Seabird Hematology and Chemistry

Journal of Wi1d1fr Diseases, 32(4), 1996. pp. 643-657

643

WEIGHTS, HEMATOLOGY, AND SERUM CHEMISTRY OF SEVENSPECIES OF FREE-RANGING TROPICAL PELAGIC SEABIRDS

Thierry M. WorkNational Biological Service, National Wildlife Health Center-Honolulu Field Station, P.O. Box 50167,Honolulu, Hawaii 96850, USA

ABSTRACT: I established reference values for weight, hematology, and serum chemistry for sevenspecies of free-ranging Hawaiian tropical pelagic seabirds comprising three orders (Procellari-iformes, Pelecaniformes, Charadniformes) and six families (Procellariidae, Phaethontidae, Di-omedeidae, Sulidae, Fregatidae, and Laridae). Species examined included 84 Hawaiian dark-rumped petrels (Pterodoma phaeopygia), 90 wedge-tailed shearwaters (Puffinus pacificus), 151Laysan albatrosses (Diomedea immutabilis), 69 red-footed boobies (Sula sula), 154 red-tailedtropicbirds (Phaeton rubricauda), 90 great frigatebirds (Fregata minor), and 72 sooty terns (Sternafuscata). Hematoent, total plasma solids, total and differential white cell counts, serum glucose,calcium, phosphorus, uric acid, total protein, albumin, globulin, aspartate aminotransferase andcreatinine phosphokinase were analyzed. Among and within species, hematology and chemistryvalues varied with age, sex, season, and island of collection. Despite this variation, order-widetrends were observed.

Key words: Hawaiian dark-rumped petrel, Pierodoma phaeopygia, wedge-tailed shearwater,Puffinus pacificus, Laysan albatross, Diomedea immutabilis, red-footed booby, Sula sula, red-tailedtropicbird, Phaeton rubricauda, great frigatebird, Fregata minor, sooty tern, Sterna fuscata, he-matology, serum chemistry, body weight.

INTRODUCTiON

Clinical chemistry and hematology arevaluable adjuncts in the diagnosis of dis-ease in animals (Campbell, 1994; Hoch-leithner, 1994). Reference values for he-matology and clinical chemistry are avail-able for a variety of species. In birds, ref-erence hematology and blood chemistryvalues are most numerous for groups thatare managed intensively in production andclinical settings. Examples include psitta-cines, raptors, and poultry (Campbell,1994; Hochleithner, 1994). Reference val-ues are less numerous for many captive orfree-ranging species outside these groups.

Most literature on hematology andblood chemistry of seabirds covers antarc-tic birds (Hawkey et al., 1989; Rosa et al.,1993) or temperate coastal seabirds (Bal-asch et al., 1974; Wolf et a!., 1985; Melroseand Nicol, 1992), and some of these in-volve either smail (

644 JOURNAL OF WILDLIFE DISEASES, VOL. 32, NO. 4, OCTOBER 1996

time of sampling or during the two previousbreeding seasons. I sampled three species ofprocellariiforms including Hawaiian dark-rumped petrels (Pterodoma phaeopygia),wedge-tailed shearwaters (Puffinus pacificus),and Laysan albatross (Diomedea immutabilis);three species of pelecaniforms including red-footed boobies (Sula sula), red-tailed tropic-birds (Phaeton rubricauda), great frigatebirds(Fregata minor); and one charadriiform, sootyterns (Sterna fuscata).

Twenty-one and 35 Hawaiian dark-rumpedpetrels chicks were sampled from HaleakalaNational Park on Maui (20#{176}43N, 156#{176}15W) inOctober 1993 and October 1994, respectively,and 28 adults were sampled from the same sitein July 1994. Forty-five wedge-tailed shearwa-ter chicks and 45 adults were sampled on Au-gust and October 1994, respectively, from off-shore islets along southeastern Oahu includingwest and east Makoluas and Popoia (21#{176}23N,157#{176}43W). Twenty and 16 Laysan albatrossadults were sampled in October 1993 fromLaysan Island (25#{176}46N, 171#{176}44W) and TernIsland-French Frigate Shoals (23#{176}45N,166#{176}10W), respectively, and 43 adults weresampled from Midway atoll (28#{176}13N,177#{176}22W) in June 1994. I sampled 41 Laysanalbatross chicks from Midway in June 1993,and 15 and 16 Laysan albatross chicks fromMidway and Kilauea Point, Kauai (22#{176}13N,159#{176}26W) respectively, in June 1994.

I sampled 35 and 34 red-footed booby adultsand chicks, respectively, from Kanehoe MarineCorps Air Station on Oahu (21#{176}27N,157#{176}44W) in August 1994. Fifty-three red-tailed tropicbirds adults were sampled fromTern Island in March 1994, and 36 adults and65 chicks from Johnston Atoll (16#{176}45N,169#{176}31W) in April 1995. I sampled 60 and 30great frigatebirds from Laysan Island and TernIsland, respectively, in March 1994. Thirty-fivesooty tern chicks and 37 adults were sampledfrom Johnston Atoll in July 1995.

Birds were classified as adults or chicks andadult frigatebirds as male or female based onplumage (Pratt et al., 1987). Lack of sexual di-morphism precluded classification by sex oftropicbirds, boobies, terns, albatrosses, shear-waters, and petrels. Petrels were classified aschicks or adults based on date of collection andpresence or absence of juvenile plumage (Si-mons, 1985).

All birds were captured manually or withlarge hand-held hoop nets. Petrels were cap-tured with double-door wire box traps (Simons,1985). Petrels and tropicbirds were weighed tothe nearest 10 g with a 1 kg spring scale, frig-atebirds and albatrosses to the nearest 100 gwith a 5 kg spring scale, boobies to the nearest

50 g with a 2.5 kg spring scale, and tems andshearwaters to the nearest 1 g with a 500 gspring scale. I assessed all birds visually andchose only healthy animals, defined as those in-dividuals that were in good flesh, bright, alert,resistive to restraint, and with no detectablemorphologic or behavioral abnormalities.

Five ml of blood was procured from the cu-taneous ulnar vein in frigatebirds, albatross,boobies, and tropicbirds using 5 ml syringesand 20 gauge 26 mm needles. Three ml ofblood were obtained from similar sites in pet-rels, terns, and shearwaters using 3 ml syringesand 22 gauge 26 mm needles. One half ml ofblood was placed in 500 i.l ethylenediamine-tetraacetate (EDTA) tubes and the remainderin 5-ml clotting tubes. Whole blood in EDTAwas stored at 4 C for up to 8 hr prior to pro-cessing for hematology. The remaining bloodwas allowed to clot for 12 hr at 27 C, centri-fuged, serum decanted into 1.5 ml cryovials(Corning, Corning, New York, USA), and fro-zen at -20 C.

For albatrosses from Midway, an extra 1 mlof blood was stored in EDTA and analyzed forlead (Fernandez and Hilligoss, 1982) at the Na-tional Wildlife Health Center, Madison, Wis-consin (USA). Only healthy birds with bloodlead levels at or below the limit of detection(0.02 p.g/ml) were included in the study.

Combined heterophil and eosinophil countswere done in the field with a Neubauer hem-ocytometer, eosinophil unopettes no. 5877(Becton Dickinson, Rutherford, New Jersey,USA) and a microscope. Total white cell counts(103/pJ) were then calculated (Campbell,1994). I obtained hematocrit values by spinningwhole blood in heparinized capillary pipettes ina microhematocrit centrifuge for 5 mm (Camp-bell, 1994). Plasma total solids were estimatedusing a temperature-adjusted refractometer(Schuco, American Caduceus Industries, CarlePlace, New York) (Campbell, 1994). Bloodsmears from EDTA blood were made in dupli-cate, allowed to air dry, stored in slide boxesand returned to the laboratory for staining andmicroscopic examination.

Prior to conducting differentials, bloodsmears for each species were pooled, random-ized, and read blind. For differential counts, Istained smears using Difquick (Fisher Scientif-ic, Pittsburgh, Pennsylvania, USA) and counted200 white cells under oil immersion (1,000x).Cells were classified as heterophils, eosinophils,lymphocytes, monocytes, or basophils based onmorphology and staining characteristics(Campbell, 1994). Percentages were calculatedand multiplied by the total white count to ob-tain absolute counts of each white cell type

WORK-WEIGHTS, HEMATOLOGY, AND SERUM CHEMISTRY OF TROPICAL SEABIRDS 645

(Campbell, 1994). I recorded presence or ab-sence of hemoparasites.

Serum chemistry values including total pro-tein (g/dl), albumin (g/dl), uric acid (mg/dl),calcium (mg/dl), phosphorus (mg/dl), aspartateaminotransferase (AST) (lUlL), creatinine phos-phokinase (CPK) (lU/L), and glucose (mg/dl),were determined at the University of Wiscon-sin School of Veterinary Medicine in Madison,Wisconsin, using a Kodak Ektachem 500 ana-lyzer (Eastman Kodak, Rochester, New York).This system is a dry analyzer that uses slides onwhich the sample is placed. The slides consistof a dry multilayer analytic element on a poly-ester support containing specific reagents foreach analyte. Globulin was calculated by sub-tracting albumin from total protein. Serumchemistries were analyzed blind.

Hematology and blood chemistry valueswere summarized using means, standard devi-ations, medians, and ranges. Chemistry valuesfrom hemolyzed serum or analytes which werebelow the limit of detection were excludedfrom analysis. I compared summarized hema-tology and serum chemistry parameters usingone way analyses of variance (ANOVA) forgroups of three or more, or t-tests for pairs. Toadjust for test-wise error and maintain anpenment-wise error rate of 0.05, I used a se-quential Bonferroni adjustment (Rice, 1989)for a; a 0.003 for n = 18, the total numberof parameters compared including weight, he-matology and chemistry. In cases where as-sumption of normality or equal variance wereviolated, a Kruskall-Wallis ANOVA or theMann-Whitney U test for multiple or pair-wisecomparisons, respectively, were used. In casesof significant differences with ANOVA, multi-ple pair-wise comparisons were done using Stu-dent-Newman-Keuls and Dunns test for para-metric and non-parametric procedures, respec-tively (Daniel, 1987). Statistical tests were doneusing Sigmastat (Jandel Scientific Software, SanRafael, California, USA).

To determine age differences, I comparedchicks versus adults for petrels, shearwaters,terns, boobies, and tropicbirds collected fromJohnston in 1995, and albatrosses collectedfrom Midway in 1994. Group-wise comparisonsfor great frigatebird males, females and chickswere done separately for Tern Island and Lay-san Island. I also compared individuals fromthe following groups to see if they could bepooled: petrel chicks collected in 1993 and1994; albatross chicks from Midway in 1993,1994 and from Kauai in 1994; albatross adultsfrom Midway in 1994, Laysan Island, and TernIsland in 1993; red-tailed tropicbird adultsfrom Tern Island in 1993 and Johnston Atoll in1995. Great frigatebird males, females, and

chicks were compared separately between TernIsland and Laysan Island.

RESULTS

In all species, heterophils were largerthan red cells, had a dense homogenous,dark, blue-purple segmented nucleus, anda clear cytoplasm packed with masses ofbrick-red fusiform granules that partiallyobscured the nucleus. Basophils weresmaller than heterophils or eosinophils,had a round, dense, homogenous, unseg-mented, purple-blue nucleus, and clear cy-toplasm with many coarse to fine purpleround granules. Lymphocytes were van-ably sized with a round purple-bluecoarsely textured nucleus surrounded byhomogenous blue cytoplasm with well-de-fined borders. Monocytes were the largestwhite cell with an ameboid, finely granularblue-purple nucleus surrounded by a paleground-glass blue wispy cytoplasm with ill-defined borders and occasional variably-sized vacuoles.

Eosinophils were similar in size to het-erophils with a segmented nucleus; how-ever, granule morphology varied amongspecies. Eosinophil cytoplasm of shearwa-ters, terns, and petrels contained denselypacked, orange, round, plump granules.Albatross eosinophils contained looselypacked tiny round bright red-orange gran-ules while granules of booby eosinophilswere somewhat larger and brighter or-ange. Great frigatebird eosinophils con-tained loosely packed, plump, elliptical,orange granules distributed among vari-ably sized clear vacuoles. Tropicbird eosin-ophils had a clear to blue cytoplasm con-taining sparse numbers of amorphous toround, large, dull-orange granules inter-spersed with numerous small, clear, welldefined vacuoles. Thrombocytes wereabout 75% as large as red cells, ovoid, witha uniformly dense purple-blue nucleus anda clear to light blue cytoplasm.

In all species, red cell morphology wasuniform and polychromasia variable. Theonly hemoparasite seen was an intracellu-lar organism in frigatebird red cells with


Adult albatrosses from Midway in 1994

TABLE 1. Reference weights, hematology and serum chemistry of Hawaiian dark rumped petrels chicks andadults from Maui.

Chicks Adults

Mean SD Range n Mean SD Range ri

Weight (g) 4955 62 390-640 53 432 32 380-500 28

HematologyHematocrit (%) 49 5 34-58 56 49 4 42-59 28Total solids (gIdl) 3.6a 0.4 2.8-4.6 56 4.1 0.6 3.1-5.4 28Lymphocyte (1&31p.l) 13.90#{176} 10.64 1.28-58.61 55 4.36 2.59 1.12-11.94 27Heterophil (1&3/il) 2.31 1.26 0.21-6.02 55 3.39 1.50 1.00-6.98 27Monocyte (10/p.l) 0.09 0.16 0.00-0.77 55 0.10 0.11 0.00-0.46 27Eosinophil (1034d) 0.68 0.58 0.09-2.73 55 1.99 1.24 0.50-5.45 27Basophil (104iJ) 1.16 0.68 0.18-3.26 55 1.11 0.53 0.22-2.06 27Total white cells (1&3/d) 18.14k 11.09 5.16-65.12 55 10.94 3.46 5.03-19.13 27

Serum chemistryGlucose (mg/dl) 316 35 222-375 28 329 43 256-405 21Calcium (mg/dl) 10.1 0.8 8.5-12.2 28 7.0 1.6 3.1-9.4 21Phosphorus (mg/dl) 3.6a 1.3 1.8-8.3 28 0.8 0.3 0.5-1.3 14Uric acid (mg/dl) 22 0.6 1.2-.3.5 28 7.3 4.4 1.9-14.1 21Protein (g/dl) 2.7a 0.9 1.7-6.5 28 3.1 0.5 2.4-4.5 21Albumin (g/dl) 1.3 0.4 1.0-3.3 28 1.5 0.2 1.2-1.8 21Globulin (g/dl) 1.3k 0.5 0.7-3.2 28 1.7 0.4 1.1-2.7 21Aspartate amino-

transferase (LU/L) 106 28 71-169 28 212 116 104-667 21

Creatininephosphokinase (lULL) 114 90 23-344 23 46 16 23-72 10

a Value significantly different that value for sar ise parameter among adul ts (P < O.(X)3).

morphology compatible to that of Hae-moproteus spp.

There were no significant differencesbetween petrel chicks collected in 1993and 1994, so their values were pooled.Compared to chicks, adult petrels had sig-nificantly lower weight, lymphocyte andtotal white cell count, calcium, phospho-rus, and creatinine phosphokinase (CPK)concentrations, but significantly greater to-tal solids, heterophil and eosinophilcounts, uric acid, total protein, globulin,albumin, and aspartate amino-transferase(AST) concentrations (Table 1).

Shearwater adults had significantly low-er weight, lymphocyte and total white cellcount, calcium, phosphorus, albumin, andCPK concentrations, but significantlygreater hematocnt, heterophil and mono-cyte count, glucose, uric acid, globulin,and AST concentrations than chicks (Table2).

had significantly lower total solids, lym-phocyte and total white counts, calcium,phosphorus, and globulin concentrations,but significantly greater hematocrits,sinophil counts, and glucose, uric acid, andAST concentrations than chicks from Mid-way in 1994 (Tables 3, 4).

Adult boobies had significantly lowerlymphocyte and total white cell counts, butsignificantly greater weight, hematocrit,heterophil and eosinophil counts, and ASTconcentrations than chicks (Table 5).

Compared to chicks, adult tropicbirdsfrom Johnston had significantly lower lym-phocyte, eosinophil, and total whitecounts, and calcium and phosphorus con-centrations, but significantly greater he-matocrits and total solids (Table 6).

On Tern Island and Laysan Island, greatfrigatebird adult males and females hadsignificantly greater hematocrits thanchicks. On Tern Island only, femalesweighed significantly more than chicks or


TABIE 2. Reference weights, hematology and serum chemistry of wedge tailed shearwater chicks and adultsfrom Oaliu.

Chicks Adults

Mean SD Range n Mean SD Range n

Weight (g) 467a 50 365-590 45 39() 35 315-450 45

Hematology

Ilematocrit (%) 375 3 30-43 45 48 3 39-.53 45Total sOli(l5 (g/dl) 3.7 0.3 3.0-4.4 45 3.9 0.4 3.()-4.8 45Lymphocyte (1034d) 26.04 13.49 7.61-70.05 45 12.93 6.21 3.49-27.42 45Ileterophil (10/jil) 2.49#{176} 0.95 0.91-5.05 45 4.00 2.09 0.57-10.47 45Monocyte (1&3/p.l) 0.15 0.19 0.00-0.77 45 0.45 0.48 0.00-2.05 45Eosinophil (1&3/p.l) 0.74 2.21 0.00-14.81 45 0.48 0.51 0.00-1.95 45Basophil (1&/pJ) 0.34 0.44 0.00-2.68 45 0.31 0.31 0.00-1.05 45Total white cells (l0/d) 29.75 13.93 9.45-76.56 45 18. 18 7. 17 5.03-34.32 45

Seniiii chemistry(;hicose (mgidl) 202 23 145-255 45 248 28 202-328 42Calcium (mg/dl) 11.8k 1.2 7.8-13.8 45 8.8 1.4 3.8-10.5 42Phosphorus (mg/dl) 8.8a 2.0 5.2-13.9 44 1.6 0.9 0.5-3.6 .35Uric acid (mg/dI) 6.2k 4,3 1.2-15.8 45 10.2 5.1 2.7-24.5 42Protein (g/dl) 3.2 0.4 2.6-4.2 45 3.4 0.4 2.7-4.2 42Albumin (g/dl) 1.7 0.2 1.4-2.2 45 1.5 0.1 1.2-1.8 42Globulin (g/dl) 1.5 0.2 1.2-2.0 45 1.8 0.3 1.4-2.5 42Aspartate amino-

transferase (lUlL) 153 41 95-274 45 258 93 121-544 42Creatinine

phosphokinase (lUlL) 89tP 899 147-4,473 45 86 69 2.5-306 35

a Value significantly different than value for same parameter among adults (P < 0.(X)3).

males. Females had significantly greatercalcium concentrations than males which,in turn, had significantly greater concen-trations than chicks. On Laysan Islandonly, adults had significantly greaterweights, and total protein, albumin andglobulin concentrations, but significantlylower uric acid concentrations than chicks.Female adults had significantly greater to-tal solids, and calcium and phosphorusconcentrations, than either males orchicks. Male adults had significantly lowertotal solids and phosphorus concentrationsthan chicks (Tables 7, 8).

Sooty tern adults had significantly lowerweights, lymphocyte and total whitecounts, and calcium, phosphorus, andCPK concentrations, but significantlygreater hematocrits and AST concentra-tions than chicks (Table 9).

Great frigatebirds of all age and sexgroups from Laysan Island had significant-ly greater glucose concentrations than cor-

responding groups on Tern Island. Greatfrigatebird adult males and chicks fromLaysan had significantly lower phosphorusconcentrations than corresponding groupson Tern (Tables 7, 8). Laysan albatrossadults from Laysan Island had significantlygreater lymphocyte counts, glucose andphosphorus concentrations, but signifi-cantly lower CPK concentrations thanthose from Tern Island (Table 3). Albatrosschicks from Kauai had significantly lowertotal solids, phosphorus, total protein, andglobulin concentrations than those fromMidway in 1994 (Table 4).

Prenesting Laysan albatross adults fromTern and Laysan collected in October1993 had significantly greater weight, totalsolids, and albumin concentrations, butsignificantly lower uric acid concentrationsthan post-incubation adults from Midwaycollected in 1994 (Table 3). Albatrosschicks from Midway in 1993 could not bepooled with those collected from Midway

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TABLE 5. Referent weight, hematology and serum chemistry of reel fcoted bo()l)y a(lultS coal chicks fromOahu.

Chicks Adults

Meami SD Range n Mean SI) llangc it

Weight (kg) 1.oa 0.1 0.9-1.2 34 1.1 0.1 0.9-1.4 35Hematology

Hematocrit (%) 44 3 37-48 34 48 3 4I-54 35Total solids (gldl) 3.5 0.4 2.8-4.4 34 3.8 0.5 3.()-4.6 35Lymphocyte (1&3/p,l) 11.40a 8.21 2.32-44.35 34 3.26 1.41 1.11-8.26 35Heterophil (1&/pi) 3.3W 1.66 0.26-6.85 34 5.73 2.18 2.52-11.97 35Monocyte (1034d) 0.10 0.12 0.()0-0.5() 34 0.19 0.23 0(30-0.79 35Eosinophil (1&3/p.l) 0.28k 0.29 0.0(3-0.97 34 0.57 0.40 0.03-1.79 35Basophil (10/el) 0.14 0.14 0(30-0.59 34 0.16 0.12 0.()0-0.47 35Total white cells (104el) 15.32a 8.44 4.40-49.28 34 9.91 2.69 5.27-15.22 35

Serum chemistryGlucose (mg/dl) 179 35 94-237 32 196 43 1 13-293 32Calcium (mg/dl) 8.2 2.8 3.4-13.2 32 8.5 1.9 4.5-10.9 32Phosphorus (mg/dl) 7.1 4.5 2.1-20.9 32 5.9 3.5 2.1-12.9 32Uric acid (mgldl) 16.2 8.8 3.0-32.7 32 13.8 7.1 3.3-27.8 32Protein (g/dl) 2.7 0.3 2.1-3.4 32 3.0 0.4 2.3-4.5 32Albumin (g/dl) 1.2 0.1 1.0-1.5 31 1.3 0.2 1.()-2.() 32Globulin (g/dl) 1.6 0.2 1.2-1.9 31 1.7 0.3 1.3-2.5 32Aspartate an)ino-

transferase (lU/L) 302 150 134-922 32 502 163 279-831 32Creatinine

phosphokinase (lUlL) 341 210 22-937 32 256 220 40-1,067 28

a Value significantly different than value for same paranie.ter among a(hllts (P < O.(X)3).

in 1994 (Table 4). Similarly, tropicbirdadults from Tern collected in 1993 couldnot be pooled with those collected fromJohnston in 1995 (Table 6).

DISCUSSION

Body weights of seabirds in this studywere within ranges observed by others(Frings and Frings, 1961; Fleet, 1974;Nelson, 1975, 1978; Flint and Nagy, 1984;Pettit et al., 1984; Simons, 1985). Thestaining method used for differentialcounts was adequate to allow distinction ofwhite cell types; for all species, morphol-ogy of heterophils, monocytes and lym-phocytes was similar to that of other avianspecies (Campbell, 1994). Variation inmorphology of eosinophils has been notedin other species (Hawkey and Dennett,1989). Often, basophil granules werebleached and looked like those of chickens(Hodges, 1974). Description of the para-site identified as Haemoproteus spp. , its

parasitemia, and prevalence are describedby Work and Rameyer (1996).

There was marked variability in hema-tology and chemistry parameters evenwhen I controlled for age, sex, location,and time of collection. All serum chemis-try samples were analyzed at the same lab-oratory by the same technician, and I readall the differential counts in attempts toeliminate human variation. However, thesereference values (10 encompas5 severalconfounders . Although population historywas known, individual history was not.Hence, things like inapparent pathologicprocesses, diurnal variation (Rehder et a!.,1982), and sex differences in species lack-ing sexual dimorphism could contnbute tothe variability observed here.

Had I not used the sequential Bonfer-roni adjustment to analyze these data,many more significant differences vouldhave been noted. Rice (1989) pointed outthat there was a 95% chance of finding a

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dIN as01asasas-mous reviewers all kindly provided constructivecomments on the manuscript. Finally, much ofthis work would not have been possible withoutthe assistance of the Hawaii Department of Ag-riculture who graciously provided laboratoryspace.

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Seabird Hematology and Chemistry