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Revista de Biología Tropical, ISSN: 2215-2075, Vol. 70: 495-503, January-December 2022 (Published Jul. 14, 2022)

Hematological reference values for Alouatta palliata

(Primates: Atelidae) and Cebus imitator (Primates: Cebidae)

from the Pacific Coast of Costa Rica

Andrea Chaves Ramírez1*; https://orcid.org/0000-0002-6237-0678

Genuar Nuñez Vega1; https://orcid.org/0000-0001-6264-335X

Randall Arguedas Porras2; https://orcid.org/0000-0001-5227-6314

José Bonilla Vargas3; https://orcid.org/0000-0002-6618-6384

Sandra Silva de la Fuente3; https://orcid.org/0000-0001-9301-9234

María Arias-Echandi4; https://orcid.org/0000-0002-8611-4433

Gustavo Gutiérrez-Espeleta1; https://orcid.org/0000-0003-4133-5002

1. Escuela de Biología, Universidad de Costa Rica, San Pedro Montes de Oca 11501-2060, San José, Costa Rica;

andrea.chavesramirez@ucr.ac.cr (Correspondence*), gustavo.gutierrez@ucr.ac.cr; gero31289@gmail.com

2. Universidad Técnica Nacional, Sede Atenas, Alajuela, Costa Rica; rarguedasp@utn.ac.cr

3. Centro de Investigación en Biología Celular y Molecular, Universidad de Costa Rica, San Pedro Montes de Oca

11501-2060, San José, Costa Rica; jose.bonilla@ucr.ac.cr, sandra.silva@ucr.ac.cr

4. Facultad de Microbiología, Universidad de Costa Rica, San Pedro de Montes de Oca, 11501-2060, San José, Costa

Rica; marialauraariasechandi@gmail.com

Received 17-VIII-2021. Corrected 07-IV-2022. Accepted 06-VII-2022.

ABSTRACT

Introduction: Wildlife hematological patterns are fundamental for health monitoring, and allows elucidating

variations both within and between populations. Among these, hematological parameters are particularly valu-

able to evaluate the health status of neotropical primate species in the wild.

Objective: To define hematological reference values for two species of monkeys in Costa Rica.

Methods: During 2014, we collected blood samples from free-ranging mantled howler monkeys, Alouatta pal-

liata (17 females, 18 males) and white-faced capuchin monkeys, Cebus imitator (5 females, 7 males) in seven

localities of the Costa Rican Pacific coast.

Results: For both species, the hematological values were higher in males, and howler monkey populations dif-

fered significantly except for platelets.

Conclusions: These hematological values, which differ by sex and locality, will help evaluate the health status

of these neotropical primate populations.

Key words: Neotropical primates; mantled howler monkey; white-faced capuchin monkey; hematology;

Costa Rica.

https://doi.org/10.15517/rev.biol.trop.2022.48062

VERTEBRATE BIOLOGY

Neotropical primates (NP; suborder Plat-

yrrhini) have a wide geographical distribution,

that includes the Southern part of Mexico, Cen-

tral and South America, and are represented by

a huge variety of species, with a remarkable

diversification in their biology, life history and

behavior (Rosenberger & Hartwig, 2001). In

Costa Rica, four different species of NP are

distributed, including mantled howler mon-

key (Alouatta palliata), white-faced capuchin

496 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 70: 495-503, January-December 2022 (Published Jul. 14, 2022)

monkey (Cebus imitator), spider monkey

(Ateles geoffroyi) and squirrel monkey (Saimiri

oerstedii). Three of these are at risk of extinc-

tion (mantled howler, spider and squirrel mon-

keys), and one (white-faced capuchin monkey)

is a threatened or vulnerable species, according

to the Costa Rican legislation (Decree No.

2635) and the International Union for Conser-

vation of Nature (IUCN) (Cuarón et al., 2008;

MINAE, 1997; Wong et al., 2008). At the same

time, these three species are included in appen-

dix 1 of the Convention on International Trade

of Endangered Species of Wild Fauna and Flora

(CITES, 2021) and the white-faced capuchin

monkey has yet to be classified.

Costa Rica is considered one of the coun-

tries with the greatest diversity in the world

and has a wide variety of microclimates and

life zones that favor its notable levels of biodi-

versity. However, the biological diversity of the

country is currently threatened by the illegal

extraction of wood, the conversion of forests

for agricultural activities or by tourist and real

estate development, which strongly affect the

connectivity between forest patches (Calvo-

Obando & Ortis-Malavassi, 2012). As natural

environments are transformed, through anthro-

pogenic activities, the natural habitat of the NP

is either reduced in size or fragmented, directly

affecting them. Furthermore, as monkey´ popu-

lations concentrate, troops decrease in number

of individuals, causing a reduction of the

genetic pool, an increase in stress, promoting

immunosuppression and the eventual transmis-

sion of diseases (Gilbert & Dodds, 1987).

Given this, counting on reference data

about health status, genetic variety, biological

characteristics, among other variables, are a

priority in conservation programs. Hematologi-

cal reference values are a valuable tool to help

determine the health status of wild populations

(Takeshita et al., 2011). This data may be used

as comparison patterns between populations

that are distributed in landscapes of different

forest types or captive environments. And, in

addition, may also be useful for reintroduction

and management programs (Sánchez-Sarmien-

to et al., 2014).

Health studies and the establishment of

normal blood values research have increased

over the last decades, providing an important

amount of information on normal parameters

for several species and are valuable tools for

assessing and monitoring the health and resil-

ience of wild populations (Maceda-Veiga et al.,

2015). This information helps identify potential

effects of diseases, pollutants, or other chang-

ing environmental conditions that would be

difficult to understand without knowledge of

normal species variations in blood variables.

These kinds of studies usually include variables

that are used in veterinary medicine and are

assumed to have the same utility in wild popu-

lations (Arguedas et al., 2021).

Health status evaluations, taking in con-

sideration hematological parameters, have been

done for several species of NP and are used

as a reference for the comparisons between or

within species (García-Feria et al., 2017). Nev-

ertheless, there are few studies published on

the hematology of NP in natural environments

from Central America, due to lack of project

financing or even research interest. In this

study, we evaluate some hematological analytes

of mantled howler monkeys (Alouatta palliata)

and white-faced capuchin monkeys (Cebus

imitator) in the wild coming from natural envi-

ronments from Costa Rica, by analyzing such

parameters and comparing the results obtained

between genders and the populations sampled.

MATERIALS AND METHODS

The authors confirm that the ethical poli-

cies of the journal, as noted on the journal’s

author guidelines page. All procedures for trap-

ping and handling NP were approved by bioeth-

ics and welfare permits given by the University

of Costa Rica and the capture permits given by

SINAC (Resolution No. 27 2013 SINAC).

Animal Sampling: During 2014, mantled

howler and white-faced capuchin monkeys

from Costa Rica were captured (Fig. 1). Cap-

ture was done using 3.3-1.1 mg/kg Zoletil

50® (Virbac) or Ketamine 10 % (Bremer

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Pharma GmhH, 5-20 mg/kg) with Xylazine

2 % (Virbac, 0.5-2.0 mg/kg) (Glander et al.,

1991; Varela, 2006; West et al., 2007) in darts

(PneuDart. Inc, Type P, 1cc) with a compressed

gas rifle (PneuDart. Inc, model X-Caliber

Gauged CO2). Lateral faces of triceps and

femoral quadriceps were the target of injection

(Glander et al., 1991). Vital signs, including

heart rate, respiratory rate, body temperature,

oximetry, and mucous membrane color were

observed during immobilization. A physical

examination was performed on the animals

looking for abnormalities that could indicate

illness. When animals were fully recovered

from anesthesia, they were released. General

body condition of the individual was evaluated

using a five-point scale.

Laboratory Analysis: Once the individual

was anesthetized, 2-4 ml blood samples were

extracted from the femoral vein using the

Vacutainer® system. Samples were collected in

EDTA tubes and transported to the laboratory

at 4 ºC. At the lab, the following hematological

parameters were evaluated using Sysmex KX

21 equipment, (Sysmex Corporation, Japan):

red blood cell count (RBC, 106/mm3), hemo-

globin (Hb, g/dl), hematocrit (Hct, %), mean

corpuscular volume (MCV, fl), mean corpuscu-

lar hemoglobin (MCH, pg), mean corpuscular

hemoglobin concentration (MCCH, g/l), plate-

let count (PLT, 103/ mm3), and white blood cell

count (WBC, 103/ mm3).

Statistical analysis: For each parameter

measured, Mann-Whitney test was performed,

depending on the normality of data a Wilcoxon

and t student tests were performed in order to

determine if there were significant differences

between females and males from each species

sampled. Also, for mantled howler monkeys,

an ANOVA tests was performed to determine

if there are significant differences between

sampled populations. Statistical analysis was

done in R program (R Core Team, 2016) with a

< 0.05 significance level.

RESULTS

A total of 35 (17 females and 18 males)

mantled howler monkeys and 12 (5 females and

7 males) white-faced capuchin monkeys were

captured in seven localities from Costa Rica,

five localities for mantled howler monkeys,

including: San Lucas island (9°56’24.28” N

& 84°54’15.24” W), Nicoya (10°08’40” N &

85°27’22” W), Hermosa beach (4°46’00” N

& 85°16’00” W), Manuel Antonio (9°22’32”

N & 84°08’09” W), Curú (9°47’35.55” N &

84°55’32.49’’ W), and 2 localities for white-

faced capuchin monkeys, including Manuel

Antonio (9°22’32” N & 84°08’09” W) and

Curú (9°47’35.55” N & 84°55’32.49” W) (Fig.

1), (Table 1). All individuals appeared to be

healthy and did not present any sign of disease.

For mantled howler monkeys, the mea-

sures of Hemoglobin (Hb), Hematocrit (Htc),

red blood cells count (RBC), mean corpuscular

volume (MCV), mean corpuscular hemoglo-

bin (MCH), Platelets (PLT) and White blood

cell count (WBC) were higher in males than

females. For white-faced capuchin monkeys,

values of Hb, Htc, RBC, PLT and WBC were

also higher for males than females, but MCV,

and MCH values were similar for both. Never-

theless, no significant differences were found

between males and females for any of the

parameters analyzed in both species (Table 2).

Significant differences for mantled howler

monkeys and in all the parameters evaluated

TABLE 1

Distribution of individual mantled howler monkeys

(Alouatta palliata) and white-faced capuchin monkeys

(Cebus imitator) according to their original location

Capture site

Species

Mantled howler

monkey

(Alouatta palliata)

white-faced

capuchin monkey

(Cebus imitator)

Curú 1 8

Manuel Antonio 2 4

Nicoya 9 0

Hermosa Beach 4 0

San Lucas Island 19 0

Total 35 12

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were determined, except for PLT. Individuals

from the Nicoya locality were the individuals

that presented the highest scored hematological

values. At Curú just one individual was cap-

tured, so it was not included in the analysis

(Table 3).

For the other hematological parameters

evaluated, 3/35 (8.6 %) of mantled howler

monkeys and 3/12 (25 %) of white-faced capu-

chin monkeys presented WBC counts above 10

400/mm3. In the same way, 16/35 (45.7 %) of

mantled howler monkeys and 2/12 (16.7 %) of

white-faced capuchin monkeys presented PLT

values above 250 000/mm3, and one howler

monkey presented an abnormally low value of

platelets (17 300/mm3).

DISCUSSION

Actual information related to the biol-

ogy, ecology, health and diseases supports and

facilitates programs related to the management,

medicine and conservation of wildlife popula-

tions (Varela, 2006). Changes in landscape,

habitat fragmentation and the anthropogenic

activities directly affect the wellness of NP,

and this may be reflected in the hematological

parameters. In order to obtain and compare the

reference patterns of hematological parameters

for mantled howler and white-faced capuchin

monkeys from Costa Rica, free-living individu-

als of both species were captured at different

geographical regions of Costa Rica.

The results of this study are the first

hematological parameters reported for mantled

howler monkeys (A. palliata) in Costa Rica.

When these results are compared with values

published for free living A palliata individuals

from Tabasco, Mexico (Canales-Espinosa et

al., 2015), and for A. pigra individuals from

Balancán, México (García-Feria et al., 2017),

differences in the averages of parameters

Fig. 1. Location of field sites in Costa Rica: A. Hermosa Beach. B. Nicoya. C. Curú. D. San Lucas Island. E. Manuel

Antonio.

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measured are evident. Nevertheless, when our

results are compared with the ones reported

for Mexican howler monkeys, values obtained

are within the maximal and minimal ranges

described (Canales-Espinosa et al., 2015).

For white-faced capuchin monkeys, the

hematological parameters obtained in this work

are similar to those reported by Bernal-Valle et

al (2020), where 16 out of 25 individuals also

from Costa Rica. The median value for HCT

reported by Bernal-Valle et al (2020) is 40.5

% for males and 37.5 % for females, compared

with the values of 43.5 and 38.6 % obtained

in this work. In the same way, the hemoglobin

values obtained for males and females in both

studies are similar (12.7 g/dl and 10.5 g/dl

compared with 12 g/dl and 11.4 g/dl respec-

tively). An important difference between both

studies lies in the values obtained for white

blood cells, where Bernal-Valle (2020) reports

median concentrations of 5 700 WBC/ mm3

in females, compared with the values of 8 900

WBC/mm3 obtained in the present study. It

is important to highlight those average values

obtained in this study for white-faced capuchin

monkeys are similar to the ones reported by

Larsson et al (1999) in Brazil. Nonetheless,

since different hematological analyzers were

used in all the studies mentioned, it is important

to always take this bias in account when com-

paring hematological values.

There are no significant differences

between genders for any of the parameters

evaluated in both species of monkeys studied.

However, this data contrasts with those report-

ed by other researchers, where values observed

for males are greater than those reported for

females in most of the parameters analyzed

(Flaiban et al., 2009; García-Feria et al., 2017;

Kagira et al., 2007; Larsson et al., 1999; Moore,

2000; Sánchez-Sarmiento et al., 2014; Takeshi-

ta et al., 2011; Wirz et al., 2008). This might be

due, principally, to hormonal influence, since

testosterone stimulates erythropoiesis, while

estrogen inhibits it (Kagira et al., 2007; Wirz et

al., 2008) or to effects of the menstrual cycle,

pregnancy period and breastfeeding.

TABLE 2

Hematological values of mantled howler monkey (Alouatta palliata) and white-faced capuchin monkey (Cebus imitator) in Costa Rica

Parameters

Mantled howler monkey White-faced capuchin monkey

Females Males Females Males

X ± SD Median MIN-MAX X ± SD Median MIN-MAX X ± SD Median MIN-MAX X ± SD Median MIN-MAX

Hb (g/dl) 11.1 ± 1.4 10.9 9.0-13.8 11.9 ± 1.1 11.9 9.2-14.0 11.7 ± 1.6 11.4 10.2-14.0 12.2 ± 1.7 12.0 10.6-15.3

Hct (%) 37.9 ± 5.7 37.7 30.5-47.5 41.2 ± 4.6 41.0 30.8-48.4 40.5 ± 5.8 38.6 34.6-50.9 42.6 ± 6.2 43.5 36.0-52.8

RBC (x 106/ mm3)4.0 ± 0.4 4.0 3.3-4.8 4.1 ± 0.5 4.2 3.1-5.0 5.2 ± 0.6 5.4 4.2-5.9 5.5 ± 0.7 5.2 4.6-6.7

MCV (fl) 95.5 ± 6.5 96.6 78.2-106.6 98.8 ± 4.5 98.1 91.3-109.0 78.7 ± 6.8 79.0 71.0-89.8 78.7 ± 7.7 82.9 66.9-86.3

MCHC (g/dl) 29.5 ± 1.5 29.1 27.2-32.5 29.0 ± 1.4 28.9 25.2-31.6 28.9 ± 0.8 29.2 27.5-29.8 28.9 ± 0.9 29.0 27.6-30.0

MCH (pg) 28.0 ± 1.8 28 22.1-30.4 28.6 ± 1.7 28.5 23.5-31.8 22.7 ± 1.5 22.3 21.0-24.7 22.6 ± 2.0 23.3 19.9-24.4

PLT (x 103/ mm3)215.4 ± 72.5 209 86-333.0 220.7 ± 71.6 238 17.3-329.0 150.0 ± 85.4 128 49.0-280 219.6 ± 132.8 214 44.0-325.0

WBC (x 103/ mm3)8.1 ± 2.4 7.8 2.9-12.7 8.7 ± 3.4 8.1 4.6-19.9 8.9 ± 4.2 9.6 3.5-13.8 11.1 ± 4.7 10.2 5.1-18.2

Hemoglobin (Hb), Hematocrit (HCT), red blood cells count (RBC), mean corpuscular volume (MCV), mean corpuscular hemoglobin concentration (MCHC), mean corpuscular

hemoglobin (MCH), Platelets (PLT) and White blood cell count (WBC).

500 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 70: 495-503, January-December 2022 (Published Jul. 14, 2022)

Differences between population may have

occurred because of the excitement and ten-

sion that wild animals suffer during its capture,

the individual may show signs of acute stress,

known as “alarm reaction,” which may be the

cause of an increase in the values of various

parameters, including RBC, Hb, HCT, MCV,

MCH, PLT and WBC (Thrall, 2004). In nor-

mal conditions, stress is an adaptive stimulus

for a changing environment (Fowler, 1978)

and causes beneficial metabolic changes for

the protection against external aggressions

(Cubas, 2007). On the other hand, other factors

may cause differences in some hematological

parameters, for example, some degree of dehy-

dration can be a reason to have higher HCT, Hb

and RBC, which can be suspected from animal

coming from drier regions such as dry forest

environments, like Nicoya.

Some of the individuals that had WBC

higher than 10 000/mm3, can be because of an

inflammatory process, bacterial infection or a

severe stress reaction during capture (Thrall,

2004), further studies evaluating leukocyte

response in these species have to be done in

order to confirm these changes.

Apparent thrombocytosis (>250 000/mm3)

here found in 16 howler monkeys and 2 capu-

chin monkeys, one cause of this, is reactive

thrombocytosis, which is driven by elevated

endogenous levels of thrombopoietin, inter-

leukin-6, other cytokines, or catecholamines

that may be produced in inflammatory, infec-

tious, or neoplastic conditions or in situations

of stress (Schafer, 2004). Another finding was

that one individual of howler monkey, pre-

sented an abnormally low platelet count, this

may be, it can be due several reasons, for

example, infectious agents or immune-mediat-

ed disorders (Thrall, 2004), or incidental, like

platelet clumping due to venipuncture, which

can be this case, since this particular indi-

vidual, showed values within the normal ranges

in the sample.

The difference in the hematological param-

eters evaluated might also be associated with

other factors, including the type of feeding,

diet and environmental factors among others.

Health evaluations of free-ranging primates

provides important information about the inci-

dence and prevalence of infectious diseases, as

well as their general health status and allows

elucidating variations both within and between

populations (Riviello & Wirz, 2001; Takeshita

et al., 2011).

Health evaluations should not be limited to

epidemiological surveillance and should also

consider animals` clinical and physiological

parameters (Sánchez-Sarmiento et al., 2014).

For example, normal hematological values are

TABLE 3

Hematological values of mantled howler monkey (Alouatta palliata) according to the sampling site in Costa Rica

Parameters Curú San Lucas Island Manuel Antonio Hermosa Beach Nicoya

1 individual X ± SD X ± SD X ± SD X ± SD

Hb (g/dl)*911.6 ± 1.3 11.6 ± 0.2 9.8 ± 0.2 12.2 ± 0.9

Hct (%)*31.9 39.8 ± 4.8 37.9 ± 1 31.3 ± 0.3 43.8 ± 3.4

RBC (x 106/mm3)* 4.1 4.1 ± 0.5 4.0± 0.2 3.5 ± 0.1 4.3 ± 0.4

VCM (fl)*78.2 98.1 ± 2.4 95.3 ± 3.3 90.1 ± 1.7 101.4 ± 5.3

MCHC (g/dl)*28.2 29.3 ± 1 30.5 ± 0.2 31.4 ± 0.3 27.8 ± 1.1

HCM (pg)*22.1 28.7 ± 1.1 29 ± 1.2 28.2 ± 0.4 27.9 ± 2.2

PLT (x 103/mm3) 86 239.5 ± 57.9 146.5 ± 23.3 190.5 ± 70.7 217.5. ± 86.6

WBC (x 103/mm3)* 2.9 8.8 + 3.1 12.8 + 4.2 7.4 + 0.4 8.4 + 2.7

Hemoglobin (Hb), Hematocrit (HCT), red blood cells count (RBC), mean corpuscular volume (MCV), mean corpuscular

hemoglobin concentration (MCHC), mean corpuscular hemoglobin (MCH), Platelets (PLT) and White blood cell count

(WBC), (*) ANOVA P < 0.05.

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of special value in Costa Rican primates, since

they frequently suffer from car accidents and

electrocutions, Several species of Costa Rican

wildlife are suffering terrible injuries along

the power lines and transformers in rural areas

of the country., and hematological parameters

can be a way to predict (up to a point) the pos-

sible outcome of the patients and to be able to

treat the animal in a more comprehensive way

(Sánchez-Murillo & Arguedas, 2021). Besides,

nonhuman primates exhibit a pronounced

stress when they are confined (Suleman et

al., 2000), and require a long period of time

for adapting to captivity. Thus, hematological

parameters may take even months to stabilize

(Kagira et al., 2007).

Hematological parameters allow research-

ers and wildlife managers to predict and under-

stand different disease processes, stress levels

and hydration status of wild populations and

thus, determine whether a population faces

any stress related to environmental changes or

anthropogenic causes. At the same time, these

results can be used as a baseline when NP must

be managed in captivity or during rehabilitation.

Ethical statement: the authors declare

that they all agree with this publication and

made significant contributions; that there is no

conflict of interest of any kind; and that we fol-

lowed all pertinent ethical and legal procedures

and requirements. All financial sources are

fully and clearly stated in the acknowledge-

ments section. A signed document has been

filed in the journal archives.

ACKNOWLEGMENTS

We appreciate the collaboration of all

those persons that participated in the field work

realized, also to Universidad de Costa Rica for

the funds granted for this research.

RESUMEN

Valores de referencia hematológicos para Alouatta

palliata (Primates: Atelidae) y Cebus imitator

(Primates: Cebidae) de la costa Pacífica de Costa Rica

Introducción: Los patrones hematológicos de la vida sil-

vestre son fundamentales para el monitoreo de la salud y

permiten dilucidar las variaciones tanto dentro como entre

poblaciones. Entre estos, los parámetros hematológicos son

particularmente valiosos para evaluar el estado de salud

de las especies de primates neotropicales en la naturaleza.

Objetivo: Definir valores de referencia hematológicos para

dos especies de monos en Costa Rica.

Métodos: Durante el 2014 recolectamos muestras de

sangre de monos aulladores de manto, Alouatta palliata

(17 hembras, 18 machos) y monos capuchinos cariblancos,

Cebus imitador (5 hembras, 7 machos) en siete localidades

de la costa Pacífica de Costa Rica.

Resultados: Para ambas especies, los valores hematoló-

gicos fueron mayores en los machos, y las poblaciones de

monos aulladores difirieron significativamente con excep-

ción de las plaquetas.

Conclusiones: Estos valores hematológicos, que difieren

según el sexo y la localidad, ayudarán a evaluar el estado

de salud de estas poblaciones de primates neotropicales.

Palabras clave: primates neotropicales; mono aullador

de manto; mono capuchino cariblanco; hematología;

Costa Rica.

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