Reports of Pennellidae Burmeister, 1835 (Copepoda: Siphonostomatoida) post metamorphosed females off the coast of southern Africa

Syst Parasitol (2024) 101:32 https://doi.org/10.1007/s11230-024-10157-0 Reports of Pennellidae Burmeister, 1835 (Copepoda: Siphonostomatoida) post metamorphosed females off the coast of southern Africa Makwena M. Sebone · Susan M. Dippenaar Received: 16 November 2023 / Accepted: 26 February 2024 / Published online: 22 April 2024 © The Author(s) 2024 Abstract Seven species belonging to Pennellidae are reported from marine teleosts caught off southern Africa. Additionally, complete re-descriptions are provided for Propeniculus stromatei and Sarcotretes scopeli. Examination of Lernaeenicus gonostomae, deposited in the Iziko South African Museum, indicated that it has the morphological features of Sarcotretes rather than Lernaeenicus and thus should be moved to Sarcotretes i.e. S. gonostomae n. comb. for which a re-description is also provided. Reports of new host records include those of Pennella instructa from Seriola lalandi; Propeniculus stromatei from Rhabdosargus holubi and Pomadasys commersonnii; Sarcotretes scopeli from Nansenia tenera, and Sarcotretes longirostris from Centrolophus niger. New geographical records include those of P. instructa, P. stromatei, S. scopeli, S. longirostris, and L. longiventris off southern Africa. Additionally, an attempt to estimate the evolutionary relationships amongst some genera is done from partial COI sequences deposited in Genbank. M. M. Sebone · S. M. Dippenaar (*) Department of Biodiversity, University of Limpopo, Private Bag X1106, Sovenga 0727, South Africa e-mail: Introduction Pennellidae (Copepoda: Siphonostomatoida) consists of 25 valid genera and 148 species (Walter & Boxshall, 2023; Yumura et al., 2024) symbiotic on marine fish and mammals (Kabata, 1979; Boxshall & Halsey, 2004). Adult metamorphosed female pennellids have large bodies and lose their maxillipeds as mesoparasite adaptations (Boxshall & Halsey, 2004). These metamorphosed females exhibit variable morphology regarding for example, the structure of the cephalothorax (ranging from a simple cephalothorax to development of a cephalic holdfast organ), the trunk (varying from straight trunks to sigmoid trunks), the abdomen (varying from an indistinct abdomen to an abdomen embedded with posterior processes) and the egg strings (varying from straight egg strings to curled egg strings) (Castro-Romero, 2014). This family has a history of intergeneric misidentifications (Kabata, 1979; Castro-Romero, 2014; Walter & Boxshall, 2023). For example, revised species of Peniculus von Nordmann, 1832 were transferred to several genera including Peniculisa Wilson C.B., 1917; Metapeniculus Castro-Romero & Baeza-Kuroki, 1985; Propeniculus Castro-Romero, 2014, and Pseudopeniculus Castro-Romero, 2014 (Wilson, 1917; Castro-Romero & Baeza-Kuroki, 1985; Castro-Romero, 2014). Similarly, several revised species of Lernaeenicus Lesueur, 1824 have already been transferred to different genera (e.g. Sarcotretes Jungersen, 1911; Protosarcotretes Ohtsuka, Lindsay & Izawa, 2018, and Vol.: (0123456789) 13 32 Page 2 of 20 Cardiodectes Wilson, C.B., 1917) due to possession of morphological characters similar to those of other genera (Wilson, 1917; Ohtsuka et al., 2018). To date, only six genera and eight species [Pennella balaenoptera Koren & Danielssen, 1877 from Balaenoptera physalus (Linnaeus); Pennella filosa (Linnaeus, 1758) from Istiompax indica (Cuvier), Mola mola (Linnaeus), Thunnus albacares (Bonnaterre), and Balaenoptera acutorostrata Lacépède; Peniculus fistula fistula von Nordmann, 1832 from Kaperangus microlepis (Norman); Peniculisa furcata (Krøyer, 1863) from Paramonacanthus frenatus (Peters); Peroderma cylindricum Heller, 1865 from Sardinella maderensis (Lowe); Cardiodectes bellottii (Richiardi, 1882) from Lampanyctodes hectoris (Günther) and Gonichthys cocco (Cocco); Lernaeenicus gonostomae Kensley & Grindley, 1973 from Sigmops elongatus (Günther); and Lernaeenicus kabatai Oldewage, 1989 from Carangoides equula (Temminck & Schlegel)] were reported from marine fish and mammals off southern Africa (Barnard, 1955; Perkins, 1983; Dippenaar, 2004). This paper reports on the Pennellidae species collected from marine fish off Southern Africa, with redescriptions of Sarcotretes scopeli Jungersen, 1911 and Propeniculus stromatei (Gnanamuthu, 1951). Notes are provided about the genus Lernaeenicus, with synonymizing and re-description of Lernaeenicus gonostomae Kensley & Grindley, 1973 based on voucher specimens from the Iziko South African museum. Additionally, the phylogenetic relationships between selected Pennellidae genera, using available mitochondrial COI (cytochrome oxidase I) sequences, are investigated. Materials and Methods Specimens collected from fish caught off the southern African coasts, from 1993 to 2019 were preserved in 70% ethanol. For morphological studies, specimens were stained with a mixture of lactic acid and a small amount of lignin pink, then examined using stereoand compound microscopes. Some appendages were dissected and drawings were made with the aid of drawing tubes. All measurements were done using a 2 mm stage micrometer and are given as mean (range) mm. Terminology used in morphological descriptions conforms to that of Kabata (1979). Host species Vol:. (1234567890) 13 Syst Parasitol (2024) 101:32 names were validated using Froese and Pauly (2023). Voucher specimens for Pennella instructa, Sarcotretes scopeli, S. longirostris and Propeniculus stromatei were deposited in the Iziko South African museum. For molecular studies, DNA was extracted from Sarcotretes scopeli. Specimens were cut into small pieces and dried in 1.5 microcentrifuge tubes on a heat block at 56°C for approximately 2 hours. Genomic DNA was extracted using the Zymo Research Quick-DNA™ miniprep plus kit, following the protocol for solid tissues. Polymerase Chain Reaction (PCR) was performed to amplify a fragment of the partial mitochondrial (mtDNA) COI gene with the forward primer mICOIintF (GGWACW GGWTGAACWGTWTAYCCYCC) and reverse primer jgHCO2198 (TAIACYTCIGGRTGICCR AARAAYCA) (Geller et al., 2013; Leray et al., 2013) in the Eppendorf Mastercycler. A 25 µl PCR reaction mixture was prepared for each sample, consisting of 12 µl of OneTaq Quick-Load 2X Master Mix with Standard Buffer, 2 µl of each primer, 1-3 µl of template DNA, and double distilled water to adjust the volume. PCR cycling conditions included 94°C (3 min) initial denaturation, followed by 35 cycles of 94°C (30 sec) denaturation, 50°C (1 min) annealing and 68°C (1 min) extension, followed by 68°C (7 min) extension. Purification of PCR products was performed using exoSAP mix and incubated in Eppendorf Mastercycler at 37°C (15 min) and 80°C (15 min) for enzyme inactivation. Sanger sequencing of the purified PCR products was conducted using the Applied Biosystems™ 3730xl DNA Analyzer. The sequences obtained from the output chromatograms were assembled using CLC genomics workbench 7 (QIAGEN) and carefully examined for (...truncated)