Abstract
A population of Acrobeloides longiuterus was recovered during a Potato South Africa Project (PSA) in the Free State Province, South Africa. Subsequently, the soil samples were baited with the larvae of darkling beetles or mealworms (Coleoptera: Tenebrionidae) to recover as many specimens as possible for morphologic and molecular studies. This member of the Cephalobidae represents a new geographical record for the Free State Province of South Africa. Acrobeloides longiuterus is distinguished from other species of the maximus group by having one acute process at the primary axil of each lip, a dextral female genital system, vulva situated towards the left side, and spicules featuring a narrow, elongate manubrium and lamina with small dorsal hump. Description, measurements, illustrations, and phylogenetic position based on 28S rDNA are provided. Phylogenetic analysis revealed that South African A. longiuterus differs from A. camberenensis, and both species are considered valid. Additionally, the results indicate that A. camberenensis, A. longiuterus, A. maximus, and A. saeedi, all with a dextral female genital system, form a clade with 1.00 posterior probability. They can be separated from A. bodenheimeri, a species with a sinistral female genital system.
Similar content being viewed by others
Data availability
This material is the authors’ original work, which has not been previously published elsewhere and has no conflict of interest. Three slides of Acrobeloides longiuterus were deposited in the Nematology collection of the Aquaculture Research Unit, University of Limpopo, South Africa. One slide was deposited in the Nematode Collection of the Department of Animal Biology, Plant Biology, and Ecology of the University of Jaén (Spain). Five slides were deposited in the National Collection of Nematodes, Biosystematics, Agricultural Research Council, Plant Health and Protection, Pretoria, South Africa.
References
Abolafia J, Peña-Santiago R (2003) Nematodes of the order Rhabditida from Andalucía Oriental, Spain. The genus acrobeloides (Cobb 1924) Thorne 1937 with description of A. arenicola sp. n. and a key to its species. J Nematode Morphol Sys 5(2):107–130
Abolafia J, Peña-Santiago R (2017) On the identity of Acrobeloides longiuterus (Rashid and Heyns 1990) Siddiqi, De Ley and Khan 1992 (Rhabditida: Cephalobidae). Nematology 19:817–820. https://doi.org/10.1163/15685411-00003088
Abolafia J, Divsalar N, Panahi H, Shokoohi E (2014) Description of paracrobeles eserticola sp. n. and nothacrobeles hebetocaudatus sp. n. (Nematoda: Rhabditida: Cephalobidae) from Iran and the phylogenetic relationships of these two species. Zootaxa 3827:1–19. https://doi.org/10.1146/zootaxa.3827.1.1
Addinsoft (2007) XLSTAT Analyse de données et statistique avec MS Excel. Addinsoft, NY, USA
Amirzadi N, Shokoohi E, Eskandari A, Abolafia J (2012) Description of acrolobus longigubernaculum sp. n. (Nematoda, Rhabditida, Cephalobidae) from Iran, the second species of the genus. Zootaxa 3407:61–68. https://doi.org/10.11646/zootaxa.3407.1.5
Bandelt H, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16(1):37–48. https://doi.org/10.1093/oxfordjournals.molbev.a026036
Darriba D, Taboada GL, Doallo R, Posada D (2012) Jmodeltest 2: more models, new heuristics and parallel computing. Nat Methods 9:772. https://doi.org/10.1038/nmeth.2109
De Grisse A (1969) Redescription ou modifications de quelques techniques utililisées dans l’étude des nématodes phytoparasitaires. Mededelingen Van De Rijksfaculteit Landbouwetenschappen Gent 34:351–369
De Man JG (1881) Über einige neue oder noch unvollständig bekannte Arten von frei in der reinen Erde lebenden Nematoden (1. Supplement zu den Aufsatz auf S. 1 dieses Bandes). Tijdschr Ned Dierkd Ver V 5:138–143
De Ley P, Geraert E, Coomans A (1990) Seven cephalobids from senegal (Nematoda: Rhabditida). J African Zool 104:287–304
De Ley P, Van de Velde MC, Mounport D, Baujard P, Coomans A (1995) Ultrastructure of the stoma in cephalobidae, panagrolaimidae and rhabditidae, with a proposal for a revised stoma terminology in rhabditida (Nematoda). Nematologica 41:153–182. https://doi.org/10.1163/003925995X00143
De Ley P, Félix MA, Frisse LM, Nadler SA, Sternberg PW, Thomas WK (1999) Molecular and morphological characterisation of two reproductively isolated species with mirror-image anatomy (Nematoda: Cephalobidae). Nematology 1:591–612. https://doi.org/10.1163/1568541995
Filipjev IN (1934) The classification of the free- living nematodes and their relation to the parasitic nematodes. Smithson Misc Collect 89:1–63
Guindon S, Gascuel O (2009) A simple, fast and accurate algorithm to estimate large phylogenies by maximum likelihood. System Biol 52:696–704. https://doi.org/10.1080/10635150390235520
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98. https://doi.org/10.1021/bk-1999-0734.ch008
Holovachov O, Boström S, Nadler SA, De Ley P (2009) Systematics and phylogenetic position of the genus Tricirronema Siddiqi, 1993 (Cephalobomorpha). J Nematode Morphol System 12:133–143
Kim T, Kim J, Park JK (2017) Acrobeloides varius sp. n. (Rhabditida: Cephalobidae) from South Korea. Nematology 19:489–496. https://doi.org/10.1163/15685411-00003064
Mehdizadeh S, Shokoohi E, Abolafia J (2013) Morphology, molecular characterization and systematic position of some known species of cephalobids (Rhabditida, Cephalobidae) from Iran based on sequences of 18S rDNA. J Nematode Morphol System 16(2):143–160
Nadler SA, De Ley P, Mundo-Ocampo M, Smythe AB, Stock SP, Bumbarger D, Adams BJ, De Ley IT, Holovachov O, Baldwin JG (2006) Phylogeny of Cephalobina (Nematoda): Molecular evidence for recurrent evolution of probolae and incongruence with traditional classifications. Mol Phylogenet Evol 40:696–711. https://doi.org/10.1016/j.ympev.2006.04.005
Rana A, Bhat AH, Bhargava S, Chaubey AK, Abolafia J (2020) Morphological and molecular characterization of Acrobeloides saeedi Siddiqi, De Ley and Khan, 1992 (Rhabditida, Cephalobidae) from India and comments on its status. J Nematol 52:1–21. https://doi.org/10.21307/jofnem-2020-027
Rashid F, Heyns J (1990) Chiloplacus and Macrolaimellus species from South West Africa/Namibia (Nematoda: Cephalobidae). Phytophylactica 22:189–199
Ronquist F, Huelsenbeck J (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574. https://doi.org/10.1093/bioinformatics/btg180
Shokoohi E (2021) Morphological and molecular characterisation of Boleodorus volutus Lima and Siddiqi, 1963 from South Africa with the first SEM observations of the species. Russ J Nematol 29(2):101–109. https://doi.org/10.24412/0869-6918-2021-2-101-109
Shokoohi E, Abolafia J (2011) New data and SEM observation of six known species of the super family Rhabditoidea Örley 1880 (Rhabditida) from Tehran province (Iran). J Nematode Morphol System 14(1):39–54
Shokoohi E, Abolafía J (2012) Nematodes of the order Rhabditidafrom Tehran Province Iran. The genus Pseudacrobeles Steiner, 1938 with description of Pseudacrobeles (Pseudacrobeles) iranicus sp. nov. Ann Zool 62:331–340. https://doi.org/10.3161/000345412X652873
Shokoohi E, Abolafia J (2019) Soil and freshwater rhabditid nematodes (Nematoda, Rhabditida) from Iran: A compendium. UJA editorial publishing, University of Jaen, Spain
Shokoohi E, Abolafía J, Kheiri A, Zad J (2008) Nematodes of order Rhabditida from Tehran province (Iran). Some known species of the family Cephalobidae. J Nematode Morphol System 11:67–85
Siddiqi MR, De Ley P, Khan HA (1992) Acrobeloides saeedi sp. n. from Pakistan and redescription of A. bodenheimeri (Steiner) and Placodira lobata Thorne (Nematoda: Cephalobidae). Afro-Asian J Nematol 2:5–16
Straube D, Juen A (2013) Storage and shipping of tissue samples for DNA analyses: a case study on earthworms. Eur J Soil Biol 57:13–18. https://doi.org/10.1016/j.ejsobi.2013.04.001
Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acid Res 22:4673–4680
Thorne G (1925) The genus Acrobeles von Linstow, 1887. Trans Am Microsc Soc 44:171–210
Thorne G (1937) A revision of the nematode family cephalobidae Chitwood and Chitwood, 1934. Proc Helminth Soc Wash 4:1–16
Van Megen H, Van Den Elsen S, Holterman M, Karssen G, Mooyman P, Bongers T, Holovachov O, Bakker J, Helder J (2009) A phylogenetic tree of nematodes based on about 1200 full-length small subunit ribosomal DNA sequences. Nematology 11:927–950. https://doi.org/10.1163/156854109X456862
Acknowledgements
The authors thank the financial support received for the Research Support Plans “PAIUJA 2019/2020: EI_RNM02_2019” and “POAIUJA 2021/2022: EI_RNM02_2021” of the University of Jaén, Spain. SEM pictures were obtained with the assistance of technical staff (Amparo Martínez-Morales) and equipment of “Centro de Instrumentación Científico-Técnica (CICT)” from the University of Jaén. Thanks are also due to Potato South Africa (PSA) for the sampling in the Eastern Free State potato production area in South Africa through the research project, “The succession of nematodes in a Free State potato rotation”. Furthermore, the authors acknowledge Dr. Amini (University of Limpopo; Aquaculture Research Unit) for the statistical analysis.
Funding
This study was financially supported by the University of Jaén (Spain) for the SEM photographs. Potato SA also supports the project.
Author information
Authors and Affiliations
Contributions
AS and MM collected the samples. ES, AS, and JA identified the species, and analysed the data, wrote and revised the manuscript. JA taken LM and SEM of the species. ES conducted the statistical analysis, and ES and NM revised the statistical analysis. All authors revised the manuscript and contributed to the final draft of the manuscript.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
Conflict of interest
The authors declare that they have no conflicts of interest.
Ethical approval
The paper reflects the authors’ own research and analysis in a truthful and complete manner.
Consent to participate
All authors have been personally involved in substantive work leading to the manuscript and contributed to preparing the final draft of the manuscript.
Consent for publication
The manuscript has not been published in whole or in part elsewhere and is not currently being considered for publication in another journal.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Shokoohi, E., Swart, A., Marais, M. et al. Characterization of Acrobeloides longiuterus (Rashid & Heyns, 1990) Siddiqi, De Ley & Khan, 1992 (Rhabditida: Cephalobidae) from South Africa including the SEM study of the species. Zoomorphology 142, 13–25 (2023). https://doi.org/10.1007/s00435-022-00583-3
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00435-022-00583-3