Environmental and behavioral influences on the comparative energetics of Anhingas, Double-crested Cormorants, and Flight...


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Environmental and behavioral influences on the comparative energetics of Anhingas, Double-crested Cormorants, and Flightless Cormorants
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v, 95 leaves : ill., maps ; 28 cm.
Hennemann, Willard W., 1954-
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Anhinga anhinga   ( lcsh )
Cormorants   ( lcsh )
Zoology thesis Ph. D
Dissertations, Academic -- Zoology -- UF
bibliography   ( marcgt )
non-fiction   ( marcgt )


Thesis (Ph. D.)--University of Florida, 1982.
Bibliography: leaves 91-94.
Statement of Responsibility:
by Willard W. Hennemann, III.
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I thank my committee members for their support and advice:
Pierce Brodkorb, John Kaufmann, J.D. Martsolf, and especially my chair-

main, Brian McNab. Their considerable investment in me and intellectual

stimulation of me shaped my maturation as a scientist.

Ralph Heath and the Suncoast Seabird Sanctuary provided me with

Double-crested Cormorants. Steve Thompson provided friendship, advice,

and served as reviewer for numerous manuscripts and letters. Mike

Konecny gave me, in addition to friendship, invaluable assistance in

many phases of the project; without his help the Galapagos segment of

the study would never have been attempted.

I am also indebted to Thomas Emmel, John Anderson, Frank Nordlie,

and Carmine Lanciani for the many favors they have done for me in the

past, and for the support and encouragement given me.

Most of all I would like to thank my wife, Jeanne, my parents, and

my family. I thank Jeanne for allowing me the freedom to work odd

hours, travel to distant places, and lead the far from "normal" life of

a biologist, while still being a constant source of love, understanding,

and constructive criticism. I thank my parents and my family for pro-

viding me with an enriched environment in which to develop, financial

and emotional support, and just the right amount of direction. Without

their help my graduate career and dissertation research would not have

been possible.

This research was funded by grants from Sigma Xi, the Frank M.

Chapman Memorial Fund, and NSF (# DEB 7906056).







Field Studies . .
Laboratory Studies . .


Anhingas . .
Double-Crested Cormorants .
Flightless Cormorants .


Energetics: Day versus Night .
Energetics: Incident Radiation .
Evaporative Water Loss .
Plumage Wetting . .








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. 91

Abstract of Dissertation Presented to the Graduate Council
of the University of Florida in Partial Fulfillment
of the Requirements for the Degree of
Doctor of Philosophy



Willard W. Hennemann, III

August 1982

Chairman: Brian McNab
Major Department: Zoology

The behavior of free-living Anhingas (Anhinga anhinga), Double-

crested Cormorants (Phalacrocorax auritus), and Flightless Cormorants

(Phalacrocorax harrisi) was monitored in the field simultaneously with

ambient temperature and solar intensity. The frequency of spread-

winged behavior in A. anhinga and P. auritus increased at higher solar

intensities and was inversely correlated with ambient temperature;

both relationships were much stronger in Anhinga. Spread-winged be-

havior in P. harrisi showed no apparent relation with solar intensity

and was positively correlated with ambient temperature. Anhingas ex-

hibiting spread-winged postures oriented with their backs to the sun,

maximizing the surface area exposed to insolation, and maintaining their

back normal to the sun's rays. Phalacrocorax auritus and P. harrisi

also oriented nonrandomly, but, unlike A. anhinga, less than 50% of

the cormorants observed "sunning" oriented with their backs to the sun.

Anhinga anhinga and P. auritus faced into the sun during gular flutter,

thereby minimizing the surface area exposed to the sun and reflecting

much of the incident radiation.

Laboratory measurements showed that A. anhinga has a lower basal

metabolic rate and a higher thermal conductance than expected from body

mass, while P. auritus has a higher basal metabolic rate and a higher

thermal conductance than expected. Both species had lower basal

metabolic rates, body temperatures, and thermal conductances at night.

Basal metabolic rates and rates of evaporative water loss of both

species were elevated under simulated solar radiation as compared to

daytime without incident radiation. Both species have elevated meta-

bolic rates and thermal conductances while wet. In the laboratory and

in the field, P. auritus only exhibited spread-winged postures when

wet; A. anhinga readily displayed such postures regardless of plumage

condition. Thermal conductance in cormorants is unchanged during

exposure to incident radiation, but Anhingas use spread-winged pos-

tures to enhance insolation absorption, thereby reducing their thermal

conductance and metabolic rates at low ambient temperatures, and

extending the thermoneutral zone. These physiological and behavioral

differences between Anhingas and Double-crested Cormorants may explain

the differences in their geographic distributions.


Few quantitative data are available concerning thermoregulation

in anhingas (Anhingidae) and cormorants (Phalacrocoracidae), two

closely related families of the Order Pelecaniformes. Bartholomew

et al. (1968) examined gular fluttering as a mechanism for evaporative

cooling in a series of birds including cormorants, and King and Farner

(1961) reported the body temperatures of the Great Cormorant

(Phalacrocorax carbo) and the Double-crested Cormorant (Phalacrocorax

auritus) as 39.8 degrees C and 40.1 degrees C, respectively. However,

virtually nothing has been published concerning the basal metabolic

rates, thermoneutral zones, and overall metabolic responses of these

birds to fluctuating ambient temperature.

Thermoregulation in these two families is especially interesting

because of their conspicuous spread-winged behavior. Both the Double-

crested Cormorant and Anhinga (Anhinga anhinga), common to Florida,

utilize a spread-winged posture, the function of which has been the

subject of considerable debate (see Clark 1969, Kennedy 1969 for

reviews). Spread-winged postures are found primarily within the

Ciconiiformes (Clark 1969, Curry-Lindahl 1970, Kahl 1971), Falconi-

formes (Clark 1969, Hatch 1970, Cade 1973, Grier 1975) and Pelecani-

formes (Snow 1966, Clark 1969, Curry-Lindahl 1970). Several functions

have been proposed for this spread-winged posture including balancing

(Rijke 1968, Kahl 1971), feather maintenance, shading of nest contents


and use as a social display (Kahl 1971), molt and skin conditioning

(Potter and Hauser 1974), wing drying (Rijke 1968, Kennedy 1969,

Kahl 1971), vitamin D production (Kennedy 1968, 1969), ectoparasite

removal (Kennedy 1969), and thermoregulation (Heath 1962, Clark 1969,

Kennedy 1969, Kahl 1971, Siegfried et al. 1975, Berry 1976). All of

these proposed functions may apply in certain species under certain

conditions; that is, there may be no one function for this behavior.

However, the two most commonly cited functions, which have been pro-

posed for the greatest number of species (including anhingas and

cormorants), are wing drying and sunning for thermoregulatory reasons

(Grier 1975).

Sunning (basking) behavior is widely studied among ectothermic

vertebrates (Heath 1970, Greenberg 1980), but the effects of incident

radiation and its importance in energetic are often overlooked in

studies of endotherms. In environments that impose energetic stress,

the tapping of auxiliary energy sources such as insolation could re-

duce an endotherm's costs of thermoregulation. Sunning behavior has

been reported within several diverse avian orders including Passeri-

formes (Hauser 1957, Lanyon 1958), Cuculiformes (Ohmart and Lasiewski

1971, Grier 1975), Ciconiiformes (Clark 1969, Curry-Lindahl 1970,

Kahl 1971), Psittaciformes (Cade 1973), Falconiformes (Clark 1969,

Hatch 1970, Cade 1973, Grier 1975), and Pelecaniformes (Snow 1966,

Clark 1969, Curry-Lindahl 1970).

The fact that birds can take advantage of solar radiation to

reduce the metabolic costs of endothermy has been demonstrated for

several species of diverse origins (Hamilton and Heppner 1967a,

1967b, Morton 1967, Lustick 1969, 1971, Heppner 1969, 1970, Lustick

et al. 1970, De Jong 1976). Ohmart and Lasiewski (1971) have shown

that Roadrunners (Geococcyx californianus) utilize solar radiation in

conjunction with nightly hypothermia to reduce metabolism, and there-

fore food intake. A similar mechanism has been proposed for the

Turkey Vulture (Cathartes aura) by Heath (1962). Nocturnal tempera-

ture decline may be widespread among avian species (Irving 1955).

The role, if any, that sunning plays in most of these cases is largely


The capacity to reduce energetic requirements through insolation

absorption is enhanced by dark pigmentation (Hamilton and Heppner 1967a&b,

Heppner 1970, Lustick 1971). An increase in surface area exposed to

the sun (such as with a spread-winged posture) increases overall

solar energy interception, i.e., sunning. At ambient temperatures

below thermoneutrality insolation may, therefore, be an aid to thermo-

regulation for many species, allowing them to reduce rates of heat

loss (thermal conductance). However, at higher ambient temperatures

insolation may tax the abilities of darkly pigmented birds to dissipate

heat produced by metabolism and to maintain normal body temperatures

in warm, humid environments such as Florida (Wunder 1979).

Cormorants and anhingas are excellent subjects fora study exam-

ining the relationships among insolation, spread-winged behavior, and

thermoregulation because of their conspicuous use of the spread-winged

posture and their predominately black coloration. In addition to

overall dark coloring, the Anhinga has a subalular apterium of darkly

pigmented skin (George and Casler 1972), which potentially has a

thermoregulatory function similar to the interscapular apterium of

the Roadrunner (Ohmart and Lasiewski 1971). Spread-winged behavior

within these two families has been considered as wing drying, as both

anhingas and cormorants have water absorbing plumage (Rijke 1968,

Casler 1973) that allows water to penetrate air spaces in the plumage,

reducing buoyancy and facilitating underwater prey capture.

This study examines the thermoregulation of the Anhinga and the

Double-crested Cormorant in the laboratory, and their behavior in the

field to determine 1) the effects of insolation on energetic and

behavior, and 2) whether their energetic and behavior support either

a wing drying or thermoregulatory function for spread-winged behavior.

Also included is a look at spread-winged behavior and thermoregula-

tion in the Flightless Cormorant (previously Nannopterum harrisi, now

Phalacrocorax harrisi, Mayr and Cottrell 1979), which shares this

behavior with its cormorant relatives.


Field Studies

Anhingas and Double-crested Cormorants

I observed Anhinga behavior at Lake Alice, 290 39' N lat.,

820 20' W long. (fresh water) in Gainesville, Florida, and Double-

crested Cormorants at Seahorse Key, 290 34' N lat., 830 4' W long.,

Florida (salt water), Lake Wauberg, 290 38' N lat., 820 34' W long.,

near Micanopy, Florida (fresh water), Bivens Arm, 290 38' N lat.,

820 18' W long., in Gainesville, Florida (fresh water), and Lake

Alice. Observations were made at all times of the day and in all

seasons during 1978-1979 (Anhingas) and 1979-1980 (cormorants). At

5-min intervals I recorded (1) the amount of time that each bird

under observation spent performing activities such as wing spreading,

preening, foraging, and gular flutter, (2) the orientation of each

individual with respect to wind and sun, (3) ambient (shade) tempera-

ture, and (4) the intensity of solar radiation measured with an

Eppley precision spectral pyranometer. This instrument measures both

direct and diffuse radiation in a 1800 field and was aimed directly at

the sun to assess the radiation levels available to sunning birds.

Unless otherwise indicated, all discussions of solar radiation in this

study refer to solar radiation measured in this fashion. The behavior

recorded at the end of each interval was considered one observation

of that behavior. If the individual under observation exhibited

more than one behavior during the 5-min interval, I recorded the

fraction of the interval devoted to each behavioral category as

no. of total observations of the behavior X 100
total no. of observations

under each specific set of environmental conditions. For example, if

I made 20 observations of Anhingas while the intensity of solar

radiation was below 222 W/m2 and ambient temperature (Ta) was between

0 and 50C, and in 2 observations birds were preening, then preening

was considered to represent 10% of the behavior observed under those

environmental conditions. I then examined these data for correlations

between the frequency of certain behaviors and environmental conditions.

Because Double-crested Cormorants are nonterritorial (unlike

Anhingas) and moved more frequently and over longer distances than did

Anhingas, it was frequently impossible to follow individuals for ex-

tended time periods. This inability to follow individuals made it

difficult to take accurate time budget data. Therefore, while observ-

ing cormorants, in addition to the data on individual birds (described

above), I also recorded the following data on the entire visible popu-

lation: number of individuals in the water, number perched out of

the water, number engaged in spread-winged behavior, and number of

individuals gular fluttering. These data recorded on the population

as a whole were used to determine the frequencies of the behaviors

listed above.

Flightless Cormorants

I observed Flightless Cormorant behavior in the vicinity of

Caleta Tagus, 00 15' S lat., 91 22' W long., Isla Isabela, Galapagos,

Ecuador, during July and August 1980. Observations were made at all

times of the day and night during the study period. At 5 minute

intervals I recorded (1) behavior, (2) orientation to sun and wind,

(3) shade Ta, and (4) solar intensity as measured with a black-body

thermometer constructed from a 5 cm by 5 cm piece of wood with a groove

into which a thermometer was fitted and covered with a fine sheet of

brass, spray-painted black. Occasional measurements of direct solar

radiant intensity were made with an Eppley precision spectral


In addition, body temperatures were measured simultaneously with

behavioral and environmental data using miniature, temperature-

sensitive, radio transmitters (Model T, Mini-mitter Co., Indianapolis,

Indiana) that emit a train of pulses, the frequency of which is tem-

perature dependent. These were received with a Lafayette walkie-

talkie. Transmitters were calibrated using a temperature controlled

water bath with a thermostat and a mercury and glass thermometer.

Cloacal Tb's were also taken with a Schultheis thermometer whenever

it was possible to do so without interfering with behavioral observa-

tions. Using these techniques, I monitored Tb's during the per-

formance of various behaviors such as spread-winged behavior, foraging,

and gular flutter, as well as for 24 hour cycles to determine normal

daily rhythms.

Laboratory Studies

I hand-raised four Anhingas (2 adult females with an average

weight of 1.12 kg; 2 juvenile females averaging 0.93 kg), housed them

in an outdoor aviary in which they were exposed and acclimated to

Gainesville weather conditions, and maintained them on a diet of

whole smelt and minnows. I borrowed five Double-crested Cormorants

(2 adults and 3 juveniles, mean weight = 1.33 kg) from the Suncoast

Seabird Sanctuary in Indian Shores, Florida, and maintained them as

with the Anhingas. I measured temperature-specific rates of metabolism

for each individual over a range of ambient temperatures (-10 to

450C) in an open flow system employing a Beckman G2 or Applied Electro-

chemistry S-3A oxygen analyzer. Measurements were made in a constant-

temperature chamber with a volume of 326 1, using flow rates of 4.4 to

6.8 1/min. Flow rates were measured with a Brooks R215-B rotameter

after the removal of CO2 and water; all values were corrected to

STPD. Chamber temperatures were measured with a mercury and glass

thermometer guarded with a radiation shield suspended inside the

chamber. I measured metabolic rates when the subjects were in a

postabsorptive state under the following environmental conditions:

(1) at night without incident radiation, (2) during the day without

incident radiation, (3) daytime with incident radiation = 450 watts/

meter2 (W/m2), (4) daytime with incident radiation = 700 W/m2.

Simulated solar radiation was provided by a pair of white heat lamps

(either 2 Westinghouse 125 W lamps or 1 125 W lamp and 1 GE 250R40/1

250 W lamp) positioned to shine through a 25 cm x 25 cm piece of Pyrex

(which transmits near ultraviolet) fitted into the chamber lid. The

subjects perched roughly 45 cm behind the Pyrex window, and radiation

intensities were measured at this distance using an Eppley precision

spectral pyranometer. I measured resting metabolism only after

chamber temperature had stabilized, equilibrium conditions had been

satisfied (Christensen 1947, Heusner 1955), and VO2 had stabilized.

I monitored the bird's deep body temperatures using Mini-mitters,

which were coated with beeswax and fed to the subjects. I also

measured cloacal temperatures after each metabolic trial using a

Schultheis thermometer. Both methods of measuring body temperature

yielded statistically similar results and are used interchangeably

throughout the text.

Mean basal rates of metabolism were estimated from independent

measurements of the minimal rate of oxygen consumption within the zone

of thermoneutrality. I estimated minimal thermal conductances (C )

from the relationship

Cm = VO2/(Tb-Ta) (1)

using simultaneous measurements of metabolic rate (V02), body tempera-

ture (Tb), and ambient temperature (Ta) at temperatures below thermo-

neutrality. I compared basal metabolic rates and minimal conductances

measured under control conditions (without incident radiation) with

those measured under experimental conditions (with incident radiation)

and with those expected from body mass. "Expected" values for basal

metabolic rate were calculated from the predictive equations derived

from Aschoff and Pohl (1970):

VO2/M = 4.0 M-027 (2)

for a nonpasserine in the quiescent phase of the diurnal cycle, and

VO2/M = 5.14 M-027 (3)

for a nonpasserine in the active phase of the diurnal cycle, where

VO2/M is basal metabolic rate in cm3 02/g h and M is mass in grams.

Expected values for mean minimal conductances were calculated from the

predictive equations of Aschoff (1980):

C/M = 0.947 M-0.583 (4)

for a nonpasserine in the quiescent phase of the diurnal cycle, and

C/M = 0.946 M-0"484 (5)

for a nonpasserine in the active phase of the diurnal cycle, where

C/M = "wet" thermal conductance in cm302/g h oC (Mcnab 1974), and

M is in grams.

To determine the effect of water on thermoregulation (during

daytime) each individual was placed unrestrained in water 16 cm deep
(to midbreast in Anhingas, to lower breast in cormorants) inside the
environmental chamber, at ambient temperatures of from 12 to 35C for

two hour time periods, while metabolic rate and body temperature were

monitored as described above. Equilibrial metabolic rates and Tb's

recorded under these conditions were compared with those recorded in

dry individuals. Before placing them in the chamber with water, each

bird was submerged fully (except for the head) for at least one

minute, until the plumage was saturated.

I also estimated evaporative water loss (EWL) to assess the in-

fluence of insolation both within and above the thermoneutral zone.

Evaporative water loss was measured during metabolic trials using

techniques similar to those described in Lasiewski et al. (1966).

Individual birds stood in the environmental chamber on a trap filled

with paraffin oil and covered with hardware cloth to capture any

excrement eliminated during the trial, thus removing a possible source

of error in the calculation of EWL.

The stream of air passing through the metabolic chamber was

analyzed for water content immediately after leaving the chamber.

I measured total water content gravimetrically by passing the air

stream through drying tube filled with dessicant (Drierite) for a

known time interval and at a constant flow rate. I then calculated

the evaporative water loss from the subject by subtracting out the

water content of room air, which was measured gravimetrically by

drying room air in a fashion similar to that used on the sample coming

from the environmental chamber. At high environmental temperatures

inside the chamber the stream of air coming from the chamber was

heated with a heating coil (controlled with a rheostat) wrapped

around the tubing housing the air stream to prevent condensation be-

fore the drying tube. As with metabolic measurements, measurements

of EWL were made only after equilibrium conditions had been satisifed

(Lasiewski et al. 1966). After calculating EWL over a range of

chamber temperatures for each species and under each set of


environmental conditions (daytime without incident radiation, daytime
with incident radiation = 450 W/m2, daytime with incident radiation =

700 W/m2), I compared the rates of evaporative water loss under each

set of environmental conditions both within and between species.



My field observations on Anhingas are summarized in Table 1.

Behavior in general, and wing spreading in particular, strongly depends

on weather. Anhingas exhibit spread-winged postures much more fre-

quently during cool than during warm weather. The frequency of this

behavior is negatively correlated with air temperature (Fig. 1, r =

-0.85, p < 0.01, 9df) but positively influenced by the intensity of

solar radiation (Table 1). When the intensity was less than 222 W/m2

(cloudy days with mostly diffuse radiation), spread-winged behavior

constituted only 3.8% of the observed behavior, but it accounted for

46.5% of the observed behavior when solar intensity exceeded 222 W/m2

(Ta < 300C in both cases, p < 0.001, test for the equality of two

percentages, Sokal and Rohlf 1969). When solar radiation levels were

low (e.g., during early evening), birds just emerging from the water

often fanned their wings and tails continuously (fan drying, Table 1)

rather than holding them steady (as was usually the case).

Thirty-four percent of the observed spread-winged behavior in-

volved birds that appeared to be wet, 49% involved individuals that

appeared to be dry, and 17% involved individuals whose plumage con-

dition could not be determined. Wet birds usually held their wings

completely outstretched, whereas dry individuals often held them

closer to the body or occasionally drooped at their sides. During

Table 1. Time budgets for Anhingas under various environmental conditions

Conditions Behavioral Frequency (%)

Solar Sun & Sun Gular nervin Fan Total
Intensity Ta Sunning Preen Total Preen Perching Flutter Swim Posture Dry Observ.

<222 W/m2 <300C 1.6 2.2 3.8 13.0 43.6 0.0 5.4* 31.8* 2.5* 387

>222 W/m2 <30C 40.2* 6.3 46.5* 9.7 22.1 2.6 16.9 1.6 0.0 860

<222 W/m2 >30C 10.0 0.0 10.0 28.0 32.5 0.0 16.9 0.0 0.0 25

>222 W/m2 >300C 8.8 0.0 8.8 17.1 32.0 23.8* 18.2 0.0 0.0 111

Total Time Budget 26.3 4.6 30.9 11.4 29.1 3.5 14.0 9.4 1.1 1383

Behavioral Frequency = percent of total observations recorded under those conditions in which that specific
behavior was observed (see text).

Sunning refers to spread-winged behavior without accompanying preening.

Sun & Preen refers to spread-winged behavior accompanied by preening.

*Statistically significant difference (Test for the equality of two percentages, Sokal and Rohlf 1969).

Figure 1. Relationship between frequency of spread-winged behavior and ambient temperature
for Anhingas and Double-crested Cormorants


100 -

"75 -

CC 50



20 30 40


-n 00 o Y=3.26- 0.067X
'-'~~~~' ~ ----- ----------p



spread-winged behavior Anhingas commonly held their wings and body

perpendicular to the direct beam incident solar radiation, flattening

out when the sun was high, standing erect when the sun was low.

Concordantly, most birds displaying spread-winged postures oriented

with their backs to the sun; in only 16 or 3.4% of 468 observations

did they orient differently. In these 16 cases, all had wet plumage,

most (14/16) were facing into the wind, and most (14/16) were observed

when the intensity of solar radiation was less than 222 W/m2. The

frequency with which Anhingas oriented with back to the sun was also

negatively correlated with Ta (r = -0.83, p < 0.01, 9df).

Anhingas oriented quite differently while heat stressed (exhibit-

ing gular flutter), facing into the sun 53% of the time, obliquely

(side to the sun) 36% of the time, and away from the sun only 11% of

the time (55 observations). This orientation is statistically non-

random (X = 43.12, p < 0.001, 2 df). Gular flutter occurred when T

was between 25 and 300C, but only when the intensity of solar radia-

tion exceeded 700 W/m2. All other observations of gular flutter oc-

curred when Ta was above 30C. Gular flutter was significantly more

common at high levels of solar radiation (Table 1) and was never

accompanied by a spread-winged posture. Orientation during gular

flutter (predominately facing the sun) is similar to that during ex-

posure to heavy winds in which individuals usually face into the wind,

thereby exposing a minimum of surface.

Anhingas spent 14.0% of the time foraging in the water during

the study. The bulk of their time (comprising over 80% of the total

observations) was spent perching (preening, sunning, or just sitting).
They spent significantly less time in the water when Ta was below 250C

(10.8% of 783 total observations) than when it exceeded 25C (23.8%

of 600 total observations, test for the equality of two percentages,

p < 0.001).

After leaving the water Anhingas shook excess water from their

plumage, and almost invariably spread their wings. However, they also

displayed spread-winged postures with dry plumage before entering the

water. Seventy-one percent of all trips to the water, and 90% of all

such trips when solar radiation exceeded 222 W/m2, were preceded by

spread-winged behavior. This value increases to 94% if one considers

only those occasions when Ta was below 300 and solar radiation exceeded

222 W/m2

At low Ta, both in the field and during metabolic trials, Anhingas

commonly folded their necks in a tight S-shape and pressed them tightly

against the upper body. Occasionally, individuals assumed a posture

in which the head and neck were laid along the back and covered with

the wings. Both postures should reduce thermal conductance by reducing

surface area and I, therefore, labelled them heat conseAving postuwes

(Table 1).

Double-Crested Cormorants

Field observations of individual cormorants are summarized in

Table 2; data taken on the population as a whole are presented in

Table 3. Unlike Anhingas, the behavior of Double-crested Cormorants is

not especially sensitive to weather. The frequency of spread-winged

behavior in these cormorants is negatively correlated with ambient

temperature (Fig. 1) (r = -0.54, p > 0.05, 5 df) but not as dramatically

as in Anhingas. As with Anhingas, spread-winged frequency is positively

Table 2. Frequencies for the behavior of individual Double-crested Cormorants under various
environmental conditions


Behavioral Frequency (%)

Ta Total
(C) Observations



Preening Perching

Gular Head
Flutter Under

>222 <20 337 4.3 0.3 30.7 49.5 12.2 3.0 0.0

<222 <20 122 0.8 0.0 23.4 70.1 0.0* 5.7 0.0

>222 >20 276 1.6 0.0 27.4 64.8 4.7 0.0* 1.5*

<222 >20 39 0.0 0.0 33.8 63.6 0.0* 2.6 0.0

774 2.6 0.1 28.5 58.8 7.1 2.3 0.5

*Significantly different (P < 0.05) from the
two percentages (Sokal and Rohlf 1969)

other percentages in the column (test for the equality of



Table 3. Frequencies for the behavior of a population of Double-crested Cormorants under various
environmental conditions

Environmental Conditions

Solar Intensity T Total Spread-wingeda Deltaa Gulara Percent in Percent out
(W/ma) () Observations Behavior Posture Flutter Water Water

<222 <20 825 2.0 0.0 0.0 7.8 92.2

>222 <20 2,932 2.7 0.0 6.6 34.0 66.0

<222 >20 586 0.0 0.0 0.0 78.5b 21.5

>222 >20 1,179 1.2 4.5 17.1 22.2 77.8

aTaken as a percent of the behavior recorded on land (not including

bBiven's Arm (see text)

observations of birds in the water)

-influenced by solar intensity. Linear correlation between spread-

winged frequency and solar intensity reveals the relationship:

y = 1.88 + 0.O01x (r = 0.36, p > 0.05, 5 df). However, spread-winged

behavior never exceeded 4.1% of the observed behavior under any en-

vironmental conditions and accounted for only 2.3% of the total ob-

served behavior of cormorants on land (Table 3).

Spread-winged behavior was only observed in birds with (apparently)

wet plumage and was often accompanied by wing fanning. Unlike Anhingas,

cormorants did not exhibit spread-winged behavior before entering the

water and did not display any but full spread-winged postures, with

wings fully extended.

Orientation with respect to the sun during spread-winged behavior

was nonrandom (x2 = 11.11, p < 0.005, 2 df) with 39.2% of the birds

facing away from the sun, 43% facing obliquely to the sun, and 17.8%

facing into the sun. Unlike Anhingas, Double-crested Cormorants did

not hold their wings and bodies perpendicular to the sun during spread-

winged behavior but always stood erect, never flattening out when the

sun was high. Orientation with respect to the wind was also nonrandom

(X2 = 51.88, p < 0.005, 2 df) with 17.9% facing away from the wind,

26.1% facing obliquely, and 56% facing into the wind during spread-

winged behavior.

As with Anhingas, cormorants also oriented differently during

gular flutter than when engaged in spread-winged behavior. Ninety per-

cent of all individuals engaged in gular flutter were facing the sun.

Gular flutter was observed at ambient temperatures as low as 120C with

incident radiation in excess of 1,000 W/m2 and was only observed once

when radiant intensity was below 222 W/m2 (Ta > 20C). Gular flutter

was never accompanied by a spread-winged posture.

Two behaviors were observed in Double-crested Cormorants that

were not observed in Anhingas. One such behavior was displaying spread-

winged postures while floating on the water's surface, which was ob-

served on 4 occasions in cormorants at Lake Wauberg. This variation

of spread-winged behavior has also been reported for European Cormorants

(P. carbo) and for Shags (P. aristotelis) (Fry 1957). The second

behavior unique to cormorants was, again, a variation of spread-winged

behavior, in which the wings were not held straight out to the side,

but were bent at the elbow and folded down into a delta-winged posture

commonly observed in storks (Kahl 1971). This behavior was only ob-

served at Seahorse Key (where much of my hot weather data were recorded)

with Ta in excess of 30C and solar radiant intensity above 900 W/m2

and was usually accompanied by gular flutter. Orientation during this

behavior was invariably facing into the sun.

Cormorants spent 32.3% of their time in the water during the

study, but, as with Anhingas, the bulk of their time was spent perch-

ing. Although cormorants spent more time in the water when Ta exceeded

200C (28.3% of the observations recorded with Ta < 200C as compared to

40.9% of the total observations with Ta > 200C, p < 0.001, test for the

equality of two percentages), the significance of this difference may

be entirely due to sampling error, as many of the observations of

birds at ambient temperatures above 20C were recorded at Biven's Arm,

where large rafts of cormorants were commonplace (apparently) irre-

spective of weather. This rafting behavior was not observed at the

other study sites and may have unfairly skewed the data with respect

to time spent in the water. However, this rafting behavior, and my

subjective observations, suggest that cormorants spend longer time

periods in the water at a stretch, and as a percentage of the day,

than do Anhingas.

Flightless Cormorants

A time budget summarizing the behavioral data for Flightless

Cormorants is presented in Table 4. I never observed Flightless

Cormorants exhibiting spread-winged postures while having dry plumage;

true spread-winged behavior was exhibited only after the animal had

left the water. Only once was a cormorant observed to leave the water

without subsequently displaying this behavior. As with Anhingas and

Double-crested Cormorants, I never observed spread-winged behavior in

Flightless Cormorants accompanied by gular flutter. A drooped-winged

posture was observed in dry individuals, often while tending the nest.

This posture differed from true spread-winged behavior in that the

wings were not fully extended out to the sides but were held loosely

downward at the side of the body. Drooped-winged postures were accom-

panied by gular flutter 87% of the time and were most commonly ob-

served when the sky was cloudy and ambient temperatures were moderate

(Tables 5, 6). Gular flutter was most commonly observed (as expected)

during sunny conditions and at high ambient temperatures (Table 5, 6).

Spread-winged behavior was most commonly observed when the sky

was cloudy and ambient temperatures were high (Tables 5, 6). Linear

correlation between the frequency of spread-winged behavior and

ambient temperature reveals a positive relationship (just the opposite

of Anhingas) with r = 0.92 (p < 0.05). Correlation between the

Table 4. Time budgets for Flightless Cormorants on and off of the nest

Behavioral Frequency (%)a

Spread- S-W &b Preen Sitting Standing Gular Drooped- Fan Head Otherc Total
winged Preen Flutter winged Dry Under Observa-
Wing tions

Nest 1.3 0.6 4.0 36.8 15.8 37.5 6.7 2.2 5.5 3.4 806

Off of
Nest 5.8 11.2 38.7 2.0 29.1 9.4 0.8 0.0 7.0 2.3 395

Combined 2.8 4.1 15.4 25.3 20.2 28.4 4.7 0.2 5.9 3.0 1201

aBehavioral Frequency = percent of
Behavioral categories are not
Preening while spread-winged

total observations devoted to
mutually exclusive.

that particular class of behaviors.

COther includes interacting socially, arranging nest material, shaking off, walking, etc.

Table 5. Some behavioral frequencies for Flightless Cormorants exposed to different amounts of
sky cover

Behavioral Frequency (%)a

Sky Cover Spread-winged Drooped-winged Gular Total
Behavior Posture Flutter Observations

Clear 8.94 8.63 52.52 475

Cloudy 12.98 15.58 44.15 39

Shadec 2.95 4.43 8.13 271 1\

aBehavioral Frequency = percent of total observations recorded under those sky conditions
devoted to that specific behavior
Total Observations refers to all observations recorded for birds on land under those specific
sky conditions
CShade refers to observations recorded when the subject was in the shade or when the sun
had set.

Table 6. Some behavioral frequencies for Flightless Cormorants exposed to different ambient

Behavioral Frequency (%)a

Ta Spread-winged Drooped-winged Gular Total b
Behavior Posture Flutter Observations

20-22.50C 8.25 0.61 10.39 164

22.5-250C 8.09 11.74 38.25 247

25-27.50C 11.63 10.34 45.68 232

27.5-30C 12.32 0.91 65.75 110

aBehavioral Frequency = percent of total observations recorded under those ambient temperatures
devoted to that specific behavior
bRecorded for cormorants on land in that specific temperature range

duration of spread-winged sunning episodes (the length of time the

wings were extended during a bout of sunning) of individual cormorants

and ambient temperature reveals a negative relationship with r = -0.28

(p > 0.05). Linear correlations between the duration of "sunning"

episodes and black-body temperature reveals a negative relationship

with r = -0.35 (p < 0.05).

Orientation of individual birds with respect to the sun during

spread-winged behavior was nonrandom (p < 0.01), with the primary skew

in the data favoring orientation with back to the sun; 46% of all ob-

servations of "sunning" birds were of individuals orienting with back

to the sun. Unlike Anhingas and Double-crested Cormorants, however,

orientation of Flightless Cormorants during gular flutter was virtu-

ally identical to orientation during spread-winged behavior, with

the primary skew in the data favoring orienting with back to the sun

(42%). In fact, orientation of cormorants without regard for behavior

was nonrandom, again with the primary skew in the data favoring orien-

tation with back to the sun (42%). Therefore, orientation in Flight-

less Cormorants does not depend (apparently) on behavior; these cormor-

ants preferentially orient with back to the sun and avoid orientations

in which they face into the sun. Orientation of all birds observed,

however, did vary with sky cover (Table 7).

Orientation to the wind during spread-winged behavior was non-

random (p < 0.05), with the primary skew favoring facing into the wind

(42%). Only 13.5% of the birds observed "sunning" were facing with

back to the wind. Orientation of Flightless Cormorants to the wind,

regardless of behavior, was again nonrandom (p < 0.05), and again the

primary direction of data skew was in favor of facing into the wind,

Table 7. Orientation of Flightless Cormorants under different sky conditions.

Orientation (% of total observations)

Sky Cover Back to the Sun Side to the Sun Front to the Sun Total Observations

Clear 48 38 14 492*

Partly Cloudy 62 36 2 46*

Overcast 26 55 19 230

Sun Set 42 56 2 57*

*Nonrandom Orientation (Chi-square, 2 df)

regardless of wind strength (34.7% of observations with wind calm to

light, 46.7% of observations with wind moderate to heavy were of birds

facing into the wind).

The amount of time spent foraging was impossible to estimate ac-

curately for these cormorants, as they frequently swam out of sight and

often left the water and "sunned," or simply rested far from the nest

(and from view). However, foraging represented at least 9.8% of the

total behavior observed (based on observations of subjects swimming in

view). Eleven foraging bouts witnessed start to finish lasted from 5

to 43 minutes in length (average = 18.4 minutes).

Body temperatures measured for Flightless Cormorants during various

behaviors and under different conditions are presented in Table 8. The

Tb's averaged higher during the day than at night, while gular flut-

tering as opposed to while not gular fluttering (day only), before

entering the water as opposed to leaving the water, and before exhibit-

ing spread-winged behavior as opposed to after "sunning" (Table 8).

The lowest body temperatures recorded were taken at approximately 0330

(mean Tb = 39.20C 0.32 SD).

Table 8. Body temperaturesa for flightless conditions under various conditions

Day Night Gular Not Gular Entering Leaving After
Flutter Fluttering Water Water Spread-winged

Range of Tb 38.7-41.3 38.7-40.2 39.8-41.3 38.7-41.2 40.3-41.2 39.0-41.2 39.4-40.1

Mean Tb 40.11 39.47 40.36 39.89 40.70 39.90 39.72

SD 0.52 0.47 0.29 0.58 0.47 0.64 0.34

Number of
Measurements 54 18 25 29 4 13 9

ain C


Energetics: Day versus Night

The relationships among metabolic rate, body temperature (Tb), and

ambient temperature for the metabolic trials featuring birds with dry

plumage and no incident radiation are presented in Figures 2 (Anhingas,

measured during the day), 3 (Anhingas, measured during the night),

4 (cormorants, measured during the day), and 5 (cormorants, measured

during the night).

Anhingas have lower than expected basal metabolic rates and higher

than expected thermal conductances; Double-crested Cormorants have

higher than expected thermal conductances and metabolic rates regard-

less of circadian phase (Table 9). Metabolic rates measured below

thermoneutrality during the day averaged 30-32% higher (Anhingas) and

15-30% higher (cormorants) than those measured at night. Body tempera-

tures averaged higher during the day than at night (Table 9) and gen-

erally rose with ambient temperature suggesting a tendency for heat

storage (Figures 2-5).

The slopes of the regression lines fitting the data presented in

Figures 2-9 cannot be used as estimates of thermal conductance because

these lines do not extrapolate to body temperature, indicating that

Anhingas and Double-crested Cormorants mix physical (i.e., postural

and plumage adjustments) with chemical thermoregulation (i.e.,

metabolism) at temperatures below thermoneutrality (McNab 1980).

Figure 2. Relationships among metabolic rate, body temperature, and ambient temperature
for 4 Anhingas as measured during the day








10 20 30 40

43 5

4 .0o J

405 1-
39 0
390 0
3e5 m

Figure 3. Relationships among metabolic rate, body temperature, and ambient temperature
for 4 Anhingas as measured during the night

405 0.
S 395
** .8* *
0 *


E \*

.O o**


\ oJ "

0 10 20 30 40 50

Figure 4. Relationships among metabolic rate, body temperature, and ambient temperature
measured for 5 Double-crested Cormorants during the day

S- 042

S. **0
: .
S_ ____-4o0


, xDAY
_ *


10 5

cn0 Q

o **

.I I I

o\ 9O

-5 0 10 20 30 40 50

Relationships among metabolic rate, body temperature, and ambient
measured for 5 Double-crested Cormorants during the night

temperature as

Figure 5.

10 20 30 40

42 L"


39 >-



o 1.0


H 05-

0 -

Table 9. Thermoregulation in Double-crested Cormorants and Anhingas: Day versus night

Species BMR (% Expected) Tb(in) Tb(below) T1 Cm (% Expected)

Phalacrocorax auritus

Day 0.85 115 41.2 40.7 21.0 0.0368 126
Night 0.74 128 40.2 39.7 17.5 0.0320 224
Anhinga anhinga

Day 0.60 75 39.9 39.7 29.5 0.0454 138

Night 0.55 89 39.1 38.0 26.0 0.0364 221

BMR is basal metabolic rate in cm 02/g-h

% Expected is a comparison of measured metabolic rates with expected values (equations 2 and 3)

Tb(in) is body temperature (oC) measured in thermoneutrality
Tb(below) is body temperature (oC) measured below thermoneutrality

T1 is the lower limit of thermoneutrality (C)

C is minimal thermal conductance in cm302/g-h-C

% Expected Cm is a comparison of minimal thermal conductances with expected values (equations 4 and 5)

Energetics: Incident Radiation

The relationships among metabolic rate, body temperature, and

ambient temperature during exposure to incident radiation are presented

in Figures 6-9. Mean body temperatures and basal rates of metabolism

in both species were higher under incident radiation, possibly reflect-

ing a higher activity level (Table 10). Thermal conductances were

lower under incident radiation, especially in Anhingas (Table 10).

Cormorants never displayed spread-winged postures with or without

incident radiation unless first fully soaked with water, and then only

for short intervals (rarely more than 10 min). No reduction in meta-

bolic rate was observed during these sunning episodes. Although

cormorant thermal conductances were slightly lower than control values
when the birds were exposed to 700 W/m2 incident radiation, and

slightly higher when exposed to 450 W/m2 (Table 10), neither differ-

ence was statistically significant. A comparison of the regression

lines fitting the three data sets (Fig. 10) indicates a slight but non-

significant (Table 10) reduction in slope under incident radiation.

Consequently, rates of metabolism measured below T1 with incident

radiation are virtually 100% of those measured without incident radia-

tion during exposure to 450 W/m2, and 90% under 700 W/m2 incident
radiation. Under incident light the extrapolated Tb (x-intercept)

is well above the actual Tb (Table 10), indicating that the added

physical factor (incident light) is being absorbed and is increasing

the physical component of thermoregulation. However, there is no

statistical difference in either thermal conductance or regression

slopes between the experimental and control data for Double-crested

Cormorants. Additionally, the lower limit of thermoneutrality (T1)


Table 10. A comparison of the energetic responses of Double-crested Cormorants and Anhingas to
variation in ambient temperature and incident radiation

Species Treatment BMR Tb Cm Cf r T1 Extrap.

Phalacrocorax auritus no lamp 0.85 40.70 0.0368 0.0281 -0.90 21.0 50.92
450 W/m2 0.91 41.110 0.0373 0.0230 -0.50 23.0 62.17
700 W/m2 0.95 41.360 0.0352 0.0176 -0.81 19.5 73.18
Anhinga anhinga no lamp 0.60 39.70 0.0454 0.0340 -0.92 29.5 47.06
450 W/m2 0.70 39.97 0.02900 0.0160* -0.79 17.5 61.84
700 W/m2 0.72 40.05 0.02720 0.0106* -0.59 17.0 84.98

BMR is basal metabolic rate in cm302/g-h

Tb is body temperature measured at temperatures below thermoneutrality in C

Cm is minimal thermal conductance in cm302/g-h-C

Cf is a measure of thermal conductance determined by the method of least squares (cm302/g-h-C)

T1 is the lower limit of thermoneutrality (oC)

Extrapolated Tb is the Tb to which the regression line fitting the data extrapolates
Experimental class differs significantly from control (Mann-Whitney U)

Experimental class differs significantly from control

Relationships among metabolic rate, body temperature, and ambient temperature
as measured for 4 Anhingas under 450 W/m2 incident radiation

Figure 6.

10 20 30 40 50

* 44



41 -

39 m





o o.0

3 0.5-


Relationships among metabolic rate, body temperature, and ambient temperature
as measured for 4 Anhingas under 700 W/m2 incident radiation

Figure 7.

43 n

,s O
41 -
40 -








0 t0 20 30 40 50

Figure 8. Relationships among metabolic rate, body temperature, and ambient temperature as
measured for 5 Double-crested Cormorants under 450 W/m2 incident radiation

10 20 30 40

43 L.





Lt. 0.5



Figure 9. Relationships among metabolic rate, body temperature, and ambient temperature as
measured for 5 Double-crested Cormorants under 700 W/m2 incident radiation



0 10



43 Q
42 2


10 20 30 40

Figure 10.

Comparison of the regression lines fitting control and experimental data sets for
Anhingas and Double-crested Cormorants

0 20 40 60 80 0 20


under incident radiation is virtually unchanged from that measured

under control conditions for this species (Table 10).

These results contrast with those for Anhingas. In the aviary I

observed spread-winged behavior in both wet and dry anhingas almost

daily, especially when ambient temperature was below T1. Attempts to

elicit this behavior in the experimental chamber were frustrated until

the incident radiation was increased to exceed 250 W/m2, indicating that

Anhingas have a threshold below which spread-winged sunning may not be

profitable. With incident radiation above this threshold and ambient

temperature below T1, experimental subjects generally extended their

wings with the onset of illumination, and often kept the wings spread

for an hour or more. Occasionally spread-winged postures were observed

above T1, but only for brief intervaTs.' Anhingas typically held the

wings perpendicular to the incident light, presumably to take full ad-

vantage of the heat-absorbing qualities of the dark plumage (Lustick

1980) and erected back and wing feathers to expose areas of the back.

With the onset of sunning, V02 steadily declined until a new equi-

librium was reached and spread-winged behavior ceased. This pattern

of continuously declining VO2 was never observed in trials in which

spread-winged behavior was absent. One individual frequently would not

sun or would not hold the spread-winged posture for longer than a

minute or two; this bird maintained metabolic rates and thermal con-

ductances equivalent to, or higher than, those observed under control

conditions. This suggests that the spread-winged posture is necessary

to reduce V02 significantly in the presence of incident radiation. In

birds displaying spread-winged postures, exposure to incident light

significantly reduced both thermal conductances and the slopes of the

regression lines (Table 10). The rates of metabolism measured under

experimental conditions at temperatures below T1 averaged 62% of those

measured under control conditions during exposure to 450 W/m2 and

only 56% of control under 700 W/m2. The reduction in thermal con-

ductance during exposure to insolation enables the Anhinga to lower T1

by 12 to 12.5C (Table 10).

Evaporative Water Loss

The relationships between log evaporative water loss and ambient

temperature for birds with dry plumage under varying intensities of

incident radiation are presented in Figure 11 (Anhingas) and Figure 12

(cormorants). Semilog plots were adopted so that these curvilinear

relationships could be transformed into linear relationships for the

purpose of comparing them statistically. In each species there is a

significant difference in the rate of evaporative water loss (p < 0.05,

Analysis of Covariance) between the measurements made without incident

radiation and those with radiation. However, there are no significant

differences (p > 0.05) between the responses to the two different in-

tensities of incident radiation. There is little difference in the

rate of evaporative water loss between the cormorant and Anhinga when

radiation is present, but in the absence of incident radiation the

Anhinga has a lower rate of water loss (Figs. 11, 12). Because the

Anhinga has a lower rate of metabolism under most conditions, the

Anhinga generally dissipates a larger portion of its metabolic heat

production (Hm) by evaporation (H ) than does the cormorant (Figs. 13,


Figure 11. Relationship between log evaporative water loss and ambient temperature as measured
for 4 Anhingas both with and without incident radiation

Anhinga anhinga


oo o
20- 0 0 100
0 .- 06

~~~~ ___. ^ -'y _______

- 0 -

S' 0

20 25


30 35 40




Figure 12. Relationship between log evaporative water loss and ambient temperature as measured
for 5 Double-crested Cormorants both with and without incident radiation

2.0 ,--- -100
-E o ---"' o ._
E -" E
O ,,-* o O

0) 0-
E 0 0 E
o l -- o
E oo E

0 0
w w
O -O/ o

0 0.
1.0- 0 INCIDENT RADIATION v 450 w/m2 10

20 25 30 35 40 45

Figure 13.

Relationship between the ratio of He/Hm and ambient
temperature as measured for 4 Anhingas both with
and without incident radiation

Anhinga Anhinga

O *


* *

* .



0.0 Ii
2.0 -


RADIATION = 0 w/m2



1f11 *



* *



Figure 14. Relationship between the ratio of He/Hm and ambient
temperature as measured for 5 Double-crested
Cormorants both with and without incident radiation

Phalacrocorax auritus


@ 0

* **




0 0



0.0 -

0.5 -







i I I I I
20 30 40



Anhingas were not observed to gular flutter during any metabolic
trial without incident radiation (day or night) even when Ta = 450C.

In cormorants, weak gular flutter first appeared at ambient tempera-

tures of from 35C to 37.50C (daytime) and generally increased in in-

tensity as Ta rose. In one instance gular flutter was observed in a

cormorant at night (Ta = 390C, Tb = 41.80C).

Under incident light, Anhingas exhibited gular flutter at ambient

temperatures as low as 290C with incident radiation = 450 W/m2 and as

-low aw-Z6.80C withT f ideTft-radiatTon =70O-W/m2.- Gular flutter was

observed in all trials in which ambient temperature exceeded 33.5C

(450 W/m2) and 32C (700 W/m2) and increased in intensity as Ta rose.

Gular flutter in cormorants exposed to incident radiation first appeared

at Ta = 330C (incident radiation = 450 W/m2) and at Ta = 200C (incident

radiation = 700 W/m2). Gular flutter was present in all trials in

which Ta exceeded or equalled 330C (450 W/m2) and 29C (700 W/m2)

and increased in intensity as Ta rose.

Plumage Wetting

Metabolic rates measured in birds with wet plumage, sitting in

16 cm of water, averaged 78-130% higher (Anhingas) and 15% higher

(cormorants) than those measured in dry birds during the day. Body

temperatures measured during exposure to these wet conditions ranged

from 36.80C to 39.8C with an average Tb of 38.720C 0.77 (SD) in

Anhingas and 39.8C to 420C with an average Tb of 40.560C 0.44 (SD)

in cormorants.

Thermal conductances measured in birds with wet plumage averaged
0.0929 cm302/g-h-oC (Anhingas), which is 205% of that measured in dry

Anhingas during the day, and 0.0532 cm302/g-h-C (cormorants), which

is 144% of that measured in dry cormorants during the day.

During the experimental trials featuring wet subjects, the An-

hingas appeared to become more saturated with water, remain saturated

longer, and were not able to stand as far out of the water as were the

cormorants. In fact, two of the Anhingas did not even attempt to stand

out of the water and were completely immersed for the entire two hours

in the chamber. Metabolic rates and thermal conductances of these in-

dividuals were higher than those of the individuals that were able to

extend the upper half of the body out of the water.

In the metabolic trials featuring wet plumage, Anhingas reached

the highest metabolic rates recorded under any experimental conditions

during the study, possibly approaching maximal rates of oxygen con-

sumption for this species, with V 02 reaching 4.11 times basal meta-

bolic rate in one soaked individual exposed to water at 15.80C

(Tb = 37.40C). Cormorant metabolic rates recorded under similar

conditions were no higher than those recorded at lower temperatures

in dry individuals.


Anhingas, Double-crested Cormorants, and Flightless Cormorants

are highly effective predators, often capturing three to five fish in

a 5 to 10 minute period. As a result these species devote the

majority of their time to activities other than foraging. All three

species, therefore, can be considered as "time minimizers" with re-

spect to feeding strategy (Schoener 1971). Their reduced buoyancy,

due to the water absorbing plumage, may improve their efficiency as

underwater predators, at the extreme permitting the Anhinga to remain

relatively motionless under water. However, the temporary increase

in thermal conductance that results from having a layer of water

adjacent the skin must subject them to thermoregulatory stress,

especially in Anhinga (Mahoney in press), a predicament similar to

that suffered by land birds exposed to heavy rains (Kennedy 1970).

This may explain why Anhingas spend so little time in the water,

especially during cool weather.

Considering the high rates of heat loss that must occur in indi-

viduals with saturated plumage, it would be energetically advantageous

for Anhingas to dry as quickly as possible after foraging, thus re-

establishing a layer of air next to the skin. Spread-winged behavior

may be an adaptation to this end. Such a function is suggested by

the appearance of this behavior in wet birds on overcast days,and by

their fan drying behavior, which almost certainly functions to dry

the plumage rapidly when sunlight is unavailable. Anhingas often ex-

pose the skin during spread-winged behavior by erecting wing and back

feathers, especially while wet. Rapid drying should be facilitated by

a combination of feather erection, the black feather pigmentation, and

exposure of the maximum surface area to the sun via wing extension and

orientation. Although the remiges may not absorb water to the extent

of the breast feathers studied by Casler (1973) and Rijke (1968), the

wing coverts may be wettable, and it may be these which the bird is

attempting to dry by fanning when the sky is overcast. Although the

wings appear water laden when birds leave the water, the contention

that Anhingas must dry their plumage before they can fly (McAtee and

Stoddard 1945) is not supported by personal observations of birds fly-

ing, albeit weakly, from the water's surface. This suggests that any

wing drying function serves primarily as an adaptation to conserve

metabolic heat.

Although a wing drying function for spread-winged behavior is

supported by these observations, other data suggest that spread-winged

behavior in Anhinga also has an overlapping thermoregulatory function.

(1) Dry Anhingas display this behavior more often than do wet


(2) The frequency of this behavior is inversely correlated with
Ta and may comprise as much as 88% of the behaviors observed with Ta

is less than 10C (Fig. 1). In contrast, the frequency is only 14% at

temperatures above 300C.

(3) Anhingas are black on the back and wings. Darkly pigmented

plumage may absorb more solar radiation than light (Hamilton and Hepp-

ner 1967a&b, Lustick 1969) depending on the wind speed (Walsberg

et al. 1978) and the angle of incidence (Lustick 1980). That Anhingas

normally gain heat from insolation is obvious because gular flutter

appeared in free-living birds when Ta was between 25.0 and 27.50C and

the intensity of solar radiation was moderate but did not appear in

my captive birds even when chamber temperatures exceeded 37C, unless

a radiant load was present.

(4) Most birds oriented away from the sun (perpendicular to the

incident radiation) during spread-winged behavior but faced the sun

during heat stress (gular flutter). Orienting perpendicular to

incident radiation would enable Anhingas to take full advantage of

the heat absorbing qualities of the black plumage by increasing the

surface area exposed to the sun and by optimizing the angle of inci-

dence (Lustick 1980). Facing the sun would reduce the amount of

surface exposed to it, as demonstrated for Herring Gulls, Larus

argentatus (Lustick et al. 1978), and reduce the angle of incidence,

making the birds effectively white with respect to the absorption

of radiant energy (Lustick 1980).

(5) Anhingas exhibit spread-winged behavior before entering the

water. This may enable them to store heat passively to offset the

high thermal conductance associated with wetting.

(6) During spread-winged behavior Anhingas expose the darkly

pigmented skin of the subalular apterium to the sun. The apterium

is the only darkly pigmented skin on the Anhinga's body and may play

a role in enhancing insolation absorption.

The spread-winged behavior of Anhingas is not a mechanism for

"dumping heat" since it never accompanies gular flutter. In addition,

spread-winged sunning in Anhingas is not simply an adaptation to re-

align the feathers after soaring as proposed for vultures and other

soaring birds by Houston (1980). Although Anhingas occasionally soar,

they maintain spread-winged postures for much longer periods of time

than would be required for this purpose, and the appearance of this

behavior is not in any way associated with soaring.

The plumage of Double-crested Cormorants, in contrast with that

of Anhingas, is only partially wettable, as only the distal portions

absorb water. They consequently maintain an air layer next to the

skin while foraging (Casler 1973). This difference in feather struc-

ture affords cormorants greater insulation while immersed and while

drying and may explain why cormorants apparently spend more time in

the water than do Anhingas.

Spread-winged behavior in Double-crested Cormorants appears to

function primarily, or solely, in wing drying and not to supplement

metabolism, as

(1) Cormorants only displayed spread-winged behavior when wet,

often accompanied by fanning behavior

(2) Spread-winged behavior comprised too small a percentage of

behavioral observations to allow sufficient time for any significant

supplementation of metabolism (2.3% overall and 4.6% maximum under any

environmental conditions as compared to 30.9% overall and 88% when

sunny and cool for Anhingas)

(3) Double-crested Cormorants did not flatten out to the sun as

Anhingas did but stood erect regardless of sun position

(4) Double-crested Cormorants oriented more strongly to the wind

than to the sun.

As with Anhingas, the spread-winged behavior of Double-crested

Cormorants is not a mechanism for "dumping heat" as it was never ac-

companied by gular flutter. The delta-winged posture of these cormor-

ants may, however, function in heat dissipation (bringing arterial

blood from the brachial artery close to an exposed, often shaded,

bodily surface), as it was only observed in conjunction with gular

flutter, and only at high ambient temperatures and solar intensities.

An alternate, but (in my opinion) unlikely, hypothesis for the function

of spread-winged behavior in cormorants is use as a social signal to

indicate foraging success (Jones 1978).

There are similarities in the use of spread-winged behavior for

both cormorant species (Flightless and Double-crested) as compared with

Anhingas. All three orient nonrandomly with respect to the sun during

spread-winged behavior, with the primary skew in the data being in favor

of orienting with back to the sun. However, the tendency is much

stronger in Anhingas. In fact, the orientation during spread-winged

behavior of Flightless Cormorants was not significantly different from

their orientation during other behaviors. None of the three apparently

use spread-winged behavior for heat dissipation (Flightless Cormorants

do not display spread-winged postures in conjunction with gular flut-

ter either). The drooped-winged posture of Flightless Cormorants (as

with the delta-winged posture of Double-crested Cormorants) may, how-

ever, serve this purpose.

There are, however, important differences in the use and function

of this behavior in the Flightless Cormorant (as with the Double-crested

Cormorant) in comparison to Anhingas. Because both species possess

wettable plumage, it was thought that perhaps Flightless Cormorants

might share the Anhinga's tendencies towards the supplementation of

metabolism, as these cormorants must forage in the cool waters of the

Humboldt Current (the nearshore surface temperature of which averaged

20.90C during my stay at Tagus Cove). This does not appear to be

the case as Flightless Cormorants

(1) do not orient strongly to the sun,

(2) do not exhibit spread-winged postures while dry,

(3) do not expose a maximum of surface area to the sun by flat-

tening out when the sun is high,

(4) actually suffered a slight decline in body temperature

during spread-winged behavior during my measurements.

In addition to these observations, Flightless Cormorants observed

during the course of this study were frequently observed to be gular

fluttering because, although ambient temperature never exceeded 300C,

black-body temperature frequently exceeded 500C. Frequently this

gular flutter continued until well after the sun had set, indicating

that perhaps these Flightless Cormorants have high rates of metabolism

to deal with the cool waters in which they forage. These observations

suggest that the heat lost during foraging might be a welcome relief,

as opposed to an energetic stress. It therefore appears that spread-

winged behavior in Flightless Cormorants (as with Double-crested

Cormorants) is primarily a mechanism for wing drying. Why this might

be necessary remains a mystery. It may be for energetic reasons (to

reduce heat loss by rapidly drying wet plumage) or even a vestigial

behavior. However, it is not a mechanism for gaining heat from the sun.


Both Anhingas and Double-crested Cormorants show a daily variation

in energetic. These diurnal species reduce their basal rates, body

temperatures, and thermal conductances during the night. However,

neither species displays the 25% reduction in basal metabolic rate

expected from Aschoff and Pohl (1970) or the 50% reduction in thermal

conductance expected from Aschoff (1981).

Anhingas are capable of saving significant amounts of energy by

lowering their body temperature and thermal conductance at night when

exposed to temperatures below thermoneutrality. This adaptation en-

ables them to extend the thermoneutral zone 3.5C lower at night than

during the day. Total energy expenditure for thermoregulation can be

calculated from the equation M = C'(Tb-Ta), where M = metabolic rate

and C' = thermal conductance (McNab 1974). Using daytime values for

Tb and C' and assuming 1 cm302 = 4.8 cal, total energy expenditure for

a 1.04 kg Anhinga would amount to 188.74 kcal/day used for thermo-

regulation at 50C. Using nighttime values for C' and Tb, and assum-

ing 12 hours of night, total daily energy expenditure for thermoregu-

lation at 50C would amount to 166.33 kcal/day, a 22.41 kcal savings.

Therefore, in addition to extending the thermoneutral zone, reducing

thermal conductance and body temperature at night enables an Anhinga

to save 12% of the energy it would spend for thermoregulation at 5C.

The slight reduction in nocturnal basal metabolic rate represents a

savings of 8% of the daily energy expenditure at ambient temperatures

within thermoneutrality (assuming 12 hrs of night). By saving energy

in this manner Anhingas can compensate somewhat for their high thermal

conductances, high rates of heat loss during aquatic behavior, and

limited thermoneutral zone. A reduction in daily energy needs trans-

lates into reduced food needs, which means that less time need be

spent in the water and/or drying out. Further reduction of daily en-

ergy requirements in Anhingas is accomplished by absorbing insolation

using the spread-winged posture, to be discussed below.

Like Anhingas, Double-crested Cormorants also extend their thermo-

neutral zone 3.5C lower at night than during the day. Using daytime

values for C' and Tb a 1.33 kg cormorant would expend 204.1 kcal/day

for thermoregulation at 5C. Using nighttime values for C' and Tb,

and assuming 12 hours of night, total daily energy expenditure for

thermoregulation would amount to 188.34 kcal/day at 5C, a 15.76 kcal

savings. Therefore, in addition to extending the thermoneutral zone,

reducing thermal conductance and body temperature at night enables a

cormorant to save 8% of the energy it would spend for thermoregulation

at 50C. The reduction in basal metabolic rate observed at night in

cormorants represents a savings of 13% of the daily energy expenditure

at ambient temperatures within thermoneutrality (assuming 12 hours of

night). Double-crested Cormorants have high thermal conductances, as

well as high basal rates. Saving energy in this fashion may help the

cormorant to balance its energy budget. Because Double-crested Cormor-

ants apparently do not suffer the same degree of thermoregulatory

stress during wetting as Anhingas, theymay not be under as intense

selection to evolve energy conserving adaptations such as facilitated

insolation absorption.

The use of insolation to reduce the metabolic costs of endothermy

contrasts greatly between the two species. Double-crested Cormorants

apparently do not use the spread-winged posture to absorb insolation

and reduce their metabolic costs. Their spread-winged behavior prob-

ably functions solely in drying the plumage, as has been proposed for

other cormorant species (Rijke 1968, Siegfried et al. 1975). In con-

trast to Anhingas, the cormorant's feather structure which maintains

an insulative air layer next to the skin while immersed (Casler 1973),

in combination with their high rates of metabolism which permits them

to have a broader thermoneutral zone than Anhingas, may have enabled

Double-crested Cormorants to fully invade the temperate zone. The

feather structure and accompanying suite of morphological/physiological

adaptations of Double-crested Cormorants is consistent with their for-

aging strategy, one of active pursuit (Owre 1967).

In contrast to cormorants, both metabolic data and field observa-

tions (Hennemann 1982) suggest that Anhingas use spread-winged behavior

to absorb insolation, which hastens the drying of their body plumage,

supplements their low metabolic rates, reduces their high thermal con-

ductances during cold weather, replaces body heat lost through convec-

tion and evaporation during and after foraging, and allows them to

extend the region of thermoneutrality. The Anhingas' world-wide re-

striction to areas with tropical or subtropical climates agrees with

the data on basal metabolic rate and thermal conductance in suggesting

that Anhingas are poorly adapted to and may be energetically stressed

during cold weather. In northern Florida Anhingas are near their

northernmost winter limit of their geographic distribution (Palmer

1962). The rather high lower limit of thermoneutrality of Anhingas

means that Anhingas face ambient temperatures below thermoneutrality

for much of the north Florida winter. Another source of potential

energetic stress acting on Anhingas is their wettable plumage. The

Anhingas' plumage, which allows water to fully penetrate air spaces

next to the skin (Casler 1973), may enhance prey capture but may also

be primarily responsible for the inability of Anhinga to tolerate frigid

weather and fully invade the temperate zone. Due to the many sources

of energetic stress operating on the Anhinga in the temperate zone, the

ability to absorb insolation may bean essential adaptation to balance

the energy budget of this species in many parts of its range.

Although spread-winged behavior is superficially identical in both

Anhingas and Double-crested Cormorants, the underlying physiological

consequences are quite different. Anhingas may have evolved a thermo-

regulatory function after first evolving spread-winged behavior to

facilitate wing drying. The development of its distinctive form of

nearly sedentary stalking fishing behavior (Owre 1967) may have required

the wetting of its plumage to reduce buoyancy, thereby increasing heat

loss and requiring the evolution of a behavioral mechanism to supplement

metabolism. This represents the first documentation of a thermoregu-

latory/energetic function for a spread-winged posture and warrants

further investigation of similar behaviors in the many other species

that exhibit them.

At high ambient temperatures, energy absorption by Anhingas may

be a source of thermoregulatory stress rather than advantage. Anhingas

may reduce the risks of heat stress by

(1) having low rates of metabolism;

(2) having high thermal conductances;

(3) having a high capacity for evaporative heat loss;

(4) having a capacity for heat storage;

(5) behavioral changes in orientation to the sun. Anhingas primar-

ily face the sun during gular flutter and away from the sun (perpendicu-

lar to the incident radiation) during spread-winged sunning (Hennemann

1982). These orientation adjustments enable Anhingas to become ef-

fectively white or black as the situation requires (Lustick 1980).

(6) not engaging in spread-winged behavior.

The higher basal metabolic rates and lower evaporative cooling

capacities of cormorants make them less well adapted to the hot, humid,

subtropical summers of Florida. They began gular fluttering at lower

temperatures than Anhingas, were less capable of dissipating as great

a fraction of their metabolically produced heat through evaporative

means than were Anhingas, and their ratio of He/H exceeded 1.0 at lower

ambient temperatures than in Anhingas.

Incident radiation elevated rates of evaporative water loss in

both species and lowered the ambient temperature at which the ratio of

He/Hm exceeded 1.0. Were it not for the virtually limitless supply of

water available for evaporative cooling, these elevated rates of

evaporative water loss might be a serious source of stress for these

species in hot, sunny environments such as Florida.

In this respect, the wettable plumage of these species, which may

be a source of thermoregulatory stress in the winter, may be an advan-

tage in rapid heat dumping in the summer. My examination of the ef-

fects of wetting on the thermoregulation of these species is not

analogous to field conditions (there are few, if any, situations in

which an Anhinga would remain in the water for two hours, Hennemann

1982). In addition, the great variability in the degree to which dif-

ferent individuals were exposed to plumage wetting due to the varia-

tion in individual behavior and in the abilities of different indi-

viduals and species to stand partially out of the water was another

source of error in making any kind of quantitative assessment of the

effects of plumage wetting on thermoregulation. However, the elevated

metabolic rates and thermal conductances, and reduced body temperatures

observed during wetting, are probably qualitatively representative of

the actual effects of plumage wetting on these two species. The con-

tention that Double-crested Cormorants are less stressed by wetting

than are Anhingas is supported by (in addition to the data presented

in this study) behavioral observations that reveal that Anhingas spend

minimal amounts of time in the water, especially at low ambient tempera-

tures (Hennemann 1982), while cormorants show no such aversion

(Hennemann, personal observations).


The geographic limits to the distribution of vertebrates are usu-

ally difficult to explain. Species may be limited by a number of

factors including physiological and ecological inabilities to cope

with environmental extremes and limitations in temperature, moisture,

resource availability, or a combination of these. With this in mind,

the northern limits of distribution-during winter of Anhingas and

Double-crested Cormorants were examined to delineate and compare the

physiological factors operating on these two species at or near their

geographic limits. To this end, the December distribution of Anhinga

anhinga in the U.S. as determined from Christmas Audubon Society bird

censuses (published in the July issues of American Birds for 1977-1981)

is presented in Figure 15. The December distribution of Phalacrocorax

auritus in northeastern North America, as determined from Audubon

Society Christmas censuses from 1977-1981, is presented in Figure 16.

The northern limit to the distribution of Anhingas in eastern

North America does not appear to depend on ecological factors such as

the availability of food or open water but rather on two interacting

parameters of the physical environment, ambient temperature and the

availability of insolation. Specifically, in December Anhingas can be

found in localities where the mean monthly temperature (for December)

is 10C, provided that there is also 160 or more hours of sunshine

available per month. If the mean hours of monthly sunshine for

Figure 15. Distribution of Anhingas in the U.S. in December

Figure 16. Distribution of Double-crested Cormorants in northeastern North America in

-to* -io*IMU


^^^^ X

x -2. c

-2 So

X ^^ x*

December are less than 160 hours per month, then Anhingas may be found

between the 100C and 12.50C mean monthly temperature isotherms (closer

to the 12.50C line) such as in southern Mississippi, or they may drop

out entirely, as is the case in south Alabama near Mobile, and in north-

western Florida near Pensacola. Anhingas extend north of the 100C

isotherm in only two areas: the eastern coasts of the Carolinas as

far north as Wilmington, North Carolina, and in northwestern Louisiana

near Shreveport, and southwestern Arkansas as far north as Texarkana,

Arkansas. Not surprisingly, these areas receive an average of better

than 175 hours of sunshine in December (Wilmington--178, Shreveport--

177, Texarkana--no available data).!

Apparently, Anhingas can balance their energy budgets in two ways:

(1) by living in areas subject to moderate temperatures or (2) by

living at less moderate temperatures in areas in which there is ample

sunshine to supplement metabolic heat production. A series of energy

budgets constructed using my behavioral and energetic data is pre-

sented in Tables 11-13. These energy budgets illustrate the energetic

costs for thermoregulation for a 1.04 kg Anhinga assuming that the

average temperature is 10C and (1) sun is available and the Anhinga

is exhibiting behavioral frequencies appropriate for a sunny period

at temperatures at or below 15C (Table 11), (2) sun is not available

(skies are overcast) and the Anhinga is behaving appropriately for a

cloudy period in which temperatures are at or below 15C (Table 12, and

(3) the sun is not available but the Anhinga is exhibiting behavioral

frequencies appropriate for a sunny day, not a cloudy one (Table 13).

Climatic data were obtained from the Climatic Atlas of the United
States, 1968 edition, a publication of the U.S. Department of Commerce

Table 11.

Daily energy budget for thermoregulation

1) Daytime Ta averages 150C (10 hours of
2) Nighttime Ta averages 6.50C (14 hours
3) Water temperature averages 10C
4) Sun is available
5) Anhinga behavior is appropriate for a


of night)

sunny day

Behavior Frequencya Cmb Tb (Tb-T) Mc Mdj Costse
(%) (cm302/ghroC) (C) (C) (cm302/g hr) (kcal/day)

S-W Sunning (Wet)f 20.4 0.0605 39.4 24.4 1.48 3,140 15.07

S-W Sunning (Dry)9 43.3 0.0281 40.0 25.0 0.70 3,516 16.88

Perchingh 20.2 0.0454 39.7 24.7 1.12 2,353 11.30

Swimming 11.1 0.0929 38.7 28.7 2.67 3,082 14.79

Total (Day) 57.76
Night 100.0 0.0364 38.0 31.5 1.15 16,690 80.13

Total (overall) 137.89

aBehavioral Frequency as a percent of total observations (see text Chapter Two)

bMinimal thermal conductance; Cm for S-W Sunning (Wet) was assumed to be the average of Cm as measured
for dry birds exposed to insolation and C as measured for wet birds

cMetabolic rate as calculated from the equation M = Cm (Tb-Ta) (McNab 1974)
dAdjusted metabolic rate calculated by multiplying M times the proportion of time devoted to that
behavior times 10 hours (day) or 14 hours (night) times Mass, expressed in cm302/10 hr or cm 02/14 hr
assumes 1 cm302 = 4.8 cal
Spread-winged sunning with wet plumage
gSpread-winged sunning with dry plumage

Perching includes all behaviors except swimming and sunning, the assumption being that all such
behaviors should have similar values for C

Table 12.


of night)

Daily energy budget for thermoregulation
1) Daytime Ta averages 150C (10 hours of
2) Nighttime Ta averages 6.50C (14 hours
3) Water temperature averages 100C
4) Skies are overcast
5) Anhinga behavior is appropriate for a

Behavior Frequency Cm Tb Tb -Ta M Madj Costs
(%) (cm302/ghroC) (0C) (0C) (kcal/day)

S-W Sunning (Wet)a 6.1 0.0692b 39.2 24.2 1.67 1,077 5.17

Perching 89.0 0.0454 39.7 24.7 1.12 10,367 49.76

Swimming 4.9 0.0929 38.7 28.7 2.67 1,360 6.53

Total (day) 61.46
Night 100.0 0.0364 38.0 31.5 1.15 16,690 80.13

Total (overall) 141.59
includes fan drying

assumed to be the average of C as measured for dry birds without insolation and C as measured for
wet birds m

cloudy day

Table 13.

Daily energy budget for thermoregulation (Anhinga)
1) Daytime Ta averages 150C (10 hours)
2) Nighttime Ta averages 6.50C (14 hours)
3) Water temperature averages 100C
4) Skies are overcast
5) Anhinga behavior is appropriate for a sunny day, not cloudy

Behavior Frequency Cm Tb (Tb Ta) M Mad Costs
(%) (cm302/g hC) (C) (0C) (kcal/day)

S-W Sunning (Wet) 20.4 0.0692 39.2 24.2 1.67 3,543 17.01

S-W Sunning (Dry) 48.3 0.0454 39.7 24.7 1.12 5,626 27.00

Perching 20.2 0.0454 39.7 24.7 1.12 2,353 11.29

Swimming 11.1 0.0929 38.7 28.7 2.67 3,082 14.79

Total (day) 70.09
Night 100.0 0.0364 38.0 31.5 1.15 16,690 80.13

Total (overall) 150.22

These time and energy budgets suggest that Anhingas often delay

feeding on cool, cloudy days, compensating for this by feeding heavily

during sunny periods. Even with reduced time in the water on cloudy

days, Anhingas still expend 6.4% more energy for thermoregulation than

they would on a sunny day in which they spend significantly more time

in the water. Table 13 indicates that if sunny periods were scarce and

Anhingas were forced to forage as much on cloudy days as they do on

sunny days, their daytime costs for thermoregulation would rise by

21%, possibly causing them to exceed the limits of their energy budget.

This offers an explanation for the apparent dependency of Anhingas on

either very moderate temperatures, or frequent sun, or both, as sug-

gested by their distribution.

The distribution of Double-crested Cormorants, on the other hand,

apparently is not limited by physical factors such as Ta or insolation,

as the coolest areas in which they are found are also the regions with

the fewest number of sunny hours per month (upstate New York, southern

Quebec with fewer than 80 hours of sunshine in December as compared

to coastal regions such as near Portland, Maine, which receives over

120 hours of sunshine in December and more moderate temperatures). A

more likely explanation for the northern limit of the distribution of

this species is an ecological factor, such as the availability of

open water.

Because Double-crested Cormorants do not use the sun to supplement

metabolism, I constructed energy budgets for them using pooled behav-

ioral frequency data from both sunny and cloudy periods at temperatures

at or below 150C. Table 14 illustrates the thermoregulatory costs for

a 1.33 kg Double-crested Cormorant assuming that ambient temperatures

Table 14. Daily energy budget for thermoregulation
1) Daytime Ta averages 150C (10 hours of
2) Nighttime Ta averages 6.50C (14 hours
3) Water temperature averages 100C

(Double-crested Cormorant)

of night)

Behavior Frequency Cm Tb (Tb -Ta) M Madj Costs
(%) (cm302/g hC) (0C) (0C) (kcal/day)

Spread-winged 2.6 0.0450 40.9 25.9 1.17 405 1.95

Perching 69.9 0.0365 41.0 26.0 0.95 8,832 42.39

Swimming 27.5 0.0532 40.6 30.6 1.63 5,962 28.62

Total (day) 72.96
Night 100.0 0.0320 39.7 32.2 1.03 19,179 92.06

Total (overall) 165.02

average 100C, to compare costs with the Anhinga at this temperature.

Table 15 presents the costs faced by these cormorants near their

northernmost distributional limit. Although Double-crested Cormorants

expend more energy than do Anhingas for thermoregulation at 100C av-

erage temperature, they expend less energy on a per gram basis (per

unit body mass). Because their plumage is only partially wettable,

cormorants can, and do, spend more time in the water than do Anhingas

at these ambient temperatures. They, therefore, are capable of cap-

turing more prey (presumably) than their completely wettable relatives,

at lower expense (as is suggested by the data on the effects of wetting

on metabolism). This ability to forage freely on cool, cloudy days

offers an explanation for the ability of the Double-crested Cormorant

to live at latitudes far north of the Anhinga's northern limit and at

ambient temperatures far lower than the Anhinga can tolerate.

The energy budgets confirm what the field and laboratory data im-

plied. The dependency of the Anhinga on a "stalking" foraging strategy

featuring totally wettable plumage tied to low rates of metabolism,

high thermal conductances, and a dependency on solar assistance restricts

Anhingas to subtropical climates with warm winters and ample sunshine,

while the "chasing" strategy of the Double-crested Cormorant featuring

partially wettable plumage tied to high metabolic rates, high con-

ductances, and no special adaptation for insolation absorption allows

these cormorants to extend well into the temperate zone.

Table 15. Daily energy budget for thermoregulation (Double-crested Cormorant)

1) Daytime Ta averages 00C (10 hours of day)
2) Nighttime Ta averages -8.60C (14 hours of night)
3) Water temperature averages 1C

Behavior Frequency Cm Tb (Tb Ta) M Madj Costs
(%) (cm302/g hoC) (C) (0C) (kcal/day)

Spread-winged 2.6 0.0450 40.9 40.9 1.84 636 3.05
Perching 69.9 0.0365 41.0 41.0 1.50 13,945 66.94

Swimming 27.5 0.0320 40.6 39.6 2.11 7,717 37.04

Total (day) 107.03
Night 100.0 0.0320 39.7 48.3 1.55 28,861 138.53

Total (overall) 245.56


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Willard W. Hennemann,III, was born in Baltimore, Maryland, on

3 November 1954. He developed an interest in natural history during

early childhood that led him to major in zoology at the University

of Maryland, where he received his B.S. in May 1976. Mr. Hennemann

entered graduate school at the University of Flor-ida in September

1976 to major in zoology, in which he will receive his Ph.D. in

August 1982. During his graduate career Mr. Hennemann pursued many

projects in the areas of physiological and behavioral ecology, where

his main interests lie, and was awarded grants from Sigma Xi, the

Frank M. Chapman memoriall Fund, and NSF to support his research. He

is a member of the American Society of Mammalogists and the Cooper

Ornithological Society. Since July 1977 Mr. Hennemann has been mar-

ried to the former Jeanne Marie Schwietz.

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