Undesirable immigrants: hobbyist vivaria as a potential source of alien invertebrate species

Diversity of invertebrates in terraria

Data on invertebrates noted from tropical vivaria located in 65 Polish cities were used for study including samples collected from 22 localities by 26 hobbyists who provided positive answers in questionnaire presented on Polish internet forum. The number of places to which Collembola (Coecobrya tenebricosa) and Isopoda (Trichorhina tomentosa) were sent by wholesalers over the course of nine months was relatively high (in total, 56 Polish cities, with the average number of 18 cities per month). Moreover, one of the wholesalers delivered such invertebrates to additional destinations, in the Czech Republic, Germany and Sweden.

A total of 12 invertebrate taxa (different taxonomic levels), alien to Polish fauna, and in most cases also to European fauna, were noted. These were classified in four animal phyla including Platyhelminthes (Tricladida), Annelida (Oligochaeta), Mollusca (Gastropoda) and Arthropoda (Collembola, Diplopoda, Chilopoda and Isopoda) (Fig. 2). The list of recorded taxa is placed in the section “Recorded taxa” (numbers indicating localities are referring to the Table S1, Fig. 1).

In case of material collected by hobbyists in their collections, we received information that invertebrates classified as Tricladida, Oligochaeta, Gastropoda, Diplopoda and Chilopoda, started to be seen in vivaria usually soon after new tropical plants were added to the tanks (Bromeliaceae, ferns and/or Peperomia spp.); Germany, the Netherlands and Czech Republic were noted as the countries from which such plants were imported. Three taxa, Rhynchodemus sylvaticus (Leidy, 1851), Trichorhina sp.1, and Guppya gundlachi (Pfeiffer, 1840), were reported from Poland for the first time. In two latter cases, the first record was based on the literature data which were compared with morphological characters of our new material. Recorded invertebrates were recognised as originally occurring in South America (two species), Central America (two species), tropical North America (1–2 depending on whether Rhynchodemus sylvaticus is accepted as native to this region or not), Africa (one species), Eastern Asia (one species) and Southern Europe (one species). In the case of Lumbricidae, Enchytraeidae, Chilopoda and juveniles of Diplopoda it was not possible to identify species and, as a result, we could not provide details about their original distribution. On the other hand, we cannot exclude that at least in some cases undetermined juveniles of Diplopoda could be classified as O. gracilis, as in the same samples adult specimens of that species were present.

Among recorded alien invertebrates, we noted two predators (Lithobiomorpha non. det. and R. sylvaticus), three herbivores (Zonitoides arboreus, Guppya gundlachi, Lehmannia valentiana), and five detritivores (Coecobrya tenebricosa, Oxidus gracilis, Diplopoda non. det., Lumbricidae non. det., Enchytraeidae non. det.). In the case of Rhynchodemus sylvaticus, we noted predatory behaviour towards fruit flies (Drosophila melanogaster) and springtails (on the basis of personal observations). In the case of Zonitoides arboreus, we have found that this species regularly feeds on miniature orchids (Orchidaceae), while Guppya gundlachi forages on other foliage plants (mainly Peperomia).

Overall, 18 mtDNA COI sequences were obtained, which were assigned to 7 BINS in the BOLD Database. Only one of them, assigned to Guppya gundlachi (Gastropoda) formed a new unique BIN. The K2p distance to its closest neighbour, Kaliella scandens (Cox, 1872), amounted 8.08%. The remaining six species were grouped in earlier established BINs (non-unique BINs) containing from one to 71 sequences already existing in BOLD database (Table 1). Maximum intraspecific pairwise K2p distances within BIN were quite low, ranging from 0.16 to 0.91%. In case of Zonitoides arboreus (BIN AAM0135) the intraspecific distance was higher than interspecific, and had a value of 2.0% comparing to 1.04% respectively (Table 1). This gastropod species is assigned to six existing BINs, which may indicate some divergent lineages or even a complex of cryptic species. Summarizing all generated NJ trees and BIN assignments confirmed our species identification (Figs. S1–S7).

Recorded taxa

Phylum: Platyhelminthes

Order: Tricladida

Family: Geoplanidae

Phylum: Arthropoda

Order: Isopoda

Family: Platharthridae

Class: Diplopoda

Family: Paradoxomatidae

Class: Chilopoda

Class: Collembola

Family: Entomobryidae

Phylum: Mollusca

Class: Gastropoda

Family: Gastrodontidae

Family: Euconulidae

Family: Limacidae

Phylum: Annelida

Class: Clitellata

Family: Lumbricidae

Family: Enchytraeidae

Diversity of alien invertebrates in terraria

As a result of the presented study, we have noted 12 invertebrate taxa alien to Polish fauna classified into four different animal phyla. Among species noted by us in this study, three taxa were recorded for the first time from Poland: Rhynchodemus sylvaticus (Rhynchodemidae), Trichorhina sp.1 (Platharthridae), and Guppya gundlachi (Euconulidae). So far Zonitoides arboreus (Gastrodontidae) was found only in one greenhouse in Poland, while Lehmannia valentiana (Limacidae) in two similar sites (Stworzewicz, 2011a; Stworzewicz, 2011b). Although we have not been able to identify all the material to the species level, we believe that this diversity is high (in terms of origin and feeding strategy), especially that we have noted species deriving from four continents including predators and herbivores. Based on the collected data, we know that quite probably most species/specimens were accidentally imported to hobbyists’ collections with plant material (probably both on plant surfaces and in the substrate in which plants were kept). Although the amount of data from vivarium collections is rather limited, there are other numerous examples of such accidental “hitchhikers” in the case of plants grown in greenhouses (e.g., Korkós et al., 2002; Kaszuba & Stworzewicz, 2008; Boros & Dózsa-Farkas, 2008; Leiss, Reischütz & Reischütz, 2008; Horsák, Juřičkova & Picka, 2013; Evangelista et al., 2013; Zawierucha et al., 2013); or aquaria (e.g.: Duggan, 2010; Patoka et al., 2015). In the case of different taxonomic groups studied before, plants and container shipments were known as the most important source of alien terrestrial invertebrates, including e.g.: mites (Kobelt & Nentwig, 2008), spiders (Niedbała, 2010; Zawierucha et al., 2013), land planarians (Ogren, 1985; Mather & Christensen, 1992; Hogan & Dunne, 1996; Winsor, Johns & Barker, 2004; Justine et al., 2014), snails (Robinson, 1999; Cowie, 2005; Dvořak & Kupka, 2007; Głowaciński et al., 2011; Von Proschwitz et al., 2017), diplopods (Stoev, 2004) or oligochaetes (Boros & Dózsa-Farkas, 2007; Boros, 2011). In addition, only in the case of two (or three) taxa, springtail Coecobrya tenebricosa and isopods Trichorhina tomentosa, as well as Trichorhina sp.1, their presence in terraria is directly connected with the use of those invertebrates as a regular food source for poison dart frogs (Lötters et al., 2007; McMonigle, 2013; Steinmann & Van der Lingen, 2013). Moreover, tropical isopods are also known as important detritivores that keep the collections clean in such husbandries (McMonigle, 2013). As a consequence at least one of these species (Trichorhina tomentosa) is widely distributed also out of its native range (Cochard, Vilisics & Secher, 2010).

Potential “dispersal power” of alien vivarium invertebrates

Most species noted in the presented study have a native range in the tropics (see aforementioned section Recorded taxa in Results), where both temperature and humidity are much higher than in temperate regions, including Poland. As a result, we can expect that most of these species can survive only under conditions identical or similar to those observed in their natural habitats, which in Central Europe can be found only in greenhouses, palm houses and collections of tropical frogs or orchids. Thus, their potential dispersal power in Poland and in Central Europe is not high, being strongly limited by climate. As a consequence, they represent only little or even no threat to e.g., local agriculture. On the other hand the results of our simple questionnaire, including information from the surveyed Polish wholesalers clearly showed that at least some alien taxa recorded by us can be widely distributed because of human activity, such as transport to many new locations (Fig. 1). Even if our data were based on information received from only two Polish wholesalers, it clearly suggests, that one season is needed to distribute such alien invertebrates throughout the entire country (in the case of Poland, it is an area of 312,679 km²). This is much faster comparing to the dispersal power of most alien terrestrial and freshwater invertebrates noted in Europe in the wild (Kappes & Hasse, 2012) but similar to species deriving from aquaria (Duggan, 2010; Chucholl, 2013; Kopecký, Kalous & Patoka, 2013; Maceda-Veiga et al., 2013; Patoka et al., 2015). We should also note that in Poland this type of hobby has not had such a long tradition as in Western Europe (especially in Germany, Belgium, the United Kingdom and the Netherlands) and it is not as popular as in countries mentioned above. As a result, the “dispersal power” of at least some of terrarium species listed by our study is even greater on the European scale.

Over 60 localities of alien terrestrial invertebrates noted during one season and located in the whole area of Poland mean dozens of new potential locations where those species can potentially be found in the wild in the near future. We do not provide data about their survival abilities in the wild in Poland (especially the winter period would especially be a natural limit for them), but at least one species from our list (Oxidus gracilis) was noted from the park areas placed close to greenhouses in Poland (Jędryczkowski, 1979; Jędryczkowski, 1982). Moreover, this exotic species was reported also from other regions of Europe, where it was found in the wild, e.g.: in Hungary (Korkós et al., 2002) and Bulgaria (Stoev, 2004). Additional alien species from our terrarium list were noted outside greenhouses in Germany, the Czech Republic, Italy (Zonitoides arboreus—Jueg & Von Proschwitz, 2003; Dvořak & Kupka, 2007; Evangelista et al., 2013) and Spain, Portugal, France (Rhynchodemus sylvaticus—Álvarez Presas et al., 2014). Molecular studies proved that one of the haplotypes of Rhynchodemus sylvaticus founded in Poland is the same as ones founded in Spain, Portugal and France by Álvarez Presas et al. (2014). Moreover, experiments made in Hungary with exotic Enchytraeidae indicated that some species noted mainly in greenhouses could survive the winter outside the greenhouse too (Boros, 2011).

Although most of the species noted by us in this study probably cannot survive in Poland outside terraria and/or greenhouses during winter because of low temperatures, we can expect that in case of future climate warming some species may have a greater chance of establishing in the future.

Potential impact of alien terrarium invertebrates on nature

Most animal invasive species recorded in Europe are terrestrial invertebrates (Roques et al., 2009). Many of them have a significant influence on native flora and fauna as they are predators, plant eaters or vectors of different parasites and diseases (Williamson, 1996). Among the species found in our study at least one taxon is predatory—Rhynchodemus sylvaticus (the undetermined Chilopoda species is most probably also carnivorous). In the vivarium collections, nocturnal R. sylvaticus was observed hunting and feeding on flightless fruit flies (Drosophila melanogaster) and collembolans, invertebrates which are characterised by a quite high escape potential. This allows us to expect that if introduced into nature, it will be able to hunt a large variety of small epigeic invertebrates and it could present a potential risk to other species that have the same dietary needs, as was shown in cases of some other terrestrial planarians by Álvarez Presas et al. (2014).

Similar conclusions can be made in case of plant eaters, especially snails. These species were mentioned by us respectively as orchid and Peperomia spp. feeders, but records of the first one, from natural habitats in the Czech Republic (Dvořak & Kupka, 2007), Germany (Jueg & Von Proschwitz, 2003) and Italy (Evangelista et al., 2013) clearly suggest that it is a much more generalist feeder. It cannot be excluded that under preferable conditions Zonitoides arboreus will have a significant influence on some plant communities, as shown for many other alien terrestrial snails and slugs (e.g.: Kozłowski, 2012). Of course, in the case of all the mentioned alien terrarium species, we can expect that they can be a potential source of some parasites dangerous for native flora and fauna (e.g.: Diéguez-Uribeondo & Söderhäll, 1993).

Moreover, although actually we do not know if any of invertebrate taxa noted by us in vivaria can be found as potential vectors of any kind of diseases, generally it is known that many arthropods or snails are associated with different viruses, bacterias, and/or nematodes. In many cases such species are known as the phoretic (and parasitic) inhabitants of arthropods/molluscs but often are obligate and facultative plant/animal parasites too (e.g.: Hogenhout et al., 2008; Kanzaki & Giblin-Davis, 2018). As a result it cannot be excluded that alien invertebrates recorded in vivaria will have significant negative impact on native flora and/or fauna in the future, as it was suggested e.g., by Hogenhout et al. (2008) and Bragard et al. (2013) for other species.