Population Dynamics and Life Strategies of Rhincalanus Nasutus

Home , Gulf of Aqaba, Levantine Sea, Planktology, Rhincalanus, Rhincalanus gigas, Rhincalanus nasutus

JOURNAL OF PLANKTON RESEARCH j VOLUME 30 j NUMBER 6 j PAGES 655–672 j 2008

Population dynamics and life strategies of Rhincalanus nasutus (Copepoda) at the onset of the spring bloom in the Gulf of Aqaba (Red Sea) Downloaded from https://academic.oup.com/plankt/article/30/6/655/1475710 by guest on 28 September 2021

SIGRID B. SCHNACK-SCHIEL1, BARBARA NIEHOFF1*, WILHELM HAGEN2, RUTH BO¨ TTGER-SCHNACK2, ASTRID CORNILS1, MOHAMED M. DOWIDAR3, ANNA PASTERNAK4, NOGA STAMBLER5, DOROTHEA STU¨ BING2 AND CLAUDIO RICHTER6 1 2 ALFRED-WEGENER-INSTITUT FU¨ R POLAR- UND MEERESFORSCHUNG, 27515 BREMERHAVEN, GERMANY, MARINE ZOOLOGIE, UNIVERSITA¨ T BREMEN, 28334 3 4 BREMEN, GERMANY, NATIONAL INSTITUTE OF OCEANOGRAPHY AND FISHERIES, KAYET-BEY, ALEXANDRIA, EGYPT, P.P. SHIRSHOV INSTITUTE OF OCEANOLOGY, 5 RUSSIAN ACADEMY OF SCIENCES, 117997 MOSCOW, RUSSIA, THE MINA AND EVERARD GOODMAN FACULTY OF LIFE SCIENCES, BAR-ILAN UNIVERSITY, 6 RAMAT-GAN 52900, ISRAEL AND ZENTRUM FU¨ R MARINE TROPENO¨ KOLOGIE, 28359 BREMEN, GERMANY

*CORRESPONDING AUTHOR: [email protected]

Received November 15, 2007; accepted in principle February 6, 2008; accepted for publication February 13, 2008; published online February 18, 2008

Corresponding editor: Roger Harris

Abundance, distribution, population structure, lipid content, lipid composition and reproductive and feeding activity of Rhincalanus nasutus were studied in the Gulf of Aqaba and in the northern Red Sea during RV “Meteor”-cruise M 44-2 in February/March 1999. Rhincalanus nasutus occurred in higher numbers in the Gulf of Aqaba (585 ind m22) than in the northern Red Sea (254 ind m22). Young developmental stages (nauplii, copepodite stages CI and CII) were absent. In the southern Gulf of Aqaba, the bulk of the population developed from stage CV to adult in the course of the 3-week study period. In contrast, immature CV stages dominated at the adjacent stations in the northern Gulf of Aqaba and in the northern Red Sea. Development was associated with the seasonal vertical migration from wintering mid-water layers and initiation of feeding starting as early as beginning of March in the southern Gulf of Aqaba. No upward migration was observed in the northern parts of the Gulf and in the northern Red Sea, where more than 90% of the females remained immature during our study. Lipids were dominated by wax esters in females and CV. The fatty acid and fatty alcohol compositions of females were very similar throughout the study region and period. Major fatty acids were 18:1(n29), 16:1(n27), 16:2(n24) and 20:5(n23). Our results support the previous reports of a seasonal dormancy of R. nasutus in the Gulf of Aqaba and suggest that the timing of vertical migration, feeding and maturation is closely coupled to the development of the spring bloom in oligotrophic subtropical waters.

INTRODUCTION phylogenetic studies identiﬁed R. nasutus as a cryptic Rhincalanus nasutus Giesbrecht 1888 is widespread in all species complex with genetic differences between popu- oceans, and its distribution extends far to the north and lations unrelated to geographic distribution (Goetze, to the south (Schmaus, 1917). Rhincalanus nasutus is 2003). In the Gulf of Aqaba and in the Red Sea described as a species with a distinct preference for the R. nasutus occurs regularly but usually in relatively low open ocean (Vervoort, 1963), but it is also reported numbers (Halim, 1969; Weikert, 1982; Almeida from shelf and slope areas (Koslow and Ota, 1981; Prado-Por, 1983; Vaissie`re and Seguin, 1984; Weikert Sameoto, 1984; Hansen et al., 2005) as well as from and Koppelmann, 1993). Beckmann (Beckmann, 1996), shallow coastal embayments (Castro et al., 1993). Recent however, found R. nasutus in high numbers in the

doi:10.1093/plankt/fbn029, available online at www.plankt.oxfordjournals.org # The Author 2008. Published by Oxford University Press. All rights reserved. For permissions, please email: [email protected] JOURNAL OF PLANKTON RESEARCH j VOLUME 30 j NUMBER 6 j PAGES 655–672 j 2008

northern Red Sea which was most pronounced in any migratory behaviour or feeding (Weikert, 1980, March 1984 (about 5000 ind m22). 1982; Weikert and Koppelmann, 1983; Beckmann, Rhincalanus nasutus inhabits a wide depth range from 1984). In contrast, Beckmann (Beckmann, 1996) found the surface to below 2000 m (Vervoort, 1946; Wheeler, seasonal vertical migrations of R. nasutus including an 1970) with maximum concentrations in mid-waters ascent to the surface in spring in the northern and (Roe, 1972; Wishner and Allison, 1986). Apart from this central Red Sea and Farstey (Farstey, 2001) in the north- general pattern, this species seems to be also associated ern Gulf of Aqaba. No comparable data are available with upwelling events (Longhurst, 1967; Peterson, from the middle and southern Gulf of Aqaba. 1998). In both upwelling and non-upwelling regions in In February/March 1999 a synoptic study focusing the eastern tropical Pacific, R. nasutus was concentrated on hydrography and planktology was conducted aboard between 300 and 400 m, where the oxygen concen- RV “Meteor” in the Gulf of Aqaba and in the northern Downloaded from https://academic.oup.com/plankt/article/30/6/655/1475710 by guest on 28 September 2021 21 trations were lower than 0.13 mL O2 L . In the Red Sea (Pa¨tzold et al., 2000; Hempel and Richter, 21 oxygen minimum zone (,0.01 mL O2 L ) at depth 2002). The objective of the present study was to charac- .400 m, R. nasutus was absent (Sameoto, 1986). In the terize the life-cycle strategies of R. nasutus during the Arabian Sea, R. nasutus occurred at oxygen concen- transition from winter convection to summer stratifica- 21 trations below 0.15 mL O2 L (Vinogradov and tion and hence, at the onset of the spring bloom. To Voronina, 1961), in the Red Sea between 0.49 and test the hypothesis that the life cycle of R. nasutus 21 1.3 mL O2 L (Weikert, 1980, 1982; Beckmann, 1984). includes a dormancy stage, we studied its vertical distri- There are distinct differences between these two bution, population structure, maturity stage, lipid regions: in the Arabian Sea, mid-water low oxygen con- content, lipid composition and feeding activities. centrations co-occur with low temperature (108C) and low salinity (36), whereas in the Red Sea, both temperature and salinity are high at these depths (ca. 228C and Investigation area ca. 40.5, respectively, Weikert, 1980; Beckmann, 1984) The Gulf of Aqaba is a semi-enclosed deep and narrow due to the shallow sill of Bab el Mandeb isolating the basin in the northeast of the Red Sea. At the southern Red Sea deep-sea from the deep circulation of the end, the Gulf is separated from the Red Sea by the world ocean. In spite of the uniquely high deep-sea narrow and shallow Straits of Tiran (sill depth temperatures, R. nasutus has been reported to survive ,250 m). Unlike the Red Sea and other subtropical extended periods of starvation as an expatriate popu- systems, the Gulf of Aqaba is characterized by distinct lation by retreating into the oxygen minimum zone of hydrographic and biological seasonality (Wolf-Vecht the Red Sea, between 400 and 600 m, and thus redu- et al., 1992; Genin et al., 1995; Labiosa et al., 2003). cing its metabolism (Weikert, 1980). However, in the High evaporation rates and cooling in winter result in adjacent Gulf of Aqaba, R. nasutus appears to fare well, relatively strong vertical mixing down to depths between in spite of well-mixed and oxygenated waters. At mid- 300 and 900 m (Genin et al., 1995), which is unusual water depths, R. nasutus occurs throughout the Gulf in for the subtropics. This winter mixing is probably the abundances comparable to those in the Red Sea most important source of nutrient transport into the (Kimor and Golandsky, 1977; Almeida Prado-Por, 1983, euphotic zone (Klinker et al., 1978; Levanon-Spanier 1990; Farstey, 2001) showing that (i) low oxygen concen- et al., 1979; Genin et al., 1995; Lindell and Post, 1995; trations are not a prerequisite for its existence and (ii) Lindell et al., 2005). Thermal stratification of the R. nasutus may not be an expatriate after all. nutrient-enriched surface layer sets the stage for phyto- It is not clear whether or not R. nasutus performs ver- plankton succession in the Gulf of Aqaba with a distinct tical migrations. Diel vertical migration was reported spring bloom (Lindell and Post, 1995; Lindell et al., from near-shore areas by Koslow and Ota (Koslow and 2005; Stambler, 2005). The magnitude of this spring Ota, 1981), Sameoto (Sameoto, 1984) and Castro et al. bloom depends on the depth of the previous winter (Castro et al., 1993). Other studies did not detect indi- mixing and the resulting infusion of nutrients into the cations of such a migration pattern (Vervoort, 1946; euphotic zone (Genin et al., 1995). Thermal stratification Roe, 1972; Wishner and Allison, 1986; Ohman et al., prevails throughout the summer and the surface layer 1998; Farstey, 2001). Ohman et al.(Ohmanet al., 1998) becomes depleted of nutrients (Reiss and Hottinger, described a seasonal vertical migration pattern of 1984). In late autumn, cooling of the sea surface R. nasutus in the San Diego Trough off California. In the deepens the mixed layer, which persists over several permanently stratified part of the Red Sea, R. nasutus is months and reaches its maximum depth (.250 m) in described as remaining in the oxygen minimum zone early spring (Klinker et al., 1978; Paldor and Anati, between 400 and 600 m for most of the year without 1979; Labiosa et al., 2003). Similar to other subtropical

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systems, picophytoplankton is abundant throughout the Table I: List of multinet stations year (Lindell and Post, 1995). During the summer Local Mesh period, the picoplankton is accompanied by the sampling Sampling size nitrogen-ﬁxing cyanobacterium Trichodesmium spp. After St. no. Date 1999 time (h) depth (m) (mm) the onset of stratiﬁcation in spring, the phytoplankton Position I (29829,520N, 34857,040E, 580 m water depth) bloom is usually dominated by Synechococcus (Lindell and 122 2 February 13:30 550 150 Post, 1995; Lindell et al., 2005; Stambler, 2005) and 139 26 February 17:40 550 150 151 3 March 18:00 450 55 diatoms (Kimor and Golandsky, 1977). The overall low 157 5 March 09:40 550 150 productivity (Levanon-Spanier et al., 1979; Labiosa 157 5 March 14:40 500 150 et al., 2003) and rapid ventilation of deep waters with 157 5 March 22:10 500 150 0 0

Position II (29817,02 N, 34848,98 E, 828 m water depth) Downloaded from https://academic.oup.com/plankt/article/30/6/655/1475710 by guest on 28 September 2021 residence times in the order of only 6–8 years (Pla¨hn 123 22 February 19:30 800 150 et al., 2002) explain the absence of an oxygen minimum Position III (29805,040N, 34846,000E, 824 m water depth) layer in the Gulf of Aqaba. 124 23 February 00:53 800 150 164 6 March 22:30 800 55 Position IV (28849,970N, 34843,930E, 1350 m water depth) 125 23 February 08:35 1300 150 136 25 February 00:09 1300 150 MATERIALS AND METHODS 165 07 March 08:50 1250 150 Position V (28834,970N, 34839,020E, 1174 m water depth) Sampling of R. nasutus was carried out in the Gulf of 126 23 February 16:09 1100 150 Position VI /28820,160N, 34832,910E, 850 m water depth) Aqaba and in the northern Red Sea during RV 117 21 February 19:05 800 150 “Meteor” cruise M44/2 (21 February to 7 March 1999) 152 2 February 09:48 800 150 (Table I, Fig. 1). Sampling locations are indicated by 152 2 March 14:50 800 150 152 2 March 21:45 800 150 roman numbers (I through XII), most of which were 152 3 March 01:45 800 150 re-sampled several times during the cruise. 152 3 March 09:00 750 55 167 7 March 19:20 853 150 Zooplankton was collected with two opening/closing 0 0 21 Position VII (27852,89 N, 34839,88 E, 646 m water depth) multi-nets towed vertically at 0.5 m s . The “maxi” 144 27 February 12:15 600 150 2 type with an opening of 0.5 m was equipped with nine 153 3 March 15:25 600 150 nets of 150 mm mesh size enabling us to sample nine Position VIII (27839,170N, 34840,000E, 891 m water depth) 145 27 February 17:38 850 150 successive depth layers between near the sea floor and Position IX (27825,020N, 34840,090E, 890 m water depth) the surface in one haul. The “midi” type with an 146 27 February 23:50 850 150 opening of 0.25 m2 was equipped with five nets of 154 3 March 21:30 850 150 Position X (27811,200N, 34839,840E, 1118 m water depth) 55 mm mesh size. Repeated hauls enabled us to sample 131 24 February 15:13 1100 150 the whole water column in 9 to 13 depth intervals. The Position XI (27823,800N, 34821,850E, 1086 m water depth) filtered volume was calculated based on the vertical dis- 148 28 February 11:25 1000 150 Position XII (27824,990N, 34804,900E, 802 m water depth) tance covered by the net’s mouth area assuming 100% 133 25 February 02:38 750 150 filtering efficiency (“midi” net) or by means of a digital 156 4 March 12:30 750 55 flowmeter (“maxi” net). Samples were preserved with borax-buffered 4% formaldehyde/sea water solution, except at St. 165 (at Position IV), which was fixed with method was used to enhance separations of station 90% ethanol. All R. nasutus individuals were sorted from groups identified from cluster dendrogram and multidi- the whole samples to determine the abundance and mensional scaling plots. A one-way ANOSIM (analysis depth distribution. The mean population stage was cal- of similarity) test was conducted to test for regional (Gulf culated according to Marin (Marin, 1987), and the of Aqaba–Red Sea) and temporal (February–March) mean depth after Roe (Roe, 1972). differences in the community composition. Analysis of similarity was performed with the Female gonad development stages were determined PRIMER5 program (Plymouth Routines in Multivariate under a dissection microscope. Four developmental Ecological Research) developed at Plymouth Marine stages of gonads (GS) were determined according to Laboratory. Standing stocks (ind m22)ofR. nasutus were Niehoff and Hirche (Niehoff and Hirche, 1996). GS1, 2 transformed by the fourth root to account for the large and 3 comprise females of increasing maturity charac- abundance differences between stages. Hierarchical terized by an increase in number and size of translucent agglomerative clustering was applied to reveal differences oocytes in the diverticula of the gonads. Mature gonads in the R. nasutus stage composition between stations, (GS4) are characterized by large brown oocytes situated using the Bray–Curtis index. The complete linkage ventrally from the opaque ones.

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pellet volume calculated assuming a cylindrical shape. Food items found in the guts were counted, and their length and width measured and the volume calculated assuming simple geometrical shapes (Smayda, 1978). For dry mass determination and lipid analysis, specimens of the later stages of R. nasutus (CV and females) were collected at various stations in the Gulf of Aqaba and the northern Red Sea from depths between 600 m and the surface. They were immediately transferred to a container with filtered seawater and sorted according to sex and stage. The individuals were pooled for each Downloaded from https://academic.oup.com/plankt/article/30/6/655/1475710 by guest on 28 September 2021 sample (total of 23 samples with usually 30–50 specimens) and directly deep-frozen at 2808C or stored frozen in dichloro-methane/methanol (2:1 by vol.) until analysis. Total lipids were extracted with dichloromethane/ methanol (2:1 by vol.) essentially after Folch et al. (Folch et al., 1957) and Hagen (Hagen, 2000), and lipid classes were determined according to Fraser et al. (Fraser et al., 1985) by thin-layer chromatography-flame ionization detection with an Iatroscan MARK IV. Calibration of wax esters was performed using natural copepod wax esters as standard. After trans-esterification of the lipids with 3% conc. sulphuric acid in methanol, fatty acid methyl esters and free alcohols were simultaneously analysed in a gas chromatograph (Hewlett-Packard HP 6890) equipped with a DB-FFAP column (30 m length, 0.25 mm inner diameter, 0.25 mm film thickness). The gas chromatographic oven was temperature- programmed and helium was used as carrier gas. The Fig. 1. Map of Gulf of Aqaba and the northern Red Sea showing fatty acid methyl esters and free alcohols were identified positions (roman numbers) of all stations, at which samples were using known standards. For analytical details, refer to taken, and standing stocks (ind m22)ofR. nasutus. Hagen (Hagen, 2000), Kattner and Fricke (Kattner and Fricke, 1986), and Kattner et al. (Kattner et al., 1994). Throughout the cruise, qualitative checks of the Data of multiple determinations (different samples) are feeding and reproductive activities of R. nasutus females presented as means with standard error. were carried out in short-term incubations at 208Cin For the determination of the distribution and compo- the dark. Females for the experimental work were sition of potential food (phytoplankton and microzooplank- sampled with a Nansen net from the upper 400 m at ton), water samples were collected at five different depth Positions I and IV (Gulf of Aqaba) and at Positions IX layers (10, 30, 50, 70 and 100 m) using 10 L General and XI (northern Red Sea). Intact females were sorted Oceanic rosette water bottles and fixed in 2% borax- immediately after collection, transferred to 0.5 L glass buffered formaldehyde–seawater solution. Major micro- jars and fed ad libitum with a mixed culture of diatoms plankton taxa were identified and counted microscopically. (small unidentified pennate diatoms, Thalassiosira spp., Picoplankton and small nanoplankton (,10 mm) were Nitzschia spp.). In each experiment, the production of measured by flow cytometry (Stambler, 2005). faecal pellets and eggs was controlled after 6–8 h. Fed females were subsequently incubated individually in 10 mL multi-wells with unfiltered surface seawater. Owing to limited space and time, the egg production RESULTS was checked every 2 h over a period of only eight hours. Feeding activity was also estimated at Positions I, VI Environmental parameters and VII as a percentage of females, copepodite stages V During our investigation period, temperature and sal- and IV with food in their guts. The length and width of inity showed only small vertical and horizontal gradi- the food pellet in the posterior gut was measured and the ents (Pla¨hn et al., 2002). The temperature in the upper

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400 m decreased northwards from .21.7 to about Aqaba and a subsurface maximum between 50 and 21.48C, and the salinity increased from ,40.45 to 100 m depth at most of the Red Sea positions. .40.63. The temperature in the northern Red Sea was The picoplankton consisted mainly of cyanobacteria higher (about 1.58C) than in the Gulf of Aqaba, (mainly Synechococcus), Prochlorococcus and diverse whereas the salinity was lower (about 0.2–0.4). In the pico-eukaryotes. Prochlorococcus dominated the picoplank- Gulf of Aqaba, the depth of vertical mixing increased ton with about 50% of the total cells in the Red Sea fol- from south to north from 200 m to 400–500 m. At the lowed by Synechococcus (+30%) whereas in the Gulf of northernmost position in the Gulf of Aqaba, the vertical Aqaba, Synechococcus made up about 50% and mixing depth was 200 m during the first sampling. Four Prochlorococcus 25% by numbers (Stambler, 2005). days later on 26 February, an intensive convection event The microplankton standing stock was lowest in the was observed, and the water column mixed down to northern Gulf of Aqaba at Position I followed by the Downloaded from https://academic.oup.com/plankt/article/30/6/655/1475710 by guest on 28 September 2021 500 m. Because no changes in wind strength and direc- stations in the northern Red Sea (Cornils, 2001). tion as well as in air temperature occurred within these Highest values were found in the middle and the 4 days, it is assumed that the convection was not pri- southern part of the Gulf. Coccolithophoriids domi- marily caused directly by local atmospheric influences nated the community at all stations by numbers and but was forced by internal waves. At Position VI in the contributed between 46 and 63% of the total. Diatoms southern Gulf, the environmental data show a very ranked second in the Gulf of Aqaba, whereas dinofla- slight increase in temperature in the surface layer at the gellates did so in the northern Red Sea. Naked ciliates last sampling on 7 March. The Red Sea stations and and tintinnids contributed between 7 and 9% of the one last sampled station at the southernmost position in microplankton assemblage in the Gulf and in the Red the Gulf of Aqaba (Position VI, St. 167; Table I) Sea, respectively (Cornils, 2001). Mobile organisms showed high stratification between 20 and 50 m, a occurred in much higher total numbers than non- mixed layer down to 200 m and homogeneous colder mobile ones and contributed between 70% in the water below. There were no major changes in hydrogra- southern Gulf of Aqaba and 90% in the northern Gulf phy during the investigation period in the northern Red as well as in the northern Red Sea. Sea (Pla¨hn et al., 2002). The oxygen concentration in the upper layers was 5mLL21 in both areas studied (Table II). In the Gulf Rhincalanus nasutus of Aqaba, the concentration was high even far below the mixing depth (Ha¨se et al., 2006), and the concen- Standing stock, population structure and distribution pattern tration decreased only slightly towards the sea floor. In The total standing stock of R. nasutus varied greatly contrast, in the northern Red Sea, oxygen concen- between locations but also between the different stations trations decreased below the euphotic zone and a local at a position (Fig. 1). High concentrations (.1000 oxygen minimum of about ,2mLL21 was observed in ind m22) were found in the Gulf of Aqaba and near the mid-waters between 400 and 600 m. Close to the entrance to the Gulf of Suez (Position XII) contrasting bottom, the oxygen concentrations again increased to with much lower values in the Red Sea proper (51 and 3mLL21 (Ha¨se et al., 2006). 65 ind m22 at Positions XI and VIII, respectively). The chlorophyll a standing stock integrated over the Females, CV and CIV stages were two to three times upper 200 m varied between 31 and 53 mg m22 in the more abundant in the Gulf of Aqaba than in the Red Gulf of Aqaba with highest values in the north (Position Sea, whereas CIII exhibited three times higher densities I) and in the south (Position VI). At the Red Sea in the Red Sea (Fig. 2). Males occurred in similar mean stations, the standing stock was between 24 and densities in both areas. Females dominated in both 36 mg m22. At all positions except the southernmost regions accounting for an average of 47% of the total ones in the Gulf (Position VI), the chlorophyll a concen- population. CV ranked second (37%), followed by CIV trations increased 1.2 to 2 times over our study period, (10 and 14%). CIII and males were found only in small up to 57 mg m22 at Position I and 48 mg m22 at numbers and contributed about 3% each to the total Position XII at the entrance to the Gulf of Suez in the population. The two earliest copepodite stages (CI and Red Sea. In the northern Gulf of Aqaba (Position I), CII) as well as nauplii were absent in all samples. the above-mentioned convection event on 26 February During the first sampling period in late February, CV resulted also in a homogeneous vertical distribution of were most abundant in the northern part of the Gulf of chlorophyll a. The mixing depth became shallower Aqaba, whereas females prevailed in the southern part of toward the south. It was accompanied by a chlorophyll the Gulf and in the Red Sea, except for the two stations a maximum in the upper 50 m in the southern Gulf of near the entrance to the Gulf of Aqaba (St. 144, 27

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Table II: Overview of environmental parameters measured during the cruise

Temperature (8C) Salinity Oxygen (mL L21)

St. no. 15 m 400 m 15 m 400 m 15 m 400 m Chl a (mg m22)

Gulf of Aqaba Position I 122 21.48 20.77 40.63 40.61 5.28 4.46 44.84 139 21.36 21.42 40.64 40.64 43.17 151 21.29 20.84 40.64 40.61 157 21.26 21.32 40.64 40.64 56.92 Position II

123 21.47 20.83 40.64 40.60 5.00 4.16 30.86 Downloaded from https://academic.oup.com/plankt/article/30/6/655/1475710 by guest on 28 September 2021 Position III 124 21.51 21.07 40.63 40.58 39.55 164 21.38 21.22 40.59 40.61 52.28 Position IV 125 21.58 20.94 40.53 40.58 136 21.46 20.91 40.55 40.58 4.90 3.97a 33.15 165 21.28 21.05 39.96 Position V 126 21.59 20.88 40.51 40.58 4.96 4.07a 38.39 Position VI 117 21.84 21.09 40.39 40.55 5.06 4.29 52.98 152 21.67 20.88 40.30 40.57 53.53 167 22.29 20.91 40.40 40.57 44.80 Northern Red Sea Position VII 144 22.94 21.53 40.16 40.84 4.89 1.83 29.15 153 22.76 21.54 40.21 40.48 45.88 Position VIII 145 23.17 21.54 40.12 40.49 4.93 1.77 24.75 Position IX 146 23.20 21.54 40.15 40.49 25.05 154 23.12 21.54 40.15 40.48 33.88 Position X 131 23.49 21.53 39.98 40.48 4.99 1.77 35.92 Position XI 148 22.72 21.53 40.10 40.49 4.88 2.88a 28.96 Position XII 133 22.87 21.56 40.17 40.49 23.52 156 22.79 21.60 40.13 40.50 47.79

Chlorophyll a integrated over the upper 200 m. aAt 500 m.

February) and to the Gulf of Suez (St. 133, 25 February) between 300 and 600 m at the first sampling in (Fig. 3). The bulk of the R. nasutus population was con- February into the upper 50 m (Fig. 4). This indicates that centrated in mid-water layers between 400 and 500 m, the time window at the surface is only short and prob- independent of station, position or day time (Fig. 3). ably coupled to the spring bloom progressing northwards Consecutive sampling showed that throughout the along the transition zone between stratified waters in the Gulf of Aqaba, the stage frequency distribution shifted in South and well-mixed waters in the North. dominance from CV to females in the course of 2 The ratio of copepodite stage V to adult females can weeks, a phenomenon not observed in the Red Sea provide an indirect measure of dormancy (Ohman (Fig. 4a–d). The sharp decrease in standing stock at the et al., 1998). If R. nasutus had previously entered dor- northernmost tip of the Gulf of Aqaba (Position I) from mancy as CV, the CV:female ratio should decrease, the first (22 February) to the second (26 February) when CVs moult to females at the end of diapause. sampling was associated with an intensive convection Indeed, this decline is evident in the Gulf of Aqaba, but event, which occurred on 26 February (Pla¨hn et al., not in the Red Sea proper (Fig. 5). 2002). The vertical distribution pattern does not indicate We found no evidence for diel vertical migration in vertical migration anywhere, with the notable exception either the well-mixed North (Position I) nor the stratified of the southern Gulf (Position VI) where part of the South (Position VI) of the Gulf of Aqaba: repeated sam- population migrated from its initial residence depth plings over periods of 12.5 and 24 h, respectively,

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Fig. 2. Mean standing stock of R. nasustus in both investigated regions. The bars indicate the standard deviation. revealed no changes in vertical distribution of either the entire population or specific stages of R. nasutus (Fig. 6). A dendrogram of density similarities revealed two groupings at a similarity degree of 70% (Fig. 7). The clusters clearly distinguished the stations according to their standing stock. The two stations with the lowest standing stock (,100 ind m22, Sts 145 and 148) are included in cluster 1. Cluster 2 can be further separated at 88% into three sub-groups and one extra station. Cluster 2a represents most Gulf of Aqaba stations and one station from the Red Sea (St. 133, Position XII), which had the highest standing stock (.600 ind m22) and a relatively high fraction of females. Stations from the northern part of the Gulf (St. 123 Position II, St. 157 Position I) are grouped in cluster 2b together with the six Red Sea stations, and all had an intermedi- 22 Fig. 3. Stage distribution (number in parentheses: mean population ate standing stock (200–600 ind m ). Three stations in stage) and vertical distribution of developmental stages expressed as the Gulf of Aqaba with standing stocks between 480 percentage of total numbers (numbers in parentheses: standing stocks 22 and 640 ind m22 are grouped together in cluster 2c; at (ind m ) integrated over the sampled water column). Light grey bars, daytime samples; black bars, nighttime samples; medium grey bars, these three stations, copepodite stage III was absent. dawn/dusk samples. The ANOSIM test revealed significant differences between the Gulf and the Red Sea (R ¼ 0.299; P , 0.02). In contrast to these regional differences, there immature stage during the entire study period. were no significant temporal differences. However, at the southernmost position (VI) in the Gulf of Aqaba, the females gradually developed to Reproduction and feeding advanced (GS3) and mature (GS4) stages, coinciding At the beginning of sampling, more than 90% of the with the upward migration. On 21 February at females were immature (GS1 and GS2) in both regions Position VI, 52% of the females were in GS1, 46% in (Fig. 8). At most stations, females remained in an GS2, and only 2% were in GS3. On 2 March, the

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Fig. 4. Temporal change in standing stock (ind m22), mean population stage (S), population structure (%) and vertical distribution as a percentage of total numbers. Numbers in parentheses: standing stocks (ind m22) integrated over the sampled water column at Position I (a), Position IV (b), Position VI (c) and Position VII (d). Light grey bars, daytime samples; black bars, nighttime samples; medium grey bars, dawn/ dusk samples. portion of GS2 had increased to 66%, whereas the Routine checks showed that all females, CV and percentage of GS1 had decreased to 31%. Within the CIVs caught in February had empty guts, except for following 5 days (2–7 March), the relative frequency of one female at Position I on 22 February between 250 GS1/GS2 decreased from 96 to 55%, whereas GS3 and 300 m which contained mainly unidentiﬁed mass increased from 4 to 29%. Mature females (GS4) in the gut but also some remnants of Rhizosolenia.In accounted for 16%. On 7 March, females were bimod- early March, in contrast, food was found in the guts of ally distributed with one peak between 200 and 400 m all developmental stages studied in the northern and and a second peak at the surface (Fig. 4c). The gonad southern Gulf of Aqaba (Table III). The percentage of developmental stage of the females in the two vertical individuals with food was higher at the southern maxima differed considerably with 65% mature indi- Position VI than at the northern one (Position I). The viduals in the upper 50 m, but no mature females in volume of the faecal pellets was rather variable at all the mid-water peak (Fig. 9). positions and no trend is obvious. The category of

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Fig. 4. Continued. unidentified mass contributed the highest fraction hence, the lack of gonad development and egg pro- (between 77 and 93% of the total content) with the duction may be related to our short-term incubation. exception of CV at Position I, where foraminiferans and tintinnids accounted for 53%. Mandible cutting edges were only found in females. Feeding experiments Lipid composition carried out on board during the last week of the The females of R. nasutus had mean total lipid contents expedition showed that females did not feed during the of 30.6 + 5.4% of dry mass (% DM) at the six stations first 4 days, independent of the geographical position, in the Gulf of Aqaba, ranging between 22.3 and 38.5% despite the high chlorophyll concentrations (1–5 mg DM. Lipid contents at three stations in the Gulf were Chl a L21) offered. However, during the last 2 days of not significantly different from those in the northern the expedition, females exhibited intense feeding activi- Red Sea [31.4 + 2.8% DM (27.9–34.4%)]. The CV ties at Position I (6 March) and Position IV (7 March), stages showed similar but more variable total lipid levels as indicated by a high faecal pellet production. Females of 29.4 + 10.8% DM at four stations in the Gulf of at both positions did not carry mature oocytes and Aqaba, compared with 34.2% DM at one station in the neither the freshly caught females nor the females pre- northern Red Sea. The transect revealed highest lipid viously fed with an algal suspension showed any devel- levels of females in the North and South of the Gulf of opment in gonad maturity stage, and hence, no egg Aqaba as well as in the northern Red Sea. A similar production over the 8 h of incubation. However, accord- trend was also detected for the CV specimens (Fig. 10). ing to Mullin (Mullin, 1993), R. nasutus produces eggs at In the females, lipids were clearly dominated by wax high rates only when feeding for more than 24 h, and esters, overall averaging 76.3 + 5.7% of total lipids.

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Wax ester levels were slightly higher in the Gulf of Aqaba (GA) with 77.5 + 5.2%, when compared with the northern Red Sea (RS) with 72.3 + 6.0%. Other lipid classes comprised triacyglycerols (mean 4.0 + 2.8%; GA: 4.3 + 2.9%; RS: 2.8 + 2.0%), phospholipids (mean 12.5 + 3.1%; GA: 11.3 + 2.1%; RS: 16.6 + 1.7%) and cholesterol (4.7 + 2.1%; GA: 4.4 + 2.1%; RS: 5.5 + 2.1%). Free fatty acids averaged 2.6 + 1.3%. The fatty acid and fatty alcohol compositions of females were very similar in the Gulf of Aqaba and the northern Red Sea (Table IV). Major fatty acids (.5%) in Downloaded from https://academic.oup.com/plankt/article/30/6/655/1475710 by guest on 28 September 2021 the total lipid extracts of females were 18:1(n29) (GA: 34.1%; RS: 31.7%), 16:1(n27) (GA: 26.0%; RS: 26.2%), 16:2 (n24) (GA: 8.7%; RS: 9.0%) and 20:5(n23) (GA: 5.3%; RS: 5.4%). These percentages were very similar to those of the CV stages. In the females, the fatty alcohols consisted mainly of the shorter-chain components, 16:0 (GA: 69.2%; RS: 68.4%), 14:0 (GA: 17.6%; RS: 19.0%) and 18:0 (GA: 12.2%; RS: 11.1%). Similar proportions were determined for the CV stages (Table IV).

DISCUSSION Seasonal vertical migration is characteristic of several calanoid species inhabiting areas with intense seasonal production cycles such as high latitudes (Conover, 1988; Schnack-Schiel, 2001) and upwelling regions (Smith, 1982; Peterson, 1998). Their life cycle strategies include residence in deep layers without diel vertical migration Fig. 4. Continued. during times of food scarcity, followed by an ascent to upper water layers when primary productivity increases.

Fig. 5. Temporal change of the ratio of copepodite stage V (CV) to adult female abundance integrated over the water column.

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Fig. 6. Depth distribution of the whole population (a) and mean depth distribution of CIV,CV and females (b) at two time stations. .NASUTUS R. JOURNAL OF PLANKTON RESEARCH j VOLUME 30 j NUMBER 6 j PAGES 655–672 j 2008 Downloaded from https://academic.oup.com/plankt/article/30/6/655/1475710 by guest on 28 September 2021

Fig. 7. Cluster analysis dendogram based on the vertically integrated abundances of all stages combined.

The animals at depth, commonly the late copepodite concentrated in the upper 50 m and intense feeding, stage V,are in a resting stage characterized by extremely but no reproductive activity could be observed. Hence, reduced metabolic rates, arrested development and ces- the shift from the dormant to the active stage of R. sation of feeding (Dahms, 1995; Williams-Howze, 1997). nasutus seems to have just started at Position VI. The lipid depots of the dormant animals are pro- According to Farstey (Farstey, 2001), the ascent of the nounced and these energy reserves consist mainly of adult copepods depends on the timing and depth of the wax esters (Lee et al., 2006). These storage lipids are vertical mixing of the water column, and takes place in essentially conserved during the resting stage for repro- the northern Gulf of Aqaba between February and ductive processes during the active phase (Hagen and April, when the water column stratifies and spring Schnack-Schiel, 1996). Resting females are not capable bloom develops, fuelling the reproduction of the of releasing eggs in short-time incubations (Ohman species. et al., 1998). Nauplii and the earliest copepodite stages (CI and Our results from the Gulf of Aqaba show similar life- CII) were absent in all samples from both regions. history traits for R. nasutus. The population investigated Farstey (Farstey, 2001) observed nauplii stage II to cope- in late February/early March concentrated in mid- podite stage II between February to April in the north- water layers, did not feed and showed no reproductive ern Gulf but with a great variability between years. The activity. These features together with intense wax ester first nauplius stage (NI) was absent in all her samples accumulation are consistent with dormancy, although probably due to their short stage duration of less than 1 no metabolic measurements were performed to unequi- day (Mullin and Brooks, 1967; Landry, 1983), whereas vocally verify the existence of a dormancy stage. At all CIII to females occurred throughout the year. northerly positions in the Gulf, CV dominated the The lipid patterns of R. nasutus resemble those of the population at the beginning of the study and females at Antarctic R. gigas (Kattner et al., 1994) and suggest a the end. In contrast, females prevailed in the southern moderate energy storage with intermediate total lipid Gulf during all sampling times. This suggests that the contents and mean wax ester levels not exceeding 80% southern population represented an advanced stage, of total lipids, although Lee and Hirota (Lee and Hirota, which is also confirmed by the fact that only at Position 1973) and Ohman et al. (Ohman et al., 1998) reported VI did all developmental stages start to ascend to the higher values. The absence of long-chain monounsatu- surface layer on the last day of sampling. Unfortunately, rated fatty acids and alcohols in R. nasutus (as in R. gigas) no samples from this date are available from Position is also in contrast to some of the dominant Calanus and V. These distributional results are in agreement with Calanoides species from polar and upwelling regions, our data on gonad maturity stages, lipid content and which exhibit very pronounced and sophisticated lipid composition as well as with the experimental data. accumulation patterns (Kattner and Hagen, 1995: Coinciding with the upward migration at Position VI Verheye et al., 2005; Lee et al., 2006). It is not clear to on the last sampling date (7 March), mature females what extent these internal energy reserves are sufficient

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Fig. 8. Mean developmental stages of gonads (GS) in the Gulf of Aqaba (a) and in the northern Red Sea (b).

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Fig. 9. Relative frequency of gonad maturity stages in different depth layers at Position VI. Numbers in parentheses: numbers of studied females. to fuel gonad maturation and egg production and, in and accumulation of wax ester reserves. This is consistent addition, supply from external food sources maybe with data on the phytoplankton community, which was required. Trophic biomarker analyses showed that the dominated by diatoms during our investigation (Cornils, lipid deposits were characterized by very high percen- 2001). Gut content analyses of R. nasutus also revealed tages of 16:1(n27), a typical signature fatty acid of diatoms as major identifiable food items. diatoms (Dalsgaard et al., 2003). The 18:4 (n23) fatty Rhincalanus nasutus seems well adapted to a diet of large acid, typical of flagellates, comprised only a very small diatoms. In the upwelling region of Somalia, Smith fraction suggesting that in contrast to diatoms flagellates (Smith, 1982) found high feeding rates on the most abun- were unimportant food items at least for the synthesis dant phytoplankton species, the diatom Nitzschia

Table III: Relative frequency of R. nasutus females, copepodite stages V and IV with food in their guts, volume of pellets, relative frequency of identiﬁed food and identiﬁed food items in the pellets

n n with % with pellet vol. % food studied food food (mm3310) identiﬁed identiﬁed food items

Position I Females St. 122 (22 February) 81 1 1.2 12 560 3 Rhizosolenia St. 157 (5 March) 107 7 6.5 9219 7 Mandibles CV St. 122 (22 February) 74 0 0 St. 157 (5 March) 67 2 3.0 15 700 47 Foraminiferans, tintinnids CIV St. 122 (22 February) 68 0 0 St. 157 (5 March) 57 6 10.5 8969 12 Pennate diatoms, Dictyocha Position VI Females St. 117 (21 February) 84 0 0 St. 167 (7 March) 110 33 30.0 12 648 23 Pennate, centric diatoms, Rhizosolenia, Dictyocha, mandibles CV St. 117 (21 February) 41 0 0 St. 167 (7 March) 21 6 28.6 5687 22 Pennate diatoms, coccolothophoriids CIV St. 117 (21 February) 38 0 0 St. 167 (7 March) 10 2 20.0 9106 15 Pennate diatoms Position VII Females St. 153 (3 March) 42 0 0

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Fig. 10. Lipid class composition in percent of dry mass (% DM) of females in the Gulf of Aqaba and in the northern Red Sea. WE, wax esters; TAG, triacylglycerols; FFA, free fatty acids; ST, sterols; PL, phospholipids. Arabic numbers, stations; roman numbers, positions; numbers in parentheses, numbers of analyses.

delicatissima (85 mm long). Rhincalanus nasutus ingested also triggers (Hairston, 1987; Kaartvedt, 1996; Niehoff and the largest species Rhizosolenia styliformis (1050 mm long), Hirche, 2005). Endogeneous factors such as reproduc- but in lower numbers. In the Gulf of Aqaba, R. nasutus tive behaviour may play a role too, e.g. short-lived fed preferentially on large food particles and showed males of dormant species may have a higher fertiliza- highest grazing rates on Nitzschia spp. (Sommer et al., tion success, if newly moulted females emerge from dor- 2002). Preferential feeding on larger items was observed mancy at predictable times of the year (Ohman et al., for all developmental stages (Mullin and Brooks, 1967). 1998). Dormant R. nasutus in the Gulf of Aqaba concen- In the Benguela upwelling, high daily egg production trate between 300 and 600 m, raising the question of rates were observed at stations dominated by large which environmental signals trigger the termination of diatoms, whereas at stations dominated by microflagel- the resting period (Peterson, 1998). Light is unlikely to lates, egg production was 67 times lower (Walker and be detectable at these depths and variations in day- Peterson, 1991). This suggests that R. nasutus does not length are insignificant between winter and early spring, fare too well in the oligotrophic Red Sea and Gulf of the onset of vertical migration (max. 4 h over the entire Aqaba, where pico- and nanoplankton predominate year, Farstey, 2001). (Lindell and Post, 1995; Yahel et al., 1998) and large phy- Although the surface temperature increased in the toplankton are scarce, except for blooms in spring course of the stratification of the water column towards (Kimor and Golandsky, 1977). However, Irigoien et al. 7 March at Position VI (22.28C compared with 21.88C (Irigoien et al., 2005) could not detect any direct effect of at 21 February), these changes are unlikely to have been phytoplankton composition on the egg production rate felt by R. nasutus at its residence depth to trigger the of R. nasutus in the Benguela upwelling, suggesting that migration. However, the concomitant decrease of 200 m omnivory may be more important in unproductive integrated chlorophyll concentration (53–45 mg Chl a periods or regions, and egg production rate relates to m22) during this period invites speculation that the flux total food rather than phytoplankton alone. of phytoplankton may be a cue. This is in line with Timing and stimuli for emergence from and entering Farstey’s (Farstey, 2001) findings, showing good corre- into dormancy are not yet well understood (Dahms, lation between the vertical mean depth of R. nasutus and 1995). Changes in light, temperature, food availability, chlorophyll a (and surface temperature) but not with the lipid levels and predation have been invoked as possible day length. No sediment trap data are available for the

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Table IV: Fatty acid and alcohol compositions FUNDING (mass%) of R. nasutus females and CV We greatly appreciate the ﬁnancial support by the stages from the Gulf of Aqaba and the Deutsche Forschungsgemeinschaft for the Meteor-cruise northern Red Sea (.0.4% not shown) 44/2 and for the grants of S. Schiel (SCHI 329/9) and Females CV W. Hagen (HA 1706/8).

Gulf of Gulf of Aqaba Red Sea Aqaba Red Sea

Mean sd Mean sd Mean sd REFERENCES n 5 6 (14) n 5 3 (3) n 5 4 (5) n 5 1 (1) Downloaded from https://academic.oup.com/plankt/article/30/6/655/1475710 by guest on 28 September 2021 Fatty acids Almeida Prado-Por, M. S. (1983) The diversity and dynamics of 14:0 3.1 0.3 3.0 0.1 3.2 0.2 3.0 Calanoidea (Copepoda) in the northern Gulf of Elat (Aqaba), Red 16:0 4.5 0.5 4.2 0.5 4.8 0.6 4.4 Sea. Oceanol. Acta, 6, 139–145. 16:1(n27) 26.0 2.1 26.2 2.4 24.8 1.0 25.0 Almeida Prado-Por, M. S. (1990) A diel cycle of vertical distribution of 16:2(n24) 8.7 2.0 9.0 1.2 4.6 0.9 8.0 the Calanoidea (Crustacea: Copepoda) in the northern Gulf of 16:3(n24) 0.5 0.1 1.0 0.5 0.5 0.1 1.1 Aqaba (Elat). Bull. Inst. Oceanogr. Monaco, 7, 109–116. 16:4(n21) 0.2 0.1 0.4 0.3 0.2 0.1 0.2 18:0 1.6 0.2 1.3 0.1 1.7 0.3 1.4 Beckmann, W. (1984) Mesozooplankton distribution on a transect 18:1(n29) 34.1 2.0 31.7 1.5 35.7 2.7 31.9 from the Gulf of Aden to the central Red Sea during winter 18:1(n27) 0.9 0.1 1.0 0.1 0.9 0.0 1.0 monsoon. Oceanol. Acta, 7, 87–102. 18:2(n26) 1.0 0.1 1.1 0.1 1.2 0.1 1.0 18:3(n23) 0.2 0.0 0.4 0.2 0.3 0.1 0.2 Beckmann, W. (1996) Der Einfluss der großraümigen 18:4(n23) 0.3 0.2 0.5 0.4 0.2 0.2 0.5 Wasseraustauschvorga¨nge auf den Zooplanktonbestand des Roten 20:1(n27) 0.3 0.1 0.3 0.1 0.4 0.1 0.4 Meeres und sein trophisches Gefu¨ge. PhD Thesis. University of 20:2(n26) 0.8 0.3 1.0 0.5 2.1 1.7 1.2 Hamburg, Germany, p. 167. 20:3(n26) 0.3 0.0 0.4 0.0 0.4 0.0 0.3 Castro, L. R., Bernal, P. A. and Troncoso, V. A. (1993) Coastal intru- 20:4(n26) 1.6 0.2 1.4 0.4 1.6 0.3 1.2 sion of copepods: mechanisms and consequences on the population 20:4(n23) 0.3 0.1 0.4 0.1 0.3 0.1 0.4 Rhincalanus nasutus. J. Plankton Res. 20:5(n23) 5.3 1.3 5.4 1.8 4.2 2.3 7.2 biology of . , 15, 501–515. 22:5(n23) 0.3 0.1 0.4 0.1 0.3 0.1 0.1 Conover, R. J. (1988) Comparative life histories in the genera Calanus 24:1(n211) 0.9 0.2 0.9 0.1 0.9 0.2 0.7 and Neocalanus in high latitudes of the northern hemisphere. 22:6(n23) 3.1 0.4 3.9 1.0 3.9 0.6 2.9 Hydrobiologia, 167/168, 127–142. Unknowns 4.8 1.0 5.0 0.7 6.3 2.7 6.8 Fatty alcohols Cornils, A. (2001) Raümliche Verbreitung von Phyto- und 14:0 17.6 1.7 19.0 0.4 15.1 1.1 16.8 Zooplankton im no¨rdlichen Roten Meer. Diploma Thesis. 16:0 69.2 1.6 68.4 1.8 72.3 1.4 69.9 University Kiel, Germany, p. 86. 16:1 0.6 0.3 1.0 0.8 0.4 0.1 1.4 Dahms, H. U. (1995) Dormancy in the Copepoda—an overview. 18:0 12.2 0.5 11.1 0.7 11.9 0.6 11.5 Hydrobiologia, 306, 199–211. 18:1(n29) 0.3 0.1 0.5 0.0 0.3 0.1 0.5 Dalsgaard, J., St John, M., Kattner, G. et al. (2003) Fatty acid trophic n, number of stations (analyses). markers in the pelagic marine environment. Adv. Mar. Biol., 46, 225–340. Farstey, V. (2001) Feeding and vertical distribution the calanoid cope- region to estimate the sinking flux of phytoplankton, but pods Rhincalanus nasutus Giesbrecht and Pleuromamma indica Niemann et al. (Niemann et al., 2004) have shown that Wolfenden in the seasonally mixed water column in the northern part of the Gulf of Aqaba. PhD Thesis. Hebrew University, gravity currents in the northern Gulf of Aqaba may Jerusalem, Israel, p. 108. carry surface phytoplankton downslope to mid-water Folch, J., Lees, M. and Sloane-Stanley, G. H. (1957) A simple method depths in the course of a cold night. for the isoloation and purification of total lipids from animal tissue. J. Biol. Chem., 226, 497–509. Fraser, A. J., Tocher, D. R. and Sargent, J. R. (1985) Thin-layer chromatography – flame ionization detection and the quantitation of marine neutral lipids and phospholipids. J. Exp. Mar. Biol. Ecol., ACKNOWLEDGEMENTS 88, 91–100. We would like to thank the captain, crew and colleagues Genin, A., Lazar, B. and Brenner, S. (1995) Vertical mixing and coral death in the Red Sea following the eruption of Mount Pinatubo. aboard RV “Meteor” for their support and collabor- Nature, 377, 507–510. ation in the field. Herwig Stibor and Thomas Hansen Goetze, E. (2003) Cryptic speciation on the high seas; global phyloge- provided the phytoplankton cultures. Special thanks are netics of the copepod family Eucalanidae. Proc. R. Soc. Lond., B 270, due to Boaz Lazar and Olaf Pla¨hn for the oxygen, 2321–2331. temperature and salinity data and to Ruth Alheit and Ha¨se, C., Al-Qutob, M., Dubinsky, Z. et al. (2006) A system in Elke Mizdalski for help in sorting the samples. balance? – Implications of deep vertical mixing for the nitrogen

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