

end of this operation, the "door" was replaced and sealed with brown plasticine. All following

inspections of nest content were done through this opening with the 'door' being replaced and

resealed each time. In addition, we occasionally observed feeding behavior and food items

brought to the nest.

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Eggs and nestlings mass and measurements. - Eggs were numbered with a pencil for

sequence of laying and length and breadth were measured with calipers to the nearest 0.05mm. In

the field eggs were weighed almost every second day, using a VDF torsion balance accurate to

the nearest 0.1g, and time of weighing was recorded. Some eggs were taken to the laboratory at

random and kept at 35ºC in a 2L sealed desiccator over a saturated Na2Cr2O7·H2O solution.

Under these conditions, the humidity in the desicator was 51% (Tracy et al., 1980), same as was

calculated for natural nest cavities (see Results, Table 2). The eggs were weighed once or more

daily using a Mettler BE 20 analytical balance (to the nearest 0.01mg). Time of weighing was

recorded and the eggs were placed back in the desiccator after they had been turned. Eggs were

kept for different periods of time in the laboratory and were then returned to their nests, to be

further incubated by the parent birds. Nestlings were weighted with a Pesola spring weighing

scale (up to 100g, with accuracy of ±3g at full load).

Nest and eggs temperatures. - In nests containing eggs: From each of the four nests

sampled approximately every two days, one egg was randomly taken to the laboratory. It was

replaced in the nest with an artificial egg to record egg temperature in the nest during incubation.

Artificial eggs were prepared from similar sized Coturnis coturnis japonica eggs, which we had

emptied, filled them with gypsum, inserted a thermistor into the center of each, and painted them

white with enamel paint. The woodpeckers accepted the artificial eggs, incubated and turned

them normally. Another thermistor was placed half-way down the nest cavity for recording nest

temperature. The two thermistors were connected to a "Rustrak" temperature paper recorder

(Gulton; accurate to the nearest 0.5ºC) which recorded changes of temperature with time. To

calibrate the recorder we inserted each probe into different water containers with different known

temperatures. In the 2 nests containing an adult and 2 nestlings, nest and ambient temperatures

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were recorded by using 2 calibrated copper-constantin thermocouples (precision = ±0.05ºC),

connected to a battery operated digital Bailey Thermocouple Reader – Model Bat 8. One

thermocouple was situated within the bottom of the nest; the second one was connected, but not

touching the tree bark.

Water vapor eggshell conductance. - (GH2O): GH2O was calculated according to (Ar et al.,

1974). We calculated egg water loss rate in the desiccator under known temperature and

barometric pressure and corrected to standard pressure at 20ºC (.

MH2O; mg·d-1), and divided the

result by the difference in water vapor pressure across the shell as shown in equation (1):

(1) GH2O = .

MH2O/(PEH2O - PDH2O)

where

PEH2O = water vapour pressure in the egg (kPa; assuming full saturation at the desiccator

temperature)

PDH2O = water vapour pressure in the desiccator (kPa; = 0)

The heat production by embryos in small eggs is too small to be considered as a factor capable of

changing PEH2O (Turner, 1987).

Nest water vapor pressure (PNH2O) and nest relative humidity. - PNH2O (kPa) was

calculated in Equation (2), in a similar way to Equation (1) by rearrangement and using PNH2O

instead of PDH2O:

(2) PNH2O = PAH2O – (.

MH2O/GH2O)

where

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PAH2O (kPa) is the appropriate saturation water vapor pressure value for the mean artificial egg

temperature measured on the same day in the nest;

.MH2O (mg·d-1) is the mean water loss rate value for all eggs in the nest on that day;

GH2O (mg ·d-1·kPa-1) is the mean value calculated in the laboratory for an egg from the same nest

on the same day, and

PNH2O (kPa) is the calculated nest water vapor pressure.

The calculated PNH2O was also expressed as the percentage of relative humidity for the mean

temperature measured in the nest cavity using the appropriate tables [1]. Data of ambient relative

and absolute humidity and temperatures were obtained from a nearby meteorological station.

Nest gas composition. - Samples were taken at night during the breeding season, when a

parent was usually present in the nest, together with eggs or young nestlings. The samples were

taken from a hole drilled into the cavity (4mm in diameter) about 5cm above the bottom on the

same side as the entrance. A plastic tube, cut to fit each hole length, was glued into the hole, flush

with the outside. A small rubber plug sealed the tube when not in use. A needle with a 3-way

stop-cock was inserted into the hole through the rubber plug. Gas samples were taken using a

closed 15ml glass syringe which fitted into the 3-way stop-cock. In order to ensure a non-

contaminated sample, each sample was preceded by three samples taken to wash out previous gas

from the syringe. The fourth sample was taken with the stop-cock closed and using a needle, for

further analysis of O2 and CO2 fractions. This was done following essentially the method

described by Scholander and Evans (1947), using a modified glass pipette. The content of each

syringe was analyzed three times and the average was taken as a final result. Following each

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sampling, the presence of the nest inhabitants was verified with the periscope. Samples were

analyzed within 3.5hrs following collection.

Oxygen consumption and CO2 production rates in occupied nests. - An attempt was made

to measure the collective O2 consumption rate (.

MO2) and CO2 production rate (.

MCO2) in two

nesting cavities in the field. Air was continuously drawn through a drilled hole as described

above by the battery-operated suction pump of an O2 analyzer (Sermovex 570A) accurate to ±5%

of the O2 fraction reading, at a rate of ca. 600ml·min-1. The flow was controlled with a calibrated

flow meter (Matheson, tube size R-2-25-D) located at the entrance to the O2 analyzer and noted.

The analyzer voltage output was recorded with a battery-operated recorder (Electro Minigor,

Goerz). An array of three parallel columns was placed in the flow between the nest and the flow

meter. These columns contained interchangeable by-passes for initial calibration, Drierite

(Hammond) and Ascarite (Thomas) columns to absorb water vapour and water vapour plus CO2

respectively. By keeping the flow constant, the changes in steady-state values of O2 fractions past

the different columns, the CO2 fractions in the outflow could be calculated essentially after

Leshem et al. (1991). These were adjusted to a standard flow rate of 600ml[STPD·min-1.

Sleeping behavior in tree cavities. - To quantify vertical movements of woodpeckers in

their tree cavities during the nights, we drilled two holes (1cm diameter each) in the tree trunk of

each cavity, 4cm below the cavity entrance and 5cm above the cavity bottom. To each of these

holes we attached an ESP infra-red intrusion detector, connected to an external voltage supply

and a buzzer. The detector's infra-red laser beam entered the cavity through the hole, so that each

time the woodpecker moved in the cavity and passed the infra-red laser beam, the buzzer sounded

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in a closed room 10m from the cavity. The two buzzers differed in their sounds, to enable the

observer to detect and record the woodpecker's location in each buzzing event. When not in use,

the two holes in the tree trunk were sealed and common flashed with brown plasticine.

RESULTS

Syrian woodpeckers nest in cavities which they drill in tree trunks or branches prior to the

breeding season (characteristics were given in Ar et al., 2004). In Israel, breeding season (egg

laying to fledging) lasts from April to June.

Egg laying and properties. - We recorded egg laying, incubation and nestlings growth in

9 nests. Egg laying occurred in 7 out of 9 nests during the last third of April. In the other two

nests egg laying occurred later in the season, until early July. Clutch size is usually 4 eggs,

sometimes 5, and rarely - 3. One egg is laid daily, in the early morning. Eggs are white, 2.65cm

±0.15SD long and 1.94cm ±0.03SD wide (n=18). Their mean initial mass is 5.4 g ±0.4SD (n=9).

Incubation. - Parents do not incubate the eggs during egg laying period, however the male

stays in the nest cavity, and probably sits on the eggs during the night. Full incubation starts

when the last egg is laid. During day time, both parents equally alternate in incubation; while

during the night only the male sits on the eggs. From the time the first egg hatches the parents

incubate the eggs only at nights. Hatching is not synchronized and takes two more days. From

cases where we could determine the order of egg laying in a nest, we know that the first eggs to

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be laid are also the first ones to hatch. This means that all eggs are not incubated for the same

amount of time: those laid first are not incubated until the clutch is completed, while those laid

last are not incubated from the time of the first hatching until all eggs hatch. Therefore, in

general, each egg stays in the nest from laying until hatching for 12-13 days: 11 days of

incubation and additional 1-2 days prior or after that.

Nest and egg temperatures. - These were measured for 9 days in 6 nests, for a total of 217

hrs (121 hrs during nights and 96 hrs during days). Mean ambient, nest cavity and egg

temperatures in occupied nests during day and night times are given in Table 1. The nest

temperature of nest containing an adult and 2 nestlings are also given in the table. Maximal egg

temperature was about 41ºC, recorded twice during a 2-days heat wave, in one of the nests, each

time for about half an hour. The respective maximal nest temperature on these times was

approximately 34ºC. Eggs in this nest hatched successfully. Minimal egg temperature in the same

nest was about 19ºC, and the respective minimal nest temperature on that time was approximately

17ºC.

Figure 1 shows a relationship between ambient and nest temperature: the lower the

ambient temperature is, the higher is the temperature difference between the nest and ambient.

Figure 2 shows that these differences are mainly emphasized from early morning to about mid-

day. This may indicate certain delay between ambient and nest warming and cooling, probably

due to the insulation and heat capacity of the nest cavity walls. In addition, the presence of

inhabitants in the nest seems to lower the temperature difference between ambient and the nest, in

comparison with an empty nest.

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Nest humidity. - When reaching into nests cavities, through the door openings which we

constructed, we felt that the air inside the nests was hot relative to the outside. We also observed

water condensation on the inner walls of the nest, indicating high nest air humidity. Relative and

absolute humidities were calculated for three nests, on different incubation days (Table 2). It can

be seen that there is a gradient in both temperature and absolute humidity from the egg through

the nest cavity to the outside environment.

Egg water loss rate. - was measured in eggs from 4 nests. Laboratory measurements:

Water loss rate from 9 eggs which were taken from their nests to the laboratory for a brief period

of time was measured (Table 3). Water loss rate from each egg did not change much or

consistently with time (mean coefficient of variation = 19%). All 9 eggs contained living

embryos when inspected before returned to the nest. However, only 2 of them eventually hatched.

One of them was brought to the lab on its laying day (a day prior to onset of incubation), and the

other was taken to the lab on the 9th day of incubation and returned shortly before hatching. There

was no statistically significant difference (p=0.20) in percent daily water loss rate of the same

eggs between the laboratory and the field (Table 3). Field measurements: Field measurements

were preformed on 4 eggs from 2 nests, in which the time of laying and initial mass were known

or could be back calculated for not more than 2 days. The eggs lost on the average, 1.4% of their

initial mass prior to the onset of incubation. The eggs lost on the average 0.5% of their initial

mass per day, after the onset of incubation. The extrapolated total water loss of these eggs was

13.1% at the end of incubation (Fig. 3).

Water vapor eggshell conductance. - (GH2O, mg/(d·Torr)): This was determined for the

eggs that were brought to the lab. Eggs from the same nest, which were taken later during

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incubation, showed higher GH2O values than those taken earlier. Each GH2O value was normalized

(see methods) to the assumed egg temperature due to metabolic heat production (Table 4).

However, paired t-test between 'early incubation' eggs and 'late incubation' ones did not yield a

significant difference.

Parental care after hatching. - Both parents start feeding immediately after first hatching,

and share this task equally throughout. Food consists of nuts (such as almonds and pecans),

succulent fruits, as well as various insects and spiders. Although nestlings increase in mass

during development, their parents maintain a constant feeding rate of about 10 items/hr. During

the first days after hatching, parents feed their young by fully entering into the nest cavity and are

not seen from the outside. When nestlings are about 15 days old, they start climbing on the inner

walls of the cavity and parents go in only half-way, standing at the cavity entrance. At the age of

about 20 days the nestlings climb even higher, and the parents only shove their heads into the

cavity. From about day 22 until fledging, (on day 26 from hatching) nestlings glance out of the

cavity entrance, taking food from the parent that stands outside the cavity entrance.

At about after 2-3 days after hatching is completed, parents remove broken egg shells and

eggs which did not hatch and usually dispose them far away from the nest. Feces are removed

from the nest cavity, but only by the male. The nest is kept very clean until the nestlings are 16

days old. From this stage until fledging, feces removal rate decreases, and feces accumulate at the

bottom of the cavity.

Nestlings’ growth and fledging. - Fig. 4 presents nestling growth and growth rate curves,

based on 16 nestlings from 6 nests. At the age of about 21-22 days, nestlings’ growth stabilizes,

when their mass reaches about 64g. It stays the same until fledging. This is not their final body

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mass, as the adults' mean mass is 75.6 g±2.3SD (n=11) for males and 70.9 g±3.1SD (n=12) for

females. Although not statistically significant, it looks as if there is a small mass decrease of the

nestlings just before fledging (Fig. 4, star symbol).

Nestlings hatch naked, eyes closed, and with a yellow tongue marking. Eyes open and

plumage appears at the age of 4 days. From day 12 on the nestlings voices are heard outside of

the nest cavity. Fledging occurs when the young reach the age of about 26 days. As in the egg

laying sequence, fledging is not synchronized and it ranges over 2-3 days. Parents continue to

feed both the young that are still in the nest, and those which have fledged. It is easy to locate the

fledglings, as they are very vocal for a few days. They spread over their parents' territory, each

one stays on the same tree for most of the day. They are distinguished by their posture which is

parallel to branches, unlike adults which stand vertically. Once fledged, the young do not return

to the nest cavity for the night. A week after fledging, the young already fly well and follow their

parents. First self-feeding attempts had been observed 25 days after fledgling, and soon after the

young disappear from their parents territories.

Nest gas composition. - Nest gas compositions at the nest bottom for O2 and CO2 is given

in Figure 5. The data are from 6 nests (73 measurements). The figure shows an initial decrease in

O2 pressure and increase in CO2 pressure from hatching up to day 15 when the hatchlings start

the activity of climbing (Fig. 5 arrow 1). There after, until day 20 (half way climbing, Fig. 5

arrow 2) and day 22 (full height climbing, Fig 5 arrow 3), there is essentially no change in gas

pressures at the nest bottom. From about day 22, when nestlings start to glance out of the cavity

entrance, until fledging (on day 26, Fig. 5 arrow 4), O2 pressure increases again and CO2 pressure

drops (note different symbols in Fig 5).

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Oxygen consumption and CO2 production rates in an occupied nest. - Calculated values

for O2 consumption rate were in accordance with the number of inhabitants and the age of the

nestlings in two populated nests. However, the metabolic rate values were much lower and higher

respectively for O2 and CO2 in comparison with the expected values based on previous laboratory

measurements (Ar et al., 2004). Details are given in Table 5. The variation in CO2 production rate

is large compared with the rate of O2 consumption, and this is also demonstrated by the mean

field RQ value of 2, as compared with the expected.

Sleeping behavior in tree cavities. - Observations on movements of 3 females and one

male inside their tree cavities were made during nights (one female was sampled twice on 2

separate nights). Time intervals and number of staying events at cavity bottom and at cavity

entrance throughout the night are summarized in Table 6. After converting to time percentages,

the percent of time away from bottom or entrance could be calculated and is given at the bottom

of Table 6. It can be seen that except from short excursions most of the night woodpeckers stay in

the cavity, away from either the bottom or the entrance.

DISCUSSION

Incubation. - The incubation period of 11-12 days of our woodpecker species was a day

shorter than the predicted from Yom-Tov and Ar (1993), and significantly shorter (p>0.001) than

the expected from egg mass for birds in general (17 days; Rahn et al., 1974). In the hole nester

bee-eater (Merops apiaster), incubation period is longer as compared with woodpeckers (Picidae)

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of the same size (19 days; Ar and Piontkewitz, 1992) vs. the predicted 13 days from Yom-Tov

and Ar (1993). The hole nester rose-ringed parakeet (Psittacula krameri) has similarly longer

incubation period (24 days; unpublished) vs. the expected 14 days of a picid species of the same

size. It may follow that the relatively short incubation period of woodpeckers is a unique feature

of this family.

Time from hatching to fledging. - The time from hatching to fledging in our woodpecker

was 26 days. Thus, the ratio of hatching-to-fledging to incubation time is ~2.3. This value is

much higher than the one typical to altricial species in general (1.23; Ar and Yom-Tov, 1978).

However, most of this ratio stems from the fact that the incubation time is much shorter than

expected, and that the sum of incubation to fledging time is similar to that of other altricial

species of the same body mass (38 vs. 42 days respectively). Yom-Tov and Ar (1993) suggested

that shortening incubation might overcome the limitation of diffusive oxygen supply to the

embryo through the shell by early onset of lung respiration in the hypoxic conditions in the nest

cavity, and therefore immature hatchling requires a longer time to achieve fledging. They also

suggested that this might be true also for some other cavity nesters such as Australian parrots and

African hornbill species which have a high hatching-to-fledging to incubation ratio. Earlier, we

have related the sleeping in cavities all year round to a strategy of protecting from enemies and

extreme climatic conditions. In addition, during the breeding season, the cavities provide shelter

for the young which allows prolonging the hatching-to-fledging period without compromising

with harsh conditions (reviewed in Ar et al., 2004).

Egg, Nest and Ambient temperatures and humidities. - It should be noted that egg

temperatures were measured in artificial eggs (see Methods). Therefore, real eggs temperatures

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might slightly differ due to reasons such as size differences between the artificial egg and the real

ones, heat capacity differences, lack of evaporative cooling and metabolic heat production

(Turner, 1987). However, from comparative studies, it is expected that temperature differences

found are similar to those of intact natural eggs.

Ar & Sidis (2001) have reviewed nest microclimate conditions during incubation in birds.

They have concluded that in tunnel and hole nesters the influence of rise in temperature during

daylight is dampened and temporally delayed due to nest mass interia and wind shielding effect.

The data in Table 1 point to the same direction: in spite of an average of ~3ºC difference between

day and night in ambient temperature, the difference in egg temperature under the same

conditions is only less than 1ºC, although the temperatures among the eggs are influenced by the

ambient temperature and differ between day and night.

The data in Table 1 are further corroborated in Figure 1: It shows that the lower the

ambient temperature is, the higher is the temperature difference between ambient and the nest

cavity. Interestingly enough, extrapolating the curve to zero temperature difference, yields an

ambient temperature of ~33ºC, meaning that around these ambient temperatures the parents can

reduce significantly their nest attentiveness. On the other hand, at the lowest ambient temperature

measured (~20ºC), the nest temperature is ~6ºC higher than the ambient, suggesting an outcome

of increased nest attentiveness, as is also the case with some other species (e.g.: Yom-Tov et al.,

1978). As is shown in Figure 2, such conditions may occur during the second half of the night.

Figure 2 also shows that temperature differences exist between occupied and empty nest,

indicating the importance of the presence of the inhabitants on the thermoregulation of the nest

interior. This is evident in particular in the cold early mornings, where the temperature in the

interior of the nest is noticeably higher than the ambient.

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To estimate temperature gradients, we calculated the average temperature difference

between the egg, nest and the outside (Table 2). The data indicate that the temperature gradient is

divided so that about 2/3 of it is between the egg and the nest and only 1/3 is between the nest

and the outside environment. Using the assumptions of Ar and Sidis (2002), this indicates that on

the average, at least in the thermo-neutral zone of the woodpeckers (Ar et al., 2004), thermal

insulation between the egg and the nest cavity is twice as much as that across the cavity wall and

the ambience.

We also calculated the differences in absolute humidity between the egg, nest and the

outside (Table 2). Absolute humidity gradient is divided so that about 3/4 of it is between the egg

and nest, while 1/4 is between the nest and the outside environment. This is different than the 2/3

and the one third ratios, respectively, estimated by Ar and Sidis (2002) for bird nests in general.

This might be due to the fact that cavity nests of woodpeckers are relatively closed (of low

conductance), compared to nests in general. The fact that humidity gradient of the nest cavity is

high in relation to the temperature gradient fraction between the egg and the nest, may stem from

the fact that while temperature is exchanged throughout the nest surface, water vapor can be

exchanged only through the nest cavity entrance.

In addition, while no correlation was found between nest and outside temperatures, a

significant one was found by regressing nest absolute humidity (Y; kPa) on outside absolute

humidity (X; kPa) (Equation 3).

(3) Y = 0.36 + 0.49 · X (r2 = 0.911; p > 0.04; n = 4)

Equation 3 shows that nest absolute humidity is only partially dependant on outside humidity and

increases only by about one half kPa for every one kPa increase in the ambient, indicating

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relative stability of nest humidity. It should be noted that part of the nest humidity may be due to

vapor emission from the tree material.

Egg water loss rate. - Laboratory measurements: Daily water loss rate, as measured in

the laboratory, was not significantly different from the one measured in nature (Table 3). This

proves that the calculated nest humidity applied to the eggs in the laboratory was accurate. Thus

the reason for the high embryonic mortality observed in the eggs that were incubated for short

periods in the laboratory must be due to other unknown reasons. Field measurements: Prior to

onset of incubation, eggs lose water at a faster rate than after the onset of incubation (Fig. 3). The

lower rate of water loss after the onset of incubation may be explained by the parent's presence

inside the nest cavity during incubation, which increases humidity in the nest (Table 2) and thus

decreases eggs' water loss. The unexpected initial high water loss before the onset of incubation

brings the total incubation water loss to an average of 13.1%, which is well within the range of

bird eggs in general (Ar and Rahn, 1974).

Water vapor eggshell conductance. - Although there is no significant increase in GH2O

values with incubation time, all pairs of eggs that were taken from the same nests at different

ages, showed a tendency of an increase in GH2O values (Table 4). The lack of statistical

significance might result from the small number of measurements. To quantify the increase in G

values, a larger and more systematical sample is needed. If proven, it suggests that this might

have a biological significance allowing eggs that were laid late to lose more water during the

shorter incubation.

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Parental care, nestlings behavior and nest gas composition. - Wickler and Marsh (1981)

found a positive correlation between the increase in nest CO2 gas composition and the increase of

nestlings' mass and age in the bank swallow. Birchard et al. (1984) who studied three species of

borrow-nesting birds concluded that bank swallows use convective means of ventilation to

significantly reduce the difference between CO2 and O2 in the nest and the atmosphere. However,

bulk flow of gases due to occupants movements is not important in determining gas composition

within borrows of the Rhinoceros Auklet, while the accumulation of CO2 in borrows of the

borrowing owl indicates a reduced diffusive gas exchange with the atmosphere. Howe and

Kilgore (1987) have suggested that in spite of the presence of occupants in the nest, their heat

production tend to significantly reduce the depletion of O2 and the accumulation of CO2. Taken

together, these examples demonstrate that a variety of mechanisms may act to equate gas

composition between the nest cavity and the atmosphere in different species.

Gas composition of the woodpecker cavity is influenced by the parents and nestlings

behavior: up to 15 days after hatching, there is a reduction in O2 pressure at the bottom of the

cavity to an average minimal partial pressure of 13 - 14 Torr (~1.75%) below atmospheric. At the

same time, CO2 pressure increases to 9 - 10 Torr (~1.21%). Throughout this period, the growing

hatchlings stay at the nest bottom and parents feed them by fully entering into the nest cavity.

From day 20 on, there is an increase in O2 pressure and a decrease in CO2 pressure in the nest

cavity (Fig. 5). This period correlates with the first partial climbing of the nestlings on the cavity

walls from day 20 on, and climbing to the nest cavity opening from about day 22 until fledging.

In parallel, the parents enter the nest cavity only to the depth which allows them to feed the

young. Such movements have been shown to cause nest ventilation in bee-eaters feeding their

young (Ar and Pointkewitz, 1992) and in woodpeckers which occupy cavities during nights

outside the breeding season (Ar et al., 2004).

20

As can be seen in Table 6, when not in movement, woodpeckers stay most of the time

during nightime midway in the cavity, away from both bottom and entrance. Although this issue

has not been yet subjected to thorough research, we suggest that assuming such a position

represents a compromise between the needs to be protected from cold and predators and the need

to avoid hypoxia and hypercapnia at the bottom.

The average respiratory exchange ratio (CO2/O2) calculated from partial gas pressures in

the nest cavity during the breeding season (Fig. 5; n=51) was 0.64±0.06, not significantly

different from the value given in Table 5, or from the value of normal RQ of birds (0.8-0.85).

Hence, this value indicates that the gas exchange of the nest cavity is chiefly a result of

convective bulk flow, as suggested by Birchard et al. (1984).

Nestlings' growth and fledging. - Typical to woodpeckers and some other hole nesters, the

Syrian woodpecker exhibits a relatively short incubation and long hatching to fledging time.

Instead of the normal ratio of fledging to hatching in most altricial birds (~1), in the present study

the ratio found is ~2.3. However, the sum of the two processes is not significantly different from

that of altricial birds of the same mass in general (Yom-Tov and Ar, 1993). This indicates a time

shift towards incubation shortening and prolongation of hatching to fledging time. The general

shape of the nestlings' growth curve shows a maximum rate at the age of about 7-8 days. The

observed feeding rate of about 10 items/hr seems to be the maximum that parents can provide.

However, the prey might increase in size as the hatchlings grow. While intensive growth might

be associated with high specific oxygen consumption rate, hatchlings mass at this age, which is

10-11 gr, is not sufficient to reduce considerably oxygen pressure in the nest. The latter occurs

much later, when hatchings are about 15 days old, reach a mass of about 60 gr (more than 90% of

21

their fledging mass), indicating that during early stages of development hatchlings have little

influence on the gas composition inside the nest cavity.

Oxygen consumption and CO2 production rates in an occupied nest. - The results of Table

5 indicate that in contrast to the assumption made in the Methods section, the nest cannot be

considered as a simple metabolic chamber. The relatively wide entrance and possible cracks in

the tree trunk apparently enabled gas exchange across them which reduced the O2 pressure

difference and the CO2 pressure between the nest and the environment. As a result, the apparent

O2 consumption and CO2 production rates gave underestimated values. A better experimental

approach is needed to obtain in situ gas exchange values.

As discussed above, in their special nest environment, the evolution of reducing

incubation time coupled with the prolongation of hatching-to-fledging time, combined with

parents and nestlings' behavior, all grant woodpeckers a unique solution for their successful

existence.

ACKNOELEDGMENTS

We wish to thank A. Yogev and family, A. Atzmon, and O. Hatzofe for their share in

performing the field research. M. Yaniv and the crew of the Canadian Center for Ecological

Zoology of the Department of Zoology at Tel-Aviv University for their help in maintaining the

birds. D. Katz helped in difficult moments.

22

LITERATURE CITED

Handbook of chemistry and physics, 87TH EDITION, RCR. http://www.hbcpnetbase.com/

Ar, A., Yom Tov, Y. 1978. The evolution of parental care in birds. Evolution 32:655-669

Ar, A., Paganelli, C. V., Reeves, R. B., Greene, D. G., and Rahn, H. 1974. The avian egg: water

vapor conductance, shell thickness and functional pore area. The Condor 76:153-158.

Ar, A., and Piontkewitz Y. 1992. Nest ventilation explains gas composition in the nest-chamber

of the European bee-eater. Respiratory Physiology 87:407-418.

Ar, A., and Sidis, Y. 2001. Nest microclimate during incubation. Pages 143 - 160 in: Avian

Incubation: Behaviour, Environment and Evolution (D.C. Deeming, Ed.). Oxford University

Press, Oxford, UK.

Ar A., Barnea, A., Yom-Tov, Y., and Mersten-Katz, C. 2004. Woodpecker cavity aeration: a

predictive model. Respiratory Physiology and Neurobiology 144:237-249.

Birchard, G. F., Kilgore, D. L. Jr., Boggs, D. F. 1984. Respiratory gas concentrations and

temperatures within the burrows of three species of burrow-nesting birds. Wilson Bulletin 96:

451-456.

23

Howe, S., and Kilgore, D. L. Jr. 1987. Convective and diffusive gas exchange in nest cavities of

the northern flicker (Colaptes auratus). Physiological Zoology 60(6):707-712.

Leshem, A., A. Ar, and R. A. Ackerman. 1991.Growth, water and energy metabolism of the soft-

shelled turtle (Trionyx triunguis) embryo: effects of temperature. Physiological Zoology 64(2):

568-594.

Rahn, H., and A. Ar. 1974. The avian egg: incubation time and water loss. The Condor 76:147-

152.

Scholander and Evans, H. J. 1947. Microanalysis of fractions of a cubic millimeter of gas.

Journal of Biological Chemistry 169(3): 551-560.

Tracy,C. R., Welch,W.R., and Porter, W. P. 1980. Properties of air. A manual for use in

biophysical ecology. The University of Wisconsin, Madison, USA.

Turner, J. S. 1987. Blood circulation and the flows of heat in an incubated egg. Journal of

Experimental Zoology Suppl. 1:99-104.

Wickler, S. J., and Marsh, R. L., 1981. Effects of nestling age and burrow depth on CO2 and O2

concentrations in the burrows of bank swallows (Riparia riparia) Physiological Zoology 54:132-

136.

24

Yom-Tov, Y., Ar, A., and Mendelsson, H. 1978. Incubation behaviour of the Dead Sea Sparrow.

Condor 80:340-343.

Yom-Tov, Y., and Ar, A. 1993. Incubation and fledging durations of woodpeckers. Condor

95:282-287.

25

Table 1: Day and night temperatures of eggs, nest cavity and ambient. Figures in brackets

represent number of nest cavities.

Nest temperature (˚C)

Day time

among eggs among

nestlings

Egg

temperature (˚C)

Ambient

temperature (˚C)

Day 29.2±1.7 (4) - 34.6±2.8 (4) 26.0±2.4 (4)

Night 25.6±4.2 (4) 28.2±2.7 (2) 33.7±3.3 (4) 23.0±0.8 (2)

Mean 27.4±4.5 (8) 34.2±4.3 (8) 25.0±2.5 (6)

Difference

(significance)

3.6

(ns)

0.9

(ns)

3.0

(ns)

26

Table 2: Humidity (absolute and relative) and temperature in the egg, and inside and outside the nest cavity.

* - A heavy heat wave occurred on this day.

Outside nest cavity Nest cavity Egg

Humidity Humidity Humidity

Relative

(%)

Absolute

(kPa)

Temp

(ºC) Relative

(%)

Absolute

(kPa)

Temp

(ºC) Relative

(%)

Absolute

(kPa)

Temp.

(ºC)

Incubation

day

Nest

code

50 1.96 23.7 82 3.33 29.0 100 6.28 37.0 4 MW

53 1.80 21.4 70 2.53 26.9 100 5.65 35.1 2 EZ

20 1.13 30.0 44 1.87 30.0 100 6.37 37.3 5 * BT

63 2.32 22.7 94 4.13 30.7 100 6.67 38.1 6 BT

47±19 1.80±0.49 24.5±3.8 73±21 2.93±0.93 29.2±1.7 100 6.24±0.43 36.9±1.3 Means

27

Table 3: Water loss rate from 9 eggs (initial mass 5.4 g ± 0.4SD), measured in the laboratory (35ºC; 51% RH = 2.92 kPa) and in the

nest.

n – number of measurements; hr – hours in incubator.

Nest Egg

sequence

Incubation day on which an egg

was taken to the lab (for hrs)

Water loss rate (% of initial

egg mass/d) in the lab (n)

Water loss rate (% of initial egg

mass/d) in the nest (n)

Hatching

success

RS III -1 (69) 0.84±0.16 (2) 1.06±0.17 (3) +

EZ II 2 (72) 0.46±0.08 (3) 0.63±0.12 (2) -

RS IV 3 (22) 0.73 (1) 0.84±0.02 (3) -

BT I 3 (43) 1.14 (1) 0.96±0.07 (3) -

MW II 4 (74) 1.84±0.26 (4) 1.29±0.13 (5) -

RS V 4 (63) 0.82±0.00 (4) 1.01 (1) -

EZ III 5 (90) 1.37±0.06 (4) 1.26 (1) -

BT II 5 (90) 1.64±0.10 (7) 1.48 (1) -

MW IV 9 (32) 1.54±0.04 (3) 1.45 (1) +

Means*) ± SD 1.26 ± 0.24 1.11 ± 0.29

*) Means were calculated from the mean values of each egg.

28

Table 4: Eggshell water vapor conductance values (GH2O) of 9 eggs measured in the laboratory. ∆t = temperature difference between

egg and incubator, as a result of embryonic metabolic heat production. GH2O values are given in mg/(d·Torr) and (100mg/(d·kPa))

Nest Egg

sequence

Incubation day on which

an egg was taken to the lab

Measured GH2O values

mg/(d·Torr); (100mg/(d·kPa))

Calculated

∆t (ºC)

Temperature corrected GH2O values

mg/(d·Torr); (100mg/(d·kPa))

II 2 1.80 (24.47) 0.04 1.79 (24.33) EZ

III 5 2.02 (11.57) 0.17 1.98 (26.91)

III 1 2.13 (11.46) 0.02 2.13 (28.95)

IV 3 1.9 (25.82) 0.06 1.89 (25.69) RS

V 4 2.18 (29.63) 0.08 2.16 (29.36)

I 5 1.76 (11.83) 0.17 1.72 (23.38) BT

II 6 3.07 (41.73) 0.19 3.01 (40.91)

II 4 2.06 (28.00) 0.09 2.04 (27.73) MW

IV 9 2.26 (30.72) 0.7 2.09 (28.41)

Mean ± SD 2.09 ± 0.377 (28.41 ± 5.124)

29

Table 5: Total O2 consumption rate (MO2) and CO2 production rate (MCO2) and RQ at night for

two natural occupied woodpeckers' nests. (Measurements are mL[STPD]/min).

Nest Inhabitants n Nest

MO2

Nest

MCO2

Laboratory

MO2

Laboratory

MCO2

Adult male + 2

nestlings

1 of age 12-15 days 1 2.51 4.51 8.05 4.22

1 of age 19-22 days 3 3.09 13.44 8.65 4.54

Nestlings alone

2 3 of age 13-15 days 1 1.74 3.00 7.21 3.78

1 2 of age 19-22 days 1 2.09 1.52 5.41 2.84

1 2 of age 22-26 days 1 3.14 2.53 5.49 2.88

Mean 2.51 5.00 5.77 3.65

RQ 2.00 0.63

30

Table 6: Woodpecker location, time intervals and number of staying events in the sleeping cavity

during 8 hours stay at night (values are means ±se).

Time

interval

(min)

0.0-3.5 4.0–7.5 8.0–11.5 12.0–15.5 16.0-19.5 20.0-23.5 24.0-27.5 28.0 &

up

Times and number of event staying at the bottom

Mean event

count

52.7

±29.2

6.7

±2.9

5.0

±1.6

1.6

±1.7

0.3

±0.7

0.0

±0.0

0.0

±0.0

2.4

±0.9

% of total

bottom time

34.1

±12.9

5.4

±3.8

5.4

±4.0

1.5

±1.5

0.5

±1.2

0.0

±0.0

0.0

±0.0

2.8

±2.3

Total

bottom time

(min)

92.2 11.7 8.8 2.8 0.5 0.0 0.0 4.2

Times and number of event staying at the nest entrance

Mean event

count

53.5

±83.1

1.2

±1.5

0.3

±0.5

0.0

±0.0

0.0

±0.0

0.2

±0.4 - -

% of total

bottom time

47.4

±39.3

1.5

±2.2

0.5

±0.9

0.0

±0.0

0.0

±0.0

0.2

±0.4 - -

Total

entrance

time (min)

93.6 2.1 0.5 0.0 0.0 0.35 - -

Predicted stay in the cavity, away from bottom or entrance

Time

(%) 18.5 93.1 94.1 98.5 99.5 99.8 - -

31

FIGURE LEGENDS

Fig. 1: Inverse relationship between nest to ambient temperature difference (ƼC) and

ambient temperature (ºC). The linear regression of this relationship is also given in the figure.

Fig. 2: A comparison of changes in ambient to nest temperature differences (ƼC)

between an empty nest (open circles) and an occupied nest cavity (black circles) along a daily

cycle (hr).

Fig. 3: Cumulative water loss (%) from 4 eggs in the field, as a function of time from

onset of laying (days). Day 4 (vertical line) represents the beginning of active incubation.

Fig. 4: Mean (X±SD) nestlings mass (gr; open circles) and nestlings growth rate (g/day;

close circles) as a function of time from hatching. The star symbol represents hatchlings mass just

before fledging.

Fig. 5: Partial pressure differences (Torr) of O2 and CO2 at the bottom of the nesting

cavity from ambient air as a function of time from hatching (days). Second order polynomial

curves were fitted to the data.