Marine Biodiversity Records, page 1 of 7. # Marine Biological Association of the United Kingdom, 2012 doi:10.1017/S1755267212000437; Vol. 5; e64; 2012 Published online Epibiota of the spider Schizophrys dahlak (Brachyura: ) from the Suez Canal with special reference to epizoic diatoms fedekar f. madkour1, wafaa s. sallam2 and mary k. wicksten3 1Department of Marine Science, Faculty of Science, Port Said University, Port Said, Egypt, 2Department of Marine Science, Faculty of Science, Suez Canal University, 41522, Ismailia, Egypt, 3Department of Biology, Texas A&M University, College Station, TX 77843-3257, USA

This study aims to describe the epibiota of the spider crab, Schizophrys dahlak with special reference to epizoic diatoms. Specimens were collected from the Suez Canal between autumn 2008 and summer 2009. Macro-epibionts consisted of the tube worm elegans, the barnacles Balanus amphitrite and B. eburneus, the bivalve Brachidontes variabilis and the urochordate Styela plicata. Total coverage of macro-epibionts was greater on females’ carapaces than those of males with apparent seasonal variations. The highest coverage was noticed in spring and winter for both males and females. Sixty-five diatoms taxa were recorded as epibionts belonging to 25 genera. The maximal total averages of cell count were observed during summer and spring with the highest average of 10.9 and 4.4 × 103 cells dm22 for males and females, respect- ively. A single diatom taxon, Fragilaria intermedia, comprising 73.5% of all epizoic diatoms, was the most dominant species during spring, whereas Amphora coffeaeformis and Cocconeis placentula were the dominants during summer. The masking behaviour of S. dahlak was discussed in terms of the significant role of epizoic diatoms.

Keywords: epizoic diatoms, epibiota, spider crab, Schizophrys dahlak, Suez Canal

Submitted 25 April 2012; accepted 28 April 2012

INTRODUCTION (Holmes, 1985) but there is no information on such growth in . In all shallow environments, space is often a limiting resource The commencement of larval settlement and metamorpho- in densely populated epibenthic communities, so hard living sis of some epibionts are possibly triggered by physical and substrates of benthic plants and become important biological stimuli. Several studies have suggested that the for epibiosis (Jackson, 1977). Crabs belonging to the super- larval substratum choice for attachment is influenced by the family Majoidea, commonly called spider crabs, are slow bio-film on the substrate, which plays an important role in moving, non-burrowing, slow growing animals with a long mediating settlement and metamorphosis (Rodriguez et al., life span (Hartnoll, 1993). They act as substrata for commu- 1993; Maki, 1999; Zhao & Qian, 2002). The bio-film is a nities of small marine organisms, carrying a variety of epi- complex network of microorganisms (bacteria, diatoms, pro- bionts on their carapaces including diatoms, green algae, tozoa and fungi) and their extracellular polymeric substances coelenterates, flatworms, mussels, oysters, , barnacles, (Wahl, 1989). Diatoms are among the earliest eukaryotic colo- tunicates, bryozoans, isopods, amphipods, gastropods, pelecy- nizers of submerged surfaces and one of the most conspicuous pods and (McLay, 1983; Sato & Wada, 2000). organisms in bio-films (Cooksey et al., 1984; Wahl, 1989). Colonization by epibionts can be beneficial and have a protec- Attachment of diatoms is a more complicated process than tive value to brachyuran crabs via camouflage (Maldonado & in bacteria (Cooksey & Cooksey, 1995). In some of them, Uriz, 1992). Most previous studies on spider crabs’ epibiota attachment is associated with the production of extracellular have focused on the macro-epibionts in order to elucidate polysaccharides in the form of pads, envelopes, stalks or their masking behaviour (Wilson, 1987; Wicksten, 1993; tubes (Chamberlain, 1976; Hoagland et al., 1993). Earlier Woods & McLay, 1994). The importance of epizoic growth studies revealed that the benthic diatom films induce and of diatoms has been described for many animals including promote larval metamorphosis of fouling invertebrates cladocerans (Gaiser, 1991), copepods (Russell & Norris, (Crisp, 1974; Brancato & Woollacott, 1982). The biochemical 1971; Gibson, 1978; Prasad et al., 1989), and whales cues offered by benthic diatoms strongly depend upon their species composition and density in the films as well as the composition of their extracellular polymeric substances (Harder et al., 2002; Zardus et al., 2008). Corresponding author: F.F. Madkour The spider crab Schizophrys dahlak Griffin and Tranter, Email: [email protected] 1986, is a Red Sea species that is well established in the Suez

1 2 fedekar f. madkour et al.

Canal. It is heavily encrusted with a relatively dense cover of Crabs were first sexed and then their moulting stage was epibionts that helps it hide from predators (Morsy, 2007). determined. The carapace width (CW) and carapace length Little work has been carried out to explain the masking or dec- (CL) of each crab was measured with a Vernier caliper. orating behaviour of spider crab species of the Suez Canal Maturity of males and females was determined based on mor- (Sallam et al., 2007; Sallam & Wicksten, 2011). Sallam et al. phological examination of the size of the chelae and abdomen (2007) was the single study to document the significance of width, respectively. All sampled individuals were examined micro-epibionts in the masking behaviour of the spider crab visually to assess the degree of coverage by macro-epibionts. Hyastenus hilgendorfi inhabiting the Suez Canal recording Each individual was placed in one of the following 5 step 49 species of epiflora. However, nothing is known on the sea- scales: 0%, 5–25%, 25–50%, 50–75%, 75–100%. sonality or the types of habitats in which epizoic diatoms Specimens (four/sex/month), free or almost free of macro- occur on spider crabs from this area. In the present study, epibionts, were chosen for the evaluation of diatom commu- the epibiosis of S. dahlak (Brachyura: Majidae) from the nities. Since the carapace (dorsal side) of S. dahlak was Suez Canal was investigated. An attempt was made to use uneven, the total area was measured by marking it into the epizoic diatoms as a tool to elucidate their role in the nearest geometric figure (4 triangles), then summing their masking behaviour or passive encrustation of S. dahlak. areas. Quantification of diatoms was carried out by scraping Identities and frequencies of occurrence of macro-epibionts the entire carapace with a brush into a known volume of fil- and epizoic diatoms on the integuments of this species were tered seawater and preserving in 4% formalin. Diatoms were assessed. Sex and size of the crabs was recorded and temporal examined prior to and after cleaning with H2O2 and differences in this epibiosis were established. K2Cr207 to oxidize organic material under an inverted micro- scope at 100 × and 400 × and identified to species using primary references for identification (Hendey, 1964; Tomas, MATERIALS AND METHODS 1996). Representative samples of diatoms were enumerated by the sedimentation technique (Hasle, 1978). Since verifying Specimens of Schizophrys dahlak were collected monthly the abundance of various diatom species on the crabs was too between autumn 2008 and summer 2009 from Elferdan, at labour-intensive for this study, seasonal average density for all 2 68 km from the northern end of the Suez Canal (Figure 1). species was expressed as number of cells dm 2/sex. Crabs were obtained from fishermen using trammel nets The total macro-epibiont percentage coverage was sub- with an approximate mesh size of 33.5 mm that are dropped jected to two-way analysis of variance (ANOVA) (Sokal & at sunset and collected at dawn. They were preserved in 4% Rohlf, 1981) in order to evaluate the differences with respect formalin for examination and enumeration of epibionts. to seasons, sex and the interaction of seasons and sex. To compare the abundance of epizoic diatoms among seasons and sexes, the presence/absence of epizoic diatoms, the diver- sity (Shannon–Wiener diversity index, H′) and evenness (J′) of the diatom community were used. The log (x + 1) trans- formed values of generic diatom abundance were further ana- lysed using cluster analysis. The dissimilarity levels were measured through squared Euclidean distance and group average method as described by Pielou (1984) using Primer Package V.5.

RESULTS

A total of 406 specimens were collected: 302 males (74.4%) and 104 females (25.6%). All individuals were in intermoult condition except four males observed in April and August and two females observed in February and May. These were all postmoult and were totally devoid of covering material. Twenty-eight ovigerous females (27%) were observed between May and August. Males had a larger size-range (CW: 28.2–73.3 mm; mean 53.9 + 8.8 mm) than females (CW: 34.6–64.7 mm; mean 45.9 + 6.3 mm). Males were found mature at the minimum size of 37.3 mm CW while females with 34.6 mm CW were mature. The percentages of mature specimens in the samples were 95% for males and 100% for females. Of all collected crabs, 78 (56 males; 22 females) comprising 19.2% of the total, had no macro-epibionts on their integu- ments. The recorded macro-epibionts included the tube worm Hydroides elegans (Haswell, 1883), the barnacle Balanus amphitrite Darwin, 1854 and Balanus eburneus Gould, 1841, the bivalve Brachidontes variabilis (Krauss, Fig. 1. Map of the Suez Canal showing sampling site. 1848) and the tunicate Styela plicata (Lesueur, 1823). Total epibiota of the spider crab s. dahlak from the suez canal 3 coverage of macro-epibionts was greater on females’ carapaces Table 1. Schizophrys dahlak: results of two-way analysis of variance than those of males with apparent seasonal variations. The comparing macro-epibiont coverage between sexes and seasons. highest coverage was recorded in spring (70.3% and 46.9%) df SS MS F P and winter (65.3% and 42.3%) for females and males, respect- ively (Figure 2). The total coverage of macro-epibionts Seasons 3 2258.21 752.74 7.98 ≤0.0018 (including all forms recorded), when subjected to two-way Gender 1 1235.54 1235.54 13.1 ≤0.0023 × ≤ ANOVA, revealed a significant variation between sexes and Seasons gender 3 574.48 191.49 2.03 0.1502 seasons (Table 1). Error 16 1509.32 94.33 Total 23 5577.55 Ninety-six individuals were examined for epizoic diatoms, three of which were totally bare. Sixty-five diatom taxa were recorded (56 pennates and 9 centrics) belonging to 25 genera (19 pennates and 6 centrics). The dominant genera, between 17 and 30 taxa in spring and winter, respectively in terms of the number of species, were Nitzschia (11 for males, and between 15 and 26 taxa during spring and species), Navicula (10 species) and Pinnularia (6 species). summer, respectively for females. The taxa, listed in Table 2, can be divided into two groups Epizoic diatom assemblages displayed indistinctly higher ′ ′ on the basis of their frequency of epizoic occurrence on all values of diversity index (H ) and evenness (J ) for females crab specimens. The first group (A) consists of eight than for males in most occasions (Figure 3C, D). Significant diatoms with frequency ranging between 20% (Cyclotella glo- seasonal difference was found when values for males and merata) and 55% (Cyclotella meneghiniana). The remaining females were averaged. Epizoic diatom were more diverse in ′ ′ 57 species (group B) had frequencies less than 20%. The winter (average H ¼ 2.43) and less in spring (average H ¼ most abundant were species of Cocconeis, Amphora, 0.97). A clear seasonal difference was found for evenness ′ Fragilaria, Nitzschia and Naviculla. Planktonic diatoms such values, the lowest (J ¼ 0.84) was in autumn and the highest ′ as C. meneghiniana and Nitzschia sigma were observed (J ¼ 1.74) in summer. The dendrograms (Figure 4A, B) are throughout the year. The benthic diatoms Pinnularia treve- derived from a matrix of 4 samples (representing seasonal lyana and Surirella ovalis also existed in all seasons. average counts of epizoic diatoms on examined crabs) × 25 The epizoic diatom species number, according to their species (representing epizoic diatoms genera) on both males presence/absence, and abundance (cells dm22) were higher and females. The dendrograms separated genus Fragilaria at for males than for females (Figure 3A, B). The maximal the greatest dissimilarity level (65% and 44%) in males and total average of cells was noticed during summer and spring females, respectively. Two additional distinct clusters could with the highest average of 10.9 and 4.4 × 103 cells dm22 be distinguished for both sexes with different samples for males and females, respectively. Minimal values were merging at a greater dissimilarity level in males (47%) than observed during autumn and winter with the lowest average females (37%). The higher dissimilarity levels in the case of of 0.67 and 0.21 × 103 cells dm22 for males and females, males indicate the greater abundance of species in males respectively. In terms of density, pennate diatoms dominated than females. The first cluster consisted of two genera, the epibiotic community with dominance that reached 96%. Navicula and Nitzschia in females in addition to Amphora In summer, many species displayed high density. Some of and Cocconeis in males. The rest of genera constituted the them were confined to males only such as Amphora coffeaefor- second group and displayed little dissimilarity. mis and Cocconeis placentula (36% and 24% of the total average density, respectively), whereas others such as Navicula placentula and Nitzschia kutzingiana occurred abun- DISCUSSION dantly on both males and females’ carapaces. Fragilaria inter- media (comprising 73.5% of the total average) appeared to be Five species of macro-epibionts and 65 species of diatoms the most dominant during spring for males and females. (micro-epibionts) were recorded as epibionts on the integu- Speciation provided a different picture than counting with ment of Schizophrys dahlak inhabiting the Suez Canal. In irregular seasonal pattern. Identified species fluctuated the study area, where soft sediments dominate the bottom substrate, slow moving spider crabs could provide a substrate for the settlement and colonization of benthic diatoms and encrusting filter feeding organisms. Substrates and microhabi- tats provided by crabs and associated epibionts greatly influ- ence the community structure by increasing the species richness of the benthic assemblages. Recorded epizoic diatoms were mostly pennates that are typically benthic taxa that commonly grow attached to substrates. Madkour et al. (2007) in their study on the phytoplankton of the Suez Canal observed the predominance of benthic pennate diatoms particularly in the middle region of the Canal. The higher frequency and density of some pennate taxa in the benthic forms could be attributed to their ability to attach to substrates by gelatinous stalks or pads (Cooksey et al., 1984; Hoagland et al., 1993). However, centric forms Fig. 2. Schizophrys dahlak: seasonal variations in the percentage cover of (e.g. Cyclotella and Biddulphia), which are usually common macro-epibionts on males and females’ carapaces. Error bars indicate members of the planktonic communities, may get entangled standard errors. with attached forms or trapped by the setae on the crab. 4 fedekar f. madkour et al.

Table 2. Epizoic diatoms on the integument of Schizophrys dahlak divided into two groups according to their frequency on the crab (see text for groups’ denotation).

Group A Pennates

Fragilaria intermedia Grunow P. trevelyana (Donkin) Raben. Nitzschia sigma Ku¨tz. Surirella ovalis Ku¨tz. Pinnularia hemiptera (Ku¨tz.) Raben. Centrics Cyclotella glomerata Bachmann Thalassiosira sp. C. meneghiniana Ku¨tz. Group B Pennates Achnanthes brevipes Agardh N. placentula (Ehr.) Ku¨tz. Amphiprora hyalina Eul. ex Van Heur. N. rostellata Ku¨tz. Amphora coffeaeformis (Ag.) Ku¨tz. Nitzschia apiculata (Greg.) Grun. A. hyalina Ku¨tz. N. denticula Grun. A. ovalis Smith N. frustulum (Ku¨tz.) Grun. Amphora sp. N. ku¨tzingiana Hilse Cocconeis danica Flogel N. palea (Ku¨tz.) Smith C. pelta A. Schmidt N. panduriformis Gregory C. placentula Ehr. N. punctata (Smith) Grunow Cymbella ventricosa Ku¨tz. N. subtilis Grun. Diploneis constricta (Grun.) Cleve N. thermalis (Ehr.) Auerswald D. crabro Ehr. N. tryblionella Hantzsch Fallacia pygmaea (Ku¨tz.) Stic. & Man. Pinnularia appendiculata (Ag.) Cleve Fragilaria capucina Desm. P. major (Ku¨tz.) Rab. Grammatophora marina (Lyng.) Ku¨tz. P. rectangulata (Gregory) Rab. G. malleus (Bright.) Van Heurck P. viridis (Nitzsch) Ehr. Gyrosigma eximium (Thw.) Boyer Pleurosigma angulatum (Quekett) Smith Licmophora tenuis (Ku¨tz.) Grun. P. distortum Smith Navicula cancellata Donk P. obscurum Smith N. dicephala (Ehr.) Smith Rhoicosigma compactum (Grev.) Grun. N. directa (Smith) Ralfs Rhoicosphenia abbreviate (Ag.) Lan.-Ber. N. divergens Smith Surirella striatula Turpin N. gracilis Ehr. Synedra amphicephala Grunow N. humerosa Bre´b. Ex Smith S. berolinensis Lemm. N. lyra Ehr. S. pulchella Ku¨tz. N. notabilis Grev. Centrics Biddulphia alternans (Bail.) Van Heur. C. radiatus Ehr. Campylodiscus eximius Greg. Melosira granulata (Ehr.) Ralfs. Coscinodiscus centralis Ehr. Thalassiosira leptopus (Grun.) Has & Fry.

The range of Shannon–Wiener diversity index (average H′: dissimilar species in terms of abundance on carapaces of 0.97–2.43) recorded in the present study was more or less both sexes compared to other recorded diatoms (Figure 4A, close to the value observed by Margalef (1978) for the actively B). The high abundance of a sole species is unusual because, growing coastal populations. Seasonal patterns of diatoms although diatoms are sensitive to environmental conditions diversity indices with the highest values (evenness: 1.74 and on very small scales, typically, not one, but many taxa occur Shannon–Wiener index: 2.43) recorded in summer and together and are characteristic of a particular microhabitat. winter, respectively, reflect the equitability of the dominant As shown by the cluster analysis, there was a variation in group complex in summer and the diversity of the assem- the association of the dominant diatoms in summer. The blages on S. dahlak in winter. abundance of Amphora coffeaeformis and Cocconeis placen- There was a clear seasonal trend in the abundance of tula on males’ carapaces only indicates that some factors, benthic diatoms with the maximum in spring and summer. often undetermined, are operating to prevent the occurrence This is consistent with the pattern described by Round of particular species on females. The present data on pres- (1960). Although the abundance and species composition of ence/absence and abundance of diatoms show that males benthic diatoms are controlled by water quality, substratum were more hospitable for epizoic diatoms than were females. and level of disturbance (Round, 1981), it is more difficult Benthic diatoms particularly pennate forms are able to to determine which of these factors had an impact in the excrete a copious amount of extrapolymeric substances case of S. dahlak. While the recorded diatoms were diversified (Hoagland et al., 1993) that provides a food source for other (65 species), only a few species had high abundance. Fragilaria organisms (Middelburg et al., 2000). Benthic diatom films intermedia represented the only abundant epizoic diatom and their components play an important role in inducing which dominated the community during spring in both larval metamorphosis and providing cues to invertebrate sexes. This was supported by the results of the cluster analysis larvae. The cues offered by benthic diatoms can also which revealed that the genus Fragilaria was the most mediate invertebrate larval metamorphosis (Crisp, 1974; epibiota of the spider crab s. dahlak from the suez canal 5

Fig. 3. Schizophrys dahlak comparison of: (A) diatom species number; (B) cell abundance (cells × 103 dm22); (C) diatom evenness (J′); and (D) Shannon–Wiener diversity index (H′) in males and females during the different seasons. Error bars indicate standard errors.

Brancato & Woollacott, 1982). In the present study, the high the highest in spring. During the winter and spring, adult density of epizoic diatoms assemblage on the carapace of forms of epibionts were seen in high densities, perhaps due S. dahlak in summer might act as a substrate for larval settle- to the settlement of larvae that underwent metamorphosis. ment. Observations of the macro-epibionts’ seasonality on S. Seasonal variations in the macro-epibiont density could be dahlak revealed that their lowest density was in summer and due to the facilitation of larval settling by the cues from benthic diatoms. Macro-epibionts recorded on the integument of S. dahlak were the same as those reported for Hyastenus hilgendorfi from the Suez Canal (Sallam et al., 2007; Sallam & Wicksten, 2011). This indicates that epibionts are generalists and not species-specific, due to the wide diversity of basibionts on which they are settled. In contrast to benthic diatoms, macro-epibiont coverage was denser on the carapaces of females. This finding is similar to that reported for Hyastenus hilgendorfi from the Suez Canal (Sallam & Wicksten, 2011). Intra-specific difference in the decoration pattern where adult males decorate less than females has been previously reported (Wicksten, 1993; Berke & Wooden, 2009). A similar pattern has been reported for the deep-sea crab Bathynectes piprritus (Abello´ et al., 1990; Gili et al., 1993). The higher density of epibionts on females than males reported for portunid crabs (Overstreet, 1983; Key et al., 1997) could also support the conclusion that females of S. dahlak harboured more epibionts. Ferna´ndez et al. (1998) concluded that the degree of inci- dence of epibiosis and self-decoration varies depending on different environmental factors, such as habitat and season, and on factors linked to the biology of the species such as the size of the individual, moult frequency, and the time elapsed from the terminal moult. Consequently, the duration of the intermoult period of S. dahlak in which individuals maintained their hard carapaces could have assisted the Fig. 4. Schizophrys dahlak: generic cluster dendrograms of the epizoic diatom density of epibiont settlement. The rate of moulting in community from (A) males and (B) females. spider crabs tends to slow as they approach maturity, at 6 fedekar f. madkour et al.

which time it stops (Hartnoll, 2001). On maturity, the cara- Brancato M.S. and Woollacott R.M. (1982) Effect of microbial films on pace would remain as a stable substrate, on which epibiota settlement of bryozoan larvae (Bugula simplex, B. stolonifera, B. could grow and flourish. The minimum size of maturity of turrjta). Marine Biology 71, 51–56. S. dahlak was 37.3 mm CW for males and 34.6 mm CW for Chamberlain A.H.L. (1976) Algal settlement and secretion of adhesive females but according to Morsy (2007) any female above material. In Sharpley J.M. and Kaplan A.M. (eds) Proceedings of the 34 mm in size could be mature. Since all of the crabs we col- 3rd International Biodegradation Symposium. London: Applied lected ranged from 28.2 to 73.3 mm CW, we suspect that any Science, pp. 417–432. over-estimate of the percentage of mature females is low. On Cooksey B., Cooksey K.E., Miller C.A., Paul J.H., Rubin R.W. and the other hand, inhabiting the Suez Canal are sea- Webster D. (1984) The attachment of microfouling diatoms. In sonal breeders; they have been reported to be sexually active Costlow J.D. and Tipper R.C. (eds) Marine biodeterioration: an inter- during June to November and have a well-defined resting disciplinary study. London: E and FN Spon Ltd, pp. 167–172. phase between January and March (Sallam, 2000; Morsy, Cooksey K.E. and Cooksey B. (1995) Adhesion of bacteria and diatoms to 2007). We saw no evidence of seasonality of moulting surface in the sea: a review. Aquatic Microbial Ecology 9, 87–96. among our crabs. Motion during mating may increase the mechanical Crisp D.J. (1974) Factors influencing the settlement of marine invert- abrasion on the carapace, which could dislodge attached ebrate larvae. In Grant P.T. and Maclue A.M. (eds) Chemoreception organisms. Barnacles and tube-building polychaetes, which in marine organisms. London, New York: Academic Press, pp. are common epibionts of the crabs, are cemented to the cara- 177–265. paces and cannot easily be removed. We suspect that, if any DeGoursey R.E. and Auster P.J. (2001) A mating aggregation of the surface abrasion takes place during mating, ascidians would spider crab (Libinia emarginata). Journal of Northwest Atlantic be the most likely organisms to be dislodged. Although Fishery Science 13, 77–82. there are no observations for the mating behaviour of Ferna´ndez L., Parapar E., Gonza´lez-Gurriara´n E. and Muı´n˜oR.(1998) S. dahlak in the Suez Canal, it could be postulated that it Epibiosis and ornamental cover patterns of the spider crab Maja has an influence on the pattern and density of distribution squinado on the Galician coast, northwestern Spain: influence of be- of epibionts on the integument of this species. DeGoursey & havioural and ecological characteristics of the host. Journal of Auster (2001) observed a variety of mating postures for Biology 18, 728–737. some spider crab species. Of these, one took place with the Gaiser E.E. (1991) Epizoic diatoms of cladoceran zooplankton. MSc thesis. male lying on its carapace with the female on top. If this is Iowa State University. the case for S. dahlak, then this posture could help make the undisturbed surface availability for macro-epibionts less on Gibson R.A. (1978) Pseudohimantidium pacificum, an epizoic diatom new to the Florida current (western North Atlantic Ocean). Journal males by the increased mechanical abrasion on their carapaces of Phycology 14, 371–373. while the whole of the female’s carapace is exposed for epi- biont settlement. On the other hand, ovigerous females are Gili J.M., Abello´ P. and Villanueva R. (1993) Epibionts and intermoult known to remain motionless in their position for some time duration in the crab Bathynectes piprritus. Marine Ecology Progress until egg hatching. 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