Confusions of Mass and Size
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COMMENTARIES Confusions of Mass and Size THEUNIS PIERSMA• AND NICK C. DAVIDSON 2 Work by Rising and Somers(1989) and Freeman combines information about structural size and nu- and Jackson(1990) has recently emphasized that mul- trient reserve massbut alone cannot provide an in- tiple, and preferably skeletal,measurements provide dicator of structural size. It is the ease with which a more accurateassessment of body sizein birds than body masscan be measured(and not the difficulty; do single, external measurements.We agree. It is re- contra Freeman and Jackson 1990) that has made it a grettable,however, that both papersperpetrate a con- muchused and interestingmeasure. Inclusion of body fusion between two useful and quite distinct vari- mass in structural size-related analysesmay not al- ables:body size and bodymass. In doing so they have ways distort interpretationof the data (e.g. seeCooke ignored several highly relevant published studies, et al. 1990),but it is usually impossibleto determine notably of nonpasserineand Europeanspedes (the this from ambiguousresults. latter bias apparently part of a more general trend By definition structuralsize is independentof the identified by Enckell 1988). nutritional status that varies with time of day and Rising and Somers(1989) and Freemanand Jackson year, reproductivestatus, and habitatquality. For this (1990) are but two recent examplesof a widespread reasonstructural size is the preferred variable in stud- misunderstanding.Smith et al. (1990) provide a fur- ies of geographicalsize variation and perhapsin be- ther instance.Another is the inclusionby Davieset havioral studies of contests. Note, however, that it al. (1988)of massin an analysisof body sizeof Lesser may not be structuralsize per se but rather muscular Snow Geese(Chen c. caerulescens),which was criticized power (possiblyreflected in the protein reservemass) recentlyby Alisauskasand Ankney (1990),although that determines contest outcomes. Whereas studies of in this casethe overall interpretationof a size-related geographicalsize variation regard all this nutritional variation in fecundityof LesserSnow Geesemay not noise as a problem to be removed, studiesof ener- have been affected (Cooke et al. 1990). Even Peters getics and nutrient reserve status require precisely (1984), in his extensive discussionof the ecological this information on reserve mass. For such studies implicationsof body size,provides no cleardefinition body masscan be a useful variable if massvariations of body size and in many instancesdiscusses body due to differences in structural size can be controlled size-relatedphenomena through body mass. (e.g. Davidson1983, Ankney and Afton 1988,Piersma Although not stated explicitly, both Rising and 1988, Piersma and van Brederode 1990). Somers (1989) and Freeman and Jackson(1990) ad- Althoughbody massis readily measured,structural dressedproblems of measuringstructural size. The Ox- size is more difficult, and there have been surpris- ford dictionarydefines structural as "of the (essential) ingly few attemptsto devise practicalmeans of mea- framework" and structuralsize accordinglyas "the suring structural size in birds. One approach is to size of the essential framework" (Piersma 1984). Be- definestructural size as the body massof starvedbirds causeindividual birds have a remarkablecapacity to (i.e. birds that have died after exhaustingall their vary their massand volume dependingon their nu- nutrient reserves[Piersma 1984, 1988; see King and tritional status,we feel it is biologicallymost mean- Ml•rphy 1985 for the distinctionbetween nutrient ingful to define structural size as the "nutrient re- reservesand nutrient stores])and then seewhich body serve-independentsize of a bird." dimensionsstatistically "explain" starvedbody mass Our point is simple.There is an importantbut wide- most accurately.There are, however, pitfalls even in ly ignored distinction that must be made between this approach.Although birds die in natural starva- two concepts:(1) the reserve-independentstructural tion eventsafter substantiallydepleting their fat and sizeand (2) the variableamounts of nutrients(chiefly protein reserves,there is evidence that the precise fat and protein) that permit birds to exerciseand to nutritional state at death is influenced by the envi- survive periodsof negativeenergy and nutrient bal- ronmentalconditions during starvation.This canlead ance, the variable nutrientreserve mass. Body mass to both the fat mass and the nonfat mass of starved birds still including some nutritional reserves,al- though absolute amounts are small (Davidson and ' NetherlandsInstitute for SeaResearch (NIOZ), Evans 1982, Davidson and Clark 1985). P.O. Box 59, 1790 AB Den Burg, Texel, Netherlands, Skeletal measurements of the sternum have been and ZoologicalLaboratory, University of Groningen, used to index pectoralmuscle size (Evansand Smith P.O. Box 14, 9750 AA Haren, Netherlands. 1975, Piersma et al. 1984), but these linear measure- 2Chief ScientistDirectorate, Nature Conservancy ments cover only part of the overall skeletal size. As Council,Northminster House, Peterborough PE1 1UA, suggestedby Wishart (1979), (dry and fat-free) skel- United Kingdom. etal massis almostentirely reserve-independent,ex- 441 The Auk 108: 441-444. April 1991 442 Commentaries [Auk, Vol. 108 cept for small variations in bone marrow mass(see reserves, clutch size, and incubation. Condor 90: Moser and Rusch 1988), and should provide an ac- 459-472. curate estimator of structural size on which linear ALISAUSKAS,R. T., & C. D. ANKNEY. 1990. Body size dimensionscan be regressedto provide an index of and fecundity in LesserSnow Geese.Auk 107: structural size. Moser and Rusch (1988) concluded 440-443. that skeletal volumeß measured by water displace- COOKE,F., J. C. DAvIEs, & R. F. ROCKWELL.1990. Re- ment of excisedbonesß provides an even more precise sponseto Alisauskasand Ankney. Auk 107:444- measureof structuralsize. Finally, the first principal 446. component of a set of linear skeletal measurements DAVIDSON,N.C. 1983. Formulae for estimatingthe likewise provides an appropriate structural size mea- lean weight and fat reservesof live shorebirds. sure (Ankney and Afton 1988, Rising and Somers Ring. & Migr. 4: 159-166. 1989). ß, & N. A. CLARI<. 1985. The effects of severe Most skeletalmeasurements require the sacrificeof weather in Januaryand February 1985on waders birds and are of little help in studies of live birds. in Britain. Wader Study Group Bull. 44: 10-16. Consequently,body-size variation in live birdsis usu- ß& P. R. EVANS.1982. Mortality of Redshanks ally controlledin analysesof body massby the use and Oystercatchersfrom starvationduring severe of one or more easily measured external measure- weather. Bird Study 29: 183-188. ments, typically the lengths of wingß tarsus,body, DAvms,J. C., R. F. ROCk'W•L,& F. COOKE.1988. Body- and bill. Choice of the appropriateexternal dimen- size variation and fitness componentsin Lesser sions to indicate structural size can be made with Snow Geese (Chen caerulescenscaerulescens). Auk appropriatemodels of regressionon starvedor skel- 105: 639-648. etal mass or volume, as outlined aboveß and their ENCKELL,P. H. 1988. Ecology: the (inter)national derivation may hold some surprises.For exampleß science. Br. Ecol. Soc. Bull. 19: 224-228. Moser and Rusch(1988) found that some commonly EvANs, P. R., & P. C. SMITH. 1975. Studies of shore- usedexternal measures were only moderatecorrelates birds at Lindisfarne, Northumberland. 2. Fat and of structural size (measuredby skeletal volume) in pectoral muscleas indicators of body condition Canada Geese (Branta canadensis).Further, the most in the Bar-tailed Godwit. Wildfowl 26: 64-76. appropriateexternal measures may differ interspecif- FromMAN,S., & W. M. JACr,SON. 1990. Univariate met- ically, even between closely related species(e.g. in ricsare not adequateto measureavian body size. Podicepsgrebesß Piersma 1988). Auk 107: 69-74. Future studies must differentiate clearly between KING, J. R., & M. E. MURPHY. 1985. Periods of nu- structural-size and nutritional-mass variation, and tritional stress in the annual cycles of endo- should avoid using body massin exercisesaimed at therms: fact or fiction? Am. Zool. 25: 955-964. describingstructural size. Failure to distinguishbe- MOSER,T. J., & D. H. Ruscrt. 1988. Indices of struc- tween the two can lead to ambiguousand misleading tural size and condition of Canada Geese. J. Wildl. interpretations.For example,the regional differences Manage. 52: 202-208. in flight-surfaceloading of Accipiterhawks described Pgrm•s,R.H. 1984. The ecologicalimplications of by Smith et al. (1990) may be purely structuraland body size. Cambridge,Cambridge Univ. Press. adaptively related to differencesin the relative use PIERSMA,T. 1984. Estimatingenergy reserves of Great of thermal updrafts, as the authors suggestßor they Crested GrebesPodiceps cristatus on the basis of may be a consequenceof differencesin fat-reserve body dimensions.Ardea 72: 119-126. massin relation to the length of the ensuingnonstop 1988. Body size, nutrient reservesand diet flight (seee.g. Smith et al. 1986). of Red-neckedand SlavonianGrebes Podiceps gri- Although easyto define in general, structuralsize segenaand P. aurituson Lake IJsselmeer,The defiesa uniform approximationin termsof a standard Netherlands. Bird Study 35: 13-24. set of external measurementsand should preferably ß N. C. DAVIDSON, & P. R. EvANs. 1984. Esti- be derived for eachspecies under study.Clearly, there