Open-access First record of the non-native rotifer Kellicottia bostoniensis (Rousselet, 1908) in Bromeliaceae phytotelma

The rotifer species Kellicottia bostoniensis (Rousselet, 1908) is a transcontinental invader native to North America that has spread to the South American continent (Branco et al., 2024). In the Upper Paraná River floodplain, the first record of the occurrence of K. bostoniensis was in 2000, and since then, this non-native species has spread across the landscape (Bomfim et al., 2016). Non-native species are organisms introduced outside their natural range due to human activities, but they do not necessarily harm ecosystems, on the other hand, invasive species, a subset of non-natives, spread rapidly and cause significant ecological, economic, or health impacts (Colautti and MacIsaac, 2004). Invasive species typically possess traits like rapid growth and high reproductive rates, which give them a competitive edge in new environments (Woods and Moriarty, 2001). K. bostoniensis, for example, produces resting eggs, which enable survival under unfavorable environmental conditions (Gomes et al., 2022) and contribute to its high dispersal capacity and persistent presence in various tropical environments. (Paggi 2002; Casanova et al., 2009; Picapedra et al., 2021; Branco et al., 2024). Recent research indicates a global expansion of this species, suggesting a high potential for colonization on multiple wetlands in the coming years (Zhdanova et al., 2016; Mantovano et al., 2021; Branco et al., 2024).

Alongside biological challenges, multiple dispersal vectors facilitate the spread of non-native species. Aquatic plants and birds serve as passive carriers for these species (Zhdanova et al., 2016), while adult insects, through their flights, actively transport invertebrates and planktonic organisms (De Bie et al., 2012).

The Bromeliaceae family is widely distributed in Brazilian rainforests and is known for their distinctive shape, with leaves arranged in a rosette shape (Hermes et al., 2018). The rosette shape of the leaves favors rainwater storage, creating true natural microcosms known as phytotelma (Farjalla et al., 2016). Bromeliads have high commercial potential and are exported to various parts of the world, which can facilitate the passive spread of non-native species for new habitats (Kolicka et al., 2016), since, in the tanks formed by the rosettes, various biological communities inhabit the retained water (phytotelma) (Little and Hebert, 1996).

Studies on the composition of species present in phytotelms are more advanced, such as zooplankton, macroinvertebrates, annelids, protozoa, algae, and cyanobacteria (Kitching, 2000; Lopez et al., 2009; Duarte et al., 2013; Mendes et al., 2020). However, there is still little research on the impact of non-native species on bromeliad phytotelms in their native areas. This study describes the first record of the species K. bostoniensis in Bromeliaceae.

The Paraná River's left bank, which is situated on the Upper Paraná River floodplain (22°50’S; 53°40’W), served as the study's site (Figure 1). The Paraná River is located in the Conservation Unit (UC): Environmental Protection Area of the Islands and Floodplains of the Paraná River (Agostinho et al., 2004; Silva et al., 2024).

Figure 1
The study area shows the upper Paraná River floodplain and the sampling point.

Sampling was carried out on a rock wall on the left bank of the Paraná River, at a height of approximately 15 meters above the river surface (22°45'02” S 53°13'29” W). Three specimens of the bromeliad Aechmea distichantha lem., endemic to South America (Barberis et al., 2020), were sampled (Figure S1, Supplementary Material). The maximum amount of water was extracted from each tank, with the largest bromeliad containing 400 ml. The bromeliad sampled had 12 leaves, varying in size from 30 to 90 cm. The water tank was 35 cm high and 30 cm in diameter. The contents were suctioned using a Pasteur pipette and a suction hose to collect the water in the tanks. The samples were stored in glass jars and fixed with Transeau solution in a 6:3:1 ratio of water, alcohol, and formaldehyde. The limnological variables of the water stored in the bromeliad couldn't be measured because the equipment wasn't available during sampling. The invertebrates were analyzed in a Sedgewick-Rafter chamber and identified to the highest possible taxonomic level, with the help of specialized literature (Koste and Hardy, 1984).

The K. bostoniensis individuals found in the evaluated phytotelmata were present in the tank with the largest size and volume of stored water, coexisting with other organisms such as macroinvertebrates, other zooplankton, and phytoplankton. This individual is stored at the Universidade Estadual de Maringá, in the Research Center for Limnology, Ichthyology, and Aquaculture. In total, two individuals, the K. bostoniensis were found in the phytotelmata, one of the individuals had damage to its structures and its measurements were not computed in this study (Figure 2). The total body length of K. bostoniensis analyzed was 330 µm, incorporating values from the posterior spine, lorica, and anterior spine. The lorica body length was 110 µm, and its width was 60 µm. The left anterior lateral spine had a length of 30 µm, and the left anterior middle spine was 35 µm. The largest right anterior spine had a length of 130 µm, and the right anterior middle spine was 30 µm. The posterior spine had a length of 90 µm.

Figure 2
Kellicottia bostoniensis in different positions. (A) lateral view, (B) ventral view, (C) lateral view with altered angle.

Our finding of K. bostoniensis in phytotelmata on the Upper Paraná floodplain demonstrates the dispersal capacity of this non-native species. Although the presence of the rotifer in A. distichantha bromeliads represents only an initial record, it suggests the species' ability to explore new ecological niches, given its already documented success in adapting and establishing itself in a variety of environments (Bomfim et al., 2016). This is due to characteristics such as morphological plasticity, such as asexual reproduction through parthenogenesis, production of resistant eggs, presence of spines to avoid predation, rapid individual proliferation, and high environmental tolerance (Allan, 1976; Drake, 2004; Zhdanova and Dobrynin, 2011; Schröder and Gilbert, 2004; Zhang et al., 2017; Gomes et al., 2022).

A species' potential invasion begins when organisms are accidentally or intentionally transported (Colautti and MacIsaac, 2004) via dispersal vectors, initiating the first stage of invasion, described by Richardson (2011) as the entry. The subsequent stages, establishment, and propagation will only occur if the species overcomes environmental and biological constraints (Lockwood et al., 2013).

The ecological impacts of the non-native species K. bostoniensis on the environments where it establishes itself have yet to be well documented (Oliveira et al., 2019). However, preliminary research indicates that K. bostoniensis can alter the dynamics of zooplankton communities (Paggi, 2002), mainly through competition for food resources (Oliveira et al., 2019). As a result, the discovery of this species in bromeliad phytotelms offers fresh proof of the organisms' ability to spread. Although they are not invasive and have not been shown in studies (Arcifa et al., 2020) to be able to compete with native species, they are steadily expanding their range of occupations in South America.

Supplementary Material

Supplementary material accompanies this paper.

Figure S1.

This material is available as part of the online article from https://doi.org/10.1590/1519-6984.289526

Acknowledgements

We thank Dr. Andréa Bialetzki, Dr. Rosemara Fugi, and Dr. Sidinei Magela Thomaz for substantially improving the manuscript. We also acknowledge Nupelia (UEM), the Programa de Pós-Graduação em Ecologia de Ambientes Aquáticos Continentais (PEA), the Programa de Pós-Graduação em Biologia Comparada (PGB), and PELD/CNPq (site 6-PIAP) for their logistical and financial support.

References

  • AGOSTINHO, A.A., THOMAZ, S.M. and GOMES, L.C., 2004. The Upper Paraná River floodplain: Biodiversity and conservation. In: S.M. THOMAZ, A.A. AGOSTINHO and N.S. HAHN, eds. The Upper Paraná River and its floodplain: physical aspects, ecology and conservation Leiden: Backhuys Publishers, pp. 59-103.
  • ALLAN, J.D., 1976. Life history patterns in zooplankton. American Naturalist, vol. 110, no. 971, pp. 165-180. http://doi.org/10.1086/283056
    » http://doi.org/10.1086/283056
  • ARCIFA, M.S., SOUZA, B.B., MORAIS-JUNIOR, C.S. and BRUNO, C.G.C., 2020. Functional groups of rotifers and an exotic species in a tropical shallow lake. Scientific Reports, vol. 10, no. 1, pp. 14698. http://doi.org/10.1038/s41598-020-71778-1 PMid:32895424.
    » http://doi.org/10.1038/s41598-020-71778-1
  • BARBERIS, I.M., KLEKAILO, G., ALBERTENGO, J., CÁRCAMO, J.I., CÁRCAMO, J.M. and GALETTI, L., 2020. Ramet demography of Aechmea distichantha (Bromeliaceae) in two contrasting years in the understory and open areas of a South American xerophytic forest. Rodriguésia, vol. 71, e00262018. http://doi.org/10.1590/2175-7860202071014
    » http://doi.org/10.1590/2175-7860202071014
  • BOMFIM, F.F., MANTOVANO, T., SCHWIND, L.T.F., PALAZZO, F., BONECKER, C.C. and LANSAC-TÔHA, F.A., 2016. Geographical spread of the invasive species Kellicottia longispina (Kellicott, 1879) and K. bostoniensis (Rousselet, 1908): a scientometric approach. Acta Scientiarum. Biological Sciences, vol. 38, no. 1, pp. 29-36. http://doi.org/10.4025/actascibiolsci.v38i1.28252
    » http://doi.org/10.4025/actascibiolsci.v38i1.28252
  • BRANCO, C.W.C., SANTOS-CABRAL, L.C., KOZLOWSKY-SUZUKI, B., LOPES, V.G., PUGA, A.L. and MACÊDO, R.L., 2024. Persistence of the non-native Kellicottia bostoniensis (Rousselet, 1908) in a large tropical reservoir. Hydrobiologia, vol. 851, pp. 3039-3060. http://doi.org/10.1007/s10750-023-05295-3.
  • CASANOVA, S.M.C., PANARELLI, E.A. and HENRY, R., 2009. Rotifer abundance, biomass, and secondary production after the recovery of hydrologic connectivity between a river and two marginal lakes (São Paulo, Brazil). Limnologica, vol. 39, no. 4, pp. 292-301. http://doi.org/10.1016/j.limno.2009.06.008
    » http://doi.org/10.1016/j.limno.2009.06.008
  • COLAUTTI, R.I. and MACISAAC, H.J., 2004. A neutral terminology to define ‘invasive’ species. Diversity & Distributions, vol. 10, no. 2, pp. 135-141. http://doi.org/10.1111/j.1366-9516.2004.00061.x
    » http://doi.org/10.1111/j.1366-9516.2004.00061.x
  • DE BIE, T., DE MEESTER, L., BRENDONCK, L., MARTENS, K., GODDEERIS, B., ERCKEN, D., HAMPEL, H., DENYS, L., VANHECKE, L., VAN DER GUCHT, K., VAN WICHELEN, J., VYVERMAN, W. and DECLERCK, S.A., 2012. Body size and dispersal mode as key traits determining metacommunity structure of aquatic organisms. Ecology Letters, vol. 15, no. 7, pp. 740-747. http://doi.org/10.1111/j.1461-0248.2012.01794.x PMid:22583795.
    » http://doi.org/10.1111/j.1461-0248.2012.01794.x
  • DRAKE, J.M., 2004. Allee effects and the risk of biological invasion. Risk Analysis, vol. 24, no. 4, pp. 795-802. http://doi.org/10.1111/j.0272-4332.2004.00479.x PMid:15357800.
    » http://doi.org/10.1111/j.0272-4332.2004.00479.x
  • DUARTE, G.S.C., ALVES, G.M., LANSAC-TÔHA, F.M., VELHO, L.F.M. and LANSAC-TÔHA, F.A., 2013. Flagellate protist abundance in phytotelmata of Aechmea distichantha Lem. (Bromeliaceae) in the upper Paraná river basin. Acta Scientiarum. Biological Sciences, vol. 35, no. 4, pp. 491-498. http://doi.org/10.4025/actascibiolsci.v35i4.17134
    » http://doi.org/10.4025/actascibiolsci.v35i4.17134
  • FARJALLA, V.F., GONZÁLEZ, A.L., CÉRÉGHINO, R., DÉZERALD, O., MARINO, N.A., PICCOLI, G.C., RICHARDSON, B.A., RICHARDSON, M.J., ROMERO, G.Q. and SRIVASTAVA, D.S., 2016. Terrestrial support of aquatic food webs depends on light inputs: a geographically-replicated test using tank bromeliads. Ecology, vol. 97, no. 8, pp. 2147-2156. http://doi.org/10.1002/ecy.1432 PMid:27859200.
    » http://doi.org/10.1002/ecy.1432
  • GOMES, A.C.A.M., MACÊDO, R.L., GOMES, L.F., VELHO, L.F.M., ROCHA, O. and VIEIRA, L.C.G., 2022. Range expansion of Kellicottia bostoniensis (Rousselet, 1908) (Rotifera) throughout a biogeographic boundary between the Brazilian savanna and the Amazon. Aquatic Sciences, vol. 84, no. 2, pp. 28. http://doi.org/10.1007/s00027-022-00861-8
    » http://doi.org/10.1007/s00027-022-00861-8
  • HERMES, M.B., MOREIRA, A.S.F.P., CASTRO, N.M. and OLIVEIRA, D.C., 2018. Structural variation among leaves in Aechmea distichantha Lem. (Bromeliaceae) rosettes, considering apical and basal differences. Flora Morphol Distrib Funct Ecol Plants., vol. 248, pp. 76-86. http://doi.org/10.1016/j.flora.2018.08.018
    » http://doi.org/10.1016/j.flora.2018.08.018
  • KITCHING, R.L., 2000. Food webs and container habitats: the natural history and ecology of phytotelmata Cambridge: Cambridge University Press. http://doi.org/10.1017/CBO9780511542107
    » http://doi.org/10.1017/CBO9780511542107
  • KOLICKA, M., GWIAZDOWICZ, D.J., HUPAŁO, K., JABŁOŃSKA, A., KOTWICKI, L., KORNOBIS, F., LAMENTOWICZ, M., MAGOWSKI, W., MARCISZ, K., PRONIN, M., RECZUGA, M.K., OLSZANOWSKI, Z. and ZAWIERUCHA, K., 2016. Hidden invertebrate diversity - phytotelmata in Bromeliaceae from palm houses and florist wholesalers (Poland). Biologia., vol. 71, no. 2, pp. 194-203. http://doi.org/10.1515/biolog-2016-0026
    » http://doi.org/10.1515/biolog-2016-0026
  • KOSTE, W. and HARDY, E.R., 1984. Taxonomic studies and new distribution records of Rotifera (Phylum Aschelminthes) from Rio Jatapú and Uatumã, Amazonas, Brazil. Amazoniana. Limnologia et Oecologia Regionalis Systematis Fluminis Amazonas, vol. 9, pp. 17-29.
  • LITTLE, T. and HEBERT, P., 1996. Endemism and ecological islands: the ostracods from Jamaican bromeliads. Freshwater Biology, vol. 36, no. 2, pp. 327-338. http://doi.org/10.1046/j.1365-2427.1996.00094.x
    » http://doi.org/10.1046/j.1365-2427.1996.00094.x
  • LOCKWOOD, J.L., HOOPES, M.F. and MARCHETTI, M.P., 2013. Invasion ecology. 2nd ed. Hoboken: Wiley-Blackwell.
  • LOPEZ, L.C.S., NÓBREGA ALVES, R.R. and RIOS, R.I., 2009. Micro-environmental factors and the endemism of bromeliad aquatic fauna. Hydrobiologia, vol. 625, no. 1, pp. 151-156. http://doi.org/10.1007/s10750-009-9704-1
    » http://doi.org/10.1007/s10750-009-9704-1
  • MANTOVANO, T., DINIZ, L.P., CONCEIÇÃO, E.O., ROSA, J., BONECKER, C.C., BAILLY, D., FERREIRA, J.H.D., RANGEL, T.F., and LANSAC-TÔHA, F.A., 2021. Ecological niche models predict the potential distribution of the exotic rotifer Kellicottia bostoniensis (Rousselet, 1908) across the globe. Hydrobiologia, vol. 848, no. 2, pp. 299-309. http://doi.org/10.1007/s10750-020-04435-3
    » http://doi.org/10.1007/s10750-020-04435-3
  • MENDES, P.M.S., LANSAC-TÔHA, F.M., MEIRA, B.R., OLIVEIRA, F.R., VELHO, L.F.M. and LANSAC-TÔHA, F.A., 2020. Heterotrophic flagellates (Amorpha and Diaphoretiches) in phytotelmata bromeliad (Bromeliaceae). Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 80, no. 3, pp. 648-660. http://doi.org/10.1590/1519-6984.218742 PMid:31644658.
    » http://doi.org/10.1590/1519-6984.218742
  • OLIVEIRA, F.R., LANSAC-TÔHA, F.M., MEIRA, B.R., SEGOVIA, B.T., COCHAK, C. and VELHO, L.F.M., 2019. Effects of the exotic rotifer Kellicottia bostoniensis (Rousselet, 1908) on the microbial food web components. Aquatic Ecology, vol. 53, no. 4, pp. 581-594. http://doi.org/10.1007/s10452-019-09710-7
    » http://doi.org/10.1007/s10452-019-09710-7
  • PAGGI, S.J., 2002. New data on the distribution of Kellicottia bostoniensis (Rousselet, 1908) (Rotifera: Monogononta: Brachionidae): its presence in Argentina. Zoologischer Anzeiger, vol. 241, no. 4, pp. 363-368. http://doi.org/10.1078/0044-5231-00077
    » http://doi.org/10.1078/0044-5231-00077
  • PICAPEDRA, P.H.S., FERNANDES, C., BAUMGARTNER, G. and SANCHES, P.V., 2021. Zooplankton communities and their relationship with water quality in eight reservoirs from the midwestern and southeastern regions of Brazil. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 81, no. 3, pp. 701-713. http://doi.org/10.1590/1519-6984.230064 PMid:32876161.
    » http://doi.org/10.1590/1519-6984.230064
  • RICHARDSON, D.M., ed., 2011. Fifty years of invasion ecology: the legacy of Charles Elton Hoboken: Wiley-Blackwell.
  • SCHRÖDER, T. and GILBERT, J.J., 2004. Transgenerational plasticity for sexual reproduction and diapause in the life cycle of monogonont rotifers: intraclonal, intraspecific and interspecific variation in the response to crowding. Functional Ecology, vol. 18, no. 3, pp. 458-466. http://doi.org/10.1111/j.0269-8463.2004.00854.x
    » http://doi.org/10.1111/j.0269-8463.2004.00854.x
  • SILVA, J.V.F., VELHO, L.F.M., LANSAC-TÔHA, F.A. and BONECKER, C.C., 2024. 30 year review of the zooplankton in three conservation units on the Upper Paraná River, Brazil, with notes for stressors, flood pulse, and public politics. Hydrobiologia, vol. 852, pp. 23-42. http://doi.org/10.1007/s10750-024-05703-2.
  • WOODS, M. and MORIARTY, P., 2001. Strangers in a strange land: the problem of exotic species. Environmental Values, vol. 10, no. 2, pp. 163-190. http://doi.org/10.3197/096327101129340796
    » http://doi.org/10.3197/096327101129340796
  • ZHANG, H., HOLLANDER, J. and HANSSON, L.A., 2017. Bi-directional plasticity: rotifer prey adjust spine length to different predator regimes. Scientific Reports, vol. 7, no. 1, pp. 10254. http://doi.org/10.1038/s41598-017-08772-7 PMid:28860451.
    » http://doi.org/10.1038/s41598-017-08772-7
  • ZHDANOVA, S.M. and DOBRYNIN, A.E., 2011. Kellicotia bostoniensis (Rousselet, 1908) (Rotifera: Brachionidae) in waterbodies of European Russia. Inland Water Biology, vol. 4, no. 1, pp. 39-46. http://doi.org/10.1134/S1995082911010147
    » http://doi.org/10.1134/S1995082911010147
  • ZHDANOVA, S.M., LAZAREVA, V.I., BAYANOV, N.G., LOBUNICHEVA, E.V., RODIONOVA, N.V., SHURGANOVA, G.V., KULAKOV, D.V. and IL’IN, M.Y., 2016. Distribution and ways of dispersion of American rotifer Kellicottia bostoniensis (Rousselet, 1908) (Rotifera: Brachionidae) in waterbodies of European Russia. Russian Journal of Biological Invasions, vol. 7, no. 4, pp. 308-320. http://doi.org/10.1134/S2075111716040111
    » http://doi.org/10.1134/S2075111716040111

Publication Dates

  • Publication in this collection
    14 Mar 2025
  • Date of issue
    2025

History

  • Received
    19 Aug 2024
  • Accepted
    13 Jan 2025
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