BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, researchlibraries, and research funders in the common goal of maximizing access to critical research.

HEMATOLOGY, PLASMA CHEMISTRY, SEROLOGY, ANDCHLAMYDOPHILA STATUS OF THE WAVED ALBATROSS (PHOEBASTRIAIRRORATA) ON THE GALAPAGOS ISLANDSAuthor(s): Luis R. PadillaD.V.M., Kathryn P. HuyvaertM.S., Jane MerkelL.V.T., R. Eric MillerD.V.M.,Dipl. A.C.Z.M., and Patricia G. ParkerPh.D.Source: Journal of Zoo and Wildlife Medicine, 34(3):278-283. 2003.Published By: American Association of Zoo VeterinariansDOI: http://dx.doi.org/10.1638/02-076URL: http://www.bioone.org/doi/full/10.1638/02-076

BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the biological, ecological, andenvironmental sciences. BioOne provides a sustainable online platform for over 170 journals and books publishedby nonprofit societies, associations, museums, institutions, and presses.

Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance ofBioOne’s Terms of Use, available at www.bioone.org/page/terms_of_use.

Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiriesor rights and permissions requests should be directed to the individual publisher as copyright holder.

278

Journal of Zoo and Wildlife Medicine 34(3): 278–283, 2003Copyright 2003 by American Association of Zoo Veterinarians

HEMATOLOGY, PLASMA CHEMISTRY, SEROLOGY, ANDCHLAMYDOPHILA STATUS OF THE WAVED ALBATROSS(PHOEBASTRIA IRRORATA) ON THE GALAPAGOS ISLANDS

Luis R. Padilla, D.V.M., Kathryn P. Huyvaert, M.S., Jane Merkel, L.V.T., R. Eric Miller, D.V.M.,Dipl. A.C.Z.M., and Patricia G. Parker, Ph.D.

Abstract: Venipuncture was performed on 50 adult, free-ranging waved albatrosses (Phoebastria irrorata) on Es-panola, Galapagos Islands, Ecuador, to establish hematologic and plasma biochemistry reference ranges and to deter-mine the prevalence of exposure to important domestic avian pathogens. Weights and plasma creatine phosphokinaseactivities differed significantly between males and females. Serum was tested for evidence of exposure to avian influ-enza, avian paramyxoviruses 1, 2, and 3, avian cholera, adenovirus groups 1 and 2, avian encephalomyelitis, Marek’sdisease, infectious bursal disease, and infectious bronchitis virus (Connecticut and Massachusetts strains). Of 44 birds,29 (66%) seroreacted to adenovirus group 1, and four seroreacted to avian encephalomyelitis. Cloacal swabs werenegative for Chlamydophila psittaci DNA.

Key words: Waved albatross, Phoebastria irrorata, hematology, plasma chemistry, serology, Chlamydophila psittaci.

INTRODUCTION

The colonial waved albatross (Phoebastria irror-ata), a member of the Procellariformes, breeds inonly two places: on the islands of Espanola in theGalapagos Islands of Ecuador1,9 and in La Platanear the west coast of Ecuador. Less than 20 breed-ing pairs have been reported on La Plata,1 and re-cent surveys suggest that the size of the Espanolapopulation, which contains 15,000–17,000 pairs,1

has been stable for 25 yr. Using criteria set by theInternational Union for Conservation of Nature andNatural Resources, the waved albatross could beconsidered ‘‘vulnerable’’ on the basis of its re-stricted breeding range.3 As with other seabird spe-cies,20, 21 colonial breeding habits and limited geo-graphic distribution could make this species sus-ceptible to epizootics and to natural or anthropo-genic environmental disasters. The long distancestraveled by waved albatrosses to unique foraginggrounds along the South American coast may ex-pose them to environmental factors and infectiousdiseases not encountered by birds that never leavethe archipelago. The natural history, ecology, con-servation, and management of this species,1,9 butnot its health status, have been described.

Baseline health parameters serve as referencepoints for future population assessments and are es-

From the Saint Louis Zoological Park, 1 GovernmentDrive, St. Louis, Missouri 63110, USA (Padilla, Merkel,Miller, Parker); College of Veterinary Medicine, Univer-sity of Missouri–Columbia, 203 Veterinary MedicineBuilding, Columbia, Missouri 65211, USA (Padilla, Mill-er); and Department of Biology, University of Missouri–Saint Louis, 8001 Natural Bridge Road, St. Louis, Mis-souri 63121, USA (Huyvaert, Parker). Correspondenceshould be directed to Dr. Padilla.

sential for determining population health.10,18 Thisstudy sought baseline hematologic and plasmachemical data for the waved albatross and data onthe prevalence of exposure to important domesticavian pathogens so that epizootics and other health-related threats to the population could be recog-nized and managed. Captive procellarids are un-common, so reference ranges were established fromwild populations.

MATERIALS AND METHODS

Fifty adult, clinically healthy waved albatrosses(22 males, 28 females) were physically restrainedduring July, 2001, on Punta Cevallos, Island of Es-panola, Galapagos Islands, Ecuador (18S, 988W),for ulnar vein venipuncture, cloacal swab collec-tion, and weight determination. Techniques hadbeen approved by the University of Missouri–SaintLouis Institutional Animal Care and Use Commit-tee. Sex was determined by morphology and be-havior and confirmed by a polymerase chain reac-tion (PCR) molecular technique.4

Whole-blood samples (1–8 ml) were collectedfrom 50 birds. Blood smears were made from 45samples using fresh, unpreserved blood. Thesewere fixed and stained with a modified Wright–Gi-emsa stain (JorVet Dip-Quick, Jorgensen Labora-tories, Loveland, Colorado 80538, USA) for he-moparasite examination. Blood was placed in lith-ium heparin tubes or serum collection tubes withseparator gel and clot activator (Vacutainer System,Becton-Dickinson, Franklin Lakes, New Jersey07417, USA). Serum and plasma were harvestedafter in-field centrifugation for 20–30 min using abattery-powered centrifuge unit (Mobilespin Model128, Vulcon Technologies, Grandview, Missouri

279PADILLA ET AL.—WAVED ALBATROSS REFERENCE VALUES

Table 1. Weight and estimated hematology parameters for free-ranging adult waved albatrosses.

Parameter Mean Range N

Weight (kg)Packed cell volume (L/L [%])Estimated leukocyte count (3 109/L)Heterophils (%)Monocytes (%)Lymphocytes (%)Eosinophils (%)Basophils (%)

3.7 6 0.60.4 6 0.05 (38.2 6 5.1)5.9 6 2.4

66.1 6 301.7 6 1.7

30.5 6 151.7 6 1.70.0 6 0.01

2.8–5.00.24–0.50 (24–50)1.5–11.11.1–8.90–0.50.27–3.90–0.40–0.2

4728454545454545

64030, USA) at 3,000 rpm. After separation, plas-ma and serum were transferred to cryotubes (NalgeNunc International, Rochester, New York 14625,USA) and frozen at #2208C. All samples were fro-zen in liquid nitrogen for preservation and transportuntil laboratory analysis. Fresh blood samples from28 of the birds (12 males, 16 females) were placedin heparinized microcapillary tubes, and packedcell volumes (PCVs) were measured in the fieldafter centrifugation. Fixed blood smears and plasmawere submitted to a commercial veterinary labora-tory (Antech Diagnostics, Chicago, Alsip, Illinois60903, USA) for estimated total and differentialwhite blood cell (WBC) counts, detection of he-moparasites, and automated plasma chemistry pro-files. The estimated WBC count is the standard pro-tocol for this commercial laboratory.6,11

Cloacal swab samples were transferred to cry-otubes, frozen in liquid nitrogen, and submitted fordetection of Chlamydophila psittaci DNA sequenc-es by PCR to the Infectious Diseases Laboratory,College of Veterinary Medicine, University ofGeorgia, Athens, Georgia 30602, USA.

Serum samples from 44 birds (20 males, 24 fe-males) were tested for antibodies to adenovirusgroup 1, avian encephalomyelitis virus, Marek’sdisease, and infectious bursal disease by agar gelimmunodiffusion (AGID); for antibodies to infec-tious bronchitis virus (Connecticut and Massachu-setts strains) and avian paramyxovirus 2 and 3 byhemagglutination inhibition; and for antibodies toreovirus by immunofluorescence at the NationalVeterinary Services Laboratory, Ames, Iowa50010, USA. Samples were also tested for antibod-ies to adenovirus group 2 (hemorrhagic enteritis ofturkeys) and avian influenza by AGID and for avianparamyxovirus 1 (Newcastle’s disease) and aviancholera by microagglutination at the DiagnosticLaboratory of the University of Missouri–Colum-bia, College of Veterinary Medicine, Columbia,Missouri 65211, USA. Insufficient serum volumesprecluded serologic testing of the other six birds.

Plasma samples with gross evidence of hemoly-sis and individual test results that were more than3.0 standard deviations from the mean were ex-cluded from analysis. Although ideal referenceranges are calculated using 1.96 standard deviationsfrom the mean,8 the limited sample size was takeninto account for establishing these reference ranges.A commercial statistical software package (NCSSt,Number Cruncher Statistical Systems, Kaysville,Utah 84037, USA) was used for data analysis.Mean and standard deviation were calculated forweights, PCV, estimated WBC count, and plasmachemistry values. Results were visually inspectedfor normal distribution, and normality was con-firmed by a Shapiro–Wilk W test for all chemistry,PCV, weight, and estimated total WBC count val-ues. To explore potential sex-related biases, the dataset was further subdivided by sex, and a two-sam-ple t-test was used to identify differences betweenmales and females. Similarly, plasma chemistriesand estimated WBC counts were compared be-tween seroreactive and seronegative birds for all thediseases tested. Because the means of 16 parame-ters were compared for each subset of the data, aBonferroni-corrected P-value #0.003 (0.05/16) wasconsidered significant.14

RESULTS

Weights, leukograms, and plasma chemistry val-ues are shown in Tables 1, 2. No hemoparasiteswere identified in the blood smears examined (n 545). Males weighed significantly more than females(P , 0.003; 4.1 6 0.5 kg, n 5 20 and 3.3 6 0.4kg, n 5 27, respectively). Creatine phosphokinase(CPK) activity was significantly lower (P , 0.003)in males (196.4 6109.4 U/L, n 5 19) than in fe-males (370.9 6 178.9 U/L, n 5 22). After Bonfer-roni correction, mean values of aspartate amino-transferase (AST) for females and males (133.6 647.1 U/L, n 5 25 and 99.4 6 40.3 U/L, n 5 22,respectively) and of cholesterol for females andmales (7.0 6 1.3 mmol/L, n 5 26 and 6.0 6 1.3

280 JOURNAL OF ZOO AND WILDLIFE MEDICINE

Table 2. Plasma chemistry parameters for free-ranging adult waved albatrosses.

Parameter Mean Range N

Total protein (g/L [g/dL])Albumin (g/L [g/dL])Globulin (g/L [g/dL])P (mmol/L [mg/dL])Ca (mmol/L [mg/dL])Glucose (mmol/L [mg/dL])Na (mmol/L [mEq/L])

45.0 6 6.0 (4.5 6 0.6)18.0 6 2.0 (1.8 6 0.2)28.0 6 5.0 (2.8 6 0.5)

1.1 6 0.3 (3.4 6 0.8)2.5 6 0.3 (9.8 6 1.1)

12.7 6 2.0 (229.4 6 35.4)152.7 6 6.2 (152.7 6 6.2)

35–57 (3.5–5.7)15–22 (1.5–2.2)19.0–38.0 (1.9–3.8)

0.6–1.9 (1.8–6.0)1.3–3.1 (5.1–12.3)9.8–19.2 (176–346)

134–166 (134–166)

48484748484745

K (mmol/L [mEq/L])Cl (mmol/L [mEq/L])Uric acid (mmol/L [mg/dL])Cholesterol (mmol/L [mg/dL])Aspartate aminotransferase (U/L)Creatine phosphokinase (U/L)

3.7 6 0.8 (3.7 6 0.8)118.0 6 7.7 (118.0 6 7.7)

0.3 6 0.2 (4.4 6 2.7)6.5 6 1.4 (251.8 6 54.0)

117.6 6 46.9290.0 6 173.1

2.0–5.4 (2.0–5.4)105–138 (105–138)

0.1–0.7 (1.4–11.7)3.4–10.4 (133–401)

45–24348–711

484647484741

Table 3. Serologic test results and methodology used for free-ranging adult waved albatrosses in the GalapagosIslands (n 5 44).

Test Seroreactive % seroreactivity Method Positivea

Avian adenovirus 1Avian encephalomyelitisAvian choleraAvian paramyxovirus 1Avian paramyxovirus 2Avian paramyxovirus 3

2940000

6690000

AGIDb

AGIDMAc

HId

HIHI

$1:8$1:8$1:8$1:8

Hemorrhagic enteritisMarek’s diseaseAvian influenzaReovirusInfectious bursal diseaseInfectious bronchitise

000000

000000

AGIDAGIDAGIDIFAAGIDHI

$1:20

$1:8

a Titer considered positive by testing laboratory. Not applicable for AGID methodology.b AGID 5 agar gel immunodiffusion.c MA 5 microagglutination.d HI 5 hemagglutination inhibition.e Connecticut and Massachusetts strains.

mmol/L, n 5 26, respectively) were not signifi-cantly different (P . 0.003).

Serology results and testing techniques are pre-sented in Table 3. Twenty-nine (66%) birds showedseroreactivity to avian adenovirus group 1 byAGID, and four (9%; three females, one male) wereseroreactive to avian encephalomyelitis virus byAGID. No statistically significant differences inplasma chemistry values or estimated total WBCswere found between seropositive and seronegativeindividuals. All 50 cloacal swabs were negative forthe presence of Chlamydophila DNA sequences byPCR.

DISCUSSION

These are the first published hematology andplasma chemistry reference ranges for the waved

albatross. Although leukocyte counts were estimat-ed from fixed blood smears, results of this tech-nique may be more variable than those of hema-cytometer-based techniques when performed underideal conditions.17 However, hemacytometer-basedtechniques are impractical in remote field situa-tions, such as the island of Espanola, where limitedaccess precludes the availability of quality micros-copy equipment and whole-blood preservation. Inthese field situations, where the decline in conditionof cell quality in unpreserved whole blood may cre-ate artifacts, estimated total WBC counts fromfreshly made and fixed blood smears are likely toprovide more reliable results.6 Fixed blood smearsalso provide permanent archival information,6

which can be a useful tool for conservation andpopulation medicine.

281PADILLA ET AL.—WAVED ALBATROSS REFERENCE VALUES

The hematology and chemistry parameters forthe waved albatross (P. irrorata) are generally con-sistent with the values for the Laysan albatross (P.immutabilis),21 with minor exceptions. Althoughdifferent count techniques were used, the Laysanalbatrosses from three different islands21 had highertotal-WBC ranges (9.8–42.55 3 109/L) than thoseestimated for the waved albatross of the Galapagosislands (1.5–11.1 3 109/L). Although this may re-flect species differences, inherent variability in theWBC estimation techniques17 and sampling differ-ences may have influenced the values. Despite dif-ferences in total WBC numbers, similar trends areobserved in heterophil to lymphocyte ratios be-tween the two species. Laysan albatross heterophil–lymphocyte ratios were roughly 1.9, 2.0, and 2.7for the three island populations, and the waved al-batross had a 2.2 ratio. In other species, these ratiosvary widely. Higher heterophil–lymphocyte ratioshave been reported for white storks (Ciconia cicon-ia), white pelicans (Pelecanus erythrorhynchos),and great frigatebirds (Fregata minor).22 The sig-nificance of these variations is unknown. They mayreflect species-specific idiosyncrasies or differentcapture, restraint, and blood collection methodolo-gies, and they highlight the need for species-spe-cific reference ranges and the danger of extrapolat-ing data between species. Plasma glucose valueswere higher for the waved albatross than those re-ported for the Laysan albatross.21 Plasma electro-lytes (Na, Cl, and K) have not been reported forthe Laysan albatross and, therefore, could not becompared, but all other plasma chemistry valueswere comparable between the two species.

The only plasma chemistry value from P. irror-ata that differed significantly between males andfemales was CPK activity. Despite lack of statisti-cal significance, sex differences in cholesterol andAST values may reflect true biological differences.In the absence of clinical signs, differences in theseinherently variable enzymes likely reflect normalreproductive or physiologic processes. The possi-bility of an age-dependent bias in the female pop-ulation cannot be ruled out because exact ages werenot available for the adult individuals sampled. Be-cause elevations in CPK are specific to muscledamage, concurrent elevations in AST are unlikelyto be of hepatocellular origin.7 Variations in plasmacholesterol between captive and recently caughtbrown pelicans have been attributed to dietary dif-ferences,22 and high cholesterol levels have beenassociated with carnivorous birds.5 Sex-dependentdifferences in foraging strategies may explain thedifferences in plasma cholesterol. Alternatively, el-evations in plasma cholesterol have been associated

with active folliculogenesis and other reproductiveprocesses,12 but this is an unlikely explanation forcholesterol elevations in female waved albatrossesbecause all birds were sampled during either lateincubation or early brooding of chicks and after theactive egg-laying season of April to early June.

The absence of hemoparasites in P. irrorata isnotable because hippoboscid flies, which can bevectors of protozoal hemoparasites,2 were observedon some of the birds. Monitoring for the presenceof hemoparasites during different times of the yearhas intrinsic ecologic interest and might influencepopulation management strategies.

Avian serologic responses must be interpretedcautiously because most of these tests have beenvalidated for only domestic chickens. Test meth-odology, sensitivity, and specificity must be takeninto account before making conclusions or gener-alizations about the health of a population. Unlikea study on wild rockhopper penguins (Eudypteschrysocome),10 plasma chemistry values did not dif-fer between seroreactive and seronegative alba-trosses.

Group 1 adenoviruses include 12 serologicallydistinct viruses that generally affect young birds,and although morbidity and mortality vary withhost and virus, clinical signs are associated withhepatitis, enteritis, and respiratory disease.16 Thehigh prevalence (66%) of seroreactivity to group 1,with no seroreactivity to group 2 adenoviruses inour study population, suggests exposure to virusesof the first group, although none showed evidenceof disease. Because the persistence or half-life ofadenovirus 1–specific antibodies in albatrosses hasnot been studied, the relevance of seroreactivity inasymptomatic birds is unknown. Group 1 adeno-viruses can be recovered from asymptomatic do-mestic birds, and antibody surveys suggest thatmost adult birds have been exposed to numerousstrains.16 Furthermore, the implications of highprevalence of seroreactivity are limited by the se-rology methods used. AGID serology tests have theinherent limitations of limited sensitivity and an in-ability to quantify antibody concentrations.15 Be-cause these tests rely on precipitation of unknownantigen with patient serum into antigen–antibodycomplexes, the possibility of cross-reaction withnonspecific proteins cannot be ruled out. Surveil-lance of hatchlings and juveniles for causes of mor-bidity and mortality may elucidate the significanceof adenoviruses in the waved albatross population.

Seroreactivity to avian encephalomyelitis byAGID must also be interpreted with caution, as ra-tionalized for group 1 adenoviruses. No birdsshowed clinical signs consistent with this entero-

282 JOURNAL OF ZOO AND WILDLIFE MEDICINE

virus, and seroreactivity may indicate evidence ofprevious exposure to this or other related viruses.Because undocumented enteroviruses are suspectedto be associated with disease in companion and avi-ary birds,13 it is possible that unidentified entero-viruses are present in the waved albatross popula-tion and cross-react to the serology methods usedin this study.

Without evidence of the clinical signs of Chla-mydophila infections, we attempted to identify sub-clinical, latent carriers. The PCR technique used inthis study has the advantage of both high sensitivityand high specificity.19 At the time of sampling, noneof the 50 albatrosses had evidence of fecal sheddingof Chlamydophila spp. Although a combination ofserology, hematology, and cloacal and choanalDNA detection by PCR maximizes the probabilityof detecting true positives,19 the absence of this or-ganism in all cloacal swab samples suggests thatChlamydophila spp. either occurs at an extremelylow prevalence and was not detected by our sam-pling methodology or is not present in the wavedalbatross population.

Continued surveillance for causes of morbidityand mortality and further resolution into age, sex,and seasonal and geographic differences is war-ranted.

Acknowledgments: This study was made possibleby the Des Lee Collaborative Vision in ZoologicalResearch and the Saint Louis Zoo. Partial financialsupport came from a Saint Louis Zoo Field Re-search for Conservation grant to one of the authors(KPH). We thank the Charles Darwin Research Sta-tion and the Galapagos National Park Service forproviding logistical and technical support, Dr. MaryDuncan and Dr. Anthony Fiumera for field assis-tance during sample collection, Dr. Dave Andersonfor logistical, technical, and equipment support dur-ing the field season, and Dr. Randy Junge for com-ments on the manuscript.

LITERATURE CITED

1. Anderson, D. J., and F. Cruz. 1997. Biology andmanagement of the waved albatross at the Galapagos Is-lands. In: Robertson, G., and R. Gales (eds.). AlbatrossBiology and Conservation. Surrey Beatty and Sons, Chip-ping Norton, Australia. Pp. 105–109.

2. Bowman, D. D. 1995. Protozoans. In: Bowman, D.D. (ed.). Georgis’ Parasitology for Veterinarians. W. B.Saunders Co., Philadelphia, Pennsylvania. Pp. 83–111.

3. Croxall, J. P., and R. Gales. 1997. An assessment ofthe conservation status of albatrosses. In: Robertson, G.,and R. Gales (eds.). Albatross Biology and Conservation.Surrey Beatty and Sons, Chipping Norton, Australia. Pp.46–65.

4. Fridolfsson, A. K., and H. Ellegren. 1999. A simpleand universal method for molecular sexing of non-ratitebirds. J. Avian Biol. 30: 116–121.

5. Fudge, A. M. 1997. Avian clinical pathology—he-matology and chemistry. In: Altman, R. B., S. L. Clubb,G. M. Dorrenstein, and K. Quesenberry (eds.). AvianMedicine and Surgery. W. B. Saunders Co., Philadelphia,Pennsylvania. Pp. 142–157.

6. Fudge, A. M. 2000a. Avian complete blood count.In: Fudge, A. M. (ed.). Laboratory Medicine: Avian andExotic Pets. W. B. Saunders Co., Philadelphia, Pennsyl-vania. Pp. 9–18.

7. Fudge, A. M. 2000b. Avian liver and gastrointestinaltesting. In: Fudge, A. M. (ed.). Laboratory Medicine: Avi-an and Exotic Pets. W. B. Saunders Co., Philadelphia,Pennsylvania. Pp. 47–55.

8. Harr, K. E. 2001. Hematologic and biochemicalmethodologies and the development of reference ranges.Proc. Am. Assoc. Zoo Vet. Am. Assoc. Wildl. Vet. 2001:58–61.

9. Harris, M. P. 1973. The biology of the waved alba-tross Diomedea irrorata of Hood Island, Galapagos. Ibis.115: 483–510.

10. Karesh, W. B., M. M. Uhart, E. Frere, P. Gandini,W. E. Braselton, H. Puche, and R. A. Cook. 1999. Healthevaluation of free-ranging rockhopper penguins (Eudypteschrysocomes) in Argentina. J. Zoo Wildl. Med. 30: 25–31.

11. Lane, R. A. 1996. Avian hematology: basic cellidentification, white blood cell count determinations andclinical pathology. In: Rosskopf, W. J., and R. W. Woerpel(eds.). Diseases of Cage and Aviary Birds. Williams andWilkins Co., Baltimore, Maryland. Pp. 739–772.

12. Langlois, I., and M. P. Jones. 2001. Ventral abdom-inal hernia associated with hepatic lipidosis in a red lory(Eos bornea). J. Avian Med. Surg. 15: 216–222.

13. McNulty, M. S., T. J. Connor, F. McNeilly, and J.B. McFerran. 1990. Biological characterisation of avianenteroviruses and enterovirus-like viruses. Avian Pathol.19: 75–87.

14. Petrie, A., and P. Watson. 1999. Statistics for Vet-erinary and Animal Science. Blackwell Science, Oxford,U.K.

15. Phalen, D. N. 2000. Avian viral diagnostics. In:Fudge, A. M. (ed.). Laboratory Medicine: Avian and Ex-otic Pets. W. B. Saunders Co., Philadelphia, Pennsylvania.Pp. 111–124.

16. Ritchie, B. W. 1995. Adenoviridae. In: Ritchie, B.W. (ed.). Avian Viruses: Function and Control. WingersPublishing Co., Lake Worth, Florida. Pp. 313–333.

17. Russo, E. A., L. McEntee, L. Applegate, and J. S.Baker. 1986. Comparison of two methods for determina-tion of white blood cell counts in macaws. J. Am. Vet.Med. Assoc. 189: 1013–1016.

18. Spalding, M. G., and D. J. Forrester. 1993. Diseasemonitoring of free-ranging and released wildlife. J. ZooWildl. Med. 24: 271–280.

19. Vanrompay, D. 2000. Avian chlamydial diagnos-

283PADILLA ET AL.—WAVED ALBATROSS REFERENCE VALUES

tics. In: Fudge, A. M. (ed.). Laboratory Medicine: Avianand Exotic Pets. W. B. Saunders Co., Philadelphia, Penn-sylvania. Pp. 99–110.

20. Warham, J. 1996. Petrels and man. In: Warham, J.(ed.). The Behaviour, Population Biology and Physiologyof the Petrels. Academic Press Limited, London, U.K. Pp.506–538.

21. Work, T. M. 1996. Weights, hematology, and serum

chemistry of seven species of free-ranging tropical pelagicseabirds. J. Wildl. Dis. 32: 643–657.

22. Zaias, J., W. P. Fox, C. Cray, and N. H. Altman.2000. Hematologic, plasma protein, and biochemical pro-files of brown pelicans (Pelecanus occidentalis). Am. J.Vet. Res. 61: 771–774.

Received for publication 21 October 2002