Calcium supplementation of breeding birds: directions for future research

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© 2004 British Ornithologists’ Union

Blackwell Publishing, Ltd.

Review paper

Calcium supplementation of breeding birds: directions

for future research

S. JAMES REYNOLDS,

1

* RAIVO MÄND

2

& VALLO TILGAR

2

1

School of Biosciences, The University of Birmingham, Edgbaston, Birmingham B15 2TT, UK

2

Animal Ecology Section, Institute of Zoology and Hydrobiology, University of Tartu, Vanemuise 46, Tartu 51014, Estonia

Calcium is an essential nutrient for avian reproduction. Calcium-rich foods are consumedby breeding birds for production of eggshells and for provisioning chicks that are mineral-izing skeletal tissues. A number of studies have documented calcium-limited reproduction,and calcium supplementation has been employed over the last decade to demonstratedegrees, causes and consequences of calcium limitation. However, supplementation studieshave produced equivocal findings resulting from an absence of calcium limitation in thestudy species, a poorly designed supplementation procedure or both. Prior to effective calciumsupplementation, many factors need to be considered. Calcium-limited breeding in birdscan only be detected by monitoring breeding attempts for more than one year and by ensur-ing that the measured breeding parameters are sensitive to calcium availability. Naturalcalcium availability needs to be estimated, and daily calcium budgets for the appropriatereproductive stages determined for the study species. Most crucially, if calcium limitationof breeding is caused by secondary calcium limitation (e.g. through heavy metal toxicity),calcium supplementation will probably be ineffective. Effective calcium supplementationwill then be achieved through careful planning – a study over several years using appropriatesupplements (i.e. naturally occurring ones used by breeding birds), applied at the appropri-ate time of year (i.e. prelaying and/or chick-rearing phases) and using a response variablethat is highly sensitive to calcium availability. If properly planned and performed, calciumsupplementation is a cost-effective and potent tool for the study of bird breeding biology.

Calcium is probably the most important micronutrientnecessary for successful breeding in birds (Reynolds &Perrins 2004). Up to 98% of the dry mass of the avianeggshell consists of a crystalline form of calcium carbonatecalled calcium hydroxyapatite. Among its numerousfunctions, the eggshell prevents the incubating adultbird from crushing the egg contents, resists the entryof pathogens into the egg, controls the exchange ofgases between the egg contents and the nest micro-environment, and provides a source of calcium to theembryo for early skeletal mineralization. For manyspecies, the requirements for dietary calcium remainhigh during postnatal development of chicks, when

mineralization of their skeletons continues (Starck1998). Precocial chicks forage extensively for calcium-rich foods, whereas altricial chicks are fed calcareousfood in the nest by their parents (see table 3 inGraveland 1996).

Apart from a few isolated reports on trace elementsand their importance in the diet of egg-laying poultry(e.g. copper, Baumgartner

et al

. 1978), micronutrientlimitation on breeding performance of birds has beenlargely neglected until recently. The focus on calciumwas sharpened, however, with the publication of apaper by Drent and Woldendorp (1989), who reporteda sharp decline in the breeding performance of GreatTits

Parus major

resident in the Buunderkamp forestin The Netherlands. Birds laid eggs with no shellsor with such thin shells that embryos died from

*Corresponding author.E-mail: [email protected]

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S. J. Reynolds, R. Mänd & V. Tilgar

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desiccation due to excessive and uncontrolled waterloss during incubation. The authors found similareggshell defects in resident Blue Tits

Parus caeruleus

,Coal Tits

P. ater

, Wood Nuthatches

Sitta europaea

and Great Spotted Woodpeckers

Dendrocopos major

,but not in migratory Pied Flycatchers

Ficedula hypo-leuca

. Drent and Woldendorp (1989) attributed thedeclines in eggshell quality to low calcium availabilityon poor sandy soils in their study area, further com-pounded by the adverse effects of acid rain on calciumretention in base-poor soils with low bufferingcapacities. Hydrogen ions leach calcium ions fromtopsoil and the latter are replaced by toxic cationssuch as aluminium and lead. As pH declines, toxiccation concentration increases and uptake of calciumis impaired. Drent and Woldendorp (1989) offeredcompelling evidence for a relationship betweenexogenous calcium availability and breeding perform

-

ance of birds. For example, they found that eggshelldefects were absent in Great Tits breeding on soils ofbetter quality (e.g. loam, clay).

Following the work of Drent and Woldendorp(1989), Graveland

et al

. (1994) supplemented GreatTits breeding in the Buunderkamp forest withfragments of snail shell and eggshell of DomesticChickens

Gallus domesticus

, which resulted in a sig-nificant increase in eggshell quality. They thereby

explained the declines in Great Tit breeding perform

-

ance in terms of the inadequate availability of snailshells, the main source of dietary calcium (Graveland1996, Graveland & Drent 1997). Since the findings ofDrent and Woldendorp (1989) and Graveland

et al

.(1994), a number of studies have provided further evid

-

ence of calcium-limited reproduction in Europeanand North American species (Table 1).

Detection of calcium-limited reproduction ofbirds is possible in habitats where the decline incalcium availability has been rapid and the impact onbreeding performance dramatic and easily monitored.For example, the percentage of territorial Great Titsbreeding in calcium-poor areas of the Buunderkampforest that produced inferior eggshells increased from12% in 1983 to 57% in 1988 (Drent & Woldendorp1989), because calcium was lost through severeanthropogenic acidification.

Calcium-limited reproduction can be much moredifficult to identify in habitats where the decline incalcium availability has been protracted and gradual.Under these circumstances, ‘snapshots’ of breedingperformance over a few years provide no grounds forconcern. Longitudinal studies of this duration pro-vide a detailed description of interannual variationfor a given species, but ‘saw-tooth’ patterns in repro-ductive parameters (e.g. laying date) often mask a

Table 1. Evidence of calcium-limited reproduction in birds. Adapted from Reynolds and Perrins (2004).

Species Evidence Reference

Black Tern Thin-shelled eggs, incomplete clutches and hatching failure

Beintema et al. (1997)

Great Spotted Woodpecker Thin-shelled eggs Drent and Woldendorp (1989)Tree Swallow Reduced egg size and clutch volume

Reduced egg size and hatching success (no. fledged per nestbox)

Blancher and McNicol (1988)St. Louis and Barlow (1993)

Great Tit Incubating empty nests Schmidt and Zitzmann (1990), Winkel andHudde (1990), Zang (1998)

Reduced clutch and egg size and abnormal shell structure

Carlsson et al. (1991), Weimer and Schmidt (1998)

Eggshell defects and clutch desertion Graveland et al. (1994), Pinxten and Eens (1997)

Blue Tit Reduced breeding success and reduced number of fledglings

Dekhuijzen and Schuijl (1996)

Incubating empty nests Schmidt and Zitzmann (1990)

Wood Nuthatch Thin-shelled eggs Drent and Woldendorp (1989)

White-throated Dipper Thin-shelled eggs Ormerod et al. (1991)

Meadow Pipit Anthus pratensis Thin-shelled eggs Bureß and Weidinger (2001)

Eastern Kingbird Tyranus tyranus Retarded laying date, reduced clutch and brood size, reduced hatching success and eggs with thin, permeable shells

Glooschenko et al. (1986)


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persistent decline of overall breeding performancethat is only detected after many decades of sustainedmonitoring (e.g. Crick & Sparks 1999). A case inpoint is the secondary calcium limitation caused bythe widespread use of the biocide dichlorodiphenyl-trichloroethane (DDT) and the consequent declineof raptor populations in Europe (Ratcliffe 1967).The best-documented case of DDT-related decline isthat of the Peregrine Falcon

Falco peregrinus

in Britain(Mellanby 1992). DDT caused the thinning of egg-shells, which subsequently broke during incubation.The incidence of shell breakage was

c

. 4% in 1939,but rose to

c

. 39% in 1951. Measurements of Peregrineeggs revealed that eggshell thickness was constantfrom 1850 to 1947, but then declined rapidly in 1947,coinciding with the extensive application of DDT.

Such studies are valuable, but they are scarce in theornithological literature. Although studies performedover a number of decades are perhaps the best wayto detect subtle fluctuations in exogenous calciumavailability, such an approach requires a substantialtemporal and financial investment (Green 2002).The detection of calcium-limited reproduction inbirds resulting from rapid and steep declines incalcium availability (e.g. through acidification – seereview by Graveland 1998) is facilitated by calciumsupplementation of birds during the breeding sea-son. A number of such investigations have beenperformed in the last decade (Table 2), but equivocalfindings from such studies have prompted us towrite this review. The cost effectiveness and ease ofemployment of calcium supplementation make it an

attractive technique that is effective if care is taken inits use (Fig. 1). Such care has not always been apparentin published accounts of calcium-supplementationexperiments. We hope that ornithologists in futurewill consider the issues that we raise, prior toperforming calcium supplementation in the field.

In this review, we present the main findings fromcalcium-supplementation experiments on birds, andsuggest possible reasons for the lack of significantresults in some investigations. We then suggest anumber of issues that should be considered in theplanning of investigations. Readers should note thatthroughout this review we refer to the methods usedby Graveland (1995) in his studies on small passer-ines (especially Great Tits) in The Netherlands. Hisstudy remains the model for calcium-supplementationand, as such, exemplifies the use of many of our sug-gestions in the planning of an effective calcium-supplementation exercise. Finally, we discuss brieflyhow findings from calcium-supplementation studiescan be applied in ornithology.

CALCIUM SUPPLEMENTATION

EXPERIMENTS: HOW EFFECTIVE

HAVE THEY BEEN?

Table 2 lists the effects of calcium supplementationon the breeding performance of birds. Althoughmost investigations have reported some measurableimprovement in breeding parameters, this has notalways been so. Effects of supplementation havebeen measured in terms of egg traits (clutch and egg

Table 2. The effects of calcium supplementation on reproductive parameters of birds. Adapted from Reynolds and Perrins (2004).

Species Effects Reference

Cape Vulture Significant decrease in the incidence of osteodystrophy in chicks

Richardson et al. (1986)

Black Tern Increase in body mass of chicks at 15 days of age Beintema et al. (1997)Great Tit Reduction in: number of females without eggs;

clutch desertion; defective eggshells; non-hatched eggs per clutch. No effect on clutch size or laying datePositive effect on: clutch size; eggshell thickness; lay date; brood size; chick growth; fledgling numbers

Graveland et al. (1994), Graveland and Drent (1997)

Mänd et al. (1998, 2000b), Tilgar et al. (1999a,1999b, 2002), Tilgar (2002)

Blue Tit No effect found on: egg mass and volume; eggshell mass and thickness; onset of laying; clutch size; fledging success

Ramsay and Houston (1999)

Pied Flycatcher Positive effect on: egg volume; eggshell thickness; lay date; chick growth; female condition

Mänd et al. (1998), Mänd and Tilgar (2003), Tilgar (2002), Tilgar et al. (1999a, 1999b)

Purple Martin No effect on growth rate of nestlings Poulin and Brigham (2001)

House Wren No effect on: egg size; number of fledglings; fledgling body mass. Tendency to lay more eggs

Johnson and Barclay (1996)

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size, eggshell thickness, eggshell defects, hatchingsuccess), chick traits (brood size, body mass, growth,fledging success) or female body condition.

Egg traits

Since Drent and Woldendorp (1989) first observedthe defective eggshell structure of forest passerines,egg properties have been the favoured responsevariables for many calcium-supplementation studies(Table 2). Most have been successful in producing

improvement in at least one egg parameter. Interest-ingly, relatively few of the food-supplementationstudies of birds have reported a significant elevationin clutch sizes, and fewer still have reported anaccompanying advancement in laying dates (reviewedin Christians 2002). Nevertheless, the savings inenergetic expenditure, and in time, accrued bybreeding birds as a result of calcium supplementa-tion might be larger than those from macronutrient(e.g. proteins, fats, etc.) supplementation, which mightexplain why calcium supplements advance laying

Figure 1. Schematic diagram summarizing the main considerations in the planning of calcium-supplementation studies of reproductivebirds. Text in boxes relates to questions (and their outcomes) before and after calcium supplementation. Italicized text relates to the mainquestions that require answering at each stage of the calcium-supplementation planning process.


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and increase clutch size more often than do macro-nutrients (Turner 1982).

In stark contrast to the studies of Dutch (e.g.Graveland 1995) and Estonian (e.g. Tilgar 2002)researchers, some calcium-supplementation studieshave been completely ineffective. Most notable ofthese was a study of breeding Blue Tits in Scotlandby Ramsay and Houston (1999). Their study area inwest-central Scotland is among the most adverselyaffected by acid precipitation in the entire UK and,as such, snail abundance and exchangeable calciumare more depressed than those in the study area ofGraveland in The Netherlands. However, provisionof supplements resulted in no significant increase inegg mass, egg size, eggshell mass, eggshell thickness,clutch size or hatching success, and in no significantadvancement of laying. Ramsay and Houston (1999)found that snail density in leaf litter and the top 2 cmof mineral soil was extremely low (i.e. 0.36 snails/m

2

),but when they examined the gizzard contents of afemale collected during egg-laying, they found largenumbers of small snails and calcareous fragments includ

-

ing bones and teeth. These results indicate that calciumavailability is difficult to measure reliably, especiallywhen some calcium-rich foods are found by birds inareas that are inaccessible to researchers (e.g. marshes).Calcium supplementation of breeding birds will beineffective in most cases if natural foods are provid-ing sufficient dietary calcium for the birds’ breedingrequirements (see also Johnson & Barclay 1996).

Even studies with captive birds in which calciumavailability can be tightly controlled have been oflimited value. Reynolds (2001) attempted to identifya dietary calcium threshold below which captiveZebra Finches

Taeniopygia guttata

would struggle toproduce eggs. Removal of all calcium-rich foods (i.e.calcareous grit, cuttlefish bone) for 72 h during egg-laying, leaving only chick flint grit (2.2% calcium bymass) as a mechanical grinding agent, resulted infemales showing some calcium stress (i.e. reducedcalcium content of shells in successively laid eggs),but no declines in other egg (volume, eggshell mass,thickness and surface area) or laying (clutch size, lay-ing interval) parameters. On the basis of publishedestimates for calcium content of millet seed anddigestive efficiency for calcium, Reynolds (2001)calculated that an average female Zebra Finch wouldhave had to consume more than 1 g of flint grit perday to produce a fully calcified egg. Such grit con-sumption seems highly unlikely given that the averagebody mass of this species is only 12.5 g (Zann 1996).Instead, this estimate casts doubt on the accuracy of

the digestive efficiency for calcium (calculated as theaverage provided by El-Wailly 1966 and Lemon 1993,respectively). Further research is required on digestiveefficiency if the assimilation efficiency of nutrients isto be calculated accurately.

Chick traits

Calcium supplementation of chicks has beenachieved either directly through supplement admin-istration to chicks by experimenters or indirectlyvia provisioning adults. Direct supplementation ofBlack Tern

Chlidonias niger

chicks by Beintema

et al

.(1997) succeeded because calcium deficiency wasidentified prior to chick-feeding trials as the majorcause of poor chick development and so depressingbreeding performance. Post-mortem examinationsof tern chicks from acid bogs in The Netherlands,which had died prior to 35 days of age, revealed theoccurrence of severe rickets and spontaneous frac-tures in wing and leg bones. Force-feeding of calciumpills three times a week dramatically improvedfledging success and mass gain, and confirmed theresearchers’ suspicions that adults were feedingchicks with prey containing insufficient calcium tosustain normal skeletal development.

By contrast, Poulin and Brigham (2001) force-fedcalcium to Purple Martin

Progne subis

chicks and,from a lack of improvement in their growth rates,concluded that growth was not limited by a calcium-deficient diet. Unlike the study of Beintema

et al

.(1997), Poulin and Brigham (2001) only hypothe-sized that the growth of martin chicks would becalcium-limited by virtue of their calcium-poor insectdiet and an inability of provisioning adults to forageeffectively on the ground, where calcareous materialwas predominantly found. Their failure to detectcalcium-limited growth may indeed indicate a genuineabsence of calcium limitation at the nestling stage;however, calcium was provided as a solution of LiquidCalcium®, whereas nestlings are usually supplementednaturally with solid forms of calcium (see Graveland1996). Although nestlings presumably assimilatedsome of the administered calcium, much of it wasprobably excreted soon after force-feeding. In mostaltricial nestlings, the loss of calcium in solutioncould be high, with both the mean retention time ofdigesta and the digestive efficiency increasing withnestling age (e.g. Caviedes-Vidal & Karasov 2001).Furthermore, unlike the study of Beintema

et al

. (1997),in which the efficacy of calcium supplementationwas easily measured through the survival of chicks,

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calcium limitations on development of PurpleMartins may be too subtle to detect from the mor-phometrics taken during the formative days of thenestling phase.

It is possible to supplement chicks successfullyby manipulating the diets of provisioning adults.Richardson

et al

. (1986) found that 6.8% of Cape

Gyps coprotheres

and 1.0% of African White-backedVulture

Gyps africanus

chicks were suffering fromosteodystrophy (metabolic bone disease) in ranchedareas of South Africa where hyaenas were absent.Hyaenas were the only carnivores that regularlychewed the bones of ungulate carcasses renderingsufficiently small bone fragments for adult vulturesto feed their chicks. In wild areas, where hyaena-produced bones were present, Richardson

et al

. (1986)found no chicks suffering from osteodystrophy. Theestablishment of ‘bone restaurants’, where crushedskeletons were provided for birds in ranched areas,resulted in a dramatic decline in the incidence ofosteodystrophy in Cape Griffon chicks.

Few studies, besides those discussed above, haveprovided supplements at the chick stage in isolationfrom other stages of reproduction. However, anumber have supplemented prelaying adults andthen investigated whether supplementation hasprotracted benefits to nestlings. Results have beenequivocal. Johnson and Barclay (1996) found thatsupplemented House Wrens

Troglodytes aedon

raisedfledglings with slightly longer feathers than unsup-plemented birds, but they did not produce more,or heavier, fledglings. Eeva (1996) found that calcium-supplemented Pied Flycatchers produced nestlingswith longer wings than did unsupplemented birds.Supplementation of Great Tit and Pied Flycatcherfemales in Estonia resulted in significant increases inchick growth in both species and in fledging successof the former (see Table 2). Furthermore, Tilgar

et al

. (2004) examined the activity of alkaline phos-phatase (ALP) in the plasma of 15-day-old GreatTit nestlings that had been raised by calcium-supplemented females and found that enzymic activitywas reduced compared with the control (unsupple-mented) group, possibly indicating lower osteoblasticactivity and more complete ossification. At the sametime, morphological parameters (tarsus length andbody mass) did not differ significantly betweenthese two treatment groups, perhaps due to compen-satory growth in the prefledging stage. Thus, bone-ALP activity might provide a more informativemeasure of skeletal development, and therefore ofoverall chick development, than morphometrics.

Female body condition

The condition of the breeding female in calcium-supplementation studies has rarely been studied.Mänd and Tilgar (2003) captured Pied Flycatcherand Great Tit females during the second half of thenestling period. They found that, in female flycatch-ers laying large clutches, calcium supplementationimproved body condition compared with unsupple-mented females. Flycatchers breeding in Estonianforests appear to invest in the current breedingattempt at the expense of their own body condition.However, calcium supplementation did not improvethe body condition of tits breeding in the samehabitat. Results concerning the significance offemale body condition in influencing the timingof reproductive events in birds remain equivocal.Whereas female body condition drives reproductive‘decisions’ in some species (e.g. Ruddy Duck

Oxyurajamaicensis

, Alisauskas & Ankney 1994), Hõrak

et al

. (1999) found that female Great Tits thatdeserted broods were in better nutritional condition(higher body mass, higher levels of free fattyacids) on day 8 of the nestling period than were non-deserters. Declines in body mass of reproductivefemale birds may indicate physiological stress (e.g.Drent & Daan 1980), but, alternatively, they mayreflect an adaptive response allowing energeticsavings to be made during breeding (e.g. Freed1981). We encourage researchers to make contem-poraneous measures of female body condition andother reproductive parameters during calciumsupplementation.

PLANNING OF CALCIUM-

SUPPLEMENTATION STUDIES

For calcium supplementation during the breedingseason to be informative, calcium must be constrain-ing the breeding performance of the study species.Although this might seem obvious, all too oftencalcium-supplementation studies have been basedon equivocal findings (see above). In some instances,calcium limitation is obvious prior to concertedinvestigation (e.g. Graveland

et al

. 1994) andsupplementation indicates the extent of calciumlimitation on breeding output. However, sometimescalcium supplementation has itself been used asan exploratory tool to identify whether calciumwas the constraint on breeding performance outof a number of potential constraints. Below wediscuss important aspects of experimental design that


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should be addressed prior to undertaking a calcium-supplementation study.

Duration of study

We recommend that the breeding performance ofindividuals be monitored for a number of successiveyears. Although within a given year an improvementin breeding performance with calcium supple-mentation may not be statistically significant (e.g.see table 1 in Tilgar

et al

. 2002), dietary calciumavailability may be detected as

the

constraint onavian reproduction when several years of a study areconsidered together. The degree of improvement inreproductive success as a result of nutrient supple-mentation is highly sensitive to environmental con-ditions, including climatic events and natural foodavailability in any given year. For example, Tilgar

et al

. (1999a) found that calcium supplementationonly advanced laying dates of tits and flycatcherssignificantly in years when the onset of breedingwas relatively late. Presumably, in such years, naturalfood availability was scarce and unsupplementedfemales had to invest significantly more time andenergy in calcium-specific foraging than they did inyears when natural food availability was higher or ifthey had been supplemented (Graveland & Berends1997).

The study site

Rarely are study sites established for the sole pur-pose of carrying out calcium-supplementation work.Therefore, such work must be designed thoughtfullywithin the constraints of an established study area.For example, the breeding performance of White-throated Dippers

Cinclus cinclus

varies markedlywith stream acidity in upland Wales (Ormerod

et al

.1991), and to test fully the merits of calcium supple-mentation at least ten acidic streams (five treatment,five control) and ten circumneutral streams(five treatment, five control) would be required(S.J. Ormerod, pers. comm.). In practice, identifying 20such sites is difficult and experimental designs requiremodification if calcium supplementation is to befeasible within the limitations imposed by a studysite.

Nevertheless, another example from Estonia dem-onstrates that with careful planning it is possible toperform effective calcium supplementation within aheterogeneous study area. Figure 2 illustrates thestudy area in southwestern Estonia where calciumsupplementation has been performed successfullyfor a number of years by two of the authors (R.M.and V.T.). Full details of the study area and thesupplementation procedure are given in Tilgar

et al

.(2002) but, briefly, Great Tits were supplemented

Figure 2. The distribution of nestbox lines within deciduous and coniferous forests of southwestern Estonia where Great Tits have beencalcium-supplemented successfully for a number of years. The lower panel shows a typical nestbox line with alternating blocks ofsupplemented and non-supplemented (control) nestboxes (see text for further details).

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by providing calcium-rich material at their nest-boxes. Nestboxes were arranged in lines, with eachline usually consisting of tens of nestboxes, confinedwithin a homogeneous habitat type (i.e. coniferousor deciduous; Fig. 2). Each nestbox line was dividedinto alternating supplemented and control blocks,each block consisting of roughly five consecutivenestboxes (see lower panel in Fig. 2). For a multiyearsupplementation study, each year the first block ofeach nestbox line was randomly assigned as supple-mented or control. Although nestboxes were 50–60 m apart, birds from control nestboxes might havetaken supplemental calcium from feeders at adjacentsupplemented nestboxes, and therefore data fromcontrol birds nesting within 100 m of a supplementedblock were disregarded.

Interspecific differences

For some species, the calcium demands of reproduc-tion can be substantial. For example, a typical clutchof Blue Tit eggs can contain more calcium than thelaying female’s entire skeleton (Perrins & Birkhead1983). Birds that regularly consume calcium-richdiets, such as raptors that eat skeletons of vertebrateprey, do not shift diet as they enter the breeding sea-son. However, many species that routinely consumecalcium-poor foods (e.g. granivores, insectivores,frugivores), and especially small passerines that areincapable of carrying substantial reserves of calcium,change their foraging strategies to consume calcium-rich foods during egg production and chick-rearing.

The calcium-rich supplements consumed by birdswhen breeding are numerous (see table 1 in Reynolds& Perrins 2004). Therefore, the detection of calciumlimitation in one species is not evidence that othermembers of the avian community are also calcium-limited during reproduction. For example, Graveland

et al

. (1994) found that Great Tits breeding oncalcium-poor soils in Dutch forests exhibited severecalcium-limited reproduction, whereas Pied Fly-catchers occupying the same habitat showed nosigns of calcium deficiency during breeding attempts.Analysis of stomach contents and droppings, andobservations of chick-provisioning by adults, revealedthat tits and flycatchers took different calcium-richmaterials during their breeding seasons (Graveland1995). Great Tits responded to a scarcity of snailshells, their principal source of dietary calcium, bytaking anthropogenic materials such as DomesticChicken eggshell and grit. By contrast, Pied Fly-catchers consumed many more millipedes

Diplopoda

spp. and woodlice

Isopoda

spp. and far fewer snailshell fragments. Woodlice and millipedes contain sig-nificantly more calcium than do other forest arthro-pods (see table 10 in Graveland & van Gijzen 1994).Furthermore, Great Tits and Pied Flycatchers exhibitdifferent responses to calcium supplementation.Calcium supplements (fragments of snail shell andchicken eggshell) were more scarce in the stomachsof egg-laying female flycatchers, in the droppings ofnestlings and in nestbox contents than they were intits. They were also taken less frequently from feedersattached to nestboxes and were fed less frequentlyby parents to nestlings (Graveland 1995).

Differences between the life histories of the twospecies might explain the different responses to cal-cium deficiency and therefore to calcium supple-mentation. Mänd and Tilgar (2003) suggest that, inresponse to low calcium availability in a given sea-son, it may be advantageous for Great Tits to restrainreproductive effort and thereby reduce breedingsuccess, whereas Pied Flycatchers may benefit frominvesting more heavily despite reproduction beingmore costly than in years when calcium-rich foodsare more abundant.

Multiple breeding attempts

We recommend that breeding attempts other thanjust the first are monitored in multi-brooding spe-cies. Although they studied second broods in onlyone year, Tilgar

et al

. (2002) found that calcium-supplemented Great Tit pairs produced significantlylarger clutches and fledged more young from secondbroods than did unsupplemented pairs. They con-cluded that calcium limitation of Great Tits breedingin Estonian deciduous and coniferous forests is not atransient phenomenon, resulting from the source ofdietary calcium being ephemeral, but instead that itpersists from early spring through to mid-summer.This is supported by studies in Wytham Woods, nearOxford in the UK, which have found that snailabundance declined significantly towards mid-summer(e.g. Phillipson & Abel 1983).

Reproductive biology of individuals

We recommend that researchers carefully considerthe variation in reproductive biology of individualswithin and between study populations. Differencesbetween individuals might explain why calcium sup-plementation has sometimes been ineffective whenresults are considered at the population level. For


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example, Sandberg and Moore (1996) suggestedthat migrant American Redstarts

Setophaga ruticilla

that arrived on the breeding grounds with greater fatloads experienced greater reproductive benefits,both direct and indirect, than those with smaller fatloads. They further suggested that fat buffered thetime budgets of individuals, potentially allowingthem more time to forage for specific nutrients (e.g.calcium) whose deficiency could limit reproduction.The findings of Sandberg and Moore (1996) high-light a poorly considered manifestation of calciumsupplementation under conditions at which dietarycalcium availability does not appear to be limiting.Any savings in time or energy that a bird can makein calcium-specific foraging, which occupies a non-trivial amount of time (e.g. Turner 1982), can beinvested in other behaviours (e.g. O’Halloran

et al

.1990) and foraging for foods that are importantsources of other nutrients (e.g. amino acids, seeRamsay & Houston 2003). In years when such foodsare limiting, calcium supplementation will have adramatic effect on the breeding performance of birds,despite natural calcium availability seemingly remain-ing stable between years.

Appropriate supplements

As Graveland (1995) acknowledges, we have limitedknowledge of the specific calcium sources favouredby breeding birds. We urge researchers to survey thestudy area thoroughly to determine the variety ofcalcareous materials available to birds. This is particu

-

larly important in species that range widely duringthe breeding season to meet the nutritional needs ofegg-laying and chick-rearing (e.g. hirundines, Turner1982).

Once local calcium availability has been deter-mined, breeding birds can be studied to learn whichcalcium-rich foods are favoured during egg produc-tion and chick-rearing. Birds use olfactory and visualstimuli to forage for calcium-rich material (Hughes& Wood-Gush 1971) and, consequently, birds shouldbe provided with supplements that occur naturallyon their breeding territories. For example, Graveland

et al

. (1994) provided Great Tits with fragments ofsnail shell and eggshells of Domestic Chickens, cal-careous foods that were available in the study areaand were used by resident birds. Supplements wereprovided in open cups attached to the outside ofnestboxes and cups were checked three times a weekto confirm that supplements were being used. Thisapproach allows identification of food items preferred

by breeding birds, by examining the relative losses ofknown quantities of the candidate supplementarymaterials. As a last resort if feeding trials fail, vacatednests can be visited at the end of the breeding seasonwhen a search of the nest contents may revealundigested calcareous food items.

Most supplementation studies (see Table 2) haveinvolved species that breed in nestboxes and there-fore the methods of Graveland

et al. (1994) havebeen adopted (see above). However, Ramsay andHouston (1999) also supplemented Blue Tits byhanging cuttlefish bone close to nestboxes, an approachthat has also been used successfully to supplementRed-cockaded Woodpeckers Picoides borealis(R. Bowman pers. comm.). Somewhat surprisingly,Dhondt and Hochachka (2001) found that acrossNorth America, 31 species used calcium supplementsprovided on the ground and/or on feeder platforms.This group included corvids, species that will readilyexploit novel food sources (e.g. Florida Scrub-JayAphelocoma coerulescens – Reynolds et al. 2003), butDhondt and Hochachka (2001) reported that evenarboreal birds, such as parids and woodpeckers, for-aged on the ground for calcium supplements.

So far our discussions have focused on the diet offemale birds prior to and during egg-laying. It is moreproblematic to determine supplement use duringthe nestling period. Although altricial species feedchicks in nests, and supplements can be adminis-tered in the same way during both the laying and thechick-rearing periods, there is no guarantee thatsupplements taken by parents during the latter arealways fed to chicks. Rarely is it possible to observeparents feeding their chicks and, even then, it is dif-ficult to identify individual food items with any con-fidence. However, there are alternatives (see reviewby Rosenberg & Cooper 1990). Faecal analysis andneck ligatures have been used successfully in the pastto study nestling diet (e.g. Bures & Weidinger 2000,Moreby & Stoate 2000). Furthermore, regurgitationof recently ingested food items can be induced byadministering emetic drugs (e.g. Johnson et al. 2002)or by oesophageal massage (R. Bowman pers. comm.).It is advisable to study the composition of nestlingdiet by using one of these techniques if the calciumsupplementation of chicks is to be effective (see below).

A good approach for studying the use of differentcalcium supplements by breeding birds in bothegg-laying and nestling periods was employed byBures and Weidinger (2003) for Collared Ficedulaalbicollis and Pied Flycatchers. They found that thediet of free-living birds was significantly richer in

610 S. J. Reynolds, R. Mänd & V. Tilgar

© 2004 British Ornithologists’ Union, Ibis, 146, 601–614

woodlice and millipedes than it was in snails. Theyalso found that birds in aviaries bred poorly whenprovided with snail shell and eggshell but breedingperformance was dramatically improved (two- tothree-fold) when woodlice were also provided.

Timing of supplementation

Some species (e.g. Red Knot Calidris canutus,Piersma et al. 1996; early breeding Ruddy Duck,Alisauskas & Ankney 1994) deplete endogenousreserves of calcium for reproduction and thereforecalcium supplementation might prove totally inef-fective as a technique to investigate calcium logis-tics for these so-called capital breeders (Drent &Daan 1980). However, in many species, the timing ofcalcium-specific foraging coincides so precisely withthe onset of egg-laying that it is highly likely that theingestion of such calciferous foods provides much ofthe calcium required for egg production (Reynolds1997). Indeed, Graveland and Berends (1997) removedsnail-shell fragments and then reintroduced them tocaptive Great Tits and found that curtailment andresumption of egg-laying, respectively, were highlysensitive to dietary calcium availability. Removal ofsnail shell after the first egg was laid resulted in egg-shell defects or interruptions in laying after 1–3 days,and many females resumed laying normal-shelledeggs within a day of snail shell being reinstated.

Although extensive information is available on thedietary intake of calcium during reproduction bypoultry species (e.g. see review by Etches 1987),such information is much more limited for wildbirds. However, estimates of calcium intake have beenobtained for wild birds breeding in captivity wheredietary intake of food can be closely monitored. Forexample, Graveland and Berends (1997) found thatcaptive Great Tits consumed a constant 4 mg ofcalcium per day in a 2-week period preceding clutchinitiation, but they increased their daily dietaryintake of calcium dramatically to 65 mg when thefirst egg was laid. Calcium intake was then main-tained until the clutch was complete.

Regardless of whether researchers investigatemacro- or micronutrient limitation using food sup-plementation to manipulate local food availability,food supplements must be provided to birds at anappropriate stage of the annual cycle. In one of themost effective food-supplementation studies to date,Reynolds et al. (2003) advanced laying and increasedclutch and egg size by providing Florida Scrub-Jayswith food supplements 2 months prior to clutch

initiation for two consecutive years. Although Reynoldset al. (2003) used supplements rich in fats andproteins (i.e. macronutrients), the timing of calciumsupplementation might be just as important ininfluencing reproductive parameters. Although largelyuntested, where calcium is the nutrient limitingbreeding performance, we might expect that cal-cium supplementation of birds early in their breed-ing seasons would influence the size of individual eggsas well as perhaps clutch size (Tilgar et al. 2002).

The comments above apply to timing of calciumsupplementation in relation to the onset of egg-laying,but we encourage researchers also to consider whetherdietary calcium limits the reproductive success ofbirds through the growth and survival of their chicks.The calcium requirements of the chick increasedramatically during the first 2 weeks after hatching.Precocial young can feed themselves almost as soonas they hatch. MacLean (1974) found bones andteeth of Brown Lemmings Lemmus trimucronatus inthe stomachs of juvenile Dunlins Calidris alpina andPectoral Sandpipers C. melanotos in July, when mostgrowth occurs. In altricial species, adults delivercalcium-rich food to chicks before they fledge. Bilbyand Widdowson (1971) found that between hatch-ing and 12 days of age, Common Blackbird Turdusmerula chicks increased in body mass by 14 times andin total somatic calcium content by 100 times. They alsofound that the gut contents of Common Blackbirdand Song Thrush T. philomelos nestlings sometimescontained half of all the calcium in their entire bodies.

Once calcium-rich food sources for chicks havebeen determined (see above, Bures & Weidinger2000) for a species in which calcium-limited skele-tal development in chicks is suspected, researchersintending to feed chicks directly should initiallydetermine the time of maximal skeletal developmentfor their study species. Skeletal development is relat-ively predictable and fixed across the altricial–precocial spectrum in birds (see Starck 1998) and, atthe very least, calcium supplements should be pro-vided when daily calcium intake rates of chicks aremaximal. Indirect supplementation of chicks shouldbe effected by providing ad libitum calcium to parentsthroughout the nestling period when adults deter-mine the calcium intake rates of chicks through theirprovisioning behaviour.

Underlying geology

Cases of calcium-limited reproduction reportedin the ornithological literature in the last 15 years


Calcium supplementation of breeding birds 611

(Table 1) have almost exclusively applied to birdsbreeding in acidified habitats, due to the dramaticreduction of exogenous calcium under such circum-

stances (Graveland 1998). Graveland and Drent(1997) recognized that calcium-limited reproduc-tion of birds may not be the exclusive domain of suchareas, but might also occur in non-acidified, naturallycalcium-poor areas of the world (e.g. large areas ofnorthern Europe (Fennoscandian block) and easternNorth America (the Canadian Shield)).

To date, only a few studies have been conductedin naturally calcium-poor areas where acidic rocksand soils support few calcium-rich food items, buttheir findings should stimulate further work in thisarea. The default assumption for such areas hastypically been that breeding birds have had sufficienttime to produce an adaptive reproductive responseto the prevailing low calcium availabilities (Graveland& Drent 1997). However, the most compellingevidence to refute this has emerged from Estonia, acountry predominantly covered with pine forests onnaturally acidic (base-poor) soils supporting relat-ively few snails and other calcium-rich foods forbreeding birds (Mänd et al. 2000a). Calcium supple-mentation in Estonia’s northern temperate forestsadvanced laying (Mänd et al. 2000a, 2000b), andincreased the clutch size, fledging success and fledg-ling tarsus length (Tilgar et al. 2002) of Great Tits,and increased the egg volume, eggshell thickness(Tilgar et al. 1999a, 1999b) and fledgling tarsuslength (Mänd & Tilgar 2003) of Pied Flycatchers.Although this study area is not adversely affectedby industrial acidification, there was no differencebetween its snail abundance and that of the forestsin acidified areas of The Netherlands (Mänd et al.2000a).

Ormerod and Rundle (1998) warned againstmaking assumptions about calcium availabilitybased simply upon the pH of the substrate. Theyfound that the calcium content of invertebrateprey did not differ significantly between artificiallyacidified, limed sites and control sites. Collectively,these findings demonstrate that considerations ofnatural calcium availability, even in study areas whereit has been stable for many decades, are paramountat the planning stage of calcium-supplementationwork.

Agents causing calcium loss

Many of the agents causing calcium loss (e.g. pollu-tion, agricultural intensification) have been discussed

comprehensively elsewhere and we refer the readerto Graveland (1998) and Pain and Donald (2002)for further detailed information. Increasing theavailability of exogenous calcium through the pro-vision of supplementary calcium-rich material willonly improve the breeding performance of birds ifdietary calcium shortage is the primary cause ofreproductive limitation. Therefore, initial planningof calcium supplementation once calcium-limitedreproduction has been detected must always involvethe determination of the factor(s) limiting calciumavailability.

The most straightforward cause of calcium-limited reproduction is a shortage of dietary calciumthat directly limits calcium supply to the egg-layingfemale or chick-provisioning parents. This is exem-plified by the constraints on the reproductive outputof forest passerines in Estonia (see above) in whichthere are minimal anthropogenic environmentalinputs that act directly and indirectly to bring aboutprimary and secondary calcium limitation, respect-ively. However, most documented cases of calcium-limited reproduction (Table 1) concern birds breedingin acidified aquatic and terrestrial habitats. Althoughacidification, and its resulting increase in the biolog-ical activity of toxic cations (e.g. aluminium, lead),causes a direct decline in calcium availability to thebreeding female (e.g. Hames et al. 2002), it also low-ers calcium uptake across the gut wall. Metal cationsoccupy sites on transport proteins in the avian gutthat are normally occupied by calcium, and therebyenter the bloodstream (Six & Goyer 1970). Toxicityof ingested metal cations is minimal when calciumintake is high, but is severe when calcium intake islow (Scheuhammer 1991). Graveland (1998) arguedthat it is sometimes very difficult to attribute thepoor breeding performance of birds on acidifiedcalcium-poor habitats definitively to either calciumdeficiency or metal toxicity.

The other agent that is a major cause of secondarycalcium limitation is DDT. Despite its use beingrestricted in the UK in 1964 and in the USA in 1972,DDT is still used extensively throughout southeastAsia and Central America. Its adverse effects on birdpopulations of North America are still detectable,and birds at higher trophic levels in sub-SaharanAfrica, where DDT use persisted until a few yearsago, still experience marked reductions in repro-

ductive success compared with pre-DDT records (e.g.Hartley et al. 1995). The effects and persistence ofDDT in relation to avian breeding performance arediscussed in Reynolds and Perrins (2004).



APPLICATIONS OF FINDINGS FROM

CALCIUM-SUPPLEMENTATION

STUDIES

Although the review of Graveland (1998) addressedacidification and its effects on avian reproduction, hisrecommendations are applicable in a wider ornitho-logical context. He recognized that the findingsof many field studies were only correlative in natureand that future experimental work (e.g. calcium sup-plementation) would be relatively more informative.

Of course, calcium supplementation is not the onlyway to investigate calcium-limited reproduction inbirds. Graveland and van der Wal (1996) employeda 4-year liming programme to demonstrate thatdeclines in snail abundance in Dutch forests hadbeen caused by a loss of soil calcium as a result ofanthropogenic acidification. Declines in snail abund-

ance had resulted in increases in eggshell defects offorest passerines. Clearly, however, improvements incalcium availability occur only after many years ofliming compared with a few weeks in the case of cal-cium supplementation. Although liming results inwholesale increases in the availability of calcium atmany trophic levels, temporal costs of the procedureare not commensurate with its employment asan exploratory tool to detect calcium limitation.Instead, if used intelligently in directed, plannedstudies, calcium supplementation could enable us toidentify cases of calcium-limited reproduction rela-tively rapidly. Furthermore, by varying the timing ofsupplementation and/or the type of supplementspresented, it should be possible to identify at whatreproductive stage(s) calcium limitation is most acute.Supplement use should also indicate the nutritionalrequirements for breeding of some species for whichthe reproductive biology is little understood.

It is hoped that findings from calcium-supplemen-tation studies will facilitate improvement of breed-ing conditions for those species that are currentlyexhibiting calcium-limited reproduction. Detectingcalcium limitation is the starting point for such anaim, and this will only be achieved through concertedand coordinated monitoring of the breeding successof birds over many years. As Hames et al. (2002)acknowledge, however, a more complete understandingof the processes that give rise to the observed pat-terns of decline (e.g. reductions in calcium availabil-ity) will only be achieved through massive researcheffort. It was with such an approach that Hameset al. (2002) combined long-term data on breedingattempts by birds (Birds in Forested Landscapes

Project and the Breeding Bird Survey) and on acidi-fication (National Atmospheric Deposition Projectand the Natural Resources Conservation Service) toshow that there was a highly significant negativeeffect of acid rain on the likelihood of breeding forthe Wood Thrush Hylocichla mustelina across NorthAmerica. Currently, the size of the task ahead of usis inestimable, but so too are the rewards.

We thank Andy Radford and three anonymous referees fornumerous valuable comments on the manuscript. Contin-ued financial support for S.J.R. has been provided by theNatural Environment Research Council, the NationalScience Foundation, the University of Memphis and theUniversity of Birmingham. Continued financial support forR.M and V.T. has been provided by the Estonian ScienceFoundation.

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Received 10 September 2003; revision accepted 15 March 2004First published online on 25 June 2004; doi: 10.1111/j.1474-919x.2004.00298.x

Calcium supplementation of breeding birds: directions for future research

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