First record of endoparasitism of Pycnogonida in Hydrozoan polyps (Cnidaria) from the Brazilian coast

Primeiro registro de endoparasitismo de Pycnogonida em pólipos de hidrozoário (Cnidaria) da costa brasileira

Abstracts

Despite the relatively high number of recent studies on Cnidaria off the Brazilian coast, we have observed only two records of parasitism on macromedusae and none on polyps. Endoparasitic associations between Pycnogonida larvae and hydroids have been well known since the early 20^th century. Protonymph larvae develop inside the gastrovascular cavity of polyps, typically gastrozooids, which are then called gallzooids. This short communication is an unprecedented record of parasitism on the polyps of Brazilian cnidarian fauna. The parasitic association between Pycnogonida Anoplodactylus stictus and a new hydroid species of Podocoryna has been casually detected on the encrusting communities of experimental polyethylene plates installed at the Paranaguá Yacht Club, Paranaguá, south of Brazil from February 2007 to February 2008. This hydrozoan host is most likely an exotic species because it had not been observed in previous studies of Paranaguá Bay or beaches along the southern coast of Brazil in the previous 20 years. Eighty-eight hydroid colonies were analyzed, of which 19 were parasitized mainly from June to August 2007. Protonymphs were pink-red colored, similar to gallzooids and all other polyps of the colony, thus indicating that they had eaten the hosts' tissues. Up to six protonymphs were observed inside the gallzooids. The gallzooid column was elongated, and the tentacles were atrophied or even absent because of the development of the larvae. Some observations of endoparasitism in two live colonies that were maintained in aquaria until their complete disappearance (one month) are also described in this note.

benthic community; hydrozoan polyp; interspecific relationship; Pantopoda; protonymph

Apesar do número relativamente elevado de estudos recentes sobre Cnidaria da costa brasileira, encontramos dois casos de parasitismo, ambos em macromedusas, e nenhum em pólipos. Associações endoparasíticas entre larvas de picnogônidas e hidroides são bem conhecidas desde início do século 20. A larva protoninfa desenvolve-se no interior da cavidade gastrovascular dos pólipos, geralmente dos gastrozoóides, que são então chamados “gallzooids”. Esta nota é um registro inédito de parasitismo em pólipos de cnidários da fauna brasileira. A associação parasitária entre o picnogônida Anoplodactylus stictus e uma espécie nova de hidroide do gênero Podocoryna foi detectada casualmente sobre a comunidade incrustante de placas experimentais, instaladas no Iate Clube de Paranaguá, Paranaguá, sul do Brasil, de fevereiro/2007 a fevereiro/2008. O hospedeiro hidrozoário provavelmente é uma espécie exótica, pois não havia sido observado em estudos anteriores da Baía de Paranaguá ou praias ao longo da costa sul do Brasil nos últimos 20 anos. Foram analisadas 88 colônias do hidroide das quais 19 estavam parasitadas, principalmente nos meses de junho a agosto/2007. As protoninfas eram rosa-avermelhadas, a mesma coloração dos “gallzooids” e dos demais pólipos da colônia, indicando que elas ingeriram tecidos do hospedeiro. Até seis protoninfas foram observados no interior dos “gallzooids”. O comprimento da coluna dos “gallzooids” alongava e os tentáculos atrofiavam ou mesmo desapareciam devido ao desenvolvimento das larvas. Algumas observações do endoparasitismo em duas colônias vivas mantidas em aquários, até seu desaparecimento completo (um mês), também são descritas nesta nota.

comunidade bentônica; hidroide; relação interespecífica; Pantopoda; protoninfa

Introduction

Interspecific relationships between hydrozoan polyps and other marine organisms, such as sponges, bryozoans, molluscs, polychaetes, tunicates and vertebrates (Gili & Hughes 1995, Puce et al. 2008), include common epibiosis (Cerrano et al. 2001, Gili et al. 2006, Cunha & Jacobucci 2010) and predation (Madin et al. 1996, Bavestrello et al. 2000, Cerrano et al. 2000) and closer associations, such as commensalism (Hand & Hendrickson 1950, Braverman 1960, Bavestrello et al. 1996, Genzano & San Martin 2002), mutualism (Caine 1998, Cerrano et al. 1998, Raskoff & Robison 2005) and parasitism (Heb & Melzer 2003).

In parasitic associations, polyps may be the parasite or act as the host (in this short communication, we consider the organism that lives inside a host or has a body part embedded into the host tissues to be the parasite, cf. Boero & Bouillon (2005)) (Boero et al. 1991, Piraino et al. 1992, Rhode 2005, Evans et al. 2008). Fungi, protozoans and rotifers can be polyp ectoparasites (Gili & Hughes 1995, Rhode 2005), and Pycnogonida is notable in its ecto- or endoparasitic associations with hydroids (Staples 2005). Pycnogonida/hydroid endoparasitism is characterized by the development of the pycnogonid protonymph inside the gastrovascular cavity of polyps, typically gastrozooids. These parasitized polyps are called gallzooids (Staples & Watson 1987, Genzano 2002, Heb & Melzer 2003).

Until the late 20^th century, 470 species of Cnidaria had previously been recorded in Brazilian continental and marine waters (Migotto et al. 1999). Currently, this number is approximately 600, with new observations in southeast and southern Brazil (Silveira & Morandini 2011, Van Ofwegen & Haddad 2011). From 1997 to 2007, many studies were published on traditional and molecular taxonomy, ecology, toxicity, life cycles and other aspects of this fauna (summary in Haddad & Marques 2009). This hydrozoan host is most likely an exotic species in Paranaguá Bay, State of Paraná, South of Brazil because it was not observed in previous studies conducted in this location (Correia & Silva 1990, Neves et al. 2007, Neves & Rocha 2008). Because the organism was identified as a new species of the genus Podocoryna M. Sars, 1846, the origin of hydroid is unknown. Molecular analysis showed that it is a sister species of P. hayamaensis Hirohito, 1988 from Japan (Dr. Maria Pia Miglietta and Dr. Peter Schuchert, pers. comm. The manuscript describing the new species is in preparation; therefore, we refer to it as Podocoryna n. sp. in this paper).

Despite the relatively high number of recent studies, we have observed only two records of parasitism in Brazilian cnidarians, both on macromedusae (Morandini et al. 2005, Nogueira Junior & Silva 2005). Cases of parasitic relationships with cnidarian polyps have not been observed, although many cases of endoparasitic associations between Pycnogonida larvae and hydroids have been recognized since the early 20^th century (Table 1). In the majority of these cases, the parasitized species are not uncommon to southeastern and southern Brazilian hydrozoan fauna (Table 1). Therefore, this short communication is an unprecedented record of parasitism on polyps for the cnidarian fauna of Brazil. Some observations of endoparasitism in live colonies are also described.

Table 1.
Records of the endoparasitism of Pycnogonida larvae in hydroid colonies (Hydrozoa). Classifications cf. the “World Register of Marine Species” (WoRMS, 2012).

Hydroid	Pycnogonida	Localities of record	Reference
Subclasse Leptothecata Cornelius, 1992
Sertulariidae Lamouroux, 1812
Amphisbetia minima (Thompson, 1879)	-	Australia	Staples & Watson (1987)
Sertularella polyzonias Hartlaub, 1901	-	-	Warren (1908)*
Sertularia Linnaeus, 1758	Anoplodactylus Wilson, 1878	Monterey Bay, California	Russel & Hedgpeth (1990)
Sertularella Gray, 1848	Unidentified pycnogonid larvae	South Africa	Warren (1908)**
Sertularella Gray, 1848	Unidentified pycnogonid larvae	South Africa	Flynn (1928)**
Campanulariidae Johnston, 1836
Ecopella everta (Clarck, 1896)	Ammothea hilgendorfi (Böhm, 1879)		Russel & Hedgpeth (1990)
Clytia Lamouroux, 1812	Anoplodactylus petiolatus (Kröyer, 1844)		Russel & Hedgpeth (1990)
Obelia Péron & Lesueur, 1810	Anoplodactylus pygmaeus (Hodge, 1862)	-	Helfer (1932)*
Obelia bidentata Clark, 1875	Anoplodactylus Wilson, 1878	Papua New Guinea	Staples & Watson (1987)
Campanularia australis Stechow, 1924	-	Australia	Staples & Watson (1987)
Campanularia integra Macgillivray, 1842	-	Australia	Staples & Watson (1987)
Plumulariidae Agassiz, 1862
Plumularia australis Kirchenpauer, 1876	-	Australia	Staples & Watson (1987)
Subclasse Anthoathecata Cornelius, 1992
Tubulariidae Goldfuss, 1818
Tubularia crocea (Agassiz, 1862)	Anoplodactylus erectus Cole, 1904	-	Frey & Leuckart (1847)*
Tubularia crocea (Agassiz, 1862)	Anoplodactylus erectus Cole, 1904	-	Hilton (1916)*
Tubularia Linnaeus, 1758	Phoxichilidium tubulariae Lebour, 1945	-	Loman (1907)*
Tubularia larynx (Ellis & Solander, 1786)	Phoxichilidium tubulariae Lebour, 1945	Gulf of Maine, New Castle, USA	Lovely (2005)
Corynidae Johnston, 1836
Sarsia eximia (Allman, 1859)	-	-	Allman (1860)*
Sarsia eximia (Allman, 1859)	Phoxichilidium coccineum (Johnston, 1837)	-	Hodge (1862)*
Sarsia radiata von Lendenfeld, 1884	Anoplodactylus Wilson, 1878	Australia	Staples & Watson (1987)
Coryne muscoides (Linnaeus, 1761)	Phoxichilidium virescens Hodge, 1864;	-	Staples & Watson (1987)
Coryne muscoides (Linnaeus, 1761)	Anoplodactylus pygmaeus (Hodge, 1862)	-	Staples & Watson (1987)
Coryne pusilla (Gaertner, 1774)	Anoplodactylus Wilson, 1878	New Zealand	Staples & Watson (1987)
Coryne sp.	Amonthea sp.	-	Allman (1860)**
Coryne sp.	Anoplodactylus pygmaeus (Hodge, 1864)	-	Sanches (1959)**
Stylasteridae Gray, 1847	Unidentified pycnogonid larva	-	Moseley (1879)**
Bougainvillidae Lütken, 1850
Bougainvillia ramosa (van Beneden, 1844)	-	-	Van Beneden (1844)*
Bougainvillia ramosa (van Beneden, 1844)	-	-	Gegenbaur (1854)*
Bougainvillia ramosa (van Beneden, 1844)	Phoxichilidium virescens Hodge, 1864	-	Staples & Watson (1987)
Bougainvillia ramosa (van Beneden, 1844)	Anoplodactylus pygmaeus (Hodge, 1862)	-	Staples & Watson (1987)
Bougainvillia Lesson, 1830	Phoxichilidium Milne-Edwards, 1840	-	Hallez (1905)*
Bimeria vestita Wright, 1859	Anoplodactylus petiolatus (Kröyer, 1844)	Mar del Plata, Argentina	Genzano (2002)
Bougainvillia muscus (Allman, 1863)	Anoplodactylus petiolatus (Kröyer, 1844)	Mar del Plata, Argentina	Genzano (2002)
Hydractiniidae L. Aggasiz, 1862
Podocoryne carnea (M. Sars, 1846)	Phoxichilidium virescens Hodge, 1864	-	Staples & Watson (1987)
Podocoryne carnea (M. Sars, 1846)	Anoplodactylus pygmaeus (Hodge, 1862)	-	Staples & Watson (1987)
Hydractinia echinata Fleming, 1823	-	-	Wright (1863)*
Hydractinia echinata Fleming, 1823	-	-	Semper (1864)*
Hydractinia echinata Fleming, 1823	-	-	Dohrn (1881)*
Hydractinia echinata Fleming, 1823	-	-	Dogiel (1913)*
Hydractinia echinata Fleming, 1823	-	-	Bourdillon (1952)*
Hydractinia echinata Fleming, 1823	Phoxichilidium virescens Hodge, 1864	-	Staples & Watson (1987)
Hydractinia echinata Fleming, 1823	Anoplodactylus pygmaeus (Hodge, 1862)	-	Staples & Watson (1987)
Hydractinia echinata Fleming, 1823	Anoplodactylus petiolatus (Kröyer, 1844)	Helgoland, Deutschland, Germany	Heb & Melzer (2003)

• ^*
  References cited in Staples & Watson (1987);
• ^**
  References cited in Bain (2003).

Material and Methods

The parasitized hydrozoan colonies were observed within a set of 48 experimental polyethylene plates (14 × 14 cm) installed at the marinas of the Paranaguá Yacht Club situated at the Itiberê River mouth (25° 31′ S and 48° 30′ W), Paranaguá Bay, State of Paraná, Brazil (Figure 1). The experiment was conducted to study the succession of encrusting species on the artificial plates between February 2007 and February 2008 (Altvater 2009, Cangussu et al. 2010).

Figure 1.
Location of the Paranaguá Yacht Club ? inside Paranaguá Bay (where Podocoryna n. sp. was observed on the polyethylene plates) and Paraná State (dark area) in Brazil.

Two polyethylene plates were also collected for tracking parasitized colonies in vivo. Only one Podocoryna n. sp. colony was maintained on the plates, and all other colonies and organisms, except Pycnogonida, were removed. Each plate was placed in separate aquaria with water from the collection site and maintained under constant aeration. The colonies were fed with Artemia salina nauplii approximately three times a week. From one of the plates, the gallzooids of the colony and Pycnogonida adults were removed to establish a control and were referred to as “desparasitized”. The other colony was denoted “parasitized”. The coverage area of the colonies and each type of zooid (gastro-, gono-, tentaculo- and gallzooids) was estimated under a stereomicroscope using a grid divided into 81 quadrants.

Results

The Pycnogonida parasite species was identified as Anoplodactylus stictus by the original description of Marcus (1940), and the hydrozoan host was a species of the Podocoryna genus. The hydroid morphology resembled that of Podocoryna carnea (M. Sars, 1846) Hydractiniidae, but the 16S rDNA analysis revealed that it was a distinct species (Haddad et al. in preparation).

Fragments of the Podocoryna n. sp. colonies were deposited into the following Cnidaria collections: 1) Museu de Zoologia da Universidade de São Paulo, Brazil (MUZUSP-001908) and 2) Departamento de Zoologia da Universidade Federal do Paraná, Brazil (DZoo-Cn 026). The specimens of Anoplodactylus stictus were also deposited in the Pantopoda collection of the Museu de Zoologia da Universidade de São Paulo, Brazil.

The parasitic association was casually detected on the encrusted communities of the artificial substrata collected in Paranaguá. We observed 88 Podocoryna n. sp. colonies on 28 of the 48 polyethylene plates of the experiment. The colonies were clear-pink, and the polyp hypostomes were highlighted by their whitish color. Nineteen parasitized colonies were distributed on nine plates mainly from June to August 2007. The gallzooids were modified gastrozooids containing one to six protonymphs of A. stictus (Figures 2a, b).

Figures 2.
Larval endoparasitism of the Pycnogonida Anoplodactylus stictus in gastrozooids of the hydroid Podocoryna n. sp.: a) A portion of a Podocoryna n. sp. colony: the arrows indicate groups of gastrozooids, and the arrow heads indicate gallzooids; scale bar: 1 cm.; b) An isolated gallzooid with tree protonymphs inside; scale bar: 0.1 cm; c) Juvenile A. stictus newly released from inside a gallzooid: a – anterior, p – posterior; scale bar: 0.5 cm. Photographs: (a, c) obtained with a Leica^® MZ16 stereomicroscope with a Leica^® DFC500 camera and processed in Auto-Montage Pro-3.5 Syncroscopy; (b) obtained with an Olympus^® BX 51 optical microscope with an Olympus^® America INC Oly-200 camera using the Honestech TVR 2.5 program.

At the initial phase of endoparasitism, the lower section of the gallzooids column appeared slightly dilated and brightly colored. The protonymphs rapidly grew inside the gallzooids and were easily recognizable by their pinkish-red color, thus indicating that they consumed the polyp tissues (Figure 2c). The gallzooids tentacles atrophied or disappeared, whereas their column was elongated and conformed to the number and arrangement of larvae that were concentrated at the bottom or distributed along the column length (Figure 2b). No parasitized gono- or tentaculozooids were observed among the polyps of the Podocoryna n. sp. colonies.

When the two live colonies (one parasitized and one desparasitized) were placed into the aquaria, the parasite larvae were easily visible inside the gallzooids (Figures 2a, b). After eight days, the pinkish colored juveniles emerged with the fourth pair of appendices yet incompletely developed. When the juveniles were released from the gallzooids, no tissues remained inside the polyps, thus demonstrating that they were completely consumed by the parasite. New gallzooids did not appear during the period that the colonies survived in the aquaria (one month).

At the beginning of the observation period, the parasitized and desparasitized colonies had a high density of polyps and covered 8.78 cm² and 16.3 cm² of the plates, respectively. The polyps were mainly gastrozooids and covered approximately 70% of the total area of the colonies (Table 2).

Table 2.
Estimate of the area and composition of the Podocoryna n. sp. colonies at the beginning of the laboratory observations.

Colony	Total area cm2	% gastrozooid	% gonozooid	% tentaculozooid	% gallzooid
Desparasitized	16.3	75.3	7.6	5.1	12.0
Parasitized	8.8	67.2	0	17.2	15.6

The degeneration began from the center of both colonies when the polyps decreased in size and lost their tentacles. The gallzooids (parasitized colony) quickly disappeared after the release of the juveniles, which became predators of the polyps. The gono- and tentaculozooids degenerated on the ninth day in the aquaria. The tentaculozooids of the parasitized colony remained active for longer. The gastrozooids degenerated gradually, and both colonies of Podocoryna n. sp. disappeared from the plates in one month (Figure 3). The desparasitized colony developed two stolons at its edge before total degeneration.

Figure 3.
Variation of the Podocoryna n. sp. colony areas while maintained in the aquaria.

Discussion

How Pycnogonida larvae locate and penetrate gastrozooids has not yet been defined. Heb & Melzer (2003) observed that when small specimens of the Pycnogonida Anoplodactylus petiolatus (Krøyer, 1844) Phoxichilidiidae walked on colonies of Hydractinia echinata (Fleming, 1828) Hydractiniidae, parts of or their entire body was retained inside the gastrovascular cavity of the gastrozooids. The captured individuals could escape without damage. This fact suggested that swallowed protonymphs could develop undamaged inside the gastrozooids (Heb & Melzer 2003). Most likely, A. stictus has an immunity against Podocoryna n. sp. nematocysts and is unpalatable to the hydroid, as proposed by Heb & Melzer (2003) for A. petiolatus. If endoparasitism depends on the ingestion of the larvae by gastrozooids, the absence of parasitized gono- and tentaculozooids in the Podocoryna n. sp. colonies is most likely because of the inability of these polyps to capture or swallow the protonymphs.

The Pycnogonida species that have an post-embryonic development with “encysted protonymphs” (see the review of Pycnogonida embryonic and post-embryonic development types in Brenneis et al. (2011a, b)) experience several molts inside the polyps. According to Bain (2003) and Lovely (2005), Pycnogonida hatch as juveniles in the fourth or fifth instar with a bud of walking leg 4 (Brenneis et al. 2011b), similar to the A. stictus that we observed in the aquaria. However, the hatching of A. stictus juveniles after the consumption of the gallzooid tissues of the Podocoryna n. sp. colonies contrasts with the report of Lovely (2005), who observed the parasite Phoxichilidium tubulariae Lebour, 1945 Phoxichilidiidae extending its legs to get rid of the gallzooids of Tubularia larynx Ellis & Solander, 1786 Tubulariidae.

The endoparasitic association between Pycnogonida and Cnidaria has been minimally investigated. The few studies regarding this association are mainly devoted to the description of the Pycnogonida life cycle (Russel & Hedgpeth 1990, Genzano 2002, Lovely 2005); therefore, whether endoparasites affect the development or growth of the hydroid colony is not clarified. Both the parasitized and desparasitized colonies of Podocoryna n. sp. survived one month inside the aquaria, gradually degenerating simultaneously. We observed that the absence or reduced number of tentacles in the gallzooids did not compromise the nutrition of these polyps. In fact, the gastrozooids efficiently captured the brine shrimp nauplii and became orange-colored internally, which also occurred with the gallzooids. The orange contents of the gallzooids indicated that if they could not catch the prey, they received food through the gastrovascular network.

Both the parasitized and desparasitized colonies of Podocoryna n. sp. possessed few gonozooids, signalizing they were about to complete their life cycle, and degeneration occurred in the natural process of their life span. When analyzing the succession of the encrusting community on the polyethylene plates from Paranaguá (pers. observ.), we observed that the parasitism by the A. stictus protonymphs mainly occurred in the larger and post-reproductive Podocoryna n. sp. colonies. After the period of parasitism, the colonies disappeared from the plates, similar to what occurred in the control colonies maintained in the aquaria. Therefore, although these preliminary observations of endoparasitism between A. stictus and Podocoryna n. sp. are not conclusive, they may suggest that the presence or absence of adult Pycnogonida on the colonies and small number of gallzooids most likely did not alter the survival time of the hydroid host.

Acknowledgements

We would like to thank the staff of the Paranaguá Yacht Club for kindly providing space for the study. We also thank Luciana Altvater, who conducted her master's dissertation at the Universidade Federal do Paraná and allowed the analysis of part of her data to be presented in this short communication. Ariane L. Bettim received a research grant from the CNPq.

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Publication Dates

• Publication in this collection
  Apr-Jun 2013

History

• Received
  28 Aug 2012
• Reviewed
  1 Apr 2013
• Accepted
  1 May 2013