Final scientific report on ITI funded research project

"Changes in Serpulid Diversity along Israel's Mediterranean Coast” #0398312

PIs- A. Chipman and M. Nechama Ben-Eliahu

The Hebrew University of Jerusalem

Data collected in the serpulid diversity project come from three sources; focused collecting of hard substrate material by scuba teams, serpulid tubes scraped from mollusc shells from the Tel Aviv University collection and tubes scraped mostly from molluscs obtained as "fishermen's rejects” from trawling.

The present ITI funding was mainly used to cover the cost of the scuba sampling by Rami Tsadok from Sedot Yam and his team. They collected rocky substrate from depths between ca. 2–20 m. Tsadok's sampling thus far comprises twenty-three samples of substrate rock from 7 locations (Rosh Hanikra, Achziv, Akko, Caesarea, Mikhmoret, Sedot-Yam, Ashdod), collected in April and in June 2012 (see appendix). The rocks were broken down with hammer and chisel to remove encrusted serpulid tubes. This depth range enables comparison with the results of a survey of serpulids carried out in 1990 (Ben-Eliahu & ten Hove, 1992) and points at possible changes in the fauna.

Altogether, the samples comprised inhabited tubes of only seven species, of which 6 were fully identified, with one (or possibly two) minute species set aside for further study. The identified species were: Hydroides diramphus, a biofouling species (1 sample, 20 m); three previously recognized Lessepsian migrants, Hydroides heterocerus (7 samples, 10–30 m), Hydroides minax (6 samples, 4–30 m) and Spirobranchus tetraceros (2 samples, 8 and 10 m). Serpula hartmanae (9 samples from 4–30 m depth) is now also recognized as a Lessepsian migrant species, bringing the total number of Lessepsian migrant serpulids reported from the Israeli coast to eight. Moreover, the observed increase in frequency and number of specimens in these samples corresponds with a trend seen in other Lessepsian migrants (see below) along with a seeming decrease in indigenous species. In the present shallow sampling, only two taxa, Vermiliopsis infundibulum (2 samples, ? and 10 m ) and minute tubes (most likely Salmacina rather than Filograna or Rhodopsis) were indigenous.

The seven species from the present sampling (23 samples) compare with 22 species from 16 samples in the 1990 survey of Ben-Eliahu & ten Hove [1992]), that contained, in addition to the four Lessepsian migrants reported in the present samples, a deeper-going migrant, Hydroides homoceros; both the marine port and ship fouling species,Hydroides diramphus and H. elegans, and nine indigenous taxa, including also Vermiliopsis infundibulum and Salmacinasp. Although the samples are not perfectly comparable (there may have been a better selection of substrates in the 1990 sampling), there appears to be a relative lack of indigenous material in the present shallow samples, pointing at a change in the fauna.

The second source of data was serpulid material scraped from mollusc samples of the Tel Aviv University Zoological Museum, courtesy of H.K. Mienis. This included 34 samples of molluscs from depths between 0–20 m (28 samples ≤15 m depth and 6 from 15–20 m depth), altogether comprising 10 taxa; those mentioned above and Hydroides elegans—a port fouling species (the substrate samples were not from port-habitats) and Pomatoceros lamarckii—a species that inhabits very shallow waters.

In the thirteen still deeper samples from the fisherman's trawls between ca. 30–40 m depth that mainly included molluscs (obtained courtesy of Dr. Dani Golani), the Lessepsian migrant Hydroides homoceros was omnipresent and abundant. Inhabited tubes of other taxa that would have been expected—based on earlier samples as well as presence of empty tubes encrusted on the molluscs—e.g., Serpula vermicularis and Vermiliopsis labiata were not present, while Serpula concharum s. str. and Pomatoceros triqueter were present in only one sample. Empty tubes encrusted on the molluscs—including Serpula concharum s. str., Serpula vermicularis, Vermiliopsis labiata,and Pomatoceros triqueter indicate that the species had settled on the molluscs in the past.

Although the Levant serpulid fauna has been under study for many years, there remain unresolved uncertainties regarding the identity of some of the taxa partly due to the extent of variability in some characters, particularly in the genus Serpula that urgently requires revision, e.g., conclusive determination that the taxon from shallow depths previously designated as Serpula cf. concharum, and Serpula concharum s. str. from deeper waters are more than one taxon (see below). Thus, a major objective of the present research was to obtain fresh specimens of species previously preserved in formalin that will enable genetic analysis, hopefully to resolve some of the taxonomic dilemmas. All the freshly collected material has been stored in 100% ethanol to enable molecular analysis following morphological identification of the specimens, subsamples of which will be sent (in the near future) to Dr. Elena Kupriyanova at the Australian Museum in Sydney, an expert on serpulid molecular analysis (a notoriously difficult group from which to extract DNA [Sun et al. 2012]).

In 1990, Serpula hartmanae was reported by Ben-Eliahu & ten Hove 1992 as Serpula cf. concharum. More recently this species was found in a collection from the Gulf of Elat and within the Suez Canal (Ben-Eliahu & ten Hove 2011). Although H. . Zibrowius and G. Bitar had found a tubeworm species off Lebanon that they attributed to Serpula hartmanae, Ben-Eliahu & ten Hove (2011) were tentative in designating this problematic material in the Mediterranean asS. hartmanae--subject to molecular confirmation. However, the present sampling provided an increased number of specimens for examination and a more confident estimate of variability. Molecular analyses could help resolve this problem.

The apparently increased abundance of Hydroides homoceros and the decrease in indigenous taxa support the impression of a change in the fauna, i.e., increase of Lessepsian migrants and decrease of indigenous taxa in these depths, and support the statistically more robust findings reported by Edelist et al (2012) for fishes, as well as for molluscs (H.K. Mienis, pers. comm.) Although additional alien species have recently been reported in the fish and mollusc fauna, our analysis did not find any new taxa in the serpulid fauna. As noted above, the sporadic nature of the current sampling makes it impossible to arrive at a statistically-significant conclusion for the serpulid tubeworms. Thus, our results are reported as a strong impression. We have no present basis of knowing whether the indigenous taxa that were frequent in 3–40 m may still be found in deeper waters. We have used the ITI funding to pay in advance for additional sampling, therefore we expect more data to be accumulated next spring from collections that will be better informed, based on this year's sampling.

Ben-Eliahu, M.N. & D. Fiege (1996). Serpulid tube-worms (Annelida: Polychaeta) of the Central and Eastern Mediterranean with particular attention to the Levant Basin. Sencken. maritima , 28 (1/3): 1–52.

Ben-Eliahu, M.N. & H.A. ten Hove (2011). Serpulidae (Annelida: Polychaeta) from the Suez Canal—From a Lessepsian Migration Perspective (a Monograph), Zootaxa, 2848: 1–147.

Ben-Eliahu, M.N., ten Hove & H.A., Rilov, G. (2012). Estimating lag-time in population buildups of Lessepsian Migrant serpulid tubeworms. The 21st International Zoological Society Meeting (ICZ), Haifa University, Sept. 2–7, 2012, Zoology in a changing world, abstract of talk, p. 15.

Ben-Eliahu, M.N., ten Hove, H.A., Rilov, G., (2012). Buildups of Lessepsian Migrant serpulid tubeworm populations along the Levant Mediterranean coast—an update. The 49th Meeting of the Zool. Soc. Israel, Dec. 9, 2012, Ben-Gurion University of the Negev, (abstracts of talks, online, p. 9).

Edelist, D., Rilov, G., Golani, D., Carlton, J.T., and Spanier, E. (2012). Restructuring the sea: profound shifts in the world's most invaded marine ecosystem. Diversity and Distributions—a Journal of Conservation Biogeography. Published online 24 Aug. 2012 (DOI: 10.1111/ddi.12002).

Sun, Y., Kupriyanova, E.K., B and Qiu, J.W. (2012) COI barcoding of Hydroides: a road from impossible to difficult. Invertebrate Systematics, 2012, 26, 539–547

Appendix: List of hard substrate samples 1, 2, 3

First set of substrate rock samples, April 2012

RTSAN12- Shell Chama pacifica, wo label,

RTSAN22-MY-0.3, Sedot Yam 0–0.3 m 17.05.2012, collected Chipman Ariel, Filograna-Salmacina or Rhodopsis,seemingly empty –set aside

RTSAN3-C24, Caesarea 32°30'24.84" N; 34°51'58.59 E, 24 m, 8.04.2012, empty serpulid tubes

RTSAN4-C10, Caesarea, 32°29'25.87"N; 34°52'58.31"E, 10 m, 8.04.2012, empty serpulid tubes

RTSAN5-C03, Caesarea, 32°29'26.38"N; 34 °53'09.09"E, 3 m, 8.04.2012, non-diagnosed serpulid fragment

RTSAN6-M10, Mikhmoret, 32°23'31.16"N; 34°51'23.11"E, 10 m, 15.04.2012 Serpula hartmanae (3x), Hydroides minax(1x), Hydroides heterocerus (2x), Vermiliopsis infundibulum (2x), non-determined fragments (discard)

RTSAN7-M04, Mikhmoret, 32°23'38.90" N; 34°51'39.2" E; 4 m, 15.04.2012, minute serpulids not yet studied

RTSAN8-M02, Mikhmoret , 32°24'08.6"N; 34°51'52.45" E, 2 m,15.04.2012, "Mikhmoret beach”, empty serpulid tubes

RTSAN10-RH10, Rosh Hanikrah, 33°04'28.52"N; 35°05'35.80"E; 10 m, 22.04.2012, empty serpulid tubes,

RTSAN11-RH04, Rosh Hanikrah, 33°04'04.34N; 35°06'07.42" E; 4 m, 22.04.2012, empty serpulid tubes,

RTSAN12-AC18, Achziv 33°02'48.52" N; 35°04'58.60"E, 18 m, 2.06.2012, Serpula hartmanae (1 x), Hydroides heterocerus (1 x), several different empty tubes

RTSAN ?qq4, --Sample without label-- SWL-3, Hydroides minax.

Can sample be RTSAN 9 or 13 or 14?

Second set of substrate rock samples, June 2012

RTSAN15-RH18, Rosh Hanikra, 33°03' 57.5" N; 35°05' 33.85" E, 18 m, 22.06.2012, Serpula hartmanae (1 x), Hydroides heterocerus (1 x), several different empty tubes including V. labiata tube, crumbly rocks

RTSAN16-AC20, Akhziv, 33°02' 37.4" N; 35°04'47.3" E, 20 m, 22.06.2012, Serpula hartmanae (5 x), Hydroides diramphus (1 x), Hydroides heterocerus (1 x), minute non-determind2,

RTSAN ?17-AC10, ?Akhziv, 33°02' 35.38" N; 35°04'59.67" E, 10 m, 22.06.2012, (reconstructed sample data), Serpula hartmanae (2 x), Hydroides heterocerus (1 x), Spirobranchus tetraceros (6 x), fragment2 reconstructed sample label, presumably Akhziv sample, crumbly coralligenous algae

RTSAN19-Ak08, Akko, 32°55' 39.51" N; 35°02' 54. "E, 08 m, 24.06.2012, Hydroides minax (1 x), Spirobranchus tetraceros (6 x), fragment n.d.

RTSAN20-As01, Ashdod 1, 31°46' 55.2" N; 34°35'08.1" E, 30 m, 20.06.2012, Serpula hartmanae |(4x), Hydroides heterocerus (1 x), Hydroides minax (1 x), empty tube of Vermiliopsis labiata

RTSAN24-SY20, Sedot Yam, – , 10 m, 18.06.2012, Hydroides minax (1),

RTSAN25-SY20, Sedot Yam, – , 04 m, 18.06.2012, Serpula hartmanae (2 x), Hydroides minax (2 x),

RTSAN-?qq1-- sample information missing, Substrate like RTSAN 16 so? Location presumably Akhziv, Serpula hartmanae (6 x), Salmacina filograna2,

RTSAN-?qq2-- sample information missing, Substrate like RTSAN 16 so? Location presumably Akhziv, Serpula hartmanae (1 x), Hydroides heterocerus (4x),Vermiliopsis infundibulum (2), empty Serpula hartmanae and Vermiliopsis labiata tubes,

1Samples of this ITI project collected by Rami Tsadok, Sedot Yam, code-labelled RTSAN

(= Rami Tsadok, Ariel Chipman & Nechama Ben-Eliahu).

2Serpulid to be further studied.

3Sample label lacking. (Several of the samples did not contain serpulid material, .five samples contained only empty tubes, for three of samples the corresponding data was lacking.),.