Macroepiphytes on Cystoseira Species (Phaeophyceae) on the Coast of Montenegro

MACROEPIPHYTES ON CYSTOSEIRA SPECIES (PHAEOPHYCEAE) ON THE COAST OF MONTENEGRO

Vesna Mačić1,* and Zorica Svirčev2

1 Institute of Marine Biology, University of Montenegro; Dobrota b.b.; 85330 Kotor, Montenegro 2 Department of Biology and Ecology; University of Novi Sad; Trg D. Obradovica 2; Novi Sad 21000; Serbia

ABSTRACT tion stress during low tide [1, 3]. Although an epiphytic life style requires specific adaptations like fast growing to The genus Cystoseira considerably supports epiphytic a small body size, early sexual or asexual reproduction, a assemblages on their thallus, but studies on their epiphytic short life span, it is also the strategy by which different species are rare. From the nine Cystoseira taxa from the organisms can avoid competition for substrate [4]. In the coast of Montenegro, 46 species of epiphytes were col- Mediterranean Sea Cystoseira (Phaeophyceae) species lected. Similarities of epiphytic assemblages on different have a dominant role on rocky substrate of coastal zone host algae were analyzed, as well as correlation between and although there are many information about this algae, epiphytes and complexicity of thallus for host Cysto- studies on their epiphytic species are rare [3, 5-8]. Be- seira species. These are the first data for epiphytes as- cause of all that, the aim of this work was to provide more semblages on Cystoseira species from the Montenegrin details on epiphyte species on Cystoseira algae on the coast and further research is needed for providing better Montenegrin coast (Adriatic Sea) and to provide a better data base for future monitoring and evaluating of envi- data base for future monitoring and evaluation of the ronmental changes on the hard-bottom communities. marine ecosystems quality status.

2. MATERIALS AND METHODS

KEYWORDS: The fieldwork was carried out on the rocky shore of epiphytes, Cystoseira, Adriatic Sea, macroalgae, Mediterranean the Montenegrin coast (Adriatic Sea) on 8 sites: Ora- hovac, Perast, Strp, Žanjice, Kočište, Budva, Bar and Port Milena (Fig. 1.). Sampling was done by SCUBA diving seasonally between autumn 2005 and spring 2007 (except winter). Samples were obtained by scraping off all the organisms from limestone substrate on the surface of 1. INTRODUCTION 25cm x 25cm on three depths (0.5m, 3m and 5m) and in three replicates. Few hours after collection samples were A rocky shore is one of the most complex and com- frozen and stored until processing in laboratory. In further pact habitats and one of the very specific characteristics analysis each Cystoseira plant was looked for the epi- is vertical zonation of sessile plants and animals [1]. phytes, subsequently epiphytes were separated from the Dominant macroalgae, usually constructors of the bio- host plant and identified to the lowest possible taxonomic cenosis, occupy extensive areas of the rocky substrate, level using a Stereomicroscope Sigma Trino and manuals while many smaller algae species grow as epibionts. Epi- for identification. All samples of host algae and epiphytes phytes play an important role in marine biocenosis con- are preserved in 10% formalin seawater and deposited in tributing to primary productivity, but they also have an the collection of the Institute of marine biology, Kotor, important role in many other interactions with host algal University of Montenegro. species and with other species of communities. Epiphytes act as a barrier to light penetration and nutrient availabil- Statistic analysis and graphics were made using Primer ity, so the photosynthesis of hosts is reduced and could be 5.0 software [9]. The statistically significant correlation a cause of population regression [2, 3]. Only a few bene- coefficients between different epyphites and Cystoseira ficial effects for the host are known: epiphytes limit graz- hosts were designated for p<0.05. Dendogram for Cysto- ing by potential herbivores and seem to reduce desicca- seira thallus complexicity is calculated on the base of volume of talus, maximal length, length of axis and pri- * Corresponding author mary branches.

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3. RESULTS AND DISCUSSION

From all sampling sites we collected nine species of Cystoseira, and they are: Cystoseira amentacea var. spi- cata (Ercegović) G. Giaccone in T. Gallardo, Cystoseira barbata (Stackhouse) C. Agardh, Cystoseira compressa (Esper) Gerloff & Nizamuddin, Cystoseira corniculata ssp. laxior Ercegović, Cystoseira foeniculacea (Linnaeus) Greville, Cystoseira spinosa Sauvageau, Cystoseira crinita (Desf.) Bory, Cystoseira crinitophylla Ercegović and Cystoseira humilis Kutz. On these species 46 species were determined as ephyphites, 27 species were algae while 19 species were fauna (Table 1). Between algae epiphytes the dominant group were Rhodophyta with 18 species while Heterokontophyta were represented with five species and Chlorophyta with four species.

Presence of different number of epi-flora and epifauna species on different Cystoseira species is shown on Fig 2. For epi-floral species except dominance of Rhodo- FIGURE 1 - Studied localities on the coast of Montenegro (1. Port phyta group it is also characteristic that the highest num- Milena, 2. Bar, 3. Budva, 4. cape Kočište, 5. Žanjice, 6. Strp, 7. Perast and 8. Orahovac) ber of epiphytes has a C. barbata and C. amentacea,

TABLE 1 - Macroepiphytes on different Cystoseira species

Cystoseira host

Macroepiphytes

C. amentacea barbata C. C. compressa corniculata C. C. crinita C.crinitophylla C. humilis C. foeniculacea spinosa C. % frekvency Chlorophyta Chaetomorpha aerea (Dillwyn) Kutzing 1 11,11 Cladophora prolifera (Roth.) Kutzing 1 1 1 33,33 Enteromorpha intestinalis (L.) Link 1 11,11 Ulva lactuca Linnaeus 1 11,11 Heterocontophyta Cystosaeira barbata J. Ag. 1 11,11 Dictyota linearis (Ag.) Grev. 1 1 1 1 1 55,56 Elachista sp. Duby 1 11,11 Halopteris scoparia (L.) Sauvag. 1 11,11 Sphacelaria cirrosa (Roth) C.Ag. 1 1 1 1 1 55,56 Rhodophyta Amphiroa rigida Lamouroux 1 11,11 Bangia fuscopurpurea (Dillw.) Lyngb. 1 1 22,22 Botryocladia botryoides (Wulf.) Feldm. 1 1 1 33,33 Callithamnion corymbosum (Smith) Lyngbye 1 1 1 33,33 Ceramium ciliatum (J.Ellis) Ducluzeau 1 1 1 33,33 Corallina elongata Aresch 1 11,11 Falkenbergia rufolanosa (Harvey) F. Schmitz. 1 1 1 1 44,44 Gelidium latifolium (Grev.) Thur e Born 1 11,11 Haliptilon virgatum (Zanardini) Garbary & Johansen 1 1 1 33,33 Hydrolithon farinosum (Lamouroux) Penrose & Chamberlain 1 1 1 1 1 1 1 77,78 Hypnea musciformis (Wulf.) Lam. 1 1 1 1 44,44 Jania rubens var. rubens (l.) Lamouroux 1 1 22,22 Laurencia sp.Lam. 1 1 22,22 Liagora viscida (Forssk.) C.Ag. 1 11,11 Mesophyllum sp. Lemoine 1 1 22,22 Peyssonnelia rubra Decaisne 1 1 1 33,33 Rhodymenia ardissonei Feldm. 1 1 1 33,33 Womersleyella setacea (Hollenberg) R. E. Norris 1 1 1 33,33

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Animal Balanus eburneus Gould 1 1 22,22 Cryptosula pallasiana Moll 1 1 1 1 44,44 Dexiospira pagenstecheri Quatrefages 1 1 1 1 1 1 1 1 1 100 Eunice vittata Delle Chiaje 1 1 22,22 Gourmya rupestris, Risso 1 1 1 1 1 1 66,67 Ircinia sp. Pallas 1 1 22,22 Lichenopora radiata, Audouin 1 1 1 1 1 1 1 77,78 Lineus geniculatus Delle Chiaje 1 1 22,22 Mytilus galloprovincialisLam. 1 1 22,22 Obelia geniculata L. 1 1 1 1 1 55,56 Ophiotrix fragilis Abild. 1 1 22,22 Plumaria setacea L. 1 1 1 1 44,44 Pomatoceros triqueter L. 1 1 1 1 44,44 Protula intestinum Sav. 1 1 22,22 Scrupocellaria reptans L. 1 1 22,22 Spongia officinalisL. 1 1 22,22 Gourmya vulgata Bruguiere 1 1 1 33,33 Bittium reticulatum da Costa 1 1 1 1 44,44 Calliostoma zizyphinus L. 1 11,11

20 epi-fauna 15 Rhodophyta

10 Heterokontophyta Chlorophyta 5

a a lla ilis at osa ul lacea n c hum u ni C.crinita C. .spi mentaceaC.barbat initophy a compressacor enic C . .cr o C. C C. C .f C

FIGURE 2 - Presence of epiphytes on different Cystoseira host species

following by C. spinosa and C. corniculata ssp. laxior. theory we can mention that C. amentacea and C. com- The smallest number of phyto-epiphytes was on C. humi- pressa in our study were collected always on the same lis but we should have in mind that in this study only two locations so, the important similarity of their epiphytes algae of this species were collected, so probably on the (correlation coefficient was r=0.45, for significance bigger sample of this Cystoseira „host“ could be found p<0.05) could be consequence of the same environmental more ephyphites. For other Cystoseira species quite small factors. Beside that the highest values of correlation coef- number of phyto-ephyphites was recorded: for C. foenicu- ficients were for the species of host collected on the same lacea 4, C. compressa 5 and C. crinita 5 species. locations, like: C. foeniculacea with C. humilis r=0.53 and C. foeniculacea with C. crinita r=0.49 (Table 2). Addi- C. spinosa and C. corniculata ssp. laxior, following tionally, for Hidrozoa on 3 Cystoseira species Faucci and by C. barbata, were with the highest diversity of epi- Boero [4] referred as the most important impact of abiotic faunal species and as it was for epi-floral species, C. hu- factors: sedimentation rate, nutrient levels, temperature milis was host species with the smallest number of epi- and especially water movement, while biological factors faunal epiphytes. such as the structure and surface of the host and competition seem to be secondary. Belegratis et al. [3] reported different composition of epiphytic assemblages on different locations, while they Higher epiphytes biodiversity was expected on the could not find differences between different host Cysto- Cystoseira species characterised for the oligotrophyc areas seira species on the same locality. In contribution to that [10, 11], but some authors [5, 12, 13] considered morphol-

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ogy and complexicity of thallus as the very important be neglected because of already mentioned reason (small factor, as well. In accordance with that are findings were number of collected individuals). Similarity for thallus for the great number of vagile species for the host species complexity is very interesting for group: C. spinosa, C. are chosen those with bigger architecture complexity [6]. crinitophylla, C. foeniculacea, C. barbata and C. cornicu- In that way instead of direct feeding preferences, priority lata ssp. laxior because that is a group (except C. foenicu- for choosing the host species is given to possible refuge lacea) also distinguished in analysis for number and spe- from predators and more sheltered habitat. cies of epiphytes on different Cystoseira species (Fig. 4).

In our case cluster analysis for complexicity of talus But these analyses are not enough for explanation of for host Cystoseira species is calculated and dendogram is all other similarities and differences between epiphytes on shown on Fig 3. A huge difference for C. humilis should Cystoseira species. Probably in some future analysis part

TABLE 2 - Correlation between presence of different epiphytes on Cystoseira host

Correlations Marked correlations are significant at p < .05000 N=44 C. amentacea C. barbata C. compressa C. corniculata C. crinita C. crinitophylla C. humilis C. foeniculacea C. spinosa Variable C. amentacea 1,00 -0,14 0,45 -0,15 0,21 -0,27 0,14 0,15 -0,26 C. barbata -0,14 1,00 0,12 -0,06 -0,04 0,34 0,16 0,07 0,02 C. compressa 0,45 0,12 1,00 -0,10 0,39 -0,07 0,34 0,35 -0,04 C. corniculata -0,15 -0,06 -0,10 1,00 -0,10 0,23 0,10 0,08 0,32 C. crinita 0,21 -0,04 0,39 -0,10 1,00 -0,07 0,34 0,49 0,19 C. crinitophylla -0,27 0,34 -0,07 0,23 -0,07 1,00 0,20 0,02 0,33 C. humilis 0,14 0,16 0,34 0,10 0,34 0,20 1,00 0,53 0,25 C. foeniculace 0,15 0,07 0,35 0,08 0,49 0,02 0,53 1,00 0,35 C. spinosa -0,26 0,02 -0,04 0,32 0,19 0,33 0,25 0,35 1,00

C. spinosa C. crinitophylla C. foeniculacea C. barbata C. corniculata C. crinita C. amentacea C. compressa C. humilis 0 20406080100 Similarity

FIGURE 3 - Dendogram of Cystoseira talus complexicity

C. foeniculacea

C. crinita

C. compressa

C. amentacea

C. crinitophylla

C. barbata

C. spinosa

C. corniculata

C. humilis

20 40 60 80 100

FIGURE 4 - Dendogram of epiphytes similarity on different Cystoseira species

of the attention should be concentrated on algae from research on the biodiversity of marine species on the deeper habitats, and only in the case of analysis of whole Montenegrin coast and to provide a better data base for vertical distribution of host species we can provide more future monitoring. In favour of needed research and moni- precise data for composition of their epiphytes and bio- toring of native and invasive species are many interna- cenosis. At the moment we can only mention our observa- tional conventions and published papers, which empha- tion of a huge number of epiphytes on C. spinosa, C. corni- size usually irreversibility of changes caused by invasive culata ssp. laxior and C. foeniculacea collected from species, changes of habitat, decline of native biodiversity deeper locations (10-30m depth). and sometimes impact on human health and economic losses-specially in fishery and aquaculture [25-28]. Fur- Furthermore we should mention that the genus Cysto- thermore, experiences from many countries are showing seira generally supports considerably epiphytic assem- that once introduced invasive species is almost impossible blages on the thalli [3, 14]. Fraschetti et al. [5] consider that to control. Because of that, the first basic task of invasive the composition of epiphytes are more dependant on envi- alien species management is to prevent or minimise trans- ronmental factor than host species, so epifauna can allow port and the risk of alien species introduction with finally better comparison among sites than the actual distribution scope to minimise threats to biodiversity, human health of the macro-algal species. But, especially for epifaunistic and economies [29]. species we should have in mind the availability of shelter from predators and food availability. Also, some Isopoda species showed seasonal variability in the presence on 4. CONCLUSION host species due to their life cycle [15], while some poly- chaeta species could be divided in epi- meso- or endo- Physical factors, such as temperature, wave exposure, bionts according to algal structure [16]. rate of sedimentation, together with biological factors, phenology and architecture of algal host, might play a Although in our study host Cystoseira algae were col- important role as determinants of epifaunal distribution, so lected only from 0.5m, 3m and 5m depth we would like to for understanding the causes driving distribution of epi- mention, as very important, our observation of alohtonous, phytic organisms on the Cystoseira species, the complex invasive algae Womersleyella setacea (Hollenberg) R.E. analysis of abiotic and biotic factors should be performed. Norris and Caulerpa racemosa var. cylindracea (Forsskal) Also, as is usually in other ecological studies, this analysis J. Agardh in deeper zones. Algae W. setacea was recorded should pass on from local and short-lasting to those of as epiphyte on Cystoseira foeniculacea f. latiramosa and wider areas and longer lasting. Only with that kind of data Cystoseira foeniculacea f. tenuiramosa and other species of we can consider epiphytes as a tool for better comparisons flora and fauna, on the cape Kočište from 12-28m depth. among sites than the actual distribution of the algal spe- This invasive algal species is of Indo-Pacific origin and cies are, and a valid tools for evaluating environmental for the first time in Montenegro was recorded in 2003 changes on coastal hard-bottom communities. [17], but according to published data [18-20] there are indications that it is becoming dominant or taking the The authors have declared no conflict of interest. place of keystone species in the infralitoral algal community. 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