Cryptic invasion of a parasitic copepod: Compromised identification when morphologically similar invaders co-occur in invaded ecosystems

Abstract

Despite their frequent occurrence and strong impacts on native biota, biological invasions can long remain undetected. One reason for this is that an invasive species can be morphologically similar to either native species or introduced species previously established in the same region, and thus be subject to mistaken identification. One recent case involves congeneric invasive parasites, copepods that now infect bivalve hosts along European Atlantic coasts, after having been introduced independently first from the Mediterranean Sea (Mytilicola intestinalis Steuer, 1902) and later from Japan (Mytilicola orientalis Mori, 1935). At least one report on M. intestinalis may have actually concerned M. orientalis, and M. orientalis thus qualifies as a “cryptic invader”. Because these two parasitic copepods are morphologically similar, knowledge about their distribution, impact and interactions depends crucially on reliable species identification. In this study, we evaluated the reliability of morphological identification of these two species in parts of their invasive range in Europe (Dutch Delta and Wadden Sea) in comparison with molecular methods of well-established accuracy based on COI gene sequences and ITS1 restriction fragment length polymorphism. Based on seven easily measured or scored macro-morphological variables that were recorded for 182 individual copepods isolated from blue mussels (Mytilus edulis Linnaeus, 1758), principal component analysis showed two relatively distinct but overlapping morphological species groups for females, but no clear separation in males. Discriminant function analysis showed that the females can be discriminated reasonably well based on some of the morphological characteristics (identification error rate of 7%) while males cannot (error rate of 25%). The direction of the dorsolateral thoracic protuberances was identified as the most important trait for species discrimination, but among the morphological features checked, none could flawlessly discriminate between both species. We recommend the use of molecular techniques in future studies of invasive Mytilicola to reliably discriminate between the species. The morphological similarity of these two invaders suggests a more general problem of cryptic invasions and compromised identification of parasites in invaded ecosystems. This problem should be borne in mind whenever invasive parasites are investigated.

How invasive oysters can affect parasite infection patterns in native mussels on a large spatial scale

“…The identification of adult Mytilicola was based on descriptions of Steuer (1902), Mori (1935), Ho and Kim (1992), and Elsner et al (2011). However, as morphological species identification is not entirely reliable when both Mytilicola species have overlapping host ranges and distributions (Elsner et al 2011;Goedknegt et al 2017;Goedknegt et al 2018b), a subset of Mytilicola specimens originating from blue mussels were also molecularly identified to species level to support and improve the morphological identification (see Online Resource 2).…”

Global invasion genetics of two parasitic copepods infecting marine bivalves

“…A possible caveat in the literature survey is that M . orientalis’ invasion in Europe has been cryptic because of difficulties with reliable species identification 69 . In the literature survey, we used the identification presented by the authors, but that may be incorrect when studies are based on morphology, as the distinguishing characteristics for M .…”

“…A 534 base pair (bp) fragment of the mitochondrial cytochrome- c -oxidase I region (COI) was amplified using the primer pair MOICOIf and MOICOIr for M . intestinalis 69 and a newly developed primer pair for M . orientalis (MoriCOI50f: 5′-TTG ATC GGG CTT AAT TGG-3′ and MoriCOI50r: 5′-GAT CGG TTA ARA GCA TGG T-3′).…”

“…intestinalis , polymerase chain reaction (PCR) and Sanger sequencing using both forward and reverse primers were performed according to Goedknegt et al . 69 at Baseclear B.V. (Leiden, Netherlands). For M .…”

Using DNA barcoding to identify host-parasite interactions between cryptic species of goby (Coryphopterus: Gobiidae, Perciformes) and parasitic copepods (Pharodes tortugensis: Chondracanthidae, Cyclopoida)

“…For example, attempts to control a pathogenic parasite may be thwarted if an unrecognized host species serves as a reservoir for the parasite even if it is extinct in recognized hosts (Besansky 1999;Haydon 2002). In addition, the impacts of invasive parasites can escape detection if invaders are mistaken for native species or other invaders that are morphologically similar (Goedknegt et al 2018). Lastly, tak-TAble 1.…”