ICES Journal of Marine Science: Journal du Conseil Advance Access published online on February 25, 2008
ICES Journal of Marine Science: Journal du Conseil, doi:10.1093/icesjms/fsm193
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A modelling study of developmental stage and environmental variability effects on copepod foraging
1 Center for Coastal Physical Oceanography, Old Dominion University, 4111 Monarch Way, Norfolk, VA 23508, USA
2 Skidaway Institute of Oceanography, 10 Ocean Science Circle, Savannah, GA 31411, USA
Correspondence to J. D. Wiggert: Department of Marine Sciences, University of Southern Mississippi, 1020 Balch Boulevard, Stennis Space Center, MS 39529, USA. tel: +1 228 6883491; fax: +1 228 6881121; e-mail: jerry.wiggert{at}usm.edu
Wiggert, J. D., Hofmann, E. E., and Paffenhöfer, G-A. 2008. A modelling study of developmental stage and environmental variability effects on copepod foraging. – ICES Journal of Marine Science, 65 We used a stochastic Lagrangian model to study how behaviour contributes to copepod grazing success. The model simulates distinct foraging behaviours of Clausocalanus furcatus, Paracalanus aculeatus, and Oithona plumifera. Three sets of simulations were performed to investigate the effects of (a) prey-size preference; (b) variation in prey-size spectra; and (c) turbulence intensity on these species’ grazing rates. The size preference simulations demonstrate that, compared with copepodites, mature females have cell ingestion rates that are an order of magnitude lower, while carbon uptake is reduced by 35%. A prey spectrum that is skewed towards cells <6 µm promotes copepodite success because the basal metabolic needs of the adult females require a prey concentration of 850–1000 cells ml–1. Variations in turbulence intensity reveal distinct ecological niches, with stronger mixing favouring O. plumifera and stable conditions favouring C. furcatus. Differences in theoretically derived and simulated prey-encounter rates demonstrate that the hopping behaviour of O. plumifera provides an order of magnitude increase in prey encounter, whereas the feeding behaviour of C. furcatus can result in localized depletion of prey. These simulations highlight the importance of species-specific feeding behaviour in defining oceanic copepod distributions.
Keywords: copepod foraging, ecological niche, emergent behaviour, Lagrangian model, turbulence
Received 14 July 2007; accepted 7 November 2007.
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Introduction |
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 Top Introduction MethodsResultsDiscussionReferences |
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Copepod grazing depends on the linked biomechanical processes of sampling method, prey perception, and size preference (Paffenhöfer, 1998). Sampling method combines foraging ambit and the means of cell acquisition (e.g. direct contact or feeding current; Price et al., 1983; Bundy et al., 1993), while prey perception depends on sensory cues such as hydrodynamic signals or chemical trails (Demott and Watson, 1991; Kiørboe and Thygesen, 2001). Size preference depends on developmental stage, morphological characteristics, or overall prey concentration (Nival and Nival, 1976; Landry and Fagerness, 1988; Paffenhöfer and Lewis, 1990; Hansen et al., 1994). Adult copepod densities in the open ocean range from 50 to 500 ind. m–3 (Head et al., 2002; Peralba and Mazzocchi, 2004), and each species uses some combination of prey acquisition strategies to meet its nutritional requirement.
One environmental effect known to modulate predator–prey encounter rates is small-scale fluid turbulence (Peters and Marrasé, 2000; Yamazaki et al., 2002). The various copepod sampling methods are affected to different degrees by alterations in the turbulence field, which is believed to result in species distributions that track spatial variations in dissipation rate (Kiørboe and Saiz, 1995; Incze et al., 2001; Visser et al., 2001). A less direct effect stems from the spatial variability observed in prey-size spectra. As prey speciation shifts in response to changing environmental conditions, distinction in prey-size preference will differentially modify foraging success and growth rates of co-occurring copepod species.
Predator–prey encounter rates and planktivorous grazing are affected by variation in turbulence intensity (Rothschild and Osborn, 1988; Hill et al., 1992). The typical range of the Kolmogorov length scale in marine environments is 0.3–10.0 mm (Marrasé et al., 1990). The perceptive range of copepods varies notably among species and their developmental stages. As a quantifying example, this range has been estimated to be 0.5–1.4 mm for the calanoid copepod Diaptomus sicilis (Bundy et al., 1998). Combined, these characteristic length scales suggest that planktonic organisms (5–100 µm for typical prey; 0.5–3.0 mm prosome length for typical copepods) are unlikely to experience eddy-like motions associated with oceanic turbulence directly. Instead, the prevailing understanding is that turbulence effects operate through the accompanying laminar shear (Kiørboe and Saiz, 1995; Gargett, 1997; Peters and Marrasé, 2000). Analytical models of predator–prey interaction have revealed that the response curve for variation of grazing success with turbulence intensity is dome-shaped (Mackenzie et al., 1994). As turbulence intensity increases from negligible levels, the increased encounter rates lead to higher ingestion rates. However, as turbulence intensity increases further, predator response time begins to limit capture success, and a negative impact on ingestion rate manifests (Mackenzie et al., 1994; Jenkinson, 1995). Other factors of prey acquisition affected by increasing intensity of small-scale turbulence are reduced prey perception through signal degradation, feeding current alteration or disruption, and behaviour modification of both predator and prey (Marrasé et al., 1990; Yen, 2000; Franks, 2001; Visser and Stips, 2002; Saiz et al., 2003). Thus, the level of turbulence can differentially affect foraging success and ingestion rates of copepod species.
A Lagrangian individual-based model (IBM) that specifically includes observed foraging ambits and area(s) of perception for three copepod species has been developed (Wiggert et al., 2005). The species chosen, Clausocalanus furcatus, Paracalanus aculeatus, and Oithona plumifera, represent three of the most common genera found in tropical/subtropical waters (Gaudy et al., 2003; Huskin et al., 2004; Smith and Madhupratap, 2005). Clausocalanus furcatus is a fast, continuous swimmer that loops repetitively, then displaces vertically before re-establishing its characteristic looping motion (Mazzocchi and Paffenhöfer, 1999). Paracalanus aculeatus is a slow, continuous swimmer that generates a feeding current to entrain potential food particles and perceives food at a distance by chemoreception (Paffenhöfer, 1984, 1998). Oithona plumifera is an ambush predator that uses its long, feathered setae to sense the hydrodynamic signals of motile particles at a distance after jumping obliquely upwards every few seconds (Svensen and Kiørboe, 2000; Paffenhöfer and Mazzocchi, 2002). Through explicit inclusion of the acquisition methods of these species, the Lagrangian IBM provided insight into how these strategies contribute to the coexistence of these three species in a dilute prey environment. The strength of this modelling approach is that it allows for emergent behaviour through the application of a fundamental rule set that is based on observed biomechanical components.
In this study, the Lagrangian IBM is used to investigate the degree to which these distinct foraging strategies allow for shifts in competitive advantage between copepod species as their environmental conditions are modified. Simulations were performed to investigate how the three species respond to variation in (i) prey-size preference that reflects differences in species morphology or developmental stage; (ii) size spectrum of the available prey field, based on observed spectra from four euphotic zone depths; and (iii) magnitude of a randomizing velocity component that encompasses the typical range of upper ocean turbulence intensities.
The emergent behaviour from these simulations provides insight into the physical and biological factors that allow for persistence and coexistence of these three copepod species. The next section provides a description of the Lagrangian model and details of the simulations performed for this study. This is followed by a description of the results. The discussion section interprets these results within the context of current understanding of how copepods function within the oligotrophic environment. The final section provides conclusions stemming from this analysis as well as some perspective regarding observational needs that would allow further development of the Lagrangian IBM.
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Methods |
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TopIntroductionMethodsResultsDiscussionReferences |
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The Lagrangian IBM simulates the time evolution of the trajectory of a given particle at location
by
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| (1) |
) include passive sinking speed, isotropic turbulence, and active swimming, where applicable. The foraging behaviour of the three copepods is introduced through parameterizations that include sampling ambit, area of perception (AOP), and prey perception (size preference and prey–predator separation distance). The AOP and sampling ambit are species-specific and are based on observational characterizations. For the chosen copepod species, there are two basic ambits, continuous swimming or episodic jumps with suitable directional modification applied at each time-step that results in spiralling or essentially linear motion or hops that range from vertical to horizontal. A basic state for the ambit of each species is defined; then random perturbations are applied to an individual’s direction and speed at each time-step, resulting in a unique ambit for each individual within each experiment (example ambits are shown in Figure 3 of Wiggert et al., 2005). A similar random perturbation of the turbulent fluid environment that affects all tracked particles is applied. Through these randomizations of the copepods’ ambits and their environment, stochasticity is introduced into the simulations. Full details of the model’s configuration and parameterizations, and the randomization scheme just described are given in Wiggert et al. (2005). The modifications to prey perception, size spectrum, and turbulence formulation newly incorporated to perform this study are detailed in the following sections.
Prey perception and size spectra
The model domain consists of a 1-l volume of water in the upper water column of the oligotrophic ocean. The initial concentration of prey (3 x 105–3 x 106 individual cells per litre) is randomly distributed throughout this domain, and each is assigned a species-based palatability ranking. For each prey item within the AOP of a given copepod, two non-dimensional prey perception factors are applied that may reduce its palatability ranking. The first perception factor (
1) defines the range of cell sizes that are accessible to a given copepod. The observation-based cell capture efficiency developed by Bartram (1980) provides the basis for relating prey-size preference and prey diameter (dC) as:
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| (2) |
As dP is increased, the preferred range of cell sizes expands to include larger prey, and access to smaller cells is impaired (Figure 1), which is similar to the size-selection curves defined by Steele and Frost (1977). In this study, four values for dP were applied (10–40 µm, in 10 µm intervals) so that the impact on carbon uptake afforded by shifts in the range of available prey sizes (Figure 1) could be assessed (see group 1 simulations described below). These curves reveal that, at higher values of dP, access to larger cells is significantly extended, whereas access to cells with dC less than 10 µm is curtailed or eliminated. These shifts in preferred prey size represent different stages of copepod growth, with the maximum value of dP coinciding with mature females.
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The second perception factor (
2) linearly reduces prey palatability with distance from the copepod. This is applied as 2 = 1.0–0.2(r/ROI), where r is prey–predator distance and ROI is the radius of influence (see Figure 1 and Table II in Wiggert et al., 2005). Thus, 2 ranges down to 0.8 at the AOP boundary, whereas 1 ranges from 0 to 1 (Figure 1). The initial palatability ranking for each potential prey within a copepod’s AOP is multiplied by both 1 and 2. If its resulting rank remains above a prescribed threshold, the particle is consumed (details of this ranking procedure are given in Wiggert et al., 2005). In Figure 1, the two horizontal lines [2(r = 0) and 2(r = ROI)] illustrate how the range of accessible prey sizes is effectively reduced when prey are at the limits of a copepod’s AOP.
In this study, four prey spectra from the Sargasso Sea (Paffenhöfer et al., 2003) are used to investigate how variation in prey-size distribution affects carbon uptake and grazing success of the model’s copepod species (see group 2 simulations, described below). Spectrum 1 is from 15 m and within the surface mixed layer (Figure 2, Table 1). The sample depths for the other three spectra range from 75 to 140 m and are all within the seasonal pycnocline. For these three profiles, the depth of the deep chlorophyll maximum (DCM) is 
120 m. Thus, the prey fields represented in spectra 2 and 3 are above the DCM, whereas the one associated with spectrum 4 lies below it (see Figure 2 in Paffenhöfer et al., 2003). Spectrum 4 is taken as the standard prey field, because it most closely adheres to the mean distribution for all measured spectra. Prey spectrum 1 has fewer cells with equivalent spherical diameter (ESD) >10 µm and, in particular, the lowest contribution by the 10–20 µm partition. Spectrum 2 is distinguished by the predominance of cells in the 4–8 µm range, and cells >8 µm ESD are most prominent in spectrum 3 (Figure 2). For the latter two spectra, the 10–20 µm partition is more than 100% greater than in the standard spectrum. These prey spectra maximize the contrast in the 10–20 µm size class. To obtain a prey field when a given simulation is initialized, the values of the percentage of total prey population (C* in Table 1) are multiplied by the total cell concentration (CT).
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Impact of turbulence
Simulated prey motion consists of sinking and stochastic fluid motions (i.e. small-scale turbulence) with velocity magnitudes that are typical of isotropic turbulence within the surface mixed layer or pycnocline. Fluid motions on larger spatial scales (e.g. geostrophic flows or internal wave oscillations) are not included because they impact all particles equally. Particle sinking (ws) is determined for each individual cell using a modified form of the Stokes equation, which includes a randomizing modification to cell density that is representative of natural variability within the plankton population [see Equation (2) in Wiggert et al., 2005]. The turbulence velocity (
) contributes a random component to the velocity vector of each copepod and planktonic prey. It is applied as a maximum speed (UD), the magnitude of which is modified for each direction by a set of random amplitude coefficients (
) that are uniformly distributed between –1 and 1 as: |
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A new set of 
is determined for each individual at every time-step. The value of UD is held constant throughout a simulation. For simulations that investigate turbulence effects on predator–prey encounter rate (see group 3 simulations described below), UD was varied over 0.1–6.0 mm s–1, which encompasses the range associated with wind-driven turbulence within the upper ocean (Mackenzie et al., 1994; Jiménez, 1997; Maar et al., 2003). Because values of 
are randomly determined, the energy spectrum of 
is white, which is clearly inconsistent with the well-known red spectrum characteristic of isotropic turbulence (e.g. Lesieur, 1987). However, this model study focuses on how copepod foraging is affected by variations in the intensity of fluid perturbation over a realistic range in magnitude. Thus, accurate representation of the distribution of turbulence velocities within the mixed layer or upper thermocline was not necessary.
An analytical method for quantifying the effect of small-scale turbulence on predator–prey encounter was introduced by Rothschild and Osborn (1988) and subsequently refined by Evans (1989). These studies provide the following general expression for encounter rate (ZA) between a predator (copepod with speed UC) and prey within a given size partition (with speed UP and concentration CP) under the influence of turbulence of the form:
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| (4) |
[Equation (3)] is the turbulence r.m.s. velocity for particles separated by a distance O(CT–1/3). Parameter definitions and resulting values of ZA for the three copepod species are given in Table 2.
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and 6.5 mm s–1) using Equation (4) and a total prey concentration (CT) of 300 cells ml–1.Simulation details
In all simulations, ten copepods of the same species were introduced into the model domain, and between six and eight one-hour simulations were performed at each value of CT (300, 534, 950, 1700, and 3000 cells ml–1) for a given set of prey accessibility or environmental conditions (see simulation groups defined below). Ten individuals per simulation yields 60–80 realizations for each set of conditions and allows calculation of statistics to assess the stochastic effects of initial prey distribution, foraging ambits, and imposed turbulence velocities. As noted below, the model tracks carbon uptake through cell ingestion. However, copepod growth is not simulated, and an individual’s size remains fixed over the duration of these short simulations. The model boundaries are periodic so that any particle exiting one side of the 1-l volume reappears on the opposite side, which prevents loss of prey or an accumulation at the base of the model domain.
Two foraging-related rates calculated from the simulations were used as diagnostic variables. The first, encounter rate (ZM), was determined by summing the eaten and uneaten occurrences for the prey. When repeated, uneaten encounters occurred for a given cell over a finite succession of time-steps (usually 
4), only the first was counted as a distinct uneaten encounter in the determination of ZM. The others were disregarded because they represent an artefact of the discretized nature of numerical simulations. The second diagnostic is ingestion rate (I, cells h–1 ind.–1), which can also be used to calculate copepod carbon uptake (ng C h–1 ind.–1) by applying the cell diameter (dC) that is tracked for each individual prey. The transformation to carbon content is accomplished through use of the relation determined by Verity et al. (1992), the assumption of sphericity, and constant stoichiometry (i.e. variation in nutritional quality of prey is not included). The basal metabolic rate for each copepod species was estimated using the relations determined by Ikeda (1985) that apply a mean animal weight and a water temperature of 20°C. This rate provides a baseline for assessing the relative increase or decrease in carbon uptake in the various simulations. The ratio of ingestion rate to encounter rate (I:ZM) gives a measure of the efficiency of ingestion.
Three groups of simulations were performed. Simulation group 1 consists of varying the size range of preferred prey by modifying dP from 10 to 40 µm in 10 µm increments [Equation (2)]. The maximum value of dP was the standard condition used in Wiggert et al. (2005) and represents adult females. The shift in preferred prey size associated with lowering dP is a parameterization for developmental-stage-related differences in foraging behaviour. Shifting the preference curve in this manner provides for transition from young copepodites to mature adult females. For the other two simulation groups, only the smallest (10 µm) and largest (40 µm) values of dP are applied, and results are reported as associated with copepodites and adult females, respectively. Simulation group 2 consists of applying four prey spectra with distinct size distributions (Figure 2, Table 2). Imposing the four prey distributions allows us to investigate the effects of natural variation in prey-field composition on grazing rate. Simulation group 3 consists of applying individually randomized velocities [UD in Equation (3)], within a prescribed range of relatively low magnitude, to all prey. The stochastic velocity field represents small-scale isotropic turbulence, and varying the range of turbulence velocities simulates conditions typical of the upper pycnocline and those of the surface mixed layer.
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Results |
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Simulation group 1: prey-size preference as a proxy for copepod developmental stage
Rates of individual and mean carbon uptake are strongly affected by shifts in prey-size preference (Figure 3). The carbon uptake rate for C. furcatus (top row, Figure 3) increases with increasing forage. The range of simulated carbon uptake rates falls within the range of observed rates (Figure 3). Similar trends in the simulated carbon uptake rate were obtained for P. aculeatus (middle panels) and O. plumifera (bottom row). For all prey densities and copepod species, the range of the individual carbon uptake rates expands as dP increases. Thus, as size preference shifts towards large cells, successfully obtaining nutritional needs is increasingly hit or miss because cells with ESD >8 µm make up only 2.5–7% of the prey population (Table 1). This trend is accentuated at low CT (total prey concentration, cells ml–1). The other trend apparent in these results is that, as dP increases, mean carbon uptake steadily decreases for all CT (Figure 3). Between dP = 10 and 40 µm at maximum CT, the decrease in mean carbon uptake is 58 ng C h–1 ind.–1 for C. furcatus, 78 ng C h–1 ind.–1 for P. aculeatus, and 64 ng C h–1 ind.–1 for O. plumifera. It is interesting that the magnitude of carbon uptake at dP = 10 µm for these species (147 ± 3, 207 ± 9, and 181 ± 7 ng C h–1 ind.–1, respectively) is not statistically different from instances when dP = 20 µm. However, for all three species, the error bars are doubled.
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Considerable differences are apparent in each species’ success at achieving basal levels of carbon uptake at low CT and dP = 10 µm. Clausocalanus furcatus requires a prey density greater than 480 cells ml–1 to obtain its basic metabolic needs, whereas P. aculeatus meets these at
400 cells ml–1, and O. plumifera can attain its basic requirements at 300 cells ml–1 (Figure 3a–c). Extrapolating from the intercept of the mean uptake curve with the minimal metabolic condition, the prey concentration necessary for all three species to meet their basal needs increases by 65–75% between dP = 10 and 40 µm (Figure 3). For C. furcatus, the lowest prey concentration yields a number of individual carbon uptake rates at larger values of dP that exceed all of those obtained when dP = 10 µm (Figure 3a, d, g, and j). However, with increasing dP, it is clear that the mean rate of carbon uptake decreases monotonically. In contrast, for P. aculeatus (Figure 3b and k) and O. plumifera (Figure 3c and l), the maximal individual rate demonstrates a consistent decrease between the smallest and largest values of dP. The carbon uptake rate is determined by carbon content of grazed cells and the rate at which these cells are ingested. The latter is bounded by the preyen counter rate, which may be reduced by multiple encounters with the same cell. The cell-encounter rate and ingestion are linked through copepod perception, degree of satiation, cell size and predator–prey distance (Figure 1), and biomechanical limits, such as prey processing time. As expected, the simulated encounter rate for each species depends on CT and is essentially independent of dP (Figure 4a–c). At a given cell concentration, the encounter rate varies within a factor of 2 for the three copepod species (Figure 4). Over the full range of size preference, the ingestion rate for each species exhibits a range of more than an order of magnitude at a given CT (Figure 4d–f). The lower values of ingestion rate coincide with the preference shift towards large prey with higher nutritional content and limited access to small cells. In addition, the ingestion rate reveals a consistent linear dependence with cell concentration for all values of dP, except for some curvature at the higher cell concentrations that is only apparent when dP = 10 µm. This change in slope with increasing cell concentration occurs because the ingestion rate is approaching a plateau beyond which increased prey concentration has little effect.
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When dP = 10 µm, essentially all of the encountered cells are grazed at the lowest values of CT, whereas at maximal CT, 70% (P. aculeatus) to 85% (C. furcatus) of the encountered cells are consumed (Figure 4g–i). This reduction in the ratio of ingestion to encounter rate (I:ZM) with increasing prey concentration is the result of the plateau in ingestion rate (Figure 4d–f). For the other three values of dP, I:ZM is comparable for all three species of copepod and essentially constant with increasing cell concentration (Figure 4g–i). A slight increase occurs at the highest cell concentrations, with this increase being a consequence of the slightly reduced encounter rates at these concentrations (Figure 4a–c). The variation in encounter rate at high prey concentration is likely an artefact of the means of tallying encounters (described under the heading "Impact of turbulence"), because no adjustment has been made for ingested cells that were not eaten in immediately preceding time-steps. Thus, the encounter rates (Figure 4a–c) may be slightly inflated, especially at high cell concentrations when dP = 10 µm. An upper bound for this artefact can be ascertained by subtracting I (dP = 40 µm) from I (dP = 10 µm), which gives a range of 2–9 x 103 cells h–1 ind.–1 over all CT (Figure 4d–f).
The percentage of carbon contributed by individual prey-size partitions reveals that contributions differ by only 2–3% for all size preferences and partitions for the three species (Figure 5). With dP = 10 µm, the 2–4 and 4–6 µm partitions each provide 22–24% of the total diet, whereas the larger sizes are monotonically less prominent. Overall, the 10–20 µm partition provides 30% of the uptake (i.e. 6% per 2 µm partition) and, as expected, there is no contribution from the 20–40 µm partition (Curve 1, Figure 1). With dP = 20 µm, the contribution from the 2–4 µm partition drops to 8–10%, whereas the 4–6 µm partition is unchanged. Indeed, it is interesting that the four intermediate size partitions appear to allow the effect of the increase in dP to "pass through" to the two largest partitions (Figure 5b). Thus, the primary compensation to the reduced grazing on small cells is provided by the 20–40 µm partition, which contributes 8% to the total diet, with the 10–20 µm partition increasing slightly to 34%.
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With dP = 30 µm, the 2–4 µm partition no longer contributes, the contribution of the 4–6 µm partition is reduced by half, and the 6–8 µm partition increases to 18% and becomes the dominant small-cell diet source (Figure 5c). The most pronounced increase occurs in the 10–20 µm partition, which contributes 42% of the total diet, whereas the 20–40 µm partition rises to 14%. With dP = 40 µm, the 4–6 µm partition is also eliminated, whereas contributions from the 10–20 and 20–40 µm partitions increase to 53% and 18% of the total carbon uptake, respectively (Figure 5d). These percentage contribution characterizations apply over a range of cell concentrations. However, for individual values of CT, no trend is apparent (not shown), which indicates that perception is the factor determining the relative contribution of a given size prey to the total diet.
Simulation group 2: prey-size spectra
Dependence of mature females on distribution of prey size
With dP = 40 µm, the two smallest size partitions are completely eliminated, whereas the 6–8 µm partition contributes only marginally to the copepod diet (Figure 1). For this preference curve, prey spectrum 1 results in a significantly reduced likelihood that the basal metabolic rates of any of the three species will be met (Figure 6a–c). The mean carbon uptake rates indicate that attainment of metabolic needs requires 35–55% higher prey concentrations, with O. plumifera exhibiting the most pronounced change (Figure 3l vs. Figure 6c). Moreover, C. furcatus and P. aculeatus require prey concentrations above 103 cells ml–1 (Figure 6a and b). The combination of fewer prey in the 10–20 µm partition and the minimal contribution to the adult diet from cells <8 µm ESD results in the 8–10 µm partition making a greater contribution to the total carbon uptake than obtained for the standard prey spectrum (24% vs. 16%, Figures 5d and 7a), despite accounting for an equivalent proportion of the prey population (Figure 2). Thus, the overall reduction in carbon uptake resulting from prey spectrum 1 is a direct consequence of the reduced contribution made by large cells to the overall diet.
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For the size distributions in prey spectra 2 and 3, there is little difference in carbon uptake rate for the three species, and all meet basic metabolic costs at prey concentrations of 500 cells ml–1 or less (Figure 6d–i). This represents a reduction of 35–40% in the prey density required to achieve basal needs relative to the simulations with standard forage conditions (Figure 3j–l). Along with the higher rates of carbon uptake, the shift towards larger prey in spectra 2 and 3, combined with the adult copepod size preference, leads to I:ZM ratios (and therefore ingestion rates) that are
2.5 times greater than when spectra 1 or 4 are applied (Figure 6i–l). Also, there is little discernible difference in this ratio or the ingestion rates of the three species when these two spectra are applied. The primary difference in size-partitioned carbon contribution between spectra 2 and 3 and the standard prey distribution (spectrum 4) lies in the contribution of 10–20 µm prey (65–72% vs. 52%; Figures 5d and 7b and c). Prey spectrum 3 results in the largest percentage contribution to total carbon uptake (20%) by the 8–10 µm partition (compare Figure 7c with Figures 5d and 7b). The highest contribution from the 20–40 µm partition occurs when spectrum 4 is applied, although this partition is more prominently represented within spectrum 3 (Figure 2). Total carbon uptake is lowest when spectrum 4 is applied (Figures 3j–l and 6d–i), despite having the strongest relative contribution by large cells to the mature females’ diet. Thus, the overall make-up of the prey field (i.e. how prey is distributed over size class) contributes to the relative success of copepod foraging.
Dependence of copepodites on distribution of prey size
Copepodite preference for small prey (Figure 1) results in a reduction in carbon uptake for spectrum 1 compared with spectrum 4 of 20% for P. aculeatus (Figure 3b vs. Figure 8b) and <10% for the other two species (Figures 3a and c vs. 8a and c). Thus, compared with spectrum 4, the shift towards smaller prey in spectrum 1 exerts much less impact on the grazing success of the copepodites than on the mature females (Figure 6a–c). Furthermore, with this prey spectrum, all three species meet their minimal metabolic needs at a prey concentration of less than 550 cells ml–1 (Figure 8a–c), a density of small cells that is maintained even in the surface summertime mixed layer of oligotrophic subtropical waters (see Figure 3 in Paffenhöfer et al., 2003). The percentage of carbon contributed by the different prey-size partitions demonstrates that, in relation to spectrum 4 (Figure 5a), the 10–20 µm prey contribution is reduced from 30% to 20%. This reduction is compensated for by prey within the 2–6 µm partition that provides more than 50% of the total carbon acquired when spectrum 1 is applied (Figure 9a). Grazing by the copepodite stages on a prey field dominated by the smallest size classes (spectrum 1) is the only instance where the 10–20 µm size class does not rank as the single largest contributor to total carbon uptake (Figures 5, 7, and 9).
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(0.2 mm s–1) was used. Corresponding results for the standard prey distribution (spectrum 4) are shown in Figure
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When prey spectra 2 and 3 are applied, all three species achieve basal needs at the minimum prey concentration (300 cells ml–1, Figure 8d–i). The availability of larger cells within these prey distributions provides some advantage in the grazing success of the copepodites, but it is considerably reduced relative to that of the adult females. Nevertheless, for spectra 2 and 3, the 10–20 µm prey partition remains dominant. In both cases, this partition contributes
45% to the overall carbon uptake (Figure 9b and c), though this is a significant reduction from the 65–72% contribution that was evident for the mature copepods (Figure 7b and c). The relative differences in dominant prey partitions over the 4–10 µm cells (Figure 2) are more directly reflected in the percentage carbon distributions than was true for the adult female simulations, with spectrum 2 exhibiting a more pronounced contribution at 4–8 µm, and spectrum 3 featuring the 8–10 µm partition (Figure 9b and c).
Simulation group 3: effect of turbulence on predator–preyen counter rate and grazing success
Theoretical encounter rates (ZA)
Theoretical rates of predator–prey encounter (ZA, Table 2) were calculated using Equation (4) to establish a baseline for comparison with the variable turbulence simulations. For a given turbulence intensity, prey-partition-specific values of the theoretical encounter rate for each copepod species demonstrate that ZA varies with the different prey densities of each size class (CP) and the associated velocities (UP). This prey velocity combines sinking speed (ws under the heading "Impact of turbulence") with the individual velocities of motile prey. For the smallest size partition and no turbulence (
mm s–1), ZA differs by more than two orders of magnitude between species. Oithona plumifera exhibits a similar variation in the magnitude of ZA between the two turbulence intensity conditions. The most mobile species (C. furcatus) derives the least enhancement to encounter rate in turbulence waters (
mm s–1). Over the three species of copepod, it is apparent that this turbulence-derived enhancement in encounter rate varies inversely with each predator’s characteristic ambit speed (UC).
Variation of ZA with prey partition and turbulence intensity reveals that C. furcatus has the lowest overall range in ZA (Figure 10a). The gradient in ZA at low turbulence intensities is significantly sharper for P. aculeatus and in particular for O. plumifera (Figure 10b and c). All three species exhibit either a plateau or a local maximum in ZA associated with the 10–20 µm size class (Figure 10, size partition 5), which results from the lower number of cells in the 20–40 µm partition and the comparable population of the narrow 8–10 µm partition that has lower UP. The predominance of smaller prey results in the 2–4 µm partition consistently exhibiting the maximum values of ZA, which are more than 1.5 orders of magnitude greater than those for the 10–20 µm partition.
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Simulated encounter rates (ZM)
For each copepod species, the impact of turbulence intensity on encounter rates increases with increasing cell concentration (Figure 11a–c). Encounter rates for C. furcatus are somewhat reduced at the highest turbulence intensities, whereas P. aculeatus reveals no trend and O. plumifera exhibits an increase of
70% (Figure 11a–c). The ingestion-to-encounter-rate ratios (I:ZM) at all three prey concentrations demonstrate that the youngest copepodites consume essentially all encountered cells, especially at the lowest prey density (Figure 11d–f). However, although this ratio remains essentially 1 for C. furcatus as prey concentration increases, both P. aculeatus and O. plumifera exhibit a clear reduction, and values of 0.9–0.95 are obtained when CT = 950 cells ml–1 (Figure 11e and f). When UD exceeds 1 mm s–1, ZM for O. plumifera exhibits an increased slope that is most pronounced at the highest prey concentration (Figure 11c) and is reflected in I:ZM (Figure 11f). For the other two species, I:ZM exhibits no dependence on UD at a given prey concentration (Figure 11d and e). Maximal ZM for C. furcatus is slightly below 4 x 103 cells h–1 ind.–1, whereas that for P. aculeatus and O. plumifera slightly exceeds this value. In conjunction with the downward shift in the ingestion-to-encounter-rate ratio exhibited for the latter species, a threshold for encounter rate of 1 cell s–1 is indicated. Further, the downward trend apparent in this ratio at the higher turbulence intensities for O. plumifera suggests that this is biomechanical in nature and does not derive from short-term satiation.
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By integrating ZA (Figure 10) over size partition, direct comparison can be made between the simulated and theoretically derived rates (Figure 11a–c). For the two faster moving predators, ZA is constant at lower values of UD, then begins to increase monotonically above a threshold in turbulence intensity (Figure 11a and b). This break in the ZA curves occurs at
30% of the typical predator velocity. For O. plumifera, ZA consistently increases but is less than ZM until UD exceeds 3 mm s–1 (Figure 11c). Thus, the theoretical encounter rates reveal a transition between behaviourally controlled rates of predator–prey encounter and rates controlled by fluid turbulence. For C. furcatus, as UD exceeds 1 mm s–1, ZA increases while ZM trends downwards (Figure 11a). At the lower turbulence intensities where the theoretical rates are constant for C. furcatus, these compare most favourably with the modelled rates when CT = 534 cells ml–1. For P. aculeatus, the theoretical and modelled encounter rates (CT = 300 cells ml–1) exhibit excellent agreement for UD below 2 mm s–1. The theoretical result approaches 104 cells h–1 ind.–1 at maximum UD, although even at a prey concentration of 950 cells ml–1, the modelled encounter rates remain below 5 x 103 cells h–1 ind.–1 (Figure 11b). However at the two highest prey concentrations (1700 and 3000 cells ml–1), ZM for youngest copepodites exceeds 104 cells h–1 ind.–1 at standard UD (Figure 4b). For O. plumifera, ZA agrees well with ZM at only the highest values of UD and is an order of magnitude lower than ZM in quiescent or reduced intensity regimes (Figure 11c).
Effect of turbulence intensity on carbon uptake
Carbon uptake dependence on turbulence intensity for the copepodites and mature females (Figure 12) exhibits the same general decrease as size preference shifts towards larger prey that was noted earlier (Figure 3). Increasing UD gives the same general carbon uptake trends as obtained for the encounter rates for each species (Figure 11a–c). Clausocalanus furcatus exhibits a consistent decrease in uptake that is most pronounced at the higher turbulence intensities (Figure 12a and d); P. aculeatus exhibits little discernible trend (Figure 12b and e); and O. plumifera exhibits increasing carbon uptake especially for UD above 1 mm s–1 (Figure 12c and f). Independent of turbulence level, C. furcatus (Figure 12a and d) and P. aculeatus (Figure 12b and e) are unable to achieve basal requirements at the lowest prey density (CT = 300 cells ml–1). Mean carbon uptake for the copepodite stage of O. plumifera is just below basal rates at low UD and surpasses this threshold when UD exceeds 1 mm s–1 (Figure 12c). For the most energetic turbulence regime, mean uptake for mature females is just below the basal rate (Figure 12f).
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Carbon uptake as a function of prey size and turbulence velocity differs for the three species and for the prey-size preferences exhibited by copepodites (Figure 13a–c) and mature females (Figure 13d–f). Consistent with the results described for the size preference simulations (Figure 5a, under the "Results" heading), the largest size partition is eliminated as a nutritional source when dP = 10 µm (Figure 13a–c). For C. furcatus, prey in the 10–20 µm partition make the greatest contribution to overall uptake, followed by prey in the 2–4 µm partition (Figure 13a). Total carbon uptake is reduced systematically with increasing turbulence for all of the individual size partitions (Figure 13a) and is most pronounced for the 10–20 µm partition. At maximum UD, the carbon derived from cells in the 2–4 µm partition is nearly equivalent to that in the 10–20 µm partition and is followed closely by prey in the 4–6 µm partition. For P. aculeatus, carbon derived from prey in the largest size partitions decreases with intensifying turbulence (Figure 13b). The total uptake for this species demonstrated no clear trend with turbulence intensity (Figure 12b), and compensation for the reduced carbon contribution derived from large prey is achieved through the smaller size classes (Figure 13b). For O. plumifera, as turbulence intensifies, carbon uptake increases across all partitions with no obvious modification to their relative contribution (Figure 13c).
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Again consistent with the preference-curve simulations (Figure 5d), prey with ESD <6 µm makes no nutritional contribution to the adult copepod diet (Figure 13d–f). For C. furcatus, the negative impact of turbulence intensity appears primarily as reduced uptake within the 10–20 µm partition (Figure 13d). For the two active smaller size partitions, the contribution to carbon uptake remains relatively constant, which indicates that successful perception is the primary factor limiting consumption. The uptake contribution of the 20–40 µm partition demonstrates a consistent decrease from minimal UD through 1.0 mm s–1. At higher UD, no clear trend in the realized contribution to carbon uptake is apparent, reflecting the greater stochasticity associated with encountering the relatively scarce large prey. For P. aculeatus, there is again no clear trend associated with increasing turbulence intensity (Figure 12e). In contrast to the copepodite simulation, no definitive trend in carbon contributed by the 10–20 µm partition appears. However, the upward shift in total carbon uptake apparent for UD = 1.4 mm s–1 (Figure 12e) primarily reflects an increased contribution from the 20–40 µm prey partition (Figure 13e), which emphasizes the stochasticity associated with capturing cells in this size class. Finally, for O. plumifera, all four of the contributing partitions exhibit increased rates of carbon uptake with more intense turbulence (Figure 13f).
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Discussion |
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Grazing-rate modification by prey-selection shifts that accompany copepod maturation
The prey-size preference simulations provided some general insights into how ingestion rates differed with developmental stage. Carbon uptake decreased with stage, which is consistent with the documented decrease in metabolism per unit body weight (QO2) as an individual matures (Epp and Lewis, 1980). The simulated carbon uptake rates became more variable as dependence on larger, less abundant prey increased. Additionally, for a given prey concentration (CT, cells ml–1), cell ingestion rates (I, cells h–1 ind.–1) changed by more than an order of magnitude from the copepodite stage to the mature females with a corresponding reduction of
65 ng C h–1 ind.–1 (35%) in carbon uptake. Along with this reduced uptake, nutritional contributions from cells with ESD <6 µm were minimized, whereas the percentage contribution of the 10–20 µm partition increased from 35% to 53% and the 20–40 µm partition increased from 0% to 18%. These model results are consistent with growth coefficients determined for natural copepod populations that decreased with advancing life stage (see Table 7 in Webber and Roff, 1995a) and offshore phytoplankton populations dominated by picoplankton that are less accessible to the more advanced developmental stages (note Figure 3 in Webber and Roff, 1995b). For the three more advanced developmental stages, I:ZM (i.e. prey selectivity) was constant with CT and consistently decreased with maturation. Thus, the shift in size preference that accompanies maturation led to reduced ingestion and carbon uptake. The simulation results suggested that short periods of satiation occur, which temporarily halt prey acquisition. These episodes were related to consumption of a large cell with high carbon content. For the copepodites, essentially all encountered cells were consumed at low CT. At higher concentrations, the ratio of ingestion-to-encounter rate decreased, suggesting a practical limit to cell acquisition associated with biomechanical limitations.
Influence of prey spectrum on vertical distribution of copepod developmental stage
With its predominance of small cells, spectrum 1 best represents oligotrophic, upper ocean conditions. With this food distribution, mature females required a 35–55% higher prey concentration to meet basal metabolic needs, with O. plumifera requiring the greatest increase. Clausocalanus furcatus and P. aculeatus required CT >103 cells ml–1 to meet their minimum metabolic needs. In the observed planktonic spectra that consisted of four profiles with five or sixth depths (15–140 m), there were five instances where such cell densities were observed (see Figure 2 in Paffenhöfer et al., 2003). Of these, all were associated with the DCM except for one occurrence within the surface mixed layer. For all the observed profiles, CT decreased monotonically with depth until the DCM was reached. Thus, with regard to dietary needs, mature female copepods are better situated near the DCM.
Prey spectrum 1 resulted in simulated carbon uptake rates derived from the 8–10 µm partition that are 50% higher despite a cell population within this partition that is identical with that of spectrum 4. This resulted from the lower large cell component of spectrum 1. For spectra 2 and 3, which emphasize larger prey, the mature females generally met basal requirements when CT was 500 cells ml–1, and always did so at higher concentrations. Additionally, more than 60% of their carbon uptake was derived from the more prominent population of 10–20 µm cells that these two spectra feature. Comparison of the simulated total carbon uptake obtained using these four spectra revealed a direct relationship with the 10–20 µm prey-size partition. In the Sargasso Sea profiles, this partition typically accounted for 25–50% of the total volume of planktonic cells (2–20 µm in size; see Figure 9 in Paffenhöfer et al., 2003). This reinforces the conclusion that the most suitable ecological niche for mature females occurs deeper in the water column where larger prey are more prevalent.
Prey spectrum 1 allowed the youngest copepodite stage of all three species to meet basal needs at or below 550 cells ml–1. When compared with spectrum 4 (standard case), simulated carbon uptake was somewhat reduced (10–20%), with P. aculeatus exhibiting the greatest decrease. The most prominently reduced portions of the prey population between spectrum 4 and spectrum 1 were the 10–20 µm partition and to a lesser degree the 6–8 µm partition. Thus, the youngest developmental stage was also influenced by the 10–20 µm partition. However, cells 6 µm ESD contribute more than 50% of the consumed carbon, and both of the two smallest size partitions individually contribute more to the copepodite diet than the 10–20 µm partition, which provided only 20% of the total. Prey spectra 2 or 3 also allowed the youngest copepodites to meet basal needs (on average) at the lowest prey concentration, and the 10–20 µm partition was again the dominant nutritional source, though its contribution dropped to 42% compared with the more than 60% contribution made to the adult female diet.
Regardless of prey-size distribution, the copepodites for all species meet nutritional needs for CT 550 cells ml–1. Measurements from the Sargasso Sea (Paffenhöfer et al., 2003) proved that more than 90% of the observed cell concentrations exceeded 640 cells ml–1 (data not shown), which ensures that immature individuals will have sufficient food. Moreover, the combination of spectra 1 and the youngest copepodite stage was the only simulation for which the 10–20 µm partition did not make the largest individual dietary contribution. This suggests that, for immature individuals, a near-surface niche exists that is less accessible for mature females. Thus, the simulations support the conclusion that the specific make-up of the prey field contributes to where various copepod developmental stages can exist. This result is consistent with natural distributions that exhibit such a vertical stratification of copepod life stages (Fragopoulu et al., 2001) and vertical copepod speciation that is associated with water-column-density structure and DCM location (Ambler and Miller, 1987; Peralba and Mazzocchi, 2004; Ramfos et al., 2006). Other analyses of in situ observations of vertical copepod distributions have addressed the possibility that their peak abundance coincides with the maximal rate of primary productivity, which is generally 5–10 m above the DCM (Napp et al., 1988; Herman, 1989). In this model, the prey population is static, which does not allow differentiation of copepod response to distinct peaks in prey biomass or growth rate within these simulations.
Varying impact of turbulence intensity on grazing success across copepod species
The divergence of the theoretically derived encounter rate from the modelled rate (ZM at 300 cells ml–1) reflected a threshold in turbulence intensity that related directly to the magnitude of each predator’s characteristic sampling velocity below which the explicit foraging behaviour dominates (Figure 11a–c). The theoretical encounter rate ZA [cells h–1 ind.–1, Equation (4)] depended solely on geometrical constraints and did not account for prey removal. Cells in the 10–20 µm partition accounted for only 1–4% of the total prey population (Table 1), so although they may contribute significantly to carbon uptake because of their volume, they exerted little influence on ZM (cells h–1 ind.–1).
For C. furcatus, there were two differences between the modelled and theoretical encounter rates. First, ZM for CT = 300 cells ml–1 was always lower than ZA. Second, ZA increased with turbulence intensity above UD = 1.0 mm s–1, whereas ZM for all three prey concentrations decreased at the highest turbulence intensities. This second distinction derives from the cell removal that was tracked in the simulations and suggested that this species can very effectively clear a given water parcel. Such a localized reduction in prey concentration would diffuse more effectively into surrounding waters as turbulence intensity increases resulting in a more extensive region with reduced prey concentration. Thus, this foraging method may be quite effective at clearing a given water parcel; however, this technique is potentially prone to self-induced grazing limitation via generation of localized patchiness in the prey population if shifting to a new location is not employed frequently enough. In nature, it is likely that species that employ foraging methods similar to C. furcatus will respond to prey gradients in a manner that minimizes this potential limitation, and models that incorporate such search strategies have been developed (Leising, 2001).
For all developmental stages of C. furcatus, an increase in turbulence intensity resulted in reduced total carbon uptake caused by a disproportionate reduction in the contribution obtained from the 10–20 µm partition (Figure 13a and d). At low UD [mm s–1, Equation (3)], this partition was clearly the dominant nutritional source; however, at maximum UD, it was notably reduced and, for the youngest copepodites, was equivalent to the contribution derived from the 2–4 µm partition. This result is consistent with Wiggert et al. (2005), where it was determined that this species had a relative disadvantage in acquiring large, non-motile prey (ESD > 40 µm). Higher sinking velocities of the larger cells produced elevated, orthogonal relative velocities between C. furcatus and its prey, which reduced the likelihood of capture. With prey ESD capped at 40 µm in this study, this species-dependent dietary distinction was no longer apparent at standard UD (Figure 5). However, as turbulence intensity increased, the associated decrease in carbon uptake derived from the 10–20 µm size class by all developmental stages suggests another interaction between behaviour and environmental conditions for this species. Because the turbulence velocity of each cell (prey) is stochastic, the directional vectors of prey and predator are not necessarily orthogonal, as can be assumed for gravitationally driven sinking velocities and the typical sampling plane of C. furcatus that is at least quasi-horizontal (cf. Figure 1 of Mazzocchi and Paffenhöfer, 1999). The simulated AOP of this species is a long, narrow cone. The clear dependence on UD for uptake of 10–20 µm ESD cells suggested that, as their relative velocities increased, the angular range of oblique predator–prey directional vectors likely to result in cell acquisition narrowed.
For P. aculeatus, ZA and ZM matched at lower values of UD and again diverged at higher turbulence intensities. In contrast to the results noted above for C. furcatus, ZM exhibited no dependence on UD for this species. Thus, the foraging mechanism of P. aculeatus was less prone to inducing self-limitation, because repeated sampling of a given water parcel did not occur. The total carbon uptake curves also exhibited no clear trend as UD increased for either developmental stage (Figure 12b and e). As turbulence intensity increased, copepodites derived less carbon from the 10–20 µm partition. This reduction was compensated for by additional carbon uptake derived from smaller prey (Figure 13b).
The strongest deviation between the theoretical and simulated encounter rates was exhibited by O. plumifera, with ZA at the least energetic turbulence condition (UD = 0.17 mm s–1), being an order of magnitude lower than ZM (Figure 11c). Although ZM exhibited a plateau at low turbulence intensity similar to that of the other two species, ZA increased monotonically over the applied range of turbulence intensities. These differences yielded the most prominent example of the contribution that foraging behaviour makes towards facilitating grazing success. Indeed, these results suggested that the frequent, oblique upward jumps employed by O. plumifera significantly mitigate the extremely low encounter rates predicted by the theoretical relation by allowing for effective sampling of the water column through frequent insertion into a completely new parcel of water with a fresh group of potential prey. Carbon uptake for O. plumifera had a clearly positive impact by increasing turbulence intensity that manifests across all contributing size partitions and developmental stages (Figure 13c and f).
Each species exhibits a unique response to increasing turbulence whereby the encounter rate decreased, remained constant, or increased. These responses relate inversely to the characteristic ambit velocity and reflect the dome-shaped relation in predator–prey encounter with increasing turbulence kinetic energy (TKE) reported in the literature (Mackenzie et al., 1994; Jenkinson, 1995). A reduced encounter rate at higher TKE reflects time spent on pursuit, handling of prey, or temporary satiation (Mackenzie et al., 1994; Metcalfe et al., 2004). The varying impact of turbulence exhibited in the simulations presented here also suggests that spatial heterogeneity in copepod speciation will develop, with Oithona preferring regions prone to stronger mixing (e.g. the surface mixed layer) and Clausocalanus favouring more stable fluid regimes. Although there is observational evidence for vertical structure in metazoan distribution associated with turbulence, determination of clear relationships and species tendencies remains elusive and often contradictory (Haury et al., 1990; Incze et al., 2001; Maar et al., 2006).
Conclusions and future prospects
The model results presented here demonstrate differential response to variation in environmental conditions by three common copepod species that employ distinct methods of grazing. This differential response extends through the range of developmental stages included in these simulations. The coincident persistence and spatial distribution of these copepod species, and their developmental stages, depend not only on prey concentration but are also controlled by the make-up of the prey field (i.e. how prey is distributed over size class). The results presented here suggest a naturally occurring niche distribution that promotes the near-surface presence of younger copepodites over the mature females. A similar impact on vertical distribution of species in response to varying turbulence intensity is indicated. Thus, preferred niches may exist that would lead to spatial heterogeneity if the underlying environmental conditions persisted. Given that the oceanic environment is typically subject to contemporaneous disequilibrium, the integrative effect results in collective persistence of species.
A primary motivation for the development of this Lagrangian IBM is to develop approaches for including species-specific meta- and mesozooplankton grazing into models designed to investigate large spatial scales and seasonal to interannual timescales. For such broad scale applications, a fundamental interest is to advance the capacity to predict how marine ecosystems and oceanic biogeochemical cycling will respond to natural and anthropogenically driven changes in global climate. For example, if climate change resulted in increased stratification and modified intensity of small-scale oceanic turbulence, the simulation results presented here suggest that Clausocalanus would do well in a less energetic turbulent regime which may then enhance biogenic export to the deep ocean. However, if climate change leads to higher windspeeds (e.g. Goés et al., 2005), the accompanying increase in the intensity of upper ocean turbulence would favour Oithona. In that case, it could be argued that export fluxes would decrease because this species employs coprophagy and produces smaller, slower sinking faecal pellets that promote upper ocean retention of organic matter via bacterial remineralization (González et al., 2000; Svensen and Nejstgaard, 2003; Huskin et al., 2004). However, whether ambush predators such as Oithona have a preference for higher levels of turbulence remains to be determined (Kiørboe and Saiz, 1995; Visser and Stips, 2002).
Development of zooplankton IBMs with a rule set sufficient to generate robust emergent behaviour that can provide parameterizations for larger scale models requires comprehensively characterizing motile prey behaviour and determining how copepod foraging ambits and prey perception are influenced by non-organic particulates (e.g. silt), salinity, density gradients, and velocity shear (Paffenhöfer, 1972; Wiggert et al., 2005; Woodson et al., 2005; Seuront, 2006). Also, process studies that characterize typical foraging behaviours and full accounting of metabolic costs incurred by the various grazing methodologies (e.g. through determination of oxygen utilization) are critical needs. Such studies, combined with the development of zooplankton IBMs that include realistic representation of environmental conditions, will allow development of parameterizations that account for the full diversity of copepod foraging behaviours in response to environmental perturbations. This approach is analogous to that now being used by marine ecosystem modellers to incorporate the myriad planktonic behaviours within a tractable set of functional groups (Legendre and Michaud, 1998; Hood et al., 2006). If this could be accomplished, then a zooplankton-based counterpart to a recent effort—wherein a realistic distribution of ecotypes (i.e. phytoplankton groupings) emerged naturally from an initial superset based on the prevailing light field, nutrient availability, and water column structure within a global general circulation model (Follows et al., 2007)—could be developed. What is especially appealing about such an application is the possibility it provides for using the inherently synthetic nature of a model to explore global-change scenarios and how planktonic community structure is likely to adjust or even possibly facilitate systemic response that mitigates climate change.
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Acknowledgements |
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The National Oceanographic Partnership Program supported this research (Grant # N00 014-02-1-0370). G-A.P was supported by the National Science Foundation (OCE-9911513, towards an understanding of the existence of small oceanic planktonic copepods). Computer facilities and support were provided by the Commonwealth Center for Coastal Physical Oceanography at Old Dominion University. Eddie Haskell initially developed this copepod model, and his guidance on its application for this study is greatly appreciated. The insightful comments of the two reviewers stimulated significant improvements to this manuscript and are appreciated.
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