DISTINGUISHING DISEASE EFFECTS FROM ENVIRONMENTAL EFFECTS IN A MOUNTAIN UNGULATE: SEASONAL VARIATION IN BODY WEIGHT, HEMATOLOGY, AND SERUM CHEMISTRY AMONG IBERIAN IBEX ( CAPRA PYRENAICA

DISTINGUISHING DISEASE EFFECTS FROM ENVIRONMENTAL

EFFECTS IN A MOUNTAIN UNGULATE: SEASONAL VARIATION IN

BODY WEIGHT, HEMATOLOGY, AND SERUM CHEMISTRY AMONG

IBERIAN IBEX AFFECTED BY SARCOPTIC MANGE

Jesus M. Perez,1,8 Emmanuel Serrano,2,3 Ramon C. Sorigue,4 Francisco J. Gonzalez,5

Mathieu Sarasa,1 Jose E. Granados,6 Francisco J. Cano-Manuel,6 Rafaela Cuenca,2 andPaulino Fandos7

1 Departamento de Biologıa Animal, Biologıa Vegetal y Ecologıa, Universidad de Jaen, Campus Las Lagunillas, s.n.,E-23071, Jaen, Spain2 Servei d’Ecopatologia de Fauna Salvatge (SEFaS), Departament de Medicina i Cirurgia Animals, Universitat Autonomade Barcelona, E-08193, Bellaterra, Barcelona, Spain3 CESAM, Departamento de Biologia, Universidade de Aveiro, Campus Universitario de Santiago, 3810-193, Aveiro,Portugal4 Estacion Biologica de Donana (CSIC), Av. Americo Vespucio, s.n., E-41092 Sevilla, Spain5 Laboratorio PROLAB, Carrera 51, E-23600, Martos, Jaen, Spain6 Espacio Natural Sierra Nevada, Carretera Antigua de Sierra Nevada, Km 7, E-18071, Pinos Genil, Granada, Spain7 Agencia de Medio Ambiente y Agua, Isla de la Cartuja, E-41092, Sevilla, Spain8 Corresponding author (email: [email protected])

ABSTRACT: Our study focuses on the Iberian ibex from the Sierra Nevada Natural Space(southern Spain), where sarcoptic mange is an endemic disease and animals are affected by ahighly seasonal environment. Our aim was to distinguish between disease and environmentalinfluences on seasonal variation in body weight, hematology, and serum biochemistry in Iberianibex. We sampled 136 chemically immobilized male ibexes. The single effect of mange influencedhemoglobin, hematocrit, mean corpuscular volume, leukocytes, band neutrophils, monocytes,cholesterol, urea, creatine, and aspartate aminotransferase. Both mange and the period of the yearalso affected values of mean corpuscular hemoglobin, mean corpuscular hemoglobin concentra-tion, neutrophils, glucose, and serum proteins. Scabietic animals showed a marked reduction inbody weight (21.4 kg on average), which was more pronounced in winter. These results reveal that1) infested animals are anemic, 2) secondary infections likely occur, and 3) sarcoptic mange iscatabolic.

Key words: Capra pyrenaica, host-parasite relationships, Sarcoptes scabiei, wildlife diseases.

INTRODUCTION

Sarcoptic mange caused by Sarcoptesscabiei is responsible for epizootic diseasein free-ranging populations of a broadrange of wild mammals around the globe(Pence and Ueckermann 2002). Hemato-logic and biochemical responses to mangeare relatively well known in domestic andwild mammals (Sarasa et al. 2010; Akomaset al. 2011; Kido et al. 2011). However,physiologic response of animals affectedby mange in highly seasonal mountainecosystems has not been evaluated. Usinga sample of 136 male Iberian ibexes fromthe Sierra Nevada Natural Space (south-ern Spain), we assessed whether mangeaffects body weight, which shows mark-edly seasonal variations, but also examined

the effects of mange on hematologic andserum chemistry values of affected ani-mals. Because ibexes in the Sierra Nevadaexperience strong seasonal changes inbody reserves (Serrano et al. 2011) andsuch body stores are correlated to somehematologic parameters (Serrano et al.2008), we expected that mange may drivethe seasonal hematologic profile of thismountain ungulate.

MATERIALS AND METHODS

Study area

We studied the Iberian ibex population ofthe Sierra Nevada Natural Space (36u009–37u109N, 2u349–3u409W, southern Spain). Thisarea comprises the alpine massif, including thehighest peaks in the Iberian Peninsula (e.g.,the Mulhacen, 3,481 m above sea level). This

DOI: 10.7589/2014-01-008 Journal of Wildlife Diseases, 51(1), 2015, pp. 000–000# Wildlife Disease Association 2015

0

area is characterized by strong seasonalclimatic variations; snow cover is present for6 mo (December to May), and most plantgrowth occurs from June to August (Peinadoand Rivas-Martınez 1987).

Ibex capture and blood collection

Between 2005 and 2012 blood samples from136 male Iberian ibexes 3–11 yr old (81clinically healthy and 55 scabietic animals)were collected. Animals were chemicallyimmobilized with a mixture of xylazine (3 mg/kg) and ketamine (3 mg/kg; Casas-Dıaz et al.2011) and aged by growth segments on thehorns (Fandos 1991). During immobilizationwe collected blood into tubes containingethylenediaminetetraacetic acid tripotassiumand serum tubes. Time required for bloodcollection was similar for all animals with amean of 5 min (range, 3–15 min).

Scabietic animals were visually assigned tofour categories according to the percentage ofskin surface affected by mites (Perez et al. 2011:0 5 ibexes without skin lesions; 1 5 skin surfaceaffected ,25%; 2 5 skin surface affected 25–50%; and 3 5 skin surface affected .50%).Skin scrapings were analyzed at the laboratoryto confirm the diagnoses.

Hematology

Whole blood samples were stored at 4 Cuntil arrival at the laboratory. Hematologicanalyses were performed within 24 hr ofcollection. Clotted tubes were centrifuged at4,750 3 G for 10 min, and sera were stored at220 C until analysis. Red blood cell count(RBC), hemoglobin concentration (Hb), he-matocrit, mean corpuscular volume (MCV),mean corpuscular hemoglobin (MCH), mean

corpuscular hemoglobin concentration(MCHC), white blood cell count, and differ-ential leukocyte count were determined with aCell-Dyn 3500H autoanalyzer (Abbott Cientı-fica, S.A., Madrid, Spain).

Biochemistry

We measured: glucose, cholesterol, urea,creatine, aspartate aminotransferase (AST),creatine kinase (CK), lactate dehydrogenase(LDH), total proteins, and albumin using anautoanalyzer (BT 2245H, Biotechnica Instru-ments, Rome, Italy). Total proteins weremeasured using the Biuret method (BioSys-temsH–Atom, Barcelona, Spain), and serumproteins were separated using a power supplyBTS-100 (Biosystems, S.A, Barcelona, Spain)on cellulose acetate strips (CellogeLH, Milan,Italy) and sodium veronal 0.04 M sodiumdiethylbarbiturate 8.25 g/L as a buffer at 220 Vfor 38 min. Bands obtained were stained withamido black and quantified using a 434photodensitometerH (Digiscan, Barcelona,Spain).

Statistical analyses

We evaluated whether the interaction be-tween mange infection and seasons influencedbody weight of ibexes using linear models(LM). Four categories of mange infectionwere considered. The effects of seasons wereevaluated in two periods of the year thatrepresent the main seasonal changes of bodystores (Serrano et al. 2011): winter–spring(December 15–June 15) and summer–autumn(June 16–December 14). To control forpotential effects of age, only ibexes close toreaching full body development were includedin our analyses (.3 yr old; Serrano et al.

TABLE 1. Mean6SE, sample size (applicable to all tables), and range (in parentheses) of body weights (kg)of 136 male Iberian ibex, Capra pyrenaica, .3 yr old, captured in the Sierra Nevada Natural Space, southernSpain, 2005–2012. WS indicates ibexes captured in winter and spring and SA in summer and autumn.Numbers in columns represent four categories based on the percentage of skin surface affected by mange.

Mange statusa

0 1 2 3

WS

Mean6SE (range) 53.561.4 (20–72) 5262.2 (35–72) 46.262.3 (32–59) 36.365.1 (28–54)n 47 19 14 5

SA

Mean6SE (range) 64.661.7 (32–75) 56.862.7 (50–65) 45.763.5 (36–52) 38.861.6 (34–46)n 34 6 4 7

a 0 5 ibex without skin lesions; 1 5 skin surface affected ,25%; 2 5 skin surface affected between 25 and 50%; 3 5 skinsurface affected .50%.

0 JOURNAL OF WILDLIFE DISEASES, VOL. 51, NO. 1, JANUARY 2015

TA

BL

E2.

Mean

6S

E(r

ange)

of

valu

es

of

hem

atolo

gic

par

amete

rsin

136

mal

eIb

eri

anib

ex,

Cap

rap

yren

aica

,.

3yr

old

,ca

ptu

red

inth

eS

ierr

aN

eva

da

Nat

ura

lS

pac

e,

sou

thern

Sp

ain

,2005–2012.

WS

ind

icat

es

ibexe

sca

ptu

red

inw

inte

ran

dsp

rin

gan

dS

Ain

sum

mer

and

autu

mn

.

Par

amete

ra

Man

ge

stat

us

01

23

RB

C(1

012/L

)

WS

14.6

36

0.2

3(1

0.4

0–18.1

1)

14.4

16

0.3

5(1

0.8

0–16.5

)13.1

46

0.5

1(9

.19–14.8

)11.4

46

0.6

9(9

.32–13.3

)S

A14.9

76

0.3

7(8

.5–20.6

)13.9

36

0.4

6(1

2.7

–15.8

)12.6

36

0.6

1(1

1.8

–13.8

)12.9

66

0.6

4(1

1.0

0–14.7

)

Hem

oglo

bin

(g/

dL

)

WS

147.6

36

2.3

4(1

06.0

–171.0

)156.0

56

6.0

8(1

21.0

–224.0

)134.3

56

4.9

6(9

2.0

–153.0

)118.3

16

7.9

8(9

5.0

–138.0

)S

A156.7

36

4.2

2(8

4.2

–200.0

)140.1

66

7.3

5(1

24.0

–173.0

)127.6

66

5.3

6(1

20.0

–138.0

)125.6

16

7.4

6(1

04.0

–145.0

)

Hem

atocr

it(%

)

WS

38.0

76

0.4

7(3

1.0

–44.0

)36.5

16

0.8

1(3

2.0

–43.0

)34.9

56

0.8

1(2

9.0

–40.0

)34.4

46

1.7

2(2

9.0

–39.0

)S

A38.1

96

0.8

4(2

6.1

–49.0

)36.0

66

1.2

7(3

2.3

–41.6

)35.4

66

0.2

4(3

5.0

–35.8

)34.2

26

1.7

1(2

9.9

–39.0

)

MC

H(p

g)

WS

10.2

66

0.0

7(8

.9–11.3

)10.5

36

0.2

1(9

.4–13.1

)10.2

96

0.1

4(9

.5–11.3

)10.2

36

0.1

7(9

.7–10.7

)S

A10.4

36

0.1

4(8

.6–12.9

9)

10.0

36

0.1

9(9

.69–10.9

5)

9.8

46

0.1

8(9

.52–10.1

6)

9.6

76

0.1

9(9

.19–10.3

1)

MC

V(f

L)

WS

26.8

26

0.3

6(2

2.9

–32.1

)25.2

86

0.5

9(2

2.6

–30.7

)26.6

26

0.9

9(2

3.7

–36.1

)30.6

26

0.5

3(2

9.3

6–32.1

6)

SA

25.2

96

0.3

9(1

7.8

–30.7

)25.9

16

0.5

6(2

3.9

3–27.9

5)

27.0

26

1.0

9(2

5.4

–29.1

1)

26.4

36

0.6

1(2

4.6

3–28.1

3)

MC

HC

(%)

WS

38.4

46

0.4

7(3

3.5

–44.4

)41.9

96

1.2

5(3

4.4

–53.3

)38.6

26

0.9

4(3

1.1

5–43.3

)33.3

60.2

6(3

2.4

8–34.1

)S

A41.6

66

0.7

3(3

2.2

6–52.6

3)

38.8

16

1.1

1(3

4.9

3–41.5

9)

36.5

16

0.8

1(3

4.9

2–37.5

1)

36.6

46

0.6

1(3

4.7

8–38.4

6)

Leu

kocy

tes/

mL

WS

8,1

79.2

16

418.4

1(2

,860–13,6

00)

9,8

04.7

6472.9

1(6

,960–13,5

00)

11,1

906

1,1

37.8

9(1

,990–17,5

00)

19,3

40.2

16

1,4

78.7

9(1

4,6

00–21,7

01)

SA

9,6

74.5

46

494.8

5(3

,370–15,8

00)

10,3

76.6

66

1,6

87.0

8(5

,880–17,5

00)

12,8

66.6

76

1,3

73.9

6(1

0,3

00–15,0

00)

12482.0

62282.1

3(6

210–20200)

Ban

ds/

mL

WS

367.2

16

57.9

3(0

–1,4

28)

427.6

46

70.0

1(9

3–1,0

80)

711.5

86

142.7

7(2

0–1,7

50)

1,8

73.4

16

260.8

5(1

,080–2,3

88)

SA

280.4

86

38.4

5(0

–810)

379.6

66

154.2

3(1

18–1,0

00)

677.6

66

38.6

2(6

18–750)

868.0

6450.3

2(6

62–2,6

26)

Neu

trop

hil

s/m

L

WS

3,4

70.3

16

224.5

9(1

,316–8,5

68)

4,0

57.7

16

340.0

4(2

,220–6,7

50)

5,2

96.3

36

543.2

7(9

95–8,2

59)

13,4

97.8

16

1,8

61.0

7(7

,866–16,7

10)

SA

2,8

04.8

06

212.8

4(1

.370–6,8

12)

3,7

96.6

06

1,4

27

(3,3

02–12,6

00)

6,7

76.6

06

1,9

53.6

1(4

,944–11,7

00)

8,6

80.0

06

1,6

53.7

4(9

94–9,9

12)

PEREZ ET AL.—WEIGHT, HEMATOLOGY, AND BIOCHEMISTRY OF SCABIETIC IBERIAN IBEX 0

2004). The mean age of ibexes did notsignificantly differ among categories of mangeinfection (F51.525, P50.2).

We evaluated the physiologic response ofibexes to mange using multivariate analysis ofvariance (MANOVA). Our sampling designincluded a balanced proportion of sick andhealthy ibexes in both periods of the year(Kruskal-Wallis53.6, P50.06), minimizing thepossibility of spurious results.

For both LM and MANOVA, a modelselection procedure based on the AkaikeInformation Criterion corrected for smallsample size (AICc) was performed (Burnhamand Anderson 2002). The model with thelowest AICc was retained, and the remainingcompeting models were ordered according totheir Akaike differences (Di) with respect tothe best model (lowest AICc). The Akaikeweight (Wi,) and the percentage of explainedvariability (R2) for the best model were alsoestimated. Statistical analyses were carried outin the statistical software R version 3.0.3 (RDevelopment Core Team 2014).

RESULTS

Descriptive statistics for body weightand hematologic and serum biochemicalparameters studied are summarized inTables 1–3. Our model selection suggest-ed a seasonal-dependent effect of mangeon ibex weight (wMange status*Period of the year

50.52; Table 4). However, and accord-ing to the principle of parsimony, thesecond competing model (Di 5 0.17),which suggested the additive effects ofboth factors, would have more support(wMange status+Period of the year50.47;Table 4). The model suggests that 40%

of the observed body weight variabilityrelied on mange infection and period ofthe year. Reduced body weight in scabi-etic ibexes appeared in the early stages ofinfection (b2nd mange category5210.19,SE52.5, t524.01) but peaked when morethan half of the skin surface was affected(b3rd mange category5221.47, SE52.9,t527.21). During the course of infection,weight loss in ibexes ranged between 32%

(17 kg) in winter and 39.9% (25.8 kg) insummer (Table 1). Winter conditions alsorepresent a challenge in terms of energy(bWinter–Spring528.46, SE51.7, t524.85),

Par

amete

ra

Man

ge

stat

us

01

23

Eosi

nop

hil

s/m

L

WS

525.2

86

82.0

8(0

–2.4

99)

704.0

56

99.9

2(0

–1,3

86)

901.0

6310.7

8(0

–3,8

50)

371.4

16

335.8

3(0

–1,7

10)

SA

369.7

26

56.9

3(0

–1.3

14)

438.3

36

190.7

9(0

–1,1

80)

810.6

16

132.2

7(0

–1,0

64)

327.0

6140.7

8(0

–816)

Lym

ph

ocy

tes/

mL

WS

3.5

53.2

16

265.8

5(4

04–8.2

50)

4,3

48.6

46

573.4

1(3

,322–6,0

48)

4,0

73.7

56

573.4

1(5

77–6,6

30)

2,7

52.2

16

782.0

2(1

,085–4,7

88)

SA

4.3

02.4

86

347.6

1(2

.234–8.4

56)

3,4

00.1

66

346.9

6(2

,234–4,7

20)

2,8

94.3

36

631.9

1(1

,650–3,7

08)

3,5

48.8

16

870.9

8(9

44–6,0

60)

Mon

ocy

tes/

mL

WS

145.2

66

60.8

4(0

–2,2

88)

163.7

16

26.2

3(0

–476)

118.1

66

41.5

7(0

–525)

739.6

16

329.1

8(0

–1,5

20)

SA

401.3

96

46.0

6(0

–1,0

53)

479.6

66

110.3

2(5

9–875)

197.3

36

56.0

4(1

33–309)

475.0

6146.2

3(2

12–1,0

10)

aR

BC

5re

db

loo

dce

llco

un

t;M

CH

5m

ean

corp

usc

ula

rh

em

oglo

bin

;M

CV

5m

ean

corp

usc

ula

rvo

lum

e;

MC

HC

5m

ean

corp

usc

ula

rh

em

oglo

bin

con

cen

trat

ion

.

TA

BL

E2.

Con

tin

ued

.


TA

BL

E3.

Mean

6S

E(r

ange)

of

valu

es

of

seru

mb

ioch

em

ical

par

amete

rsin

136

mal

eIb

eri

anib

ex,

Cap

rap

yren

aica

,ove

r3

yrof

age,

cap

ture

din

the

Sie

rra

Neva

da

Nat

ura

lS

pac

e,

sou

thern

Sp

ain

,2005–2012.

WS

ind

icat

es

ibexe

sca

ptu

red

inw

inte

ran

dsp

rin

gan

dS

Ain

sum

mer

and

autu

mn

.

Par

amete

ra

Man

ge

stat

us

01

23

Glu

cose

(mm

ol/

L)

WS

3.3

66

0.3

3(0

.15–9.2

)3.1

76

0.5

1(0

.22–7.1

7)

3.4

16

0.7

9(0

.88–11.6

)0.5

16

0.1

9(0

.17–1.2

7)

SA

5.4

66

0.5

8(0

.27–13.6

5)

2.5

36

0.6

6(0

.22–4.2

7)

0.7

96

0.2

9(0

.27–1.6

5)

2.8

16

1.5

4(0

.11–10.7

6)

Ch

ole

stero

l(m

mol/

Ll)

WS

1.1

16

0.0

3(0

.77–1.6

5)

1.0

56

0.0

5(0

.64–1.5

7)

1.0

66

0.0

6(0

.38–1.4

9)

0.8

26

0.1

3(0

.51–1.1

8)

SA

1.3

36

0.0

4(0

.82–2.0

9)

1.3

76

0.0

8(1

.16–1.6

5)

1.3

56

0.1

1(1

.07–1.6

4)

1.1

56

0.1

1(0

.74–1.6

1)

Ure

a(m

mol/

Ll)

WS

35.8

86

0.9

4(2

4.0

6–51.4

1)

32.0

96

1.4

5(2

2.8

4–47.1

2)

39.0

66

3.4

9(2

6.4

1–80.6

8)

46.8

66

15.4

1(1

6.4

2–84.6

1)

SA

24.3

36

1.5

4(9

.56–64.2

)35.2

76

6.3

2(1

9.3

2–64.9

7)

29.4

36

1.7

6(2

6.4

1–33.7

7)

45.2

26

8.0

4(2

8.1

3–89.9

6)

Cre

atin

ine

(mm

ol/

L)

WS

86.6

36

1.6

6(6

4.5

3–111.3

8)

89.3

36

2.8

8(6

8.9

5–114.9

2)

88.5

26

2.6

8(7

3.3

7–110.5

)92.1

16

11.2

6(6

8.0

6–134.3

6)

SA

108.7

66

3.5

1(6

9.3

1–152.9

3)

116.6

86

6.8

7(9

9.8

9–143.2

1)

87.9

56

3.3

3(8

3.0

9–97.2

4)

78.0

46

5.9

8(5

3.0

4–99.8

9)

AS

T(I

U/L

)W

S142.3

46

4.5

7(9

1–263)

151.2

16

9.2

3(9

7–263)

147.9

26

18.2

1(1

06–375)

144.3

16

73.2

1(3

0–426)

SA

133.8

16

10.4

6(9

0.4

–442)

142.6

66

13.0

8(1

15–199)

120.9

26

10.7

5(9

5.8

–148)

194.2

86

41.1

5(8

7–405)

CK

(IU

/L)

WS

367.6

86

42.5

1(1

15–2,1

10)

451.3

16

89.5

0(1

37–1,8

76)

365.8

56

79.7

9(1

37–1,3

33)

412.9

16

67.1

8(2

41–573)

SA

267.5

26

24.4

5(8

1–816)

356.6

66

54.8

9(2

00–557)

176.2

56

35.5

9(1

15–255)

461.5

76

233.4

4(1

58–1,8

57)

LD

H(I

U/L

)

WS

475.2

96

15.9

7(1

30–716)

585.1

56

68.0

8(3

45–1,7

46)

478.6

46

45.5

7(2

22–990)

473.7

16

87.3

3(2

94–680)

SA

467.1

46

35.2

3(2

47–1,2

27)

4886

27.9

8(4

23–600)

395.7

56

20.7

1(3

42–443)

555.4

26

95.7

4(3

63–1,0

99)

Pro

tein

s(g

/L)

WS

66.3

36

11.2

3(5

0.5

–80.0

)68.3

76

17.5

2(4

9.0

–86.0

)68.7

16

17.5

8(6

0.0

–81.0

)87.9

06

45.1

2(7

6.0

–98.5

)S

A72.1

26

14.4

7(4

3.1

–90.0

)72.0

629.2

1(5

8.0

–78.0

)79.2

56

29.2

6(7

2.0

–86.0

)85.1

46

18.9

5(7

9.0

–93.0

)

Alb

um

in(g

/L)

WS

32.9

76

10.2

8(2

4.3

–61.1

)32.7

66

15.3

1(2

6.6

–40.7

)29.1

16

7.7

2(2

7.4

–34.2

)18.8

64.6

3(1

7.0

–19.5

)S

A43.4

86

38.3

1(3

0.3

–57.7

)30.9

36

27.9

3(2

3.0

–35.0

)27.9

36

11.9

2(2

6.5

–30.3

)28.5

613.1

2(2

3.5

–31.3

)

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par

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with both infested and healthy ibexesbetween 2 and 11 kg, respectively, heavierin the warm season (see Table 1).

The effects of mange on both hemato-logic and serum biochemical parametersdepended on the period of the year(wMange status*Period of the year51 for bothparameters; Table 4). This model ex-plained between 97.8% (F7,1285848.4) to82.6% (F7,128551.44) of the observedhematologic and serum biochemicalchanges of ibexes, respectively. Neverthe-less, all hematologic parameters were notaffected by mange or seasons in the sameway (Tables 5, 6). The single effect ofmange influenced RBC, hemoglobin, he-matocrit, MCV, leukocytes, band neutro-phils, and monocytes, but MCH, MCHC,and neutrophils were affected by bothmange and the period of the year(Table 5). Similarly, cholesterol, urea,and AST were solely influenced by theseverity of mange infection, whereasglucose and proteins were also influencedby the period of the year. The interaction

of effects of mange and the period of theyear influenced values of creatine, LDHand albumin (Table 6), and CK wasexclusively affected by the period of theyear.

DISCUSSION

Ibexes in our study were chemicallyimmobilized in a way similar to thatdescribed elsewhere (Casas-Dıaz et al.2011), so confounding effects due todifferent capture methods were not ex-pected. Anemia detected by reducedRBC, Hb, and hematocrit in scabieticibexes was in agreement with previousstudies (Arlian et al. 1988; Kido et al.2011). Anemia in scabietic ibexes might bedue to the inflammatory process associat-ed with mange (Pence and Ueckermann2002). In response to inflammatory cyto-kines, iron may be sequestered in bonemarrow macrophages as a protectivemechanism to deny this key element topotential pathogens that require it forgrowth and multiplication (Carlson 1990;

TABLE 4. Model selection for the seasonal effects of sarcoptic mange on body weight and hematologic andserum biochemical parameters in 136 male Iberian ibex, Capra pyrenaica, .3 yr old, captured in the SierraNevada Natural Space, southern Spain, 2005–2012. Models with substantial support are in bold.a

Biological models K AICc Di W i

Body weight

Mange status*Period of the year 9 1,008.31 0 0.52Mange status+Period of the year 6 1,008.47 0.17 0.47

Mange status 5 1,028.80 20.49 ,0.01Period of the year 3 1,054.21 45.90 ,0.01Mo 2 1,066.92 58.61 ,0.01

Hematologic parameters

Mange status*Period of the year 9 10,354.79 0 1Mange status+Period of the year 6 10,436.41 80.84 0

Mange status 5 10,439.68 83.92 0Mo 2 10,847.27 491.14 0Period of the year 3 10,848.08 492.04 0

Serum-biochemical parameters

Mange status*Period of the year 9 9,341.04 0 1Mange status+Period of the year 6 9,378.06 37.01 0Mange status 5 9,405.88 64.83 0Period of the year 3 9,419.90 78.86 0Mo 2 9,446.14 105.10 0

a K 5 number of parameters; AICc 5 Akaike Information Criterion corrected for small samples sizes Di 5 difference ofAICc with respect to the best model; W i 5 Akaike weight; Mo 5 null model.


Weiss and Goodnough 2005). Iron-relatedmeasurements were not carried out in ourstudy. Iron may also have a nutritionalorigin due to combined protein, vitamin,and mineral deficiencies (Watson andCanfield 2000). Neutrophils were higherin ibexes affected by sarcoptic mange thanin clinically normal animals, in agreementwith previous studies on infected mam-mals (Kido et al. 2011). Season-relatedneutrophilia has been reported in wildungulates (Cross et al. 1994). In winter,the additive effect of season and diseasecould lead to a rise in neutrophils and,therefore, in total leukocytes.

Ibexes showing more extensive andchronic lesions (category 3) showed thelowest values of blood eosinophilsthroughout the year. The number of

eosinophils in the dermis was positivelycorrelated with the density of mites(Skerrat 2003); the fact that mites de-crease in lesions as the hypersensitivityreaction progresses (Arlian 1996) mayexplain our finding. However, we did notcount mites.

The increased blood urea, particularly inwinter-spring, coupled with a decrease increatine concentration suggest an acceler-ating net catabolism of body proteinstorage consistent with the progressiveweight loss previously reported in scabieticAlpine chamois (Tataruch et al. 1985).Scabietic animals had higher values of totalserum proteins than nonaffected animals,which is expected in chronic infections(Jain 1993; Lastras et al. 2000). Values ofother analytes such as AST, CK, and LDH

TABLE 5. Analysis of variance table showing those hematologic parameters influenced by the period of year,mange infection, or their interaction in 136 male Iberian ibex, Capra pyrenaica, .3 yr old, captured in theSierra Nevada Natural Space, southern Spain, 2005–2012. For both eosinophils and lymphocytes, neithermange infection, period of year, nor their interaction were statistically significant.

Parametera Mean sum of squares F P

RBC

Mange status 35.59 12.92 ,0.001

Hemoglobin

Mange status 5,214.21 13.61 ,0.001

Hematocrit

Mange status 99.08 7.41 ,0.001

MCH

Mange status*Period of the year 1.39 3.22 0.02

MCV

Mange status 28.16 4.88 ,0.001

MCHC

Mange status*Period of the year 5,214.2 13.61 ,0.001

Leukocytes

Mange status 0.32 13.71 ,0.001

Bands

Mange status 2.28 11.72 ,0.001

Neutrophils


Monocytes

Mange status 1.97 5.28 0.001

a RBC 5 red blood cells; MCH 5 mean corpuscular hemoglobin; MCV 5 mean corpuscular volume; MCHC 5 meancorpuscular hemoglobin concentration.


differ and agree with those described insouthern chamois and Iberian ibex (Lopez-Olvera et al. 2006; Casas-Dıaz et al. 2008).

In conclusion, sarcoptic mange pro-duced a marked reduction of body weightin infested ibexes with a clear seasonaltrend. Scabietic animals exhibited anemiaand poor nutritional condition. Most ofthe hematologic parameters studied wererelated to mange status and leukograms,suggesting secondary infection was in-volved. Some of the biochemical parame-ters sampled depended on both thedisease stage and the period of the year(e.g., glucose, creatine, LDH, proteins,and albumin); others (e.g., cholesterol,urea, and AST), depended exclusively onmange status; finally, CK depended solelyon the period of the year.

Continued studies of how food shortag-es, due to changes in feeding behavior,

primary productivity, or overpopulation ofwild and domestic herbivores, influencethe response of ibexes to mange infectionwill provide new strategies and opportuni-ties for controlling this disease in the wild.

ACKNOWLEDGMENTS

Thanks to the staff of the Sierra NevadaNatural Space for their help. Our study wasfunded by the Ministerio de Economıa yCompetitividad of the Spanish Government(project CGL2012-40043-C02-01). The au-thors’ research activities are partially fundedby the Plan Andaluz de Investigacion (RNM-118 group), and E.S. was supported by thepostdoctoral program (SFRH/BPD/96637/2013) of the Fundacao para a Ciencia e aTecnologia, Portugal. This study compliedwith current Andalusian and Spanish laws.

LITERATURE CITED

Akomas SC, Obijuru OC, Herbert U. 2011. Hema-tologic and serologic changes following ivermec-

TABLE 6. Analysis of variance table showing those serum biochemical parameters influenced by period ofthe year, mange infection, or their interaction in 136 male Iberian ibex, Capra pyrenaica, .3 yr old, capturedin the Sierra Nevada Natural Space, southern Spain, 2005–2012.

Parametera Mean sum of squares F P

Glucose

Mange status 15.09 3.2 0.02Period of the year 28.66 6.18 0.02

Cholesterol

Mange status 0.19 3.99 0.01

Urea

Mange status 507.2 3.79 0.01

Creatinine


AST

Mange status 28.16 4.88 ,0.001

CK

Period of the year 177,796.5 4.58 0.03

LDH

Mange status*Period of the year 69,493 3.36 0.02

Proteins

Mange status 103,139 16.53 ,0.001Period of the year 60,057 9.62 0.002

Albumin

Mange status*Period of the year 16,369 3.81 0.01

a AST 5 aspartate aminotransferase; CK 5 creatine kinase; LDH 5 lactate dehydrogenase.


tin treatment in mange infested West Africandwarf goats. Adv Environ Biol 5:2557–2560.

Arlian LG. 1996. Immunology of scabies. In: Theimmunology of host-ectoparasitic arthropodrelationships, Wikel SK, editor. CAB Interna-tional, Wallingford, UK, pp. 232–258.

Arlian LG, Ahmed M, Vyszenski-Moher DL. 1988.Effects of S. scabiei var. canis (Acari: Sarcopti-dae) on blood indexes of parasitized rabbits.J Med Entomol 25:360–369.

Burnham KP, Anderson DR. 2002. Model selectionand multimodel inference: A practical informa-tion-theoretic approach. Springer-Verlag, NewYork, 488 pp.

Carlson GP. 1990. Diseases of the hematopoietic andhemolymphatic systems. In: Large animal internalmedicine, Smith BP, editor. C. V. Mosby Compa-ny, Maryland Heights, Missouri, pp. 1068–1126.

Casas-Dıaz E, Lopez-Olvera JR, Mentaberre G,Marco I, Lavın S. 2008. Hematologic andbiochemical values for Spanish ibex (Caprapyrenaica) captured via drive-net and box-trap.J Wildl Dis 44:965–972.

Casas-Dıaz E, Marco I, Lopez-Olvera JR, MentaberreG, Lavın S. 2011. Comparison of xylazine-ketamine and medetomidine-ketamine anaesthe-sia in the Iberian ibex (Capra pyrenaica).Eur J Wildl Res 57:887–893.

Cross JP, Mackintosh CG, Griffin JFT. 1994.Haematological reference values for farmedred deer (Cervus elaphus) in New Zealand.Comp Haematol Int 4:76–85.

Fandos P. 1991. La cabra montes (Capra pyrenaica)en el Parque Natural de las Sierras de Cazorla,Segura y Las Villas. ICONA-CSIC, Madrid,Spain, 176 pp.

Jain NC. 1993. Essentials of veterinary hematology.Lea and Febiger, Philadelphia, Pennsylvania,417 pp.

Kido N, Kamegaya C, Omiya T, Wada Y, TakahashiM, Yamamoto Y. 2011. Hematology and serumbiochemistry in debilitated, free-ranging raccoondogs (Nyctereutes procyonoides) infested withsarcoptic mange. Parasitol Int 60:425–428.

Lastras ME, Pastor J, Marco I, Ruiz M, Vinas L,Lavin S. 2000. Effects of sarcoptic mange onserum proteins and immunoglobulin G levels inchamois (Rupicapra pyrenaica) and Spanish ibex(Capra pyrenaica). Vet Parasitol 88:313–319.

Lopez-Olvera JR, Marco I, Montane J, Lavın S. 2006.Haematological and serum biochemical values ofsouthern chamois (Rupicapra pyrenaica). VetRec 158:479–484.

Peinado M, Rivas-Martınez S, (editors). 1987. Lavegetacion de Espana. Servicio de Publicaciones

de la Universidad de Alcala de Henares, Alcalade Henares, Spain, 744 pp.

Pence DB, Ueckermann E. 2002. Sarcoptic mange inwildlife. Rev Sci Tech OIE 21:385–398.

Perez JM, Granados JE, Sarasa M, Serrano E. 2011.Usefulness of estimated surface area of damagedskin as a proxy of mite load in the monitoring ofsarcoptic mange in free-ranging populations ofIberian wild goat, Capra pyrenaica. Vet Parasitol176:258–264.

R Development Core Team. 2014. R: A language andenvironment for statistical computing. R Founda-tion for Statistical Computing, Vienna, Austria,http://www.R-project.org. Accessed January 2014.

Sarasa M, Rambozzi L, Rossi L, Meneguz PG,Serrano E, Granados JE, Gonzalez FJ, FandosP, Soriguer RC, Gonzalez G, et al. 2010.Sarcoptes scabiei: Specific immune response tosarcoptic mange in the Iberian ibex Caprapyrenaica depends on previous exposure andsex. Exp Parasitol 124:265–271.

Serrano E, Gallego L, Perez JM. 2004. Ossification ofthe appendicular skeleton in the Spanish ibexCapra pyrenaica Schinz, 1838 (Artiodactyla:Bovidae), with regard to determination of age.Anat Histol Embryol 33:33–37.

Serrano E, Gonzalez FJ, Granados JE, Fandos P,Soriguer RC, Perez JM. 2008. The use of totalserum proteins and triglycerides for monitoringbody condition in the Iberian wild goat (Caprapyrenaica). J Zoo Wildl Med 39:646–649.

Serrano E, Granados JE, Sarasa M, Gonzalez FJ,Fandos P, Soriguer RC, Perez JM. 2011. Theeffects of winter severity and population densityon body stores in the Iberian wild goat (Caprapyrenaica) in a highly seasonal mountain envi-ronment. Eur J Wildl Res 57:45–55.

Skerrat LF. 2003. Cellular response in the dermis ofcommon wombats infected with Sarcoptes sca-biei var. wombati. J Wildl Dis 39:93–202.

Tataruch F, Steineck T, Onderscheka K. 1985.Investigations on the metabolism of chamoissuffering from sarcoptic mange. In: The biologyand management of mountain ungulates, LovariS, editor. Croom Helm, London, UK, pp. 250–255.

Watson ADJ, Canfield PJ. 2000. Nutritional defi-ciency anaemias. In: Schalm’s veterinary hema-tology, 5th Ed., Feldman BF, Zinkl JG, Jain NC,editors. Lippincott Williams & Wilkins, Balti-more, Maryland, pp. 190–195.

Weiss G, Goodnough LT. 2005. Anemia of chronicdisease. N Engl J Med 352:1011–1123.

Submitted for publication 13 September 2013.Accepted 6 June 2014.


Documents

DISTINGUISHING DISEASE EFFECTS FROM ENVIRONMENTAL EFFECTS IN A MOUNTAIN UNGULATE: SEASONAL VARIATION IN BODY WEIGHT, HEMATOLOGY, AND SERUM CHEMISTRY AMONG IBERIAN IBEX ( CAPRA PYRENAICA