Biol. Bull. 216: 335-343. (June 2009)
© 2009 Marine Biological Laboratory
Feeding Ability of Early Zoeal Stages of the Norway Lobster Nephrops norvegicus (L.)
Patricia N. Pochelon1,2,*,
Ricardo Calado1,
Antonina Dos Santos2 and
Henrique Queiroga1
1 CESAM, Departamento de Biologia, Campus Univeristario Santiago, Universidade de Aveiro, 3810 Aveiro, Portugal
2 Instituto Nacional de Recursos Biológicos–IPIMAR, Avenida de Brasilia s/n, 1449-006 Lisbon, Portugal
* To whom correspondence should be addressed. E-mail: ppochelon{at}ua.pt
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Abstract
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The wide geographical distribution of the Norway lobster, Nephrops norvegicus, results in a delay, with latitudinal decrease, in the larval season from spring to winter. Newly hatched larvae of the species may therefore be exposed to suboptimal levels or types of prey and face intermittent periods of starvation at low latitudes. This work investigated the feeding response of the first two zoeal stages of N. norvegicus under variable prey densities, prey types, feeding histories, and photoperiods. Both zoeae (Z) I and II increased the number of consumed prey with increasing food levels. ZI preferred Artemia sp. nauplii over larger metanauplii, while in ZII, higher ingestion was observed only for metanauplii at higher food concentrations. The number of prey ingested by larvae previously starved or under low food conditions was always higher than that of larvae exposed to high food levels. These findings seem to indicate that larvae may maximize prey ingestion in the presence of plankton patches with higher food abundance and minimize the deleterious effects induced by previous periods of intermittent starvation or unsuitable prey densities or types. Extreme photoperiods (24 and 0 h of light) did not improve larval feeding ability and are not a suitable option for larviculture.
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Introduction
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The Norway lobster, Nephrops norvegicus (Linnaeus, 1758), is a commercially important benthic decapod crustacean commonly found in northeastern Atlantic waters from the coast of Iceland to Morocco and in the Mediterranean Sea (d'Udekem d'Acoz, 1999). Its depth range extends from 15 to 800 m, although it is typically found on the northeastern Atlantic shelf at depths between 300 and 600 m (Tuck et al., 1997) and beween 200 and 800 m in the Mediterranean (Maynou and Sardà, 1997). In addition to differences in the depth range, the reproduction period of this species also varies latitudinally, with average embryo incubation being 10 months in the northeastern Atlantic but only 6 months in the Mediterranean (Sardà, 1995). These differences in embryo incubation duration are known to affect the hatching period of N. norvegicus larvae, with hatching occurring by early spring in the northeastern Atlantic and at the end of winter in the Mediterranean (Rotlland et al., 2004). Off the coast of Portugal, adults are encountered at depths ranging from 400 to 800 m, and the hatching period extends from December until April with, however, larval release peaking earlier in the south than the north. Under these scenarios, early larval development at the end of winter will occur in a nutritionally poor environment, since the chlorophyll a peak occurs only during spring (Moita, 2001; Santos et al., 2007). Late larval release will overlap with the beginning of thermal stratification and spring bloom (Santos et al., 2007).
Regardless of geographical and seasonal differences in nutritional conditions, it is widely accepted that planktonic larvae are naturally subjected to intermittent periods of starvation or suboptimal prey availability due to the natural patchiness of plankton distribution in the oceanic environment (Pinel-Alloul, 1995; Folt and Burns, 1999; Andersen and Nielsen, 2002). Studies addressing larval feeding in clawed lobsters have highlighted how early larval feeding greatly affects development, since these organisms may not recover from nutritional stress if suitable food is not available shortly after hatching (Anger et al., 1985; Rotlland et al., 2001). Newly hatched N. norvegicus larvae from the Mediterranean are larger in size and richer in lipids and proteins than those from the Irish Sea, which emphasizes the major role that these features may play for larval survival in oligotrophic environments (Rotlland et al., 2004).
Larvae subjected to low food conditions use several feeding strategies and may either morphologically (Strathmann et al., 1993; Fenaux et al., 1994) or behaviorally (McConaugha, 2002) enhance their overall feeding efficiency. Planktonic larvae of many benthic species appear to have evolved a certain feeding plasticity in order to be able to feed over a broad range of prey sizes, types, and abundances (Strathmann and Bone, 1997; Hinz et al., 2001; McConaugha, 2002; Perez and Sulkin, 2005). By feeding on smaller or suboptimal food items, developing larvae may minimize the negative effects of low food density and avoid starvation. In fact, this feeding plasticity had already been documented in homarid lobsters, with the last zoeal stage of Homarus americanus being recorded to successfully perform suspension feeding rather than raptorial feeding, the most commonly recorded behavior (Barshaw and Bryant-Rich, 1988).
Despite the number of studies addressing the larval biology (Dickey-Collas et al., 2000a; Briggs et al., 2002; Rotlland et al., 2004; dos Santos and Peliz, 2005) and aquaculture potential (Figueiredo and Vilela, 1972; Anger and Puschel, 1986; Morais et al., 2001; Rotlland et al., 2001; Rosa et al., 2003) of N. norvegicus, little is known about the feeding ability of early zoeal stages.
Our objective was to assess the feeding ability of N. norvegicus zoea (Z) I and II under variable feeding scenarios and to identify the existence of feeding plasticity in these early zoeal stages. To this end, we investigated the feeding response of N. norvegicus ZI and ZII under variable prey densities, prey types, and previous feeding histories. Additionally, due to the current interest in the larviculture of N. norvegicus, mainly for restocking purposes, we also evaluated the effect of extreme photoperiods (24 and 0 hours of light) on prey consumption for both zoeal stages.
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Materials and Methods
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Larval production and selection
Five ovigerous females of Nephrops norvegicus were collected between February and April 2008 using baited traps near Peniche (west coast of Portugal), at an approximate depth of 400 m, and kept in the laboratory until their larvae hatched. Newly hatched larvae were either selected for the experiments described below or reared to the second zoeal stage using a recirculating larviculture system employing 20-l cylindrico-spherical culture tanks (see Calado, 2008, for further details). Larvae were fed daily with newly hatched Artemia sp. nauplii (San Francisco Bay Brand Inc., Newark, CA) supplied at a density of 5 nauplii per milliliter, with Artemia sp. cysts being incubated according to the procedures described by Sorgeloos et al. (1998). During the culture period, N. norvegicus larvae were maintained in constant darkness at 15 ± 1 °C in a temperature-controlled culture room. Natural seawater at a salinity of 35 was 1-µm-filtered, passed through activated carbon, and UV-irradiated before being used in the larviculture system. Larvae were only used in the experimental trials 24 h after hatching or molting to the second zoeal stage, to guarantee that the larval appendages involved in prey capture, manipulation, and ingestion were fully functional in tested specimens. Additionally, only those specimens displaying strong phototactic responses were selected for the experimental trials, since this behavior is commonly employed in crustacean aquaculture to evaluate larval quality (see Treece and Fox, 1993). In all experimental trials, larvae at both zoeal stages were placed individually in 40-ml plastic beakers with filtered seawater at a salinity of 35 in a climatized chamber at 15 ± 1 °C. Larvae recorded as dead or moribund (lying motionless in the bottom of the plastic beaker for prolonged periods but still beating the exopods of their pereiopods) at the end of experimental trials were discarded, and those replicates were repeated. To ensure a homogenized distribution of prey in the water column during the experimental trials, minimizing the positive phototactic behavior of larvae and dietary prey, each plastic beaker was gently aerated at a rate of about one air bubble per second.
Effect of prey densities and photoperiods
The feeding ability of N. norvegicus larvae was evaluated by providing both ZI and ZII with four densities of prey (Artemia sp. nauplii at 0.5, 1, 3, and 5 ml–1) under three photoperiods (24, 12, and 0 h of light). After 24 h, the number of live prey remaining in the plastic beaker was counted under a binocular stereomicroscope, with damaged Artemia sp. nauplii (e.g., missing one or both antenna or their abdomen) being considered as ingested. Five replicates were used for each treatment, for a total of 60 specimens (4 densities x 3 photoperiods x 5 replicates = 60) of each larval stage. The variable used to assess the feeding ability of both ZI and ZII was the total number of larval prey ingested after 24 h.
Effect of prey types and prey densities
We evaluated the combined effect of four prey types at four densities on the feeding ability of the first and second zoeal stages of N. norvegicus. The prey types were (1) Artemia sp. nauplii (Naup, average size 450 ± 10 µm); (2) Artemia sp. metanauplii (Meta, average size 590 ± 5 µm); (3) Artemia sp. metanauplii enriched with the commercial product Algamac 2000 produced by Aquafauna, Biomarine Inc., Hawthorne, CA (MetaAlga, average size 592 ± 7 µm); and (4) Artemia sp. metanauplii enriched with the spray-dried microalga Spirulina (MetaSpi, average size 591 ± 6 µm). The four prey densities were 0.5, 1, 3, and 5 prey per milliliter.
Prior to the experiment, Artemia enrichments were conducted according to the protocols described by Morais et al. (2001). The nauplii were kept for 16 h in 1-l beakers, at a maximum density of 50 ml–1, with strong aeration and 0.1 g of enrichment product per liter of seawater. The enriched metanauplii were placed in beakers, each containing one N. norvegicus larva which was allowed to feed for 24 h. Then the number of live Artemia remaining in each beaker was counted using the methods and criteria described above. Five replicates were used for each treatment, for a total of 80 specimens (4 prey types x 4 densities x 5 replicates = 80) per larval stage. The variable used to assess the feeding ability of both ZI and ZII under the experimental conditions was the total number of larval prey ingested after 24 h.
Effect of previous feeding histories
To investigate the feeding ability of N. norvegicus ZI and II with different feeding histories, larvae were acclimated for 12 h to three feeding scenarios: starvation, low prey density (0.5 ml–1), and high prey density (5 ml–1). After the 12-h acclimation period, larvae from each feeding scenario were placed at either low or high prey densities (dietary prey concentrations of 0.5 and 5 ml–1, respectively) for an additional 12 h. The dietary prey provided to ZI and ZII were newly hatched Artemia sp. nauplii and Artemia sp. metanauplii enriched with Algamac 2000, respectively. The two stages were not fed with the same prey item because they displayed a different preference in the experiment "Effect of prey types and prey densities." ZI ate more nauplii and ZII more MetaAlga. All trials were performed under a photoperiod of 12 h light :12 h dark. At the end of the experimental period, the number of live dietary prey was counted according to the criteria previously described. Five replicates were used for each treatment, for a total of 30 specimens (6 feeding histories x 5 replicates = 30) per larval stage. The variable used to assess the feeding ability of both zoeal stages was the total number of larval prey ingested in the 12 h following the end of the acclimation period.
Statistical analysis
The feeding ability of the two first zoeal stages of N. norvegicus under the first two experimental conditions was compared using multi-way factorial analysis of variance (ANOVA). The factors tested for each ANOVA were prey density (4 levels), photoperiod (3 levels), and zoeal stage (2 levels) for the experiment "Effect of prey densities and photoperiods"; and prey type (4 levels), prey density (4 levels), and zoeal stage (2 levels) for the experiment "Effect of prey types and prey densities." Finally, for the experiment "Effect of feeding histories," a one-way ANOVA (6 levels) was used separately for each zoeal stage. Statistical analyses were performed using the software STATISTICA 6.0 (StatSoft Inc., USA). Prior to analysis, assumptions were verified and data transformed whenever necessary. Whenever significance was accepted, at P < 0.05, the Tukey multiple comparison test was used (Zar, 1999). Average prey consumption is subsequently always reported with its standard deviation (mean ± SD).
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Results
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Effect of prey densities and photoperiods
There was a significant interaction between larval stage x light regime x prey density (ANOVA; df = 6, F = 7.77; P < 0.001). Feeding responses under either 0 h or 24 h of light differed according to prey density (Fig. 1). Zoeae I (ZI) average prey consumption was higher under the lowest and highest prey densities when exposed to 24 h of light (19.0 ± 0.7 and 112.0 ± 18.6 prey consumed, respectively) than in complete darkness (14.4 ± 0.3 and 96.0 ± 7.4 prey consumed, respectively). Under the three highest prey densities, ZI prey consumption was highest under 12 h of light. For ZII, average prey consumption under 24 h of light was the same as in complete darkness under all three of the lowest prey densities but was lower (83.6 ± 8.6 and 120.8 ± 13.1) at the highest prey concentration. Under all tested feeding densities, prey consumption of larvae at the second zoeal stage was significantly higher under 12-h illumination (17.2 ± 2.7, 34.2 ± 2.8, 99.0 ± 4.3, and 142.8 ± 4.1 prey consumed for larvae fed at prey concentrations of 0.5, 1, 3, and 5 ml–1, respectively; Fig. 1). Other general trends can also be observed, such as a significant overall increase of consumed prey with increasing food levels (from 15.6 ± 3.2 to 112.9 ± 21.7, df = 3, F = 1750.34; P < 0.001), for both larval stages and light regime experienced combined (Fig. 1). Additionally, prey ingestion for both zoeal stages varied significantly with light conditions (df = 2, F = 35.38; P < 0.001), but was identical for both stages under the same light regime (df = 1, F = 2.92; P = 0.91).
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Figure 1. Prey consumption of Nephrops norvegicus zoeal stages ZI and ZII under different prey densities and light conditions after a 24-h period. Prey concentration is expressed as the number of prey per milliliter. Light conditions are expressed as hour of illumination—that is, constant darkness (0 h), 12:12 light/dark photoperiod (12 h), and constant illumination (24 h). Error bars represent standard error. Different letters represent significantly different feeding rates.
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Effect of prey types and prey densities
A significant interaction between larval stage x prey type x prey density was observed (ANOVA; df = 9, F = 22.2; P < 0.001). For ZI at low prey density, the number of prey ingested did not differ across prey types (17.6 ± 2.2, 15.0 ± 0.7, 13.4 ± 1.3, and 12.8 ± 0.8 for Naup, Meta, MetaAlga, and MetaSpi, respectively; Fig. 2). However, as prey density increased, prey consumption of metanauplii was reduced. For a prey concentration of 1 ml–1, consumption of Naup and Meta were identical but higher than consumption of MetaAlga and MetaSpi. Finally, for the two highest prey densities, significantly more Naup were consumed than Meta, which, in turn, was consumed in higher quantities than MetaAlga and MetaSpi (P < 0.001). There was no significant difference (P > 0.972) in the number of ingested enriched metanauplii at all tested prey densities (Fig. 2). For ZII, number of prey ingested also did not differ among prey types when these were provided at the lowest concentration (17.2 ± 2.7, 19.4 ± 0.9, 19.2 ± 0.8, and 19.2 ± 0.8 Naup, Meta, MetaAlga, and MetaSpi, respectively; Fig. 2). However, under the two highest prey densities, consumption of Naup was always significantly lower (P < 0.001) than that of all metanauplii. Under all tested prey densities, consumption of Meta, MetaAlga, and MetaSpi was always similar (P > 0.999) (Fig. 2). Finally, larval feeding ability was significantly different between both zoeal stages, with ZI consuming less prey than ZII (stage; df = 1, F = 3802.3; P < 0.001).
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Figure 2. Prey consumption of Nephrops norvegicus zoeal stages ZI and ZII under different prey densities and prey type after a 24-h period. Prey concentration is expressed as the number of prey per milliliter. Tested prey types were Artemia nauplii (Naup), metanauplii (Meta), metanauplii enriched with Algamac 2000 (MetaAlga), and metanauplii enriched with Spirulina (MetaSpi). Error bars represent standard error. Different letters represent significantly different feeding rates.
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Effect of previous feeding histories
A significant effect of feeding history was recorded for both stages (ANOVA, ZI: df = 5, F = 1116.13, P < 0.001; ZII: df = 5, F = 1873.40, P < 0.001). Larvae of either stage previously starved for 12 h always consumed more prey than those allowed to feed under the higher or lower prey densities during the acclimation period (Fig. 3). However, exposing larvae to a higher (5 ml–1) or lower (0.5 ml–1) prey concentration during the acclimation period promoted different feeding responses by larvae subsequently placed under high or low food conditions (Fig. 3). Zoeae acclimated to low and high food concentrations did not show differences in the number of prey consumed (P > 0.999) when subsequently placed under low food concentrations (8.8 ± 0.4, and 9.2 ± 0.8 Naup consumed by ZI and 8.8 ± 1.3 and 9.0 ± 1.0 MetaAlga consumed by ZII, respectively). In contrast, larvae acclimated to low food conditions consumed significantly more prey (P < 0.001) than those acclimated to high food densities, when subsequently placed in high food conditions (69.4 ± 2.4 and 56.6 ± 4.7 Naup consumed by ZI, and 97.2s ± 4.1 and 84.4 ± 3.8 MetaAlga consumed by ZII, respectively; Fig. 3).
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Figure 3. Prey consumption of Nephrops norvegicus larvae under different prey densities previously acclimated to different prey densities after a 12-h period. The right (A) and left (B) portions of the figure depict the number of Artemia sp. consumed by Zoea 1 and Zoea 2, respectively. Low and high prey concentration represent densities of 0.5 and 5.0 Artemia sp. per milliliter, respectively. Zoea I and II were offered nauplii and metanauplii, respectively. Error bars represent standard error. For each zoeal stage separately, different letters represent significantly different feeding rates.
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Discussion
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In this study, prey consumption by larvae of Nephrops norvegicus increased with prey density (from 0.5 to 5 prey per milliliter). The number of prey ingested did not reach a plateau, suggesting that maximum prey consumption was not reached and would probably be attained only at higher prey densities. Successful culture of N. norvegicus larvae to the juvenile stage is possible using a diet of enriched Artemia sp. metanauplii, although survival to metamorphosis is always low (Figueiredo and Vilela, 1972; Anger and Puschel, 1986; Dickey-Collas et al., 2000b). In the present study it is possible that larval energetic requirements were not fulfilled. A lack of satiation is consistent with the observed linear increase in the number of ingested prey and supports the general belief that Artemia sp. is an inferior diet when compared to natural plankton such as copepods (Sorgeloos et al., 1998; Shields et al., 1999; Helland et al., 2003). As a result, energetic needs were not met. If the present study had been performed using natural food items, the tested prey densities may have produced different results, and food intake at higher densities would have stabilized at a saturation prey density. However, further experiments are needed to support this hypothesis.
Although consumption under low prey density was not affected by prey type or larval stage, larval ingestion under higher prey densities was influenced by these two factors. Concerning zoeal stage I (ZI), the smaller size and inferior swimming speed of Artemia sp. nauplii can explain the higher consumption recorded for this type of prey when compared to metanauplii. The lower consumption of enriched metanauplii, in comparison to unenriched ones, was probably due to their higher nutritional value, since unenriched and enriched metanauplii had similar sizes and swimming speeds. Feeding on enriched metanauplii may have caused ZI to reach satiation faster than when ingesting a similar number of less nutritive unenriched metanauplii. Therefore, the present results suggest that the nutritional value of food items in a plankton patch will directly influence the number of prey ingested by ZI of N. norvegicus. The quality of a prey item is likely to vary with its nutritional state, and this in turn affects larval feeding on that item (Dalsgaard et al., 2003). Therefore, larvae at the same development stage (thus with identical predatory ability) will capture and ingest different numbers of the same dietary item in a plankton patch, as a function of its nutritional value.
Regarding ZII, these larvae clearly displayed a preference for larger prey, eating significantly more metanauplii than nauplii. The small-sized Artemia sp. nauplii did not trigger a proper predatory response and promoted lower prey consumption. In larval decapods it is not unusual to record a shift in larval prey preference during development, with early stages preferring smaller food items and later stages preferring larger food (McConaugha et al., 1991). Nonetheless, larger stages continue to ingest smaller prey if these are available (Harvey and Epifanio, 1997), although larvae become increasingly selective at higher prey densities (Yúfera et al., 1984). In contrast to ZI, larvae in the second zoeal stage ingested similar numbers of enriched and unenriched Artemia sp. metanauplii. This similar feeding response to metanauplii may have been prompted by the fact that with neither prey type were the larvae able to reach satiation. Apparently, N. norvegicus ZII require larger or more nutritious dietary prey. In the wild this feeding response will result in a lower energetic intake if larvae dwell in a plankton patch dominated by prey with low nutritional quality. It is possible that many dietary prey types can be available in a plankton patch but that the one available at the highest concentration is not nutritionally balanced to support optimal zooplankton growth. Ultimately, these prey may occur at high concentration because they are avoided by feeding larvae (Mitra and Flynn, 2006a). At least under culture conditions, the nutritional inadequacy of prey items can result in partial starvation and lower growth and survival (Harvey and Epifanio, 1997). If developing N. norvegicus larvae are regularly exposed to suboptimal dietary prey, which they will ingest to avoid starvation, the resulting nutritional stress may still induce larval mortality. Therefore, to develop successfully, larvae must not only have regular access to suitable numbers of dietary items, but those items must also be nutritionally balanced.
Zoeal stages of decapods are not capable of long periods of sustained horizontal swimming and may not be able to remain in food patches (Harden Jones, 1980). This constraint will probably impair the ability of larvae to feed continuously throughout their ontogenic development (Pitchford et al., 2003). In the present research, early-stage N. norvegicus larvae increased the number of prey consumed after previously experiencing food deprivation or low prey abundance. These feeding behaviors may allow the larvae to overcome intermittent periods of starvation, or suboptimal feeding levels, caused by the natural patchiness of plankton and lack of suitable prey. A similar reaction would be expected in response to changes in food conditions due to variable prey composition caused by diel vertical migration of zooplankton (Forward, 1988). Although both zoeal stages displayed distinct prey preferences, larvae readily ingested all types of tested prey, even if these were "suboptimal" (e.g., the consumption of Artemia sp. nauplii by ZII).
Adjacent plankton patches are not always similar in their species composition and may vary in the shape, size, quantity, and quality of the prey they contain (Petrone et al., 2005). The plasticity displayed by N. norvegicus larvae in the prey types ingested may therefore be an important adaptation to pelagic life. Even though their yolk reserves may differ spatially and seasonally (Rotlland et al., 2004), the larvae of N. norvegicus do not exhibit primary lecithotrophy, being unable to advance to ZII in the absence of food (pers. obs.). Given the fact that, and as suggested by modeling studies (Gentleman et al., 2003; Mitra and Flynn, 2006b), the capability to maximize food intake when prey are available, regardless of their type or quality, can temporarily reduce the effects of starvation in oligotrophic winter conditions until suitable prey are available. In contrast, when the hatching of N. norvegicus occurs at the time of the spring bloom when prey items are more abundant and varied (dos Santos et al., 2007), adequate prey are more likely to be available for newly hatched and developing larvae. In that situation, optimal foraging theory would predict that a predator adopts the feeding behavior that generates the highest intake rate of energy, with the consumption of suboptimal prey being highly reduced (Kiørboe et al., 1996). However, no study has ever addressed the existence of potential morphological and behavioral constraints in N. norvegicus larvae that may mask or preclude optimal foraging. Thus the present results and those from previous laboratory studies addressing the feeding of Norway lobster larvae should be extrapolated with caution to a pelagic environment with complex plankton patch dynamics.
Larval feeding ability was affected by photoperiod duration, with the number of ingested prey being consistently superior when the light was on for 12 h, regardless of prey density or larval stage. However, responses to light may vary significantly during larval development of decapods (Bermudes and Ritar, 2008). Several studies on crustacean larvae (Starkweather, 1976; Gardner and Maguire, 1998; Teschke et al., 2007; Calado et al., 2008), and especially on spiny lobsters (Mikami and Greenwood, 1997; Bermudes and Ritar, 2008; Bermudes et al., 2008), have demonstrated that food intake, survival, and molt stage duration are positively impacted by the presence of any kind of periodic light regime. Although decapod larvae are good swimmers, true hunting behaviors (e.g., prey chasing) are not displayed, and these organisms rely solely on chance encounters with dietary prey (Gonor and Gonor, 1973; Epelbaum and Borisov, 2006). This feeding behavior has been termed "encounter feeding" by Berkes (1975). Since the swimming activity of many decapods increases in the presence of light (Forward et al., 1984; Sulkin, 1984), larvae will have increased chances of encountering dietary prey. However, constant illumination will increase energy expenditure and therefore reduce survivorship since larvae remain permanently active in the laboratory (Dawirs, 1982; Calado et al., 2008). Although feeding remained possible under constant darkness, despite a lower consumption rate, 24 h of light did not promote higher prey ingestion than 12 h of light. These results seem to indicate that N. norvegicus larvae may also feed during the dark:light interface, as already suggested for spiny lobster larvae (Bermudes and Ritar, 2008). Apparently, the occurrence of a light:dark phase optimizes larval growth and feeding performances, regardless of the duration of the light phase, suggesting that the transition between day and night is more important than the duration of the photoperiod itself (Starkweather, 1976; Bermudes and Ritar, 2008; Bermudes et al., 2008).
In conclusion, the results of the present study suggest that unsatiated N. norvegicus larvae are able to increase prey ingestion in the presence of plankton patches with higher food abundance. The feeding plasticity indicates that early-stage larvae may be able to withstand and recover from periods of suboptimal food conditions by switching prey preference and then increasing consumption once optimal foraging conditions are encountered. Both prey availability and prey size play a crucial role in the trophodynamics of developing N. norvegicus larvae. Extreme photoperiods resulted in lower prey consumption for both larval stages, and their use in larviculture of N. norvegicus is not recommended.
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Acknowledgments
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The authors thank Dr. M. Castro and the crew of the fishing vessel Praia Rosa for providing the ovigerous females; Susanna Perreira for technical support; and Fundação para a Ciência e a Tecnologia (scholarship SFRH/BD/27615/2006 and research project LobAssess; "Norway lobster stocks in Portugal: Basis for assessment using information on larval production and ecology" [POCI/BIA-BDE/59426/2004 and PPCDT/BIA-BDE/59426/2004]) from the Portuguese government for their financial support.
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Footnotes
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Received 14 October 2008; accepted 24 February 2009.
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Literature Cited
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Andersen, C., and T. Nielsen. 2002. The effect of a sharp pycnocline on plankton dynamics in a freshwater influenced Norwegian fjord. Ophelia 56: 135–160.[Web of Science]
Anger, K., and C. Puschel. 1986. Growth and exuviation of Norway lobster (Nephrops norvegicus) larvae reared in the laboratory. Ophelia 25: 157–167.[Web of Science]
Anger, K., V. Storch, V. Anger, and J. M. Capuzzo. 1985. Effects of starvation on moult cycle and hepatopancreas of Stage I lobster (Homarus americanus) larvae. Helgol. Mar. Res. 39: 107–116.
Barshaw, D., and D. Bryant-Rich. 1988. A long-term study on the behavior and survival of early juvenile American lobster, Homarus americanus, in three naturalistic substrates: eelgrass, mud, and rocks. Fish. Bull. 86: 789–796.
Berkes, F. 1975. Some aspects of feeding mechanisms of euphausiid crustaceans. Crustaceana 29: 266–270.
Bermudes, M., and A. J. Ritar. 2008. Response of early stage spiny lobster Jasus edwardsii phyllosoma larvae to changes in temperature and photoperiod. Aquaculture 281: 63–69.[Web of Science]
Bermudes, M., A. J. Ritar, and C. G. Carter. 2008. The ontogeny of physiological response to light intensity in early stage spiny lobster (Jasus edwardsii) larvae. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 150: 40–45.[Medline]
Briggs, R. P., M. J. Armstrong, M. Dickey-Collas, M. Allen, N. McQuaid, and J. Whitmore. 2002. The application of fecundity estimates to determine the spawning stock biomass of Irish Sea Nephrops norvegicus (L.) using the annual larval production method. ICES J. Mar. Sci. 59: 109–119.[Abstract/Free Full Text]
Calado, R. 2008. Marine Ornamental Shrimp—Biology, Aquaculture and Conservation. Wiley-Blackwell, Ames, IA.
Calado, R., G. Dionísio, C. Bartilotti, C. Nunes, A. dos Santos, and M. T. Dinis. 2008. Importance of light and larval morphology in starvation resistance and feeding ability of newly hatched marine ornamental shrimps Lysmata spp. (Decapoda: Hippolytidae). Aquaculture283: 56–63.[Web of Science]
Dalsgaard, J., M. St. John, G. Kattner, D. Müller-Navarra, and W. Hagen. 2003. Fatty acid trophic markers in the pelagic marine environment. Adv. Mar. Biol. 46: 225–340.[Medline]
Dawirs, R. R. 1982. Methodical aspects of rearing decapod larvae, Pagurus bernhardus (Paguridae) and Carcinus maenas (Portunidae) Helgol. Mar. Res. 35: 439–464.
Dickey-Collas, M., R. P. Briggs, M. J. Armstrong, and S. P. Milligan. 2000a. Production of Nephrops norvegicus in the Irish Sea. Mar. Biol. 137: 973–981.
Dickey-Collas, M., N. McQuaid, M. J. Armstrong, M. Allen, and R. P. Briggs. 2000b. Temperature-dependent stage durations of Irish Sea Nephrops larvae. J. Plankton Res. 22: 749–760.[Abstract/Free Full Text]
dos Santos, A., and A. Peliz. 2005. The occurrence of Norway lobster (Nephrops norvegicus) larvae off the Portuguese coast. J. Mar. Biol. Assoc. UK 85: 937–941.
dos Santos, A., A. M. Santos, and D. V. P. Conway. 2007. Horizontal and vertical distribution of cirripede cyprid larvae in an upwelling system off the Portuguese coast. Mar. Ecol. Prog. Ser. 329: 145–155.
d'Udekem d'Acoz, C. 1999. Inventaire et distribution des crustacés décapodes de l'Atlantique nord-oriental, de la Méditerranée et des eaux douces continentales adjacentes au nord de 25°N. Patrimoines Naturels (MNHN/SPN) 40: 1–383.
Epelbaum, A., and R. Borisov. 2006. Feeding behaviour and functional morphology of the feeding appendages of red king crab Paralithodes camtschaticus larvae. Mar. Biol. Res. 2: 77–88.
Fenaux, L., M. F. Strathmann, and R. A. Strathmann. 1994. Five tests of food-limited growth of larvae in coastal waters by comparisons of rates of development and form of echinoplutei. Limnol. Oceanogr. 39: 84–98.
Figueiredo, M. J., and M. H. Vilela. 1972. On the artificial culture of Nephrops norvegicus reared from the egg. Aquaculture 1: 173–180.
Folt, C. L., and C. W. Burns. 1999. Biological drivers of zooplankton patchiness. Trends Ecol. Evol. 14: 300–305.[Medline]
Forward, R. B., Jr. 1988. Diel vertical migration: zooplankton photobiology and behaviour. Oceanogr. Mar. Biol. Annu. Rev. 26: 361–393.
Forward, R. B., Jr., T. W. Cronin, and D. E. Stearns. 1984. Control of diel vertical migration: photoresponses of a larval crustacean. Limnol. Oceanogr. 29: 146–154.
Gardner, C., and G. B. Maguire. 1998. Effect of photoperiod and light intensity on survival, development and cannibalism of larvae of the Australian giant crab Pseudocarcinus gigas (Lamarck). Aquaculture 165: 51–63.[Web of Science]
Gentleman, W., A. Leising, B. Frost, S. Strom, and J. Murray. 2003. Functional responses for zooplankton feeding on multiple resources: a review of assumptions and biological dynamics. Deep-Sea Res. Part II 50: 2847–2875.
Gonor, S. L., and J. J. Gonor. 1973. Feeding, cleaning and swimming in larval stages of porcellanid crabs (Crustacea: Anomura). Fish. Bull. 71: 225–234.
Harden Jones, F. R. 1980. The nekton: production and migration patterns. Pp. 119–142 in Fundamentals of Aquatic Ecosystems, R. S. K. Barnes and K. H. Mann, eds. Blackwell Scientific, Oxford.
Harvey, E. A., and C. E. Epifanio. 1997. Prey selection by larvae of the common mud crab Panopeus herbstii Milne-Edwards. J. Exp. Mar. Biol. Ecol. 217: 79–91.[Web of Science]
Helland, S., B. F. Terjesen, and L. Berg. 2003. Free amino acid and protein content in the planktonic copepod Temora longicornis compared to Artemia franciscana. Aquaculture 215: 213–228.[Web of Science]
Hinz, S., S. Sulkin, S. Strom, and J. Testermann. 2001. Discrimination in ingestion of protistan prey by larval crabs. Mar. Ecol. Prog. Ser. 222: 155–162.
Kiørboe, T., E. Saiz, and M. Viitasalo. 1996. Prey switching behaviour in the planktonic copepod Acartia tonsa. Mar. Ecol. Prog. Ser. 143: 65–75.
Maynou, F., and F. Sardà. 1997. Nephrops norvegicus population and morphometrical characteristics in relation to substrate heterogeneity. Fish. Res. 30: 139–149.
McConaugha, J. 2002. Alternative feeding mechanisms in megalopae of the blue crab Callinectes sapidus. Mar. Biol. 140: 1227–1233.
McConaugha, J. R., P. A. Tester, and C. S. McConaugha. 1991. Feeding and growth in meroplanktonic larvae of Callinectes sapidus (Crustacea: Portunidae). Mem. Queensl. Mus. 31: 320.
Mikami, S., and J. G. Greenwood. 1997. Influence of light regimes on phyllosomas growth and timing of moulting in Thenus orientalis (Lund) (Decapoda: Scyllaridae). Mar. Freshw. Res. 48: 777–782.
Mitra, A., and K. J. Flynn. 2006a. Promotion of harmful algal blooms by zooplankton predatory activity. Biol. Lett. 2: 194–197.[Abstract/Free Full Text]
Mitra, A., and K. J. Flynn. 2006b. Accounting for variation in prey selectivity by zooplankton. Ecol. Model. 199: 82–92.[Web of Science]
Moita, M. T. 2001. Estrutura, variabilidade e dinâmica do fitoplâncton na costa de Portugal Continental [Structure, variability, and dynamics of phytoplankton in the Portuguese Mainland coast]. Ph.D. thesis, University of Lisbon, Portugal.
Morais, S., R. Calado, and L. Narciso. 2001. The effect of different live diets on the first zoeal stages of the Norway lobster Nephrops norvegicus (L.) (Crustacea: Decapoda). Pp. 393–396 in Larvi'01 Fish and Crustacean Larviculture Symposium, C. I. Hendry, G. Van Stappen, P. Wille, and P. Sorgeloos, eds. European Aquaculture Society, Special Publication No. 30, Ghent, Belgium.
Perez, M., and S. Sulkin. 2005. Palatability of autotrophic dinoflagellates to newly hatched larval crabs. Mar. Biol. 146: 771–780.
Petrone, C., L. B. Jancaitis, M. B. Jones, C. C. Natunewicz, C. E. Tilburg, and C. E. Epifanio. 2005. Dynamics of larval patches: spatial distribution of fiddler crab larvae in Delaware Bay and adjacent waters. Mar. Ecol. Prog. Ser. 293: 177–190.
Pinel-Alloul, P. 1995. Spatial heterogeneity as a multiscale characteristic of zooplankton community Hydrobiologia 300/301: 17–42.
Pitchford, J. W., A. James, and J. Brindley. 2003. Optimal foraging in patchy turbulent environments. Mar. Ecol. Prog. Ser. 256: 99–110.
Rosa, R., S. Morais, R. Calado, L. Narciso, and M. L. Nunes. 2003. Biochemical changes during the embryonic development of Norway lobster, Nephrops norvegicus. Aquaculture 221: 507–522.[Web of Science]
Rotlland, G., M. Charmantier-Daures, G. Charmantier, K. Anger, and F. Sardà. 2001. Effects of diet on Nephrops norvegicus (L.) larval and postlarval development, growth, and elemental composition. J. Shellfish Res. 20: 347–352.
Rotlland, G., K. Anger, M. Durfort, and F. Sardà. 2004. Elemental and biochemical composition of Nephrops norvegicus (Linnaeus 1758) larvae from the Mediterranean and Irish Seas. Helgol. Mar. Res. 58: 206–210.
Santos, A. M. P., A. Chícharo, A. dos Santos, T. Moita, P. B. Oliveira, Á. Peliz, and P. Ré. 2007. Physical-biological interactions in the life history of small pelagic fish in the Western Iberia Upwelling Ecosystem. Prog. Oceanogr. 74: 192–209.
Sardà, F. 1995. A review (1967–1990) of some aspects of the life history of Nephrops norvegicus. Pp. 78–88 in Shellfish Life Histories and Shellfishery Models, D. E. Aiken et al., eds. Selected papers from a Symposium held in Moncton, New Brunswick, 25–29 June 1990. ICES Marine Science Symposia, 199.
Shields, R. J., J. G. Bell, F. S. Luizi, B. Gara, N. R. Bromage, and J. R. Sargent. 1999. Natural copepods are superior to enriched Artemia nauplii as feed for halibut larvae (Hippoglossus hippoglossus) in terms of survival, pigmentation and retinal morphology: relation to dietary essential fatty acids. J. Nutr. 129: 1186–1194.[Abstract/Free Full Text]
Sorgeloos, P., P. Coutteau, P. Dhert, G. Merchie, and P. Lavens. 1998. Use of brine shrimp, Artemia spp., in larval crustacean nutrition: a review. Rev. Fish. Sci. 6: 55–68.
Starkweather, P. L. 1976. Influences of light regime on postembryonic development in two strains of Daphnia pulex. Limnol. Oceanogr. 21: 830–837.
Strathmann, R. R., and Q. Bone. 1997. Ciliary feeding assisted by suction from the muscular oral hood of phoronid larvae. Biol. Bull. 193: 153–162.[Abstract]
Strathmann, R. R., L. Fenaux, A. T. Sewell, and M. F. Strathmann. 1993. Abundance of food affects relative size of larval and postlarval structures of a molluscan veliger. Biol. Bull. 185: 232–239.[Abstract]
Sulkin, S. D. 1984. Behavioral basis of depth regulation in the larvae of brachyuran crabs. Mar. Ecol. Prog. Ser. 15: 181–205.
Teschke, M., S. Kawaguchi, and B. Meyer. 2007. Simulated light regimes affect feeding and metabolism of Antarctic krill, Euphausia superba. Limnol. Oceanogr. 52: 1046–1054.
Treece, G. D., and J. M. Fox. 1993. Design, Operation and Training Manual for an Intensive Culture Shrimp Hatchery. Texas A&M University, Sea Grant Collection Program, Galveston, TX.
Tuck, I. D., C. J. Chapman, and R. J. A. Atkinson. 1997. Population biology of the Norway lobster, Nephrops norvegicus (L.) in the Firth of Clyde, Scotland—I: Growth and density. ICES J. Mar. Sci. 54: 125–135.[Abstract/Free Full Text]
Yúfera, M., A. Rodriguez, and L. M. Lubián. 1984. Zooplankton ingestion and feeding behavior of Penaeus kerathurus larvae reared in the laboratory. Aquaculture 42: 217–224.[Web of Science]
Zar, J. H. 1999. Biostatistical Analysis. Prentice Hall, Upper Saddle River, NJ.
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Abstract
Introduction
