ISSN Versión impresa 2218-6425 ISSN Versión Electrónica 1995-1043

Neotropical Helminthology, 2017, 11(2), jul-dic: 309-316.

ORIGINAL ARTICLE / ARTÍCULO ORIGINAL

OCCURRENCE OF AMBLYOMMA ROTUNDATUM (KOCH, 1844) IN RHINELLA MARINA

(LINNAEUS, 1758) (ANURA: BUFONIDAE) FROM IQUITOS, PERU

OCURRENCIA DE AMBLYOMMA ROTUNDATUM (KOCH, 1844) EN RHINELLA MARINA

(LINNAEUS, 1758) (ANURA: BUFONIDAE) DE IQUITOS, PERÚ

1Federal University of Piauí (Universidade Federal do Piauí), Piauí, Brazil.

2São Paulo State University (Unesp), Institute of Biosciences, Botucatu.

3Federico Villarreal National University, El Agustino, Lima, Peru.

4Ricardo Palma University, Santiago de Surco, Lima, Peru.

5Global Health Initiative, Wabash College, Crawfordsville, Indiana, USA.

6National University of the Peruvian Amazon (Universidad Nacional de la Amazonía Peruana), Loreto, Iquitos, Peru.

Corresponding author: marilucefonseca@hotmail.com

1 1 2 3,4

Mariluce Gonçalves Fonseca ; Gleice Ribeiro Orasmo ; Lucia Helena O'Dwyer ; Jose Iannacone ;

5 6 6

Jorge Cardenas Callirgos ; Carmén Reategui-Bardales ; Mirle Cachique Pinche ;

6 2

Erme Gloria Pizango Paima & Reinaldo José da Silva

ABSTRACT

Keywords: Amazon – Amblyomma rotundatum – Peru – Rhinella marina – Seasonality

The present study evaluated the influence of seasonality on the occurrence of ectoparasites in a population

of Rhinella marina Linnaeus, 1758 from the region of Loreto, Iquitos, Peru. Hosts were collected during

active night searches. Thirty individuals were collected in the dry season (September 2013) and 20 in the

rainy season (March 2014). The collected hosts underwent morphometric evaluation and subsequently

surveyed for the presence of ectoparasites through examination of the entire body surface under a

stereomicroscope. Only one species of ectoparasite, Amblyomma rotundatum Koch, 1844, was found on

the analyzed hosts. The prevalence and mean abundance of A. rotundatum on R. marina collected in the

rainy season were higher than in the dry season. However, the mean intensity of infestation was similar in

both seasons. The higher prevalence and abundance are likely related to the greater spatial distribution of

R. marina in the environment during the rainy season because, at this time, more water bodies are

available for reproduction. In addition, in the dry season, these organisms are buried and in estivation,

which theoretically would decrease their encounter with ectoparasites. Our results demonstrate that the R.

marina population presents a high prevalence of A. rotundatum in the rainy season and corroborates the

hypothesis that seasonality is a factor that influences the occurrence of these ectoparasites in these hosts in

the studied area. This is the first record that demonstrates the effect of seasonality on A. rotundatum

infestation in R. marina in the Peruvian Amazon.

Neotropical Helminthology

309

INTRODUCTION

310

RESUMEN

Palabras clave: Amazon – Amblyomma rotundatum – Estacionalidad – Perú – Rhinella marina

El presente estudio evaluó la influencia de la estacionalidad en la ocurrencia de ectoparásitos en una

población de Rhinella marina Linnaeus, 1758 de la región de Loreto, Iquitos, Perú. Los hospederos fueron

colectados durante búsquedas nocturnas activas. Treinta individuos fueron recolectados en la estación

seca (septiembre / 2013) y 20 en la estación lluviosa (marzo / 2014). Los hospederos recolectados fueron

sometidos a evaluación morfométrica, y posteriormente, fueron examinados para la presencia de

ectoparásitos a través del examen de la entera superficie corporal bajo un estereomicroscopio. Sólo una

especie de ectoparásito, Amblyomma rotundatum Koch, 1844, se encontró en los hospederos analizados.

La prevalencia y abundancia media de A. rotundatum en R. marina en la temporada de lluvias fue mayor

que en la estación seca. Sin embargo, la intensidad media de infestación fue similar en ambas temporadas.

La mayor prevalencia y abundancia probablemente se relaciona con la mayor distribución espacial de R.

marina en el medio ambiente durante la estación lluviosa porque en este momento, hay más cuerpos de

agua disponibles para la reproducción. Además, en la estación seca, estos organismos están enterrados y

en estivación, que teóricamente disminuirían su encuentro con los ectoparásitos. Nuestros resultados

demuestran que la población de R. marina presenta una alta prevalencia de A. rotundatum en la estación

lluviosa y corrobora la hipótesis de que la estacionalidad es un factor que influye en la ocurrencia de estos

ectoparásitos en estos hospederos en el área estudiada. Este es el primer registro que demuestra el efecto

de la estacionalidad en la infestación de A. rotundatum en R. marina en la Amazonía peruana.

Information about Ixodidae Murray, 1877

ectoparasites in R. marina and their seasonality is

scarce for this Amazonian region, with the great

majority of published reports being isolated

records of occurrence. These records report a small

number of hosts and ectoparasites in different

localities, including Brazil (Antonucci et al., 2011;

Labruna et al., 2010; Gambale et al., 2014),

Argentina (Rivas et al., 2012), Guatemala

(Bermudez et al., 2013); India (Drake et al., 2014),

and the United States (Florida) (Goddard et al.,

2015).

Infestation occurs through the introduction of the

oral apparatus of the tick, which penetrates the skin

of the amphibian deeply, with the tick remaining

fixed via the hypostomium and salivary secretion

solidification. The action of parasitism causes the

laceration of tissues and blood vessels, and the tick

ingests blood and other tissue fluids from the hosts.

During the feeding process, the ticks cause trauma,

mechanical effects, direct spoliation, and toxic

effects (Luz & Faccini, 2013). Thus, they can cause

lesions in the hosts during the blood meal intake,

resulting in the appearance of ulcerative and

hemorrhagic lesions that can alter the behavior of

the host animal, thereby affecting the host's

The order Anura has the highest record of

association with ticks among the amphibians, and

the family Bufonidae (Gray, 1825) is associated

with the highest number of reports in South

America, represented mainly by the species of the

genus Rhinella (Fitzinger, 1826) (Duellman &

Trueb, 1986; Luz & Faccini, 2013).

Rhinella marina (Linnaeus, 1758) is a bufonid

species of nocturnal and terrestrial habits and is

found in dry and tropical forest environments. This

species shows great adaptation to anthropogenic

environments near human populations (Seebacher

& Alford, 1999; Segalla et al., 2014). Its

geographical distribution extends throughout

South and Central America, southern North

America, and Australia (Zug & Zug, 1979; Frost,

2014).

Iquitos, Peru, which belongs to the district of

Loreto, Maynas Province, is considered the capital

of the Peruvian Amazon, and R. marina is one of

six bufonid species recorded for the city (Medina

Torres et al., 2012).

Neotropical Helminthology, 2017, 11(2), jul-dic

Fonsecaet al.

biological, behavioral, and reproductive

interactions with the environment (Luz & Faccini,

2013).

The present study evaluated the influence of

seasonality on the occurrence of Amblyomma

rotundatum Koch, 1844 in a population of R.

marina from the region of Loreto, Iquitos, Peru.

Host collection

The collections were carried out in an urban area

known as Boulevard (3°45'8.3" S 73°14'25'' W)

(Fig. 1) in the district of Loreto, Iquitos, through

active night searching between 06:00 pm and 12:00

am in the dry season in September 2013 and in the

rainy season in March 2014. Fifty R. marina

individuals were collected: 30 in the dry season and

20 in the rainy season. The collection was

authorized by Director's Resolution N°024-2014-

SERFOR-DGGSPFFS.

The individuals collected were placed in individual

plastic bags with a small amount of water and

vegetation to maintain moisture and were

transported immediately to the Laboratory of

Parasitology of the National University of the

Peruvian Amazon (Universidad Nacional de la

Amazonía Peruana - UNAP). They were then

anesthetized with Benzotop, a xylocaine derivative

with local action, for the morphometric procedures

and investigation of ectoparasites.

The species of the individuals was verified, and the

snout-to-vent length (SVL) was measured with

digital calipers with an accuracy of 0.01 mm.

Ectoparasite search

The analysis performed on all hosts consisted of

observation of the dorsal, ventral, and lateral

regions of the body; the orifices; and the limb

extremities using a stereomicroscope. The

ectoparasites were removed with tweezers to

preserve the mouthpiece, identified according to

the occupied sites, counted, and placed in bottles

with 70% ethanol, properly labeled for each host.

The taxonomic identification of the ectoparasites

was carried out at the Laboratory of Parasitology of

RESULTS

311

Wild Animals (Laboratório de Parasitologia de

Animais Silvestres - LAPAS) of the Institute of

Biosciences, São Paulo State University

(Universidade Estadual Paulista - UNESP),

Botucatu, São Paulo, Brazil, where ectoparasites

were deposited.

Statistical analysis

The infestation patterns calculated for R. marina

were estimated by prevalence (P, number of hosts

infested divided by total number of hosts,

expressed as a percentage), mean abundance (MA,

number of collected ectoparasites divided by the

total number of analyzed hosts), and mean

infestation intensity (MII, number of collected

ectoparasites divided by the number of parasitized

hosts) according to Bush et al. (1997). The values

presented for MA and MII are the mean ± standard

error, followed by the minimum and maximum

values in parentheses.

The Mann-Whitney test was used to test the

influence of seasonality on the occurrence of

ectoparasites. The Z test was applied to compare

the prevalences. The Spearman correlation test (r )

was applied to test the correlation between the

number of ectoparasites and the host size. All

statistical tests were performed in SigmaStat 3.10,

and the significance level was 5%.

The search for ectoparasites on R. marina

specimens collected in Boulevard, Iquitos, Peru,

during both seasons resulted in the identification of

a single species of ectoparasite, A. rotundatum.

The R. marina population analyzed in this study

had a total prevalence of 56% infestation with A.

rotundatum in both seasons, and 315 ticks were

recovered from the hosts. The mean total

abundance was 6.30 ± 1.65 (0-58) ticks per

individual, and the MII was 11.25 ± 2.61 (1-58)

ticks per host.

Of the total number of hosts analyzed in the dry

season, 36% were positive for A. rotundatum, with

ticks recovered mainly from the dorsal trunk and

plantar regions (Fig. 2A-C). In the rainy season, A.

rotundatum exhibited an infestation level of 85%,

Neotropical Helminthology, 2017, 11(2), jul-dic Amblyomma rotundatum in Rhinella marina

MATERIAL AND METHODS

312

with all ticks located on the dorsal trunk (Fig. 2B-

C). The level of infestation was significantly higher

in the rainy season (Z = 3.12, p = 0.002). We also

found that the MA was higher in the rainy season,

but the MII was similar in the two seasons (Table

1). We did not observe a correlation between the

host body size and the number of A. rotundatum

recovered in the dry season (r = -0.04, p = 0.84) or

in the rainy season (r =-0.03; p = 0.83).

Table 1. Number of collected hosts (N), snout-to-vent length (SVL) (mm), prevalence (P%), mean abundance (MA),

mean infestation intensity (MII), and total number of Amblyomma rotundatum recovered from Rhinella marina from

Iquitos, Peru, Peruvian Amazon.

Variable

Dry

(n = 30) Rainy

(n = 20) Statistic

SVL (mm)

Number of ticks collected

222

Prevalence (%)

36.67a

85.00b Z = 3.12; p = 0.002

Mean abundance

3.10 ± 1.13a

(0-27)

11.1 ± 3.56b

(0-58)

U = 658; p = 0.003

Mean intensity of infestation

8.46 ± 2.36a

(2-27)

13.06 ± 4.01a

(1-58) U = 156.5; p = 0.90

Figure 1. A) Overview of the collection area, Boulevard, municipality of Iquitos, Peru (yellow circle); B) view of the

area in the dry season; C) view of the area in the rainy season. Source: A) Google Earth; B) Fonseca, 2013; and C) Silva,

2014.

Neotropical Helminthology, 2017, 11(2), jul-dic

Fonsecaet al.

313

Neotropical Helminthology, 2017, 11(2), jul-dic Amblyomma rotundatum in Rhinella marina

Figure 2. Location of Amblyomma rotundatum collected from Rhinella marina in the municipality of Iquitos, Peru: A-

B) dorsal trunk region; C) limb extremities.

314

Antonucci, AM, Oda, FH, Signorelli L, Santana,

NF & Mendes, MC. 2011. Parasitismo de

Amblyomma rotundatum (Koch, 1844)

(Acari: Ixodidae) em Rhinella schneideri

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In the present study, we found that seasonality

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rotundatum, which parasitizes ectothermic animals

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This tick is often reported infesting reptiles and

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buried and in estivation, which theoretically would

decrease their encounters with ectoparasites.

Our results demonstrate that the population of R.

marina has a high incidence of ectoparasites in the

rainy season and corroborate the hypothesis that

seasonality influences the incidence of

ectoparasites for this species in the Peruvian

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According to Duellman & Trueb (1989), bufonids

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Thus, further studies are needed to evaluate in the

short and long term how the populations of these

hosts and their descendants interact with the

spoliation effect of the ectoparasites and the

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Reinaldo J. da Silva was supported by CNPq-

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