Hematological and Biochemical Parameters of Captive

Andean Condors
Author(s): Daniela Doussang and Cristina Palma Lucila Moreno Brayan
Zambrano Eduardo Pavéz Fabiola Cerda Daniel González-Acuña
Source: Journal of Raptor Research, 52(1):72-81.
Published By: The Raptor Research Foundation
https://doi.org/10.3356/JRR-16-14.1
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J. Raptor Res. 52(1):72–81
Ó 2018 The Raptor Research Foundation, Inc.

HEMATOLOGICAL AND BIOCHEMICAL PARAMETERS OF CAPTIVE

ANDEAN CONDORS
DANIELA DOUSSANG AND CRISTINA PALMA
Universidad de Concepción, Facultad de Ciencias Veterinarias, Casilla 537, Chillán, Biobı́o, Postal code 3810024,
Chile

LUCILA MORENO
Universidad de Concepción, Facultad de Ciencias Naturales y Oceanográficas, Concepción, Biobı́o, Postal code
4030000, Chile

BRAYAN ZAMBRANO
Universidad Andrés Bello, Facultad de Ecologı́a y Recursos Naturales, Casilla 444, Santiago, Postal code 8370146
Chile

EDUARDO PAVÉZ
Bioamérica Consultores, Chile

FABIOLA CERDA
Facultad de Ciencias de la Salud y los Alimentos, Universidad del Biobı́o, Chile

DANIEL GONZÁLEZ-ACUÑA1
Universidad de Concepción, Facultad de Ciencias Veterinarias, Casilla 537, Chillán, Biobı́o, Postal code 3810024,
Chile

ABSTRACT.—Hematological and biochemical parameters are used to assess the health of birds and to support
conservation plans for threatened species, such as the Andean Condor (Vultur gryphus). We studied 22
captive Andean Condors from the Rehabilitation Center for Raptors of the Unión de Ornitólogos of Chile to
determine reference values. We measured packed cell volume, total plasma solids, and total and differential
leukocyte counts; we analyzed aspartate aminotransferase, gamma-glutamyl transpeptidase, lactate
dehydrogenase, alkaline phosphatase, creatine kinase, creatinine, calcium, inorganic phosphorus, and uric
acid. We found no blood parasites and no significant differences between sexes (P . 0.05). Our results
establish a baseline for hematological and serum biochemistry parameters for the Andean Condor.

KEY WORDS: Andean Condor; Vultur gryphus; biochemistry; captivity; hematology; parameter; reference values.

PARÁMETROS HEMATOLÓGICOS Y BIOQUÍMICOS DE VULTUR GRYPHUS EN CAUTIVIDAD

RESUMEN.—Los parámetros hematológicos y bioquı́micos se usan para evaluar la salud de las aves y para
apoyar los planes de conservación de especies amenazadas como Vultur gryphus. Se estudiaron 22 individuos
de Vultur gryphus en cautividad mantenidos en el Centro de Rehabilitación de Aves Rapaces de la Unión de
Ornitólogos de Chile, para determinar valores de referencia. Medimos el volumen celular, los sólidos
plasmáticos totales y el recuento total y diferencial de leucocitos. Analizamos aspartato aminotransferasa,
gamma-glutamil transpeptidasa, lactato deshidrogenasa, fosfatasa alcalina, creatina quinasa, creatinina,
calcio, fósforo inorgánico y ácido úrico. No encontramos parásitos sanguı́neos ni diferencias significativas
entre sexos (P . 0.05). Los resultados obtenidos en este estudio establecen una referencia para los
parámetros hematológicos y de bioquı́mica sérica para esta especie.
[Traducción del equipo editorial]

1
Email address: [email protected]

72
MARCH 2018 HEMATOLOGY OF CAPTIVE ANDEAN CONDORS 73

The Andean Condor (Vultur gryphus) is a mono- 2005). In this study, conditions such as habitat, diet,
typic species. It is distributed in the Andes Moun- and veterinary management were the same for all
tains, from Venezuela to Cape Horn (Martı́nez and individuals sampled.
González 2005). It is an uncommon, nearly threat- Sample Analysis. We measured packed cell volume
ened species (BirdLife International 2012), and has (PCV; %) from the microhematocrit tubes (Hirsch-
been protected in Chile since 1929 (Law No. 4601 of mann Laborgeräte GmbH & CO. KG, Eberstadt,
1929 and Law No. 40 of 1972, Republic of Chile). Germany) after centrifuging for 4 min at 14,490 3 g
The status of populations is difficult to determine, in a microhematocrit centrifuge (Campbell and
but it is probably declining (BirdLife International Coles 1986; Digital micro centrifuge, KHT-410E,
2012). Taipei, Taiwan, Republic of China). We determined
Serum biochemistry and hematology are the basis total plasma solids (TPS; g/L) using Goldberg’s
of medical diagnosis of diseases (Harr 2002). refractometer (Golberg TS Meter Clinical Refrac-
Clinical parameters of Andean Condors have been tometer, Reichert Analytical Instrument, New York,
measured in captive (Balasch et al. 1976, Gee et al. NY U.S.A.). We calculated white blood cell (WBC;
1981, Toro et al. 1997) and wild populations (Toro x109/L) using a Neubauer chamber (Brand GmbH
et al. 1997), but these studies lack some important & Co. KG, Wertheim, Germany) and a modified
parameters. In this study, we report baseline version of the Rees and Ecker solution (Lucas and
hematologic and blood chemistry values for Andean Jamroz 1961).
Condors, which could be used to assess the health of We stained blood smears with Diff-Quickt (Roma-
individuals in captivity. nowski stain variant, Quick Panoptic, Quı́mica
Clı́nica Analı́tica, Barcelona, Spain). We performed
METHODS a differential white blood cell count by counting 200
Sample Collection. In January 2015, we studied 22 leukocytes by oil immersion microscopy (Merck
captive Andean Condor (10 adult females, seven KGaA, Darmstadt, Germany) at 10003 magnification
adult males, and five immature birds) from the (Microscopy Zeiss Primo Star, Carl Zeiss Inc.,
Rehabilitation Center for Raptors of the Unión de Oberkochen, Germany). We determined the pres-
Ornitólogos de Chile, city of Talagante (33840.0 0 S, ence of blood parasites in the stained smear by oil
70856.0 0 W). Adult birds were 5–29 yr old, and immersion at 10003 magnification (Merino et al.
immatures 1–4 yr old. The Andean Condors were 1997; Microscopy Zeiss Primo Star, Carl Zeiss Inc.,
fed either chicken (Gallus gallus domesticus) or day- Oberkochen, Germany).
old chicks once a day, and water was provided ad We centrifuged the blood samples at 2500 3 g for
libitum. We collected 4 ml of blood from the 10 min (Centrifuge DSC 200A-2, Already Enterprise
metatarsal vein of each condor using sterile syringes Inc., Taipei, Taiwan, Republic of China) and
with 21-gauge needles, and transferred the samples obtained serum for blood chemistry analyses. We
to Vacutainert tubes with ethylenediaminetetraace- determined gamma-glutamyl transpeptidase (GGT;
tic acid (EDTA) as an anticoagulant (Becton, Dick- U/L), aspartate aminotransferase (AST; U/L),
inson and Company, Franklin Lakes, NJ U.S.A.), and lactate dehydrogenase (LDH; U/L), alkaline phos-
plain Vacutainert tubes (Becton, Dickinson and phatase (AP; U/L), creatine kinase (CK: U/L),
Company, Plymouth, U.K.) for hematology and creatinine (CRE; lmol/L), calcium (Ca; mmol/L),
biochemistry analyses, respectively. We collected inorganic phosphorus (Phos; mmol/L), and uric
blood samples between 1200 and 1500 H to avoid acid (UA: lmol/L) using a commercial test (DiaSys
variations in the blood parameters due to the Diagnostic Systems GmbH, Alte Strasse 9, Holzheim,
circadian rhythm (Garcı́a-Rodrı́guez et al. 1987). Germany). The AST, LDH, Phos, and CK were read
We stored samples at 48C, and analyzed them within at 340 nm wavelength, GGT and AP at 405 nm, CRE
12 hr of collection at the Clinical Laboratory of the at 546 nm, Ca at 570 nm, and UA at 520 nm in a
Facultad de Ciencias Veterinarias, Universidad de spectrophotometer (Wiener lab, MetroLAB 2300
Concepción. We used serum for biochemical anal- Plus, UV-Vis Metrolab S.A., Buenos Aires, Argenti-
yses and whole blood for hematological analysis. A na).
veterinarian physically evaluated all Andean Con- Statistical Analysis. We tested normality with the
dors included in this study and considered all to be Anderson-Darling test (RefValAdv, National Veteri-
clinically healthy. We determined age and sex of nary School, Toulouse, France). Many analytes were
each bird by plumage (Martı́nez and González not normally distributed, and data were transformed
74 DOUSSANG ET AL. VOL. 52, NO. 1

Table 1. Hematological parameters of Andean Condor juveniles (n ¼ 5), from the Rehabilitation Center for Raptors of
the Unión de Ornitólogos de Chile, Talagante, Chile.

ANALYTE MEAN SD MINIMUM MAXIMUM

a
PCV (%) 46.2 4.1 42.0 51.0
TPSb (g/L) 44.0 4.0 38.0 48.0
WBCc (3109/L) 8.9 1.4 6.6 10.1
Heterophil (3109/L) ND 1.1 5.6 8.0
Lymphocytes (3109/L) 0.6 0.2 0.1 1.6
Monocyte (3109/L) 0.9 0.3 0.5 1.2
Eosinophils (3109/L) 0.0 0.0 0.0 0.1
Basophils (3109/L) 0.0 0.1 0.0 0.2
a
PCV ¼ packed cell volume.
b
TPS ¼ total plasma solids.
c
WBC ¼ white blood cell count.

to approximate a normal distribution using the Box- RESULTS

Cox transformation. This transformation is a family Hematology and blood chemistry values of An-
of transformations expressed by the equation: dean Condors did not differ between males and
females (P ¼ 0.9883; Tables 1–4). We did not find
Y ðkÞ ¼ ðY k  1Þ=kðfor k „ 0Þ blood parasites in the blood smears.

Y ðkÞ ¼ loge ðY Þðfor k ¼ 0Þ DISCUSSION

This study established baseline reference intervals
where k is the number that maximizes the log- for common serum biochemical and hematological
likelihood function: parameters in healthy captive Andean Condors and
v vX n evaluated sex-related differences. Many of hemato-
L ¼  loge ðST2 Þ þ ðk  1Þ loge y logical and biochemical ranges recorded in this
2 n i¼1
study were within the values given in literature for
where m is the degrees of freedom, n is the sample Andean Condors (Table 5). However, there are
size, and ST2 is the variance of the transformed values some hematological parameters recorded in this
of Y (Gotelli and Ellison 2004). study with variations outside the ranges observed for
We assessed outliers using a strict Dixon’s test and other raptors. These variations could be attributed
to characteristics of the species, nutritional status,
excluded data identified as outliers and suspect
environmental variables, conditions of captivity, age,
outliers from subsequent calculation RefValAdv.
sex, social structure, health status, and techniques
However, after analysis of the residuals from the
used for sample analysis (Clark et al. 2009). With
transformed data, the heterogeneity of the variance
respect to this issue, other studies indicate some
was not reduced with any transformation; therefore,
parameters are affected by the use of EDTA. For
we treated those variables as ordinal. We determined
example, plasma protein and PCV values were
nonparametric reference intervals using a bootstrap significantly lower in samples with lithium heparin
method. than in those with K2EDTA, whereas lymphocyte
We determined reference intervals and 90% confi- numbers were significantly higher in lithium hepa-
dence intervals of the limits using the RefValAdv. rin samples than in K2EDTA samples (Sanchez-
We used MANOVA on the normal data to detect Migallon et al. 2008). We recommend using the
differences between sexes with JMPt7.0.1 (SAS same anticoagulant to follow trends within the same
Institute). The sample size for immatures (n ¼ 5) individual, especially when considering plasma
was too small to assess whether values differed protein concentration, PCV, and lymphocyte count
from adults. All statistical findings were consid- (Sanchez-Migallon et al. 2008). However, EDTA has
ered significant at P  0.05. Data are expressed as little effect on cell morphology and produces fewer
mean 6 standard deviation (SD), minimum and staining artifacts. It is the anticoagulant of choice in
maximum. hematology to conserve samples for short periods of
MARCH 2018 HEMATOLOGY OF CAPTIVE ANDEAN CONDORS 75

Table 2. Hematological parameters of Andean Condor adults (seven males and 10 females), from the Rehabilitation
Center for Raptors of the Unión de Ornitólogos de Chile, Talagante, Chile.

ANALYTE SEX MEAN SD MINIMUM MAXIMUM

a
PCV (%) Male 47.3 2.9 41.0 49.0
Female 46.6 2.9 41.0 51.0
TPSb (g/L) Male 46.0 2.8 42.0 50.0
Female 45.6 4.8 38.0 50.0
WBCc (3109/L) Male 7.0 2.4 3.1 10.4
Female 7.0 1.4 5.2 9.8
Heterophil (3109/L) Male 5.6 1.7 2.7 7.8
Female 5.9 1.1 4.5 7.5
Lymphocytes (3109/L) Male 0.6 0.5 0.1 1.5
Female 0.5 0.4 0.1 1.2
Monocyte (3109/L) Male 0.7 0.3 0.2 1.0
Female 0.5 0.3 0.2 1.0
Eosinophils (3109/L) Male 0.0 0.0 0.0 0.1
Female 0.0 0.0 0.0 0.1
Basophils (3109/L) Male 0.1 0.1 0.0 0.3
Female 0.1 0.1 0.0 0.1
a
PCV ¼ packed cell volume.
b
TPS ¼ total plasma solids.
c
WBC ¼ white blood cell count.

time. However, in very small samples, EDTA causes for captive Andean Condors by Balasch et al. (1976)
hemolysis (Beynon and Cooper 1999), which did not and Gee et al. (1981; Table 5). The season in which
occur in our study because the blood samples were samples were collected could explain these differ-
fairly large (4 ml). ences. Balasch et al. (1976) collected samples in
Mean values for PCV were within the normal range winter, Gee et al. (1981) collected samples in
(35–55%) reported for bird species in general autumn, and we collected samples in summer. The
(Campbell 1994), but higher than those described hydration status and water availability are important

Table 3. Biochemical parameters of Andean Condor juveniles (n ¼ 5), from the Rehabilitation Center for Raptors of the
Unión de Ornitólogos de Chile, Talagante, Chile.

ANALYTE MEAN SD MINIMUM MAXIMUM

a
Ca (mmol/L) 3.1 0.2 2.8 3.4
Phosb (mmol/L) 1.6 0.6 0.9 2.4
UAc (lmol/L) 452.4 181.7 281.7 761.9
CKd (U/L) 509.8 97.0 403.7 617.8
CREe (lmol/L) 25.1 12.7 9.4 42.0
LDHf (U/L) 456.8 78.3 378.8 546.0
GGTg (U/L) 6.1 2.8 2.5 9.8
APh (U/L) 291.3 155.5 143.9 536.2
ASTi (U/L) 11.4 3.1 7.6 16.0
a
Ca ¼ calcium.
b
Phos ¼ inorganic phosphorus.
c
UA ¼ uric acid.
d
CK ¼ creatine kinase.
e
CRE ¼ creatinine.
f
LDH ¼ lactate deshidrogenase.
g
GGT ¼ gamma-glutamyl transpeptidase.
h
AP ¼ alkaline phosphatase.
i
AST ¼ aspartate aminotransferase.
76 DOUSSANG ET AL. VOL. 52, NO. 1

Table 4. Biochemical parameters of Andean Condor adults from the Rehabilitation Center for Raptors of the Unión de
Ornitólogos de Chile, Talagante, Chile.

ANALYTE SEX n MEAN SD MINIMUM MAXIMUM

a
Ca (mmol/L) Male 6 2.7 0.2 2.4 2.9
Female 8 2.8 0.1 2.6 2.9
Phosb (mmol/L) Male 7 1.5 0.5 0.9 2.3
Female 9 1.4 0.4 1.0 2.0
UAc (lmol/L) Male 7 305.1 103.6 180.8 449.0
Female 9 309.0 66.6 226.5 445.8
CKd (U/L) Male 7 362.5 66.6 231.4 447.7
Female 9 346.2 75.6 243.7 501.5
CREe (lmol/L) Male 7 28.3 6.4 18.9 36.2
Female 10 31.6 15.5 14.3 62.8
LDHf (U/L) Male 7 361.0 93.3 249.9 530.3
Female 10 356.7 71.8 256.1 478.2
GGTg (U/L) Male 6 4.9 2.3 2.2 7.1
Female 9 5.9 2.3 2.0 10.1
APh (U/L) Male 7 100.2 29.5 66.8 153.6
Female 10 150.0 87.8 81.8 359.8
ASTi (U/L) Male 7 6.9 2.2 3.6 9.6
Female 9 6.9 1.7 4.1 9.4
a
Ca ¼ calcium.
b
Phos ¼ inorganic phosphorus.
c
UA ¼ uric acid.
d
CK ¼ creatine kinase.
e
CRE ¼ creatinine.
f
LDH ¼ lactate deshidrogenase.
g
GGT ¼ gamma-glutamyl transpeptidase.
h
AP ¼ alkaline phosphatase.
i
AST ¼ aspartate aminotransferase.

factors to consider when interpreting PCV values, as 1976, Gee et al. 1981; Table 5) and for other species
high levels of PCV may indicate dehydration (Smith of vultures (Balasch et al. 1976, Coleman et al. 1988,
and Bush 1978). Although our values were higher, Polo et al. 1992, Dell’Omo and Cavallina 1996,
they were within the normal ranges reported for Dobado-Berrı́os and Tella 1998, Dujowich et al.
other species of free-living vultures (Coleman et al. 2005, Hernández and Margalida 2010). Moreover,
1988, Hernández and Margalida 2010). PCV values variations in TPS could be attributed to environ-
tend to be higher in males than females (Campbell mental conditions at the time of sampling. TPS
2015). Our results were consistent with these increased with the rise in environmental tempera-
findings; males appeared to have higher mean ture, because plasma water was used to dissipate heat
values than females, but differences were not by evaporation (Dawson and Bortolotti 1997). As
statistically significant and the sample size was small. with PCV, the sampling season could affect these
Differences may result from higher estrogen levels in values. Unfortunately Toro et al. (1997) did not
females, which depresses erythropoiesis, whereas in report the sample collection season. False elevations
males, it is stimulated by androgens and thyroxine will occur if samples are hemolyzed (Samour 2006).
(Campbell 2015). Otherwise, the method used to measure proteins
Values of TPS were within the normal range also can contribute to observed variations. Some
described for birds (30 to 50 g/L; Gee et al. 1981, authors demonstrated that total proteins measured
Ferrer et al. 1987, Coleman et al. 1988), and within by refractometry were higher than those provided by
the ranges previously described for the species by the spectrophotometric method (Biuret methods),
Toro et al. (1997) in captive (Table 5) and free-living because substances other than proteins contribute
condors. However, the mean value was higher than to the total solids of the refractive index (Caprita et
that determined for Andean Condors (Balasch et al. al. 2013). Lumeij and Maclean (1996) indicated that
Table 5. Hematological and biochemical parameters obtained in our study and in other studies of captive Andean Condor (Vultur gryphus) adults. The symbol –
indicates that the authors did not report this value.
MARCH 2018

THIS STUDY BALASCH ET AL. GEE ET AL. 1981 TORO ET AL. 1997
(n ¼ 17) 1976 (n ¼ 2) (n ¼ 9) (n ¼ 12)
ANALYTE MEAN (6SD) MIN MAX MEAN (6SD) MEAN (6SD) MIN MAX MEAN (6SD) MIN MAX
Hematological parameters
PCVa (%) 46.9 (2.8) 41.0 51.0 43.7 (6.7) 42 (3) 39 48 - - -
TPSb (g/L) 45.8 (4.0) 38.0 50.0 29.8 (7.8) 37 (2) 35 42 43 (10) 26 62
WBCc (3109/L) 7.0 (1.8) 3.1 10.4 - - - - - - -
Heterophil (3109/L) 5.8 (1.3) 2.7 7.8 - - - - - - -
Lymphocytes (3109/L) 0.6 (0.4) 0.1 1.5 - - - - - - -
Monocyte (3109/L) 0.6 (0.3) 0.2 1.0 - - - - - - -
Eosinophils (3109/L) 0.0 (0.0) 0.0 0.1 - - - - - - -
Basophils (3109/L) 0.1 (0.1) 0.0 0.3 - - - - - - -
Biochemical parameters
Cad (mmol/L) 2.7 (0.1) 2.4 2.9 - 2.2 (0.1) 2.1 2.4 2.7 (0.4) 1.4 2.7
Phose (mmol/L) 1.4 (0.4) 0.9 2.3 - 0.7 (0.3) 0.2 1.0 1.3 (0.5) 0.8 2.4
UAf (lmol/L) 307.3 (81.6) 128.0 449.0 - 529.4 (142.8) 267.7 672.1 - - -
CKg (U/L) 353.3 (69.9) 231.4 501.5 - - - - 143 (48.5) 77 242
CREh (lmol/L) 30.2 (12.4) 14.3 62.8 - 70.7 (8.8) 53.0 88.4 - - -
LDHi (U/L) 358.5 (78.5) 249.9 530.3 - 274 (56) 192 360 - - -
GGTj (U/L) 5.5 (2.3) 2.0 10.1 - 2.0 (1) 1 3 - - -
APk (U/L) 129.5 (72.8) 66.8 359.8 - 69.0 (51) 36 193 277.5 (107.5) 121 414
ASTl (U/L) 6.9 (1.9) 3.6 9.6 - - - - 13 (4.0) 6 19
HEMATOLOGY OF CAPTIVE ANDEAN CONDORS

a
PCV ¼ packed cell volume.
b
TPS ¼ total plasma solids.
c
WBC ¼ white blood cell count.
d
Ca ¼ calcium.
e
Phos ¼ inorganic phosphorus.
f
UA ¼ uric acid.
g
CK ¼ creatine kinase.
h
CRE ¼ creatinine.
i
LDH ¼ lactate deshidrogenase.
j
GGT ¼ gamma-glutamyl transpeptidase.
k
AP ¼ alkaline phosphatase.
l
AST ¼ aspartate aminotransferase.
77
78 DOUSSANG ET AL. VOL. 52, NO. 1

plasma protein concentration measured by a refrac- Dobado-Berrı́os and Tella 1998, Villegas et al. 2002,
tometer may be considered only a rough estimate of Dujowich et al. 2005). False elevations will occur if
total protein concentration obtained by the Biuret samples are hemolyzed, because the phosphate
method. Nevertheless, other authors demonstrated concentration in erythrocytes is higher than that of
that there was no difference and recommended plasma (Hochleithner 1994). In this study the
refractometry because it is faster and less expensive samples were not hemolyzed.
than other methods (Pessoa et al. 2017). The mean value obtained for UA was lower than
This study reported a wide range in WBC; the mean values in Andean Condors determined by
nevertheless, these results coincided with reference Gee et al. (1981; Table 5). Nevertheless, levels of UA
intervals reported previously in other species of were similar to those reported in other vultures
vultures (Polo et al. 1992, Dujowich et al. 2005, (Polo et al. 1992, Dujowich, et al. 2005, Hernández
Naidoo et al. 2008, Hernández and Margalida 2010) and Margalida 2010). Uric acid concentrations in
and raptors (Cooper 2002). The WBC estimate serum is used to detect renal disease in birds
method may lack accuracy and precision depending (Hochleithner 1994), but other factors such as
on the quality of the stained blood film (Hernández postprandial state and dehydration can increase
et al. 1990). In our study, the same person the values obtained (Harr 2006).
performed cell counts using the same procedure. The mean value obtained for CK (390.6 U/L) was
Our results of leukogram indicated that heterophils higher than those described for Andean Condors
were the most numerous leukocyte in the peripheral (Toro et al. 1997; Table 5) and California Condors
blood of Andean Condors. The stress of handling (Gymnogyps californianus; Dujowich et al. 2005), but
can cause an increase in the number of heterophils. similar mean values for CK were measured in other
This response is not immediate, because although studies of vultures (Polo et al. 1992, Naidoo et al.
corticosteroid levels change rapidly in response to 2008). High CK activity is associated with muscular
stress, the absolute number of leukocytes changes trauma in vulture species (Naidoo et al. 2008). In
more slowly (30–60 min after capture; Cirule et al. this study no individual had traumatic injuries.
2012). We believe that this was not the case due to Mean values obtained for LDH and GGT were
the short time of handling the birds. higher than those determined for Andean Condors
Calcium values were higher than those deter- by Gee et al. (1981; Table 5). The range of LDH
mined in other studies of Andean Condors (Gee et recorded for raptors is wide (100–750 U/L) and
al. 1981, Toro et al. 1997; Table 5), and for other higher values may indicate liver disease (Cooper
vulture species (Polo et al. 1992, Dell’Omo and 2002). Differences in methodologies for measuring
Cavallina 1996, Dobado-Berrı́os and Tella 1998, GGT may account for the marked differences in
Dujowich et al. 2005, Hernández and Margalida reference values (Harr 2006). Enzyme activity in
2010). The higher levels of calcium reported in our normal birds typically falls below the sensitivity range
study could be correlated with protein levels, of most analyzers (Hochleithner 1994), which may
because there is a positive correlation between be the case in this study. Values outside the range
plasma proteins and calcium (Lumeij et al. 1993). (0–6.0 U/L) can be observed when there is liver
Calcium concentrations depend on the reproductive disorder (Cooper 2002).
cycle, sex, and possibly breeding season (Harr 2006), The mean value obtained for AP was higher than
but samples in this study were not from the breeding that determined by Gee et al. (1981) but lower than
season. Increased calcium concentrations have been that obtained by Toro et al. (1997) for Andean
reported with dietary excesses of Vitamin D, Condors (Table 5). Compared to others species of
osteolytic bone tumors, and hyperparathyroidism vultures, the mean value was higher (Polo et al. 1992,
(Harr 2006). Furthermore, dehydration can cause Dobado-Berrı́os and Tella 1998, Villegas et al. 2002,
hyperkalemia (Hochleithner 1994). Dujowich et al. 2005, Hernández and Margalida
Mean values obtained for inorganic phosphorus 2010). Large ranges have been described in birds of
were similar to those determined in female and male prey (25–500 U/L) and high values may indicate
of Andean Condors by Toro et al. (1997) in captive osteoblastic activity (Cooper 2002).
vultures and Gee et al. (1981) in females (1.9 mmol/ AST was lower than the mean described by Toro et
L) but they obtained higher mean values in males al. (1997) for captive Andean Condors (Table 5) but
(2.8 mmol/L; Table 5). Similar values were obtained within the ranges and similar to other species of
in other vultures (Dell’Omo and Cavallina 1996, vultures (Polo et al. 1992, Dobado-Berrı́os and Tella
MARCH 2018 HEMATOLOGY OF CAPTIVE ANDEAN CONDORS 79

1998, Villegas et al. 2002, Dujowich et al. 2005, season can produce variation. As a result, Maceda-
Naidoo et al. 2008, Hernández and Margalida 2010). Veiga et al. (2015) recommend standard protocols
Damage in skeletal muscle and high levels of protein for extraction and analysis of samples, and suggest
in the diet can influence the values of AST (Polo et storing results in a public database to facilitate
al. 1992, Dobado-Berrı́os and Tella 1998). comparative studies and meta-analysis.
TPS, PCV, calcium, and UA increase due to Hematological studies are currently being used to
dehydration (Hochleithner 1994); therefore, when evaluate the health of ecosystems. Any of the
these parameters are altered, the conditions of biochemical parameters analyzed could indicate
captivity and sampling station should be considered. tissue damage (Polo-Cavia et al. 2013) that could
We took our samples in summer; this could explain be associated with environmental contamination.
the difference in our results compared to other For example, blood plasma activity is described as a
studies. biomarker sensitive to the exposure of insecticides
We found no significant differences between such as organophosphorus, carbamate, paraoxon-
males and females in parameters examined (Table methyl, carbofuran, and carbaryl, which cause
2, 4). Results were similar to that described in wild inhibition of cholinesterase in plasma or serum
Bearded Vultures (Gypaetus barbatus; Hernández and (Oropesa et al. 2013). Hematological parameters
Margalida 2010) and Andean Condors (Toro et al. may be useful to monitor contamination events,
1997); in both studies, males and females did not because the blood redistributes contaminants to the
differ. Moreover, Gee et al. (1981) found significant tissues. Bioaccumulation of toxins may occur in the
differences in the values of serum AST and CA liver and cause liver damage, which when associated
between males and females of Andean Condors, but with other antecedents may be markers of environ-
the sample size was small (n ¼ 9). Also Dujowich et al. mental contamination (Pérez et al. 2008). The
(2005) found that chloride, cholesterol, and TPS hematological and biochemical values published in
concentrations were higher in males than females this study can assist the veterinarian laboratory and
among California Condors. The effect of the sex of clinical assessment of condors kept in captivity for
the birds on the hematological characteristics of conservation programs.
some species and the hematological values may vary
depending on reproductive status of birds. Clark et ACKNOWLEDGMENTS
al. (2009), for example, found that ovulating hens
The authors thank the Centro de Rehabilitación de Aves
have significantly higher calcium levels than non- Rapaces de la Unión de Ornitólogos de Chile (and
reproductive females (Hochleithner 1994). personally Jürgen Rottmann and Francisca Izquierdo).
Age may be an important factor affecting hema- We also thank Daniel Bengtsson, Karen Ardiles, Sofia
tological parameters. We could not compare adults González, and Hakan Johansson for their help in gathering
samples. Thanks to the Chilean Livestock and Agricultural
and immatures because the sample size for imma-
Services (SAG) for granting official permit No. 815, issued
tures was very small (n ¼ 5). Wild Bearded Vultures on 21 March 2014.
exhibited significant age-related differences in bio-
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heparin or dipotassium ethylenediaminetetraacetic Received 3 February 2016; accepted 6 September 2017
acid anticoagulants in Hispaniolan Amazon Parrots Associate Editor: Karen Steenhof