The land flatworm Amaga expatria (Geoplanidae) in Guadeloupe and Martinique: new reports and molecular characterization including complete mitogenome.

BACKGROUND: The land flatworm Amaga expatria Jones & Sterrer, 2005 (Geoplanidae) was described from two specimens collected in Bermuda in 1963 and 1988 and not recorded since. METHODS: On the basis of a citizen science project, we received observations in the field, photographs and specimens from non-professionals and local scientists in Martinique and Guadeloupe. We barcoded (COI) specimens from both islands and studied the histology of the reproductive organs of one specimen. Based on Next Generation Sequencing, we obtained the complete mitogenome of A. expatria and some information on its prey from contaminating DNA. RESULTS: We add records from 2006 to 2019 in two French islands of the Caribbean arc, Guadeloupe (six records) and Martinique (14 records), based on photographs obtained from citizen science and specimens examined. A specimen from Martinique was studied for histology of the copulatory organs and barcoded for the COI gene; its anatomy was similar to the holotype, therefore confirming species identification. The COI gene was identical for several specimens from Martinique and Guadeloupe and differed from the closest species by more than 10%; molecular characterisation of the species is thus possible by standard molecular barcoding techniques. The mitogenome is 14,962 bp in length and contains 12 protein coding genes, two rRNA genes and 22 tRNA genes; for two protein genes it was not possible to determine the start codon. The mitogenome was compared with the few available mitogenomes from geoplanids and the most similar was Obama nungara, a species from South America. An analysis of contaminating DNA in the digestive system suggests that A. expatria preys on terrestrial molluscs, and citizen science observations in the field suggest that prey include molluscs and earthworms; the species thus could be a threat to biodiversity of soil animals in the Caribbean.

The invasive land flatworm Obama nungara (Platyhelminthes: Geoplanidae) reaches a natural environment in the oceanic island of São Miguel (Açores).

During an entomological sampling trip in the island of São Miguel (Açores, Portugal) on 02-11-2019 by José Rafael González-López, one specimen of the invasive flatworm Obama nungara Carbayo et al. 2016 was found under a rock (Fig. 1A). The specimen was photographed in situ and identified by its external morphology based on its large and broad leaf-like body with nearly parallel body margins, narrow and rounded anterior end, rounded posterior end, and dorsal pigmentation consisting of a light brown ground color covered with dark longitudinal and irregular stripes, and ventral surface grayish-white. Recent studies (Justine et al. 2020; Negrete et al. 2020) showed the reliability of photograph-based identification of O. nungara specimens. It is the sixth island where this species has been found (after Guernsey, Great Britain, Ireland, Corsica, and Madeira).

New records of the giant planarian Polycladus gayi Blanchard, 1845 (Platyhelminthes: Geoplanidae) with notes on its conservation biology.

Land planarians (Tricladida:Geoplanidae) comprise about 910 species distributed in four subfamilies and can be found on all continents except Antarctica (Sluys Riutort 2018; Sluys 2019). The Neotropical region possesses nearly 31% of all the described terrestrial planarian species, most of them belonging to the subfamily Geoplaninae (Sluys 1999; Grau Carbayo 2010). Land planarians are mostly habitat-specialists, living in the humid soils of native forest, and predating on invertebrates like earthworms, isopods, mollusks and harvestmen, among others (Ogren 1995; Carbayo Leal-Zanchet 2003; Boll Leal-Zanchet 2016). Although most planarian species seem to be physiologically sensitive, for example to environmental moisture, a few land planarian genera like Bipalium Stimpson and Obama Carbayo et al., have successfully invaded many habitats, even in highly perturbed areas (Kawaguti 1932; Sluys 2019). Therefore, some of these invertebrate species appear to be good candidates as habitat quality bioindicators according to some authors (Sluys 1998; Gerlach et al., 2013; Negrete et al., 2014).

Diversity out of simplicity: interaction behavior of land planarians with co-occurring invertebrates.

Land planarians have a simple anatomy and simple behavioral repertoire in relation to most bilaterian animals, which makes them adequate for the study of biological processes. In this study, we investigate the behavior of land planarians during interaction events with other invertebrates found in the same environment. We observed 16 different behavioral units, including seven different capture behaviors and three different prey ingestion behaviors. The capture behavior varied from very simple, such as simply covering the prey with the body, to more complex ones, including two forms of tube formation that are described for the first time. In general, the capture behaviors were similar among different predators but different for different prey. Similarly, prey ingestion type was more related to prey type than to predator species, with small soft prey being swallowed without fragmentation, large prey being crushed, and prey with a hard skeleton being perforated. Considering that land planarians face limitations due to their lack of efficient ways to retain water, thus being highly dependent on a moist environment, the set of behaviors shown by them in this study was considerably rich, especially concerning strategies to capture prey.

Preference for different prey allows the coexistence of several land planarians in areas of the Atlantic Forest.

Land planarians are recognized as important predators, yet studies on their feeding habits are usually restricted to invasive species. Thus, it is difficult to determine the real ecological role of this group in ecosystems and how their communities are structured. In the present study, we analyzed the diet of six co-occurring Neotropical land planarians and their success in capturing prey, based on experiments in the laboratory, in order to determine how they share resources in the same environment. We also calculated indices of food niche breadth and food niche overlap for land planarians for the first time. The diet of Luteostriata abundans comprises only woodlice and the diets of Obama ficki and Obama ladislavii are composed only of gastropods, while Paraba multicolor and Obama anthropophila feed on both gastropods and other land planarians. An invasive species recently found in Western Europe, Obama nungara, showed the highest food niche breadth, feeding on gastropods, earthworms and planarians. We found the highest niche overlap between O. anthropophila and P. multicolor. The results suggest that land planarians are frequent predators of woodlice and land gastropods in the Neotropical ecozone and thus are important for the maintenance of native ecosystems and for the control of invasive species. The coexistence of several species in the same habitat is possible due to the use of different species as main prey, which reduces interspecific competition.

A taste for exotic food: Neotropical land planarians feeding on an invasive flatworm.

Invasive species establish successfully in new habitats especially due to their ability to include new species in their diet and due to the freedom from natural enemies. However, native species may also adapt to the use of new elements in their ecosystem. The planarian Endeavouria septemlineata, first recorded in Hawaii, was later found in Brazil. Recently, we found it in human-disturbed areas in southern Brazil and here we investigate its interactions with other invertebrates both in the field and in the laboratory. We observed the species in the field during collecting activities and hence maintained some specimens alive in small terraria in the laboratory, where we offered different invertebrate species as potential prey and also put them in contact with native land planarians in order to examine their interaction. Both in the field and in the laboratory, E. septemlineata showed a gregarious behavior and was found feeding on woodlice, millipedes, earwigs and gastropods. In the laboratory, specimens often did not attack live prey, but immediately approached dead specimens, indicating a scavenging behavior. In an experiment using the slug Deroceras laeve and the woodlouse Atlantoscia floridana, there was a higher consumption of dead specimens of woodlice and slugs compared to live specimens, as well as a higher consumption of dead woodlice over dead slugs. Four native land planarians of the genus Obama and one of the genus Paraba attacked and consumed E. septemlineata, which, after the beginning of the attack, tried to escape by tumbling or using autotomy. As a scavenger, E. septemlineata would have no impact on the populations of species used as food, but could possibly exclude native scavengers by competition. On the other hand, its consumption by native land planarians may control its spread and thus reduce its impact on the ecosystem.

Composição das comunidades de planárias terrestres (Platyhelminthes, Tricladida, Terricola) do Parque Nacional dos Aparados da Serra, Brasil

The National Park of Aparados da Serra (PNAS), located at the Eastern border of Araucarian Plateau, is one of the main protected areas of Southern Brazil, being characterized by the occurrence of fragments of mixed ombrophilous forest, surrounded by wet and dry grassland fields, and a continuous area of dense ombrophilous forest. We registered for the PNAS 35 species of land planarians, distributed into five genera (Geoplana Stimpson, 1857, Choeradoplana Graff, 1896, Notogynaphallia Ogren & Kawakatsu, 1990, Pasipha Ogren & Kawakatsu, 1990 and Cephaloflexa Carbayo & Leal-Zanchet, 2003) of the family Geoplanidae, subfamily Geoplaninae. We observed 23 and 21 species, respectively, in the areas of mixed ombrophilous forest and dense ombrophilous forest. The Jaccard's similarity coefficient between the two areas was 0.42. In areas of dry grassland field, only one species was observed. Seven species were collected in disturbed open habitats, four of them also observed in the forest areas. The known distribution of four species, i.e., Cephaloflexa bergi (Graff, 1899), Notogynaphallia graffi Leal-Zanchet & Froehlich, 2006, Geoplana franciscana Leal-Zanchet & Carbayo, 2001, and Geoplana josefi Carbayo & Leal-Zanchet, 2001, the two latter ones having been known only from their type-locality, is amplified.

O Parque Nacional dos Aparados da Serra (PNAS), localizado na borda oriental do Planalto das Araucárias, é uma das principais unidades de conservação do sul do Brasil, caracterizando-se pela ocorrência de fragmentos de floresta ombrófila mista, intermediada por campos secos e úmidos, e por uma área contínua de floresta ombrófila densa. Registraram-se, para o PNAS, 35 espécies de planárias terrestres, distribuídas em cinco gêneros (Geoplana Stimpson, 1857, Choeradoplana Graff, 1896, Notogynaphallia Ogren & Kawakatsu, 1990, Pasipha Ogren & Kawakatsu, 1990 e Cephaloflexa Carbayo & Leal-Zanchet, 2003), pertencentes à família Geoplanidae, subfamília Geoplaninae. Observaram-se 23 e 21 espécies, respectivamente, nas áreas de floresta ombrófila mista e floresta ombrófila densa. O coeficiente de similaridade de Jaccard entre as duas formações foi de 0,42. Em áreas de campo nativo foi observada apenas uma espécie. Sete espécies foram coletadas em áreas abertas antropizadas, sendo quatro delas também observadas nas áreas de floresta. Amplia-se a distribuição de quatro espécies, a saber, Cephaloflexa bergi (Graff, 1899), Notogynaphallia graffi Leal-Zanchet & Froehlich, 2006, Geoplana franciscana Leal-Zanchet & Carbayo, 2001, e Geoplana josefi Carbayo & Leal-Zanchet, 2001, as duas últimas conhecidas somente da sua localidade-tipo.

Composição das comunidades de planárias terrestres (Platyhelminthes, Tricladida, Terricola) do Parque Nacional dos Aparados da Serra, Brasil

The National Park of Aparados da Serra (PNAS), located at the Eastern border of Araucarian Plateau, is one of the main protected areas of Southern Brazil, being characterized by the occurrence of fragments of mixed ombrophilous forest, surrounded by wet and dry grassland fields, and a continuous area of dense ombrophilous forest. We registered for the PNAS 35 species of land planarians, distributed into five genera (Geoplana Stimpson, 1857, Choeradoplana Graff, 1896, Notogynaphallia Ogren & Kawakatsu, 1990, Pasipha Ogren & Kawakatsu, 1990 and Cephaloflexa Carbayo & Leal-Zanchet, 2003) of the family Geoplanidae, subfamily Geoplaninae. We observed 23 and 21 species, respectively, in the areas of mixed ombrophilous forest and dense ombrophilous forest. The Jaccard's similarity coefficient between the two areas was 0.42. In areas of dry grassland field, only one species was observed. Seven species were collected in disturbed open habitats, four of them also observed in the forest areas. The known distribution of four species, i.e., Cephaloflexa bergi (Graff, 1899), Notogynaphallia graffi Leal-Zanchet & Froehlich, 2006, Geoplana franciscana Leal-Zanchet & Carbayo, 2001, and Geoplana josefi Carbayo & Leal-Zanchet, 2001, the two latter ones having been known only from their type-locality, is amplified.

O Parque Nacional dos Aparados da Serra (PNAS), localizado na borda oriental do Planalto das Araucárias, é uma das principais unidades de conservação do sul do Brasil, caracterizando-se pela ocorrência de fragmentos de floresta ombrófila mista, intermediada por campos secos e úmidos, e por uma área contínua de floresta ombrófila densa. Registraram-se, para o PNAS, 35 espécies de planárias terrestres, distribuídas em cinco gêneros (Geoplana Stimpson, 1857, Choeradoplana Graff, 1896, Notogynaphallia Ogren & Kawakatsu, 1990, Pasipha Ogren & Kawakatsu, 1990 e Cephaloflexa Carbayo & Leal-Zanchet, 2003), pertencentes à família Geoplanidae, subfamília Geoplaninae. Observaram-se 23 e 21 espécies, respectivamente, nas áreas de floresta ombrófila mista e floresta ombrófila densa. O coeficiente de similaridade de Jaccard entre as duas formações foi de 0,42. Em áreas de campo nativo foi observada apenas uma espécie. Sete espécies foram coletadas em áreas abertas antropizadas, sendo quatro delas também observadas nas áreas de floresta. Amplia-se a distribuição de quatro espécies, a saber, Cephaloflexa bergi (Graff, 1899), Notogynaphallia graffi Leal-Zanchet & Froehlich, 2006, Geoplana franciscana Leal-Zanchet & Carbayo, 2001, e Geoplana josefi Carbayo & Leal-Zanchet, 2001, as duas últimas conhecidas somente da sua localidade-tipo.