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Ecology, karyology, and anatomy of the planarian Pentacoelum hispaniense Sluys, 1989 (Platyhelminthes, Tricladida)

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Miquel Vila-Farré at Max Planck Institute for Multidisciplinary Sciences
Miquel Vila-Farré
R Romero
R Romero
R Romero
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R. Sluys
R. Sluys
R. Sluys
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Juana Fernández-Rodríguez at Catalan Institute of Oncology
Juana Fernández-Rodríguez
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Abstract and Figures

On the basis of recently discovered new populations of the triclad flatworm Pentacoelum hispaniense new data are detailed on the ecology, reproduction, karyology, and anatomy of the species, including the first description of the external appearance of living specimens. Living animals show three refringent patches on the dorsal surface of which the nature and function remain unknown. The diploid chromosome complement consists of 14 chromosomes. The species appears to be restricted to relatively warm, lowland bodies of water, where it may be found in heterogeneous habitats. The species reproduces only sexually through the production of cocoons. This study presents the first record of a digenean flatworm parasitizing a marine triclad in the form of a metacercaria.Basándonos en las nuevas poblaciones descubiertas del tríclado Pentacoelum hispaniense aportamos nuevos datos ecológicos, reproductivos, cariológicos y anatómicos de la especie, incluyendo la primera descripción de la anatomía externa. Estos animales presentan tres manchas dorsales refringentes de naturaleza y función desconocidas. El complemento cromosómico diploide consta de 14 cromosomas. La especie parece restringida a masas de agua relativamente cálidas de tierras bajas, donde puede ser encontrada en hábitats heterogéneos. Su reproducción es exclusivamente sexual mediante la producción de capullos. El presente estudio recoge la primera cita de un digenio parasitando un tríclado del grupo de las marícolas, en el estadio de metacercaria.
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Ecology, karyology, and anatomy of the planarian Pentacoelum hispaniense Sluys, 1989 (Platyhelminthes, Tricladid
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... These all concerned the same species as described from Hawaii and Valencia. Therefore, based on morphological and anatomical similarities, it was concluded that the correct species name is P. kazukolinda and that the species has an extensive distributional range (Sluys 1989;Sluys et al. 1990Sluys et al. , 2015Vila-Farré et al. 2008). ...
... It is interesting to relate here the two facts that the presence of larval trematodes was established in specimens from Spanish populations of P. kazukolinda (Vila-Farré et al. 2008;Sluys et al. 2015) and that specimens of the snail P. antipodarum may be infested with several larval stages of trematodes as well (Gérard et al. 2003). In the planarians, the larval stages (metacercaria) were located in both the gut and the mesenchyme, and thus, they may have acquired the parasites through consumption of their mollusc prey. ...
... It is noteworthy that the ponds at Humedales de Ventanilla in Peru are brackish, so that P. kazukolinda is capable of living under such conditions. Similarly, Vila-Farré et al. (2008) reported P. kazukolinda from brackish waters of the Ebro River. ...
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... The species was first described from a single locality in eastern Spain, where the animals were collected from artificial irrigation channels transporting freshwater from the river X uquer to orange groves near the village of Algemes ı (Sluys 1989a; Sluys et al. 1990). More recently, specimens were collected from several populations in the vicinity of the type locality and also at several locations in the Ebro basin; these new finds considerably expanded our knowledge on the external morphology , ecology, karyology and reproduction of this species (Vila-Farr e et al. 2008). We obtained specimens from several new populations of a maricolan triclad that externally looked remarkably similar to the continental Spanish representatives of P. hispaniense, despite the fact that these new samples came from freshwater habitats in Germany, the Netherlands, Mallorca and Japan. ...
... The dorsal surface shows a brown pigmentation, which leaves four whitish areas, particularly under field conditions: (i) a narrow , mid-dorsal stripe, running posteriorly from not far behind the eyes (about 1/4th of the body length from the anterior margin) to a short distance behind the pharynx (Fig. 1), (ii) a broad, more or less rectangular patch directly anterior to the eyes (this patch may be composed of 2–3 separate patches, situated close to each other), (iii) a small, mid-dorsal spot about halfway between the eyes and the root of the pharynx, (iv) a narrow, rectangular patch about halfway between the pharyngeal pocket and the posterior body margin (this patch may consist of 2–3 separate spots close together). Although these four whitish patches are usually clear in living specimens, and also in preserved animals, there are three spots that become very conspicuous in reflected light, thus forming bright, refringent patches (Vila-Farr e et al. 2008). This concerns the patches 2, 3 and 4 listed above. ...
... Therefore, we conclude that the pigmentation causing these spots to be refringent in reflected light generally dissolves during the usual fixation and preservation procedure, in contrast to the rest of the body pigmentation. That the pigment composition of the refringent spots is different from that of the body pigmentation may be deduced also from the fact that hatchlings are unpigmented, except for the refringent spots (Vila-Farr e et al. 2008). A marginal adhesive zone is present, also in the animals from the Ullals de Baltasar locality (see above), but adhesive papillae are absent. ...
The diet and distribution of Pentacoelum kazukolinda (Kawakatsu & Mitchell, 1984), a maricolan planarian with a freshwater ecology
Article
  • Oct 2014
  • ZOOL SCR
Among the marine triclads or Maricola, the genus Pentacoelum represents one of the few exceptions in that species occur in brackish water or in freshwater. We examined specimens of a maricolan triclad that externally looked remarkably similar to the continental Spanish representatives of freshwater Pentacoelum hispaniense, albeit that these new samples came from habitats in Germany, the Netherlands, Mallorca and Japan. Comprehensive comparative morphological studies revealed that the animals from these populations are identical to a species described earlier from Hawaii, viz. Oahuhawaiiana kazukolinda Kawakatsu & Mitchell, 1984. It is argued that the species now should be called Pentacoelum kazukolinda (Kawakatsu & Mitchell, 1984) comb. nov. Remarkably, Dutch and German specimens of P. kazukolinda almost completely lack any signs of the presence of the lateral gonopore system, being the defining feature of their taxonomic family, the Bdellouridae. The reason for this reduction or even complete absence of this structure remains obscure. Nonetheless, morphological similarities and 18S rDNA sequences strongly suggest that all animals belong to the same species. Analyses of the mitochondrial gene sequences Cox1 and 16SrDNA of the gut content of P. kazukolinda revealed that the flatworm has a preference for different species of gastropods, while in one population annelids were detected. Our study suggests that gastropods may form the food refuge of P. kazukolinda. Circumstantial evidence suggests that the worldwide distribution of P. kazukolinda may result from human-mediated transport of the aroid Colocasia esculenta and/or the introduced snail Potamopyrgus antipodarum. The use of P. antipodarum as a food resource may have facilitated the spread and establishment of new populations of P. kazukolinda.
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... The cocoons are deposited though the gonopore and usually, but not always, attached to an appropriate substrate by an adhesive substance. Embryonic development is complex and the rate of development depends upon ambient temperature [83,140]. Embryos progress through an intermediate "larval" stage during which the multiple embryos inside a cocoon feed on and likely compete for the yolk cell food resource [141]. ...
The Ecology of Freshwater Planarians
Chapter
Full-text available
  • Jun 2018
Planarians are on the rise as a model system for regeneration and stem cell dynamics. Almost in parallel the interest in planarian field biology has declined. Besides representing an independent research discipline in its own right, understanding of the natural habitat is also directly relevant to optimizing culture conditions in the laboratory. Moreover, the current laboratory models are but few of hundreds of planarian species worldwide. Their adaptation to a wide range of ecological niches has resulted in a fascinating diversity of regenerative abilities, body size, reproduction strategies, and life expectancy, to name just a few. With the currently ongoing establishment of large planarian species collections, such phenotypic diversity becomes accessible to comparative mechanistic analysis in the laboratory. Overall, we hope that this chapter inspires an integral view of the planarian model system that not only includes the molecular and cellular processes under investigation but also the evolutionary forces that shaped them in the first place.
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Freshwater planarians (Platyhelminthes, Tricladida) from the Iberian Peninsula and Greece: Diversity and notes on ecology
Article
Full-text available
  • Feb 2011
  • ZOOTAXA
Few studies have examined the diversity of freshwater planarians in the Iberian Peninsula and Greece. We have searched extensively for specimens, mainly in the Iberian Peninsula, and have gathered information on their taxonomy and biogeography. Two new species of Dendrocoelum and six new species of Phagocata are described. We also review the status of five other species and present distribution maps that summarize records of freshwater planarians in the Iberian Peninsula. The diversity of three ecological groups of freshwater planarians in this area is discussed and we show that it has a rich, stream-dwelling freshwater triclad fauna, contrary to the findings of earlier studies. But our findings support the traditional viewpoint that European lake-dwelling species are scarce in Spain. The distribution pattern of Girardia tigrina is also discussed. We conclude that the critical status of Schmidtea mediterranea in this area is partly due to habitat alteration through human interference.
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Marine planarians (Platyhelminthes: Tricladida: Maricola) from the western Mediterranean Sea and the Cantabrian coast: New records, one new genus, and immunocytochemistry of the nervous system
Article
Full-text available
  • Mar 2010
  • J MAR BIOL ASSOC UK
Marine planarians were collected extensively from the Iberian Peninsula and Italy. As a result we provide new distributional records of six species of marine triclads, including the description of one new genus and species. The study increases substantially our knowledge of the distribution of this group of animals in Spain and reveals that even relatively well studied areas, such as Italy, still yield new species. In addition, we performed immunostaining studies of the nervous system of three of the species, which revealed the detailed organization of the main nerve cords and their branches. In the new species, the lateral nerve branches showed an arrangement that is different from that of the other species.
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The Effect of Temperature on the Life-Cycle of Four Species of Lake-Dwelling Triclads
Article
  • Feb 1965
1. The effect of constant temperatures on cocoon production, incubation period, development of young to maturation and the complete cycle of Polycelis nigra (Müll.), P. tenuis (Ijima), Dugesia lugubris (O. Schmidt) and Dendrocoelum lacteum (Müll.) has been studied over a range of 1.5-25 degrees C. 2. D. lacteum is the species most tolerant of cold and least tolerant of heat, and can complete more generations per year than the others below 10 degrees C. Dugesia lugubris is least tolerant of cold and most tolerant of heat, and can complete more generations than the others above 10 degrees C. The Polycelis species are intermediate with P. nigra slightly more tolerant of cold than P. tenuis. 3. Failure to breed at low temperatures was in part due to retardation in testis development. At high temperatures both testes and ovaries were adversely affected. But failure to copulate, to produce cocoons, to develop and mature at low and high temperatures also determined the thermal ecology of the species. 4. The temperature thresholds for breeding in these triclad species as determined by laboratory experiments agreed with field data on this parameter and was further confirmed by outdoor experiments with P. tenuis and Dugesia lugubris. 5. Comparison of the thermal ecology of these organisms with the climate of their areas of distribution suggested that temperature may be a contributory factor in determining distribution except for Dendrocoelum lacteum in Britain.
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On Pentacoelum punctatum, an Amphi-Atlantic Marine Triclad (Platyhelminthes: Tricladida: Maricola)
Article
  • Apr 1988
  • Trans Am Microsc Soc
The marine triclad Sabussowia punctata is redescribed on the basis of type material and recently collected specimens from Louisiana, U.S.A. The species is shown to belong to the genus Pentacoelum. Clearly distinguishable lateral bursae in the recently collected specimens confirm that Pentacoelum must be placed in the Bdellouridae. The habitat of the species is in brackish water. In Louisiana, sexually mature specimens may be found throughout the year, but cocoon-laying appears to occur only in spring. The recently collected material indicates that the species has a disjunct, amphi-Atlantic distribution.
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Biodiversity of marine planarians revisited (Platyhelminthes, Tricladida, Maricola)
Article
  • Feb 2005
An account is given of new distributional records and the taxonomy of nine species of marine triclad, including the description of two new species. After more than 100 years of uncertainty, the paper resolves the taxonomic status of the enigmatic nominal species Procerodes solowetzkianus Sabussow, 190011. Sabussow HP Beobachtungen über die Turbellarien der Inseln von Solowetzk. 1900 Trudy Obshchestva Estestvoispytatelei pri Imperatorskom Kazanskom Universitete 34 1 208 pls I–III (in Russian, with German summary) View all references. The study concludes with a biogeographic analysis of all species of marine planarian by documenting patterns of species richness on an equal area grid map of the world.
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Cocoon production, deposition, hatching, and embryonic development in the marine planarian Sabussowia dioica (Platyhelminthes, Tricladida, Maricola)
Article
  • Jul 1999
Cocoons and embryonic development of the dioecious marine planarian Sabussowia dioica are described for the first time. Characteristics of cocoon production, deposition, hatching time, number of hatchlings, and embryonic development are compared with data reported in the literature for other triclads.
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The freshwater planarian Dugesia sicula Lepori, 1948 (Platyhelminthes, Tricladida) in Tunisia: Ecology, karyology, and morphology
Article
  • Apr 2004
A study was carried out on freshwater planarians of the genus Dugesia from three localities in northern Tunisia: Joumine, Chiba, and Lebna. The three populations are fissiparous under field conditions and do not possess reproductive organs, except for some cases of hyperplastic ovaries in the Joumine population. After five months of breeding under laboratory conditions, with water temparature between 18 and 25C and under short photoperiod, 8.33 to 26% of specimens from the Joumine stream became sexualized, together with considerable increase of body length and width. For the other two populations the sexualization rate was very small. Extended period of darkness apparently played a positive role in this sexualization. The phenomenon of sexualization is discussed in the context of reproductive strategies. Histological and karyological studies of the sexualized animals allowed identification of these usually fissiparous planarians as representatives of Dugesia sicula Lepori, 1948. The species is here reported for the first time from Tunisia. The populations are restricted to permanent water basins resulting from the construction of dams in large rivers.
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Ancylid Snails as First Intermediate Hosts of Lissorchis mutabile comb. n. (Trematoda: Lissorchiidae)
Article
  • May 1968
A lissorchiid infection was found in 12% of 7,000 Laevapex fuscus (Adams) and 2,000 Ferrissia rivularis collected in southeastern Michigan. By infecting other hosts experimentally, life history stages were found to be identical to those described for Triganodistomum mutabile. Triganodistomum is reduced to synonymy with Lissorchis; the species accordingly becomes L. mutabile. It is the second trematode species for which both ancylid and planorbid snails are known to serve as natural first intermediate hosts, the other being Megalodiscus temperatus as previously reported.
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Les transformacions econòmiques al Delta de l'Ebre. Serveis d'Estudis, Banca Catalana
  • Jan 1972
  • R Maymó
SERÓ, R. & MAYMÓ, J., 1972. Les transformacions econòmiques al Delta de l'Ebre. Serveis d'Estudis, Banca Catalana. Barcelona. 165 pp.
Life history and embryology of Triganodistomum mutabile (Cort) (Lissorchiidae, Trematoda)
  • Jan 1941
  • 309-326
WALLACE, H. E., 1941. Life history and embryology of Triganodistomum mutabile (Cort) (Lissorchiidae, Trematoda). Transactions of the American Microscopical Society, 60: 309-326.