Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72(S1): e58676, marzo 2024 (Publicado Mar. 01, 2024)

Noble hosts: effects of internal parasites

on the physiology of an intertidal brooding Sea-star

Cintia Pamela Fraysse1*; https://orcid.org/0000-0002-0254-2263

Claudia Clementina Boy1; https://orcid.org/0000-0002-0819-8205

Marianela Veyñ 1; https://orcid.org/0009-0006-0465-314X

Ayelen Farias 1; https://orcid.org/0009-0007-6798-0671

Analía Fernanda Pérez 2; https://orcid.org/0000-0001-5945-7468

1. Laboratorio de Ecología, Fisiología y Evolución de Organismos Acuáticos, Centro Austral de Investigaciones

Científicas (CADIC), Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Ushuaia, Tierra del

Fuego AeIAS, Argentina; fraysse.cintia@gmail.com (*Correspondence), ccboy@conicet.gov.ar, marianela.veyn@gmail.

com, ayelenfarias11790@gmail.com

2. Centro de Ciencias Naturales, Ambientales y Antropológicas (CCNAA), Universidad Maimónides, Laboratorio de

Invertebrados Marinos, Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Ciudad Autónoma

de Buenos Aires, Argentina; analiafperez1@gmail.com

Received 23-I-2023. Corrected 14-IX-2023. Accepted 27-IX-2023.

ABSTRACT

Introduction: The endoparasite Dendrogaster argentinensis infects the intertidal brooder sea star Anasterias

antarctica. This sea-star species is in the highest trophic level in the Beagle Channel.

Objective: To study the effects of parasitism by D. argentinensis on the fitness and reproduction of A. antarctica.

Methods: Adults from the brooder sea-star were collected from the rocky intertidal of Ensenada Zaratiegui bay

(54°51’ S & 68°29’ W), Argentina. Eight seasonal samplings were performed (four seasons in two years) in the

upper and low intertidal. During dissection, parasites were removed, and all organs were extracted and weighed

separately.

Results: Dendrogaster argentinensis prevalence was the highest for the region (20.4 %). Parasitized individuals

were more frequent in the low intertidal in all seasons, with a higher difference in summer, where it is likely that

the higher temperatures and strong winds could make the upper intertidal more challenging for a parasitized

individual. Five parasitized individuals were castrated. Generally, the gonadal (GI) and somatic (pyloric caeca,

PCI; stomach, SI; body wall, WI) indexes were lower in parasitized than non-parasitized individuals.

Conclusions: Parasitism by D. argentinensis negatively affects A. antarctica condition. It affects reproduction

because it reduces the GI, and can also produce castration. The parasite competes for the sea-stars’ ener-

getic resources, also decreasing the individual’s capacity for feeding (reduced stomach) and growth (reduced

body wall).

Key words: Asteroidea; Ascothoracida; parasite; gonadal index; somatic indexes; prevalence; Beagle Channel.

RESUMEN

Huéspedes nobles: los efectos de parásitos internos en la fisiología

de una estrella de mar incubadora del intermareal

Introducción: El endoparásito Dendrogaster argentinensis infecta a la estrella de mar Anasterias antarctica, espe-

cie que se encuentra en el nivel trófico más alto del Canal Beagle.

https://doi.org/10.15517/rev.biol.trop..v72iS1.58676

SUPPLEMENT

2Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72(S1): e58676, marzo 2024 (Publicado Mar. 01, 2024)

INTRODUCTION

Parasites infect animals ranging from

invertebrates to fish and even whales (Pou-

lin & Hamilton, 1997). Parasitic associations

have been casually reported in the literature

between echinoderms and polychaetes, tardi-

grades, barnacles, amphipods, tanaidaceans,

acarians, pycnogonids and insects (Jangoux,

1987). Parasitism is a typical life form among

crustaceans (Bowman et al., 1982) and it has

emerged independently on several occasions in

their phylogenetic history. Generally, parasites

impact marine organisms by decreasing fertil-

ity, increasing mortality and altering the growth

and normal behavior of their hosts. These

direct effects may also indirectly increase the

possibility of predation on parasitized organ-

isms (Dunne et al., 2013; Lafferty et al., 2006;

Mouritsen & Poulin, 2002). Ascothoracida is an

infraclass with six recognized families within

the Crustacea subphylum that comprises a few

more than 100 species with the ability to para-

sitize echinoderms or/and cnidarians (Grygier

& Høeg, 2005; Saito et al., 2020). There are

over thirty species of the genus Dendrogaster

described from various sea stars around the

world, which inhabit from the intertidal to 4

000 m deep (Grygier, 1985; Grygier & Høeg,

2005). This genus consist of endoparasites

species that occupy part of their host’s perivis-

ceral coelom (Grygier, 1985). Females have a

reduced abdomen and thorax with simplifica-

tion or loss of limbs (Webber et al., 2010). The

carapace is enlarged and completely distorted,

forming branches unrecognizable as a crus-

tacean (Webber et al. 2010). Males are tiny,

with a typical crustacean larvae-like morphol-

ogy and are found within the mantle cavity of

females (Boxshall et al., 2005; Grygier, 1985;

Grygier & Høeg, 2005; Grygier & Salvat, 1984;

Webber et al. 2010). Their feeding is poorly

known. A primitive feature of the ascothoracid

parasites is that they feed by the piercing-suck-

ing mouth apparatus (Grygier & Høeg, 2005).

However, the ultrastructure of the cuticle of

the best-known genus of ascothoracid parasite,

Ulophysema, suggests absorptive feeding as rhi-

zocephalan barnacles, it is unclear if it is their

primary mode of food intake (Boxshall et al.,

2005; Grygier & Høeg, 2005). The complete life

cycle, the host infection or the copulation has

not been studied for any ascothoracidan (Box-

shall et al., 2005).

The endoparasite, Dendrogaster argen-

tinensis was first noted to infect Anasterias

minuta [junior synonym of Anasterias ant-

arctica (Mah, 2023; Romanelli-Michel, 2014)]

by Grygier and Salvat (1984). Salvat (1985)

reported an infection rate of 1.5 % in A. minuta

Objetivo: Estudiar los efectos del parasitismo de D. argentinensis en la condición fisiológica y reproducción de

A. antarctica.

Métodos: Adultos de la estrella de mar incubadora fueron recogidos del intermareal rocoso de la bahía Ensenada

Zaratiegui (54°51’ S & 68°29’ W). Se realizaron ocho muestreos estacionales (cuatro temporadas en dos años) en

el intermareal superior y bajo. Durante la disección, se removieron los parásitos, y todos los órganos, los cuales

fueron pesados por separado.

Resultados: La prevalencia de D. argentinensis fue la más alta de la región (20.4 %). Los individuos parasitados

fueron más frecuentes en el intermareal bajo en todas las estaciones, siendo la mayor diferencia en verano, donde

es probable que las temperaturas más altas y los fuertes vientos puedan hacer que el intermareal superior sea

más desafiante para un individuo parasitado. Se observaron cinco individuos parasitados que estaban castrados.

Generalmente, los índices gonadales (GI) y somáticos (ciego pilórico, estómago, y pared del cuerpo) fueron

menores en los individuos parasitados que no parasitados.

Conclusiones: El parasitismo de D. argentinensis afecta negativamente la condición fisiológica de A. antarctica.

Afecta a la reproducción en términos de bajo GI y puede causar castración. El parásito compite por los recursos

energéticos de las estrellas de mar, disminuyendo también la capacidad del individuo para alimentarse (reducción

del estómago) y crecer (reducción de la pared del cuerpo).

Palabras clave: Asteroidea; Ascothoracida; parásito; índice gonadal; índices somáticos; prevalencia; Canal Beagle.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72(S1): e58676, marzo 2024 (Publicado Mar. 01, 2024)

from Ría de Puerto Deseado (Santa Cruz,

Argentina); all parasites were found in the celo-

mic cavity during dissection. Pérez et al. (2017)

found a high prevalence of 11 % in A. antarctica

from the Beagle Channel, the region of high-

est prevalence so far. Anasterias antarctica is a

brooder species inhabiting the intertidal zone

to 185 m depth (Bernasconi, 1964; Romanelli-

Michel, 2014). This species exhibits a wide

distribution, from about 40° S to the south of

Isla Grande de Tierra del Fuego and the north

of the Antarctic Peninsula. They are within

the highest trophic level in the Beagle Channel

(Adami & Gordillo, 1999) and are top predators

of intertidal and sub-tidal communities (Cure-

lovich, 2012). Females brood the lecithotrophic

embryos on the oral surface over the mouth for

eight months, from April to November. (Fraysse

et al., 2021; Pérez et al., 2015; Pérez et al., 2017),

and do not feed during this period (Gil &

Zaixso, 2008; Gil et al., 2011). A recent study

on their reproductive cycle showed that females

undergo two consecutive and different annual

cycles (Fraysse et al., 2021). The first cycle cor-

responds to the production of large oocytes

(approx. 1 080 µm) that, once fertilized, will

develop into a modified lecithotrophic brachio-

laria larva, which will be retained and brooded

(Fraysse et al., 2021). In the second consecutive

cycle, the gonadal maturation produces many

smaller oocytes (approx. 219.30 µm) while the

females are still brooding. Although the female

reproductive effort is 25 % higher than males

(Pérez et al., 2015), males’ gametes production

is greater (Pérez et al., 2017).

The Beagle Channel (55°S, 68° W) has two

semidiurnal tides, which define daily two low

tides and two high tides. The intertidal habitat

is a stressful environment in which species

are exposed to highly variable atmospheric

and oceanographic conditions (Davenport &

Davenport, 2005; Helmuth & Hofmann, 2001).

Stresses resulting from varying environmental

conditions or internal constraints are important

factors causing a decrease in the reproductive

output (Lawrence & Herrera, 2000). In this

context, the main objective of this work was

to study the physiological constraints that may

produce the presence of the endoparasite D.

argentinensis in the brooder sea-star, A. antarc-

tica, which inhabits a stressful environment as

the rocky Fuegian intertidal.

MATERIALS AND METHODS

Area of study: The Beagle Channel (55°S,

68° W) connects the Pacific and Atlantic oceans

at their southernmost extreme. Its waters are

characterized by their low salinity due to

the profuse drainage in both margins; small

streams and rivers that descend from melting

and glaciers towards the sea keep surface values

of salinity below 32 UPS (Fraysse et al., 2021;

Iturraspe et al., 1989; Pérez et al., 2008). Anaste-

rias antarctica individuals were collected from

the rocky intertidal of Ensenada Zaratiegui bay

(Beagle Channel, Fig. 1), in Parque Nacional

Tierra del Fuego (54°51’ S & 68°29’ W; Tierra

del Fuego AIAS, Argentina), where tides are

semidiurnal, defined by two high tides and two

low tides with a marked (0.1–2.3 m) difference

in amplitude (Balestrini et al., 1998; Curelov-

ich, 2012). Eight seasonal samplings (February,

May, August, and November) were carried out

in both 2017 and 2018 from two tidal levels: low

(0.2 m) and upper (1.2 m).

Sampling: A total of 510 adults of A.

antarctica [(> 1.5 cm radius, (Gil et al., 2011,

Pérez et al., 2017)] were collected. They were

transported to the Centro Austral de Inves-

tigaciones Científicas (CADIC) in 3l plastic

containers with portable aerators and seawa-

ter from the sampling site. Before dissection,

each individual was superficially dried with

tissue paper, weighed (total weight ± 0.01 g),

and photographed.

All individuals were anaesthetized by

immersion in MS-222 (ethyl 3-aminobenzo-

ate methanesulfonate acid salt, 98 %, Sigma-

Aldrich) 1 % in seawater, for 45 min (O’Neill,

1994), before dissection (Fraysse et al., 2021).

During dissection, the following variables were

registered: sex (if possible), brooding or non-

brooding condition in females, castration (if

gonads were no present), and presence of the

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coelomic parasites, D. argentinensis (Fig. 2).

Subsequently, gonads, pyloric caeca, stomach

and body wall were weighed.

Population prevalence and gonadoso-

matic indexes: Population prevalence (parasit-

ized frequencies) was calculated as the quotient

between the number of parasitized individuals

and the total number of individuals collected

for each intertidal level and season.

Whereas the prevalence by sex (pro-

portion of parasitized individuals) was con-

structed by season. Castrated individuals were

treated separately.

Fig. 1. Location of the sampling site in Beagle Channel. The Beagle Channel, Ushuaia City, Tierra del Fuego National Park,

Route 3, and sampling area in Ensenada Zaratiegui bay (red dot) are shown.

Fig. 2. A. Oral view of a parasitized individual of Anasterias antarctica from the rocky intertidal of Ensenada Zaratiegui bay

(Beagle Channel) during dissection. B. Dendrogaster argentinensis parasite extracted from A. References: coelomic cavity

(CC), parasite (P), pyloric caeca (PC), main branch (MB), middle piece (MP), and dissection cut (dotted line) to expose the

coelomic cavity.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72(S1): e58676, marzo 2024 (Publicado Mar. 01, 2024)

Gonadal, somatic and parasite load

indexes: Were calculated as follows:

Where Wbc stands for the wet weight of the

body component and Tw is the total wet weight

of the individual before dissection.

Statistical analyses: To evaluate the sex

ratio of the total of parasitized individuals, in

all seasons a Chi-square test was performed.

Also, to evaluate differences in the gonadal

and somatic indexes between parasitized and

non-parasitized individuals T-test were per-

formed for each sex or reproductive condition

(males, brooding and non-brooding females).

This analysis was performed separately for

each body component (gonads, pyloric caeca,

stomach and body wall). The assumptions of

normality (Shapiro–Wilk) and homoscedas-

ticity (Levene) were tested (Sokal & Rohlf,

1995). When assumptions were not met, non-

parametric statistical method was used (Wil-

coxon–Mann-Whitney). For the parasite load

index by season a Kruskal-Wallis test was

performed, followed by Dunn post hoc com-

parisons. Statistical analyses and graphs were

performed using Rstatix package from R soft-

ware (Kassambara, 2023).

RESULTS

Population prevalence: Of the 510 indi-

viduals collected, 104 were parasitized, result-

ing in a prevalence of 20.4 %. Parasitized

individuals were more frequent in the low

intertidal for all seasons (autumn, spring, sum-

mer and winter). However, the greatest dif-

ference between the frequency of parasitized

and non-parasitized individuals was found in

summer (Fig. 3).

Prevalence by sex: On the total of para-

sitized individuals, in almost all seasons, the

sex ratio was 1:1, showing no preference of

the parasite for either sex (Chi-square test,

p = 0.27, p = 0.62 and p = 0.12, for autumn,

spring and summer, respectively), in winter

sex ratio was biased towards males (Chi-square

test, p = 0.04). In spring and summer there

were a few parasitized individuals castrated

(n=2 and n=3, respectively) where the gonads

were absent. Although the number of castrated

individuals was low, all of them were parasit-

ized (Fig. 4).

Fig. 3. Population prevalence of Dendrogaster argentinesis in Anasterias antarctica, from both rocky intertidal levels (upper

and low) of Ensenada Zaratiegui bay (Beagle Channel) by season.

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Gonadal indexes: In females, there were

significant differences between the gonadal

indexes (GI) of parasitized and non-parasitized

individuals, showing lower values (thus reduced

resource allocation to reproduction) in the par-

asitized females than non-parasitized, regard-

less of the reproductive condition, brooding

and non-brooding (Wilcoxon–Mann–Whitney

test, p = 0.04 and p = 0.02, respectively, Fig. 5).

Differences in the GI between brooding and

non-brooding females are due to the fact that

their gonads are in different condition, while

non-brooding females might be ongoing game-

togenesis, brooding females gonads are mainly

post spawned (Fraysse et al. 2021). There were

no significant differences between the GI of

parasitized and non-parasitized males (Wil-

coxon–Mann–Whitney test, p = 0.49).

Somatic indexes: Females in the non-

brooding reproductive condition and males

showed significant differences (t-test, p = 0.04

and Wilcoxon–Mann–Whitney test, p = 0.04,

respectively) between the pyloric caeca index

(PCI) of parasitized and non-parasitized indi-

viduals (Fig. 6), showing lower values those

that were parasitized. However, females in the

brooding reproductive condition did not show

significant differences (t-test, p = 0.06).

There were significant differences between

the stomach index (SI) of parasitized and non-

parasitized individuals. Parasitized females

showed lower values than non-parasitized

(Fig. 7), regardless of the reproductive condi-

tion (Wilcoxon–Mann–Whitney test, p = 0.04

and p < 0.01, for brooding and non-brooding

females, respectively). Also, males showed sig-

nificant differences between parasitized and

non-parasitized individuals (t-test, p < 0.01),

being the SI lower in those parasitized.

Significant differences between the body

wall index (WI) of parasitized and non-parasit-

ized individuals were found. Parasitized females

exhibited lower values than non-parasitized

individuals (Fig. 8), regardless of the reproduc-

tive condition (t-test, p = 0.04 and p = 0.04, for

Fig. 4. Prevalence of Dendrogaster argentinensis in Anasterias antarctica by sex, from the rocky intertidal of Ensenada

Zaratiegui bay (Beagle Channel) showed by (castrated, females, and males) and season.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72(S1): e58676, marzo 2024 (Publicado Mar. 01, 2024)

Fig. 5. Gonadal indexes (GI) expressed in percentages from females in different reproductive condition (brooding and

non-brooding) and males of Anasterias antarctica from the rocky intertidal of Ensenada Zaratiegui bay (Beagle Channel),

compared by parasitized and non-parasitized. Significant differences between parasitized and non-parasitized are indicated

with an asterisk. The horizontal line in the middle of the boxes represents the median and the edges of the boxes the first and

third quartiles. Outliers are shown as points, and a white square indicates the mean.

Fig. 6. Pyloric caeca indexes (PCI) expressed in percentages from females in different reproductive conditions (brooding and

non-brooding) and males of Anasterias antarctica from the rocky intertidal of Ensenada Zaratiegui bay (Beagle Channel),

compared by parasitized and non-parasitized. Significant differences between parasitized and non-parasitized are indicated

with an asterisk. The horizontal line in the middle of the boxes represents the median and the edges of the boxes the first and

third quartiles. Outliers are shown as points, and a white square indicates the mean.

8Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72(S1): e58676, marzo 2024 (Publicado Mar. 01, 2024)

Fig. 7. Stomach indexes (SI) expressed in percentages from females in different reproductive conditions (brooding and

non-brooding) and males of Anasterias antarctica from the rocky intertidal of Ensenada Zaratiegui bay (Beagle Channel),

compared by parasitized and non-parasitized. Significant differences between parasitized and non-parasitized are indicated

with an asterisk. The horizontal line in the middle of the boxes represents the median and the edges of the boxes the first and

third quartiles. Outliers are shown as points, and a white square indicates the mean.

Fig. 8. Body wall indexes (WI) expressed in percentages from females in different reproductive conditions (brooding and

non-brooding) and males of Anasterias antarctica from the rocky intertidal of Ensenada Zaratiegui bay (Beagle Channel),

compared by parasitized and non-parasitized. Significant differences between parasitized and non-parasitized are indicated

with an asterisk. The horizontal line in the middle of the boxes represents the median and the edges of the boxes the first and

third quartiles. Outliers are shown as points, and a white square indicates the mean.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72(S1): e58676, marzo 2024 (Publicado Mar. 01, 2024)

brooding and non-brooding females, respec-

tively). Also, males presented significant differ-

ences between parasitized and non-parasitized

individuals (t-test, p < 0.01), showing the lower

values of WI, those that were parasitized.

Parasite load index: There were significant

differences among the parasite load index (PI)

of individuals from different season (Kruskal-

Wallis, p < 0.01, Fig. 9). The PI values in sum-

mer were lower than autumn (Dunn-test, p <

0.01), spring (Dunn-test, p < 0.01), and winter

(Dunn-test, p = 0.04).

DISCUSSION

This study gathers information on the

physiologic constraints of the brooding sea-star

Anasterias antarctica, when it is parasitized by

Dendrogaster argentinensis (Fig. 2). This sea-

star plays an essential role as a top predator of

the intertidal and subtidal zone in the coasts of

the Beagle Channel.

The overall prevalence of D. argentinesis

was 20.4 %, twice the percentage reported in

2009 by Pérez et al. (2015) in the same region.

While the objective of the study was not to con-

duct an interannual comparison, this increase

in prevalence after almost ten years could be

due to a gradual rise in the average annual

temperature or a high eventual contagion rate

favoring D. argentinensis infection. However,

further studies in this line should be conducted.

By definition, any parasite will harm its host to

a certain degree, from minor metabolic changes

to severe tissue damage (Mouritsen & Poulin,

2002). Regarding the population prevalence

by intertidal zone (upper and low intertidal),

it is evident, in all seasons, that parasitized

individuals are more frequent to find in the

low intertidal (Fig. 3). Furthermore, the dif-

ference between zones becomes more evident

Fig. 9. Parasite load index (PI) expressed in percentages from individuals of Anasterias antarctica from the rocky intertidal

of Ensenada Zaratiegui bay (Beagle Channel), compared by season. Different letters denote significant differences, the

horizontal line in the middle of the boxes represents the median and the edges of the boxes the first and third quartiles.

Outliers are shown as points, and a white square indicates the mean.

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in summer when it is likely that the higher

temperatures and strong winds (Iturraspe et

al., 1989) could make the upper intertidal

more challenging for a parasitized individual

to survive. Whether this is caused by the para-

sitized individuals moving towards a more

comfortable environment or a higher mortal-

ity of parasitized individuals from the upper

intertidal remains unknown. Under usual envi-

ronmental conditions, the infection may not

be mortal, but when conditions approach the

host adaptation limits, a reduced survival may

be expected, particularly in intertidal species

that inhabit the edge of their thermal, osmotic

and oxygen conditions (Mouritsen & Poulin,

2002). For instance, several species of intertidal

or estuarine gastropods show decreased resis-

tance to extreme conditions when infected by

trematodes (Lauckner, 1987; McDaniel, 1969).

In long-term field experiments the higher mor-

tality among infected snails was observed in

winter and summer, when the abiotic factors

also reach their extremes (Huxham et al., 1993;

Mouritsen & Poulin, 2002). Compromised sur-

vival of infected individuals is not restricted to

gastropods. This was also reported in bivalves,

such as Mytilus edulis, that acts either as first

or second intermediate host of trematodes, and

experience reduced condition, byssus thread

production, and may be easier to open by pred-

ators (Calvo-Ugarteburu & McQuaid, 1998;

Zwarts, 1991). A third plausible hypothesis

could be that the dispersal or survival of the

parasite is lower in the upper intertidal, but

more biological studies of the species are need-

ed to confirm this.

When analyzing the prevalence by sex in

each season, the parasite only shows a prefer-

ence for male individuals in winter (Fig. 4). The

difference in prevalence between males and

females in this season could be either because

females are committed to brooding in winter, or

a higher mortality of brooding females during

this season. The first hypotheses lays on the fact

that during brooding females carry their off-

spring on the oral area and do not feed (Gil et

al., 2011); they may be less active and thus, less

exposed to D. argentinensis infection. Males may

also be more susceptible to infection since they

are more active during this period because they

dynamically search for food and refuge. The

second hypothesis of the higher mortality of

brooding females in winter is founded upon the

idea that in this season they have already faced

half of the brooding period. Also, the cost of the

incubation effort must be added to the extreme

winter conditions that may hinder the survival

of the females. In addition, the parasitic load

in winter remains high (Fig. 9). Salvat (1985)

reported five parasitized individuals, two were

females, two males and one had no gonads. In

this work, although the number of castrated

individuals was low, they were all parasitized

(present only in spring and summer). This is

an important observation since this parasite is

known to castrate their host (Hamel & Mercier,

1994; Jangoux, 1987; Tyler & Pain, 1982). The

presence of castrated individuals with endo-

parasite in the celomic cavity was also noticed

by Pérez et al. (2015). According to Brattström

(1947), castration results from competition for

resources between gonads and the ascothoracid

parasites, Ulophysema oeresundense, in Spa-

tangoids (heart sea urchins). This competition

leading to castration was also noted by Wagin

(1976) in Ophiocten sericeum (Ophiuroid host)

infested by Ascothorax ophioctenis.

Several works on parasitism of different

ascothoracid parasites mention adverse effects

on reproduction and fecundity in sea-stars

(Grygier, 1985; Grygier, 1986; Grygier & Sal-

vat, 1984; Hamel & Mercier, 1994; Jangoux,

1987; Tyler & Pain, 1982). D. argentinensis

negatively affects the reproduction in A. ant-

arctica. Concerning the gonadal indexes (GI,

Fig. 5), parasitized females showed lower GI

than non-parasitized individuals, regardless of

the reproductive condition (brooding and non-

brooding). In the case of non-brooding females,

this will result in the reduction of fecundity,

given either by fewer oocytes and then fewer

embryos of equal quality to those not parasit-

ized females or same number of oocytes of

lower quality than the non- parasitized females

that could led to decreased survival. Repro-

duction it is metabolically more expensive for

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72(S1): e58676, marzo 2024 (Publicado Mar. 01, 2024)

females of A. antarctica (Fraysse et al., 2021;

Pérez et al., 2017) than males, therefore, being

parasitized will help increase that cost result-

ing in reduced gonadal index and fecundity.

In contrast, males do not go through starva-

tion periods, and their reproductive expenses

are also lower than females, so the costs of

parasitism may not be reflected in the gonadal

index. Gonad’s atrophy was observed in Hip-

pasteria phrygiana individuals compared with

other unparasitized sea-stars (Hamel & Mer-

cier, 1994). This gonad decrease was explained

as being probably induced by interference with

nutrient translocation to the gonads (Hamel &

Mercier, 1994).

Regarding the somatic indexes, the pyloric

caeca (PCI, Fig .6), the stomach (SI, Fig. 7), and

body wall (WI, Fig. 8) indexes of parasitized

individuals were significantly lower than non-

parasitized from each sex, except in brooding

parasitized females, where the PCI showed the

same pattern, but without significant difference.

Thus, evidence is presented on how the parasite

restricts the feeding ability, the nutrients stor-

age, and the growth, which led to a decrease of

the overall condition. In Ría de Puerto Deseado

(Santa Cruz, Argentina) an infected individual

of A. antarctica presented atrophied pyloric

caeca which was explained by the lack of avail-

able space in the celomic cavity (Grygier &

Salvat, 1984; Salvat, 1985). In heavy infestation

of Ophionotus victoriae by Ascothorax gigas, the

stomach volume was observed to be reduced,

but there was no demonstrable reduction in the

volume of stomach contents (Grygier & Fratt,

1986). The reduction of the stomach volume,

also noted in this study, can be related to the

endoparasite feeding on the celomic fluids

of the host as Brattström (1947) determined

for Ulophysema oeresundense parasite and its

echinoid host. Wagin (1976) proposed that the

main diet of Dendrogaster sp could be encap-

sulating coelomocytes. This same competition

from nutrients between the host and the endo-

parasite could lead to a decrease in the body

wall index since it could be affecting growth in

A. antarctica. Contrary, the parasites found in

Hippasteria phrygiana did not seem to affect the

host’s pyloric caeca nor the body wall (Hamel

& Mercier, 1994). The decreased parasite load

index in summer (Fig. 9) could be because the

endoparasite females mature throughout the

year and, in summer, release the cypris larvae.

Consequently, on one hand, this will place

new hosts and begin their maturation, and on

the other hand will leave the mature female

spawned, thus exhibiting lower parasite load

indexes in the host. Nevertheless, D. argenti-

nensis reproduction cycle is not yet described

(Boxshall et al., 2005). This work suggests

that the ascothoracid parasite D. argentinensis

would affect the physiological condition and

reproduction of A. Antarctica from the Beagle

Channel. We provide evidence of how the endo-

parasite adversely affects its host and its overall

condition. It affects reproduction by decreasing

fecundity and fitness, it enhances the reduction

of the feeding capacity, nutrient storage, and

growth by consuming and competing for the

host resources (nutrients), and it is also prob-

ably related to the castration of individuals.

Nevertheless, it is important to note that the

biology of D. argentinensis and its interaction

with A. antarctica can be influenced by vari-

ous environmental and biological factors, and

more studies are needed to fully understand

the dynamics of this parasite-host relationship.

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.

ACKNOWLEDGMENTS

We are grateful to Sonia Rimbau and Dan-

iel Aureliano, technicians of Laboratorio de

Ecología, Fisiología y Evolución de Organismos

Acuáticos (CADIC-CONICET), Ing. Maximil-

iano Rubel, and Dr. Pablo Di Salvatore for their

technical assistance during the samplings. We

12 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72(S1): e58676, marzo 2024 (Publicado Mar. 01, 2024)

also thank Consejo Nacional de Investigaciones

Científicas y Técnicas (CONICET) and Felipe

Fiorellino Foundation.

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