Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72: e58705, enero-diciembre 2024 (Publicado Set. 10, 2024)

Infestation of ectoparasite of Probopyrus (Isopoda: Bopyridae) in

Macrobrachium amazonicum (Caridea: Palaemonidae) in the Amazon River

Sting Silva-Duarte1*; https://orcid.org/0000-0001-6878-5762

Sheyla Regina-Marques Couceiro1,2; https://orcid.org/0000-0001-8186-4203

Jô de Farias-Lima1,3; https://orcid.org/0000-0001-6910-7672

Lucio André-Viana1,4; https://orcid.org/0000-0002-0932-0479

1. Postgraduate Program in Tropical Biodiversity, Federal University of Amapá, Amapá, Brazil; stingduarte@gmail.com

(*Correspondence)

2. Laboratory Aquatic Insects, Federal University of west of Pará, Brazil; sheylacouceiro@yahoo.com.br

3. Embrapa Amapá, Rodovia Josmar Chaves Pinto, Caixa Postal 10, 68903-419 Macapá, AP, Brazil; jo.lima@embrapa.br

4. Laboratory of Morphophysiological and Parasitic Studies, Department of Biological and Health Sciences, Federal

University of Amapá, Amapá, Brazil; lucviana74@gmail.com

Received 07-II-2024. Corrected 31-V-2024. Accepted 30-VIII-2024.

ABSTRACT

Introduction: Macrobrachium amazonicum is widely distributed in South America, occurring in the Orinoco,

Amazon and Paraguay river basins, being used as an important source of protein for feeding riverside popula-

tions. This prawn is host to the crustacean ectoparasites Probopyrus pandalicola, Probopyrus floridensis and

Probopyrus bithynis (Bopyridae) that infest the gill cavity of the species.

Objective: To report the prevalence and abundance of ectopasites (P. pandalicola, P. floridensis and P. b i t h y ni s )

and the condition factor in M. amazonicum from the Amazon River, Eastern Amazon.

Methods: The prawns were collected from May 2017 to April 2018, with the artisanal trap matapi in the munici-

palities of Mazagão (state of Amapá) and Santarém (state of Pará), Brazil.

Results: 216 prawns infected with ectoparasites were captured, 133 in the Mazagão region (53 P. pandalicola, 48 P.

bithynis and 32 P. floridensis) and 83 in the Santarém region (45 P. pandalicola and 38 P. b i t h y n i s ). In Mazagão, the

highest prevalence values were recorded in May (1.98 %) for P. floridensis, July (2.18 %) for P. b i t h y n i s , and March

(1.93 %) for P. pandalicola. In the Santarém region, the highest prevalence values were recorded in February, 3.47

for P. pandalicola and 2.89 for P. b i t h y n i s . Regarding the abundance of parasites, there was no difference between

the species grouped between the regions (t = 0.32, p = 0.739). Parasitized prawns from Mazagão and Santarém

presented condition factors below expectations, with an average of 0.85 ± 0.55 for Santarém and 0.88 ± 0.44 for

Mazagão.

Conclusions: During the study it was found that P. pandalicola, P. bithynis and P. floridensis were present in

M. amazonicum throughout the year. Furthermore, there was an effect of parasitism on M. amazonicum in the

study areas.

Key words: amazonian shrimp; ectoparasite; parasitism; condition factor.

https://doi.org/10.15517/rev.biol.trop..v72i1.58705

AQUATIC ECOLOGY

2Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72: e58705, enero-diciembre 2024 (Publicado Set. 10, 2024)

INTRODUCTION

Macrobrachium amazonicum (Heller, 1862)

is a freshwater prawn with a wide distribution

in South America and is the native species

with the most widespread occurrence in the

inland waters of Amazonia (Odinetz-Collart &

Moreira, 1993). Despite being endemic to the

Amazon region (Odinetz-Collart, 1991), it is

also found in the basins of the Paraná and São

Francisco rivers (Bialetzki et al., 1997; Sampaio

et al., 2007), as well as many other hydrographic

basins in South (Kensley & Walker, 1982; Melo,

2003; Valencia & Campos, 2007) and Central

America (Vergamini et al., 2011).

Parasitic interactions between isopods of

Bopyridae and prawns are common and rea-

sonably well known in the scientific literature,

mainly because many parasitic isopods are

crustacean-specific and feed on their hemo-

lymph (Boxshall et al., 2005). Generally, the

growth of prawns is significantly affected by

parasitic infestation, which results in a decrease

in the production potential of the prawn

(Conner & Bauer, 2010). Bopyrid isopods for

instance, are ectoparasites the genus Probopyrus

with 46 species widely distributed in tropical

and subtropical areas of the globe, commonly

found in brackish to freshwater (e.g estuaries)

and freshwater (e.g. lakes and rivers) (Jiménez

& Vargas, 1990; Jayasree et al., 2001; Chinabut,

2002). They are rarely found under aquaculture

conditions but are common in the wild among

freshwater organisms with genus Macrobra-

chium as their definitive hosts (Chaplin-Ebanks

& Curran, 2005).

The presence of Probopyrus is easily spot-

ted due to the noticeable swelling in the gills of

the prawns (Marina et al., 2011), and it remains

until the host dies. In M. amazonicum have

been reported, a number of studies have related

on the specie Probopyrus bithyni, Richardson,

1904 (Oddinetz-Collart, 1990; Lima-Corrêa

et al., 2018) for example, found evidence of a

stable interaction between the two species, sup-

ported by data on the infestation rates and life

cycle of the host, based on specimens collected

on the lower Tocantins River, in the Brazilian

RESUMEN

Infestación de ectoparásitos de Probopyrus (Isopoda: Bopyridae)

en Macrobrachium amazonicum (Caridea: Palaemonidae) en el río Amazonas

Introducción: Macrobrachium amazonicum está ampliamente distribuido en América del Sur, se encuentra en

las cuencas de los ríos Orinoco, Amazonas y Paraguay, se utiliza como una fuente importante de proteínas para

alimentar a las poblaciones ribereñas. Este camarón es hospedero de los ectoparásitos crustáceos: Probopyrus pan-

dalicola, Probopyrus floridensis y Probopyrus bithynis (Bopyridae), que infestan la cavidad branquial de la especie.

Objetivo: Reportar la prevalencia y abundancia de ectoparásitos (P. pandalicola, P. floridensis y P. b i t h y n i s ) y el

factor de condición de M. amazonicum en el| río Amazonas, al este de la Amazonía.

Métodos: Los camarones fueron recolectados entre mayo 2017 y abril 2018, con la ayuda de matapis (trampa

artesanal) en los municipios de Mazagão (Estado de Amapá) y Santarém (Estado de Pará), Brasil.

Resultados: Se capturaron un total de 216 camarones parasitados con ectoparásitos, 133 de ellos en la región de

Mazagão (53 P. pandalicola, 48 P. bithynis y 32 P. floridensis) y 83 en la región de Santarém (45 P. pandalicola y 38

P. bithynis). En Mazagão, los valores más altos de prevalencia se registraron en mayo (1.98 %) para P. floridensis,

julio (2.18 %) para P. bithynis y marzo (1.93 %) para P. pandalicola. En la región de Santarém, los valores más

altos de prevalencia se registraron en febrero, de 3.47 para P. pandalicola y 2.89 para P. bithynis. En cuanto a la

abundancia de parásitos, no hubo diferencia entre las especies agrupadas entre las regiones (t = 0.32, p = 0.739).

Los camarones parasitados de Mazagão y Santarém mostraron factores de condición por debajo de lo esperado,

con un promedio de 0.85 ± 0.55 para Santarém y 0.88 ± 0.44 para Mazagão.

Conclusiones: Durante el estudio, se encontró que P. pandalicola, P. bithynis y P. floridensis estuvieron presen-

tes en M. Amazonicum todo el año. Además, hubo un efecto de parasitismo sobre M. Amazonicum en las áreas

de estudio.

Palabras clave: camarón amozónico; ectoparásitos; parasitismo; factores de condición.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72: e58705, enero-diciembre 2024 (Publicado Set. 10, 2024)

state of Pará, given that the body length of the

female isopods correlated positively with that of

the prawn host (Odinetz-Collart, 1991). More

recently, Lima-Corrêa et al. (2018) described

histopathological alterations in the gills of M.

amazonicum specimens collected from the

lower Amazon River, in Pará state, caused by P.

bithynis infestation. However, such relation for

the species Probopyrus floridensis Richardson,

1904 and Probopyrus pandalicola Packard, 1879

has not been done in previous studies.

Information on the intensity of infection,

specificity and even the geographic range of

ectoparasitic isopods from the family Bopyri-

dae is scarce for most species, compared with

the number of reports on their taxonomy. Only

six species of Bopyridea and one of Entonisci-

dae have been recorded from 10 host species

(Román-Contreras, 2008; Román-Contreras &

Martínez-Mayén, 2011). The apparently low

number of bopyrids in the Brazil region is

probably due to limited sampling effort (Shields

et al., 2015) or to their omission from studies

on the ecological aspects of their hosts (Boyko

& Williams, 2009). In this paper, we register

prevalence, abundance, the parasite’s preference

for host sex and evaluate whether parasitism

influences the condition facto host and a new

locality and host record for ectoparasitic spe-

cies of the genus Probopyrus, associated with M.

amazonicum captured from in the mouth and

lower Amazon River.

MATERIAL AND METHODS

Prawn study, collection and analysis

areas: We conducted captures at two locations:

the mouth of the Mazagão River in the Munici-

pality of Mazagão, State of Amapá (00º15’39.9’’

S & 051º20’42.3’’ W) and Marrecas Island in

the Municipality of Santarém, State of Pará

(02º12’19.3’ S & 054º46’17.9’’ W) as shown in

(Fig. 1). The Mazagão municipality region con-

nects to numerous drainage channels of varying

sizes and depths that are affected by the daily

tide. On Marrecas Island, the hydrodynamics

are different as there is no influence from the

tide, and the water levels varies only due to

seasonal floods. These regions experience tem-

peratures ranging from 24 to 33 °C (Oliveira

et al., 2020). The Eastern Amazon has two dis-

tinct seasonal periods related to precipitation:

the rainy season from December to May and

the less rainy season from June to November

(Oliveira et al., 2020). These periods coincide

with variations in the water level of the Amazon

River, which result in floods during the rainy

season and low waters in the less rainy season.

Between May 2017 and April 2018, and

July to May 2021, 40 pit traps (20 in each study

region) known locally as matapi (Vieira, 2003)

were used to collect monthly specimens of M.

amazonicum. The captured organisms were

transported alive in containers with water to the

laboratory and stored at -20 °C before use. The

identification of the samples was done using the

taxonomic keys of Holthuis (1952) and Melo

(2003). Sexual differentiation was determined

by the presence or absence of the appendix

masculine in the second pair of pleopods for

males and females, respectively (Ismael & New,

2000). The prawns with large parasites were

visually detected by the bulge in the (Carvalho

et al., 2014), exoskeleton in the gill chamber.

Parasites of small size or immature females

were recognized by the pattern of spots on the

branchiostegite (Conner & Bauer, 2010).

The parasites were identified based on

the original descriptions presented by Lemos

de Castro and Silva (1985), Román-Contreras

(2004) and Paul et al. (2010). References are

provided for the taxonomic authority of all

parasitic taxa, but not for those of hosts.

Data analysis: Difference in parasitism

levels between male and female prawn using

the chi-square (χ2) test (Zar, 1999) to determine

if they deviated from the expected 1:1 ratio. The

ecological terms of prevalence (P) and mean

abundance (MA) followed the definitions of

Bush et al. (1997). The monthly prevalence and

abundance data were then tested using the Stu-

dent (t) test to compare the variables between

the two areas of study after assessing normality

and homoscedasticity. The equation Kn = Wt/

We (Le-Cren, 1951) was used to determine

4Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72: e58705, enero-diciembre 2024 (Publicado Set. 10, 2024)

the relative condition factor of prawns. Thirty

parasitized and thirty non-parasitized prawn

were selected from each collection site/month

to obtain data on total body mass (Wt) and

standard length (Lp). The values were adjusted

to the model Wt = a.Lpb using the least squares

method after the logarithmic transformation

of the values of the total mass/standard length

ratio curve. The coefficients “a” and “b” were

estimated as they were used in the calculation

Fig. 1. The location of M. amazonicum captures areas in the mouth and lower Amazon between May 2017 and April 2018,

and July 2021 to May. The black circle (l) represents Mazagão, while the green triangle (s) represents Marrecas Island.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72: e58705, enero-diciembre 2024 (Publicado Set. 10, 2024)

of the theoretically expected values of total

weight (We) for a given value of Lt through the

equation: We = a.Lpb. The Mann-Whitney (U)

test compared the mean Kn values of parasit-

ized and non-parasitized prawn to the theoreti-

cal value 1 (Le-Cren, 1951). The test was also

used to determine any differences in the mean

Kn between parasitized and non-parasitized

prawn in both study regions, with significant

differences being considered when P < 0.05.

RESULTS

Total of 6 796 prawns were caught dur-

ing the study, with 4 163 females and 2 633

males. The majority of the prawn, 4 132, were

obtained in Mazagão with the remaining 2 664

found in Marrecas Island. The average monthly

catch was 531.66 specimens. The sex ratio in

both areas was skewed towards females, with

ratios of 1.32 females to 1 male in Mazagão

and 2.34 females to 1 male on the Marrecas

island. Among the females caught, 1 579 were

carrying eggs, with 871 found in Mazagão

and 708 in Marrecas Island. The ovigerous

females in Mazagão were larger in size (56.85

± 11.34) than those found on Marrecas Island

(43.57 ± 10.48).

Out of the total catch, 216 prawn (3.7 %)

were found to be parasitized, with prevalence

of 3.2 % in Mazagão and 3.1 % in Marrecas

Island. The majority of the parasitized prawn

were female (163) with the rest being male (53).

None of the ovigerous females were found to be

parasitized. Most of the parasitized prawn had

only one gill chamber infected (98.1 %). The

parasites were always found in pairs, with a 1

female to 1 male sex ratio.

Examining the parasites’ morphology

allowed for identifying the three species P.

pandalicola (Fig. 2), P. bithynis (Fig. 3), and P.

floridensis (Fig. 4). As shown in Mazagão, 133

parasites were collected, with 53 showing mor-

phological traits consistent with P. pandalicola,

48 with P. bithynis, and 32 with P. floridensis.

On the Marrecas Island, 83 parasites were

collected, with 45 displaying morphological

characteristics of P. pandalicola and 38 of P.

bithynis; P. floridensis was not found in this area.

The specimens P. pandalicola the pereo-

meres are distinct dorsally and separated by

notches laterally; lateral margins of all pereo-

meres are greatly reflexed ventrally. Abdomen

with all somites well developed, fused in the

center but separated laterally by deep incisions.

Telson with rounded contour and pointed distal

end. The pleopods form five pairs of rounded

tubercles, one for each pair. Pleopoda are pres-

ent in pairs of small, rounded processes, one

pair on each segment of the abdomen. Eyes

are present. All regions and segments of the

male body are distinct dorsally and separated

laterally (Fig. 2C). The sides of the pereon are

subparallel, but the pleon suddenly becomes

broader than the pereon. Most of the dorsal

surface of the body has dark brown pigment.

The specimens P. bithynis, based on the

illustrations and descriptions presented by

Richardson in 1904, we propose that the speci-

mens that differed from the type P. b i t h y ni s are

different species. We observed that the absence

of anterolateral processes on the head of the

female, the presence of patches of black on the

lateral margins of all the segments of the thorax

on one side of the body, and the presence of a

bilobed telson are morphologically similar to

what was observed in specimens later designat-

ed by Lemos de Castro & Brasil-Lima (1974).

The specimens P. floridensis, based on the

illustrations the female’s body is light brown

and has distinct parts such as the head, abdo-

men, ovarian bosses and light yellow epimera.

There are dark markings all over the thorax and

a few black lines on the abdomen. The incuba-

tory lamellae are almost entirely covered with

black markings, giving a uniformly dark color.

On the ventral side of the thorax, the lateral

parts have black markings with yellow areas

separating them, and all the legs on this side

are yellow (Fig. 4). The legs on the opposite

side are dark.

Based on grouped species, there was no

significant difference in the monthly preva-

lence of Probopyrus-infected prawn in the two

locations (t = 0.33; p = 0.738). In Mazagão, the

6Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72: e58705, enero-diciembre 2024 (Publicado Set. 10, 2024)

highest prevalence rates were observed for P.

floridensis in May (1.9 %), P. b it hy n i s in July

(2.1 %), and P. pandalicola in March (1.9 %)

(Table 1). On the Marrecas Island, the highest

prevalences were observed in February, with

3.4 % for P. pandalicola and 2.8 % for P. b i t hy n i s

(Table 1).

There was no significant difference in the

monthly abundance of grouped parasite spe-

cies between the various locations (t = 0.32,

p = 0.739). In Mazagão, P. pandalicola and P.

bithynis had the highest average abundance

values in the region, with values of 0.0105 ±

0.0031 for each species (Table 2). On Marrecas

Island, the species P. pandalicola had the high-

est average abundance value of 0.0179 ± 0.0093

(Table 2).

The prawn parasitized in Mazagão and

Marrecas Island had lower than expected con-

dition factors, with a mean of 0.85 ± 0.55 for

Ilha de Marrecas and 0.88 ± 0.44 for Mazagão.

The condition factor of shrimp infested with

Fig. 2. Probopyrus pandalicola. A. Ventral view female. B. Dorsal view female. C. Dorsal view male.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72: e58705, enero-diciembre 2024 (Publicado Set. 10, 2024)

Probopyrus (grouped species) differed signifi-

cantly from those not infested in both locations,

with a t-value of -2.76 and P-value of 0.006 in

Mazagão (Fig. 5A) and a t-value of -2.27 and

P-value of 0.024 in Marrecas Island (Fig. 5B).

DISCUSSION

The M. amazonicum females were more

abundant than males in both areas of study,

corroborating to be expected for estuarine and

coastal populations of this species in the Ama-

zon region (Freire et al., 2012; Lima et al., 2014;

Sampaio et al., 2007). Regarding ovigerous

females’ standard length, it was found that

female M. amazonicum was larger in Mazagão

than in Marrecas. This difference in length

may be associated with the characteristic of

the Mazagão region, with proximity to the

mouth of the Amazon River and an area of

Fig. 3. Probopyrus bithynis. A. Ventral view female. B. Dorsal view female. C. Dorsal view male.

8Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72: e58705, enero-diciembre 2024 (Publicado Set. 10, 2024)

intense tidal activity and daily transport of

organic matter, which may be contributing to

an ‘enrichment’ of this region. Then promoting

better nutritional conditions for the growth of

females. Thus, the standard length of females

collected in Mazagão was similar to that report-

ed in studies involving other estuarine areas in

the Amazon region (Freire et al., 2012; Hayd &

Anger, 2013). Likewise, the females collected in

the Marrecas Island had similar lengths to the

shrimps collected of Amazon River in conti-

nental areas (da Silva et al., 2004).

Female shrimp had a significantly high-

er prevalence of parasites compared to male

shrimp. This is a common characteristic

observed in the genus Probopyrus according

to several sources (Truesdale & Mermilliod,

1977; Oddinetz-Collart, 1990; Lima-Corrêa et

al., 2018). Additionally, all the infested females

were found to be non-ovigerous, as reported by

Fig. 4. Probopyrus floridensis. A. Ventral view female. B. Dorsal view female. C. Dorsal view male.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72: e58705, enero-diciembre 2024 (Publicado Set. 10, 2024)

Table 1

Monthly prevalence of the parasitized Probopyrus pandalicola, Probopyrus bithynis, and Probopyrus floridensis sampled in the

shrimp Macrobrachium amazonicum from regions of Mazagão-AP and Marrecas Island-PA from April 2017 to March 2018.

Months Site Prevalence (%)

P. pandalicola P. b i t hy ni s P. floridensis Grouped

April M 1.08 1.08 0.36 2.53

MI 0.71 0 0 0.71

May M 0.99 1.98 1.98 4.55

MI 2.04 2.04 0 4.08

June M 1.12 1.30 0.93 3.35

MI 1.68 2.35 0 4.03

July M 1.09 2.18 0.66 3.93

MI 0.86 0.22 0 1.08

August M 1.07 1.43 0.54 3.04

MI 1.17 1.95 0 3.13

September M 1.12 1.50 0.75 3.36

MI 2.48 1.42 0 3.90

October M 0.72 2.88 0 3.60

MI 1.49 1.98 0 3.47

November M 0.89 1.12 0.22 2.23

MI 0.56 0.37 0 1.12

December M 0.76 0.76 1.53 3.05

MI 3.48 1.74 0 5.22

January M 1.25 0.93 0.62 2.80

MI 1.55 2.58 0 4.12

February M 0.67 2.0 1.0 3.67

MI 3.47 2.89 0 6.36

March M 1.93 0.97 0.48 3.67

MI 2.11 1.05 0 3.16

M: mean and sd 1.05 ± 0.31 1.51 ± 0.60 0.75 ± 0.52 3.32 ± 0.67

MI: mean and sd 1.80 ± 0.93 1.55 ± 0.91 0 3.36 ± 1.62

Abbreviations: M - Mazagão, MI - Marrecas Island.

Vargas-Ceballos et al. (2016). This may be due

to isopods, which act as castrating parasites that

inhibit gonadal development, negatively affect-

ing reproductive success (Conner & Bauer,

2010; Sánchez-Murillo, 2016). In the case of M.

amazonicum, energy and nutrients that should

be used for reproduction are instead diverted

to the growth and reproduction of the parasite

interrupting the gonadal maturation of the

shrimp (Conner & Bauer, 2010).

In Mazagão and Marrecas Island was it

possible to distinguish three clear morphologi-

cal patterns that indicate the species P. pandali-

cola, P. bithynis, P. floridensis, based in original

descriptions and illustrations are recognized as

valid by the World Register of Marine Species

(World Register of Marine Species [WoRMS],

2023). According to Nunes-Pralon et al. (2018),

infestations of Probopyrus species are not lim-

ited to specific host species or genera, sup-

ported by the present study that reports three

Probopyrus species infesting M. amazonicum.

Thes Parasites of the genus Probopyrus have a

well-established relationship with a number of

different representatives of the family Palae-

monidae, in particular, the prawns of the genus

Macrobrachium (Markham, 1985; Saito et al.,

2010). In the specific case of M. amazonicum,

10 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72: e58705, enero-diciembre 2024 (Publicado Set. 10, 2024)

records of infestation by P. bithynis are restrict-

ed to the coastal region of the Amazon basin,

in areas near the Tucuruí hydroelectric dam on

the Tocantins River, which is approximately 300

km from the Atlantic Ocean (Odinetz-Collart,

1988; Odinetz-Collart, 1990). More recently,

records of this parasitism were obtained from

the lower Amazon, near the community of

Maruim, in the municipality of Gurupá, around

400 km from the Atlantic Ocean, in the Bra-

zilian state of Pará (Lima-Corrêa et al., 2018;

Pereira et al., 2022).

According to Ribeiro & Horch (2023),

P. pandalicola has widespread distribution in

Brazil. See Ribeiro et al. (2019) for a discussion

on the distribution and taxonomic history of

this widespread species. Several studies have

cited the Southern edge of P. pandalicola distri-

bution as the state of São Paulo, Brazil, follow-

ing Beck (1979). However, it should be noted

that Beck (1979) considered P. floridensis to

be a synonym of P. pandalicola and combined

their distributions when discussing the species.

As far as we have been able to discern through

separating the two species in the literature, the

southernmost location of P. pandalicola is in

the state of Rio de Janeiro and the northern-

most is in the state of Amapá, Brazil.

Table 2

Monthly abundance of the parasitized Probopyrus pandalicola, Probopyrus bithynis, and Probopyrus floridensis sampled in the

shrimp Macrobrachium amazonicum from regions of Mazagão-AP and Marrecas Island-PA from April 2017 to March 2018.

Months Site Abundance mean

P. pandalicola P. b i t h y n i s P. floridensis Grouped

April M 0.0108 0.0108 0.0036 0.0252

MI 0.0071 0 0 0.0071

May M 0.0099 0.0099 0.0198 0.0495

MI 0.0204 0.0204 0 0.0408

June M 0.0111 0.0111 0.0093 0.0335

MI 0.0167 0.0234 0 0.0402

July M 0.0109 0.0109 0.0065 0.0393

MI 0.0086 0.0021 0 0.0107

August M 0.0107 0.0107 0.0053 0.0304

MI 0.0117 0.0195 0 0.0312

September M 0.0112 0.0112 0.0074 0.0336

MI 0.0248 0.0141 0 0.0390

October M 0.0071 0.0071 0 0.0359

MI 0.0148 0.0198 0 0.0390

November M 0.0089 0.0089 0.0022 0.0223

MI 0.0055 0.0198 0 0.0346

December M 0.0076 0.0076 0.0152 0.0305

MI 0.0347 0.0173 0 0.0521

January M 0.0124 0.0124 0.0062 0.0280

MI 0.0154 0.0257 0 0.0413

February M 0.0066 0.0066 0.0100 0.0366

MI 0.0346 0.0289 0 0.0635

March M 0.0193 0.0193 0.0048 0.0338

MI 0.0210 0.0105 0 0.0315

M: mean and sd 0.0105 ± 0.0031 0.0105 ± 0.0031 0.0075 ± 0.0052 0.03325 ± 0.0067

MI: mean and sd 0.0179 ± 0.0093 0.0154 ± 0.0091 0 0.0336 ± 0.0162

Abbreviations: M - Mazagão, MI - Marrecas Island.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72: e58705, enero-diciembre 2024 (Publicado Set. 10, 2024)

Recently, Pereira et al. (2022) conducted

a study on Probopyrus sp. populations that

parasitize M. amazonicum, which were sampled

in coastal (Abaetetuba, Afuá, Augusto Corrêa

and Breves-state of Pará, Brazil) areas of the

Amazon and continental (Santarém-state of

Pará, Brazil). They concluded that the coastal

populations analyzed could be assigned to P.

bithynis, while the inland populations consisted

of a different species, probably P. palaemoni.

P. floridensis, like P. bithynis, was initially

considered to be a synonym of P. pandali-

cola, by Markham (1985). However, it was later

established as a distinct species by Román-Con-

treras (1993), in agreement with Dale & Ander-

son (1982). Two studies have been conducted

on the population structure and prevalence of

this species on the host Macrobrachium potiuna

in Brazil. One was conducted in Paraná (Masu-

nari et al., 2000), while the other was conducted

in São Paulo (Rocha & Bueno, 2000). The

study by Masunari et al. (2000) registered the

southernmost location known for this species,

while Rocha & Bueno (2000) discussed the

taxonomic validity of the species. The present

study provides the first report of this parasite in

M. amazonicum from Brazil.

In the present study, infestation in just one-

gill chamber were frequent. This is consistent

with observations in many other palaemonid

species (Jiménez & Vargas 1990; Oddinetz-

Collart, 1990; Román-Contreras, 2004; Hassan

et al., 2017; Lima-Corrêa et al., 2018; de Bar-

ros et al., 2021) being strategy de survival of

parasite to keep the host alive (Lima-Corrêa et

al., 2018). A cryptoniscus larva initially infects

one of the shrimp’s gill chambers, inhibiting

another pair of parasites’ presence in one of

the gill cavities (Oddinetz-Collart, 1990). How-

ever, the present study observed several cases

of double parasitism of the same species in one

host. This occurrence had already been noted

in M. amazonicum (Odinetz-Collart, 1990) and

Macrobrachium ohione (Truesdale & Mermil-

liod, 1977).

In the present study, prevalence and abun-

dance there was no significant difference of

grouped parasite species between Mazagão

and Marrecas Island. It is noteworthy that P.

floridensis was not found on Marrecas Island.

In prevalence and abundance may be attrib-

uted to variations in environmental conditions

such as salinity, which can interfere with the

life cycle of intermediate hosts and the varying

abundance of intermediate hosts can have a

direct impact on the reproductive cycle of the

parasites. This suggests that intermediate hosts

of the parasites observed in this work can be

Fig. 5. Relative condition factor (Kr) of Macrobrachium amazonicum infested Probopyrus spp. (grouped species) and healthy

from regions of Mazagão-AP and Marrecas Island-PA from April 2017 to March 2018.

12 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72: e58705, enero-diciembre 2024 (Publicado Set. 10, 2024)

more commonly found in estuarine areas than

in continental ones.

In both Mazagão and Marrecas Island,

prawn infested with all three species of Probopy-

rus had a Kn value of less than 1.00. In contrast,

non-infested prawn had values similar to the

standard value for Macrobrachium prawn (Kn

= 1.00). Infected samples of M. amazonicum

may have experienced nutritional status retar-

dation due to stress and respiration distortion.

This is evident in the condition factor values of

the prawns as compared to the non-parasitized

prawns. The hypothesized nutritional status

retardation may have resulted from the nutri-

ent absorption of the parasite through the

hemolymph (Romero-Rodríguez et al., 2016;

Romero-Rodríguez et al., 2017). The branchial

chamber of the host, being the primary site of

infection for the bopyrid isopods has serious

consequences for gaseous exchange as well as

the effectiveness of the host metabolic rate.

These actions eventually lead to stress and

affect the growth rate of the infected prawn.

According to Conner & Bauer (2010), the

parasite is also capable of meddling with the

feeding abilities of the host. Hence, the energy

and nutrients that the host normally channels

towards their reproduction and growth appear

to be used for survival instead (Boxshall, 2005).

During the study. it was found that P.

pandalicola. P. bithynis. and P. floridensis were

present in M. amazonicum throughout the year.

However, the levels of prevalence and abun-

dance were low. Additionally, female shrimp

were found to be more susceptible to the

parasites. The condition factor (Kn) of M.

amazonicum showed adverse effects due to the

parasites. This study provides essential data on

the prevalence, abundance, and occurrence of

these three parasite species in M. amazonicum

across different areas.

Ethical statement: the authors declare that

they all agree with this publication and made

significant contributions; that there is no con-

flict 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 acknowledgments sec-

tion. A signed document has been filed in the

journal archives.

ACKNOWLEDGMENT

The Coordination for the Improvement of

Higher Education Personnel (CAPES) for the

PhD scholarship granted to the first author.

To the National Council for Scientific and

Technological Development (CNPq) for the

financial support according to processes nº

407698/2013-2 and process nº 444367/2014-4.

The Brazilian Agricultural Research Corpora-

tion for structural and logistical support.

REFERENCES

Beck, J. T. (1979). Population interactions between a

parasitic castrator, Probopyrus pandalicola (Isopo-

da: Bopyridae), and one of its freshwater shrimp

hosts, Palaemonetes paludosus (Decapoda: Caridea).

Parasitology, 79(3), 431–449. https://doi.org/10.1017/

S003118200005383X

Bialetzki, A., Nakatani, K., Baumgartner, G., & Bond-

Buckup, G. (1997). Occurrence of Macrobrachium

amazonicum (Heller) (Decapoda, Palaemonidae) ln

Leopoldo’s inlet (Ressaco do Leopoldo), upper Paraná

river, Porto Rico, Paraná, Brazil. Revista Brasileira

de Zoologia, 14(2), 379–390. https://doi.org/10.1590/

S0101-81751997000200011

Boxshall, G., Lester, R., Grygier, M., Høeg, J., Glenner, H.,

Shields, J., & Lützen, J. (2005). Crustacean parasites.

In K. Rohde (Ed.), Marine Parasitology (pp. 123–169).

CSIRO Publishing.

Boxshall, G. (2005). Copepoda (copepods). In K. Rodhe

(Ed.), Marine Parasitology (pp. 138–144). CSIRO

Publishing.

Boyko, C. B., & Williams, J. D. (2009). Crustacean parasites

as phylogenetic indicators in decapod evolution. In

J. W. Martin, K. A. Crandall, & D. L. Felder (Eds.),

Decapod Crustacean Phylogenetics (pp. 197–220).

CRC Press.

Bush, A. O., Lafferty, K. D., Lotz, J. M., & Shostak, A. W.

(1997). Parasitology meets ecology on its own terms.

Journal of Parasitology, 83(4), 575–583. https://doi.

org/10.2307/3284227

Carvalho, F. L., Magalhães, C., & Mantelatto, F. L. (2014).

Molecular and morphological differentiation bet-

ween two Miocene-divergent lineages of Amazo-

nian shrimps, with the description of a new species

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72: e58705, enero-diciembre 2024 (Publicado Set. 10, 2024)

(Decapoda, Palaemonidae, Palaemon). ZooKeys, 457,

79–108. https://doi.org/10.3897/zookeys.457.6771

Chaplin-Ebanks, S. A., & Curran, M. C. (2005). The effect

of the parasitic isopod, Probopyrus pandalicola (Pac-

kard, 1879), on tidal activity patterns of the grass

shrimp, Palaemonetes pugio (Holthuis, 1949). Crusta-

ceana, 78(9), 1053–1061.

Chinabut, S. (2002). A case study of isopod infestation in

Tilapia cage culture in Thailand. In R. Arthur, M. J.

Phillips, R. P. Subasinghe, M. B. Reantaso, & I. H.

MacRae (Eds.), Primary Aquatic Animal Health Care

in Rural, Small-scale, Aquaculture Development (pp.

201–202). FAO Fisheries Technical Paper.

Conner, S. L., & Bauer, R. T. (2010). Infection of adult

migratory river shrimps. Macrobrachium ohione. by

a branchial bopyrid isopod Probopyrus pandalicola.

Invertebrate Biology, 129(4), 344–352. https://doi.

org/10.1111/j.1744-7410.2010.00210.x

da Silva, R. R., Sampaio, C. S., & Santos, J. A. (2004).

Fecundity and fertility of Macrobrachium amazoni-

cum (Crustacea, Palaemonidae). Brazilian Journal of

Biology, 64(3A), 489–500.

Dale, W. E., & Anderson, G. (1982) Comparison of mor-

phologies of Probopyrus bithynis, P. floridensis, and P.

pandalicola larvae reared in culture (Isopoda, Epica-

ridea). Journal of Crustacean Biology, 2(3), 392–409.

https://doi.org/10.2307/1548055

de Barros, M. S. F., da Silva Neto, L. S., & Calado, T. C.

(2021). First record of parasitism by Probopyrus

pandalicola (Isopoda, Bopyridae) on the freshwater

prawn Macrobrachium acanthurus (Decapoda, Palae-

monidae) and ecological interactions. Journal of Para-

sitic Diseases, 45, 273–278. https://doi.org/10.1007/

s12639-020-01306-5

Freire, J. L., Marques, C. B., & Silva, B. B. (2012). Estrutura

populacional e biologia reprodutiva do camarão-da-

amazônia Macrobrachium amazonicum (Heller, 1862)

(Decapoda: Palaemonidae) em um estuário da região

nordeste do Pará, Brasil. Brazilian Journal of Aquatic

Science and Technology, 16(2), 65–76.

Hassan, M., Sharoum, F. M., Wahid, M. E. A., Ghaffar, M.

A., Ambak, M. A., Musa, N., & Nadzir, S. M. (2017).

Infestation of Probopyrus sp. on Macrobrachium lan-

chesteri from Chalok River and Nyathoh River. Teren-

gganu. Malaysia. Journal Sustain Science Management,

(3), 111–118.

Hayd, L., & Anger, K. (2013). Reproductive and morphome-

tric traits of Macrobrachium amazonicum (Decapoda:

Palaemonidae) from the Pantanal, Brazil, suggests

initial speciation. Revista de Biología Tropical, 61(1),

39–57. https://doi.org/10.15517/rbt.v61i1.10881

Holthuis, L. B. (1952). A general revision of the Palae-

monidae (Crustacea, Decapoda, Natantia) of the

Americas. II. The subfamily Palaemoninae. University

of Southern California Press.

Ismael, D., & New, M. B. (2000). Biology. In M. B. New, &

W. C. Valenti (Eds.), Freshwater prawn culture: the

farming of Macrobrachium rosenbergii (pp. 18–40).

Wiley-Blackwell Science.

Jayasree, L., Janakiram, P., & Madhavi, R. (2001). Epi-

bionts and parasites of Macrobrachium rosenbergii

and Metapenaeus dobsoni from Gosthani estuary.

Journal of Natural History, 35(2), 157–167. https://doi.

org/10.1080/00222930150215297

Jiménez, P., & Vargas, M. (1990). Probopyrus pandalicola

(Isopoda: Bopyridae) infesting Palaemonetes hiltonii

(Crustacea: Caridea) along the Pacific coast of Costa

Rica. Revista de Biología Tropical, 38(2B), 457–462.

Kensley, B., & Walker, I. (1982). Palaemonid shrimps

from the Amazon Basin, Brazil (Crustacea: Decapo-

da: Natantia). Smithsonian Contributions to Zoology,

(362), 1–28. https://doi.org/10.5479/si.00810282.362

Le-Cren, E. D. (1951). The lenght-weight relationship and

seasonal cycle in gonad weight and conditions in the

perch. Journal of Animally Ecologic, 20(2), 201–219.

https://doi.org/10.2307/1540

Lemos de Castro, A., & Brasil-Lima, I. M. (1974). Crus-

táceos isópodes epicarídeos do Brasil IX. Gênero

Probopyrus Giard and Bonnier. Revista Brasileira de

Biologia, 34, 209-218.

Lemos de Castro, A., & Silva, J. L. (1985). Isopoda. Manual

de Identicação de Invertebrados Límnicos do Brasil.

CNPq.

Lima, J. F., Silva, L. M. A., Silva, T. C., Garcia, J. S., Perei-

ra, I. S., & Amaral, K. D. S. (2014). Reproductive

aspects of Macrobrachium amazonicum (Decapoda:

Palaemonidae) in the State of Amapa. Amazon River

mouth. Acta Amazonica, 44(2), 245–254. https://doi.

org/10.1590/S0044-59672014000200010

Lima-Corrêa, L., Oliveira-Sousa, E. M., Flores-Silva, L.

V., Aparecido-Adriano, E., Brito-Oliveira, M. S., &

Tavares-Dias, M. (2018). Histopathological altera-

tions in gills of Amazonian shrimp Macrobrachium

amazonicum parasitized by isopod Probopyrus bithy-

nis (Bopyridae). Diseases of Aquatic Organisms, 129,

117–122. https://doi.org/10.3354/dao03236

Marina, H., Suhairi, M., Wahidah, W., & Ihwan, Z. (2011).

Infestation of Probophyrus sp. on Macrobrachium

rosenbergii from Setiu River, Malaysia. Australian

Society for Parasitology Annual Conference.

Markham, J. C. (1985) A review of the bopyrid isopods

infesting caridean shrimps in the northwestern Atlan-

tic Ocean, with special reference to those collected

during the Hourglass Cruises in the Gulf of Mexico.

Memoirs of the Hourglass Cruises, 8(3), 1–156.

14 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72: e58705, enero-diciembre 2024 (Publicado Set. 10, 2024)

Masunari, S., Castagini, A. S., & Oliveira, E. (2000).

The population structure of Probopyrus floriden-

sis (Isopoda, Bopyridae), a parasite of Macrobra-

chium potiuna (Decapoda, Palaemonidae) from

the Perequê River, Paranaguá basin, southern Bra-

zil. Crustaceana, 73(9), 1095–1108. https://doi.

org/10.1163/156854000505100

Melo, G. A. S. (2003). Manual de identificação dos Crustacea

Decapoda de água doce do Brasil. Editorial Loyola.

Nunes-Pralon, B. G., Antunes, M., Campanelli-Mortari, R.,

de Sequeira-Bueno, S. L., & Negreiros-Fransozo, M. L.

(2018). Infestation of two shrimp species of the genus

Palaemon Fabricius, 1798 (Decapoda,Palaemonidae)

by an isopod of the genus Probopyrus Giard &

Bonnier, 1888 (Bopyridae) from the Brazilian

southeast coast. The Journal of The Brazilian Crus-

tacean Society: Nauplius, 26, e2018026. https://doi.

org/10.1590/2358-2936e2018026

Oddinetz-Collart, O. (1990). Interactions entre le parasite

Probopyrus bithynis (Isopoda, Bopyridae) et l’un de

ses hôtes, la crevette Macrobrachium amazonicum

(Decapoda, Palaemonidae). Crustaceana, 58(3), 258–

269. https://doi.org/10.1163/156854090X00174

Odinetz-Collart, O. (1988). Aspectos ecológicos do

camarão Macrobrachium amazonicum (Heller, 1862)

no baixo Tocatins (PA-Brasil). Memoria de la Socie-

dad de Ciencias Naturales La Salle, 48, 341–353.

Odinetz-Collart, O. (1991). Tucurui dam and the popula-

tion of the prawn Macrobrachium amazonicum int the

Lower Tocantins (Pa-Brazil): a four year study. Archiv

für Hydrobiologie, 122(2), 213–227.

Odinetz-Collart, O., & Moreira, L. (1993). Potencial pes-

queiro de Macrobrachium amazonicum na Amazônia

Central (Ilha do Careiro): variação da abundância e

do comprimento. Amazoniana, XII(3/4), 399–413.

Oliveira, L. S., Cajado, R. A., Bentes dos Santos, L. R., Lima-

Suzuki, M. A., & Zacardi, D. M. (2020). Bancos de

macrófitas aquáticas como locais de desenvolvimento

das fases iniciais de peixes em várzea do baixo ama-

zonas. Oecologia Australis, 24(3), 644–660. https://doi.

org/10.4257/oeco.2020.2403.09

Paul, M., Chanda, M., Maity, J., Gupta, S., Patra, B. C., &

Dash, G. (2010). Parasitic prevalences in freshwater

prawn Macrobrachium rosenbergii in onrth and South

24 parganas districts of West Bengal. Choron Young

Soi, 1(4), 48–50.

Pereira, R. I. dos S., Maciel, C. R., & Iketani, G. (2022). Mole-

cular features of Probopyrus sp. (Isopoda: Bopyridae)

from Brazilian Amazonia and the parasitism of inland

populations of Macrobrachium amazonicum (Deca-

poda: Palaemonidae). Parasitology, 149(2), 203–208.

https://doi.org/10.1017/S0031182021001657

Ribeiro, F. B., Horch, A. P., & Williams, J. D. (2019).

New occurrences and host records for two species

of parasitic isopods (Isopoda, Cymothoida, Bopyri-

dae) associated with caridean shrimps (Decapoda,

Caridea) from Brazil. Journal of Natural History,

53(39–40), 2437–2447. https://doi.org/10.1080/0022

2933.2019.1704589

Ribeiro, F. B., & Horch, A. P. (2023). Checklist of parasitic

isopods from Brazil: Bopyroidea and Cryptoniscoidea

(Isopoda: Cymothoida: Epicaridea). Zootaxa, 5325(2),

151–185. https://doi.org/10.11646/zootaxa.5325.2.1

Rocha, S. S., & Bueno, S. L. S. (2000). Probopyrus floriden-

sis Richardson, 1904 (Isopoda, Bopyridae) parasiti-

zing the freshwater prawn Macrobrachium potiuna

(Müller, 1880), from São Paulo, Brazil. Nauplius, 8(1),

133–140.

Román-Contreras, R. & Martínez-Mayén, M. (2011) Regis-

tros nuevos de parásitos epicarideos (Crustacea: Iso-

poda) en México y suroeste del Golfo de México.

Revista Mexicana de Biodiversidad, 82(4), 1145–1153.

https://doi.org/10.22201/ib.20078706e.2011.4.707

Román-Contreras, R. (1993). Probopyrus pacificensis, a new

species of parasite (Isopoda: Bopyridae) of Macrobra-

chium tenellum (Smith, 1871) (Decapoda: Palaemoni-

dae) from the Pacific coast of Mexico. Proceedings of

the Biological Society of Washington, 106(4), 689–697.

Román-Contreras, R. (2004). The genus Probopyrus Giard

and Bonnier. 1888 (Crustacea: Isopoda: Bopyridae) in

the eastern Pacific with seven new records for Mexico.

In M. E. Hendrickx (Ed.), Contributions to the study

of east Pacific crustaceans (pp. 153–158). Universidad

Nacional Autónoma de México, Instituto de Ciencias

del Mar y Limnología.

Román-Contreras, R. (2008) Estudios y registros de isópo-

dos epicarideos en México: 1897–2005. En F. Álva-

rez-Noguera, & G. A. Rodríguez-Almaraz (Eds.),

Crustáceos de México: Estado Actual de su Conoci-

miento (pp. 81–114). Biblioteca Universitaria Raúl

Rangel Frías.

Romero-Rodríguez, J., Roman-Contreras, R., & Bortolini-

Rosales, J. L. (2017). Male influence on the ovarian

development of the crustacean parasite Bopyrina

abbreviate (Isopoda, Bopyridae). Journal of the Mari-

ne Biological Association of the United Kingdom, 97(1),

91–98. https://doi.org/10.1017/S0025315415002258

Romero-Rodríguez, J., Roman-Contreras, R., & Chaza-

ro-Olvera, S. M. A (2016). Growth of individuals

within the parasite-host association Bopyrina abbre-

viate (Isopoda, Bopyridae) and Hippolyte zosterico-

la (Decapoda, Caridea), and variations in parasite

morphology. Invertebrate Reproduction, 60(1), 39–48.

https://doi.org/10.1080/07924259.2015.1126536

Saito, N., Shokita, S., & Naruse, T. (2010). A new spe-

cies of freshwater bopyrid, Probopyrus iriomotensis

(Crustacea: Isopoda), parasitizing Macrobrachium

spp. (Crustacea: Decapoda), from Iriomote Island,

Ryukyu Islands, Southwestern Japan. Species

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72: e58705, enero-diciembre 2024 (Publicado Set. 10, 2024)

Diversity, 15(3–4), 169–183. https://doi.org/10.12782/

specdiv.15.169

Sampaio, C. M. S., Silva, R. R., Santos, J. A., & Sales, S. P.

(2007). Reproductive cycle of Macrobrachium ama-

zonicum females (Crustacea, Palaemonidae). Brazi-

lian Journal of Biology, 67(3), 551–559. https://doi.

org/10.1590/S1519-69842007000300022

Sánchez-Murillo, J. M. (2016). Sobre el parasitismo de isó-

podos en langostinos. Badajoz Veterinaria, (4), 23–25.

Shields, J. D., Boyko, C. B., & Williams, J. D. (2015) Chapter

Parasites and pathogens of Brachyura. In P. Castro,

P. Davie, P. D. Guinot, F. Schram, & von Vaupel

Klein, C. (Eds.), Treatise on Zoology-Anatomy, Taxo-

nomy, Biology. The Crustacea (Volume 9 Part C, pp.

639–774). Brill.

Truesdale, F. M., & Mermilliod, W. J. (1977). Some obser-

vations on the host-parasite relationship of Macrobra-

chium ohione (Smith) (Decapoda. Palaemonidae) and

Probopyrus bithynis Richardson (Isopoda. Bopyri-

dae). Crustaceana, 32(2), 216–220.

Valencia, D. M., & Campos, M. R. (2007). Freshwa-

ter prawns of the genus Macrobrachium Bate, 1868

(Crustacea: Decapoda: palaemonidae) of Colombia.

Zootaxa, 1456(1), 1–44. https://doi.org/10.11646/

zootaxa.1456.1.1

Vargas-Ceballos, M. A., López-Uriarte, E., García-Guerre-

ro, M. U., Vega-Villasante, F., Román-Contreras, R.,

Akintola, S. L., Valencia-Martínez, R. E., Rio-Zarago-

za, O. B., Avalos-Aguilar, J. J., & Chong-Carrillo, O.

(2016). Infestation of Probopyrus pacificensis (Isopo-

da: Bopyridae) in Macrobrachium tenellum (Caridea:

Palaemonidae) in the Ameca River. Jalisco. Mexico:

prevalence and effects on growth. Pan-American

Journal of Aquatic Sciences, 11(1), 39–46.

Vergamini, F. G., Pileggi, L. G., & Mantelatto, F. L. (2011).

Genetic variability of the Amazon River prawn

Macrobrachium amazonicum (Decapoda, Caridea,

Palaemonidae). Contributions to Zoology, 80(1),

67–83. https://doi.org/10.1163/18759866-08001003

Vieira, I. M. (2003) Bioecologia e pesca do camarão, Macro-

brachium amazonicum (Heller, 1862) no baixo Rio

Amazonas. [Tesis de maestría]. Universidade Federal

do Amapá.

World Register of Marine Species. (2023). WoRMS: World

cies.org

Zar, J. H. (1999). Biostatistical Analysis (4a ed.).

Prentice-Hall.