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Health and nutritional status of wild Australian psittacine birds: an evaluation of plasma and hepatic mineral levels, plasma biochemical values, and fecal microflora.

Abstract: To evaluate the health and nutritional status of 3 wild Australian psittacine species, plasma and hepatic mineral concentrations and plasma biochemical values were measured in wild-caught galahs (Eolophus roseicapilla), long-billed corellas (Cacatua tenuirostris), and sulphur-crested cockatoos (Cacatua galerita). No correlations were found between hepatic and plasma mineral levels. Mean plasma calcium (1.79 mmol/L [7.16 mg/dL]) and sodium (103 mmol/ L [103 mEq/L]) concentrations were lower, whereas mean total phosphorus (6.53 mmol/L [20.22 mg/dL]) and potassium (8.87 mmol/L [8.87 mEq/L]) concentrations were higher than values for captive counterparts. Plasma iron levels were higher than those reported for captive counterparts, with evidence of interspecific (sulphur-crested cockatoos, 109 [micro]mol/L [609 [micro]g/dL]; corellas, 57 [micro]mol/L [318 [micro]g/dL]; galahs, 90 [micro]mol/L [503 [micro]g/dL]) and temporal variation (galahs: May, 107 [micro]mol/L [598 [micro]g/dL]; July, 59 [micro]mol/L [330 [micro]g/dL]). Hepatic iron concentrations were as high as 1030 mg/kg. Interspecific variation was minimal in mean plasma selenium (11.8 [micro]mol/L [929 [micro]g/L]) and zinc (31.2 [micro]mol/L [204 [micro]g/dL]) concentrations. Plasma biochemical values varied significantly from reported reference ranges. Ranges for total protein, albumin, and bile acid concentrations were lower, whereas uric acid, glutamate dehydrogenase, amylase, and cholesterol concentrations were higher than those previously reported for these species, and interspecific variation was evident. Variation in measures of mineral status or plasma biochemical values between males and females were negligible. An evaluation of fecal microflora showed a distinct absence of gram-negative bacteria or budding yeast. Results of this study show that analyte values used to determine health and nutritional status of wild birds differ from those published for captive counterparts. Although analyte values appear to vary minimally by sex, distinct taxonomic and some temporal differences exist in values from wild birds of these 3 species.

Key words: nutrition, plasma biochemical analysis, minerals, avian, psittacine, sulphur-crested cockatoo, Cacatua galerita, long-billed corella, Cacatua tenuirostris, galah, Eolophus roseicapilla

Introduction

Malnutrition is prevalent among birds maintained in captivity, negatively influencing reproductive output, survival of chicks, and longevity. Because of a paucity of comprehensive data to develop reference ranges from wild birds, clinicians must extrapolate from data applicable to agricultural species or captive populations that appear clinically normal. However, these data can be influenced by husbandry, including diet, as well as taxonomic variations, and intraspecific comparisons between healthy and compromised individuals do not take into account the degree of variability within a normal population. (1) Erroneous interpretation of nutritional status can lead to misplaced dietary supplementation or treatment. Therefore, reference ranges need to be established from data collected from healthy wild birds.

Calcium concentrations of unsupplemented, seed-based diets are generally inadequate for pet psittacine birds, whereas standards set for agricultural species (2) might overestimate requirements for species such as budgerigars (Melopsittacus undulatus) and blue and gold macaws (Ara ararauna). (3) Deficiencies of trace elements are rarely diagnosed in pet birds, but metal toxicosis is particularly problematic, and a lack of baseline data could result in an erroneous diagnosis of health status. Although copper toxicosis is rare, iron and zinc toxicoses are regularly reported. Excess dietary iron is implicated in the development of iron storage disease in many species of birds, 4-11 including several psittacine species. (10,12,13) However, definitive diagnosis from measurement of blood iron levels is difficult, (14) and it is unclear whether plasma iron levels correlate with hepatic concentrations in psittacine birds. Accurate interpretation of zinc nutritional status is essential because erroneous conclusions could result in inappropriate treatment. Although deficiencies of zinc are rarely reported, zinc toxicosis is reported in psittacine birds, (15-22) usually arising from ingestion of zinc-coated aviary wire or metallic foreign bodies and rarely dietary in origin.

Many studies of nutritional parameters of birds do not include an evaluation of health status. However, most published data for plasma biochemical reference ranges in Australian cockatoos appear to be based on captive birds. (23) Captive management systems, including diet, and subclinical disease in individual birds could affect the data collected from these groups. Furthermore, reference ranges derived from a mix of cockatoo species or from inadequately identified specimens (24-27) is common, and the extent of taxonomic variation in many of these parameters is not known.

An important component of a complete health evaluation of captive psittacine birds is the investigation of fecal microflora with a fecal Gram's stain. The bacterial population of the psittacine gastrointestinal tract is a part of the nonspecific defense mechanism, and normal resident microflora maintain an acidic environment that inhibits the proliferation of gram-negative rods and yeast. An imbalance in homeostasis results in alterations to the normal functions of microflora, thus influencing the distribution of bacteria in the gastrointestinal tract. Results of early studies indicate that many birds have low levels of gram-negative bacteria on fecal culture. (28,29) Other researchers maintain that autogenous flora in parrots are not gram-negative, (30) with normal fecal flora of psittacine birds composed of 100% gram-positive, non-spore-forming rods and cocci. (31) However, no reports evaluating the composition of fecal microflora in wild psittacine birds have been published. Whether low levels of gram-negative bacteria in apparently healthy captive birds resemble levels in their wild counterparts is unclear.

To establish reference ranges and to identify whether health and nutritional parameters in wild Australian psittacine birds vary by sex, taxonomy, or season, blood and liver samples collected from 3 species of cockatoos in the northwestern district of Victoria were evaluated. The sulphur-crested (SC) cockatoo (Cacatua galerita) has great nutritional flexibility, occupying a wide range of habitats and feeding predominantly on the seeds of grasses and herbs while supplementing its diet with roots, rhizomes, nuts, berries, flowers, corms, blossoms, and insect larvae. (32) By contrast, the long-billed (LB) corella (Cacatua tenuirostris) relies on water, which restricts its range to areas where watercourses are located. (32) It feeds predominantly on the ground and favors corms of the onion grass Romulea longifolia as well as seeds, nuts, berries, fruits, roots and bulbs, and insects and their larvae. The galah (Eolophus roseicapilla), also called the rose-breasted cockatoo, is one of the most common Australian parrots in the wild, with its distribution encompassing almost the entire Australian continent, including Tasmania. Throughout its range, it feeds on the ground, mainly on seeds of native button grasses such as Dactyloctenium raulans, Flinders grass (Iseilema membranaceum), and Mitchell grass (Astrebla lappacea), as well as on insect larvae, berries, buds, flowers, and eucalyptus seeds. (32) Variations in the feeding ecology of these species possibly influence health and nutritional status, but which parameters are most likely to be affected is not clear.

The overall aims of this study were 1) to establish reference ranges for mineral nutritional status of 3 species of Australian cockatoos, 2) to identify possible correlations between hepatic and plasma mineral concentrations, 3) to establish reference ranges for plasma biochemical values of Australian cockatoos, and 4) to determine whether fecal gram-negative bacteria are prevalent in wild Australian psittacine birds.

Materials and Methods

Three species of Australian cockatoos were evaluated: the SC cockatoo, the LB corolla, and the galah. Birds were trapped with book-type traps by government staff of the annual Cockatoo Mitigation Project, Department of Natural Resources and Environment (DNRE), Victoria. Blood and tissue samples were obtained under DNRE scientific research permit number 10001736.

Birds were visually assessed before blood sampling, and any bird exhibiting clinical or postmortem evidence of disease was eliminated from the study. Plasma and liver samples were collected in May (SC cockatoos and galahs) and July 2002 (galahs and LB corellas), from the Horsham region in the northwest of Victoria. Biochemical parameters in LB corellas were also evaluated in January 2003 to determine whether temporal variation is present in health status in this species. Birds were weighed and sex was determined with concurrent postmortem examination. All birds were processed within 15 minutes of trapping.

Evaluation of the prevalence of fecal gram-negative bacteria was confined to galahs, with fecal samples heat-treated in the field before being evaluated microscopically by Gram's stain. (33) Bacterial culture and sensitivity testing of fecal samples was not done. Birds were anesthetized with chloroform administered via a field mask per government protocol. Blood samples were collected from the jugular vein of anesthetized birds and stored in lithium-heparinized tubes, with plasma separated and immediately stored on ice before being transported to an analytical laboratory within 12 hours for use in subsequent analyses. Plasma biochemical analyses were performed within 48 hours by standard commercial techniques on an Olympus AU400 (Idexx Laboratories, Sydney, Australia). Analytes evaluated included total protein, albumin, globulin, uric acid (UA), urea, total bile acids (TBA), glutamate dehydrogenase (GLDH), glucose, amylase, calcium, and cholesterol. Samples for mineral analysis were stored frozen and analyzed within 5 days of collection. Birds were euthanatized after blood collection by government officials according to official protocol. Livers were removed and stored immediately on ice before being frozen and transferred to a commercial laboratory (Bernard Heath and Associates, Melbourne, Australia). Minerals (calcium, copper, iron, lead, magnesium, phosphorous, potassium, selenium, sodium, and zinc) were evaluated by inductively coupled plasma spectrometry.

Data were analyzed by ANOVA for variation by species, season (summer and winter), and sex by SigmaStat, (Aspire Software, Ashburn, VA, USA). Results were considered significant at P < .05.

Results

Physical condition of birds varied between May and July. Birds sampled in May showed general characteristics of the species observed under ideal situations in captivity, whereas those sampled in July exhibited dry, flaking skin of the crown, lateral region of the neck, and feet. The contour feathers surrounding the vents of birds sampled in July were soiled by loose feces, which were often full of sand particles. Examination of the gonads showed a change from quiescent in May to a hypertrophied state in July. Mean weights and ranges for each species are presented in Table 1.

Mineral analysis

Data for plasma mineral concentration are reported in Tables 2 and 3. No significant differences between sexes were detected. Mean plasma calcium levels (1.79 mmol/L [7.16 mg/dL]) did not differ significantly by species, although concentrations were marginally lower in wild birds than values reported for captive birds (1.90-2.37 mmol/L [7.6-9.5 mg/dL]) (34-37) and poultry (2.24-3.99 mmol/L [8.9-15.9 mg/dL]). (38) By contrast, mean plasma total phosphorus concentrations for wild birds (6.53 mmol/L [20.22 mg/dL]) were lower than values reported for other psittacine birds. (39) Phosphorous concentrations were significantly higher in galahs (P = .017) and LB corellas (P = .007) than in SC cockatoos; note that values for total phosphorous are not equivalent to inorganic phosphate that is generally reported by veterinary clinical pathology laboratories.

Mean plasma copper levels of birds in this study were substantially higher than those reported for captive Hispanolan Amazon parrots (Amazona ventralis) (1.89 [micro]mol/L) (1) but within the range reported for poultry (1.26-7.09 [micro]mol/ L). (38) Mean plasma iron levels were significantly higher in wild birds than in captive counterparts (22 [micro]mol/L [123 [micro]g/dL]), (40) with values for SC cockatoos (P = .002) and galahs (P = .038) significantly higher than that of LB corellas. The higher mean plasma iron concentration in SC cockatoos also corresponded to a significantly higher mean plasma zinc concentration in this species. Mean plasma potassium concentrations of wild birds (8.87 mmol/L [8.87 mEq/L]) were higher than those reported for captive psittacine birds (1.7-5.2 mmol/L [1.7-5.2 mEq/L]), (34-37) with mean values for sodium (103 mmol/L [103 mEq/ L]) lower than those for captive psittacine birds (135-158 mmol/L [135-158 mEq/L). (34-37) Plasma mineral values did not correlate with weight or with hepatic values.

Data for hepatic mineral content are presented in Tables 4 and 5 and expressed on a wet weight basis. No significant differences were found between males and females in any hepatic minerals analyzed. Mean hepatic copper content was lowest, whereas mean iron concentration was highest in LB corellas, with iron concentrations highest in females (females, 654 mg/kg; males, 538 mg/kg), but this difference was not significant (P = .39). Hepatic iron concentrations varied significantly by species (SC cockatoos > galahs, P = .015; LB corellas > galahs, P < .001; LB corellas > SC cockatoos, P = .002). Hepatic lead content was only evaluated for 2 species, with the higher mean value for female LB corellas (0.14 mg/kg). Mean hepatic manganese concentration was highest in LB corellas, whereas mean hepatic selenium concentration was highest in SC cockatoos.

Hepatic zinc concentrations are presented in Table 6, comparing previously published data (15,16,22,41) with results from this study. In wild birds in this study, hepatic zinc content varied minimally by species, with significant differences only between SC cockatoos and galahs (SC cockatoos > galahs, P = .017). Values in this study were below published values for various psittacine species maintained in captivity, especially for those diagnosed with zinc toxicosis.

Biochemical analysis

Data from plasma biochemical analyses are presented in Table 7. For LB corellas and galahs, ranges are defined as maximum and minimum analyzed values because these species provided fewer than 20 samples, whereas ranges for SC cockatoos are defined as the mean [+ or -] 2 standard deviations.

No temporal differences were identified in plasma biochemical parameters for LB corellas. There was little evidence of variation by sex within a species, with the only significant difference being mean glucose values higher in male than in female SC cockatoos (P = .03). By contrast, values for many analytes varied significantly by species. Mean values were higher in SC cockatoos than in the other 2 species for total protein (LB corellas, P = .02; galahs, P < .001); albumin (LB corellas, P = .003; galahs, P < .001); amylase (LB corellas, P < .001; galahs, P < .001); and calcium (LB corellas, P < .001; galahs, P = .005). Mean values were lower in SC cockatoos than either of the other 2 species for GLDH (LB corellas, P = .004; galahs, P = .01), glucose (LB corellas, P = .002; galahs, P = .01), and cholesterol (LB corellas, P = .009; galahs, P < .001). Mean concentrations of uric acid and urea were lower for LB corellas than the other species (SC cockatoos, P = .01; galahs, P < .001), whereas galahs exhibited lower mean albumin (P = .004) and higher mean GLDH (P = .001) concentrations than LB corellas and a higher mean urea concentration than SC cockatoos (P < .001).

Although not evaluated statistically, noteworthy variations in analytes in the current study were apparent when compared with reported reference ranges (Table 7). Ranges for total plasma protein and albumin were lower for all 3 species, whereas globulin concentrations were higher in corellas and lower in SC cockatoos than reported ranges. Ranges for uric acid were higher in galahs and SC cockatoos, whereas ranges for urea were lower for all 3 species than that previously reported. In all 3 species, ranges for total bile acids were lower in galahs and SC cockatoos, whereas those for GLDH, cholesterol, and amylase were higher than previously reported ranges. Calcium reference ranges were lower in LB corellas and SC cockatoos than reported ranges.

Fecal microflora

Wide variations in total bacterial morphology were observed in fecal samples, with gram-positive rods more numerous than gram-positive cocci. Gram-negative bacteria and yeasts were not observed in the 8 samples from June 2002, with red blood cells (RBCs) evident in only 4 birds in the January 2003 sampling. No other differences were observed. Yeasts were only detected in 1 bird, with 1 yeast per field (x 1000 oil field) of which 30% were budding. In 1 bird with more than 3 RBCs per field (x 1000 oil field), 30% of bacteria present were gram-negative rods.

Discussion

Nutritional status

Mean concentrations of plasma calcium were only marginally lower in birds in this study than those of captive counterparts or other psittacine species. However, measures of total calcium are not indicative of the biologically active ionized form, (42) with the ionized portion ranging from 40% to 57% of total calcium concentration in SC cockatoos and LB corellas. (43) Ionized calcium and vitamin [D.sub.3] concentrations are evaluated in more detail in a separate study. (44) Although the phosphorous concentrations appear to be comparatively high, these values relate to total phosphorous and not to inorganic phosphate that is routinely measured by veterinary clinical pathology laboratories. These phosphorous concentrations were lower than those previously reported for other psittacine birds, (39) but results were possibly influenced by the ongoing drought in Victoria at the time of this study and the subsequent focus of birds on supplementary oats and commercial crops.

Copper toxicosis can arise from ingesting copper-coated wire products, but exposure to copper-based fungicides, causing testicular atrophy, can also be problematic. The higher plasma copper concentrations of female LB corellas and galahs (data not shown) are unlikely to have resulted from exposure to agricultural fungicides, in that these characteristics would be expected to be reflected in all 3 species. However, these results are higher than those reported for captive Hispanolan Amazon parrots, (39) implying variation by both sex and species in copper status of psittacine birds.

Iron storage disease is prevalent in many frugivorous and insectivorous birds maintained on commercially formulated foods. Various factors have been implicated in the development of this disease, including genetic predisposition, immunologic stress, viruses, and nutrition. Although iron toxicosis is most prevalent in frugivorous and insectivorous birds, it has also been reported in some psittacine species. (10,12,13) Plasma iron concentrations for birds in this study varied significantly, ranging from 36 to 215 [micro]mol/ L (201-1201 [micro]g/dL), with the mean value for SC cockatoos (109 [micro]mol/L; 609 [micro]g/dL) nearly twice that of LB corellas (57 [micro]mol/L; 318 [micro]g/dL). Temporal variation in plasma iron concentration was also detected in galahs, with autumn values nearly double those of winter. These higher values exceed serum levels reported in macaws (Ara species; 14.1-24.2 [micro]mol/L; 79-135 [micro]g/dL) (45) and Hispanolan Amazon parrots (40.3-112.0 [micro]mol/L; 225-626 [micro]g/dL). (1) Additionally, serum iron concentrations for affected sulfur-breasted toucans (Ramphastes sulfuratus; 62 [micro]mol/L; 343 [micro]g/dL) (45) equate to the lowest mean value for birds in this study, and concentrations reported for a greater Indian hill mynah (Gracula religiosa) suffering from hemochromatosis (161 [micro]mol/L; 899 [micro]g/dL) (6) were still within the reference range for Australian psittacine birds. Although the ideal serum iron concentrations in birds susceptible to iron storage disease might be less than 26.87 [micro]mol/L (150 [micro]g/ dL), (47) this value does not equate to that of birds evaluated in this study. Therefore, truly frugivorous or insectivorous birds could have comparatively lower dietary iron requirements.

Although biochemical iron levels and results of histologic analyses correlate well in channel-billed toucans (Ramphastos vitellinus), (48) it is generally accepted that blood iron concentrations are not indicative of liver stores. (8,14) Since organ biopsy is not always convenient or recommended in severely ill birds, a lack of correlation between blood and hepatic iron stores could result in erroneous diagnosis of iron toxicosis. Normal hepatic iron concentrations range between 100 and 300 mg/kg for most species, (8) but liver stores in this study (mean 417 mg/kg) were somewhat higher than values reported for psittacine birds from other labs (60 300 mg/kg). (13) However, concentrations were still lower than the 3750 mg/ kg reported for a hawk-headed parrot (Deroptyus accipitrinus) diagnosed with hemochromatosis (13) and rhamphastids exhibiting clinically normal signs (up to 26 000 mg/kg). (8) The data also do not support findings by Dierenfeld and Sheppard49 that granivorous birds have hepatic iron concentrations below 50 mg/kg, in that the lowest value recorded in this study was 110 mg/kg.

Taxonomic variation in hepatic iron concentrations could lead to erroneous diagnosis of iron toxicosis, (50) as highlighted in this study, with mean values for LB corellas more than double those of galahs. The data also emphasize the lack of correlation between blood and liver concentrations of iron; the species with the lowest plasma concentration (LB corellas) had the highest liver concentration. Although higher hepatic iron levels are associated with higher zinc levels in poultry, (51) similar correlations were not evidenced in this study.

Measures of plasma zinc concentrations are generally considered a poor indicator of zinc status. Hepatic zinc concentrations have been used to evaluate nutritional status of birds, especially if zinc toxicity is suspected. However, zinc concentration in most soft tissues varies little with nutritional status, with excess zinc stored in bone and only birds deprived of adequate zinc generally exhibiting low plasma levels. Normal serum zinc concentrations reported for parrots and chickens range between 7 38 [micro]mol/[L.sup.21] (45-248 [micro]/dL) and 30-46 [micro]mol/L (196-301 [micro]g/dL), (38) respectively. Mean plasma zinc concentrations of birds in this study fell within the range reported for parrots in general (7 38 [micro]mol/L; 45-248 [micro]/dL) (21) and clinically normal Hispafiolan parrots (19 35 [micro]mol/L; 124-228 [micro]g/dL). (1,19) However, values in this study were generally lower than values summarized for other clinically normal psittacine birds16.22-41 and were approximately 50% of values reported for wild-caught lorikeets. (16) Although values fell below those reported for other birds exhibiting signs of toxicosis (~150 [micro]mol/L [980 [micro]/dL] (16,22,41)), they still exceeded plasma and serum concentrations considered diagnostic for zinc toxicosis (30 [micro]mol/ L [196 [micro]/dL] (21,52-54)). This suggests that equating zinc toxicosis with plasma concentrations above 30 [micro]mol/L (196 [micro]g/dL) could lead to an erroneous diagnosis in some species. Doneley (16) also reported a lack of correlation between hepatic zinc concentrations and clinical diagnosis of zinc toxicosis, as evidenced in this study.

Biochemical analysis

Because of the variation in plasma biochemical values between species, the use of species-specific reference ranges are important in the accurate interpretation of plasma biochemical values. The few reports of species-specific reference ranges for Australian birds that are available are commonly derived from captive birds and often use analytic techniques not used as standard techniques in commercial laboratories, such as dry chemistry (55) or serum protein electrophoresis for determination of albumin and total globulin concentrations. (56) As such, the use of these reference ranges could result in a bias toward accepting "diseases of captivity" as clinically normal and might result in misinterpretation of data because of variations of means or sensitivity of differing analytic techniques. For these reasons, collecting reference data from healthy, wild-caught birds and developing reference ranges with the use of common commercial laboratory techniques is important.

Although protein status of birds is most commonly evaluated from plasma samples in commercial laboratories, reference ranges derived from electrophoresis of serum are commonly reported in texts, (56) with data for plasma protein electrophoresis less commonly reported. (57_ However, protein data from serum and plasma are not interchangeable, and it is necessary to highlight which portion of the blood has been evaluated. Results from this study indicate that plasma total protein and albumin concentrations are lower than previously reported ranges. (57) This might reflect differences in the sample population, either because a single species was assessed (the ranges depicted in Table 7 for galahs and SC cockatoos from other studies are not species specific) or reflecting differences in the management and diets of the sample group (wild versus presumed captive birds). In a study comparing laboratory values between wild-reared and hand-reared macaws, total protein and albumin concentrations were lower in captive-reared birds, but no dietary analysis was provided and no inferences discussed?8 In our study, the 3 species exhibited similar ranges of globulin values, in contrast with the relatively wide variations previously reported. This might reflect the consistency of a single methodology used in the current study.

Uric acid concentration ranges were significantly higher in the birds in our study than those previously reported. These higher values are unlikely to have been caused by acute dehydration (59) because urea concentrations were lower than previously reported values. (25) Furthermore, toxic levels of zinc, a known cause of high plasma uric acid concentrations, were not evident in these birds. (60) Because there is no evidence of previously reported values being derived from fasted birds, it is also unlikely that this variation is caused by an increase in uric acid concentration in postprandial birds. (3,61,62) Mean plasma urea concentration was lower than that previously reported for cockatoos. As suggested with measurements of protein status, this might reflect differences in the sample population, including age (values could be significantly higher in young birds than in adult birds (58)), analysis of a single species, or dietary effects.

Because capture and restraint were expected to result in significant muscle trauma and, hence, significant increases in creatinine kinase, aspartate aminotransferase, and alanine aminotransferase concentrations, our assessment of hepatic enzymes was limited in this study, as demonstrated by analysis of representative samples from each species (data not shown). Glutamate dehydrogenase is considered the most liver specific enzyme in birds, with low concentrations in muscle (23,63); hence, it was predicted to exhibit minimal increase with the expected muscle trauma. Previously quoted reference ranges of GLDH for cockatoos are psittacine reference ranges,24,25 and some variation between species is expected. Because these data were developed outside of Australia, (24) it is likely that few, if any, Australian species were included in the reference group. A published reference range for another Australian species, the cockatiel (Nymphicus hollandicus), of 0-8 IU/L, (64) is more consistent with the reference ranges derived in our study. This apparent variation between Australian and other bird species is unexplained. The total bile acid reference ranges determined in our study tended to be lower than those previously reported, which might reflect a possible lower incidence of hepatopathy in the wild bird group or variations in analytic methods.

Amylase reference ranges in the current study were significantly higher than those previously reported for cockatoos. As with uric acid, there was no evidence of zinc toxicosis in the study group; thus, zinc-associated pancreatic disease is unlikely to have caused increases in amylase concentration, as has been previously reported .23'60 No gross evidence of pancreatic disease was identified in any bird at postmortem examination, nor was significant leukocytosis or heterophilia identified in a separate study of SC cockatoos (data not shown). However, histopathologic evaluation of the pancreas was not done. As discussed above, plasma calcium reference ranges were lower than those previously described for this species. Cholesterol values were higher than reference ranges derived from birds outside of Australiaz3 but were similar to those previously reported in Australian-held birds of 3.0 9.4 mmol/ L [116-363 mg/dL], 3.2-11.6 mmol/L [124-449 mg/dL], and 4.8 10.0 mmol/L [186-387 mg/ dE] in SC cockatoos, galahs, and little corellas (Cacatua sanguinea), respectively?5 The reason for this variation between data derived from the same species held in differing geographic locations is unclear.

Although not definitive in making a diagnosis, a fecal Gram's stain provides a visual screen of the proportions of bacteria present in the gastrointestinal tract at the time of sampling. The presence of specific Enterobacter species in avian feces has been correlated with the consumption of seeds containing more than 106 bacteria/g food. (30) Conversion of African grey parrots (Psittacus erithacus) from a typical seed-based diet to a nutritionally balanced, formulated diet is correlated with a reduction in fecal gram-negative bacteria.65 Although only a small number of birds were evaluated in this study, preliminary evidence suggests that there is a distinct absence of both gram-negative bacteria and budding yeasts in feces in wild Australian psittacine birds. However, this warrants further investigation in a larger sample size and a variety of species.

From the results of this study, it is evident that values of analytes used to determine health and nutritional status of wild birds differ from those published for captive counterparts. Although the analytes we studied appear to vary minimally by sex, distinct taxonomic and some temporal differences exist that need to be considered when evaluating patients. Further studies on a greater number of species in the wild are required to continue development of a reference database for clinicians.

Acknowledgments: We acknowledge funding from HBD International and Idexx Laboratories for laboratory expenses. Staff members from the Cockatoo Mitigation Project of the Department of Natural Resources and Environment (DNRE) were instrumental in coordinating access to birds in the field, and their input is gratefully acknowledged. Birds were obtained under DNRE scientific research permit number 10001736.

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Debra L. McDonald, PhD, Susan Jaensch, BVSM, PhD, Greg J. Harrison, DVM, Dipl ABVP (Avian), Dipl ECAMS (Avian), Stacey Gelis, DVM, David Brennan, Phil Sacks, DVM, and Domenico Bernardo, BSc

From the Australian Institute of Zoo Nutrition, PO Box 1064, Healesville, Victoria, Australia 3777 (McDonald, Bernardo); IDEXX Laboratories, PO Box 227, Rydalmere, NSW, Australia 2116 (Jaensch); 3610 S Ocean, Unit 601, Palm Beach, FL 33480, USA (Harrison); PO Box 580, Coolum Beach, Queensland, Australia 4573 (Gelis); the Department of Sustainability and Environment, Private Bag 260, Horsham, Victoria, Australia 3400 (Brennan); and Highbury Veterinary Clinic, 128 Highbury Rd, Burwood, Victoria, Australia 3125 (Sacks).
Table 1. Weights (mean [+ or -] SD, range) for 3 species of wild
Australian psittacine birds that were evaluated for hepatic and
plasma mineral and biochemical content.

                                   Weight, g

Species                     Male             Female

Galah                 359 [+ or -] 18   317 [+ or -] 19
                         (335-392)         (288-350)
Long-billed corella   614 [+ or -] 54   556 [+ or -] 45
                         (560-698)         (498-640)
Sulphur-crested       900 [+ or -] 55   780 [+ or -] 56
cockatoo                 (770-994)         (650-900)

Table 2. Concentrations (mean [+ or -] SD, range) of plasma
macrominerals in 3 species of wild Australian psittacine birds.

           Mineral                          Galah (n = 17)

Calcium, mmol/L [mg/dL]           1.8 [+ or -] 0.2 [7.2 { 0.8]
                                           1.5-2.2 [6.0-8.8]
Magnesium, mmol/L [mg/dL]         0.8 [+ or -] 0.1 [1.9 [+ or -] 0.2]
                                           0.7-1.2 [1.7-2.9]
Total phosphorus, mmol/L [mg/     6.9 [+ or -] 2.0 [21.4 [+ or -] 6.2]
  dL]                                     3.6-13.2 [11.1-40.8]
Potassium, mmol/L [mEq/L]        10.3 [+ or -] 3.6 [6.7-19.0]
Sodium, mmol/L [mEq/L]          106.0 [+ or -] 4.7 [98.8-114.0]

           Mineral                   Long-billed corella (n = 13)

Calcium, mmol/L [mg/dL]          1.7 [+ or -] 0.1 [6.8 [+ or -] 0.4]
                                          1.6-1.9 [6.4-7.6]
Magnesium, mmol/L [mg/dL]        0.7 [+ or -] 0.1 [1.7 [+ or -] 0.2]
                                          0.6-0.8 [1.5-1.9]
Total phosphorus, mmol/L [mg/    7.0 [+ or -] 1.5 [21.7 [+ or -] 4.6]
  dL]                                    3.9-10.2 [12.1-31.6]
Potassium, mmol/L [mEq/L]        8.0 [+ or -] 0.7 [7.2-10.0]
Sodium, mmol/L [mEq/L]          108.0 [+ or -] 6.6 [92.0-115.0]

           Mineral                Sulphur-crested cockatoo (n = 23)

Calcium, mmol/L [mg/dL]          1.8 [+ or -] 0.3 [7.2 [+ or -] 1.2]
                                               0.8-2.1 [3.2-8.4]
Magnesium, mmol/L [mg/dL]        0.9 [+ or -] 0.2 [2.2 [+ or -] 0.5]
                                               0.4-1.2 [1.0-2.9]
Total phosphorus, mmol/L [mg/   5.7 [+ or -] 1.4 [17.7 [+ or -] 4.3]
  dL]                                          2.0-9.7 [6.1-30.0]
Potassium, mmol/L [mEq/L]             8.3 [+ or -] 1.6 [2.8-10.5]
Sodium, mmol/L [mEq/L]              95.4 [+ or -] 11.0 [47.9-106.0]

Table 3. Concentrations of plasma microminerals (mean [+ or -]
SD, range) in 3 species of wild Australian psittacine birds.

Mineral                                 Galah (n = 17)

Copper, [micro]mol/L        3.4 [+ or -] 0.6 [21.6 [+ or -] 3.8] (a)
  [[microg]g/dL]
                                     1.9-4.6 [12.1-29.2]

Iron, [micro]mol/L       90.0  [+ or -] 49.0 [502 [+ or -] 106]
  [[microg]g/dL]
                                  38.0-174.0 [805-972]

Lead, [micro]mol/L        0.30 [+ or -] 0.03 [6.2 [+ or -] 0.6]
  [[microg]g/dL]
                                   0.20-0.30 [4.1-6.2]

Selenium, [micro]mol/L     11.9 [+ or -] 2.5 [937 [+ or -] 197]
  [[microg]/L]
                                    7.6-16.5 [598-1299]

Zinc, [micro]mol/L         28.5 [+ or -] 6.7 [186 [+ or -] 44]
  [[microg]/L]
                         18.4  [+ or -] 41.3 [120-2691

Mineral                         Long-billed corella (n = 13)

Copper, [micro]mol/L       3.9 [+ or -] 1.4 [24.8 [+ or -] 8.9 (a)
  [[microg]g/dL]
                                    2.2-7.9 [14.0-50.21

Iron, [micro]mol/L       57.0 [+ or -] 20.6 [318 [+ or -] 1151
  [[microg]g/dL]
                                 36.0-102.0 [201-570]

Lead, [micro]mol/L       0.40 [+ or -] 0.10 [8.3 [+ or -] 2.1]
  [[microg]g/dL]
                                  0.20-0.50 [4.1-10.4]

Selenium, [micro]mol/L    12.9 [+ or -] 4.0 [1016 [+ or -] 315]
  [[microg]/L]
                                   7.6-21.5 [598-1693]

Zinc, [micro]mol/L        29.8 [+ or -] 7.8 [195 [+ or -] 511
  [[microg]/L]
                                  18.4-44.4 [120-290]

Mineral                     Sulphur-crested cockatoo (n = 23)

Copper, [micro]mol/L       2.9 [+ or -] 0.8 [18.4 [+ or -] 5.11
  [[microg]g/dL]
                                          1.1-5.2 [7.0-33.01

Iron, [micro]mol/L       109.0 [+ or -] 50.0 [609 [+ or -] 279]
  [[microg]g/dL]
                                       37.0-215.0 [207-1201]

Lead, [micro]mol/L                        n.d.
  [[microg]g/dL]

Selenium, [micro]mol/L     10.6 [+ or -] 2.9 [835 [+ or -] 228]
  [[microg]/L]
                                    3.8-16.5 [299-1299]

Zinc, [micro]mol/L         35.3 [+ or -] 8.1 [231 [+ or -]531
  [[microg]/L]
                                   16.8-50.5 [110-330]

Abbreviation: n.d. indicates not done.

(a) an = 6.

Table 4. Concentrations of hepatic macrominerals (mean [+ or -]
SD, range) in 3 species of wild Australian psittacine birds.

Mineral                     Galah (n = 17)

Calcium, mg/kg             39 [+ or -] 8 (23-49)
Magnesium, mg/kg       223 [+ or -] 14 (200-240)
Phophorus, mg/kg      3219 [+ or -] 158(2910-3510)
Potassium, mg/kg     872 [+ or -] 188 (2600-3200)
Sodium, mg/kg         831 [+ or -] 65 (710-930)
Sulfur, mg/kg       2709 [+ or -] 2330 (2320-3120)

Mineral             Long-billed corella (n = 13)

Calcium, mg/kg           44 [+ or -] 9 (29-64)
Magnesium, mg/kg      216 [+ or -] 13 (190-240)
Phophorus, mg/kg   3102 [+ or -] 163 (2870-3360)
Potassium, mg/kg   2665 [+ or -] 255 (2200-2930)
Sodium, mg/kg       962 [+ or -] 118 (800-1190)
Sulfur, mg/kg      2448 [+ or -] 147 (2220-2670)

Mineral            Sulphur-crested cockatoo (n = 24)

Calcium, mg/kg           39 [+ or -] 6 (29-49)
Magnesium, mg/kg       218 [+ or -] 12 (190-240)
Phophorus, mg/kg     3114 [+ or -] 177 (2700-3390)
Potassium, mg/kg     2768 [+ or -] 166 (2460-3050)
Sodium, mg/kg          842 [+ or -] 97 (690-1180)
Sulfur, mg/kg        2889 [+ or -] 189 (2390-3170)

Table 5. Concentrations (mean [+ or -] SD, range) of hepatic
microminerals in 3 species of wild Australian psittacine birds.

Mineral                    Galah (n = 17)

Copper, mg/kg        4.7 [+ or -] 0.4 (3.8-5.4)
Iron, mg/kg          254 [+ or -] 86 (140-460)
Lead, mg/kg        0.06 [+ or -] 0.04 (0.03-0.14)
Manganese, mg/kg     4.7 [+ or -] 0.8 (3.3-6.3)
Selenium, mg/kg      0.7 [+ or -] 0.2 (0.4-0.9)
Zinc, mg/kg        32.0 [+ or -] 5.5 (24.0-45.0)

Mineral             Long-billed corella (n = 13)

Copper, mg/kg        3.8 [+ or -] 0.4 (3.0-4.3)
Iron, mg/kg         609 [+ or -] 224 (360-1030)
Lead, mg/kg        0.07 [+ or -] 0.02 (0.04-0.10)
Manganese, mg/kg     5.5 [+ or -] 1.5 (3.3-8.6)
Selenium, mg/kg      0.7 [+ or -] 0.2 (0.5-0.9)
Zinc, mg/kg        37.3 [+ or -] 9.8 (29.0-64.0)

Mineral            Sulphur-crested cockatoo (n = 24)

Copper, mg/kg         4.9 [+ or -] 0.6 (4.1-6.0)
Iron, mg/kg           382 [+ or -] 187 (110-790)
Lead, mg/kg                      n.d.
Manganese, mg/kg      4.3 [+ or -] 0.7 (2.6-5.6)
Selenium, mg/kg       1.2 [+ or -] 0.3 (0.1-1.6)
Zinc, mg/kg          37.6 [+ or -] 7.9 (25.0-59.0)

Abbreviation: n.d. indicates not done.

Table 6. Hepatic zinc concentrations (mean [+ or -] SD, range) in
3 species of wild Australian psittacine birds compared with
concentrations reported in captive psittacine birds. Data are
listed as physiologic (normal) or as clinical toxicosis.

                                        Zinc, mg/kg

Species                    Physiologic             Toxicosis

Budgerigar (22) (n =    50.5 [+ or -] 12.7        153.0-250.0
10)                        (37.6-70.5)

Budgerigar (aviary      64.7 [+ or -] 37.0             --
bred) '6(n = 8)            (29.0-126.0)

Monk parakeet (41)      57.9 [+ or -] 34.5    179.0 [+ or -] 73.7
(Myiopsitta                (28.1-156.0)             (n = 7)
monachus) (n = 14)

Lovebird (15)           42.5 [+ or -] 8.9          75.0-156.0
(Agapornis                 (37.5-50.2)
roseicolli) (n = 5)

Macaw (41) (Ara         38.9 [+ or -] 22.0    150.0 [+ or -] 37.0
chloroptera, Ara           (12.0-115.0)             (n = 3)
macao) (n = 77)

Rosella and lorikeet    74.0 [+ or -] 63.0             --
(16) (n = 4)               (27.0-166.0)

Galah (n = 16)          31.6 [+ or -] 5.4              --
                           (24.0-45.0)

Sulphur-crested         37.5 [+ or -] 7.8              --
cockatoo (n = 21)          (25.0-59.0)

Long-billed corella     37.3 [+ or -] 9.8              --
(n = 13)                   (29.0-64.0)

Table 7. Plasma biochemical reference ranges in 3 species of wild
Australian psittacine birds. Previously published data are
presented in parentheses.

                            Long-billed corella (n = 16)

Albumin, g/L [g/dL]            7-13 [0.7-1.3]
                               (16-20 [1.6-2.0] (a))
Amylase, IU                    326-1083
                               (228-876 (c))
Total bile acids, pmol/L       4-90
                               (26-96 (c))
Calcium, mmol/L                1.75-2.23
                               (2.02-2.96 (a))
Cholesterol, mmol/L            4.3-9.2
                               (4.5-5.8 (a))
Globulin, g/L [g/dL]           14-21 [1.4-2.1]
                               (11-14 [1.1-1.4] (a))
Glucose, mmol/L                13.2-27.7
                               (12.2-21.0 (a))
Glutamate dehydrogenase,       0-6.1
                               (>2 (d))
Total protein, g/L [g/dL]      21-32 [2.1-3.2]
                               (26-38 [2.6-3.8] (a))
Urea, mmol/L                   0.30-0.80
                               (0.8-2.11)
Uric acid, mmol/L              0.26-0.70
                               (0.18-0.6 (a))

                            Galah (n = 15)

Albumin, g/L [g/dL]            6-11 [0.6-1.1]
                               (16-18310-11941 [1.6-1.8] (b))
Amylase, IU
                               (228-876 (c))
Total bile acids, pmol/L       18-85
                               (101-148 (b))
Calcium, mmol/L                1.64-2.26
                               (2.10-2.27 (b))
Cholesterol, mmol/L            5.3-7.9
                               (3.8-5.86)
Globulin, g/L [g/dL]           14-22 [1.4-2.2]
                               (10-22 [1.0-2.2] (b))
Glucose, mmol/L                7.6-27.1
                               (11.0-2.096)
Glutamate dehydrogenase,       1.7-6.9
                               (<2 (d))
Total protein, g/L [g/dL]      22-31 [2.2-3.1]
                               (24-45 [2.4-4.5] (b))
Urea, mmol/L                   0.60-1.70
                               (-0.8-2.1 (e))
Uric acid, mmol/L              0.45-0.95
                               (0.23-0.64 (b))

                            Sulphur-crested cockatoo (n = 31)

Albumin, g/L [g/dL]            8-16 [0.8-1.6]
                               (12-24 [1.2-2.4] (c))
Amylase, IU                    170-2170
                               (228-876 (c))
Total bile acids, pmol/L       -80
                               (34-112 (c))
Calcium, mmol/L                1.83-2.31
                               (2.05-2.86 (c))
Cholesterol, mmol/L            3.5-7.3
                               (2.5-5.5 (c))
Globulin, g/L [g/dL]           13-24 [1.3-2.4]
                               (20-34 [2.0-3.4] (c))
Glucose, mmol/L                7.4-22.7
                               (11.4-23.2 (c))
Glutamate dehydrogenase,       0.7-4.3 (<2 (d))

Total protein, g/L [g/dL]      21-39 [2.1-3.9]
                               (26-48 [2.611.5] (c))
Urea, mmol/L                   0.45-1.13
                               (0.8-2.1 (c))
Uric acid, mmol/L              0.16-1.04
                               (0.26-0.65 (c))

(a) Corella reference range. (23)

(b) Galah reference range. (23)

(c) Generic cockatoo range. (23)

(d) Psittacine range. (25)

(e) Generic cockatoo range. (25)
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Title Annotation:Original Studies
Author:McDonald, Debra L.; Jaensch, Susan; Harrison, Greg J.; Gelis, Stacey; Brennan, David; Sacks, Phil; B
Publication:Journal of Avian Medicine and Surgery
Article Type:Report
Geographic Code:8AUST
Date:Dec 1, 2010
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