© 2004 by ICES/CIEM International Council for the Exploration of the Sea/Conseil International pour l'Exploration de la Mer
Life-history strategies of calanoid congeners under two different climate regimes: a comparison
a Alfred Wegener Institute for Polar and Marine Research Postfach 120161, DE-27515 Bremerhaven, Germany
b Laboratoire d'Océanographie Biologique 2 rue du Prof. Jolyet, F-33120 Arcachon, France
c DZMB, Senckenberg Research Institute Notkestrasse 85, D-22607 Hamburg, Germany
*Correspondence to C. Halsband-Lenk: tel: +1 206 543 3469; fax: +1 206 543 0275. e-mail: halsband{at}ocean.washington.edu.
To evaluate the relationship between different environmental temperature regimes and life-history traits of key planktonic taxa, the life cycles of congener pairs of Temora and Centropages species at two sites, a cold-temperate shelf sea (Helgoland Island, North Sea) and a warm-temperate oceanic site (Bay of Villefranche, Mediterranean) were compared in a multi-annual time-series. In an attempt to assemble a variety of parameters – some detailed, others sporadically measured – a synthesis of the life cycle is presented for each population. Although closely related, congeners showed distinct temperature preferences and specific adaptations of their life cycles to temperature regime. On the other hand, co-existing species such as T. longicornis and C. hamatus in the North Sea showed some analogous life-history traits. C. typicus occupied an intermediate position and was able to tolerate both temperature regimes by shifting its reproductive period between seasons. We point out interannual and inter-site variability in the populations investigated and identify the unsolved questions in regard to the seasonal dynamics of these species that require verification.
Keywords: Centropages, life cycle, reproduction, Temora, temperature regime
 |
Introduction |
|---|
 Top Introduction Material and methodsResultsDiscussionReferences |
|---|
Knowledge of copepod distribution patterns and population dynamics is crucial for modelling the marine foodweb and carbon flux. In recent decades, information on the population dynamics of calanoid copepods in coastal temperate regions of the Atlantic and adjacent seas has emerged: Le Ruyet-Person et al. (1975) first presented complete life cycles for Centropages sp. and Temora sp. in the Mediterranean and the English Channel, followed by a number of studies at mid-latitudes, e.g. by Razouls (1982) and Halsband-Lenk et al. (2001) in the Western Mediterranean, Kiørboe and Nielsen (1994) and Halsband and Hirche (2001) in the North Sea. Ianora (1998) presented a review of life-history traits of subtemperate calanoid copepods. In order to specify adaptations to temperature regimes, we here compare the life cycles of congeneric pairs of Temora (T. longicornis and T. stylifera) and Centropages (C. hamatus and C. typicus) species from a cold-temperate (North Sea) and a warm-temperate (Mediterranean) environment. These free-spawning species differ in their spatial or seasonal distribution patterns (Halsband-Lenk et al., 2001). At the Helgoland Roads station in the southern North Sea, T. longicornis is present all year round, while C. hamatus and C. typicus show a seasonal succession and virtually disappear from the samples in winter (Halsband and Hirche, 2001). T. stylifera and C. typicus are found year round with alternating abundance maxima in the Bay of Villefranche (Gilat et al., 1965). We assembled data on hydrographic settings, food conditions, abundance, and several reproductive parameters at the two locations from five copepod populations and present conceptual models of their life-history strategies. We identify the missing links in their life histories that are still unknown, but indispensable to predict their population dynamics, especially in regard to climate change.
|
Material and methods |
|---|
|
TopIntroductionMaterial and methodsResultsDiscussionReferences |
|---|
We combine two multi-annual series, the study by Halsband and Hirche (2001) at Helgoland Island (54°11'N 7°54'E) from July 1995 to August 1996 and additional data from September/October 1998 (except T. longicornis), June–October 1999, and March/April and July/August 2000. Zooplankton were sampled in the morning by horizontal surface tows of a CalCOFI net (diameter 1.5 m, 280-µm mesh size) at the "Helgoland Roads" station at 10-m depth. Abundance data, sea surface temperature, and phytoplankton concentrations are available from the Helgoland Roads time-series (courtesy W. Hickel and W. Greve, partly unpublished). These data were compared to a study in the Bay of Villefranche (43°41'N 7°19'E) conducted from November 1997 to December 1999 by Halsband-Lenk et al. (2001). Vertical hauls were taken at "Point B" from 80-m depth to the surface with a plankton net ("Superhomogène", diameter 0.5 m, 280-µm mesh size). For details on methods of incubation, measurement of reproductive parameters, hatching success, female carbon content, and body size, refer to Halsband-Lenk et al. (2001). Abundances are given on a log scale for ease of comparison. Egg production rates represent the mean number of eggs produced by females that were actively reproducing, referred to as "corrected egg production rate" by Halsband-Lenk et al. (2001) and are also shown on a weight-specific scale (note that annual averages of female carbon content and egg carbon were used here, while data differ significantly between seasons and years). The proportion of reproducing females refers to the percentage of all incubated females that spawned. The sequence of generations in Figures 6 and 7 has been estimated from changes in body size, along with developmental rates at different temperatures determined by Halsband-Lenk et al. (2002) and assigned to average in situ temperatures in different seasons.
|
Results |
|---|
|
TopIntroductionMaterial and methodsResultsDiscussionReferences |
|---|
Hydrographic conditions
The North Sea is subject to a boreal temperature cycle with distinct seasons. Maximum temperatures at Helgoland Roads occurred in August in the range 17.6–20.2°C. Winter minima ranged from 3.4°C to 4.4°C, except in 1996 when ice covered the Wadden Sea and temperatures at Helgoland Island sank to –0.5°C in February (Figures 2, 3). The sampling station was never stratified because of shallowness and strong currents. The southern North Sea is rich in nutrients due to eutrophication from coastal river run-off (Hickel et al., 1997). Consequently, particulate phytoplankton carbon concentrations (PPC) were high, with peaks of 340–900 mg C m–3 (Figure 1). Strong interannual variability was observed in phytoplankton development: in 1995, 1996, and 1999, blooms were characterized by high diatom abundance in spring. The dominant species were Coscinodiscus sp., Thalassiosira sp., and Gyrodinium sp., while flagellates played a minor role with maxima in summer. A very strong bloom of the large introduced C. wailesii (diameter >250 µm) dominated from January to April 1996. The years 1998 and 2000 were different. Spring blooms were less intense than the summer peak; diatom maxima occurred later, in June or July, while high flagellate abundances were observed in spring (2000) or summer (1998). Lowest phytoplankton density (0.2–4.0 mg C m–3) was recorded in autumn and winter in all years.
|
The thermal cycle in the Bay of Villefranche was characterized by strong summer stratification starting in May. A distinct thermocline was established in 15–30-m depth in June and July, which descended to depth in autumn until the upper layer was completely mixed. Surface temperature ranged from 13.5°C in winter to 25.8°C in summer. The deep water below 50 m remained at 14°C all year round. The NW Mediterranean is oligotrophic as compared to the North Sea station. Phytoplankton concentrations were around 25 times lower than at Helgoland Island, assuming a conversion factor from PPC to chlorophyll a (Chl a) of 40 (Riemann et al., 1989). The annual cycle of Chl a was almost identical in 1998 and 1999 with a weak phytoplankton bloom in spring. A subsurface Chl a maximum usually occurred at 30-m depth. A single extraordinary peak was recorded in July 1998 with 3.78 mg m–3 at 30-m depth. In 1999, the phytoplankton bloom in March reached peak values of 1.22 mg Chl a m–3. A bloom of salps of up to 40 individuals m–3 followed in late April, causing a decline of the Chl a maximum (all data courtesy of S. Dallot, Marine Station of Villefranche-sur-Mer). The microplankton community determined by cell counts showed three peaks in both years in May, September, and November, respectively (Gomez and Gorsky, 2003). Diatoms dominated in spring and autumn, dinoflagellates in summer. Ciliates were abundant in July and from November to January with a major peak in November 1999.
Temora longicornis at Helgoland Roads
T. longicornis was present all year round (Figure 2A, only females shown). In winter, abundance was low, but both adults and younger stages were found. Although timing and magnitude of abundance peaks were variable, highest numbers of individuals generally occurred in summer in the order of 1000–14 000 individuals m–3 (CI–VI).
|
Prosome length of female T. longicornis varied seasonally between 726 and 1360 µm, while interannual variability was small. Largest females were found in April, then body size decreased during summer with the smallest specimens from August to October (Figure 2B).
Reproduction of T. longicornis continued throughout the year. The highest rate was measured in May 1996 with 66 eggs female–1 d–1. Egg production rates varied between 20 and 40 eggs female–1 d–1 in summer, declined in September, and remained low in winter until the following spring. They were higher in summer 1995 than in 1999 and 2000 (Figure 2C).
Carbon content of females decreased from July to September 1995, but increased in October despite small prosome length. In spring 1996, female weight increased to a maximum of 26.7 µg C. In summer 1999, female carbon content showed little variation and was significantly lower than in summer 1995 (t-test, p<0.001) with a minimum of 6.7 µg C in July 1999 (Figure 2D).
The proportion of reproductive females was lowest in December and January, when less than 20% of the females were spawning (Figure 2E), and highest from May to October. In 1996 and 2000, the number of spawning females was unusually low (<50%) in July and August.
In autumn 1995, hatching success decreased from 66% to 33%, then increased to 55% in December. In March and June 1996, 92% and 94%, respectively, of all incubated eggs developed to nauplii, respectively, while in April only 51% hatched. In summer 1999, high proportions of around 90% of the eggs hatched, decreasing to 53% in October (Figure 5A).
Centropages hamatus at Helgoland Roads
From late March to November, females of C. hamatus were present and always spawning, except on two dates in April 1996 when the reproductive period had just started. The species was most numerous from June to August, with copepodite numbers ranging from 340 to 2500 m–3 (females shown in Figure 3A). Prosome length varied by a factor of 2 from the minimum of 750 µm in October 1995 to the maximum of 1570 µm in May 1996 (Figure 3B).
|
Reproduction patterns were similar between years (Figure 3C). Highest spawning activity was in spring (95 eggs female–1 d–1), but smaller peaks (30–50 eggs female–1 d–1) could also occur during summer. In September, egg production rates were moderate (20–40 female–1 d–1) and declined until October to <10 eggs female–1 d–1. Thereafter, no females were caught until April. After a period of low egg production in spring, reproduction rates increased rapidly to the annual maximum in May.
Female carbon content was higher in summer 1995, with around 12 µg C, than in summer 1999, with a minimum of 1.3 µg C in July. The largest animal was found in May 1996 containing 20.8 µg C (Figure 3D).
The proportion of reproducing females showed a maximum around 80% from May to September followed by a decrease in October and November. In March and April, an increasing trend may be assumed from the scarce data (Figure 3E). Matching the observations in T. longicornis, low proportions of spawning females were observed in July 1996 and August 2000.
Hatching success was 63% and 74% in April and June 1996, respectively. In 1999, it ranged from 60% to 100% in June and July. In September, hatching rates showed a large variability between 14.7% and 100%, both between different years and within 1998 (Figure 5B).
Centropages typicus at Helgoland Roads
The occurrence of C. typicus at Helgoland Roads was subject to great interannual variability (Figure 3F). In 1995, no adults were observed before September; then they remained present until January. In spring 1996, females were absent until the end of sampling in August. The species was abundant throughout the study period from September to October 1998. In 1999, C. typicus was regularly found already from June on. In 2000, single individuals were recorded even earlier in April. Abundance of C. typicus tended to correlate positively with high salinity, since females appeared in September 1995 and April 2000 paralleling an increase in salinity, while the species was absent in spring 1996 when salinity was relatively low. Since young stages could not reliably be distinguished from C. hamatus, their numbers are unknown. Female abundance maxima ranged from 10 to 35 m–3, except in 2001 when 130 females m–3 were recorded (Figure 3F).
Body size of C. typicus was consistent in the different years. Individual female prosome length ranged from 900 µm in December 1995 to 1434 µm in early April 2000 (Figure 3G).
The reproductive cycle of C. typicus was determined by the presence and absence of females, which occurred usually in the second, warmer half of the year and disappeared again in winter. In 1995 and 1998, females appeared in September and produced 30–80 eggs female–1 d–1, while very high rates of 80–122 eggs female–1 d–1 were recorded in June 1999 and August 2000. Reproduction rapidly decreased through October and nearly ceased from November to January. In April 2000, moderate egg production rates (20 eggs female–1 d–1) were observed (Figure 3H).
Carbon content of females varied from 12 to 18 µg C in September 1995. During summer 1999, female weight increased from 4.7 µg C in July to 18.7 µg C in early October (Figure 3I).
The monthly mean percentage of spawning females was highest in August and September 2000 with around 80%. It varied from 35% to 79% in 1999, while lowest proportions were measured in 1995 and 1998, ranging from 10% in December to 60% in September (Figure 3J).
Hatching success generally was high (82–100%), except in September 1998 when some single clutches did not hatch at all (Figure 5C).
Temora stylifera in the Bay of Villefranche
T. stylifera was rare in the first half of the year, increased in August, and dominated the zooplankton until November with a maximum of 60 individuals m–3 (CIV–VI). After a rapid decline in late November, individuals remained scarce until next summer (Figure 4A).
|
Prosome length varied between 747 and 1167 µm. Largest females occurred in February and November with a mean of 1040 and 1042 µm, respectively (Figure 4B).
Egg production of T. stylifera was similar in both years: decreasing during winter, then rising from 10 to 24 eggs female–1 d–1 May through July (Figure 4C). After another drop in late summer, egg production peaked in November to >33 eggs female–1 d–1. In March 1999, egg production completely ceased and females disappeared when salps appeared in high numbers in the Bay (Figure 4C). Females remained absent until May, and thereafter only a few females with moderate egg production rates were found until September.
Carbon content of adult females was measured only in autumn 1998, and was in the range 8.4–17.6 µg C female–1, with a mean of 12.4 µg C female–1 (Figure 4D).
The percentage of spawning females varied between 28% in March and 78% in December 1998. In 1999, no eggs were produced in March and April, while in May no females were found. The number of spawning females peaked in August and November with 75% and 70%, respectively (Figure 4E). Egg viability was 83% in June 1998 and ranged from 65% to 91% in November 1998 (Figure 5D).
|
Centropages typicus in the Bay of Villefranche
In contrast to T. stylifera, C. typicus was found in highest numbers in spring, with a maximum of 330 individuals m–3 (CIV–VI) in May 1998 (Figure 4F). The population began to decline in June; this continued to the end of the year.
Female prosome length ranged from 850 to 1277 µm (Figure 4G). Females were largest in winter. Smallest females were recorded in July 1998 and at the end of May 1999, respectively.
Annual patterns of egg production were similar to those observed for T. stylifera (Figure 4H). Adult females were rare in the samples in autumn 1997, but reproduction rates were relatively high, exceeding 20 eggs female–1 d–1. In winter and spring, egg production ranged between 10 and 20 eggs female–1 d–1 and peaked in summer with 26 eggs female–1 d–1. While egg production rates increased during September and October 1998 to the maximum of 33.5 eggs female–1 d–1, reproduction was more variable in 1999 during this period. Maximal egg production rates occurred in November in both years. Females contained between 4.3 µg C (March 1999) and 10.0 µg C (November 1998), with a mean of 6.7 µg C (Figure 4I). Proportions of spawning females reflected the continuous reproduction and showed a parallel decrease in spring in both years and lowest values in May (25% in 1998; 29% in 1999). The highest numbers of reproducing females were recorded in autumn and winter (Figure 4J).
In June 1998, 83% of the incubated eggs hatched, and in November and December 91% and 100%, respectively. In spring 1999, mean hatching success decreased from 94% in March to 71% in May. On 18 May, only 6% of the incubated eggs were viable (Figure 5E).
|
Discussion |
|---|
|
TopIntroductionMaterial and methodsResultsDiscussionReferences |
|---|
We present a synthesis of life cycles that are summarized schematically in conceptual models (Figures 6, 7). Our interpretations are based on three different types of data: (i) detailed multi-annual analyses that provide a clear depiction of certain aspects of the life cycle, e.g. abundance, egg production rates, and prosome lengths, (ii) sporadically measured parameters that are likely to have effects on copepod life history, e.g. hatching rates, carbon content, categories of food items, presence/absence of competitors, and (iii) hypotheses on traits that are rarely measured or lacking, but crucial for a complete understanding of copepod life strategies, e.g. the succession of generations, the production of resting eggs, the importance of mortality due to cannibalism and/or predation, potentially harmful effects of prey, inter- and intraspecific competition, etc. These interpretations complement the analyses for a more complete picture of the life cycles and should be considered as prospective topics for future research that may validate or reject our suggestions.
|
|
Life cycles at Helgoland Roads
Figure 6 is a summary of the life cycles of T. longicornis, C. hamatus, and C. typicus at Helgoland Roads and combines information on (from top to bottom): the seasonal temperature cycle as inversely related to prosome length; a hypothetical succession of generations deduced from body sizes, temperatures, and published developmental rates (Halsband-Lenk et al., 2002); female carbon content relative to the annual mean; seasonal abundance and egg production patterns; and hypothetical over-wintering strategies. Hypotheses are indicated with question marks.
T. longicornis was present throughout the year in the waters around Helgoland (Figure 6), similar to Roscoff, where Le Ruyet-Person et al. (1975) suggested a cycle of five generations derived from abundance and body size patterns. At Helgoland, we suggest that the first generation, consisting of the largest and most reproductive females, appeared in March and lasted until early May. The second (May–June) and third generations (July–August) were characterized by a gradual decrease in body size. After intense recruitment, the fourth generation was recorded from the end of August to mid-October. Owing to a lack of data in late autumn, we do not know whether a fifth generation follows, but the last generation persisted until February, when new large females developed.
T. longicornis bred continuously throughout the year, although egg production rates and the number of spawning females were low in winter. Low spawning activity resulted either from spawning intervals >24 h at low temperature (Hirche, 1990), or from a high percentage of young, immature females in spring. In summer, the population had reached a steady state with a constant proportion of 80% mature females. An increasing percentage of senescent females diminished spawning activity in autumn. T. longicornis is known to produce resting eggs in addition to subitaneous eggs (Lindley, 1986, 1990), which might contribute to a rapid recruitment in early spring (Le Ruyet-Person et al., 1975). Reproduction rates were maximal in April, moderate in summer, and further declined during autumn. A comparable cycle was reported from the Kattegat by Kiørboe and Nielsen (1994). In conclusion, T. longicornis is a typical neritic boreal species, with reproduction and population growth adapted to cold temperatures and a recruitment strategy that benefits from the shallow shelf, where buried eggs can hatch and add to the population.
Female C. hamatus first appeared in March/April and were present until the end of October. Then they were absent from the water column until April, although in the Kattegat (Kiørboe and Nielsen (1994)) and in the English Channel (Le Ruyet-Person et al., 1975) the species is recorded year round. A stock seems to persist in specific areas of the North Sea during winter (Rae and Rees, 1947). McLaren (1978) found eight generations of C. hamatus in Loch Striven (Scotland), while Martens (1980) stated that C. hamatus had longer generation times than T. longicornis in the German Wadden Sea. Le Ruyet-Person et al. (1975) identified five generations off Roscoff: the first generation (largest females) developed from March to April. The second generation was May and June, the third generation June and July, and the fourth mid-August to early September. The last generation persisted with a few specimens until February. At Helgoland Roads, we propose three to four generations per year (Figure 6). No over-wintering C. hamatus were found in the water column and were probably replaced by resting eggs (Lindley, 1986, 1990), which developed to adults during February/March when first females were recorded in the samples. The species is known to produce true diapause eggs (Pertzova, 1974; Marcus, 1989; Chen and Marcus, 1997) which follow a genetic protocol and require a defined refractory phase before hatching can take place. Like T. longicornis, the reproductive maximum was in early May, shortly after the first adult females emerged. In early summer, reproduction rates declined before a second smaller peak in August and September. C. hamatus is a cold-water summer species with a strategy to persist in unfavourable winter conditions in a resting life stage.
While C. typicus has been considered as a rare or sporadic immigrant in the North Sea or was not mentioned at all in earlier studies (e.g. Rae and Rees, 1947; Wiborg, 1955; Hickel, 1975; Fransz, 1975), it has become more abundant in the last decade (present study). The large interannual variability in timing of the first appearance of adults at Helgoland indicates that occurrence in this area is dependent either on advection of Atlantic Water into the German Bight (Fransz et al., 1991; Hay et al., 1991), or on favourable conditions for the species. Le Ruyet-Person et al. (1975) deduced a perennial distribution of C. typicus in the waters off Roscoff, but noted lower abundance there compared to C. hamatus. They proposed five generations with major peaks in June, July, and August. Abundance and length frequency data from Helgoland Roads were scarce and thus the number of generations could not be estimated properly (Figure 6). C. typicus probably colonized the German Bight coming from the warmer waters south of the British Isles and became most abundant in late summer and autumn towards the end of the reproductive period. Maximal reproduction occurred later in the year than in the other species, mainly in September and October in 1995, similar to the Kattegat (Kiørboe and Nielsen, 1994). However, after 1999 an extension of the reproductive period was observed, with high reproduction already in June or April. Lindley (1986) reported resting eggs for C. typicus, which have not been observed by other authors (e.g. Smith and Lane, 1987). They seem to play at best a minor role for C. typicus. Eggs found along the British Coast (Lindley, 1986, 1990) may be quiescent rather than true diapause eggs, persisting for a certain time under unfavourable conditions. Therefore, it is not yet clear if C. typicus maintains a continuous population with or without over-wintering stages. The biological cycle of C. typicus is clearly different from the two other northern species. Although the annual body size cycle responded similarly to temperature, carbon content did not and reproduction patterns were different. This supports the hypothesis that the population is not indigenous in the German Bight, but might have grown in warmer waters, e.g. in the English Channel (Le Ruyet-Person et al., 1975; Krause et al., 1995). However, very recently (2001), the species has increased considerably at Helgoland Roads. Whether this is exceptional, induced by a singular inflow event (Edwards et al., 1999), or a long-term trend (Lindley and Batten, 2002), remains to be determined.
Life cycles in the Bay of Villefranche
Figure 7 presents the life cycles of the Mediterranean populations (structure as for Figure 6). T. stylifera reproduced almost all year long in the Bay of Villefranche. The population developed to its maximum abundance only in late summer and autumn, however, possibly due to competition from C. typicus, which dominates in spring and early summer (Razouls, 1974). The peak in body size and reproduction of T. stylifera in November was followed by decline of the population at the end of the year. It is not clear whether T. stylifera developed five to seven generations as suggested by Le Ruyet-Person et al. (1975) for the Gulf of Lion. Individual numbers were at times low and the species virtually disappeared during the salp bloom in 1999. Thus, the number of generations might vary from year to year. In contrast to C. typicus, abundance and reproduction maxima of T. stylifera coincided during the cooling phase in autumn. Sensitivity of female survival and reproduction to high temperatures were confirmed in tolerance experiments (Halsband-Lenk et al., 2002) and revealed a preference for moderate warm temperatures. As a result, the life cycle of T. stylifera in the Bay of Villefranche appeared as a balance between the interaction with the co-dominant C. typicus and temperature tolerance. However, T. stylifera was adapted to the warm environment and differed clearly from its northern congener T. longicornis.
C. typicus generally peaked in April (Gilat et al., 1965, this study) and the first generation growing up in March and April reached the highest abundance (Figure 7). Despite scarce data coverage in late summer, we suggest four to six more generations until the end of November, according to Le Ruyet-Person et al. (1975). Due to continuous reproduction and fast development during the warm summer, we can assume more generations than in the boreal North Sea. C. typicus breeds continuously in the Gulf of Marseille (Gaudy, 1971), the Gulf of Lion (Razouls, 1975), the Gulf of Naples (Ianora and Buttino, 1990; Ianora et al., 1992), and the Bay of Villefranche (Halsband-Lenk et al., 2001). The reproductive cycle is similar to that of T. stylifera with maxima in autumn and lower rates during the remainder of the year. Consequently, abundance and reproduction peaks alternated. An unexpected recurring decline in the percentage of spawning females occurred in spring at a time of high primary production and independent of the presence of salps. We suggest three causes that have to be confirmed or rejected by future studies: first, decreasing numbers of reproducing females may indicate increasing senescence of females from the last generation, while young females were still immature. Second, the decline of spawning activity coincided with the abundance maximum of the population and could reflect intraspecific competition for space, food, and/or mating partners. Third, a defence strategy of certain phytoplankters could inhibit the reproductive output of their grazers (Ianora et al., 2003).
Inter-site variability
Reproduction was independent of food in the eutrophic North Sea and showed a pronounced seasonal cycle, primarily temperature-driven via its effect on body size, with the maximum in spring. Abundance peaks of all populations more or less overlapped in summer. Conditions in the Mediterranean appeared to be more stable, between seasons and between years. Low variation in temperature and food concentration was reflected in low but continuous reproduction. However, food limitation led to seasonal separation of competing species and food competitors (salps) had a high impact on reproduction. In contrast to the North Sea, the limiting food conditions seemed to affect not only reproduction rates, but also body weight and size in Villefranche, which showed phases of increase and decrease independent of the overlying seasonal trend (decreasing body size with increasing temperature).
Interannual variability
At Helgoland, interannual environmental variability was expressed most strongly as winter temperatures and phytoplankton concentrations. The waters around Helgoland are dynamic and influenced by advection of different water masses (e.g. Otto et al., 1990), with patchy distribution of copepods. Consequently, abundance maxima varied by a factor of up to 10 between years. Although we assume here that we are dealing with consistent populations, it is possible that copepod patches from different regions at times get mixed in the area because of advective processes and alter the size and stage structure of a given population.
The timing of adult female appearance was subject to annual changes in C. typicus, a species at the edge of its geographic distribution in this area. Females appeared only in September in 1995, but already in June 1999 (when sampling started in that year) and single reproductive individuals already in April 2000. They must be specimens of a new generation due to their great size, since over-wintered females from the preceding year would have been smaller. Also, maximal egg production rates of C. typicus increased from 30 eggs female–1 d–1 in 1995 to >100 eggs female–1 d–1 in 1999. Therefore, this species merits attention as an indicator of climate-induced changes in the plankton community of the North Sea.
Some aspects of interannual variation were similar in T. longicornis and C. hamatus and hence are attributed to external factors: first, the differences in female body weights, which were considerably higher in 1995 than in 1999, were partly reflected in egg production rates, but not in prosome lengths, possibly due to different food quality (Bonnet and Carlotti, 2002). Second, we recorded unusually low spawning activity in July 1996 and August 2000 in both species that remains unexplained. Inadequate or even toxic diets, increased costs for escape behaviour in the presence of predators or reduced food availability due to competition with other zooplankton could be possible reasons for this reduced reproductive output.
In Villefranche, no pronounced interannual variability was observed due to stable conditions in the Liguro-Provençal current that confines a homogenous coastal zone within 10–15 miles offshore (Prieur, 1981) with one exception: the bloom of salps in spring 1999 had a great impact on reproduction and abundance. Salps are efficient phytoplankton grazers (Anderson, 1985; Braconnot et al., 1988) and remove a large portion of food particles also used by herbivorous copepods. T. stylifera suffered in particular from the invasion of these competitors and ceased egg production before it disappeared from the samples for 2 months, probably due to starvation and a following lack of recruitment. C. typicus reproduction also decreased but could recover more rapidly after that, indicating a more omnivorous feeding behaviour and thus less competition pressure from the salps. These different responses to food competition may greatly affect population fitness in this oligotrophic environment and require further study.
Inter-specific analogies
Both in the North Sea and the Mediterranean, a remarkable parallel of some life-history traits was observed, despite different strategies: there was an apparent congruence of abundance, body size, and reproduction cycles of T. longicornis and C. hamatus at Helgoland Roads, despite different length of spawning periods and maximal reproduction rates. In addition, both are reported to produce resting eggs, although these were not distinguished in our experiments. This can be an important advantage on continental shelves, where conditions (e.g. temperature) might become extreme owing to the shallow water. Validation for the resting egg hypothesis is still needed, since strategies range from quiescence to genetically determined diapause and may underlie genetic plasticity and rapid evolutionary response if the, as yet unknown, environmental cues responsible vary between years or on a longer term (Katajisto, 2003).
Similar patterns were also observed off Villefranche, where reproduction of T. stylifera and C. typicus peaked at the same time, despite entirely different times of population increase. Hence, abundance did not reflect reproductive patterns and must be controlled by other factors, e.g. death rates. Information on mortality due to predation and/or cannibalism, however, is unavailable as yet.
|
Acknowledgements |
|---|
We thank W. Hickel and S. Dallot for providing hydrological data from the "Helgoland Roads Time-Series" (maintained by the Alfred Wegener Institute for Polar and Marine Research, Germany) and the "Point B" program (maintained by ESA 7076, the observation service "Rade de Villefranche" and SOMLIT, France), respectively. The manuscript has benefited from comments by D. L. Mackas and an anonymous reviewer.
|
Footnotes |
|---|
1 Present address: School of Oceanography, University of Washington, PO Box 357940, Seattle, WA 98195-7940, USA.
|
References |
|---|
|
TopIntroductionMaterial and methodsResultsDiscussionReferences |
|---|
-
Andersen V. (1985) Filtration and ingestion rates of Salpa fusiformis Cuvier (Tunicata: Thaliacea): Effects of size, individual weight and algal concentration. Journal of Experimental Marine Biology and Ecology 72:125–145.[CrossRef]
Bonnet D and Carlotti F. (2002) Development and egg production in Centropages typicus (Copepoda: Calanoida) fed different food types: a laboratory study. Marine Ecology Progress Series 224:133–148.[Web of Science]
Braconnot J.-C, Choe S.M, Nival P. (1988) La croissance et le développement de Salpa fusiformis Cuvier (Tunicata: Thaliacea). Annales de l'Institut d'Océanographie de Monaco Nouvelle Série 64:101–104.
Chen F and Marcus N.H. (1997) Subitaneous, diapause, and delayed-hatching eggs of planktonic copepods from the northern Gulf of Mexico: morphology and hatching success. Marine Biology 127:587–597.[CrossRef]
Edwards M, John A.W.G, Hunt H.G, Lindley J.A. (1999) Exceptional influx of oceanic species into the North Sea late 1997. Journal of the Marine Biological Association of the United Kingdom 79:737–739.[CrossRef][Web of Science]
Fransz H.G. (1975) The spring development of calanoid copepod populations in the Dutch coastal waters as related to primary production. 10th European Symposium on Marine Biology Ostend, Belgium 1975:247–269.
Fransz H.G, Haslund O.H, Wohlgemuth O. (1991) Development, growth and egg production of the two copepod species Centropages hamatus and Centropages typicus in the laboratory. Journal of Plankton Research 13:683–689.
Gaudy R. (1971) Étude expérimentale de la ponte chez trois espèces de copépodes pélagiques (Centropages typicus, Acartia clausi et Temora stylifera). Marine Biology 9:65–70.[CrossRef]
Gilat E, Kane J.E, Martin J.C. (1965) Study of an ecosystem in the coastal waters of the Ligurian Sea. Bulletin de l'Institut océanographique de Monaco 65:1–56.
Gomez F and Gorsky G. (2003) Microplankton annual cycles in the Bay of Villefranche, Ligurian Sea (northwest Mediterranean Sea). Journal of Plankton Research 25:323–339.
Halsband C and Hirche H.-J. (2001) Reproductive cycles of dominant calanoid copepods in the North Sea. Marine Ecology Progress Series 209:219–229.[Web of Science]
Halsband-Lenk C, Nival S, Carlotti F, Hirche H.-J. (2001) Seasonal cycles of egg production of two planktonic copepods, Centropages typicus and Temora stylifera, in the northwestern Mediterranean Sea. Journal of Plankton Research 23:597–609.
Halsband-Lenk C, Hirche H.-J, Carlotti F. (2002) Temperature impact on reproduction and development of congener copepod populations. Journal of Experimental Marine Biology and Ecology 271:121–153.[CrossRef][Web of Science]
Hay S.J, Kiørboe T, Matthews A. (1991) Zooplankton biomass and production in the North Sea during the Autumn Circulation Experiment, October 1987–March, 1988. Continental Shelf Research 11:1453–1476.[CrossRef][Web of Science]
Hickel W. (1975) The mesozooplankton in the Wadden Sea of Sylt (North Sea). Helgoländer wissenschaftliche Meeresuntersuchungen 27:254–262.[CrossRef][Web of Science]
Hickel W., Eickhoff E., Spindler H., Berg J., Raabe T., Müller R. (1997) Auswertung von Langzeit-Untersuchungen von Nährstoffen und Phytoplankton in der Deutschen Bucht. Umweltbundesamt. Texte 23/97. 215 pp.
Hirche H.-J. (1990) Egg production of Calanus finmarchicus at low temperature. Marine Biology 106:53–58.[CrossRef]
Ianora A. (1998) Copepod life history traits in subtemperate regions. 6th International Conference on Copepoda, Oldenburg/Bremerhaven (Germany), 29 Jul–3 Aug 1996. Journal of Marine Systems 15:337–349.[CrossRef][Web of Science]
Ianora A and Buttino I. (1990) Seasonal cycles in population abundances and egg production rates in the planktonic copepods Centropages typicus and Acartia clausi. Journal of Plankton Research 12:473–481.
Ianora A, Mazzochi M.G, Grottoli R. (1992) Seasonal fluctuations in fecundity and hatching success in the planktonic copepod Centropages typicus. Journal of Plankton Research 14:1483–1494.
Ianora A, Poulet S.A, Miralto A. (2003) The effects of diatoms on copepod reproduction: a review. Phycologia 42:351–363.[Web of Science]
Katajisto T. (2003) Development of Acartia bifilosa (Copepoda: Calanoida) eggs in the northern Baltic Sea with special reference to dormancy. Journal of Plankton Research 25:357–364.
Kiørboe T and Nielsen T.G. (1994) Regulation of zooplankton biomass and production in a temperate, coastal ecosystem. 1. Copepods. Limnology and Oceanography 39:493–507.[Web of Science]
Krause M, Dippner J.W, Beil J. (1995) A review of hydrographic controls on the distribution of zooplankton biomass and species in the North Sea with particular reference to a survey conducted in January–March 1987. Progress in Oceanography 35:81–152.[CrossRef][Web of Science]
Le Ruyet-Person J, Razouls C, Razouls S. (1975) Biologie comparée entre espèces vicariantes et communes de copépodes dans un écosystème néritique en Méditerranée et en Manche. Vie Milieu 25:283–312.
Lindley J.A. (1986) Dormant eggs of calanoid copepods in sea-bed sediments of the English Channel and southern North Sea. Journal of Plankton Research 8:399–400.
Lindley J.A. (1990) Distribution of overwintering calanoid copepod eggs in sea-bed sediments around southern Britain. Marine Biology 104:209–217.[CrossRef]
Lindley J.A and Batten S.D. (2002) Long-term variability in the diversity of North Sea zooplankton. Journal of the Marine Biological Association of the United Kingdom 82:31–40.[Web of Science]
Marcus N.H. (1989) Abundance in bottom sediments and hatching requirements of eggs of Centropages hamatus (Copepoda: Calanoida) from Alligator Harbor region, Florida. Biological Bulletin of Marine Biology Laboratory, Woods Hole, Massachusetts 176:142–146.
Martens P. (1980) Beiträge zum Mesozooplankton des Nordsylter Wattenmeers. Helgoländer wissenschaftliche Meeresuntersuchungen 34:41–53.
McLaren I.A. (1978) Generation lengths of some temperate marine copepods: estimation, prediction, and implications. Journal of the Fisheries Research Board Canada 35:1330–1342.
Otto L, Zimmermann J.T.F, Furnes G.K, Mork M, Saetre R, Becker G. (1990) Review of the physical oceanography of the North Sea. Netherlands Journal of Sea Research 26:161–238.
Pertzova N.M. (1974) Life cycle and ecology of a thermophilus copepod Centropages hamatus in the White Sea. Zoologichesky Zhurnal 53:1013–1022 (in Russian).
Prieur L. (1981) Hétérogénéité spatio-temporelle dans le bassin Liguro Provençal. Rapports de la Commission Internationale pour l'Exploration Scientifique de la Mer Méditerranée 29:35–36.
Rae K.M and Rees C.B. (1947) Continuous plankton records: the copepoda in the North Sea, 1938–39. Hull Bulletins of Marine Ecology 11:95–132.
Razouls C. (1974) Variations annuelles quantitatives de deux espèces dominantes de copépodes planctoniques Centropages typicus et Temora stylifera de la région de Banyuls: cycles biologiques et estimations de la production. III. Dynamique des populations et calcul de leur production. Cahiers de Biologie Marine 15:51–88.[Web of Science]
Razouls S. (1975) Fécondité, maturité sexuelle et différenciation de l'appareil génital des femelles de deux copépodes planctoniques: Centropages typicus et Temora stylifera. Pubblicaziones della Stazione Zoologica di Napoli 39:297–306.
Razouls S. (1982) Étude expérimentale de la ponte de deux copéodes pélagiques Temora stylifera et Centropages typicus. II. Dynamique des pontes. Vie et Milieu 32:11–20.
Riemann B, Simonsen P, Stensgaard L. (1989) The carbon and chlorophyll content of phytoplankton from various nutrient regimes. Journal of Plankton Research 11:1037–1045.
Smith S.L and Lane P.V.Z. (1987) On the life history of Centropages typicus: responses to a fall diatom bloom in the New York Bight. Marine Biology 95:305–313.[CrossRef]
Wiborg K.F. (1955) Zooplankton in relation to hydrography in the Norwegian Sea. Fiskeridirektoratets skrifter, Serie Havundersókelser 11:1–6.
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  E. Gentsch, T. Kreibich, W. Hagen, and B. Niehoff Dietary shifts in the copepod Temora longicornis during spring: evidence from stable isotope signatures, fatty acid biomarkers and feeding experiments J. Plankton Res., January 1, 2009; 31(1): 45 - 60. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. Devreker, S. Souissi, J. Forget-Leray, and F. Leboulenger Effects of salinity and temperature on the post-embryonic development of Eurytemora affinis (Copepoda; Calanoida) from the Seine estuary: a laboratory study J. Plankton Res., March 1, 2007; 29(suppl_1): i117 - i133. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||