Research Article: Living apart-together: Microhabitat differentiation of cryptic nematode species in a saltmarsh habitat

Date Published: September 27, 2018

Publisher: Public Library of Science

Author(s): Rodgee Mae Guden, Anna-Maria Vafeiadou, Nele De Meester, Sofie Derycke, Tom Moens, Nikolaos Lampadariou.


Coexistence of highly similar species is at odds with ecological theory of competition; coexistence, then, requires stabilizing mechanisms such as differences in ecological niche. In the bacterivore nematode Litoditis marina species complex, which occurs associated with macro-algae, four cryptic lineages (Pm I-IV) co-occur in the field along the south-western coast and estuaries of The Netherlands. Here we investigate the temporal and/or spatial niche differentiation in their natural environment using a qPCR-based detection and relative quantification method. We collected different algal species (i.e. two Fucus species and Ulva sp.) and separated algal structures (i.e. receptacula, thalli, non-fertile tips and bladders) at different sampling months and times (i.e. twice per sampling month), to examine differences in microhabitat use between coexisting L. marina species. Results demonstrate that the cryptic species composition varied among different algal species and algal structures, which was also subject to temporal shifts. Pm I dominated on Fucus spp., Pm II showed dominance on Ulva sp., while Pm III overall had the lowest frequencies. Microhabitat partitioning was most pronounced between the two cryptic species which had similar microbiomes (Pm I and Pm II), and less so between the two species which had significantly different microbiomes (Pm I and Pm III), suggesting that species which share the same microhabitats may avoid competition through resource partitioning. The interplay of microhabitat differentiation and temporal dynamics among the cryptic species of L. marina implies that there is a complex interaction between biotic components and abiotic factors which contributes to their coexistence in the field.

Partial Text

Most estimates of biodiversity rely on inventories of morphologically identifiable species. In the past two decades, the prominence of cryptic species, i.e. morphologically (nearly) identical but genetically distinct species, in many taxa has challenged existing estimates of biodiversity [1, 2]. Cryptic diversity is common across phyla and biogeographic regions [3] and may be particularly prominent in marine habitats, where many species rely on chemical signals for mating and for ecological interactions [4–6]. Interspecific differences in these non-visual traits hardly leave a morphological imprint [1]. Multiple cryptic species can also coexist at local scales [7–9], which is at odds with our traditional view of ecological competition theory since strong interspecific competition is expected between species occupying the same ecological niche [10–12]. With neutral dynamics, ecologically similar species are able to coexist for extended periods of time as their relative abundances change through a completely stochastic drift process [13,14]. Nevertheless, species with high phenotypic similarity can also strongly differ in ecologically significant means, for instance in behaviour and physiology or in life history traits, which may lead to utilization of different niches [15,16], suggesting that traditional niche partitioning mechanisms may be enough in at least some communities to promote stable coexistence [17].

Our results indicated that the cryptic species composition of the L. marina complex varied among different algal species and algal structures, patterns which were also subject to temporal shifts. We used the relative abundances of Pm I, Pm II, and Pm III to assess the cryptic species composition on different microhabitats. No Pm IV was found throughout our investigation. A summary of the collected samples indicating the number of replicates for every sampling time and algal species is presented in Table 1.

Owing to the difficulties of distinguishing cryptic species, the use of molecular genetic methods such as real-time quantitative PCR offers a rapid, specific and sensitive approach for detecting and quantifying the cryptic species of Litoditis marina [48]. This requires the use of species-specific primers. The ITS region showed an appropriate level of variation between species while intraspecific differences remain low [19,52]. Moreover, the high variability of the ITS region between nematode species makes it unlikely for more distantly related species to be amplified with the primers [48]. Nevertheless, critical analysis is required to avoid overestimation of the target species, and thus be able to use this technique for field studies. Real-time quantitative PCR may even be extended to encompass nearly assemblage-wide analyses as it allows quantification of multiple specific species within communities [53,54].

Using real-time qPCR, we demonstrate that the cryptic species composition of the Litoditis marina complex on macroalgae varies among different species of macroalgae, but also among different structures of a particular algal species, which indicates that a single macroalga represents a spatially heterogeneous habitat. Different algal species and algal structures may provide different food resources and/or reflect different ranges of environmental conditions, leading to microhabitat partitioning in the L. marina complex. Nevertheless, the cryptic species composition of L. marina on different microhabitats was also subject to temporal shifts. This suggests that both microhabitat differences and temporal dynamics may offer several niches for L. marina, hence providing ample opportunities for co-occurrence of the cryptic species in the field.




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