HEMATOLOGY, SERUM CHEMISTRY, AND SEROLOGY OF GALA PAGOS PENGUINS (SPHENISCUS MENDICULUS) IN THE GALA PAGOS ISLANDS, ECUADOR
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Journal of Wildlife Diseases, 42(3), 2006, pp. 625–632
# Wildlife Disease Association 2006
HEMATOLOGY, SERUM CHEMISTRY, AND SEROLOGY OF
GALÁPAGOS PENGUINS (SPHENISCUS MENDICULUS) IN THE
GALÁPAGOS ISLANDS, ECUADOR
Erika K. Travis,1,2,6,7 F. Hernan Vargas,3 Jane Merkel,1,4 Nicole Gottdenker,5 R. Eric Miller,1
and Patricia G. Parker1,4
1
Saint Louis Zoo, One Government Drive, Saint Louis, Missouri 63110, USA
2
College of Veterinary Medicine, University of Missouri, 203 Veterinary Medicine Building, Columbia, Missouri 65211,
USA
3
Wildlife Conservation Research Unit, University of Oxford, Tubney House, Abingdon Road, OX13 5QL, UK
4
Department of Biology, University of Missouri—Saint Louis, 8001 Natural Bridge Road, Saint Louis, Missouri 63121,
USA
5
Institute of Ecology, The University of Georgia, Athens, GA 30602, USA
6
Current address: Utah’s Hogle Zoo, 2600 E. Sunnyside Avenue, Salt Lake City, Utah 84108, USA
7
Corresponding author (email: erikazoovet@yahoo.com)
ABSTRACT: The Galápagos penguin (Spheniscus mendiculus) is an endangered species endemic
to the Galápagos Islands, Ecuador. In 2003 and 2004, 195 penguins from 13 colonies on the islands
of Isabela and Fernandina in the Galápagos archipelago were examined. Genetic sexing of 157
penguins revealed 62 females and 95 males. Hematology consisted of packed cell volume (n5134),
white blood cell differentials (n583), and hemoparasite blood smear evaluation (n5114).
Microfilariae were detected in 22% (25/114) of the blood smears. Female penguins had
significantly higher eosinophil counts than males. Serum chemistry on 83 penguins revealed no
significant differences between males and females. Birds were seronegative to avian paramyxovirus
type 1–3, avian influenza virus, infectious bursal disease virus, Marek’s disease virus (herpes),
reovirus, avian encephalomyelitis virus, and avian adenovirus type 1 and 2 (n575), as well as to
West Nile virus (n587), and Venezuelan, western and eastern equine encephalitis viruses (n526).
Seventy-five of 84 (89%) penguins had antibodies to Chlamydophila psittaci but chlamydial DNA
was not detected via polymerase chain reaction in samples from 30 birds.
Key words: Chemistry, filarid, Galápagos Islands, hematology, hemoparasite, penguin,
serology, Spheniscus mendiculus.
INTRODUCION fluctuating population (BirdLife Interna-
tional, 2000). Galápagos penguin popula-
The Galápagos Islands straddle the tions were dramatically reduced during
equator and are 1,000 km west of conti- the 1982–83 (Valle and Coulter, 1987) and
nental Ecuador in the Pacific Ocean. 1997–98 El Niño events (Vargas et al.,
Galápagos avifauna is comprised of 58 2006). Since 1998, the adult population
resident species, of which 52% are en- has been relatively stable whereas the
demic (Tye et al., 2002). The Galápagos juvenile population has been variable
penguin (Spheniscus mendiculus) is an (Vargas and Wiedenfeld, 2004). In 2004,
endemic species with the majority of the the population was estimated at 1505
population residing on two western islands individuals (Vargas and Wiedenfeld,
of the archipelago, Isabela and Fernan- 2004).
dina; smaller populations reside on Flor- No avian species have become extinct
eana, Bartolomé, and Santiago Islands from the Galápagos Islands (Wikelski et
(Mills and Vargas, 1997). The Galápagos al., 2004), but the possibility of disease
penguin is one of the world’s smallest causing significant morbidity and mortality
penguin species and it is the only species is of great concern. Avian health studies in
found in the tropics, with part of its the Galápagos Islands have been ongoing
population inhabiting the northern hemi- since 2001, and to date, 16 avian species
sphere (Boersma, 1977). It is considered on 11 islands have been sampled. The first
endangered due to its small range and comprehensive health assessment of the
625626 JOURNAL OF WILDLIFE DISEASES, VOL. 42, NO. 3, JULY 2006
penguin population occurred in August venipuncture was performed with 20 gauge
2003 and March 2004. Serologic tests needles and syringes to collect up to 12 ml of
blood per bird. Several drops of blood were
were determined from previous penguin immediately placed into cryogenic vials con-
disease surveys (Austin and Webster, taining a lysis buffer preservative solution
1993; Wallace et al., 1997; Clarke and (Longmire et al., 1988) for genetic testing of
Kerry, 2000; Gauthier-Clerc et al., 2002; gender, as well as preliminary hemoparasite
molecular analysis. During the 2003 field
Tuttle et al., 2005). Penguins also were
season, whole blood was placed in lithium
tested for exposure to multiple poultry heparin (Vacutainer PST gel, Becton Dick-
pathogens that could be associated with inson, Franklin Lakes, New Jersey, USA);
chickens in the Galápagos Islands (Gott- during the 2004 field season a small amount
denker et al., 2005). Potential spillover of of whole blood was placed in ethylenediamine-
tetraacetic acid (EDTA) (Microtainer gel,
poultry pathogens to penguins exists via Becton Dickinson), and the remainder placed
poultry waste or other infective material in in serum separator tubes (Vacutainer SST gel
freshwater runoff, aerosol transmission of and clot activator, Becton Dickinson). Blood
viruses from inhabited coastal regions tubes were kept on ice packs until processing. A
adjacent to penguins, discarded poultry single sterile swab (Copan Diagnostics, Corona,
California, USA) was used to collect a combined
products from commercial (fishing and conjunctival, choanal, and cloacal swab per bird
tour) boats in areas where penguins (n597). The swabs were stored in cryogenic
reside, and contact with volant birds (i.e., vials (Nalge Nunc International, Rochester,
yellow warblers or finches) that might New York, USA). No ectoparasites were
observed on feathers during either year. Fecal
transmit pathogens of poultry origin to
samples from 11 individual penguins from 2004
penguin nesting sites. Serologic test selec- were collected opportunistically from fresh
tion was also directed by positive serologic excreta during restraint. Feces were preserved
results from other endemic Galápagos in cryogenic vials with potassium dichromate
avian species (Padilla et al., 2003, 2004). and/or formalin and stored at room tempera-
ture for later microscopic examination.
In order to establish a baseline for future
monitoring of the endangered Galápagos Sample processing
penguin, hematology and serum chemistry
The timing of full sample processing varied
parameters also are reported. from less than 1 hr up to 6 hr after collection.
Most samples were centrifuged within 3 hr of
MATERIALS AND METHODS collection. Two blood smears were made from
whole blood (lithium heparin in 2003, EDTA
Study area and sample collection in 2004), and air dried and fixed with methanol
Galápagos penguins were studied on the in the field. Microhematocrit tubes (n5134)
coasts of Isabela (0u259300S, 91u79W) and were centrifuged (Mobilespin Model 128,
Fernandina (0u22900S, 91u319200W) Islands. Vulcon Technologies, Grandview, Missouri,
All sampling procedures were in accordance USA) for 20 min, and the packed cell volumes
with Saint Louis Zoo institutional animal care (PCV) determined. The blood in lysis buffer
and use committee standards. Eighty-four and solution was held at ambient temperature. The
112 penguins were examined in August 2003 lithium heparin whole blood samples (n574)
and March 2004, respectively. On Fernandina and serum separator samples (n597) were
Island, 27 penguins in 2003 and seven in 2004 centrifuged for 20 min, and the plasma or
were sampled, and on Isabela Island, 57 serum decanted and stored in cryogenic vials.
The plasma, serum, and swabs were stored in
penguins in 2003 and 105 in 2004 were
liquid nitrogen in the field and in the
evaluated. Information on capture technique
laboratory.
(Vargas et al., 2005), and morphometric mea-
surements and aging (Boersma, 1977), has
Sample and data analysis
previously been described. During manual
restraint, a transponder (AVID Microchip, Blood smears were stained using a modified
Folsom, Louisiana, USA) was placed subcuta- Wright–Giemsa stain (JorVet Dip-Quick, Jor-
neously over the left dorsal mid phalangeal area gensen Laboratories, Loveland, Colorado,
and the skin defect sealed with tissue glue (3M USA) at the Saint Louis Zoo for white blood
Vetbond, St Paul, Minnesota, USA). Jugular cell (WBC) differentials based on 100 cellsTRAVIS ET AL.—HEMATOLOGY, CHEMISTRY, SEROLOGY GALÁPAGOS PENGUINS 627
counted at 10003 magnification. Blood RESULTS
smears were evaluated for thrombocytes and
hemoparasites. Genetic testing for sex de- Genetic sexing, body weight, hematolo-
termination (n5157) was performed at the gy, and microscopic hemoparasite evalua-
University of Missouri–Saint Louis (UMSL)
via polymerase chain reaction (PCR) (Fridolfs- tions were performed on the 2003 and
son and Ellegren, 1999). Ninety of the 2004 2004 samples, counting each individual
samples were processed for serum biochemis- once because some individuals were
try (AVL Veterinary Laboratory, Saint Louis, sampled both years. Serum chemistries,
Missouri, USA), in one batch on the Ace
serology, and fecal analysis were con-
Clinical Chemistry System (Alfa Wassermann,
Inc., West Caldwell, New Jersey, USA). Seven ducted only for the 2004 samples. All
results were not included in the analysis due to penguins examined were in good body
hemolysis or lipemia. condition, as determined both by palpa-
Serology testing was restricted to the 2004 tion of pectoral muscles and body weight
samples. Testing for antibodies to Chlamydo-
phila psittaci was done by the Texas Veterinary
measurement. There were no external
Medical Diagnostic Laboratory, College Sta- signs of disease. In 2003, 84 penguins
tion, Texas, USA using direct complement were sampled; eight (10%) nestlings, five
fixation (DCF) on serum (n584); combined (6%) juveniles, and 71 (84%) adults. In
conjunctival, choanal and cloacal swabs from 30 2004, 112 penguins were sampled; four
of the antibody positive penguins were also
tested for C. psittaci DNA by real-time PCR. (4%) nestlings, 28 (25%) juveniles, and 80
Serologic tests for viral antibodies, except (71%) adults. Twenty-five penguins in
for WNV, were conducted at the National 2004 were recaptured from the previous
Veterinary Services Laboratory, US Depart- year. Genetic sexing of 157 individuals
ment of Agriculture, Ames, Iowa, USA. revealed 62 females (39.5%) and 95 males
Hemagglutination inhibition (HI) testing was
used to test for antibodies to avian para- (60.5%). Body weight and hematology
myxovirus type 1–3 (n575; titers $8 were results are provided in Table 1. Because
considered positive) and Venezuelan (VEE), there was a significant difference between
western (WEE), and eastern (EEE) equine the sexes for body weight and PCV,
encephalitis viruses (n526; titers $10 were separate gender means are listed. There
considered positive). Agar gel immunodiffu-
sion (AGID) testing was used to test for were no differences in PCV or differen-
antibodies to avian influenza virus, infectious tials between heparin or EDTA blood.
bursal disease virus, Marek’s disease (herpes) The mean PCV of the combined male and
virus, avian adenovirus types 1 and 2, and female sampled population was 44.1%
avian encephalomyelitis virus (n575). Indirect (SD 6.8%, n5134). Males had significant-
fluorescent antibody (IFA) testing was used to
test for antibodies to reovirus (n575). Serum ly higher body weights (P,0.00001) and
was tested for antibodies to West Nile virus by PCV results (P,0.006) compared to fe-
plaque reduction neutralization (n587) at the males. There were no differences in WBC
Animal Health Diagnostic Center, Cornell differentials between genders except that
University, Ithaca, New York, USA. Fecal
females had elevated eosinophils
analysis from fecal floatation and sedimenta-
tion was conducted with microscopy at the (12.269.1%, n529) compared to males
Southeastern Cooperative Wildlife Disease (5.360.7%, n554) (P,0.0002). Micro-
Study, College of Veterinary Medicine, The scopic evaluation of blood smears revealed
University of Georgia, Athens, Georgia, USA. microfilariae in 21.9% (25/114) of the
A statistical software package (NCSSH,
Kaysville, Utah, USA) was used for data
penguins. Thrombocytes were adequate
analysis. Results were inspected for normality for both genders because at least two to
using a Shapiro-Wilk W test and t-tests were three thrombocytes were seen on each
performed. Mann-Whitney U-tests were used high power field (Pierson, 2000).
on samples where normality was rejected. A Results of serum chemistries are pro-
statistical significance was determined as
P#0.05 except for the serum chemistry values vided in Table 2; there were no significant
where a Bonferroni-corrected P#0.004 (0.05/ differences between female and male
12) was used. penguin biochemistry values. All penguins628 JOURNAL OF WILDLIFE DISEASES, VOL. 42, NO. 3, JULY 2006
TABLE 1. Weight, packed cell volume, and white blood cell differentials for free-ranging Galápagos penguins.
Parameter Mean6SD Range n
Female weight (kg)a 1.960.3 1.4–2.5 62
Male weight (kg)a 2.360.3 1.7–3.5 103
Female packed cell volume (%)b 41.767.0 28.0–52.0 53
Male packed cell volume (%)b 45.366.8 23.0–58.0 79
Heterophils (%) 57.6616.0 8.0–85.0 83
Lymphocytes (%) 31.5615.5 6.0–84.0 83
Monocytes (%) 2.462.1 0.0–9.0 83
Eosinophils (%) 8.067.5 0.0–37.0 83
Basophils (%) 0.460.7 0.0–3.0 83
a
Significant difference P,0.00001.
b
Significant difference P,0.006.
were serologically negative to all viruses. boldti) is closely related to the Galápagos
Seventy-five of 84 penguins (89.3%) were penguin (Robert Fleischer, pers. comm.);
seropositive to C. psittaci with titers of 8 to therefore, blood work from a free ranging
64. Combined swabs were submitted for Humboldt population (Wallace et al.,
C. psittaci PCR on 30 of the 75 seropos- 1995) was used for comparison. Because
itive penguins; all were negative. Hema- the methodology of the studies was
tology and biochemistry results did not different, trends between the penguin
differ between C. psittaci or filarial species is discussed instead of statistical
positive penguins and those that were differences. The Galápagos penguins had
negative. Fecal samples were negative for higher chloride, calcium, uric acid, and
helminth eggs and larval nematodes, but aspartate aminotransferase values, but
one penguin (1/11) had three Eimeria lower PCV, glucose, and albumin com-
oocysts detected (17316 mm). pared to the Humboldt penguins. Labo-
ratory results can be affected by many
DISCUSSION variables such as species, gender, age,
nutritional status, or geographic location
These are the first published hematol- (Dein, 1986), and the difference between
ogy, serum chemistry, and large-scale the Galápagos and Humboldt penguins
serology results for the Galápagos pen- likely are not clinically significant.
guin. The Humboldt penguin (S. hum- A change in the Galápagos penguin
TABLE 2. Serum chemisty results for free-ranging Galápagos penguins (n583).
Parameter (SI units) Mean6SD Range
Aspartate aminotransferase (U/l) 282.5689.8 132.0–525.0
Total protein (g/l) 56.06 7.7 36.0–77.0
Albumin (g/l) 12.261.5 9.0–17.0
Phosphorus (mmol/l) 1.660.8 0.8–4.2
Calcium (mmol/l) 2.560.2 2.2–3.7
Glucose (mmol/l) 12.161.9 5.3–15.7
Sodium (mmol/l)a 156.366.1 133–169.0
Potassium (mmol/l)a 3.961.3 2.2–8.1
Chloride (mmol/l)a 118.564.6 102.0–132.0
Creatine kinase (U/l) 174.46144.5 18.0–675.0
Uric acid (mmol/l) 1.160.4 0.2–1.9
a
n576.TRAVIS ET AL.—HEMATOLOGY, CHEMISTRY, SEROLOGY GALÁPAGOS PENGUINS 629 sampling protocol between years resulted one penguin fecal sample are not consid- in blood smears from lithium heparin ered significant in a healthy bird. Cocci- anticoagulated blood in 2003 and EDTA dial infections have been reported as anticoagulated blood in 2004, but no incidental findings in little penguins (Eu- differences were appreciated microscopi- dyptula minor) (Obendorf and McColl, cally between the two anticoagulants. 1980; Harrigan, 1992). Evaluating the Field conditions did not allow for hemo- impact of these various parasites in the cytometer total WBC counts. An estimat- Galápagos penguins necessitates a long- ed total WBC count from fixed blood term study. smears (Fudge, 2000) was attempted The Galápagos penguins were seroneg- months after sample collection, but the ative for exposure to all tested viruses. The blood smear quality had diminished suffi- seronegative Marek’s disease (herpesvirus) ciently to yield inaccurate results. There- results concurred with a previous study fore, total WBC counts are not reported. (Miller et al., 2001). Because most tests Fortunately, the WBC differentials and have been validated for domestic chickens, hemoparasite evaluations were performed serologic results should be interpreted in a timely manner after sample collection with caution. The Galápagos penguins while the cells were easily identifiable. were seropositive for C. psittaci (89%, The authors speculate that the marine 75/84). Chlamydophila psittaci is found environment was detrimental to the slides, worldwide in asymptomatic birds (Ger- and that the lack of cover slips further lach, 1994) and antibodies have been caused cell deterioration. The leukocyte detected in multiple penguin species differentials for the Galápagos penguin (Sieburth, 1958; Moore and Cameron, population, combining male and females 1969; Wallace et al., 1997; Karesh et al., (n583), fell within the ranges reported for 1999). An outbreak at a zoo in the USA in wild Humboldt penguins (Wallace et al., a Spheniscus penguin species revealed 1995). The clinical significance of the that C. psittaci can be an important elevated eosinophil count in female Galá- penguin pathogen (Freeland Dunker, pagos penguins remains unknown. Galá- pers. comm.). The significance of seropos- pagos penguins were evaluated over two itive Galápagos penguins in the absence of distinct environmental seasons, but no DNA from PCR is unclear. A false positive seasonal difference was found in eosino- antibody result or a latent or inactive phil counts. Furthermore, eosinophil va- infection cannot be ruled out. Chlamydo- lues between microfilarid positive and phila psittaci has been extensively studied negative penguins did not differ. in the Galápagos Islands and antibodies Extraerythrocytic microfilariae were de- have been detected in flightless cormor- tected in the Galápagos penguins. Similar ants (Travis et al., 2006) and domestic microfilariae have been detected in the chickens (Gottdenker et al., 2005), and flightless cormorant (Phalacrocorax har- chlamydial DNA has been detected in risi) which shares the same geographic Galápagos doves (Zenaida galapagoensis; distribution as the penguins (Travis et al., Padilla et al., 2004) and cormorants 2006). Filarids are usually incidental find- (Travis et al., 2006). ings (Greiner and Ritchie, 1994), and are Chickens in the Galápagos Islands have rarely reported in penguins. There is only tested positive for parasites and diseases one known case of filariasis in Galápagos for which penguins might be susceptible, penguins (Chabaud and Ball, 1964). A including Newcastle disease (Gottdenker detailed investigation is currently under- et al., 2005). Although this study suggests way to further classify and characterize the that Galápagos penguins have not been microfilaria seen in 22% of the Galápagos exposed to poultry pathogens, the threat of penguins. The Eimeria oocysts found in pathogen transmission is real. Chickens
630 JOURNAL OF WILDLIFE DISEASES, VOL. 42, NO. 3, JULY 2006
range freely in Puerto Villamil on South- crashes caused by strong El Niño events,
ern Isabela and they have been observed disease could jeopardize the survival of
on beachfront properties adjacent to this species. Disease surveillance should
where a small penguin population resides continue, as well as the development of
(Vargas and Wiedenfeld, 2004). Recent contingency plans in order to respond
surveys suggest that penguin numbers are rapidly to new pathogens.
slowly increasing at this site through
migration (Vargas, unpubl. data); there- ACKNOWLEDGMENTS
fore, measures should be implemented to The Des Lee Collaborative Vision in Zoo-
reduce or prevent contact between pen- logical Research and the Saint Louis Zoo
guins and poultry. generously funded this study. Complementary
funding was provided by the Darwin Initiative
We report the most extensive West Nile and D. Swarovski & Co. The authors would
virus (WNV) monitoring in the archipela- like to acknowledge the Galápagos National
go to date with negative results for the Park and the Charles Darwin Research Station
Galápagos penguins, flightless cormorants for their support, especially David Wieden-
(Travis et al., 2006), and domestic chick- feld, Gustavo Jiménez Uzcátegui, Maria de
Lourdes Barcia, and Susana Cardenas. We
ens (Gottdenker et al., 2005). WNV is an thank Kelly Halbert for performing molecular
emerging threat to naÏve avian populations gender tests in the Des Lee Animal Molecular
especially where known mosquito vectors Ecology laboratory at the University of Mis-
reside (Peck et al., 1998; Turell et al., souri—Saint Louis, Amy Glaser from Cornell
2001). Because penguins are susceptible University for WNV testing, and Michael
Yabsley from the Southeastern Cooperative
to WNV and mortality has been confirmed Wildlife Disease Study of the University of
in black-footed (Spheniscus demersus) and Georgia for performing fecal analysis. We also
Humboldt penguins (Centers for Disease thank Kate Huyvaert for statistics help and
Control, 2005), monitoring and prevention Ben Murray for sample and database work.
programs for WNV are in place or being
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