Investigating the role of an alien baitworm as a consumer in a protected estuarine bay: the case of Diopatra aciculata (Annelida: Onuphidae) in the Knysna Estuary of South Africa

Thesis (PhD)--Stellenbosch University, 2025.

van Rensburg, H. 2025. Investigating the role of an alien baitworm as a consumer in a protected estuarine bay: The case of Diopatra aciculata (Annelida: Onuphidae) in the Knysna Estuary of South Africa. Unpublished doctoral dissertation. Stellenbosch: Stellenbosch University [online]. Available: https://scholar.sun.ac.za/items/fe5ab424-f687-47c1-a11d-564ab4b885ff

ENGLISH ABSTRACT: The thesis provides an in-depth exploration of the ecological role, diet and potential threats posed by the estuarine moonshine worm, Diopatra aciculata Knox and Cameron, 1971 (Annelida: Onuphidae), within South African estuarine ecosystems. Diopatra aciculata is an invasive tube-building polychaete worm that never completely leaves its semi-permanent tube. Estuarine ecosystems are critical transitional zones that provide essential services such as nurseries for fish, feeding grounds for migratory birds, and overall support for biodiversity and human well-being. However, these ecosystems face significant threats from anthropogenic activities, including habitat destruction, pollution, and the introduction of invasive species such as D. aciculata. As a known ecosystem engineer with an unknown diet, D. aciculata introduces new dynamics into native estuarine environments, likely influencing sediment stability and trophic dynamics. This research aims to understand its trophic role, dietary habits, and potential influence on native communities, thereby addressing concerns about its effects on native biodiversity and ecosystem functionality. The studies conducted used a combination of methods including two different applications of stable isotope analysis (SIA) and DNA metabarcoding of gut contents to explore D. aciculata’s role, influence and connections with native species. By measuring carbon (δ13C) and nitrogen (δ15N) isotopic signatures of various estuarine organisms from three ecologically different sampling sites over four seasons in the Knysna Estuary (Western Cape, South Africa), I determined that D. aciculata is a facultative carnivore, with a relatively distinct niche and high trophic level relative to other macroinvertebrates. By comparing stable isotope signatures of sympatric species in two ecologically similar estuaries, one with and one without D. aciculata populations, I found its presence is associated with a decrease in trophic niche size and level for sympatric community members. This highlights the potentially broad impact D. aciculata may have on a wide range of native species. Utilizing DNA metabarcoding techniques, the thesis explores the dietary profile of D. aciculata across four sampling areas in the Knysna Estuary and the nearby Keurbooms Estuary (~30 km east of Knysna). The findings reveal that D. aciculata exhibits a generalist feeding strategy, with its gut contents containing predominantly arthropods, molluscs, and fish, which reflects the local community composition. Notably, variations in diet across and within different sampling sites underscore the species' adaptability and reliance on available resources within its restricted range of movement. This thesis underscores the importance of understanding the dietary profiles and ecological effects of invasive species like D. aciculata. My results have enhanced our understanding of how invasive consumers can influence local ecosystems. I suggest that D. aciculata derives its main advantage through its facultative carnivorous diet and tube-dwelling lifestyle which allows it to primarily consume highly nutrient- and calorie-dense foods while having the ability to rely on plant-derived food sources if necessary. The findings highlight the necessity for robust local DNA libraries and further research into the ecological roles of invasive species, particularly in sensitive estuarine environments where biodiversity and ecosystem functions are highly susceptible to changes in species composition. This work contributes to the growing body of literature on invasive species of estuarine ecosystems in South Africa.

AFRIKAANSE OPSOMMING: Die tesis verskaf 'n in-diepte verkenning van die ekologiese rol, dieët en potensiële bedreigings wat deur die riviermonding maanskynwurm, Diopatra aciculata Knox and Cameron, 1971 (Annelida: Onuphidae), in Suid-Afrikaanse riviermonding-ekosisteme inhou. Diopatra aciculata is 'n indringer, buisbouende borselwurm wat nooit die semi-permanente buis heeltemal verlaat nie. Riviermonding ekosisteme is kritieke oorgangsones wat noodsaaklike dienste verskaf soos kleutergronde vir visse, voerplekke vir trekvoëls, en algehele ondersteuning vir biodiversiteit en menslike welstand. Hierdie ekosisteme staar egter beduidende bedreigings in die gesig van menslike aktiwiteite, insluitend habitatvernietiging, besoedeling en die bekendstelling van indringerspesies soos D. aciculata. As 'n bekende ekosisteemingenieur met 'n onbekende dieët, bring D. aciculata nuwe dinamika na inheemse riviermondingekosisteme, wat waarskynlik sedimentstabiliteit en trofiese dinamika beïnvloed. Hierdie navorsing het beoog om die trofiese rol, dieetgewoontes en potensiële invloed op inheemse gemeenskappe van D. aciculata te verstaan, om sodoende kommer oor die uitwerking daarvan op inheemse biodiversiteit en ekosisteemfunksionaliteit aan te spreek. Die studies wat uitgevoer is, het 'n kombinasie van metodes gebruik, insluitend twee verskillende toepassings van stabiele-isotoopanalise (SIA) en DNS-meta-streepieskodering van derminhoud om D. aciculata se rol, invloed en verbande met inheemse spesies te ondersoek. Koolstof (δ¹³C) en stikstof (δ¹⁵N) isotopiese handtekeninge van verskeie riviermonding-organismes is versamel van drie steekproef-areas, wat ekologies verskil, oor vier seisoene, in die Knysna-riviermond (Wes-kaap, Suid Afrika). Daarvan kon ek vasstel dat D. aciculata 'n fakultatiewe karnivoor is, met 'n nis wat relatief uniek is en op ‘n hoë trofiese vlak lê relatief tot ander makro-ongewerweldes. Deur stabiele-isotoop verhoudings van gemeenskapslede in twee, ekologies soortgelyke, riviermondings te vergelyk, een met en een sonder D. aciculata-bevolkings, het ek gevind dat die teenwoordigheid daarvan geassosieer word met 'n afname in trofiese nisgrootte en -vlak vir gemeenskapslede. Dit beklemtoon die potensiële breë impak wat D. aciculata op 'n wye reeks inheemse spesies kan hê. Deur gebruik te maak van DNS-meta-strepieskoderingstegnieke, ondersoek die tesis die dieetprofiel van D. aciculata oor vier steekproef-areas in die Knysna- en die nabye Keurbooms- (~30 km oos vanaf Knysna) riviermonde. Die bevindinge toon dat D. aciculata 'n algemene voedingsstrategie toon, met derm-inhoud wat hoofsaaklik geleedpotiges, skulpdiere en visse bevat, wat die plaaslike gemeenskapsamestelling weerspieël. Verskille in dieët oor, en binne, verskillende steekproef-ares onderstreep die spesie se aanpasbaarheid en afhanklikheid van beskikbare hulpbronne binne sy beperkte omvang van beweging. Hierdie tesis beklemtoon die belangrikheid van dieetprofiele en ekologiese effekte van indringerspesies, soos D. aciculata, te bestudeer. My resultate verbeter ons begrip van hoe indringende verbruikers plaaslike ekosisteme kan beïnvloed. Ek vermoed dat D. aciculata sy voordeel verkry deur sy fakultatiewe vleisetende dieët asook die buisbewonende lewenstyl wat dit in staat stel om hoofsaaklik energie- en voedseldigte voedsel te verbruik terwyl dit ook moontlik is om vanaf plantmaeriaal te oorleef indien nodig. Die bevindinge beklemtoon die noodsaaklikheid van voldoende plaaslike DNS-biblioteke en verdere navorsing oor die ekologiese rolle van indringerspesies, veral in sensitiewe riviermondingomgewings waar biodiversiteit en ekosisteemfunksies hoogs vatbaar is vir veranderinge in spesiesamestelling. Hierdie werk dra by tot die groeiende hoeveelheid literatuur oor indringerspesies van estuariene ekosisteme in Suid-Afrika.

Doctoral