ANNALES - Ser. hist nat. • 9 • 1999 • 2 (17) original scientific paper UD C 593(262.3-17)(26.3) SEASONAL AN D LONG-TERM VARIABILITY OF MEIOFAUNA IN THE ENVIRONMENT FREQUENTLY AFFECTED BY HYPOXIA IN CENTRAL PART OF THE GULF OF TRIESTE Borut VRISER & Aleksander VUKOViC National institute of Biology, Marine Biological Station, Sl-6330 Piran, Fornafe 41 ABSTRACT The article deals with benthic meiofauna studied for three years in central part of the Culf of Trieste. The obtained results present meiofauna's seasonal reproduction cycles and long-term trends in these cycles. The seasonal dynamics was in positive correlation with thermal conditions and salinity, and in negative correlation with oxygen and phytoplankton's chlorophyll in the bottom-water layer. A 2-month lag in meiofauna's dynamics was noted behind phytoplankton's seasonal cycle (spring and autumn blooms), while at a long-term scale a 3-year trend ofgrowth in meiofauna's mean yearly abundances was observed. Key words: seasonal dynamics, benthic meiofauna, Gulf of Trieste INTRODUCTION Meiofauna's seasonal dynamics is one of most often investigated topics as far as benthic fauna is concerned. The situation is quite different when dealing with long-term changes in meiofaunal communities, which have been studied to a much lesser extent, particularly peri­ods exceeding one year. Such up to ten years lasting studies have been presented in various works, e.g. by Coull (1985, 1986), Eskin & Coull (1 987), Rudnick et al. (1985), in contrast to numerous one year long investiga­tions in coastal environments comparable with our coastal waters (e.g. Bovee & Soyer, 1974; Harris, 1972). investigations were repeated during the 1996-1999 pe­riod. For financial reasons the research was somewhat limited although still carried out on the basis of similar methodology and with equal aims: to investigate sea­sonal dynamics of the total meiofauna and its main groups, to ascertain the impact of common and separate ecological factors of the physical environment on meiofauna in normal as well as in potentially hypoxic conditions, and to detect eventual signs of long-term oscillations or cycles. METHODS The research on meiofauna occurring in the Slovene part of the Gulf of Trieste has been till now focused on both topics, i.e. on its seasonal dynamics as well as on its long-term changes, in the latter we were involved for the first time in the 1992-1995 period, namely in con­nection with elsewhere poorly researched impacts of the lack of bottom-water oxygen (hypoxia and anoxia) on meiobenthos. The results of this research (Vriser, 1996a, b, 1997) have shown an unexpectedly great meiofaunal variability, trophic links of its seasonal cycles with pelagic and benthic microflora, as well as its fairly contradictory and diverse response to fortnightly hypoxic conditions in autumn 1994. As the results have also indicated a need for a long-term monitoring, the The meiofauna was sampled with monthly frequency in the years 1996, 1997 and 1998 in the same area as during the 1992-1995 period, i.e. in the centre of the Gulf of Trieste, 25 m deep. As a result of the troubles with the research vessel and unfavourable weather conditions, no sampling was carried out from January to April 1996, in June 1997 and from November to De­cember 1998; no data are therefore available for these months. Surface sediment containing meiofauna was taken with gravity core sampler (Meischner & Rumohr, 1974), 5 cm deep, always with three replicates. Meiofauna was extracted from fixed samples (5% formalin) by sieving 203 Borut VRIŠE R & Aleksander VUKOVlC : SEASONA L AN D LONG-TER M VARIABILIT Y O F MEIOFAUN A 203-208 2j s j —— — O . ^^ 3 dj H i " 1996 o • 1997 -­ tw s .a \ ÜJ i c !_ . i JAN FEU WP APR syvf JUN JUL A ^ SÉP OC7 MC'V 0L C JAN FEB MAR APR t-Wf JW J'u c WG SEP (XT HCV DEC JAN FEB P.'AH M*Y .'UN JUL FUG SE ? iX T fiOV Ci C Fig. 1: Three year bottom - water layer dynamic (phy­sical and chemical parameters) of the investigated area. Si. 1: Triletna dinamika fizikalnih in kemijskih para­metrov v pridnenem vodnem sloju raziskovanega ob­ mčja. and decantation (Wieser, 1960), identified to major taxa, counted and statistically processed (Statsoft, Statistica 5.0). Meiobenthic sampling was accompanied by physical and chemical measurements (temperature, salinity, oxy­gen) and measurements of chlorophyll biomass (Chi a) of the bottom- water layer, carried out with electronic fine-scale prophyler. A more detailed description of the used methods and a chart of the study area has been presented in one of the earlier papers (VriSer, 1996a). Due to drastically reduced financial support we were compelled to make use of gravity core sampler instead of carrying out manual sampling by SCUBA technique (as in the 1992-1995 period). Thus we had to give up the originally planned monthly measurements regarding the concentrations of benthic algae, sedimentation and the content of organic matter, and chemical characteris­tics of pore water of the sediment. RESULTS Ecological characteristics of the investigated area The dynamics of the 3-year physical and chemical parameters is presented in figure 1. At the time of sam­pling, the seasonal oscillations of temperatures in the bottom-water layer ranged from the lowest winter values in February (8.5 - 9.5°C) to the highest summer values (18 - 21°C) with mean three-year temperature of 14.1 °C. The seasonal salinity oscillations showed expected raised values in the drier months of winter (December ­February) and summer (July - September) and low values in the rainy months of spring (especially April 1997) and autumn {especially October 1996 and 1997). At the av­erage salinity of 37.5%o, the measured extreme values ranged between 35.1 and 38%». Three-year movements of the oxygen content at the bottom showed a stable winter-spring period (January ­April) of high values (90 - 100% saturation), a lower content (75%) in summer (june - July), and even lower content (70% or less) in early autumn when only 35% concentration of oxygen was measured in August 1997 and in October 1997 and 1998. The mentioned autumn mínimums indeed neared hypoxic conditions, but the oxygen concentrations did not fall below the marginal value of 2 rng/1. The sediment of the investigated station belongs, in geological terms, to silts situated between clayey silts of the coastal belt and siity sands of the open waters of the Gulf of Trieste. Granulomere structure: 65% silt, 25% clay, 10% sand (Ogorelec etaL, 1991). Average amounts of the chlorophyll biomass (chlorophyll a) of the bottom pelagic microflora indi­cated periods of increased values in spring and autumn maximums: 1.9 mg/l in May and 4 mg/l in November. The latter was merely a statistical reflection of an ex­tremely intensive algal bloom in autumn 1998. Meiofauna Structural and quantitative characteristics of the in­vestigated meiofauna, i.e. its taxonomic structure (main groups and its abundance) are given, in the form of a summary statistical survey, in table 1. The dominant group (75% relative density) was represented by Nema­toda, followed by Harpacticoida (12%) and Polychaeta (7%), while the following 12 groups (Turbellaria, Gastro­poda, Bivalvia, Kinorhyncha, Acarina, Hydroidea, Ostra­coda, Ophiuroidea, Amphipoda, Mysidacea, Cumacea, Decapoda) represented 6% of the entire meiofauna. Seasonal dynamics of some more abundant meio­faunal groups are shown by diagrams of annual abun­dances (Fig. 2). The great majority of the groups showed low winter and high summer abundances. Characteristic 204 Borut VRIŠE R & Aleksander VUKOVIČ : SEASONA L AN O LONG-TER M VARIABILIT Y O E MEtOfAUN A 203-20« Tab. i: Three year meiofauna abundance. Tab. 1: Pregled triletnih abundančnih vrednosti meiofavne. TAXA tota! meiofauna Mean No./lO cm2 478.96 Rei. abundance % 100.00 Range No./10 cm3 44 1338 S D of mean No. 296.95 SE of mean No. 31.30 Nematoda 361.29 75.43 16 1051 218.91 23.08 Harpactícoida Poiychaeta Turbeílaria 57.19 35.09 10.63 11.94 7.33 2,22 "" 130 237 114 49 93.95 25.15 9.50 5.69 2.65 1.00 Gastropoda Bivalvia 4.53 4.20 0.88 0.80 00 5 37 1.07 7.15 0.11 0.75 Kinorhyncha Acarina 2.77 0.50 0.58 0.28 00 21 3 4.42 0.52 0.47 0.05 Hydroidea Ostracoda 0.49 0.41 0.22 0.11 00 7 23 1.29 5.18 0.14 0.55 Ophiuroidea Amphipoda Mysidacea C ii macea 1.36 1.34 1.04 1.03 0.07 0.04 0.00 0.00 0000 30 4 1 1 4.01 0.78 0.11 9.48 0.42 0.08 0.01 1.00 Decapoda 0.02 0.00 0 1 0.15 0.02 Fig. 2: Seasonal changes (1996, 97, 98) of some Si. 2: Sezonske spremembe (1996, 97, 98) posameznih meiofaunal groups. Abundance as mean (No.ind./ skupin meiofavne. Abundanca kot srednja vrednost 10cm2) or sum of 3 replicates (No.ind./30 cm2). (St.os./IOcm2) ali vsota osebkov (Št.os./30cm2) treh paralel k. 205 BOrot VR1ŠER & Aieksandcf V U K O ViČ : SEASONA L AN D LONG-TER M VARIABILIT Y O F M El O F AU N A ..., 203-208 of the annual abundance cycle of the dominant Nema­toda was a distinct summer peak (July), followed by somewhat weaker maximum in autumn (September). The winter Nematoda maximum lasted from December to March. Harpacticoida reached the summer maximum in July and August. This was followed by a decrease to the autumn stagnation (October, November), and this by an explicit winter-spring depression from December to April. Seasonal development of Polychaeta showed a summer increase in density with the peak in August (the few rare deviations can be assessed as atypical). Meiofauna's long-term trends were monitored with an estimate of mean annual abundances for the 3-year 1996-1999 period (Fig. 3). In the entire meiofauna and in the first three leading groups the abundance was on the increase in this period. While a more distinct rise was noted in Nematoda and, consecutively, in the entire meiofauna in the 1997-1998 period, the mean annual abundance in Harpacticoida and Polychaeta was on the increase largely in 1996-1997. Tab. 2: Pearson's correlation coefficients for meio­faunal taxon correlations with temperature, salinity, oxygen and phytoplankton (Chi a). Tab. 2: Pearsonovi korelacijski koeficienti taksonom­skih skupin meiofavne s temperaturo, slanostjo, kisikom in fitoplanktonom (Chi a). TAXA temperature salinity oxygen chlorophyll a Meiofauna +0.66 * -0,02 -O.54X -0.16 Nematoda +0.6?x -0.05 -0.50x -0.1 fl Harpacticoida +0.66 +0.00 -O.55X -Ü.01 Polychaeta +0.65 * +0.07 -0.69* -0.20 Turbeilaria +0.47 * -0.05 -0.24 -0.14 Gastropoda +0.55 * +0.16 -0.20 -0.16 Bivalvia +0.53 * +0-20 -0.31 -0.08 Kinorhyncha +0.42x -0.07 -0.24 -0-02 Acarina +0.35 +0.23 +0.06 Hydroidea +0.23 +0.14 +0.15 -0.08 Ostracoda +0.33 -0.07 -0.01 -0.07 Ophiuroidea +0.34 +0.03 -0.47x -0.13 Amphipoda +0.51x +0.11 -0.25 +0.21 Mysidacea +0.15 +0.05 +0.01 Cumacea +0.30 +0.23 -0.24 -0.05 Decapods +0.2 7 +0.02 -0.44* +0.13 sign, at p < 0.05 The relation between the selected ecological factors (temperature, salinity, oxygen, chlorophyll a) and meio­fauna was checked with Pearson's correlation coefficient (Tab. 2). The coefficients show predominantly positive correlation of the entire meiofauna and its groups with temperature and salinity, while the correlation with the chlorophyll biomass and oxygen content is negative. The mean 3-year course of the seasonal cycle of the bottom plankton microflora (microphytopelagic biomass Mean annual abundance of the enure meiofauna Wean annua! abundance - NEMATODA Mean annual abundance - HARPACTICOIDA Mean annual abundance - POLYCHAETA S20 «o JJÇ «o 2:0 540 Fig. 3: Yearly mean abundances (+-SE) of total meio­fauna and some dominant groups. SI. 3: Srednje letne abundance (+-SE) celotne meio­favne in nekaj vodilnih skupin. - chlorophyll a) and meiofauna is shown in figure 4. The 1996-1999 Nematoda abundance curve is, very much as noticed during the earlier investigations in 1992­1995, to a certain extent a repetition of the changes in the chlorophyll biomass, this time with even greater (2­month) lag. Thus the Nematoda follow algal blooms in March and May with successive maximums in May and July, while the smaller algal increase in August is prob­ably reflected in somewhat slowed down decrease in the Nematoda abundance in September and October. At the end of the research period in December the meio­fauna did not yet respond to the exceptionally intense autumn phytoplankton blooms in November 1998. Har­ 206 ANN ALES • Ser. hist, nat . • 9 • 1999 • 1 (15) Borut VRIŠE R & Aleksander VUKOVIČ : SEASONA L AN D LONG-TER M VARIABILIT Y O F M El O F AU N A ..., 203-208 pacticoida reached the summer maximum, the same as Nematoda, in |uiy, two months after alga! blooms (in May), while in the sparse Polychaeta the seasonal lag seems less distinct. 603 [ — 1 ­ ^ I ^ N=MATODA a , a HflRPACriCOIDA / \ , . . — — —I 0 JAM PSB MAS APR MAy JUN JUS. AUO SEP OCT MOV fJIÍC Fig. 4: Three year mean seasonal dynamic of dominant meiofaunal groups and phytoplankton (Chi a). SI. 4: Triietna srednja sezonska dinamika freh vodilnih skupin meiofavne in fitoplanktona (Chi a). DISCUSSIO N The results of the investigations carried out from 1996 to 1999 on seasonal and long-term meiofaunal variations in central part of the Gulf of Trieste showed fairly similar qualitative relations, seasonal cycles and the impacts of the ecological factors as some previously investigations in the same place in 1992-1995. As quantitative changes (by a third lower abundances) manifested themselves for already mentioned methodo­logical reasons (sampling with gravity core instead of by diver), no direct comparisons between absolute abun­dances of both periods are possible. - Meiofaunal seasonality more or less confirmed the previously obtained characteristics, especially as far as most abundant groups are concerned, and less in re­spect of rarer species, where some greater "anomalous" deviations from seasonal pattern were noted. This prob­lem, however, could be solved only with a selective sampling of substantially larger series of samples. In Nematoda, Harpacticoida and Polychaeta their distinct summer culmination (particularly in July) follows the spring phytoplankton blooms (in May), in Nematoda a slight autumn rise is perceived after the July peak, which is also notable in Harpacticoida and especially in Polychaeta - in 1997, for example, very distinctly, and in other years very scantily. The three-year observations thus confirmed and more or less clarified the picture of seasonal changes in the investigated groups of the stud­ied fauna. The response of meiofauna to some ecological fac­tors was similar to that in 1992-1995: positive Pearson's correlation coefficients with temperature and salinity, and negative coefficients with the oxygen content and pelagic chlorophyll. A special attention as far as the ecological factors are concerned deserves to be given particularly to plankton chlorophyll, especially in its re­lation to meiofauna. The already mentioned trophic links between meiofauna and primary producers (Vriser, 1996) have been described by many studies (Blanshard, 1990; Fieeger et ai, 1989; Grant & Schwinghamer, 1987; Montagna eta!., 1995; Rudnick ef ai, 1985). In comparison with a one-month lag of meiofauna behind seasonal blooming cycle of benthic one-celled algae (as shown by a few years old data), the processes of sedimentation, accumulation and decomposition from one-celled pelagic algae into bacterial agglomera­tions and bottom organic detritus are probably respon­sible for a similar but greater two-month lag of the meiofaunal cycle behind the rhythm of phytoplankton. To confirm this thesis, a carefully planned and distinctly lasting study of simultaneous monitoring of environ­mental phytoplanktonic, phytobenthic and meiofaunis­tic components would be needed. As no true hypoxic conditions occurred in the re­search period, this phenomenon could not be investi­gated anew. The oxygen level was therefore not critical even for hypoxically sensitive macrobenthos. From our earlier investigations as well as from literature (Dauer & Alden, 1995), a substantially greater meiobenthos' abil­ity to survive in hypoxic conditions is known. The seemingly illogical meiofauna's negative corre­lation with oxygen and phytoplankton chlorophyll is explainable with meiofauna's phase or seasonal lag: the curves of meiofauna, especially Nematoda, and of both ecological factors are almost in alternation! We interprete our results that the seasonal cycles of meiofauna in the investigated area are directly con­trolled particularly by temperature, by oxygen more or less periodically in stressful hypoxic conditions, and in­directly and thus behind time by phytoplankton through complex processes of sedimentation and decomposition in direction from pelagic to benthic trophic levels, most probably in combination with other mechanisms, such as competition and predation. Although the changed sampling methodology pre­vent us, as already said, to make direct comparisons with earlier abundances, the yearly mean values of the key groups and the whole show a 3-year rising trend in the meiofauna's abundance. This trend upwards indicate, in connection with the 3-year trend of decline established during earlier investigations, a first possible trace of long-term oscillations hiding behind the "curtain" of seasonal dynamics. For a clearer picture, at least a 10-year continued observations would be necessary. For this very reason and for the sake of other already mentioned open questions, we shall resume the investi­gations in this particular sphere. 207 Boru! VRtŠE R & Aleksander VUKOVIČ : SEASONA L AN D IONG-TER M VARÍA8IUT Y O F MEIOFAUN A ..., 203-20 8 SEZONSK E I N VEČLETN E SPREMEMB E MEIOFAVN E V OKOLJ U POGOST O PRIZADETI M S HIPOKSSJAM I V OSREDNJE M DEL U TRŽAŠKEG A ZALIV A Borut VRIŠER & Aleksander VUKOVIČ Nacionalni institut za biologijo, Morska biološka postaja, Si-6330 Piran, Fornače 41 POVZETEK V triletnem obdobju 1996-99 smo z mesečno frekvenco raziskovali meiofavno v centru Tržaškega zaliva. Rezultati študije, ki je nadaljevanje starejših raziskav iz let 1992-95, so pokazali podobno sezonsko dinamiko in vpliv nekaterih ekoloških faktorjev na meiofavno. Prevladovali so Nematoda s 75% relativne abundance, sledili so Harpacticoida (12%) in Polychaeta (7%), preostalih 12 skupin je predstavljalo skupno 6%. Raziskave so nekoliko izostrile in dopolnile dosedanje poznavanje sezonskih sprememb meiobentosa, ki pri vodilnih skupinah kaže izrazito povišane poletne gostote in manjši jesenski maksimum. Opazili smo dvomesečni časovni zamik sezonskega cikla meiofavne za letnim ciklom fitoplanktona. Časovna razlika morda ustreza procesom sedimentacije in razgradnje fitoplanktona v organski detrit sedimenta kot pomembnega prehranjevalnega vira meiofavne. V raziskovanem obdobju nI bilo hipoksičnih razmer. Srednja enoletna povprečja celotne meiofavne in vodilnih skupin kažejo triletni trend naraščanja abundanc in tako sledijo triletnemu trendu upadanja, vidnega iz starejših opazovanj. Ključne besede: sezonska dinamika, bentoška meiofavna, Tržaški zaliv REFERENCES Blanshard, C . F. 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