MARINE ECOLOGY PROGRESS SERIES - Published May 31 Mar. Ecol. Prog. Ser. I

The Mobile Fauna - Especially - of Sargassum cymosum*

A. S. Tararamand Y. Wakabara

Instituto Oceanografico. Universidadede Sao Paulo. Cidade Universitaria. Butanta - 05508, SP. Brazil

ABSTRACT: A comparative study was made on the composition of the vagile fauna Inhabiting the alga Sargassum cymosum collected at 2 sites, d~ffer~ngin wave action, on the northern coast of Sao Paulo State, Braz~l(23"30'S and 45"06'W). A total of 122.886 specimens were collected at 2 stdt~ons,belonging to 23 taxonomic groups. Gammaridea comprised the dominant group at both sites. 15 species were recorded, among these 14 common specles. Water rn0vemen.t - even at the exposed shore - and sediment quantlty of the sheltered site do not seem to affect gamrnaridean specles variety. Species dominance thl-oughout the yedr varied In exposed and sheltered localities. Hyale medla was dominant at the exposed shore, and neapolitanus was the most abundant species at the sheltered shore.

INTRODUCTION the rocks is considerable. The second area is located at Enseada do Flamengo, on a sheltered shore, with Marine macro-algae are inhabited by a variety of waves of moderate intensity; the amount of detritus 1s sessile and vagile . Among the latter, the not large, but dur~ngheavy rains the runoff of terrigen- frequently comprise the dominant group. ous material can be considerable (Boffi, 1972). During Authors such as Truchot (1963), Fenwick (1976), Moore the study, the annual average values of dissolved oxy- (1978) and Nelson (1979) have dealt with the phytal gen, salinity and temperature of sea water at Praia amphipod fauna. Dommasnes (1968) and Moore (1973) Grande were 5.19 m1 I-', 34.97 S and 23.66 "C, studied the phytal fauna from shores exposed to diffe- respectively; they are 5.30 m1 I-', 34.05 %O S and rent wave action. In Brazil, investigations on the phytal 25.01 "C at Praia do Lamberto. Monthly data of these fauna were made by Lima (1969), Boffi (1972), Leite parameters are given in Figure 2. (1976), Masuna.ri (1976) and Montouchet (1979). Moreira (1973,a,b), Pereira Leite (1976) and Pires (1977) studied the biology of phytal species. Pereira MATERIAL AND METHODS Leite (1976) analyzed the life cycle of the gammai-l- dean Hyale media. The present investigation is con- Sampling was carried out monthly, during low tide, cerned with the qualitative and quantitative analysis from July 1974 to June 1975. The algae were picked of the vagile fauna of Sargassum cymosum, especially from the substratum and rapidly placed in a plastic Gammaridea, inhabiting two shores with different bag In the laboratory the samples were treated as degrees of exposition to waves. follo\vs: (1) The algae were transferred to an enclosure containing water with a few drops of formaldehyde. (2) They were then carefully shaken, branch by AREA OF INVESTIGATION branch, in buckets containing water with a few drops of formaldehyde. (3) The water was passed through a The material was collected at Ubatuba, northern sieve (285 mesh size) where the animals were coast of Sao Paulo State (23'30's and 45"06'W), at the retained. (4) The different groups were sorted rocky parts of Praia Grande and Praia do Lamberto out under an ordinary microscope, counted and then (Fig. 1). The first site is considered an exposed shore preserved in 70.0 % alcohol. (Nonato and Peres, 1961) where the impact of waves on For some gammaridean genera (, Lysianassa; 1 species of Hyale) identification to Contribution No. 476 of Instituto Oceanogrcifico. Univer- species was impossible either because they were pre- sidade Sao Paulo, Brazil sent in very small numbers, or were still in their early

Inter-Research/Pr~ntedIn F R Germany 158 Mar Ecol. Prog. Ser. 5: 157-163, 1981

Fig. 1. Sampling stations: Praia Grande (A) and Praia do Lamberto (B) developmental stages. Quantitative analysis was the total fauna wlth 6.94 ind. g-' Sargassum; at the effectuated by making use of dominance (Da), mean sheltered site the number of specimens (63,709) rep- dominance (mD), frequency of occurrence (Fr) and resented 51.85 96 with 7.34 ind. g-' Sargassum. Sorensens's quotient of simil.arity (Q.S.). Dominance Foraminifera, Polycladida, Nemertea, Nematoda, and frequency of occurrence were calculated accord- Polychaeta, Ostracoda, Copepoda, Tanaidacea, ing to Moore (1971). It was assumed that high domi- Isopoda, Gammaridea, Caprellidea. Decapoda nance occurred when mD > 40.00 %; 40.00 % > mD > Natantia, Decapoda Reptantia, Acarina. Pycnogonida, 10.00 % were considered intermediate dominances Ophiuro~dea, Echinoldea, Crynoidea, Amphineura, and mD values < 10.00 '10 as low dominances For Gastropoda Prosobranchia, Gastropoda Opistobran- chia, Lamellibranchia and Pisces were found at both Sorensen's quotient of similarity OS. = &, where shores; Sipunculidea, Mysidacea and Holothuroidea a = number of species of Station A (exposed); b = occurred only at the sheltered shore (Table 1). The number of species of Station B (sheltered); j = number dominance of Crustacea, Mollusca, Ech~nodermata, of species at both stations (Southwood, 1958). Polychaeta and remaining groups (referred to as 'other groups') were at the ex p OS e d site . Crustacea, 59.24 %; Mollusca, 28.65 "/o;Echinodermata, 0.09 %; RESULTS Polychaeta, 4.64 %; 'other groups', 7 26 %; at the S h e l t er e a S i t e : Crustacea, 79.98 %; Mollusca, Total Fauna 6.81 %; Echinodermata, 0.24 %; Polychaeta, 3.43 %; 'oth.er groups', 9.42 % (Fig. 3). In Figure 3 the predomi- A total of 122,886 specimens were recorded during nance of Crustacea is evident; among them the Gam- 12 months at the two stations. At the exposed site the maridea are most conspicuous. Table 1 also lists the number of specimens (59,177) represented 48 15 % of annual dominance of each group. Table 1 Ann11'1l domirlnnct. ('l(#) of groups of orgdnrsnls col lected at Prclld C;rdnde (exposcsd sit(,) rlnd Prald do Lcln~herto (.;h~ltrrt~tts~tt.J

For.~n~rn~lcr<~ P~l}~cl~~(l~da Nc,rncrtt,'l Xt'llldtOtld S~pi~nculida P~ly~hdl'Ia Os(t.dcoda Copcpoda hlysiddctsd Tanaidacea lsopoda Gammaridc~~ Caprcllidrd Decapoda Natant~d Decapodd Reptantia Acarina Pycnogonida Ophiuro~dca Ech~noidca I Jolotliuroiclca Crinoiclea Arnphineura Gastropoda Prosobranchla Gastropoda Opistobr-anchia 211 Lamellibranchia .i ISCHD,T"*U Pisces Fig. 2. Var~<~tionin physlco-chcm~cdl pardmrters at the sur- vey s~tes Groups with Da less than 0.01%

Gammaridean Fauna

At the exposed site the monthly contribution of Gam- maridea attained a maximum in December 1974

(69.60 'Yo)and a minimum in hhy 1975 (8.50 Or)); at the sheltered site the maximum occurred in September 1974 (76.75 %), the minimum in Llarch 1915 (8.43 "6) (Fig. 4). Frequency of occurrence (Fr) and medn donli- nance (mD)of gammaridrdn species arc listed in Table

2. Hyale media had 100.00 O/oFr at both sites through- out the period of obs~rvation,but with a high mD only at the exposed site. , with 83.33 % Fr at the exposed site and 100.00 'Yo at the sheltered one, revealed at the sheltered site a high mD. Sunamphithoe pelagica with 100.00 % Fr at both shores had an intermediate mD at the both sites. Stenothoe valida occurred almost throughout the year at both shores with an intermediate mD at the exposed and with a low mD at the sheltered site. Ampithoe ramondi, Aora atlantidea, Ericthonius brasjljensis and Tethygeneia longleyi attained 100.00 % Fr at the shel- tered site, b'ut had a lower occurrence in the exposed area, with a low mD at both sites. The Fr of Elasrnopus pectinicrus, Gammaropsis atlantica, Hyale sp. and Fig. 3. Dominance of Crustacca, Mollusca. Echinodermala, Jassa falcata was, respectively, 91.66 %, 66.66 %, Polychacta dnd 'other groups' Mar. Ecol. Prog. Ser. 5: 157-163. 1981

EXPOSED

- SHELTERED

JJ ASONOJFMAM 60- Fig. 4. Gammaridean monthly dominance at both shores

Table 2. Frequency of occurrence (Fr),mean dominance (mD;%) of gammaridean species at exposed and sheltered sites

2 0 Species mD Fr Ex- Shel- Ex- Shel- posed tered posed tered IIIIlIIIIIII LIIIIIII~III Amphilochus neapolitanus 10.87 47.67 83.33 100.00 JJbSONOJFMIM JJASONDJFMAM Ampithoe ramondi 0.37 8.29 66.66 100.00 Fig. 5. Variation in monthly dominance of Arnphilochus Cymadusa filosa 0.08 1.47 41.66 66.66 neapolitanus, Hyale media, Stenothoe valida and Sunam- Sunamphithoe pelagica 13.32 17.02 100 00 100 00 phithoe pelagica Atylus minikoi - - 8.33 Aora atlantidea 0.11 2.85 75.00 100.00 Gammaropsis atlantica 0.17 - 66.66 - sheltered shore was Arnphilochus neapolitanus (mD Tethygeneia longleyi 0.26 4.60 0.16 100.00 47.67 %), followed by Sunamphithoe pelagica (mD Elasmopus pectinicrus 1.73 ' 91.66 16.66 17.02 %) and Hyale media (mD 11.97 %). The other Hyale media 52.35 11.97 100.00 100.00 mD ranged between 8.29 % and less than 0.01 % The Hyale sp. 1.63 ' 91.66 8.33 Ericthonius brasiliensis 0.03 4.43 16.66 100.00 exposed shore was dominated by Hyale media (mD Jassa falcata 0.18 66.66 8 33 52.35 %), followed by Stenothoe valida (mD 18.85 %) Leucothoe sp. 0.01 0.07 16.66 33.33 and Sunamphithoe pelagica (mD 13.32 %). The mD of Lysianassa sp. 0.07 8.33 41.66 the remaining species ranged between 10.87 Yo and Stenothoe valida 18.85 1.36 83.33 91.66 less than 0.01 %. (mD) less than 0.01 % The patterns of monthly fluctuations of one species differ at each shore (Figs 5, 6 and 7). At the exposed site Hyale media showed the highest Da in December

91.66 % and 66.66 O/O at the exposed shore; at the and March, at the sheltered one in July and Sep- sheltered one Elasmopus pectinicrus, Hyale sp. and tember. At the exposed site the Da of Sunamphithoe Jassa falcata had a lower Fr and Gammaropsis pelagica was higher in October, at the sheltered one in atlantica was absent. Cymadusa filosa presented March. The Da of Stenothoe valida increased in Sep- 41.66 % and 66.66 % of Fr at exposed and sheltered tember and April on the exposed shore and decreased sites, respectively. A low mD was verified at both sites on the sheltered one during the whole study period. for these last 5 species. The dominant species at the Amphilochus neapolitanus revealed a minor Da on the Tararam and Wakabara: Mobile fauna of Sargassum cymosum 161

?ernygsna/o /ongleyi

Exposed

Exposed - Sheltered

111111111111IIIIIIIIIIII JJASONDJFMAMJJASONDJFMAM

Illlllllllll IIIII111111Fig. 7 Variation In monthly dominance of Hyale sp . Elas- JJISONDJFMAMJJASONDJFMAM mopus pectinicrus, Jassa falcata and Garnmaropsis atlantica Fig. 6. Varlatlon In monthly dominance of Amp~thoeramond~, Tethygeneia longleyi, Aora atlantidea and Erlcthonius (Hagerman, 1966; Hallfors et al., 1975). The reasons for brasiliensis the difference in the number of individuals collected on the two shores are difficult to explain. A number of exposed shore and on the sheltered one a higher Da in factors may have acted differentially on both shores, June and January. Ampithoe ramondi had a decreased such as the rate of sedlment deposition on the algae Da at the exposed site and the highest Da in April at (Hagerman, 1966), and variation in plant biomass the sheltered one. The remaining species showed a Da (Mukai, 1971; Hallfors et al., 1975). A detailed analysis below 30.00 % throughout the study period. The of the factors lies outside the scope of the present monthly data of Sorensen's quotient of similarity in study. Gammarldea were 60.00 % to 70.00 %; they are illus- The dominance of Gammaridea over other animals trated in Figure 8. on Sargassurn - 4 1.18 '10 at the exposed and 53.30 % at sheltered site (Tab. 1) - was conspicuous during the present study on both shores. On several types of DISCUSSION algae, Dahl (1948) records Amphipoda and Harpac- ticoidea as being dominant; for Laminaria hyperboria The number of specimens collected on the exposed Moore (1973) also found a dominance of Amphipoda. shore did not differ significantly from that on the shel- However, on Fucus serratus, Ostracoda dominate tered shore. Of the total number of animals collected, throughout the major part of the year; Lammelibran- 48.15 % (density: 6.94 ind. g-' Sargassum) were found chia only in summer (Hagerman, 1966); Nematoda in at the exposed and 51.85 % (7.34 ind. g-' Sargassum) the spring, summer and autumn; Harpacticoidea in at the sheltered site. winter (Ohm, 1964). Sheltered sites usually entertain a greater diversity The characteristic species on the exposed shore of species and fauna1 density than exposed sites (Tab. 2) was Hyale media (high mD and Fr), accom- Mar Ecol. Prog. Ser. 5: 157-163, 1981

on the exposed shore. Therefore, neither water move- ment nor the amount of sediment seem to affect species variety, but their quantity. Moreover, Sorensen's quo- tient of similarity, for Gammaridea of the two localities revealed no conspicuous differences. Different views exist with regard to the number of individuals of Gammaridea, living under different con- ditions of wave actions. Fenwick (1976) reports a lower density on a sheltered shore; Moore (1978) found no significant differences in amphipod densities; accord- ing to Gibson (1972) stomachs of fishes from the shel- tered site contained h~gherpercentages of amphipods than those from exposed localities. In our study, the Da of Gammaridea was higher on the sheltered than on the expored shore (Fig. 4), during the greater part of the study period. Increases in the number of individuals of a given species at a certain time of the year (Figs 5, 6.7),could bc due to differential reproductive activities of the species involved. Studying the life cycle of Hyale media Pereira Leite (1976) concluded that this species breeds continuously throughout the year, with two periods of intense reproduction. Pires (1977) found continuous reproduction, with peaks twice a year, in -- - Janaira gracilis. According to Thorson (1950), tropical JJDSONDJFMAM species are noted for such pattern of reproduction. Fig. 8. Annual var~ationin quotient. or s~lnllarltytor gdnlrnan- dean species on survey shores panied by Sunamphithoe pelagica, Stenothoe valida, LITERATURE CITED Amphilochus neapolitanus (intermediate mD and high Boffi, E. (1972). Ecolog~calaspects of ophiurolds from the Fr), Elasrnopus pectinicrus, Gammaropsis atlantica, phytal of S. W. Atlantic Ocean warm waters. Mar 8101 15: Hyale sp. and Jassa falcata (low mD and high Fr). On 316-328 the sheltered shore the most conspicuous species was Dahl, E. (1948). On the smaller Arthropoda of rnarlne algae, specially in the polyhaline waters off the Swedish west Amphilochus neapolitanus (high mD and Fr), followed coast. Dissertation, Lund. Unders. over Oresund 35: 1-193 by Sunarnphithoe pelagica and Hyale media (inter- Donimasnes, A. (1968). Variation in the meiofaund of Coral- mediate mD and high Fr). Finally, Ampithoe ramondi, lina offic~nalisL. with wave exposure. Sarsia 34: 117-124 Aora atlantidea, Ericthonius brasiliensis, Tethygeneia Fenwlck. G. D. (1976). The effect of wave exposure on the longleyi and Stenothoe valida, although presentin.g amphipod fauna of the alga Caulerpa brownii. J. exp. mar. Biol. Ecol 25: 1-18 low mD values, were present - except the last species - Gibson. R. N. (1972). The vertlcal distribution and feeding throughout the study period. relationships of intertidal fish on the Atlantic cudst of The same number of gammaridean species. 15 in Frdnce. J. Aninl. Ecol. 41: 189-201 both localities, ot which 14 were comnlun species, Hallfors, G.. Kangas, P., Lappalainen, A. (19751. L~llordl Benthos of the Northern Baltic sea. 111. Macrobenthos of appear to indicate that these species are well adapted the hydrolittoral belt of filamentous algae on rocky shores to life under conditions of different wave exposure. in Tavarminne. Int. Revue ges. Hydrobiol. 60: 313-333 Among phytal Gammaridea, some species avoid dis- Hdgerman. L (1966). The rndcro and microfdund dssociated placement by inhabiting tubes, others are able to hold with Fucus serratus L., with some ecological remarks. 3: on to the algae, or to swim to more secure sites during Ophelia 1-43 Moreira, P. S. (1973a). Behavioral aspects of .4rclurella storm. Tube-dwellers require building material sawayae Moreira, 1973 (Crustacea, Isopoda, Valvifera). (Moort!, 1973); however, even on the sheltered shore, Bolrn 2001. Biol. Mar. n.s. (30): 195-216 th.e small quantity of sediment available on the algae Moreira, P. S. (1973b) Food and feedingbehav~or of Arc- may have limited the variety of species. Nevertheless, turella sa wayae Morelra. I973 (Crustacea. Isopoda, Val- vifera). Boln~2001. Blol. Mdr, n.s. (30);217-232 the mD values of certain tube-builders - such as Mukdi, H. (1971).The phytal animals on the thalli of Sargas- Cymadusa filosa, Ericthonius brasiliensis, and sum serratifoliurn in the Sargassum region, with reference Amp~thoeramondi -were higher on the sheltered than to their seasonal fluctuations. Mar. Biol. 8: 170-182 Tararan~and Wakabara: ~Mob~lefauna of Sargdssunl cymosum 163

Nelson, W. G. (1979). An analvsis of structural pattern in an ndeus) Lamouroux, 1816 da Praia do Lazaro, Ubatuba, Sao eelgrass (Zostera marina L.) dmphipod community. J. exp. Paulo. M. Sc. thesis, Instiluto dr Bloci6ncias da Univer- mar. Biol. Ecol. 39: 231-264 sidade de Sdo Paulo, Brdsil Nonato, E. F., Peres, J. M. (1961). Obsrrvat~onssur quelques Montouchet, P. E. G. (1979). Sur la communaute des anllnaux peuplements intertidaux substrat dur dans Id 1.6g1on vagiles associes a Sargassurn cymosum C. Agardh, h d'ubatuba tat de SSo Paulo). Cah. Biol, rlldr 2 (3): Ubdtuba, Etat de Sao Paulo, Bresil. Stud. neotrop Faund 263-270 Env~ronnl.14: 33--64 Ohrii, G. (1964). Die Besledlung der Fucus-zone ~ierK~eler Moorc, P. C. (1971). The nematode fauna associated w~th Bucht und der westlichen Ostsee unter besonderer holdfdst of kelp (Lamlnaria hyperborea) in North-East Berucksicht~gung der Mikrofauna. Kieler Meeresforsch Britain. J. mar. biol. Ass. U.K. 51. 589-604 20: 30-64 Moore, P. G. (1973). The larger Crustacea associated w~th Pereira Leite, F. P. (1976). Estadlos de crescimento e aspectos holdfasts of kelp (Laminar~ahyperborea) in North-East da reprodu~dode Hyale med~a(Crustacea, Amphipodd, Britain. Cah. Biol. mar. 14 (4): 493-518 ) da fauna vagil de Sargassum cyrnosum. M. Sc. Moore, P. G. (1978).Turbid~ty and kelp holdfast Arnphipoda. thesis, Instituto Oceanografico da Universidade de Sao I. Wales and S.W. England. J. exp. mar. Biol. Ecol. 32 (1): Paulo, Brasil 53-96 Leite, Y M. R. (1976). Aspectos ecologicos do fital da Pires, A. M. S. (1977). Ciclo reprodutivo e flutua~aoanual da Halimeda opuntia (Linnaeus) Lamouroux. M. Sc. thesis. popula~aode Janaira gracilis (Crustacea, Isopoda. Asel- Instituto de Biocigncias da Universidade de Sao Paulo, lota). Bolm Inst. oceanogr S. Paulo 26: 201-217 Brasil Southwood, T R. E (1958). Ecological methods, Methuen. Lima, H. S. (1969). Fauna sessil do Sargassum cyrnosum da London Praia do Lamberto, Ubatuba (Estado de SAo Paulo): com- Thorson, G. (1950). Reproductive and larvae ecology or posicio qualitativa e considera~dessobre a localiza~ao marine bottom invertebrates. Biol. Rev. 25 (1): 1-45 das especies na planta. M. Sc. thesis, Instituto Oceanog- Truchot, J. P. (1963). Etude faunistique et ecologique des rafico da Universidade de Sao Paulo, Brasil Amphipodes des faunes rocheaux intertidaux de Roscoff. Masunari, S. (1976). 0 fital de Amphjroa fragilissima (Lin- Cah. B~ol.mar 4: 121-176

This paper was presented by Professor R. L. Haedrich; it was accepted for printing on January 28, 1981