Existence and significance of Acartia grant resting eggs (Copepoda: Calanoida) in sediments of a coastal station in the Alboran Sea (SE Spain)

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1 Journal of Plankton Research Vol.2 no.2 pp , 1998 Existence and significance of Acartia grant resting eggs (Copepoda: Calanoida) in sediments of a coastal station in the Alboran Sea (SE Spain) Francisco Guerrero 1 and Valeriano Rodriguez Departamento de Ecologia, Facultad de Ciencias, Universidad de Malaga, Campus Teatinos s/n, 2971 Malaga, Spain 1 Present address: Departamento de Biologia Animal, Vegetal y Ecologia, Facultad de Ciencias Experimentales, Universidad de Jaen, Paraje Las Lagunillas s/n, 2371 Jaen, Spain Abstract. The seasonal abundance of copepod eggs in bottom sediments of Malaga harbour was documented during an annual cycle between June 1989 and June 199. The concentration noted ranged from 6.6. x 1* to.19 X 1* m~ 2. The number of adults in the water column and eggs recovered from the bottom sediments fluctuated markedly with season. The highest egg abundance in sediments was found coincidentally with the early population growth season, although the values remained high until the adults disappeared from the water column. During the winter, the number of eggs decreased until the development of the next copepod population. When bottom sediments were incubated in the laboratory, a large number of Acartia nauplii hatched, which showed that eggs laid in the autumn remain viable at the bottom until late spring, thus providing a large pool of potential recruits for the planktonic population. Introduction Copepods living in fluctuating coastal ecosystems can disappear from the plankton when environmental conditions become unfavourable for growth and reproduction. Advection of individuals from offshore and dormancy are the two main mechanisms to ensure the perpetuation of these copepods in the ecosystem (Grice and Marcus, 1981; Hairston and Munns, 1984; Levin et al, 1984; Taylor and Spalding, 1988). Consistent with this, the production of resting eggs by small copepods that inhabit shallow temperate waters [see references in Uye (1985)] has become increasingly evident. It is commonly accepted that these stages make up part of the life history of many freshwater and marine copepods, and play an important role in the succession of copepod species in these waters (Kasahara et al, 1974). Recently, the existence of a viable egg bank representing a potentially important source for recruitment of nauplii into the plankton has been suggested (De Stasio, 1989; Marcus et al, 1994). Malaga harbour (South Spain) is a shallow, semi-isolated environment where copepods inhabiting the water enclosure are mainly of the genus Acartia. Three species of copepods of the genus Acartia co-exist in Malaga harbour: A.clausi, A.discaudata var. mediterranea and A.grani. Acartia grani is the dominant copepod species of the group. In a previous paper, Rodriguez and Vives (1984) showed that this species disappears from the water column during a portion of the year and appears again when favourable conditions are re-established. This Oxford University Press 35

2 EGoerrero and V.Rodriguez pattern of appearance-disappearance and the absence of this species in offshore waters (Rodriguez, 1979) suggest the existence of a benthic resting phase that ensures the species' persistence in the system every year. Such a hypothesis is supported by previously published work on the presence of resting eggs in the families Acartiidae, Pontellidae and Centropagidae, among others (see Kasahara etal, 1974; Johnson, 198; Uye, 1985; Marcus, 1991; Naess, 1991; Belmonte, 1992; Belmonte and Puce, 1994). All this stresses the importance of this mechanism as a suitable overwintering strategy that allows planktonic populations to survive adverse pelagic conditions. The aims of this work were: (i) to confirm the presence of calanoid copepod eggs in Malaga harbour sediments; (ii) to analyse the coupling between the abundance of copepod eggs in the bottom sediments and the occurrence of naupliar, copepodite and adult planktonic stages; (iii) to elucidate the status of eggs (subitaneous versus dormant) present in the sediment as an overwintering strategy in the calanoid copepod A.grani. Method Samples were collected weekly between June 1989 and June 199 at a station in Malaga harbour (South Spain) over 1 m-deep sea-bed sediments. Temperature was measured with a YSI Model 57 monitor at depth intervals of 1 m throughout the entire water column. On each sampling date, quantitative zooplankton samples were taken by means of a short vertical haul from 7 m to the surface, using a 1 urn mesh plankton net. The samples were fixed immediately with formaldehyde to a final concentration of 4%. In the laboratory, the plankton samples were analysed to estimate the number of nauplii, copepodites and adult stages. The scanning criterion was to count at least 2 individuals of the most abundant developmental stage. Samples of sediments were collected with an Eckman-Birge dredge (chamber dimensions 152 X 152 X 229 mm). Three sediment subsamples were extracted from the dredge in 2.8-cm-diameter Plexiglas tubes while the dredge was submerged just below the sea surface. Once the supernatant water was eliminated with an aspirator, the undisturbed samples were stored in cold conditions, transported to the laboratory and processed within 4 h of collection. We used an ultrasound treatment (Marcus, 1984) to isolate the eggs present in the first centimetre of sediment, as follows. The sample was sieved through a 2 urn mesh screen and the filtrate was sonicated in an ultrasound bath for 1-15 min. Then, the sample was sieved again through a 45 urn mesh screen and the retentate was fixed with formaldehyde to a final concentration of 4%. The retentate was studied within a period of 5 months from collection to determine the number of eggs per square metre. To elucidate the presence of resting eggs in the sediment, irrespective of their diapause or quiescent status, and to test the hatching response to temperature as an environmental trigger, we carried out an in situ incubation-laboratory experiment. Fourteen cores of sediment were collected by a scuba diver in December 199, when the abundance of copepods in the water column was <1 individual I" 1. 36

3 Copepod resting eggs in AJboran coastal waters Immediately, the first centimetre of sediment was placed in 1 ml incubation flasks covered with a 2 um mesh screen and filled with filtered seawater. The 14 flasks were incubated in situ at.5 m above the bottom. About every 1 days, a flask was retrieved at random and, in the laboratory, we checked for the presence of nauplii in the supernatant, which never occurred except for the last sampling date. Then, theflaskswithout nauplii were gradually warmed from the in situ temperature to 18 C at a rate of 1 C day 1, in order to determine whether the eggs present in the sediment samples were able to hatch in optimal temperature conditions. Eighteen degrees Celsius is the typical temperature at which Acartia species increase their population abundances in this area and, particularly, the temperature at which A.grani exhibits the highest egg production rate (Rodriguez and Vives, 1984; Rodriguez et ai, 1995). After 72 h at 18 C, the number of nauplii that appeared in the supernatant was determined. Results Water temperature in Malaga harbour ranged from 15 C in winter to 25.5 C in mid-summer (Figure 1A). Temperatures showed marked short-term fluctuations during the summer, but due to the shallowness of the water column, the differences between surface and bottom layers were not so marked. The abundance of planktonic stages of Acartia also varied strongly with season, as previously reported by Rodriguez and Vives (1984). The number of nauplii, copepodites and adults decreased from maximum values in the summer period (July-August) to minimum values in the cold season (Figure IB). The number of eggs recovered from the sediment varied coupled with the seasonal change in the planktonic populations: highest densities in the summer-autumn period (September-October) and the lowest just before the resurgence of the planktonic copepod population in the water column (Figure 1C). We found a positive Pearson's correlation between both variables during the annual cycle (r =.59; P -.2), which indicates the covariation of resting egg abundance; the number of adults in the water column at some times of the year, as much as the population size with resting eggs at other times of the year. The Acartia planktonic populations (nauplii to adult stages) ranged from 288 ind. I" 1 in July-August to 3 ind. I" 1 in March. The average egg abundance in the sea-bed sediment declined gradually from a maximum of 6.6 X 1 6 eggs nr 2 in September-October to minimum values of.19 X 1 6 eggs nr 2 in May. Table I shows the number of nauplii hatched from the in situ incubated sediments and the temperature values at this time. Although we have not quantified the initial number of eggs in sediment, this experience shows that eggs present in the bottom sediment were capable of hatching after incubation at appropriate temperatures even several months after spawning. So, eggs collected in December could survive for >5 months in the sediment and only hatched to the nauplii stage in situ or in the laboratory conditions when temperatures reached 18 C. Thus, the temperature of 18 C seems to be favourable for leaving the dormancy phase. Prior to this experiment, we identified two morphological types of eggs, spiny 37

4 F.GaeiTero and V.Rodnguez o o CD 2 O Q. E NAUPLII NAUPLII + COPEPODITES + ADULTS > 73 C E 3 CD O O) O) CD <D S O N D J F M A M Fig. "L Seasonal variation in temperature values in the water column (A), abundance (ind. I" 1 ) of Acania planktonic stages (B) and abundance of eggs (egg nr 2 ± SD) in the bottom sediments (C) during the period of study. 38

5 Copepod resting eggs in Alboran coastal waters Table I. Temperature values in the water column and number of nauplii that hatched at in situ conditions and after warming to 18 C (increment rate 1"C day 1 ) for 72 h Days after sample collection Nauplii in situ 166 Nauplii after heating Water temperature ( C) and smooth, in the sediment using scanning electron microscopy (Guerrero, 1993). Spiny diapause eggs of Acartia can be distinguished from smooth subitaneous ones of the same species just by using light microscopy (Belmonte, 1992; Belmonte and Puce, 1994). However, it is only under electron microscopy that a reliable distinction between diapause and subitaneous eggs can be achieved, based on the morphology of the thick outer chorion (Ianora and Santella, 1991; Hairston and Van Brunt, 1994). However, the egg abundance was measured in this study using a stereomicroscope lens and, thus, we could not distinguish between both egg types during the regular countings. In consequence, we were not able to calculate the percentage for each type of eggs during the sampling period. The nauplii that emerged from the sediment samples were members of the Acartiidae. We did not carry out incubations to allow them to reach the adult stage, but they could be identified as A.grani based on the facts that (i) this species was numerically dominant during a great part of the year (on average it accounts for 7 ± 26% of the adult copepod abundance) (Figure 2) and (ii) the nauplii found after the incubations showed a close morphological similarity with the nauplii of A.grani described by Vilela (1972) as well as with the nauplii of the same species that we had obtained in previous laboratory experiments. Discussion Most calanoid copepod species spawn their eggs freely into the water column and, in shallow systems, it is easy for many of them to reach the sediment prior to hatching. In our case, the A.grani eggs could reach the bottom in only 5 h (value estimated in laboratory conditions: 25 C and 36.4%o; Guerrero, 1993). The presence of calanoid copepod eggs in sediments is well documented in the literature (see, for example, Kasahara et ai, 1975; Marcus, 1984; Naess, 1991), although it is lacking for our geographical area. The calanoid copepod A.grani has been found 39

6 F.Guerrero and V.Rodrignez 3 O 8 D I A.dau8l Q A. (Sscaudata B A.grani 'j 'A 'S 'O 'N 'D 'J 'F 'M 'A 'M 'J Fig. 2. Total abundance (ind. I- 1 ) of adult copepods and abundance (percentage) of the three Acartiidae species that co-exist in Malaga harbour. in several semi-isolated coastal environments of Spain (see, for instance, Alcaraz, 1977; Villate, 1982; Rodriguez and Vives, 1984), but direct evidence of the presence of dormant resting eggs had not been reported before. The pattern of the seasonal changes observed in this study for the abundance of adults and copepodites of Acartia species and of their eggs in the bottom sediments is similar to that reported in the literature for marine cladocerans (Onbe, 1985) and marine copepods (Kasahara et al, 1975; Uye, 1982; Naess, 1991; among others). Our results on egg abundance (.19 to 6.6 X 1 6 eggs nr 2 ) also fell in the same range or were higher than those previously reported for shallow neritic waters. Thus, Kasahara et al. (1975) reported 3-1 X 1 6 eggs nr 2 in the Inland Sea of Japan, while Naess (1991) obtained between 3.3 X 1 5 and 1.6 X 1 6 eggs m- 2. Marcus (1991) reported 4.2 x 1 5 to 7.8 x 1 4 eggs nr 2 in a subtropical estuary. The peak of egg abundance found during the summer-autumn period can be explained by the high in situ egg production rates from copepods that are found in this ecosystem in the same season (Rodriguez et al., 1995). This, in turn, depends mainly on the in situ food condition variability (Runge, 1985). At this time, eggs spawned are mainly subitaneous (Grice and Marcus, 1981), which hatched in a few days and are responsible for the recruits of nauplii into the plankton. Rodriguez et al (1995) observed in the same system, in August, that 89% of eggs produced hatched in h. At the end of this period, just before the decrease in the planktonic populations, we detected a second peak in the number of eggs in the sediment that 31

7 Copepod resting eggs in AJboran coastal waters does not give rise to new planktonic populations. Two explanations can be suggested: (i) most eggs of the second peak were non-viable eggs such as those described in Ban et al (1997) or (ii) they were resting eggs. Nevertheless, we observed a high viability (high percentage of eggs hatched) in experiments carried out during the cold season (November) of the same year (Rodriguez et al, 1995). This contradictory result is only apparent if we take into account that even though resting eggs are produced at a greater cost than subitaneous ones, the former are produced more rapidly than the latter (Watras, 198). This rapid production of resting eggs might facilitate their colonization of the benthos during periods of stress. In addition, this second egg peak is quite important for the notion of a seed bank (De Stasio, 1989; Marcus et al, 1994). Once the number of adults in the water column becomes consistently low, the total egg production must also be low. Then, the number of eggs in the sediment begins to decrease during a period of 2-3 months until it reaches a very low steady value. In addition to the fact that there are fewer females producing eggs at this time, the decrease in the abundance of eggs in the sediments can be related to a loss by hatching, predation by invertebrates (Onbe, 1985), decomposition by microorganism (Marcus and Fuller, 1986), bioturbation (Marcus, 1984; Marcus and Gengebach, 1986), resuspension and transport of the sediment (Lindley, 199), prolonged exposure to low oxygen and ambient SH 2 (Uye et al., 1984), or other reasons. The results obtained in this research show that, even taking into account the loss mechanisms mentioned above, the presence of eggs in the sediment of the studied system plays a decisive role in the life cycle of A.grani, providing this species with a suitable overwintering strategy. Tranter and Abraham (1971) suggested that a benthic diapause phase might be the basis of the seasonal replacement of several Acartia species in the Cochin backwater in India, and the same idea was pointed out by Villate (1982) in ria of Mundaka (Spain) and by Rodriguez (1981) in our own study system. In the same way, Marcus (1991) suggests that the presence of resting eggs in the sediments is an important source of recruits for the planktonic population, especially during the spring. Our results show that the eggs collected from the sediment, of unknown age, hatch when the temperature rises to 18 C, even 5 months after being collected. There is no direct proof that eggs are dormant, but the fact that the eggs that remained in sediments responded to the temperature increment indicates that they can be diapause eggs. This evidence indicates that this species can repopulate the water column from resting eggs in sediment. Environmental factors influencing the induction of resting egg production in A.grani have not been elucidated yet, but it seems that temperature is the controlling factor of this behaviour in Acartiidae (Uye and Fleminger, 1976). Results obtained in this study seem to confirm this idea, but in any case, some other factors may be also responsible for the induction of the spawning of resting eggs. For instance, Uye (1985) found that the seasonal photoperiodic variation is an inducer of diapause egg production in A.clausi, and similar results were shown by Marcus (198,1982) in Labidocera aestiva. Ban (1992) showed that the type of eggs spawned by Eurytemora affinis is determined by the environmental conditions experienced by the 311

8 F.Guerrero and V.Rodriguez females during the nauplii stage. Again the photoperiod is the first inducer for resting egg production, together with low temperatures and high densities of individuals. The same author found that egg dormancy in E.ajfinis may be an adaptation to avoid food shortage, and the same phenomenon was found in the copepod Onychodiaptomus birgei by Walton (1985). In our analysis, the chlorophyll a concentration was very low during the period when A.grani disappeared from the water column. Rodriguez et al. (1995) found that when the temperature decreases below 18 C, and with the lowest chlorophyll a concentration, the egg production rate is always <5 eggs female" 1 day 1. Therefore, the elucidation of factors that influence the induction, maintenance and termination of copepod resting eggs is critical to achieve a better understanding of the population dynamics of the zooplankton. In conclusion, the presence and hatching of eggs in the sediments seems to be an indicator of their importance in the overwintering strategy for A.grani. The accumulation of viable eggs in the sediment, as put forward by some authors (De Stasio, 1989; Marcus et al., 1994), may act as a seed bank that implies a source of new nauplii to the planktonic population, a potential source for the recruitment of individuals into the planktonic population, and that allows survival during unfavourable environmental periods. Acknowledgements This research was support by a F.P.I.-J.A. grant to EG. and by CICYT projects MAR and MAR We thank the Junta de Obras del Puerto de Malaga which provided logistic support in sampling. M a Pilar Castro translated and revised the English style. We also thank Mark Ohman and two anonymous referees for their helpful comments and corrections. References Alcaraz^M. (1977) Ecologia, competencia y segregacidn de especies congene'ricas de cope'podos {Acartia). PhD Thesis, University of Barcelona, Spain, 191 pp. Ban.S. (1992) Effects of photoperiod, temperature, and population density on induction of diapause egg production in Eurytemora affinis (CopepodaiCalanoida) in lake Ohnuma, Hokkaido, Japan. /. Crust BioL, 12, Ban,S. et al. (1997) The paradox of diatom-copepod interactions. Mar. EcoL Prog. Ser, 157, Belmonte.G. (1992) Diapause egg production in Acartia (Paracartia) latisetosa (Crustacea.Copepoda, Calanoida). BolL ZooL, 59, Behnonte.G. and Puce,M. (1994) Morphological aspects of subitaneous and resting eggsfromacartia josephinae (Calanoida). Hydrobiologia, 292T293, De Stasio,B-T. (1989) The seed bank of a freshwater crustacean: copepodology for the plant ecologist. Ecology, 7, Grice.G.D. and Marcus,N.H. (1981) Dormant eggs of marine copepods. Oceanogr. Mar. BioL Anna. Rev., 19, Guerrero^F. (1993) Production, estrategias reproductivas y proliferation de Acartia (Copepoda: Calanoida) en sistemas costeros sometidos a distintas escalas temporales de fluctuation ambiental. PhD Thesis, University of Malaga, Spain, 26 pp. Hairston,N.G.,Jr and Munns,W.R.,Jr (1984) The timing of copepod diapause as an evolutionarily stable strategy. Am. NaL, 123, Hairston,N.G.,Jr and Van Brunt,R.A. (1994) Diapause dynamics of two diaptomid copepod species in a large lake. Hydrobiologia, 292/293,

9 Copepod resting eggs in Alboran coastal waters Ianora,A. and SantellaJL (1991) Diapause embryos in the neustonic copepod Anomalocera patersoni. Mar. BioL, 18, JohnsonJ.K. (198) Effects of temperature and salinity on production and hatching of dormant eggs otacartia californiensis (Copepoda) in an Oregon estuary. Fish. Bull, TJ, Kasahara.S., Uye.S. and OnW.T. (1974) Calanoid copepod eggs in sea-bottom muds. Mar. BioL, 26, Kasahara.S., Uye.S. and Onbe\T. (1975) Calanoid copepod eggs in sea-bottom muds. II: seasonal cycles of abundance in the populations of several species of copepods and their eggs in the Inland sea of Japan. Mar. BioL, 31, Levin.S.A., CohenJ). and Hastings^- (1984) Dispersal strategies in patchy environments. Theor. Pop. BioL, 26, Lindley,J.A. (199) Distribution of overwintering calanoid copepods in sea-bed sediments around southern Britain. Mar. BioL, 14, Marcus,N.H. (198) Photoperiodic control of diapause in the marine calanoid copepod Labidocera aestiva (Copepoda:Calanoida). BioL Bull., 159, Marcus,N.H. (1982) Photoperiodic and temperature regulation of diapause of Labidocera aestiva. BioL Bull., 162, Marcus,N.H. (1984) Recruitment of copepod nauplii into the plankton: importance of diapause eggs and benthic processes. Mar. EcoL Prog. Ser., 15, Marcus,N.H. (1991) Planktonic copepods in a sub-tropical estuary: Seasonal patterns in the abundance of adults, copepodites, nauplii, and eggs in the sea bed. BioL Bull., 181, Marcus,N.H. and Fuller.C.M. (1986) Subitaneous and diapause eggs of Labidocera aestiva Wheeler (Copepoda:Calanoida): differences in fall velocity and density. J. Exp. Mar. BioL Ecol., 99, Marcus.N.H. and Gengebach J.S. (1986) Recruitment of individuals into the plankton: the importance of bioturbation. Limnol. Oceanogr., 31, Marcus^N.H., Lutz,R., Burnett,W. and Cable,P. (1994) Age, viability and vertical distribution of zooplankton resting eggs from an anoxic basin: evidence of an egg bank. Limnol. Oceanogr, 39, Naess.T. (1991) Marine calanoid resting eggs in Norway: abundance and distribution of two copepod species in the sediment of an enclosed marine basin. Mar. BioL, 11, Onb,T. (1985) Seasonalfluctuationsin the abundance of populations of marine cladocerans and their resting eggs in the inland sea of Japan. Mar. BioL, 87, RodriguezJ. (1979) Zooplancton de la bahfa de Malaga: aproximaci6n al conocimiento de una comunidad planct6nica neritica en el mar de Alboran. PhD Thesis, University of Malaga, Spain, 147 pp. Rodriguez,V. (1981) Estudio de un ecosistema portuario: estructura de la comunidad planct6nica y explotaci6n de recursos por especies congen ricas de Acartia en sistemas fluctuantes. PhD Thesis, University of Malaga, Spain, 228 pp. Rodriguez,V. and VivesJF. (1984) Cope'podos de las aguas portuarias de Malaga. Invest. Pesq., 48, Rodriguez,V., GuerreroJF. and Bautista.B- (1995) Egg production of individual copepods of Acartia grant Sars from coastal waters: seasonal and diel variability. /. Plankton Res., 17, RungeJ.A. (1985) Relationship of egg production of Calanus pacificus to seasonal changes in phytoplankton availability in Puget Sound, Washington. Limnol. Oceanogr, 3, TaylorJF. and SpaldingJ.B. (1988) Fitness functions for alternative pathways in the timing of diapause induction. Am. Nat., 131, Tranter,DJ. and Abraham.S. (1971) Coexistence of species of Acartiidae (Copepoda) in the Cochin Backwater, a monsoonal estuarine lagoon. Mar. BioL, 11, Uye,S. (1982) Population dynamics and production of Acartia clausi Giesbrecht (Copepoda:Calanoida) in inlet waters;/. Exp. Mar. BioL EcoL, 57, Uye.S. (1985) Resting eggs production as a life history strategy of marine planktonic copepods. Bull. Mar. ScL, 37, Uye,S. and Fleminger,A- (1976) Effects of various environmental factors on egg development of several species of Acartia in Southern California. Mar. BioL, 38, Uye,S., Yoshiya,M., Ueda,K. and Kasahara.S. (1984) The effect of organic sea-bottom pollution on survivability of resting eggs of neritic calanoids. Crustaceana, 7(SuppL), Vilela,M.H. (1972) The development stages of the marine calanoid copepod Acartia grani Sars bred in the laboratory. Notas Estudos Inst. BioL Marit., 4, 38 pp. VillateJ 7. (1982) Contribuci6n al conocimiento de las especies de Acartia autoctonas de zonas salobres: Acartia (Paracartia) grani, G.O. Sars en la ria de Mundaka (Vizcaya, Espana). Kobie, 12,

10 EGneirero and V.Rodriguez Walton,W.E. (1985) Factors regulating the reproductive phenology of Onychodiaptomus birgei (Copepoda:Calanoida). LimnoL Oceanogr, 3, Watras.CJ. (198) Subitaneous and resting eggs of copepods: relative rates of clutch production by Diaptomus leptopus. Can. J. Fish AquaL ScL, 37, Received on May 29,1997; accepted on October 8,