Arxius de Miscel·lània Zoològica. Volum 21 (2023) Pàgines: 253-260
Distribution of the alien Tubificid worm Branchiura sowerbyi (Beddard, 1892) in Morocco
Taybi, A. F., Mabrouki, Y., van Haaren, T.DOI: https://doi.org/10.32800/amz.2023.21.0253
CitaTaybi, A. F., Mabrouki, Y., van Haaren, T., 2023. Distribution of the alien Tubificid worm Branchiura sowerbyi (Beddard, 1892) in Morocco. Arxius de Miscel·lània Zoològica, 21: 253-260, DOI: https://doi.org/10.32800/amz.2023.21.0253
Data de recepció:
Data de publicació:
Distribution of the alien Tubificid worm Branchiura sowerbyi (Beddard, 1892) in Morocco
The tubificid worm Branchiura sowerbyi Beddard, 1892 is one of the most successful invasive freshwater oligochaetes worldwide. In the Maghreb region, this species was known only from two localities in Morocco and from one locality in Libya. This paper presents novel information about the current distribution and presence of this invasive species in Morocco, and provides guidance on further areas of research regarding invasive oligochaetes in North African.
Key words: Alien species, Red worm, Progressive dispersal, New records, North Africa
Distribución del gusano tubifícido Branchiura sowerbyi (Beddard, 1892) en Marruecos
El gusano tubifícido Branchiura sowerbyi Beddard, 1892 es uno de los oligoquetos de agua dulce invasores con mayor éxito en todo el mundo. En la región del Magreb, esta especie se conocía únicamente en dos localidades de Marruecos y una de Libia. Este artículo ofrece nueva información sobre la distribución actual y la presencia de esta especie invasora en Marruecos y orienta sobre nuevas áreas de investigación de los oligoquetos invasores norteafricanos.
Palabras clave: Especie exótica, Lombriz acuática, Dispersión progresiva, Nuevos registros, Norte de África
Distribució del cuc tubifícid Branchiura sowerbyi (Beddard, 1892) al Marroc
El cuc tubifícid Branchiura sowerbyi Beddard, 1892 és un dels oligoquets d'aigua dolça invasors amb més èxit arreu del món. A la regió del Magrib, aquesta espècie només era coneguda en dues localitats del Marroc i una de Líbia. Aquest article ofereix nova informació sobre la distribució actual i la presència d'aquesta espècie invasora al Marroc i orienta sobre noves àrees de recerca dels oligoquets invasors nord-africans.
Paraules clau: Espècie exòtica, Cuc d'aigua, Dispersió progressiva, Nous registres, Nord d'Àfrica
Alien species are among the main threats to global biodiversity and are recognized as the second leading cause of extinctions around the world (Njiru et al., 2005; Pimentel et al., 2005). In addition, alien and invasive species can reduce genetic diversity of autochthonous biodiversity and biotic homogenization through a variety of mechanisms and interactions (Canonico et al., 2005; Fenoglio et al., 2016). Freshwater ecosystems are the most invaded and threatened ecosystems worldwide, with proportionally more invaders than terrestrial habitats, in part because of habitat alteration and degradation (Rahel, 2002; Alcaraz et al.,2005). Among invertebrates, exotic and invasive species can belong to various branches and classes. A good example of the success biological invasion in phylum Annelida is the tubificid worm Branchiura sowerbyi Beddard, 1892, which is one of the most successful alien freshwater oligochaetes worldwide.
Branchiura sowerbyi is a large red worm. It is easily identified and can be differentiated from other tubificid species by the presence of gills. It has a pair of gills on each segment in the posterior part of the body; dorsal and ventral chaetae differ, with ventral chaetae simple-pointed to bifid and the dorsal bundles with hairs and bifid chaetae (Liebig et al., 2023). This thermophilic species originates from the Sino-Indian region, but is now found all over the world except for Antarctica, and is currently considered a cosmopolitan species because of human activity (Tobias, 1972; Timm, 1979; Timm and Abarenkov, 2023). Due to its fast dispersal, success in adaptation and mass occurrence in different biotopes, B. sowerbyi could be characterized as an invasive species (Raposeiro et al., 2009; Cebulska and Krodkiewska, 2017).
In North Africa (Maghreb), this species was known from only two localities in Morocco and from one locality in Libya (Martin and Boughrous, 2012 ). Branchiura sowerbyi was observed for the first time in Morocco from Sebou River at Moulay Yacoub Province, Fès-Meknès region (Baroudi, 1985) and later from the N'Fis River below the Lalla Takerkoust Reservoir, Marrakesh-Safi region (Juget and Yacoubi-Khebiza, 1997). It has remained unstudied since these first records. The aim of this paper is to update information about the current distribution of Branchiura sowerbyi in Moroccan waters, to point out its progressive dispersal, and to contribute to knowledge of its ecology in the invaded areas of North Africa.
Material and methods
As part of hydrobiological monitoring, field surveys have been conducted since 2014 in the northern part of Morocco, with a focus on Protected Areas, especially great geographical barriers such as the Middle Atlas Mountains, Sebou and Moulouya River basins. The benthic fauna was collected using a Surber sampler (surface of 20 x 25 cm and 0.4 mm mesh net), and eight samples were taken covering the whole micro-habitats heterogeneity represented within each locality, mainly determined by the type of substrate, macrophyte cover and flow velocity. The samples were stored in 75% ethanol. Conductivity, pH, and dissolved oxygen were measured in situ with a multiparametric measuring device (WTW, Multi-Line P4). The other parameters, i.e. ammonium, nitrates, orthophosphates and biological oxygen demand (BOD5) were measured in the laboratory.
Since its first record in Morocco, Branchiura sowerbyi has quietly spread in the country and it is reported here for the first time in the Moulouya River from a number of localities. In addition, we record it from another locality of the Sebou River basin, from Ain Chkef Park (fig. 1, 2; table 1). The fact that this spread has gone undetected is related to the lack of studies carried out to date on Moroccan oligochaetes.
In the new localities, B. sowerbyi was often found associated with shallow, stagnant, or slowly flowing waters. Table 2 shows the abundance and the physicochemical parameters of the water in each new locality.
Branchiura sowerbyi is recorded for the first time in the Oriental Region of Morocco, in the Za River, a major tributary of the Moulouya River. This area was poorly studied in terms of macroinvertebrate assemblages before 2014. Therefore, the alien worm could either have gone unnoticed for years since its first record in Morocco, or it could be in its early stages of invasion in this hydrographic network. Moreover, the 2020 record at Ain Chkef Park is located very close to the record of 1985; both belong to the Sebou River basin. This recent record adds further evidence to support the long-standing presence of the worms in the Fez-Meknes area. The species was absent in the remaining sampling points (more than 150) situated in various regions of central and northern Morocco where we have been performing hydrobiological monitoring of the aquatic ecosystems since 2014 (e.g., see Mabrouki et al., 2020 ; Taybi et al., 2023 for details on localities). However, it is still possible that the invasive worm could have escaped our captures in some of these localities.
Our work confirms the existence of the alien tubificid B. sowerbyi in Morocco, and therefore, in addition to the leech Helobdella europaea Kutschera 1987, the number of exotic freshwater annelids amounts to two species, and the total number of aquatic alien species with confirmed presence in the continental waters of the country rises to 43 taxa (Mabrouki et al., 2019; Ford et al., 2020; Taybi et al., 2023). The main areas harbouring xenodiversity in Moroccan freshwaters correspond to protected areas such as Ramsar Sites and sites of biological and ecological interests known as SIBE, where almost half of the alien species were introduced intentionally throught fish restocking programs, mainly using ‘Asian carps’ such as the common carp Cyprinus carpio (Linnaeus, 1758), the bighead carp Hypophthalmichthys nobilis (Richardson, 1845) and the silver carp H. molitrix (Valenciennes, 1844). Commercial activities around aquarium and ornamental species appear as the second source favouring colonization by alien freshwater animal species (Mabrouki et al., 2020; Taybi et al., 2023).
The introduction and propagation of B. sowerbyi worldwide is strongly correlated with the transport of exotic plants and fish stocking, accentuated by other human related activities and mechanisms (Paunovic et al., 2005; Georgieva et al., 2012). The introduction of this species in Morocco could be related to transport of ornamental plants, since its first record in the country was in the region of Fez, which has been heavily infested by exotic and aquatic plants (Khabbach et al., 2019; Mabrouki et al., 2023a). It has since spread elsewhere via various mechanisms (e.g., fish for stocking, active movement, and river currents).
Since Morocco represents a contact area between Europe and Africa and a compulsory passage for much of the fauna between the Palaearctic and Afrotropical regions, another hypothesis behind its introduction and dissemination in Morocco is through water fowl (bird excrements or hitchhiking) migrating from areas of Europe already invaded by the species, as is suggested for other exotic species in the country. Such a mechanism is hypothesised for exotics including the North American freshwater limpet Ferrissia californica (Rowell, 1863), the New Zealand Mudsnail Potamopyrgus antipodarum (J. E. Gray, 1843) and the freshwater leech Helobdella europaea Kutschera, 1987 (Mabrouki et al., 2019; Taybi et al., 2021; Mabrouki et al., 2023b).
Branchiura sowerbyi is known for its abilities to adapt to a wide range of environmental conditions. It can live in both natural and entropized environments, in sediments nearly devoid of oxygen (Brinkhurst and Jamieson, 1971). The worm usually lives with its anterior buried in the sediment, while the posterior waves actively in the water layer above the bottom, often in large numbers (Dumnicka, 2016). The species has also been reported as abundant from areas influenced by organic enrichment as a consequence of urban pressures (Gonçalves et al., 2008; Raposeiro et al., 2009). For instance, the alien worm was found in good water conditions in the studied localities (table 2), but this plastic species could be in larger numbers in the polluted parts of Za River, which is one of the most threatened watercourses in the country, due to liquid pollution (Mabrouki et al., 2016; Bensaad et al., 2017; Taybi et al., 2020). Future prospections could reveal other population of this species.
Due to its invasive character, the presence of B. sowerbyi could disturb relations within the native benthic community and consequently influence the entire aquatic ecosystem (Raposeiro et al., 2009). Furthermore, it has been shown that B. sowerbyi is an alternate host for some fish parasites, such as Thelohanellus hovorkai Achmerov, 1960 (Myxosporea, Myxozoa), which can cause reduction of fish abundance (Liyanage et al., 2003; Paunovic et al., 2005). Climate changes and the increase in water temperatures, in addition to the continuous deterioration of freshwater ecosystems in Africa, will put this thermophilic species in a better position against native fauna, favouring its expansion (Verdonschot, 2007; Cebulska and Krodkiewska, 2017). Therefore, detecting and monitoring the expansion of this alien species within the colonized areas and studies improving biological, ecological and phylogenetic knowledge are urgently required.
We are grateful to the Editor and three anonymous reviewers for valuable corrections and comments. Our thanks to Rianna Vlierboom for proofreading the English of this manuscript.
Alcaraz, C., Vila-Gispert, A., García-Berthou, E., 2005. Profiling invasive fish species: the importance of phylogeny and human use. Diversity and Distributions, 11(4): 289-298. DOI: 10.1111/j.1366-9516.2005.00170.x
Baroudi, M., 1985. Contribution à l'étude des oligochètes d'un cours d'eau pollué: systématique, écologie. Mémoire de fin d'études, Université Paul Sabatier, Toulouse.
Bensaad, H., Mabrouki, Y., Taybi, A. F., Chafi, A., 2017. Assessment of wastewater discharges from Taourirt City on the water quality of the Oued Za (Eastern Morocco). Journal of Materials and Environmental Science, 8(7): 2365-2371.
Brinkhurst, R. O., Jamieson, B. G. M., 1971. Aquatic Oligochaeta of the world. Oliver and Boyd, Edinburgh.
Canonico, G. C., Arthington, A., Mccrary, J. K., Thieme, M. L., 2005. The effects of introducing tilapias on native biodiversity. Aquatic Conservation: Marine and Freshwater Ecosystem, 15(5): 463-483. DOI: 10.1002/aqc.699
Cebulska, K., Krodkiewska. M., 2017. A new locality of alien oligochaete species Branchiura sowerbyi in Upper Oder River in Poland. Polish Journal of Ecology, 65: 432-438. DOI: 10.3161/15052249PJE2017.65.4.012
Dumnicka, E., 2016. Alien Naididae species (Annelida: Clitellata) and their role in aquatic habitats in Poland. Biologia, 71: 16-23.
Fenoglio, E., Bonada, N., Guareschi, S., Lopez-Rodriguez, M., Millan, A., 2016. Freshwater ecosystems and aquatic insects: A paradox in biological invasions. Biology Letters, 2(4): 20151075. DOI: 10.1098/rsbl.2015.1075
Ford, M., Brahimi, A., Baikeche, L., Bergner, L., Clavero, M., Doadrio, I., Lopes-Lima, M., Perea, S., Yahyaoui, A., Freyhof, J., 2020. Freshwater fish distribution in the Maghreb, a call to contribute. OSF Preprints 2020. DOI: 10.31219/osf.io/kx4gc
Georgieva, G., Varadinova, E., Uzunov, Y., 2012. Distribution of non-indigenous tubificid worm Branchiura sowerbyi (Beddard, 1892) in Bulgaria. Journal of BioScience and Biotechnology. Special Edition/Online, 105-113.
Gonçalves, V., Raposeiro, P., Costa, A., 2008. Benthic diatoms and macroinvertebrates in the assessment of the ecological status of Azorean streams. Limnetica, 27(2): 317-328. DOI: 10.23818/limn.27.25
Juget, J., Yacoubi-Khebiza, M., 1997. Contribution à l'écologie de l'espèce Astacopsidrilus naceri Giani and Martin, 1995 (Phreodrilidae, Oligochaeta) en provenance des eaux souterrains du Maroc. International Journal of Limnology, 33(3): 149-161.
Khabbach, A., Libiad, M., Ennabili, A., 2019. Invasion increasing risk of Al Jawahir Wadi lentic habitats by Pistia stratiotes L. (North-Central Morocco). Botanica Complutensis 43: 97-10. DOI: 10.5209/bocm.64280
Liebig, J., Larson, J., Fusaro, A., 2023. Branchiura sowerbyi: U. S. Geological Survey, Nonindigenous Aquatic Species Database, Gainesville, FL, and NOAA Great Lakes Aquatic Nonindigenous Species Information System, Ann Arbor, MI, https://nas.er.usgs.gov/queries/greatlakes/FactSheet.aspx?Species_ID=1151 [Accessed on 17 March 2023].
Liyanage, Y., Yokoyama, H., Wakabayashi, H., 2003. Evaluation of a vector-control strategy of haemorrhagic thelohanellosis in carp, caused by Thelohanellus hovorkai (Myxozoa). Diseases of Aquatic Organisms, 55: 31-35. DOI: 10.3354/dao055031
Mabrouki, Y., Ben Ahmed, R., Taybi, A. F., Rueda, J., 2019. Annotated checklist of the leech (Annelida: Hirudinida) species of the Moulouya river basin, Morocco with several new distribution records and an historical overview. African Zoology, 54(4): 199-214. DOI: 10.1080/15627020.2019.1671218
Mabrouki, Y., Taybi, A. F., Bensaad, H., Berrahou, A., 2016. Variabilité spatio-temporelle de la qualité des eaux courantes de l’Oued Za (Maroc Oriental). Journal of Materials and Environmental Science, 7(1): 231-243.
Mabrouki, Y., Taybi, A. F., Bahhou J., Doadrio I., 2020. The first record of the green swordtail Xiphophorus helleri (Miller, 1966)(Poeciliidae) established in the wild from Morocco. Journal of Applied Ichthyology, 36(6): 795-800, DOI: 10.1111/jai.14105
Mabrouki, Y., Taybi, A. F., Vila-Farré M., 2023a. New to Africa: first record of the globally invasive planarian Girardia tigrina (Girard, 1850) in the continent. Bioinvasion Records, 12(1): 257–264. DOI: 10.3391/bir.2023.12.1.21
Mabrouki, Y., Taybi, A. F., Glöer, P. 2023b. The first record of the North American freshwater limpet Ferrissia californica (Mollusca, Gastropoda) in Morocco. Nature Conservation Research, 8(1):108-112. DOI: 10.24189/ncr.2023.004
Martin, P., Boughrous, A. A., 2012. Guide taxonomique des oligochètes dulçaquicoles du Maghreb. Abc taxa 12, https://www.invemar.org.co/redcostera1/invemar/docs/RinconLiterario/2012/mayo/AbcTaxaVol12(2012).pdf [Accessed 17 March 2023].
Njiru, M., Waithaka, E., Muchiri, M., Van Knaap, M., Cowx, I. G., 2005. Exotic introductions to the fishery of Lake Victoria: what are the management options? Lakes and Reservoirs: Research and Management, 10(3): 147-155. DOI: 10.1111/j.1440-1770.2005.00270.x
Paunovic, B., Miljanovic, V., Simic, P., Cakic, V., Djikanovic, D., Jakovcev, T., Stojanovic, B., Veljkovic, A., 2005. Distribution of Non-Indigenous Tubificid Worm Branchiura Sowerbyi (Beddard, 1892) in Serbia, Biotechnology and Biotechnological Equipment, 19(3): 91-97. DOI: 10.1080/13102818.2005.10817234
Pimentel, D., Zuniga, R., Morrison, D., 2005. Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecological Economics 52(3): 273-288. DOI: 10.1016/j.ecolecon.2004.10.002
Rahel, F. J., 2002. Homogenization of freshwater faunas. Annual Review of Ecology and Systematics, 33: 291-315. DOI: 10.1146/annurev.ecolsys.33.010802.150429
Raposeiro, P., Ramos, J., Costa, A., 2009. First record of Branchiura sowerbyi Beddard, 1892 (Oligochaeta: Tubificidae) in Azores. Aquatic Invasions, 4(3): 487-490. DOI: 10.3391/ai.2009.4.3.8
Taybi, A. F., Mabrouki, Y., Berrahou, A., Legssyer, B., 2020. Spatio-temporal typology of the physico-chemical parameters of the Moulouya and its main tributaries. African Journal of Aquatic Sciences. 45(4): 431-441. DOI: 10.2989/16085914.2020.1727832
Taybi, A. F., Mabrouki, Y., Glöer, P., 2021. First record of the New Zealand Mudsnail Potamopyrgus antipodarum (J. E. Gray, 1843) (Tateidae, Mollusca) in Africa. Graellsia, 77(2): e140. DOI: 10.3989/GRAELLSIA.2021.V77.303
Taybi, A. F., Mabrouki, Y., Piscart, C., 2023. Distribution of Freshwater Alien Animal Species in Morocco: Current Knowledge and Management Issues. Diversity, 15(2): 169. DOI:10.3390/d15020169
Timm, T., 1979. Distribution of aquatic oligochaetes. In: Aquatic Oligochaete Biology (R. O. Brinkhurst, D. G. Cook, Eds.). Plenum Press, New York.
Timm, T., Abarenkov, K., 2023. World distribution of the aquatic Oligochaeta. PlutoF. Occurrence dataset https://doi.org/10.15468/2ywn3u [Accessed via GBIF.org on 16 March 2023].
Tobias, W., 1972. Ist der Schlammröhrenwurm Branchiura sowerbyi Beddard 1892 (Oligochaeta: Tubificidae) ein tropischer Einwanderer im Untermain. Natur und Museum, 102(3): 1-3.
Verdonschot, P. F. M., 2007. Spatial and temporal re-distribution of Naididae (tubificoid naidids and naidids s. str., Annelida, Clitellata) in Europe due to climate change: a review based on observational data. Acta Hydrobiologica Sinica, 31: 116-138.