Physiological variability in the Fiscal Shrike Lanius collaris along an altitudinal gradient in South Africa

Journal of Thermal Biology 28 (2003) 581–594

ARTICLE IN PRESS

*Correspond

33-2605105.

E-mail addr1Present add

Sciences, UNIT

Auckland, New

0306-4565/$ - se

doi:10.1016/j.jth

Physiological variability in the Fiscal Shrike Lanius collarisalong an altitudinal gradient in South Africa

S. Soobramoneya, C.T. Downsb,*, N.J. Adamsa,1

aSchool of Life and Environmental Sciences, University of Natal, Private Bag X10, Dalbridge, Durban 4014, South AfricabSchool of Botany and Zoology, University of Natal, Private Bag X01 Scottsville, Pietermaritzburg 3209, South Africa

Received 27 January 2003; accepted 13 August 2003

Abstract

Oxygen consumption, evaporative water loss and body temperature were investigated in four subpopulations of

sedentary Fiscal Shrike in South Africa across an altitudinal gradient from east to west. Subpopulations were found to

be significantly different in the physiological parameters investigated. Fiscal Shrikes from the more mesic habitats at

low altitude (Durban and Merrivale) were found to have higher basal metabolic rates, evaporative water loss and body

temperatures, compared with shrikes from semi-arid areas of low habitat productivity at high altitude (Estcourt and

Harrismith). Fiscal Shrikes also displayed significant differences in circadian rhythms of oxygen consumption,

evaporative water loss and body temperature. Fiscal Shrikes showed seasonal acclimatisation of thermoregulatory

parameters, increasing their basal metabolic rates and oxygen consumption in cold conditions, and reducing their body

temperatures from summer to winter. Deviations of physiological parameters from those predicted by allometry were

attributed to the plasticity at a phenotypic level that allows survival in a range of environmental conditions associated

with unpredictable resource availability in southern Africa.

r 2003 Elsevier Ltd. All rights reserved.

Keywords: Physiological variability and adaptation; Oxygen consumption; Evaporative water loss; Body temperature; Circadian

rhythms; Seasonal adjustments

1. Introduction

The adaptations that similar animals display to

different environments are of particular evolutionary

interest (Garland and Adolph, 1991). Studies have

focussed on describing average species or population

responses and elucidating mechanisms underpinning

observed responses. Intraspecific variability of physio-

logical responses and geographic variation in this

variability have been relatively rare, and studies on

intraspecific variation in thermoregulation and thermal

ing author. Tel.: +27-33-2605127/04; fax: +27-

ess: [email protected] (C.T. Downs).

ress: Faculty of Health and Environmental

EC Institute of Technology, Private Bag 92025,

Zealand.

e front matter r 2003 Elsevier Ltd. All rights reserve

erbio.2003.08.004

biology of wild species are also limited (Garland and

Adolph, 1991). Few studies have investigated the

physiological variation of avian populations along an

environmental gradient (Ambrose and Bradshaw, 1988).

Populations from contrasting or extreme (arid or desert)

environments have a tendency to avoid the extreme

conditions of their natural environment by displaying

seasonal migratory or nomadic tendencies to areas that

possess milder climates and temporary abundance of

natural resources (Ambrose and Bradshaw, 1988;

Maddocks and Geiser, 1997). The physiology of

sedentary species in arid or semi-arid areas is little

understood.

Climate may influence physiological parameters di-

rectly through its impact on thermoregulatory processes,

or indirectly, through its influence on vegetation and

food availability (D’miel and Tel-Tzur, 1985). An early

study by Scholander et al. (1950a) concluded that

d.

ARTICLE IN PRESSS. Soobramoney et al. / Journal of Thermal Biology 28 (2003) 581–594582

metabolic rate has not been shown to vary predictably

with climate. However, later studies have found contrary

evidence. Some authors have suggested that a low basal

metabolic rate may be adaptive for endotherms living in

hot, humid areas, because lower heat production might

reduce heat stress (Hudson and Kimzey, 1966; Kendeigh

and Blem, 1974; Weathers, 1977; Wasser, 1986). Other

authors have suggested that birds that may face periods

of decreased energy availability may alleviate the effects

of energy shortages by reducing metabolic rates when

resting, which may be adaptive in cold, semi-arid areas

of low productivity (Steen, 1958; Warren, 1960; Law-

sieski, 1963; Yarborough, 1971; Chaplin, 1974; Vleck

and Vleck, 1979). There may be similar patterns

displayed by populations distributed across steep

altitudinal gradients, correlated with increased daily

and seasonal temperature variation. While considerable

effort has been devoted to study adaptations to cold in

lowland birds (Dawson and Hudson, 1970; Calder and

King, 1974), very few studies have tested physiological

responses to cold in birds native to high altitude (Castro

et al., 1985). Cold temperatures at high altitude require

homeotherms to increase metabolic heat production.

Fiscal Shrikes Lanius collaris were chosen as a model

because of their wide geographical and altitudinal

distribution that allows for a comparative ecophysiolo-

gical study. They are one of the most common

passerines in sub-Saharan Africa (MacDonald, 1980;

Lefranc and Worfolk, 1997; Parker, 1997). They occur

throughout most of southern Africa, except central

Botswana, northwest Zimbabwe and most of Mozambi-

que (Maclean, 1993). The Fiscal Shrike is a medium-

sized pied bird, and is the most widespread resident

breeding shrike in southern Africa (Harris and Arnott,

1988; Lefranc and Worfolk, 1997; Parker, 1997),

breeding over an altitudinal gradient from sea level to

at least 3000m (Little and Bainbridge, 1992). They

occupy a variety of habitats (MacDonald, 1980; Parker,

1997) that range from the tropical north to the

temperate south, and from lowland to highland areas.

The non-migratory status of the shrike implies that

individuals are subjected to environmental influences in

the same locality throughout the year.

On the eastern seaboard of southern Africa, there is a

change in temperature, humidity and rainfall (and hence

water availability) from east to west (Schulze, 1997).

This aridity gradient also has an accompanying gradient

of rainfall unpredictability (Schulze, 1997). The aridity

gradient is also influenced by the El Nino Southern

Oscillations (ENSO) (Schulze, 1997). ENSO events are

negative rainfall anomalies and result in animals being

subjected to unpredictably low habitat productivity.

This study sets out to utilise some standard ecophy-

siological techniques to assess variability of integrated

physiological function in the Fiscal Shrike. The objec-

tives of the study were to examine thermoregulatory

(oxygen consumption, evaporative water loss and body

temperature) responses to temperature stress of Fiscal

Shrikes selected from subpopulations distributed across

altitudinal and aridity gradients over the eastern half of

southern Africa, and to determine whether physiological

clines exist.

A less-obvious energy and water-saving mechanism is

that associated with endogenous circadian rhythms of

metabolism and body temperature. Circadian rhythms

typically consist elevated metabolic rates and body

temperatures during an endotherm’s active phase and

depressed values during its resting phase (Hudson and

Kimzey, 1966; Schleucher et al., 1991; Boix-Hinzen and

Lovegrove, 1998), and reductions in these physiological

parameters could represent energy and consequently

water conservation responses (Lovegrove and Heldma-

ier, 1994). Seasonal changes in circadian rhythms

(acclimatisation) have been documented in a wide

variety of avian species (Hart, 1962; Kendeigh et al.,

1977; Weathers and Caccamise 1978; Cooper and

Swanson 1994; Boix-Hinzen and Lovegrove, 1998). In

the present study seasonal changes in circadian rhythms

of oxygen consumption, evaporative water loss and

body temperature were measured over two temperature

regimes (intending to simulate two different seasons,

summer and winter).

2. Materials and methods

2.1. Study site

Fiscal Shrikes were selected for sampling across an

east–west altitudinal gradient from coastal KwaZulu-

Natal, KwaZulu-Natal Midlands and the high altitude

grasslands of the Free State, South Africa. Birds were

chosen as close as possible to the 29� latitude to limit

possible latitudinal effects. The four localities (each

representing a subpopulation) chosen were Durban

(29�530S 30�590E), Merrivale (29�300S 30�110E), Est-

court (29�030S 29�550E) and Harrismith (28�180S

29�080E) (Table 1). Altitude and grid references were

plotted using a Magellan GPS 4000 XL. The sites

represent a gradient of increasing altitude, decreasing

temperature, humidity and precipitation and increasing

coefficient of variation of annual precipitation and solar

radiation westward from Durban to Harrismith (Table

1, see Soobramoney, 2002 for more information on

climatic variables and a description of vegetation).

2.2. Bird capture and maintenance

Fiscal Shrikes were captured from the four sites

during 1999. Birds were caught within a 10 km radius of

the degree location given. Birds were collected under

permit from KwaZulu-Natal Wildlife (Permit Number

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Table 1

Climatic and geographic variables of the localities where subpopulations of L. collaris were captured

Climatic variable Durban Merrivale Estcourt Harrismith

Mean annual temperature (�C) 20.65 16.91 15.70 14.20

Mean daily maximum temperature—January (�C) 28.0 26.2 26.1 25.9

Mean daily minimum temperature—July (�C) 10.2 4.1 1.6 �0.4Mean annual precipitation (mm) 924 900 697 622

Coefficient of variation (%) of annual precipitation 21.4 21.9 26.5 28.2

Mean daily relative humidity (%) 73.8 65.6 62.3 61.1

Mean daily relative humidity—January (%) 78.6 71.2 67.7 65.1

Mean daily relative humidity—July (%) 65.9 58.8 55.3 55.7

Mean daily solar radiation (MJm�2 day�1) 19.54 22.46 23.85 24.61

Mean daily solar radiation—January (MJm�2 day�1) 23.7 27.4 29.4 30.9

Mean daily solar radiation—July (MJm�2 day�1) 14.8 16.0 16.9 17.2

Altitude (m) 130 1000 1400 1800

S. Soobramoney et al. / Journal of Thermal Biology 28 (2003) 581–594 583

722/1999) and the Free State Conservation Service

(Permit Number HK/P1/02508/001).

Five non-breeding, non-moulting males and five

female Fiscal Shrikes were captured from four sites

using bal-chatri traps and Zebra Finches (Taeniopygia

guttata) as bait. After capture, birds were ringed with

unique plastic split rings in order to identify individuals.

They were then transported to the Animal House of the

School of Life and Environmental Sciences at the

University of Natal, Durban, South Africa. Birds were

housed in individual wire mesh cages

(80 cm� 50 cm� 80 cm) with wooden perches located

in a temperature- (20�C) and light-controlled

(12L:12D—lights on from 06:00 to 18:00 h) room. Food

and water were provided ad libitum. The birds were

maintained on a diet of ground meat and mealworms

(Tenebrio larvae) and a generic sugar-free liquid

vitamin–mineral supplement, Multivitamin Syrups

(Portfolio Pharmaceuticals). The birds were allowed a

minimum of 2 weeks to acclimate and adjust to captivity

before any gas-exchange measurements were made. The

birds were weighed once weekly for 5 weeks to 0.001 g

on a Mettler PM 400 balance, to monitor their body

mass.

2.3. Physiological measurements

All physiological experiments were carried out in a

darkened constant temperature room during the resting

phase to ensure minimal disturbance. Metabolic cham-

bers of 2.7 l volume were made of Perspexs were used.

The birds were provided with a wooden perch mounted

on a plastic mesh. The floor of the chamber was covered

with a thin layer of mineral oil to absorb droppings. This

was covered with plastic mesh to avoid contact with the

birds. In order to reduce errors created by changes in

thermal radiation at different ambient temperatures, the

chambers were painted matt black (Ward and Pinshow,

1995).

The system was designed to carry out physiological

measurements on five birds simultaneously, each housed

in an individual metabolic chamber, with a sixth

chamber acting as a control. Measurements were carried

out between 18:00 and 24:00 h, the normal rest phase of

their daily cycle. Birds were tested over a temperature

range of 7�C, 10�C, 15�C, 20�C, 25�C, 30�C, 35�C and

38�C, respectively. Eight different temperature regimes

were thus sampled. Each test day involved sampling the

birds at two different temperatures. The birds were

placed in the metabolic chambers and allowed an hour

to acclimate at the experimental temperature before any

readings were taken. This also ensured 99% equilibrium

times were achieved with the chamber/flow rate combi-

nation. Thereafter, four readings per hour per individual

of each temperature were taken. The lowest reading was

used to calculate oxygen consumption. The experiments

were repeated on a different day, providing a final two

readings per temperature. Each bird was allowed to

recover for at least 2 days before being used again.

Oxygen consumption, evaporative water loss and body

temperature were measured simultaneously.

2.3.1. Oxygen consumption rates

A negative pressure open flow air respirometry system

was used to measure the oxygen consumption rates of

the Fiscal Shrikes. Air was drawn from outside the

constant temperature room by a Labotec pump. This air

was passed through tubes containing soda lime (carbon

dioxide absorbent) with a silica gel scrubber (water

absorbent). This was then passed through the chambers

where the birds were housed throughout the experiment.

Bailey Fischer Porter Flowmeters were used. For the

chamber on which the oxygen consumption rate was

being measured, the air was pulled at a constant rate of

300mlmin�1 using a Teledyne Hastings-Raydist Flow-

meter (model ECPR-4A) situated downstream from the

chamber. Air was drawn through the remaining five

metabolic chambers by a Labotec Pump (model


N010KN.18) at a rate of 150mlmin�1 situated down-

stream from the chambers. All data were recorded using

a Teledyne MC Systems 120 Data Logger. Air was then

passed into a humidity chamber that had a humidity

thermocouple (calibrated setting up a chamber and two

reference humidities) that recorded the humidity

(70.1%) in the chamber on the above data logger.

The temperature (70.1�C) in each chamber was

measured by a Physitemp thermocouple (calibrated with

a water and ice slurry bath) connected to the above data

logger. This enabled the chamber temperature to be

monitored. The air was dried with soda lime and silica

gel and O2 content measured using an Applied Electro-

chemistry Oxygen analyser (S-3A/II with N-22M sensor.

A time delay for change over and because of the tubing

was allowed.

Oxygen consumption rates were determined using the

following equation (Gessaman, 1987): mass-specific

oxygen consumption rate ¼ VeðFi � FeÞ=ð1� FiÞðgÞ;where Fi is the oxygen percentage in the ambient air

entering the chamber (set at 20.94%), Fe is the oxygen

percentage in the air exiting the chamber, Ve is the flow

rate of the air exiting the chamber (mlmin�1) and m is

the mass of the bird (g). These were then corrected to

standard temperature and pressure.

DurbanTa (°C)

VO

2V

O2

0

2

4

6

8

10

12

7 10 15 20 25 30 35 38

EstcourtTa (°C)

7 10 15 20 25 30 35 380

2

4

6

8

10

12

Fig. 1. The relationship between oxygen consumption (VO2) (ml O

subpopulations of L. collaris where the subpopulations are Durban,

2.3.2. Evaporative water loss

Evaporative water loss (EWL) was calculated by

measuring the relative humidity (RH) and temperature

of the incurrent and excurrent air, as well as the flow rate

over the animal (Louw, 1993). The humidity of the air

passing through the blank chamber was measured at the

beginning of each experiment. The amount of water

vapour in the air was calculated from the temperature

and vapour pressure (RH) using the appropriate tables

(Louw, 1993). The water vapour lost from the animal

was calculated by subtracting the water vapour in the

incoming stream from that in the excurrent stream:

water vapour lost by animal=(flow rate� absolute

amount of water excurrent from blank)�(flow rate

� absolute amount of water).

2.3.3. Body temperature

Body temperature (Tb) was measured using a Physi-

temp thermocouple (calibrated as above) that was

inserted 2 cm into the cloaca prior to placing the bird

in the metabolic chamber. The wire was passed through

a hole drilled into the lid of the chamber. The hole was

sealed with silica sealant. This was connected to the data

logger. The thermocouple was held in place by fastening

the wire to the retrices using metal clips.

MerrivaleTa (°C)

7 10 15 20 25 30 35 38

HarrismithTa (°C)

7 10 15 20 25 30 35 38

VO

2

0

2

4

6

8

10

12

VO

2

0

2

4

6

8

10

12

2 g�1 h�1) and ambient temperature (Ta) in the four respective

Merrivale, Estcourt and Harrismith.

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WL

0

2

4

6

8

10

12

14

16

EW

L

0

2

4

6

8

10

12

14

16

EW

L

0

2

4

6

8

10

12

14

16

EW

L

0

2

4

6

8

10

12

14

16

DurbanTa (°C)

7 10 15 20 25 30 35 38

Merrivale

Ta (°C)

7 10 15 20 25 30 35 38

HarrismithTa (°C)

7 10 15 20 25 30 35 38

Estcourt

Ta (°C)

7 10 15 20 25 30 35 38

Fig. 2. The relationship between EWL (mg H2Og�1 h�1) and ambient temperature (Ta) in the four respective subpopulations of

L. collaris where the subpopulations are Durban, Merrivale, Estcourt and Harrismith.


2.3.4. Circadian rhythms

Circadian rhythms were investigated at two different

temperatures 25�C and 15�C (representative of two

different seasons, summer and winter, respectively). The

birds were placed into darkened chambers at 17:00 h.

The birds were allowed an hour to acclimate and the first

set of readings recorded at 18:00 h. The lights were

switched off at 18:00 and on at 05:30 h after the 05:00 h

reading was taken. Oxygen consumption, EWL and Tb

were recorded between 18:00 and 17:00 h the following

day, a total of 24 h. Food was removed 5 h prior to all

experiments to ensure that the birds were postabsorp-

tive. The birds were weighed before testing. Percentage

estimates of energy conservation were calculated as

follows:

ðVO2max � VO2minÞ=VO2max � 100 ¼ %VO2 savings ð1Þ

for both temperature regimes.

Similarly estimates of water savings were calculated as

follows:

ðEWLmax � EWLminÞ=EWLmax � 100

¼ %EWL savings ð2Þ

for both temperature regimes.

2.3.5. Statistics

Statistica (Statsoft Inc., USA) software was used for

all statistical analyses. Mean and standard errors for all

respective characters measured were calculated for each

subpopulation. As two readings were obtained for each

individual at each Ta, repeated measures analysis of

variance (RM ANOVA) was used to calculate differ-

ences between subpopulations.

3. Results

3.1. Body mass

There was a significant difference in body mass of

Fiscal Shrikes between sites at capture (RM ANOVA,

F3,36=230.52, Po0.05). The shrikes weighed

(mean7SE) 30.8570.48, 36.8670.56, 43.8070.49 and

50.5370.68 g at Durban, Merrivale, Escourt and Harri-

smith, respectively. The birds maintained a constant

body mass whilst in captivity (RM ANOVA,

F12,144=1.02, P>0.05) and there was no significant

difference in body mass of individual birds between the

different trials at different ambient temperatures

(F21,252=1.11, P>0.05). A Scheffe test showed that

ARTICLE IN PRESS

39

40

41

42

43

44

45

Tb

(°C

)

39

40

41

42

43

44

45

Tb

(°C

)

39

40

41

42

43

44

45

Tb

(°C

)

39

40

41

42

43

44

45

Tb

(°C

)

DurbanTa (°C)

7 10 15 20 25 30 35 38

Merrivale

Ta (°C)

7 10 15 20 25 30 35 38

Estcourt

Ta (°C)

7 10 15 20 25 30 35 38

HarrismithTa (°C)

7 10 15 20 25 30 35 38

Fig. 3. The relationship between body temperature (Tb) and ambient temperature (Ta) in the four respective subpopulations of

L. collaris where the subpopulations are Durban, Merrivale, Estcourt and Harrismith.

S. Soobramoney et al. / Journal of Thermal Biology 28 (2003) 581–594586

there was a significant difference in body mass between

the sites over the 5 weeks (P=0.00).

3.2. Metabolic rates

The relationship between VO2 at different Tas is

shown in Fig. 1 for the four subpopulations of Fiscal

Shrike. Basal metabolic rates (defined here as the

minimum VO2 at thermoneutrality) remained essentially

unchanged within the temperature range of 25–35�C,

but increased linearly at temperatures above and below

this range. Since there was no significant difference in

resting VO2 between 25�C and 35�C this can be

considered the thermoneutral zone (Scheffe test,

P > 0:05). The four subpopulations of Fiscal Shrike

differed significantly in their VO2 at all ambient

temperatures (RM ANOVA, F21;252 ¼ 82:90; P ¼ 0:00).The Durban Fiscal Shrikes showed the highest minimum

VO2 followed by Merrivale, Estcourt and Harrismith

(4:4070:14; 3:5670:30; 2:3170:33 and 0:7770:45 mlO2 g

�1 h�1, respectively).

3.3. EWL

The rates of EWL at different Tas are shown for the

four subpopulations of Fiscal Shrike in Fig. 2. Each

displayed a significant difference in rates of EWL (RM

ANOVA, F21;252 ¼ 277:54; P ¼ 0:00) with Ta. Between

7�C and 15�C EWL was relatively low and constant.

There was no significant difference in EWL at these

temperatures within the populations (Scheffe test,

P > 0:05). The Durban shrikes displayed the highest

EWL rates at all Tas followed by the Merrivale, Estcourt

and the Harrismith shrikes (6:8470:34; 5:3770:35;3:4570:46 and 1:0570:57 mg H2Og�1 h�1, respec-

tively).

3.4. Body temperature

There was a significant difference in Tb between the

four subpopulations of Fiscal Shrike (RM ANOVA,

F21;252 ¼ 72:10; P ¼ 0:00) at all Tas (Fig. 3). Fiscal

Shrikes exposed to Ta of 7–30�C maintained a constant

Tb (Scheffe test, P > 0:05) at all Ta with Durban

having the highest Tb followed by Merrivale, Est-

court and Harrismith (41:6570:11�C; 41:1670:11�C;40:5470:11�C and 39:7570:22�C; respectively). The

Tbs were lower (2.5%, 3.3%, 4.5% and 6.2%) than

predicted for the Durban, Merrivale, Estcourt and

Harrismith subpopulations, respectively (McNab,

1966). When exposed to higher temperatures all four

subpopulations became hyperthermic (Fig. 3). At Ta ¼

ARTICLE IN PRESS

Durban

Time (Hours)

VO

2

0

2

4

6

8

10

12

14

16

18

VO

2

0

2

4

6

8

10

12

14

16

18

VO

2

0

2

4

6

8

10

12

14

16

18

VO

2

0

2

4

6

8

10

12

14

16

18

18 19 20 21 22 23 24 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17

Estcourt

Time (Hours)

18 19 20 21 22 23 24 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17

Harrismith

Time (Hours)

18 19 20 21 22 23 24 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17

Merrivale

Time (Hours)

18 19 20 21 22 23 24 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17

Fig. 4. The circadian change in oxygen consumption (VO2) (ml O2 g�1 h�1) of the four respective subpopulations of L. collaris at 25�C

where the subpopulations are Durban, Merrivale, Estcourt and Harrismith.


35�C; the Tbs of Durban, Merrivale, Estcourt and

Harrismith shrikes were 43:7570:11�C; 43:1570:11�C;42:5170:16�C and 41:5670:22�C; respectively. At Ta ¼38�C; the Tbs were 44:8570:11�C; 44:2570:11�C;43:5970:17�C and 42:7170:26�C for Durban, Merri-

vale, Estcourt and Harrismith shrikes, respectively.

3.5. Circadian rhythms

Fiscal Shrikes showed clear circadian changes in VO2,

EWL and Tb at temperatures of 25�C and 15�C,

respectively.

At 25�C (representative of summer) the four sub-

populations of Fiscal Shrike displayed significant

differences in oxygen consumption rates in their

circadian rhythms (RM ANOVA, F3;36 ¼ 180:00;P ¼ 0:00), and at any given temperature the oxygen

consumption was significantly lower at night than

during the day (RM ANOVA, F69;828 ¼ 180:00;P ¼ 0:00) (Fig. 4). Fiscal Shrikes maintained a constant

VO2 during the rest phase (b) (RM ANOVA, F33;396 ¼0:90; P > 0:05), and there was also no significant

difference in VO2 between the hours of the active phase

(a) (RM ANOVA, F33;396 ¼ 1:61; P > 0:05).

At Ta ¼ 25�C the four subpopulations of Fiscal

Shrike displayed significant differences in EWL in their

circadian rhythms (RM ANOVA, F3;36 ¼ 381:80;P ¼ 0:00) (Fig. 5). There was a clear diurnal pattern of

EWL, and at any given temperature, the EWL was

significantly lower at night than during the day (RM

ANOVA, F69;828 ¼ 269:80; P ¼ 0:00). Fiscal Shrikes

maintained a constant EWL during the rest phase (b)(RM ANOVA, F33;396 ¼ 0:99; P > 0:05), and there was

also no significant difference in EWL between the hours

of the active phase (a) (RM ANOVA, F33;396 ¼ 1:16;P > 0:05).There was a significant difference between the

subpopulations of Fiscal Shrike in Tb in their circadian

rhythms (RM ANOVA, F3;36 ¼ 321:40; P ¼ 0:00) at

Ta ¼ 25�C (Fig. 6). Tb displayed circadian rhythms and

was significantly higher during the day than at night at

any given ambient temperature (RM ANOVA, F69;828 ¼33:90; P ¼ 0:00). During the rest phase (b) Fiscal Shrikesmaintained a constant Tb (RM ANOVA, F33;396 ¼ 1:34;P > 0:05), and there was also no significant difference in

Tb between the hours of the active phase (a) (RM

ANOVA, F33;396 ¼ 43:10; P > 0:05).At 25�C the circadian drop in VO2 represented energy

savings 73%, 77%, 83% and 93% for the Durban,

ARTICLE IN PRESS

DurbanTime (Hours)

EW

L

0

2

4

6

8

10

12

14

16

18

18 19 20 21 22 23 24 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17

EstcourtTime (Hours)

18 19 20 21 22 23 24 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17

MerrivaleTime (Hours)

18 19 20 21 22 23 24 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17

HarrismithTime (Hours)

18 19 20 21 22 23 24 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17

EW

L

0

2

4

6

8

10

12

14

16

18

EW

L

0

2

4

6

8

10

12

14

16

18

EW

L

0

2

4

6

8

10

12

14

16

18

Fig. 5. The circadian change in EWL (mg H2Og�1 h�1) of the four respective subpopulations of L. collaris at 25�C where the

subpopulations are Durban, Merrivale, Estcourt and Harrismith.


Merrivale, Estcourt and Harrismith subpopulations,

respectively. The simultaneous drop in EWL represented

water conservation of 50%, 56%, 64% and 81% for the

Durban, Merrivale, Estcourt and Harrismith shrikes,

respectively.

At 15�C (representative of winter) significant differ-

ences in oxygen consumption rates were displayed by the

subpopulations of Fiscal Shrike in their circadian

rhythms (RM ANOVA, F3;36 ¼ 262:80; P ¼ 0:05) (Fig.7). Oxygen consumption was significantly lower at night

than during the day at any given temperature (RM

ANOVA, F69;828 ¼ 17:70; P ¼ 0:05). Shrikes maintaineda constant VO2 during the rest phase (b) (RM ANOVA,

F33;396 ¼ 1:13; P > 0:05), and there was also no signifi-

cant difference in VO2 between the hours of the active

phase (a) (RM ANOVA, F33;396 ¼ 1:55; P > 0:05).The four subpopulations of Fiscal Shrike also

displayed a significant difference in EWL in their

circadian rhythms at Ta ¼ 15�C (RM ANOVA, F3;36 ¼372:73; Po0:05) (Fig. 8). At any given temperature therewas a significantly greater amount of water evaporated

during the day than the water evaporated at night (RM

ANOVA, F69;828 ¼ 189:64; Po0:05). Shrikes maintaineda constant EWL during the rest phase (b) (RM

ANOVA, F33;396 ¼ 1:00; P > 0:05), and there was also

no significant difference in EWL between the hours of

the active phase (a) (RM ANOVA, F33;396 ¼ 1:05;P > 0:05).In addition, the four subpopulations of Fiscal Shrike

displayed a significant difference in Tb in their circadian

rhythms at Ta ¼ 15�C (RM ANOVA, F3;36 ¼ 326:50;Po0:05) (Fig. 9). At any given ambient temperature Tb

was significantly lower at night than during the day (RM

ANOVA, F69;628 ¼ 33:50; Po0:05). Shrikes maintaineda constant Tb during the rest phase (b) (RM ANOVA,

F33;396 ¼ 1:53; P > 0:05), and there was also no signifi-

cant difference in Tb between the hours of the active

phase (a) (RM ANOVA, F33;396 ¼ 42:97; P > 0:05).The drop in VO2 represented energy savings 64%,

67%, 71% and 77% for the Durban, Merrivale,

Estcourt and Harrismith subpopulations of Fiscal

Shrike, respectively. The drop in EWL represented

water conservation of 53%, 57%, 64% and 84% for

the Durban, Merrivale, Estcourt and Harrismith popu-

lations, respectively.

Metabolic rates, EWL and Tb also differed between

the subpopulations of Fiscal Shrike at 15�C and 25�C.

Oxygen consumption was significantly higher during

winter (15�C) than summer (25�C), both during the rest

phase (RM ANOVA, F3;36 ¼ 1:16; P ¼ 0:00) and active

phase (RM ANOVA, F3;36 ¼ 2:04; P ¼ 0:00). EWL was

significantly higher in summer than in winter during

ARTICLE IN PRESS

DurbanTime (Hours)

Tb

(°C

)

38

39

40

41

42

43

44

Tb

(°C

)

38

39

40

41

42

43

44

Tb

(°C

)

38

39

40

41

42

43

44

Tb

(°C

)

38

39

40

41

42

43

44

18 19 20 21 22 23 24 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17


18 19 20 21 22 23 24 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17


18 19 20 21 22 23 24 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17


18 19 20 21 22 23 24 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17

Fig. 6. The circadian change of body temperature (Tb) of the four respective subpopulations of L. collaris at 25�C where the



both the rest phase (RM ANOVA, F3;36 ¼ 1:65;P ¼ 0:00) and active phase (RM ANOVA, F3;36 ¼2:36; P ¼ 0:00). Tb was significantly higher in summer

than in winter, during the rest phase (RM ANOVA,

F3;36 ¼ 2:66; P ¼ 0:00) and the active phase (RM

ANOVA, F3;36 ¼ 1:83; P ¼ 0:00).

4. Discussion

The subpopulations of Fiscal Shrike were not

different on a genetic basis; however, they showed

differences in morphological features, anatomical and

skeletal characteristics (Soobramoney, 2002). This sug-

gests that the Fiscal Shrike displays plasticity at a

phenotypic level that allows survival in a range of

environmental conditions. This is further supported by

the thermal biology in this study.

4.1. Metabolic rates

The metabolic rates of several members of the family

Laniidae have been measured. The basal metabolic rate

of the Great Grey Shrike L. excubitor was 3.656ml

O2 g�1 h�1 (Kendeigh et al., 1977). The basal metabolic

rates of the Redbacked Shrike L. collurio, Great Grey

Shrike and Brown Shrike L. cristatus were 2.54, 2.01 and

1.68ml O2 g�1 h�1, respectively (Bennett and Harvey,

1987). The basal metabolic rate of the Brown Shrike

was also found to be higher (7.03ml O2 g�1 h�1) in

the tropics (Hails, 1983) than in colder regions

(1.68ml O2 g�1 h�1 in Russia) (Bennett and Harvey,

1987). The opposite has been found to be true for

Fiscal Shrikes. Fiscal Shrikes from the warmer sites

had higher metabolic rates than shrikes from the

colder sites. The shrikes from Durban (the warmest

site) had a BMR of 4.4070.14ml O2 g�1 h�1 followed

by Merrivale, Estcourt and Harrismith (the coldest

site) with basal metabolic rates of 3:5670:30; 2:3170:33and 0:7770:45 ml O2 g

�1 h�1, respectively. The VO2

values for the Durban and Merrivale Fiscal Shrikes

were higher than the predicted by Lasiewski and

Dawson (1967) for a passerine of similar body

mass (34% and 22%), while the values for the

Estcourt and Harrismith shrikes were lower (13% and

70%). The values for the Durban and Merrivale

subpopulations were also higher (41% and 31%)

and the Estcourt and Merrivale subpopulations lower

(1.7% and 66%) than predicted by Aschoff and Pohl

(1970).

ARTICLE IN PRESS

DurbanTime (Hours)

VO

2

018 19 20 21 22 23 24 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17


18 19 20 21 22 23 24 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17

Harrismith Time (Hours)

18 19 20 21 22 23 24 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17


18 19 20 21 22 23 24 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17

2

4

6

8

10

12

14

16

18

20

22

VO

2

0

2

4

6

8

10

12

14

16

18

20

22

VO

2

0

2

4

6

8

10

12

14

16

18

20

22

VO

2

0

2

4

6

8

10

12

14

16

18

20

22

Fig. 7. The circadian change in oxygen consumption (VO2) (ml O2 g�1 h�1) of the four respective subpopulations of L. collaris at 15�C

where the subpopulations are Durban, Merrivale, Estcourt and Harrismith.


Thermoregulatory heat production comprises the

largest component of an endotherm’s daily energy

budget. The ability to maintain an optimal level

of metabolism which minimises thermoregulatory

costs, but which still maintains homeothermy, would

be advantageous. Basal metabolic rates that are

lower than expected may reduce daily energy

requirements. In addition, the drop in VO2 during

the night would be important in lowering energy costs.

This requires a concomitant drop in Tb, i.e. hetero-

thermy.

4.2. EWL

The high metabolic rates that are associated with

endothermy, high body temperatures and the respiratory

demands imposed by flight have resulted in the high

rates of evaporative water loss experienced by birds

(Dawson, 1982). Also, most species are diurnal and

unable to use shelters such as underground burrows,

which make this problem worse in hot and dry climates

(Dawson and Bartholomew, 1968). Early allometric

equations (Brody, 1945) have suggested that evaporative

water loss tends to exceed metabolic production of water

even at moderate temperatures (Bartholomew and

Dawson, 1953). This makes small birds dependent on

succulent food or drinking for attaining water balance

(Bartholomew and Cade, 1963; Dawson, 1982).

The Durban and Merrivale shrikes had higher EWL

(35% and 28%), while the Estcourt and Harrismith

shrikes (8% and 70%) had lower than that predicted

EWL for passerines (Crawford and Lasiewski, 1968).

These values were similar to those predicted for all birds

in general: 37% and 25% higher in Durban and

Merrivale shrikes, while 8% and 71% lower than

predicted in the Estcourt and Harrismith birds, respec-

tively (Crawford and Lasiewski, 1968; Dawson and

Hudson, 1970; Calder and King, 1974; Dawson, 1982).

The values of EWL of the Fiscal Shrike were similar to

the Loggerhead Shrike L. ludovicianus of arid regions in

the United States that had an evaporative water loss rate

of 2.42mg H2Og�1 h�1 (Bartholomew and Dawson,

1953). The Loggerhead Shrike displayed a pulmocuta-

neous evaporation rate 1.5 times that anticipated for

other passerines of similar body mass (48 g) (Bartholo-

mew and Dawson, 1953). This was possible because of

its succulent diet that consists of small vertebrates and

insects. Even though Fiscal Shrikes regularly took water

in captivity, they were not observed to take surface

water in the field (pers. obs.). This also suggests that they

are dependent, like the Loggerhead Shrike, on succulent

food items for their water requirements.

ARTICLE IN PRESS


EW

L

0

2

4

6

8

10

12

14

16

EW

L

0

2

4

6

8

10

12

14

16

EW

L

0

2

4

6

8

10

12

14

16

EW

L

0

2

4

6

8

10

12

14

16

18 19 20 21 22 23 24 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17


18 19 20 21 22 23 24 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17


18 19 20 21 22 23 24 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17


18 19 20 21 22 23 24 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17

Fig. 8. The circadian change in EWL (mg H2Og�1 h�1) of the four respective subpopulations of L. collaris at 15�C where the



The role of evaporative cooling in heat defence

is important. Birds respond to heat stress by increas-

ing EWL in hot environments (Dawson and Hudson,

1970). The birds of Durban and Merrivale, which

are exposed to higher temperatures (and higher

humidities) had a greater EWL than birds from

Estcourt and Harrismith. The birds from Estcourt

and Harrismith are exposed to colder, more

arid enviroments than the birds from Durban and

Merrivale.

The Great Grey Shrike was found to have an

evaporative water loss of 4.65mg H2Omin�1, which

was 41% higher than that predicted by allometry, and

was not expected for a desert bird (Ward and Pinshow,

1995). However, the increased passive hyperthermia

within the thermoneutral zone contributed to the reduced

water loss and increased the rate of dry heat loss.

Williams (1996) analysed data for 102 avian species

and found that birds from arid environments had a

statistically lower EWL than birds from more mesic

environments. Even at thermally unstressful tempera-

tures, arid-adapted species had a reduced EWL, a

diminution amounting to as much as a third less than

more mesic counterparts. This indicated that natural

selection has operated to reduce water loss in these

species even when they were experiencing moderate

temperatures.

4.3. Body temperature

The body temperatures of the Fiscal Shrikes from all

subpopulations fell within the range reported for

passerines and birds in general (King and Farner,

1961; Prinzinger et al., 1991). At high air temperatures

all four subpopulations of Fiscal Shrike became

hyperthermic, their Tbs ranging between 42�C and

44�C. A moderately hyperthermic bird may have some

respite from heat stress (Calder and King, 1974; Ward

and Pinshow, 1995), since an elevated Tb reduces the

heat flow from the hot environment to the body and

thus reduces the amount of evaporative water needed to

prevent a further Tb rise. If the body temperature is

lower than expected, it may reduce the metabolic

demands of maintaining a constant body temperature

and may therefore represent an energy-conservative trait.

4.4. Circadian cycles

The relationship between photoperiod and metabo-

lism indicated a circadian rhythm in the Fiscal Shrike.

ARTICLE IN PRESS

DurbanTime (Hours)

Tb

(°C

)

38

39

40

41

42

43

Tb

(°C

)

38

39

40

41

42

43

44

Tb

(°C

)

38

39

40

41

42

43

Tb

(°C

)

38

39

40

41

42

43

18 19 20 21 22 23 24 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17


18 19 20 21 22 23 24 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17


18 19 20 21 22 23 24 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17


18 19 20 21 22 23 24 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17

Fig. 9. The circadian change in body temperature (Tb) of the four respective subpopulations of L. collaris at 15�C where the



Birds are known to possess a distinct diurnal cycle in

metabolism and Tb, with higher metabolic rates, EWL

and Tb displayed during the active phase than the rest

phase (Bartholomew and Dawson, 1954; Prinzinger

et al., 1991), and this was also found for the Fiscal

Shrike.

The modes of acclimatisation to cold include that of

metabolic, insulative, nutritional and behavioural ad-

justments (Calder and King, 1974). In this study,

increased oxygen consumption was found in the

‘‘winter’’ birds. Other investigators have also found that

small birds in winter have higher rates of heat

production (Hart, 1957; Cooper and Swanson, 1994).

An elevated basal metabolic rate may be due to

maintenance of increased metabolic machinery needed

for increased thermogenic capacity (Swanson, 1991;

Cooper and Swanson, 1994). Tb of the Fiscal Shrikes

dropped during the colder temperature regime. The

ability to reduce their Tb under conditions of cold stress

increases their adaptedness to unpredictable environ-

ments. This has also been found in other avian species

(Rintam.aki et al., 1983; Cooper and Swanson, 1994). A

reduction in Tb at low ambient temperatures results in

the conservation of energy without reducing the ability

of the animal to carry out normal activity. Under

conditions of cold stress, lower body temperatures

would be advantageous since less heat production would

be required to maintain body temperature by lowering

the thermal gradient between the core and the skin of the

animal.

A variety of behavioural activities may also serve to

reduce heat stress imposed on birds (Dawson and

Hudson, 1970; Thomas and Maclean, 1981). Fiscal

Shrikes are sit-and-wait predators that spend much of

their time perched in the open, exposed to various

elements of the environment. Under warm conditions,

the Fiscal Shrikes retreated to shaded areas during the

middle of the day like most other species (pers. obs.),

which served to reduce heat loading by radiation

(Dawson and Hudson, 1970; Thomas and Maclean,

1981). Residing in cold climates would require the bird

to improve the effectiveness of its thermal insulation

(Scholander et al., 1950a, b; D’miel and Tel-Tzur, 1985).

During cold conditions birds conserved heat (insulation

by feather erection). The Fiscal Shrikes in the colder

regions (Estcourt and Harrismith) probably benefited

because of their increased body size and hence increased

amount of plumage and insulative control of heat loss.

It is ecologically relevant that the more xeric popula-

tions of Fiscal Shrikes have lower rates of metabolism

and evaporative water loss at high ambient temperatures

and lower dependence on evaporative cooling mechan-

ARTICLE IN PRESSS. Soobramoney et al. / Journal of Thermal Biology 28 (2003) 581–594 593

isms than the more mesic species. These physiological

traits would appear to enhance survival in semi-arid

regions, and minimise the cost of survival in terms of

body water. The small body size (high surface/volume

ratio) in the subpopulations where temperatures and

humidities were higher (Durban and Merrivale) than in

colder, drier regions (Estcourt and Harrismith) were heat

adaptive (McNab, 1970; Schleucher et al., 1991). Natural

selection has resulted in greater heat tolerance in the

smaller birds (Durban and Merrivale) and greater cold

tolerance in the larger birds (Estcourt and Harrismith).

Allometric equations for various avian physiological

parameters are well established and can be useful in

indicating quantitative shifts in function (Roberts and

Baudinette, 1986). Fiscal Shrike subpopulations showed

clinal trends in oxygen consumption, evaporative water

loss and body temperature that were correlated with

altitudinal and aridity gradients. Circadian rhythms also

showed climatic adaptations. The basal metabolic rates,

evaporative water loss and body temperatures in the

lowland (Durban and Merrivale) subpopulations were

higher than predicted by allometry, while the high

altitude populations (Estcourt and Harrismith) had

lower basal metabolic rates, evaporative water loss and

body temperatures than predicted by allometric equa-

tions. The deviations of the physiological parameters

examined from those predicted by allometry were

attributed to the phenotypic plasticity of this species to

physiological energy stresses associated with unpredict-

able resource availability in southern Africa. Climate

(which acts directly), combined ecologically through a

secondary effect on food availability, resulted in the

observed physiological parameters of the four subpopu-

lations. The effects of this plasticity in thermal character-

istics contributes to the overwintering success of Fiscal

Shrikes in severe climates throughout their winter range.

Acknowledgements

The project was funded by the National Research

Foundation (NRF: GUN 2039451), University of Natal,

and KwaZulu-Natal Ornithological Trust. S. Shezi took

excellent care of the Fiscal Shrikes whenever I was away.

A. Grace constructed the metabolic chambers. V. Reddy

and M. Natasen-Moodley assisted with bird capture.

Birds were collected with permission from the KwaZulu-

Natal Wildlife (Permit Number 722/1999) and the Free

State Department of Environmental Affairs and Tour-

ism (Permit Number HK/P1/02508/001).

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Documents

Physiological variability in the Fiscal Shrike Lanius collaris along an altitudinal gradient in South Africa