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First record of the cryptogenic amphipod Ampithoe bizseli (Ampithoidae) in the European Atlantic waters

Published online by Cambridge University Press:  30 January 2025

Daniele Arduini  and
Emanuele Mancini Open the ORCID record for Emanuele Mancini [Opens in a new window]
Daniele Arduini
Affiliation:
Department of Biological and Environmental Sciences and Technologies, DiSTeBA, University of Salento, 73100 Lecce, Italy
Emanuele Mancini*
Affiliation:
Department of Biological and Environmental Sciences and Technologies, DiSTeBA, University of Salento, 73100 Lecce, Italy National Biodiversity Future Center (NBFC), 90100 Palermo, Italy Ente Fauna Marina Mediterranean, Scientific Organization for Research and Conservation of Marine Biodiversity, Avola, Italy
*
Corresponding author: Emanuele Mancini; Email: emanuele.mancini@unisalento.it
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Abstract

The amphipod Ampithoe bizseli Özaydinli and Coleman, 2012 is a cryptogenic species that was recently described in Turkey. Although to date it has only been recorded in the Mediterranean Basin, it is potentially native to the Red Sea and Indian Ocean. During a macrozoobenthos sampling campaign carried out in the Canary Islands in 2023, 25 individuals of A. bizseli were found in association with some fish farm facilities. This work represents the first report of this amphipod in European Atlantic waters and increases knowledge of the ecology of this non-indigenous species.

Keywords

Canary IslandscrustaceaEricthonius didymusfish farmsnon-indigenous
Type
Marine Record
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 105 , 2025 , e6
Copyright
Copyright © The Author(s), 2025. Published by Cambridge University Press on behalf of Marine Biological Association of the United Kingdom

Introduction

The family Ampithoidae Boeck, Reference Boeck1871 is highly diverse and represents the most specious family of algae-dwellers herbivorous amphipods (Myers and Lowry, Reference Myers and Lowry2003; Poore et al., Reference Poore, Hill and Sotka2008; Hughes and Peart, Reference Hughes and Peart2013; Sotka et al., Reference Sotka, Bell, Hughes, Lowry and Poore2017). Ampithoids are cosmopolitan and are generally found in a wide range of vegetated shallow water marine environments (Poore and Lowry, Reference Poore and Lowry1997; Poore et al., Reference Poore, Hill and Sotka2008; Peart and Ahyong, Reference Peart and Ahyong2016). These peracarids can be locally very abundant and exert a significant influence on the structure of the host algal community (Duffy and Hay, Reference Duffy and Hay2000; Poore et al., Reference Poore, Hill and Sotka2008; Peart and Ahyong, Reference Peart and Ahyong2016). This taxon comprises 16 genera and 246 species (Horton et al., Reference Horton, Lowry, De Broyer, Bellan-Santini, Copilas-Ciocianu, Corbari, Costello, Daneliya, Dauvin, Fišer, Gasca, Grabowski, Guerra-García, Hendrycks, Hughes, Jaume, Jazdzewski, Kim, King, Krapp-Schickel, LeCroy, Lörz, Mamos, Senna, Serejo, Souza-Filho, Tandberg, Thomas, Thurston, Vader, Väinölä, Valls Domedel, Vonk, White and Zeidler2024), all characterized by an entire and dorsoventrally thickened telson and the outer ramus of uropod 3 armed with 1 or 2 recurved and robust apical setae (Barnard and Karaman, Reference Barnard and Karaman1991; Myers and Lowry, Reference Myers and Lowry2003; Sotka et al., Reference Sotka, Bell, Hughes, Lowry and Poore2017). Ampithoe Leach, 1814 is the most speciose genus belonging to the family Ampithoidae and these amphipods are associated with a very high diversity of habitats such as soft and hard substrates, marine phanerogams, algae, corals and anthropogenic substrates (Poore and Lowry, Reference Poore and Lowry1997; Peart, Reference Peart2007). Species belonging to this genus can be identified by certain common morphological characters such as: entire and thickened telson which can be armed with enlarged hooks or little knobs, striate setae on the distal margin of the propods and an atypical lower lip (Peart, Reference Peart2007; Peart and Ahyong, Reference Peart and Ahyong2016; Iwasa-Arai et al., Reference Iwasa-Arai, Siqueira, Sobral-Souza, Leite and Andrade2024). Nine species of this genus have been reported in European waters (Costello et al., Reference Costello, Emblow and White2001) and among them Ampithoe bizseli Özaydinli and Coleman, Reference Özaydinli and Coleman2012 was recently described in the Mediterranean basin (Özaydinli and Coleman, Reference Özaydinli and Coleman2012). To date, only two species of Ampithoe are recorded from the Canary Islands: Ampithoe ramondi Audouin, Reference Audouin1826 and Ampithoe rubricata (Montagu, Reference Montagu1808) (Krapp-Schikel and Ruffo, Reference Krapp-Schikel and Ruffo1990; Navarro-Mayoral et al., Reference Navarro-Mayoral, Fernandez-Gonzalez, Otero-Ferrer and Tuya2020; Ugalde-Pozo and Riera, Reference Ugalde-Pozo and Riera2024). Ampithoe bizseli Özaydinli and Coleman, Reference Özaydinli and Coleman2012 was described from Izmir Bay and until now was reported only for Turkey, Tanzania and Cyprus (Özaydinli and Coleman, Reference Özaydinli and Coleman2012; Ulman et al., Reference Ulman, Ferrario, Occhpinti-Ambrogi, Arvanitidis, Bandi, Bertolino, Bogi, Chatzigeorgiou, Çiçek, Deidun, Ramos-Esplá, Koçak Lorenti, Martinez-Laiz, Merlo, Princisgh, Scribano and Marchini2017). Although this species has been reported from the Mediterranean Sea, some authors considered A. bizseli cryptogenic (Marchini and Cardeccia, Reference Marchini and Cardeccia2017) and potentially native to the Red Sea and Indian Ocean (Ulman et al., Reference Ulman, Ferrario, Occhpinti-Ambrogi, Arvanitidis, Bandi, Bertolino, Bogi, Chatzigeorgiou, Çiçek, Deidun, Ramos-Esplá, Koçak Lorenti, Martinez-Laiz, Merlo, Princisgh, Scribano and Marchini2017; Bilecenoğlu and Çınar, Reference Bilecenoğlu and Çınar2021). In this work, for the first time, we report A. bizseli in the European Atlantic water and provide new information on the ecology and distribution of this species. Finally, this manuscript presents a dichotomous key and a descriptive table that facilitates the accurate identification of the three Ampithoe species that inhabit the waters of the Canary Islands.

Materials and methods

During a sampling campaign conducted on 10th October 2023 in an aquaculture facility located near the marinas of Los Cristianos, Island of Tenerife (Canaries Islands, Spain, Eastern Atlantic Ocean) (28.0333°N, 16.7124°W) (Figure 1), 25 individuals of A. bizseli were sampled from artificial hard substrates. Specifically, the specimens were found in association with fouling assemblages colonizing fish cages at a depth of approximately 0.5 m. The macrozoobenthos samples were collected using a 20 × 20 cm2 hand-operated net (0.5 mm mesh size), provided with a stainless-steel blade on the board. All the collected materials were fixed in 85% ethanol and preserved in 75% ethanol. In the laboratory the collected material was sorted and the macrozoobenthic species were identified under a stereomicroscope (Olympus SZX-16) and optical microscope (Leica DM2000LED). All the specimens of A. bizseli (Figure 2A) were identified following Özaydinli and Coleman (Reference Özaydinli and Coleman2012) and were also achieved through direct comparison with some individuals of A. ramondi. All the individuals are deposited in the marine invertebrate collection of the Museum of Marine Biology ‘Pietro Parenzan’ of the University of Salento (Porto Cesareo, Italy), collection code: CA-CAN1123-AB01.

Figure 1. Map of study area.

Figure 2. Male individual of Ampithoe bizseli, diagnostic characters. (A) Whole specimen; (B) gnathopod 2; (C) ischium of gnathopod 2, the red arrow indicates the circular lobe; (D) gnathopod 1; (E) ischium of gnathopod 1, the red arrow indicates the anteroventrally directed lobe; (F) maxilliped palp.

The original descriptions of the species previously recorded in the Canary Islands, together with the subsequent manuscripts, formed the basis for the development of the key and Table 1: Sars (Reference Sars1890); Ruffo (Reference Ruffo1982); Barrett (Reference Barrett1966); Lincoln (Reference Lincoln1979); Uryupova (Reference Uryupova2005).

Table 1. Distinctive diagnostic characteristics, distribution, type locality and habitat and of the three species of Ampithoe species recorded in Canary waters

Results

All sampled and analysed individuals of the genus Ampithoe, representing by 16 males and 9 females, were found to be A. bizseli, their total length was between 10.5 and 7 mm. The distinctive morphological characters of the males analysed corresponded with those described by Özaydinli and Coleman (Reference Özaydinli and Coleman2012). These authors pointed out that the species resembles A. ramondi and therefore we performed a direct comparison between the two species to validate our identifications. Specifically, the diagnostic characteristics to distinguish these two species are: propodus of gnathopod 2 subrectangular with a conspicuous anterodistal lobe and a long and pointed posteromarginal tooth (Figures 2B, 3A); ischium of gnathopod 2 characterized by an anterior margin produced into a large circular lobe (Figures 2C, 3B); shape of gnathopod 1 (Figures 2D, 3C) and margin of its ischium extended into a rather narrow anteroventrally directed lobe (Figures 2E, 3D); third article of maxilliped palp inflated (Figures 2F, 3E).

Figure 3. Drawings of dignostic characters useful for the identification of Ampithoe bizseli: (A) gnathopod 2; (B) ischium of gnathopod 2, the red arrow indicates the circular lobe; (C) gnathopod 1; (D) ischium of gnathopod 1, the red arrow indicates the anteroventrally directed lobe; (E) maxillary palpus.

Furthermore, male individuals of A. bizseli were compared with several descriptions of A. rubricata (Montagu, Reference Montagu1808; Sars, Reference Sars1890; Barrett, Reference Barrett1966; Lincoln, Reference Lincoln1979; Uryupova, Reference Uryupova2005). The diagnostic characters useful for distinguishing the three species of Ampithoe occurring in the Canary Islands are detailed in Table 1.

Finally, we provide a dichotomous key useful for the correct identification of males of the three species of Canary Island Ampithoe.

  1. 1. ♂ Gn 1-2 ischium without distal lobe; Gn2 propodus with weakly concave palmA. rubricata

    ♂ Gn 1-2 ischium with distal lobe; Gn2 propodus with strongly concave palm2

  2. 2. ♂ Gn 2 ischium with anterior margin produced into a rather narrow anteroventrally directed lobe; third article of maxilliped palp subrectangularA. ramondi

    ♂ Gn 2 ischium with anterior margin produced into a large circular lobe that is directed anteriorly; third article of maxilliped palp inflatedA. bizseli

Discussion

Ampithoe bizseli is considered to be a non-indigenous species in the Mediterranean (Marchini and Cardeccia, Reference Marchini and Cardeccia2017; Ulman et al., Reference Ulman, Ferrario, Occhpinti-Ambrogi, Arvanitidis, Bandi, Bertolino, Bogi, Chatzigeorgiou, Çiçek, Deidun, Ramos-Esplá, Koçak Lorenti, Martinez-Laiz, Merlo, Princisgh, Scribano and Marchini2017; Bilecenoğlu and Çınar, Reference Bilecenoğlu and Çınar2021) and, like other species that lack the capacity for wide natural dispersal, this amphipod was probably introduced and spread secondarily by recreational boating through hull fouling (Ulman et al., Reference Ulman, Ferrario, Occhpinti-Ambrogi, Arvanitidis, Bandi, Bertolino, Bogi, Chatzigeorgiou, Çiçek, Deidun, Ramos-Esplá, Koçak Lorenti, Martinez-Laiz, Merlo, Princisgh, Scribano and Marchini2017). Additionally, it is conceivable that the distribution of this species in the Mediterranean and Tanzania has been underestimated, as it has likely been misidentified on numerous occasions as A. ramondi (Özaydinli and Coleman, Reference Özaydinli and Coleman2012; Ulman et al., Reference Ulman, Ferrario, Occhpinti-Ambrogi, Arvanitidis, Bandi, Bertolino, Bogi, Chatzigeorgiou, Çiçek, Deidun, Ramos-Esplá, Koçak Lorenti, Martinez-Laiz, Merlo, Princisgh, Scribano and Marchini2017). Several studies have demonstrated that anthropogenic hard bottoms represent a preferred substrate for the colonization by non-native amphipods (Ros and Guerra-Garcia, Reference Ros and Guerra-García2012; Ros et al., Reference Ros, Guerra-García, González-Macías, Saavedra and Lopez-Fe2013, Reference Ros, Lacerda, Vázquez-Luis, Masunari and Guerra-García2016; Bonifazi et al., Reference Bonifazi, Mancini and Ventura2018; Ulman et al., Reference Ulman, Ferrario, Occhpinti-Ambrogi, Arvanitidis, Bandi, Bertolino, Bogi, Chatzigeorgiou, Çiçek, Deidun, Ramos-Esplá, Koçak Lorenti, Martinez-Laiz, Merlo, Princisgh, Scribano and Marchini2017; Guerra-Garcia et al., Reference Guerra-Garcia, Revanales, Saenz-Arias, Navarro-Barranco, Ruiz-Velasco, Pastor-Montero, Sempere-Valvedrde, Chebaane, Velez-Ruiz, Martinez-Laiz, Santos-Simon, Ferrario, Marchini, Nour, Gouuillieux, Hosie, Gerovasilieu, Carvalho, Balistrieri, Sirchia, Ruvolo, Mancini, Bonifazi, Tempesti, Tiralongo, Ignoto, Fernandez-Gonzalez, Vazquez-Luis, Cabezas and Ros2013). In this context, anthropogenic fouling-rich surfaces facilitate colonization by non-native species, acting as a source of food and providing shelter and protection for many macrozoobenthic invertebrate species due to their structural complexity (Jenkins and Martins, Reference Jenkins and Martins2010; Lezzi et al., Reference Lezzi, Del Pasqua, Pierri and Giangrande2018; Lezzi and Giangrande, Reference Lezzi and Giangrande2018). Furthermore, artificial substrates are regarded as a potential conduit for the dispersal of allochthonous and potentially invasive species, acting as a ‘springboard’ for these organisms (Mineur et al., Reference Mineur, Belsher, Johnson, Maggs and Verlaque2007; Giangrande et al., Reference Giangrande, Arduini, Borghese, Del Pasqua, Lezzi, Petrocelli, Cecere, Longo and Pierri2021). The finding of A. bizseli in association with fish farm facilities leads us to this conclusion, as these conditions have been observed by other authors for other non-indigenous amphipods (Savini et al., Reference Savini, Occhipinti-Ambrogi, Marchini, Tricarico, Gherardi, Olenin and Gollasch2010; Fernandez-Gonzalez and Sanchez-Jerez, Reference Fernandez-Gonzalez and Sanchez-Jerez2014; Fernandez-Leborans et al., Reference Fernandez-Leborans, Fernandez-Gonzalez, Sanchez-Jerez and Roura2016). These anthropogenic structures could be considered an additional vector for the transport and dissemination of this species. In fact, the analysis of the fouling macrozoobenthic community with which our A. bizseli individuals were associated revealed the presence of other non-indigenous amphipods: the stenothoid Stenothoe georgiana Bynum and Fox, Reference Bynum and Fox1977, the ischyrocerid Ericthonius didymus Krapp-Schickel, Reference Krapp-Schickel2013 and the cryptogenic maerid Elasmopus rapax A. Costa, Reference Costa1853. Regarding Ericthonius didymus, this work represents the first report of this species in the area, but it must be highlighted that this report, like the others from the Mediterranean, probably refers to the alien Indo-Pacific species Ericthonius pugnax (Dana, Reference Dana1852) (Ulman et al., Reference Ulman, Ferrario, Occhpinti-Ambrogi, Arvanitidis, Bandi, Bertolino, Bogi, Chatzigeorgiou, Çiçek, Deidun, Ramos-Esplá, Koçak Lorenti, Martinez-Laiz, Merlo, Princisgh, Scribano and Marchini2017). Furthermore, given that A. bizseli has only been observed in the Mediterranean, it is plausible that it reached the Atlantic via the Strait of Gibraltar. Although our study represents the first report of A. bizseli in the Atlantic, further research is required to ascertain whether the species spread into the Atlantic waters via the Strait of Gibraltar or whether this amphipod was already present in the coastal areas of the Canaries. It is possible that A. bizseli had already been present in the coastal waters of these islands for some time but was misidentified as A. ramondi. This work contributes to expanding knowledge on the distribution of this cryptogenic species and represents the first report of A. bizseli in the Atlantic Ocean. Given that A. bizseli is regarded as an invasive species, it is imperative to maintain surveillance of the study area to ascertain whether the species is extending its range into neighbouring regions.

Acknowledgements

We are particularly grateful to Professor Sergio Rossi for his support during sampling operations. We would like to thank the three anonymous reviewers for improving the quality of this manuscript.

Author contributions

D. A. collected and analysed the specimens and wrote the manuscript. E. M. analysed, drew and photographed the specimens at stereo and optical microscope and wrote the manuscript. All authors read and approved the final version of the manuscript.

Financial support

This work is partially funded by the National Recovery and Resilience Plan (NRRP), Mission 4 Component 2 Investment 1.4 – Call for tender No. 3138 of 16 December 2021, rectified by Decree n.3175 of 18 December 2021 of Italian Ministry of University and Research funded by the European Union – Next Generation EU; Project code CN_00000033, Concession Decree No. 1034 of 17 June 2022 adopted by the Italian Ministry of University and Research, CUP D33C22000960007, Project title ‘National Biodiversity Future Center – NBFC’.

Competing interest

None.

Data availability statement

The authors confirm that the data supporting the findings of this study are available within the article [and/or its supplementary materials].

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Figure 1. Map of study area.

Figure 1

Figure 2. Male individual of Ampithoe bizseli, diagnostic characters. (A) Whole specimen; (B) gnathopod 2; (C) ischium of gnathopod 2, the red arrow indicates the circular lobe; (D) gnathopod 1; (E) ischium of gnathopod 1, the red arrow indicates the anteroventrally directed lobe; (F) maxilliped palp.

Figure 2

Table 1. Distinctive diagnostic characteristics, distribution, type locality and habitat and of the three species of Ampithoe species recorded in Canary waters

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Figure 3. Drawings of dignostic characters useful for the identification of Ampithoe bizseli: (A) gnathopod 2; (B) ischium of gnathopod 2, the red arrow indicates the circular lobe; (C) gnathopod 1; (D) ischium of gnathopod 1, the red arrow indicates the anteroventrally directed lobe; (E) maxillary palpus.