gy, Part A 143 (2006) 459–468www.elsevier.com/locate/cbpa

Comparative Biochemistry and Physiolo

Development of parameters influencing blood oxygen carryingcapacity in the welcome swallow and fairy martin

Prudence Simmons a, Alan Lill a,b,⁎

a Wildlife Ecology Research Group, School of Biological Sciences, Monash University, Victoria 3800, Australiab School of Psychology, Psychiatry and Psychological Medicine, Monash University, Victoria 3800, Australia

Received 31 August 2005; received in revised form 12 December 2005; accepted 18 December 2005

Abstract

Welcome swallow (Hirundo neoxena) and fairy martin (Petrochelidon ariel) nestlings develop relatively slowly. They exceed adult mass earlyin development, then lose weight and fledge at about adult mass, i.e. have a mass-overshoot-recession (MOR) growth profile. Development ofparameters influencing blood oxygen carrying capacity (O2Cap) was documented to determine if O2Cap also reached a plateau substantiallybefore fledging or increased continuously throughout nestling development. Hematocrit (Hct), erythrocyte count (RBC) and whole bloodhaemoglobin (Hb) increased 1.8- to 2.8-fold, so that O2Cap doubled during development in both species. Increase in Hct, Hb and RBC was notcontinuous, peak values occurring well before fledging, in contrast to passerines with standard growth profiles in which the increase occursthroughout nestling development and peak values occur at fledging. However, the timing of O2Cap increase differed from that in some other MOR

species (e.g. shearwaters). Mean erythrocyte volume (MCV) decreased linearly throughout development by 30–41%, but mean erythrocytehaemoglobin content (MCH) remained constant, so that mean erythrocyte haemoglobin concentration (MCHC) increased linearly 1.3- to 1.5-fold.Possible reasons for the apparent differences in the timing of O2Cap increase between rapidly and slowly growing altricial species and amongMOR species are discussed.© 2006 Elsevier Inc. All rights reserved.

Keywords: Swallow; Martin; Blood oxygen carrying capacity; Nestling development; Mass overshoot

1. Introduction

Growth curves (body mass as a function of age) of altricialnestlings are usually sigmoidal, but there is variation amongspecies in when, and at what proportion of adult mass, theasymptote is reached (O'Connor, 1984). It can be: (a) attainedafter fledging and equivalent to adult mass, (b) attained sub-stantially before fledging and either significantly less than or thesame as adult mass (standard or STD growth profile) and (c)reached relatively early in development and significantly exceedadult mass, before declining to adult level at fledging (mass-overshoot-and-recession or MOR growth profile) (Bryant andGardiner, 1979; O'Connor, 1984; Bolton et al., 1999).

⁎ Corresponding author. Wildlife Ecology Research Group, School ofBiological Sciences, Monash University, Victoria 3800, Australia. Tel.: +61 3990 55664; fax: +61 3 9905 5613.

E-mail address: Alan.Lill@sci.monash.edu.au (A. Lill).

1095-6433/$ - see front matter © 2006 Elsevier Inc. All rights reserved.doi:10.1016/j.cbpa.2005.12.018

Ricklefs et al. (1998) argued that tissue growth and attain-ment of mature function cannot be achieved simultaneously indeveloping birds due to molecular or biochemical constraints.Selection appears to have favored rapid tissue growth in specieswith STD growth profiles because of its anti-predation value;the ‘trade-off’ has been relatively immature function at fledging.In contrast, selection has apparently favored the attainment of ahigh level of mature function at fledging in species with theMOR growth pattern, probably because their food resources areunpredictable and exacting to exploit; the ‘trade-off’ has beenrelatively slow nestling development (O'Connor, 1984). The keyecological factors distinguishing the two patterns may thus be thespatio-temporal dispersion of food resources and the energeticcost of exploiting them (Bryant and Gardiner, 1979; Kostelecka-Myrcha and Jaroszewicz, 1993). These heritable growth patternshave different energetic consequences for nestlings and parentswith respect to the timing of resource allocation to growth andmaintenance and the magnitude of peak daily and total energyexpenditures (O'Connor, 1984; Weathers, 1992). Therefore,

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notwithstanding the equivocal evidence concerning a stronggeneral correlation between growth rates and metabolic rates(MR) of birds (Ricklefs et al., 1998), it is pertinent to examinewhether these different altricial growth patterns are associatedwith differing patterns of metabolic development.

Blood oxygen carrying capacity (O2Cap), a key factor inoxidative metabolism, has a development pattern that appears tovary as a function of growth profile. Thus in altricial species withSTD profiles, some of the key variables influencing O2Cap tendto increase linearly throughout nestling development (Kost-elecka-Myrcha et al., 1970, 1971, 1972, 1973; Bolton et al.,1999). In contrast, in the altricial northern house martin(Delichon urbicum) which has a MOR growth profile, thesevariables increase rapidly initially and then either do not increaseany further or increase much more slowly (Kostelecka-Myrchaand Jaroszewicz, 1993). Three Procellariiform species, whosedevelopment is intermediate between the altricial and precocialmodes (Sotherland and Rahn, 1987) but which have MORgrowth profiles, also exhibit a developmental pattern of O2Capincrease that is not continuous (Kostelecka-Myrcha and Myrcha,1989; Arnold et al., 1999; O'Dwyer, 2004). These contrasts in thetiming of developmental increase in O2Cap therefore appear tobe associated with the differing growth profiles evolved byMORand STD growth species. However, this conclusion is currentlybased on data for only about eight species, two of which are notfully altricial, and so it requires further verification.

In SE Australia, the welcome swallow (Hirundo neoxena)(adult mass 15 g) and fairy martin (Petrochelidon ariel) (11 g) arepartial seasonal migrants that breed in spring and summer (Pizzeyand Knight, 1997). Fairy martins always, and welcome swallowssometimes, nest colonially. The swallow's mean nestling period(NP) in Australia is 6% longer and the martin's 37% longer thanpredicted from adult bodymass using Eq. (6) ofWeathers (1992).Nestlings of both species have MOR growth profiles, substan-tially exceeding adult mass before declining to be about equal toit at fledging. Fledglings of both species are relatively mature andhighly mobile (Tarburton, 1991, 1993; Magrath, 1999).

This investigation documented the development pattern ofsome of the main blood parameters influencing O2Cap innestlings of these two species: Hct, Hb, RBC, mean erythrocytevolume (MCV), mean erythrocyte haemoglobin content (MCH)and mean erythrocyte haemoglobin concentration (MCHC).Given the growth profile of these aerial insectivores, wepredicted that the increase in Hct, Hb and RBC would not be acontinuous, linear function of nestling age. We also determinedprecisely when the main period of increase in these key variablesoccurred, because the timing varies among the fewMOR speciesstudied to date (Kostelecka-Myrcha and Jaroszewicz, 1993;Arnold et al., 1999; O'Dwyer, 2004) and the functional signif-icance of this variation is not entirely clear.

2. Materials and methods

2.1. Study areas

The study was conducted from September 2002 toFebruary 2003 at 10 sites in 5 districts in southern Victoria,

Australia: the Yarra Valley (37°40′S, 145°24′E), Murrindindi(37°46′S, 145°02′E), Clayton (37°46′S, 145°07′E), Beveridge(37°28′S, 145°02′E) and the You Yangs (37°55′S, 144°26′E).Mean monthly rainfall during the study period ranged from 10.22(Beveridge, December) to 71.6 mm (Yarra Valley, October). Thelowest mean monthly minimum ambient temperature was 4.1 °C(Yarra Valley, September) and the highest mean monthly maxi-mum ambient temperature was 30.7 °C (Murrindindi, January).Nests of both species were situated mainly under bridges and inculverts beneath roads, but some swallow nests were attached tobuildings. Many adults in colonies made multiple breeding at-tempts during the study, particularly where adverse weathercaused failure early in the season.

2.2. Sampling techniques

Breeding chronology was monitored by inserting a smalllight source and either a mirror or an Olympus BF laparascopeinto enclosed martin nests and inspecting open-cup swallownests directly or with a mirror attached to an extendable alumi-num pole. Martin nestlings were accessed by cutting a smallhole in the nest wall, which was re-sealed with mud after theyoung had been processed. We sampled entire martin broodssimultaneously to minimize disturbance, but swallow broodmembers were sometimes sampled separately and marked withnon-toxic food dye to preclude later re-sampling.

We determined exact ages of all martin and about half of theswallow nestlings by recording hatching, but had to estimateapproximate ages (±2 days) of the other swallow nestlings fromtheir plumage development and body mass (using the mass×age relationship derived from our own data and that of Tarbur-ton, 1993). We sampled nestlings of ages encompassing theentire development range once each to maintain statisticalindependence of the data. Nestlings were weighed (±0.5g) witha Pesola spring balance. A blood sample was obtained from theunderside of the wing by venipuncture with a 27 gauge hypo-dermic needle and withdrawal by capillarity into heparinisedmicrohematocrit tubes (for Hct and RBC) or a cuvette coatedwith sodium salts (for Hb). The former samples were stored onice until they were processed in the laboratory within 1–6 h ofsampling, but Hb was measured immediately.

Blood variables were measured with standard techniques de-veloped for human blood and commonly used on birds (Lewis etal., 2001; Campbell, 1995). Hct (%) was measured after centri-fugation for 3 min at 13,000 g. Hb (g dl−1 blood) was measuredon a 5 μl blood sample with a HemoCue Classic® hemoglobinphotometer, which converts hemoglobin to azidemethemoglo-bin, whose absorbance is measured at 570 and 880 nm. Thisphotometer generates Hb values for human blood closely compa-rable to those provided by the ICSH reference method (Bäck etal., 2004) and for avian blood values averaging 1.0 g dl−1 greaterthan those provided by cyanomethaemoglobin spectrophotom-etry (Lill and Baldwin, unpublished data). Erythrocyte counts(RBC) (cells×1012 l−1) were determined from 10 to 20 μl bloodsamples with an Improved Neubauer hemocytometer. Each sam-ple was counted three times and the mean was calculated; theaverage variation among the three counts from the same bird

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was 8.1%. From these measurements and with appropriatecorrections to common units, we also calculated MCV (in femto-litres fL) (Hct÷RBC), MCH (in picograms pg) (Hb÷RBC) andMCHC (g l−1) (Hb×10/Hct). Measurement error for Hct (0.02%)and RBC (16%) determined from repeated sampling of sixindividuals waswithin normally accepted limits for the techniquesused (Campbell, 1995) and should have been relatively constantamong samples for all nestling ages as the same experimentermade all measurements.

To compare fledging with adult values, we trapped samplesof breeding adults at nest sites in mist nets, a few of the swal-lows being caught in November 2003. Body mass and bloodparameters of adults were measured as for nestlings and the birdswere uniquely banded before release to preclude repeated sam-pling of individuals.

2.3. Data analysis

Statistical analyses were conducted with Systat version. 10.Data were normally distributed and therefore not transformed.We calculated the least squares regression that gave the best fitfor each variable as a function of nestling (estimated) age. Forbody mass, Hct, Hb and RBC, this was a quadratic regression,but in order to define the pattern of change in these variables

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s (g

)M

ass

(g)

Fig. 1. Postnatal growth curves for the welcome swallow and fairy martin. Dashed linby Oddjob two-phase regression procedure. Formulae and test statistics for the regres

more clearly, we also used the two-phase regression routine inOddjob version 5.1 (Dallal, 1989). This program fits apiecewise linear regression composed of two intersectingstraight lines to the relationship between two variables. Weused it to identify the two linear regressions with the biggestdifference from each other in slope that best described theunderlying relationship. When a development pattern was bestdescribed by a single linear regression term, change in theparameter was considered to be continuous; when the Oddjobtwo-phase regression test fitted two significant linear regres-sions to a pattern best described by a quadratic term, change wasdeemed not to be continuous. Development trends in MCV,MCH and MCHC were best described by linear regressions.Significance tests applied to the regression analyses testeddeviation of the slope from zero.

3. Results

3.1. Welcome swallow

The mean NP was about 23 days (n=20). Mean body massincreased 14-fold during nestling development and exhibited aMOR pattern (Fig. 1). It increased steadily during early develop-ment and peaked around day 12–13 when, on average, it was 26%

12 14 16 18 20 22 24

12 14 16 18 20 22 24

(days)

d Age (days)

e is the quadratic regression; solid lines are the two linear regressions generatedsions are given in Table 1. The mean adult value is indicated by a black triangle.

462 P. Simmons, A. Lill / Comparative Biochemistry and Physiology, Part A 143 (2006) 459–468

greater thanmean adult mass. However, by fledging, nestlingmasshad declined to 95%of themean adultmass of 14.6±1.2 g (n=20).

On average, Hct increased 2.3-fold during nestling develop-ment, from an estimated 18.5% at hatching to 42% at fledging(Fig. 2) However, two-phase regression analysis showed that itincreased linearly at a rate of about 2.7% daily until about day 9,but then remained constant (Table 1). Estimated mean Hct atfledging was 0.79× the mean value of 53% for 19 adults. RBCincreased 2.8-fold during the NP. However, two-phase regres-sion analysis revealed that it increased steadily only until day 16and then exhibited no further significant change prior to fledgingwhen, on average, it was only about 64% of the mean value of3.48±0.48×1012 cells l−1 for 17 adults. Hb increased 2.8-foldduring the initial 18 days of development and peaked at an esti-mated mean of approximately 17 g dl−1. However, it then declined

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Fig. 2. Developmental trends in blood variables in welcome swallow nestlings. Graphthe two linear regression functions derived from the Oddjob two-phase regressionregression functions. Formulae and test statistics for the regressions are given in Ta

significantly, to average an estimated 12.5 g dl−1 at fledging or68% of the mean adult value. MCVexhibited a continuous, lineardecline at a rate of 3.4 fl day−1 during nestling development toreach an estimated 160 fl at fledging, a value 30% less than athatching, but only 14% greater than the mean value of 140±41 flfor 16 breeding adults. However,MCH remained constant through-out nestling development and was within 1% of the mean adultvalue (53±8 pg; n=17) at fledging. MCHC increased linearlythroughout development at a daily rate of 3.8 g l−1, to bewithin 2%at fledging of the average value of 347±21 g l−1 for 15 adults.

3.2. Fairy martin

The mean NP was about 25 days (n=30). Mean nestlingmass increased 7.7-fold from hatching to fledging and exhibited

d Age (days)

d Age (days)

12 14 16 18 20 22 24

12 14 16 18 20 22 24

12 14 16 18 20 22 24

d Age (days)

s for Hct, RBC and Hb show the quadratic regression function (dashed line) andprocedure (solid line). Graphs for MCV, MCH and MCHC show simple linearble 1. All graphs also show the mean adult value (black triangle).

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MC

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HC

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per

litre

)

Fig. 2 (continued).

463P. Simmons, A. Lill / Comparative Biochemistry and Physiology, Part A 143 (2006) 459–468

a MOR pattern (Fig. 1). It increased steadily during earlydevelopment and peaked half way through the NP at a value27% greater than the mean mass of 20 breeding adults (10.6±0.8 g). It then declined steadily to be only about 9% above meanadult mass at fledging.

Mean Hct increased from an estimated 26% at hatching to42% at fledging (Fig. 3). Two-phase linear regression anal-ysis indicated that there was a steady increase until about onethird of the NP had elapsed, but no significant change thereafter(Table 1). Mean Hct of fledglings was 87% of the average valueof 47±8% for 19 adults. Mean RBC increased 2.2-fold duringnestling development. However, two-phase regression analysisagain showed that there was no significant increase after aboutday 20. Estimated mean RBC at fledging (2.15×1012 cells l−1)

was 70% of the mean value for 18 adults (3.06±0.6×1012

cells l−1). Hb (and hence O2Cap) increased by a factor of 2.4during the first 19 days of nestling development. However,there was no further significant change prior to fledging,when estimated mean Hb was 11.5 g dl−1 or 78% of themean value recorded for 20 breeding adults.

In martin nestlings, MCV decreased continuously andlinearly throughout development at a rate of 4.74 fl day−1 andwas estimated to be 145 fl at fledging. This value was 69% ofthe value at hatching and 90% of the mean value for 16adults (162±25 fl). Nestling MCH remained constantthroughout development and was 96% of the adult meanvalue (50±9 pg, n=18) at fledging. MCHC exhibited a linear,1.5-fold increase during nestling development and at fledging

Table 1Regression of body mass and blood parameters on nestling age in the welcomeswallow and fairy martin

Dependent Regression Regression equation r2 N Pvariable type

Welcome swallowM Quadratic M=−0.086 (A)2+2.369

(A)−2.9870.822 76 b0.001

Linearp1(b12.5) Mp1=1.555 (A)−0.647 0.870 49 b0.001Linearp2(N12.5) Mp2=−0.507 (A)+25.116 0.295 27 0.003

Hct Quadratic Hct=−0.126 (A)2+3.892(A)+13.452

0.67 73 b0.001

Linear p1(b9.6) Hctp1=2.71 (A)+15.531 0.659 33 b0.001Linear p2(N9.6) Hctp2=0.029 (A)+41.29 0.659 40 0.905

RBC Quadratic RBC=−0.007 (A)2+0.342(A)+0.342

0.476 75 b0.001

Linearp1(b16) RBCp1=0.135 (A)+0.71 0.505 57 b0.001Linearp2(N16) RBCp2=−0.118 (A)+4.761 0.187 13 0.141

Hb Quadratic Hb=−0.04 (A)2+1.358(A)+2.707

0.71 74 b0.001

Linearp1(b17.7) Hbp1=0.634 (A)−5.167 0.718 61 b0.001Linearp2(N17.7) Hbp2=−1.262 (A)+38.816 0.611 13 b0.001

MCV Linear MCV=−3.402 (A)+234.69 0.125 68 0.003MCH Linear MCH=−0.366 (A)+64.088 0.019 71 0.256MCHC Linear MCHC=3.75 (A)+256.46 0.275 72 b0.001

Fairy martinM Quadratic M=−0.044 (A)2+1.497

(A)−0.0060.838 91 b0.001

Linearp1(b12.5) Mp1=1.0 (A)+0.874 0.691 51 b0.001Linearp2(N12.5) Mp2=−0.167 (A)+15.477 0.101 40 0.046

Hct Quadratic Hct=−0.056 (A)2+2.023(A)+21.893

0.59 79 b0.001

Linearp1(b8) Hctp1=1.88 (A)+21.414 0.407 30 b0.001Linearp2(N8) Hctp2=0.27 (A)+34.286 0.072 49 0.062

RBC Quadratic RBC=−0.003 (A)2+0.149(A)+0.724

0.787 75 b0.001

Linearp1(b19.5) RBCp1=0.097 (A)+0.878 0.799 53 b0.001Linearp2(N19.5) RBCp2=0.183 (A)+6.348 0.118 22 0.118

Hb Quadratic Hb=−0.013 (A)2+0.664(A)+4.389

0.772 81 b0.001

Linearp1(b19) Hbp1=0.425 (A)−5.022 0.792 59 b0.001Linearp2(N19) Hbp2=−0.616 (A)+25.016 0.052 22 0.307

MCV Linear MCV=−4.725 (A)+248.58 0.501 71 b0.001MCH Linear MCH=−0.215 (A)+52.617 0.05 70 0.063MCHC Linear MCHC=4.865 (A)+214.58 0.581 73 b0.001

A = age, N = sample size, M = mass and P = probability (to 3 decimal places).Abbreviations for blood parameters given in Materials and methods. p1 and p2

indicate first and second linear regressions fitted to blood parameters by Oddjobtwo-phase regression routine; numbers in parentheses indicate split pointdetermined by this routine.

464 P. Simmons, A. Lill / Comparative Biochemistry and Physiology, Part A 143 (2006) 459–468

was estimated to be 320 g l−1 or within 2% of the mean adultvalue.

4. Discussion

4.1. Basic mechanism of O2Cap developmental increase inaltricial nestlings

The basic mechanism through which O2Cap increases duringnestling growth has only been documented for a few fullyaltricial bird species. Characteristically, RBC increases at a pro-portionately faster rate than MCV decreases, so that Hb and

O2Cap increase markedly during nestling development (e.g.Kostelecka-Myrcha and Jaroszewicz, 1993; Bolton et al., 1999).Usually MCH decreases but MCHC increases (e.g. Kostelecka-Myrcha et al., 1972), although neither trend is universal amongthe studied species (e.g. Kostelecka-Myrcha et al., 1970, 1973;Kostelecka-Myrcha and Myrcha, 1980). MCV decrease mayenhance the rate of blood oxygenation and deoxygenationbecause of the concomitant decrease in the length of the oxygendiffusion pathway within the erythrocytes (Jones, 1979; Lay andBaldwin, 1998) and it may also prevent Hct reaching levelswhere blood flow rate is significantly reduced by increasedblood viscosity (Wells and Baldwin, 1990).

Development of O2Cap in nestling welcome swallows andfairy martins broadly conformed to this basic mechanism.RBC, Hct and Hb increased 2.2- to 2.8-fold during devel-opment; however, Hb increased by a similar factor as RBC,because MCH actually remained constant during develop-ment. The increase in Hct was proportionally less than that inRBC because MCV decreased continuously and linearly by30% to 41% during development. MCHC exhibited a con-tinuous, linear increase throughout development that resultedin a fledging value 32–47% higher than at hatching and within2% of typical adult levels. The conformity of the mechanismof O2Cap increase in the study species with that reported forother altricial species supports the contention that the me-chanism responsible for O2Cap development is common toall altricial bird species (Kostelecka-Myrcha et al., 1996),although further comparative investigations would bevaluable.

4.2. Functional significance of swallow and martin O2Capdevelopment patterns

Increase in the key variables influencing O2Cap was notcontinuous throughout nestling development in either species.RBC and Hb increased steadily during the first 67–80% ofdevelopment and then remained constant or even decreased(welcome swallow Hb) until fledging occurred. Hct exhibited asimilar pattern, but the fledging value was attained after just 36–39% of development had occurred. Presumably adult Hct is anoptimal compromise between the competing demands of oxy-gen transport and constraint of blood viscosity (Wells andBaldwin, 1990; Schmidt-Nielsen, 1995). The very early devel-opmental peak in this parameter at 80–87% of mean adult levelshighlights the critical role that reciprocally tuned rates of changein RBC and MCV must play in the development of O2Cap inswallow and martin nestlings.

If O2Cap is closely ‘tuned’ to the rate of aerobic metabolismin nestlings of the two study species, as the concept ofsymmorphosis (Taylor and Weibel, 1981) would predict, thedocumented development patterns of the blood parametersinfluencing O2Cap seem to make sense functionally. O2Capincreased continuously and rapidly throughout the main periodof body mass gain. Although by analogy this period probablyinvolves some fat deposition, it is also when most of the tissuesynthesis probably occurs and metabolic rate increasesexponentially (Bryant and Gardiner, 1979; Ar and Piontkewitz,

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(%

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Fig. 3. Developmental trends in blood variables in fairy martin nestlings. Graphs for Hct, RBC and Hb show the quadratic regression function (dashed line) and the twolinear regression functions derived from the Oddjob two-phase regression procedure (solid line). Graphs for MCV, MCH and MCHC show simple linear regressionfunctions. Formulae and test statistics for the regressions are given in Table 1. All graphs also show the mean adult value (black triangle).

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1992; Turner, 2004). Subsequent mass recession results mostlyfrom water loss from the integument (Turner, 2004) and totalMR decreases at this stage, which is thought to be a time ofphysiological maturation rather than synthesis of new tissue(Bryant and Gardiner, 1979; Bryant and Hails, 1983; Ar andPiontkewitz, 1992). If this scenario applies to welcome swallowand fairy martin nestlings, any further increase in O2Cap at themass asymptote-recession stage would be unnecessary, becausethe parameter is already close to the adult level, tissue growth isminimal and further increase would entail the costs of metabolicmaintenance of additional erythrocytes and possibly of a reducedblood flow rate caused by a rise in blood viscosity (Wells and

Baldwin, 1990). Even if O2Cap were not closely tuned to thedeveloping nestlings' oxidative capacity (Konarszewski, 1994;Bech and Klaassen, 1996), most aspects of oxidative metabolismwould probably increase in parallel if nestling MR were mass-dependent.

4.3. Interspecific variation in the timing of O2Cap increase

STD and MOR species seem to differ in the timing ofincrease in the blood parameters influencing O2Cap. Nestlingsof five passerine species with STD growth exhibit a pattern ofcontinuous increase in Hct, RBC and Hb during development

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Fig. 3 (continued).

466 P. Simmons, A. Lill / Comparative Biochemistry and Physiology, Part A 143 (2006) 459–468

(Kostelecka-Myrcha et al., 1970, 1971, 1972, 1973; Bolton etal., 1999), whereas in nestlings of the five MOR species in-vestigated to date (including the two studied here) these pa-rameters do not increase continuously throughout development.Ricklefs' theory (see Ricklefs et al., 1998) of the adaptivesignificance of variation in altricial growth profiles proposesthat the STD profile evolved under selection for rapid tissuegrowth and early fledging in predation-prone species, but theprotracted MOR profile evolved in species in which it isadvantageous in relation to food acquisition for young to fledgein a relatively more mature state. The longer NP required for thelatter strategy is supposedly permitted by the relative safety ofthe nest site. The theory is founded on the assumption that tissue

growth and attainment of mature function cannot be achievedsimultaneously in developing birds. In STD species, total MRand the rate of vascular O2 transport might therefore generallybe expected to increase continuously throughout the relativelyshort NP, whereas in MOR species increase should tend to bemore restricted to the early mass gain phase. The developmentpatterns of O2Cap in welcome swallows and fairy martinsappear to fit this prediction. In adult chickens, Hct is linearlyrelated to heart weight (Yahav et al., 1997); this is not surprisingbecause the required cardiac capacity will increase as bloodviscosity increases. It is conceivable that this relationship alsooccurs during nestling growth in altricial birds, so it would beinteresting to explore whether heart growth trajectories differ

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between species with STD and MOR growth profiles. It is alsoplausible that the development patterns of other facets ofvascular oxygen transport and nestling metabolism may differbetween altricial species with these two types of growthprofile.

Commencement of, and restriction largely to the earlymass gain period of O2Cap increase does not, however, occurin all MOR species. In the semi-altricial Wilson's stormpetrel (Oceanites oceanicus), short-tailed shearwater (Puffinustenuirostris) and Gould's petrel (Pterodroma leucoptera),which all have MOR growth profiles, O2Cap increase occursmainly after the main period of mass gain (Kostelecka-Myrchaand Myrcha, 1989; Arnold et al., 1999; O'Dwyer, 2004).Arnold et al. (1999) speculated that the relatively low MR ofgrowing shearwater nestlings and the fact that much of theirmass gain stems from deposition of lipid, which has relativelylow metabolic maintenance costs (Hayes, 2001; Fitzherbert,1985), might have permitted adaptive temporal separation ofthe metabolic costs of tissue synthesis from those of main-tenance of an increased population of smaller erythrocytes.The NPs of the welcome swallow and fairy martin are notlong enough to permit such a complete separation and there isa substantial overlap. The energetic basis of the MOR growthprofile varies among species; overshoot can involve adap-tive or default lipid storage or tissue biosynthesis; recessioncan involve lipid catabolism or water loss (O'Connor, 1984;Fitzherbert, 1985; Thomas et al., 1993). These differencescould potentially be reflected in even greater variation in thedevelopment pattern of O2Cap increase among MOR speciesthan identified here.

Acknowledgements

We thank Kevin Simmons and Belinda Lees for assistancewith fieldwork and Michael Magrath for advice about studyingfairy martins and access to unpublished growth data. We alsothank John Baldwin and two anonymous referees for valuablecomments on the manuscript. We gratefully acknowledge thestaff of the You Yangs Regional Park, Gwen, Fred and SteveSadlier, Gill dePuery, Mike Tarburton, Eric Tetlow, and ScottGroves for facilitating the study in various ways. The study wasapproved by the Monash University School of Biological Sci-ences AEC and the Victorian Department of Sustainability andEnvironment.

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