The rhizome layer of Posidonia oceanica: an important habitat for Mediterranean brachiopods
Mediterranean brachiopods are elusive organisms to find alive even if the bathymetric range of some species extends to very shallow waters. We here record an abundant population of Joania cordata (Risso, 1826) and Argyrotheca cuneata (Risso, 1826) in the rhizome layer of a Posidonia oceanica (Linné) Delile, 1813 meadow in Plakias, southwestern Crete from 5 to 20 m depth. Altogether, we collected 963 living individuals and 4309 shells by suction sampling; it is the largest collection of living brachiopods in Posidonia meadows ever reported. Although literature records on the occurrence of shallow-water brachiopods in this habitat are few, we claim that Posidonia rhizomes are a particularly suitable infralittoral habitat for these organisms due to their sciaphilous conditions. Suction sampling is an effective technique to collect them and can enable the discovery of many more populations in the Mediterranean Sea.
KeywordsJoania cordata Argyrotheca cuneata Seagrass Suction sampling Crete Eastern Mediterranean Sea
The present-day Mediterranean Sea hosts only 14 species of brachiopods (Logan et al. 2004; Robinson 2017) which prefer habitats with low illumination and are generally reported from coralligenous substrates, coralline algae frameworks typical of the Mediterranean Sea, below 40 m. Some species are known to occur also in shallower waters but only in shaded and protected environments such as caves and beneath boulders (Logan 1979). Shallow-water species are often reported as empty shells from death assemblages whereas findings of living individuals are uncommon and usually limited to a few individuals (e.g. Taddei Ruggiero 1994; Grobe and Lüter 1999; Evangelisti et al. 2011).
We here report an abundant collection of two megathyrid brachiopods, Joania cordata (Risso, 1826) and Argyrotheca cuneata (Risso, 1826), in the rhizome layer of Posidonia oceanica (Linné) Delile, 1813 between 5 and 20 m depth from southwestern Crete. We found hundreds of living individuals and thousands of shells of both species. We claim that direct sampling of this habitat with proper methods, such as suction sampling, can lead to the discovery of similarly abundant populations elsewhere in the Mediterranean Sea.
Material and methods
Samples were sieved with a 1-mm mesh size and sorted under a stereomicroscope in seawater to pick living organisms more easily. The residue was dried and again sorted to pick the empty shells, valves, and overlooked living organisms.
We identified each specimen to the species level on the basis of Logan’s review (Logan 1979), counted the individuals, the empty shells, and the valves (as half shell). Photographs were taken using a Zeiss SteREO Discovery.V20 stereomicroscope at multiple focus levels and stacked with Helicon Focus 6 (Helicon Soft Ltd., Roseau Valley, Dominica).
Quantitative data have been deposited in the OBIS database and the samples in the Natural History Museum in Vienna (inventory numbers NHMW 112930/LM/0201 to NHMW 112930/LM/0350 (Mollusca collection)).
Total and mean abundance per square meter of living brachiopods and empty shells in the rhizome layer of the Posidonia oceanica meadow in Plakias, southwestern Crete
28 ± 33
54 ± 62
11 ± 11
28 ± 32
30 ± 16
127 ± 88
10 ± 8
33 ± 19
41 ± 23
202 ± 156
14 ± 12
57 ± 45
15 ± 5
156 ± 66
12 ± 3
61 ± 21
Joania cordata and Argyrotheca cuneata are two common brachiopods in the Mediterranean Sea and were reported in shallow water also from Greece (Gerovasileiou and Bailly 2016), including Crete (Logan 1979; Brunton 1988; Logan et al. 2002). Their presence in Posidonia oceanica meadows was first reported from death assemblages in southern Italy (Taddei Ruggiero 1985). Joania cordata was then reported alive in Posidonia oceanica rhizomes for the first time on an off-shore reef in the Tyrrhenian Sea: 7 living individuals, along with 97 shells, were collected by suction sampling (Evangelisti et al. 2011). This reef hosted small seagrass patches on a hard substrate covered by extensive coralligenous concretions with similar but distinct molluscan assemblages characterized by the presence of several species typical of deeper sciaphilous environments (Albano and Sabelli 2011, 2012). Although we found a few specimens also in the leaf samples, in the Crete meadow, these brachiopods definitely prefer the rhizomes and their low hydrodynamism and dim light. Moreover, this layer has plenty of small and large objects for the brachiopods to attach such as the rhizome themselves and other plant debris, shells, foraminiferal tests, and bryozoan colonies (Fig. 3). Nonetheless, because the shoot density declined monotonically with depth, the abundance peak at 15-m depth, which is particularly remarkable for Joania cordata, cannot be easily explained by a calmer or darker environment. Megathyrid brachiopods were found in similar sciaphilic and cryptic habitats also in other regions such as the Caribbean (Asgaard and Stentoft 1984), the Red Sea (Zuschin and Mayrhofer 2009), and the Bay of Fundy, eastern Canada (Noble et al. 1976). The habit of most brachiopods to settle in such habitats may have evolved as a response to the increasing occurrence of grazing invertebrates (e.g. gastropods) during the Mesozoic (Witman and Cooper 1983; Tomašových 2008a, b; Radley 2010).
Megathiris detruncata and Novocrania anomala were not found alive. M. detruncata is rare in so shallow waters, its optimum range being 20–160 m (Logan 1979). Still, the presence of shells suggests that also this species can be encountered alive, albeit rarely, in Posidonia meadows. Novocrania anomala does occur in very shallow waters but lives cemented to boulder and shell substrates (Logan 1979). Suitable hard substrates may be rare among the rhizomes and in any case difficult to intercept with our sampling gear.
The absence of previous records of abundant living brachiopods in the rhizome layer may be due to the difficulties in sampling this habitat. Brachiopods are too small to be seen and picked individually. Grabs and other indirect methods do not easily penetrate the matte, and, in any case, they would be extremely damaging for the seagrass meadow. For similar reasons, the collection of pieces of rhizomes to be inspected in the laboratory, similar to the direct or indirect collecting of rocks and coralligenous concretions, is not advisable; moreover, cutting into the dense matte would be extremely laborious and strenuous. Suction sampling offers a practical alternative that enables collecting small organisms effectively with minimal harm to the substrate. It can be operated with a diver tank or a motorized pump (Templado et al. 2010) and enables the collection of large amounts of organisms and species perfectly suiting biodiversity inventory needs (Bouchet et al. 2002; Linnane et al. 2003; Albano et al. 2011; Ringvold et al. 2015; Evans et al. 2018). We think that the lack of appropriate sampling approaches has prevented the discovery of shallow-water brachiopod populations in other Posidonia meadows so far. This habitat is easily accessible and can offer large sample sizes of living individuals and shells for biological and ecological studies (e.g. Grobe and Lüter 1999; Lüter 2001; Evangelisti et al. 2012, 2014).
PGA research in the Eastern Mediterranean is in the framework of the project “Historical ecology of Lessepsian migration” (PI: PGA) funded by the Austrian Science Fund (FWF) P28983-B29. MS’s fieldwork was supported by the Kurzfristige wissenschaftliche Auslandsstipendien of the University of Vienna, the non-profit organization Mare Mundi, and the diving school Dive2gether. We thank Martin Zuschin for his support during the project, Denny Morchner and Nadja Loferer for their help in the field and in the lab, and Emanuela Di Martino for the identification of the bryozoans. We also thank Adam Tomašových and an anonymous reviewer for useful comments on a first version of the manuscript.
Open access funding provided by University of Vienna.
Compliance with ethical standards
The authors declare that they have no conflict of interest.
No animal testing was performed during this study.
Sampling and field studies
No permits were required to conduct our fieldwork. The study is compliant with CBD and Nagoya protocols.
Quantitative data have been deposited in the OBIS database and the samples in the Natural History Museum in Vienna (inventory numbers NHMW 112930/LM/0201 to NHMW 112930/LM/0350 Mollusca collection).
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