The effect of food concentration on fecal pellet size in marine copepods

Transcription

1 Limnol. Oceanogr., 31(5), 1986, Q 1986, by the American Society of Limnology and Oceanography, Inc. The effect of food concentration on fecal pellet size in marine copepods Michael J. Dagg and W. Edward Walser, Jr. Louisiana Universities Marine Consortium, Star Route Box 541, Chauvin Abstract Three species of copepods, Temora turbinata, Eucalanus pileatus, and Neocalanus plumchrus, were fed cultures of the diatom, Thalassiosira weissflgii, at concentrations ranging from 0.3 to 14.5 fig Chl liter- to determine whether fecal pellet size was related to food concentration. In all three copepods, pellet size increased with food concentration up to about 3 pg Chl liter-. At higher concentrations pellet size was constant. Pellets were less compact and appeared to be more fragile at low food concentrations. The level of gut contents in these copepods was also related to food concentration up to about 3 pg Chl liter-l. Below this concentration, ingestion and defecation were balanced in such a way that the gut did not fill, and therefore pellet size was smaller. Food concentrations sufficient to allow a copepod to fill its gut result in the production of fecal pellets of maximum size. It is concluded that fecal pellets produced by large copepods under conditions of low food availability are less likely to sink out of the euphotic zone than pellets produced by the same copepods under conditions of higher food availability. Zooplankton fecal pellets play an important role in the downward transport of organic material in the ocean (e.g. Small et al. 1979; Turner and Ferrante 1979; Urrere and Knauer 198 1; Lorenzen and Welschmeyer 1983). Grazing organisms ingest many small, slowly sinking, phytoplankton cells and defecate the unassimilated remains in relatively large packages that are, in many cases, surrounded by a smooth peritrophic membrane (Honjo and Roman 1978). The sinking speed of zooplankton fecal pellets is closely related to their size (Paffenhiifer and Knowles 1979; Small et al. 1979), and in a general manner, pellet size is related to the size of the grazer, with larger organisms producing larger pellets. The size composition of the grazer community can therefore affect the transport rate of material out of the euphotic zone; small pellets have a higher probability of being recycled in the euphotic zone because they sink slowly. In addition, small pellets are in the right size range to be captured by particle-grazing copepods (Paffenhiifer and Knowles 1979). On the ba- I This work was supported in part by grant OCE 8 l from the NSF Biological Oceanography Program, in part by grant OCE , as a component of the multidisciplinary program titled SUPER (Subarctic Pacific Ecosystem Research), from the NSF Biological Oceanography Program, and in part by the Louisiana Universities Marine Consortium. sis of these general relationships between body size and pellet size, and pellet size and sinking rate, information on the size composition of the grazer community has been deduced from the size composition of the fecal material collected in the water column and in sediment traps (Welschmeyer and Lorenzen 1985). Calculation of sinking speeds based on pellet size alone can result in erroneous conclusions concerning the vertical flux of materials because sinking speed is also affected by pellet shape and density (Bienfang 1980; Komar et al ). Both of these characteristics are partly determined by food type, but other factors may also be important. Ingestion rate in copepods is strongly dependent on food concentration. This has been demonstrated in numerous laboratory (e.g. Frost 1972; Mullin et al. 1975) and field (e.g. Poulet 1978) experiments. Furthermore, food concentrations in the ocean are rarely sufficient to permit maximum ingestion rates of particle grazing copepods. This is especially true for large copepods (Mullin and Brooks 1976; Dagg et al. 1980). The rate of fecal production is closely related to the rate of ingestion (Corner et al. 1972), and therefore the amount of fecal material produced by a copepod will depend on the available food concentration. It is also possible that the size of the pellets produced 1066

2 Fecal pellet size 1067 will be related to the ingestion rate. If in- ment, 5 or 6 copepods were placed in 2.0- gested material is processed continuously liter polycarbonate bottles filled with food by the copepod digestive system, then the medium - Thalassiosira weissflogii in filpellet size could be a function of ingestion. tered seawater. A l-mm-mesh screen was rate. Conversely, if the copepod fills its gut placed over the mouth of each bottle and and then digestively processes that food attached with a rubber band. Bottles were (Boyd et al. 1980; Simard et al. 1985), pellet size could be relatively constant for that individual over a wide range of ingestion rates. We examine here the relationship between food concentration and the size of fecal pellets produced by three marine copepods, Neocalanus plumchrus C5, Eucalanus pileatus C6 females, and Temora turbinata C6 females. The technical assistance of J. White and P. Morgan is appreciated. M. Landry provided equipment and assistance for experiments at Friday Harbor, Washington. Methods and materials The three species of copepods used in these experiments were of different body size: prosome length of N. plumchrus was about 4.0 mm and dry weight was about 300 pg, E. pileatus was about 2.2 mm and 45 fig, and T. turbinata was about 1.0 mm and 25 pg. Neocalanus plumchrus was collected with a 0.75-m plankton net fitted with 500~pm mesh and a Plexiglas cod-end of about 5 liters. This net was towed vertically from 160 m to the surface at a collection site at about N, W (near Friday Harbor, Washington). All collections and experiments were done during a 4-week period in May 1985, when N. plumchrus is actively developing through the late copepodid stages in this region (Fulton 1973). Eucalanus pileatus and T. turbinata were collected with a 0.5-m plankton net fitted with 254-pm mesh and a solid cod-end of 650 ml. This net was towed vertically from near the bottom, about 20 m, to the surface at a collection site at about N, W (near Cocodrie, Louisiana). The single experiment with each species was done during October Neocalanus plumchrus was kept in filtered seawater for several hours before each experiment so that the animals would not have food remains in their guts at the onset of the incubation period. For each experi- then inverted so that the mouth of each bottle was in a 50-ml beaker containing the same food medium. Incubations were for 6-8 h at 8 C in the dark. During the incu- bation, many of the pellets settled through the 1 -mm mesh into the 50-ml beaker. After the incubation, the contents of the 50-ml beaker were preserved with Formalin to a final concentration of about 3-4%. Pellets that had not settled through the 1 -mm mesh were collected by filtering the entire contents of the bottle through a gridded polycarbonate filter, which was placed in a Petri dish on an absorbant pad with a few drops of Formalin. The length and width of all pellets were measured under a dissecting microscope with the aid of an ocular micrometer. The experiment with E. pileatus was done differently. Triplicate sets of loo-ml beakers, each containing 80 ml of T. weissflogii medium, were set up, and a copepod, previously kept in filtered seawater for several hours, was added to each beaker. Incubation was for 12 h at 25 C. The complete contents of each container were preserved in a weak Formalin solution. All fecal pellets were measured by pouring the contents into a Petri dish, letting the pellets settle, and measuring the length and width of each pellet with an ocular micrometer. The experiment with T. turbinata was similar except that 20 ml of T. weissflogii medium was used in each of 30 Petri dishes, with a single copepod added to each dish. Incubation was for 14 h at 25 C, after which the contents of the dishes were preserved with Formalin and the pellets measured. Fecal pellet volumes were calculated by assuming that the pellets are cylindrical. Equilibrium levels of gut fullness were determined for each copepod by placing 4 N. plumchrus, 5 E pileatus, or 10 T. turbinata into l- or 2-liter containers of T. weissfogii medium and incubating for 4-l 6 h. After incubation, copepods were collected on a coarse mesh, picked onto a glass-fiber filter

3 1068 Dagg and Walser s op Y 5 30 g P i 6 6 i ii il 1 3 CHLOROPHYLL CONCENTRATION (Wliter) Fig. 1. The relationship between fecal pellet size and food concentration. a-temoru turbinata C6 females; b-neocalanus plumchrus C5; c-eucalanus pdeatus C6 females. Sinking speeds are calculated from the equation of Small et al. (1979). Vertical bars represent 1 SD. with fine forceps, and fluorometrically analyzed for their level of gut chlorophyll and pheopigments. These were directly summed to determine the amount of gut pigment (see Dagg 1983). Results As expected, fecal pellet size was related to copepod size. Pellets produced by T. turbinata, the smallest of the three experimental copepods, ranged in average volume from 0.13 to 0.44 x 10 pm3, by E. pileatus from 0.75 to 1.85 x lo6 gm3, and by N. plumchrus, the largest copepod of the three, from 1.76 to 3.90 x lo6 pm3. Totals of 108, 298, and 220 pellets were measured for the three copepods. Fecal pellets of all copepods were smaller at lower food concentrations (Fig. 1). In each 0.0s CHLOROPHYLL CONCENTRATION (w/liter) Fig. 2. The relationship between the level of gut fullness and food concentration when ingestion and egestion are in equilibrium. a-temoru turbinata C6 females, from Dagg (1985); b- Neocalunus plumchrus C5; c-eucalanus pileatus C6 females. case, the volume of a pellet at the lowest experimental food concentration was about half that at the high concentrations. For all copepods, pellet width did not significantly vary with food concentration; the differences in pellet volume were due to variations in length. The relationships in Fig. 1 are described by lines that reach a plateau at concentrations between 2.5 and 3.5 pg Chl liter-l. This is somewhat arbitrary but was selected because the degree of gut fullness that is

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5 1070 Dagg and Walser Small et al. (1979) noted that pellets collected after copepods had been in filtered seawater for 2-3 h were less compact and lighter in color than freshly collected pellets and that these second collection pellets had lower sinking rates. A copepod with an empty gut will begin feeding, and thus begin filling its gut, as soon as it is placed in food (Dagg 1983). At low food concentrations, defecation begins before feeding processes can fill the gut, and levels of gut fullness remain low. At slightly higher food concentrations, the level of gut fullness at which equilibrium between ingestion and defecation is reached is also higher. At high food concentrations, the equilibrium is reached at the maximum level of gut fullness. At food concentrations that will not permit a copepod to fill its gut, fecal pellets are less than the maximum size for that copepod. At food concentrations high enough to permit a copepod to fill its gut, fecal pellets are the maximum size for that copepod. For these three copepods feeding on T. weissflogii, this food concentration was between 2.5 and 3.5 pg Chl liter- I, equivalent to between 129 and 18 1 cells ml-, based on direct comparisons made with a particle counter. Welschmeyer and Lorenzen (1985) studied the production and fate of phytoplankton pigments in a moderately productive fjord and in the oligotrophic Pacific Ocean. They assumed that pheopigment residue from macrozooplankton grazing will rapidly leave the euphotic zone in the form of fecal pellets, but that the pheopigment residue from microzooplankton grazing will have neglible sinking rates and be broken down within the euphotic zone. Recovery of small amounts of pheopigment in their sediment traps is taken as an indication that macrozooplankters are insignificant grazers on phytoplankton in the euphotic zone, whereas large amounts are taken to mean that macrozooplankters are important grazers. However, as we show here, the pellets produced by large grazers at low food concentrations are smaller and less dense than pellets produced by the same copepod at high food concentrations and will therefore sink more slowly. We believe that attempts to partition grazing between macro- and microzooplankton on the basis of the ratio of trap-caught to water-column fecal remains require that food concentration effects be considered. In open ocean locations with low concentrations of phytoplankton in the surface waters, such as the Central Pacific Gyre, fecal material produced by macrozooplankton is less likely to sink rapidly than material produced by macrozooplankton in more productive regions such as Dabob Bay. A possible confounding factor is the presence of a subsurface chlorophyll maximum in the Central Pacific, which may provide a zone of enhanced feeding activity and result in the production of larger pellets in the subsurface waters. None of this alters the basic conclusion of Welschmeyer and Lorenzen, that the vertical transport of materials out of the euphotic zone in the oligotrophic gyres is comparatively small. But, macrozooplankton may still be responsible for a major portion of the community grazing in such areas. Neocalanus plumchrus is one of the dominant copepods in terms of biomass in the subarctic Pacific Ocean, where phytoplankton concentrations are almost always < 0.5,ug Chl liter- (Miller et al. 1984). At this concentration of T. weissfloggii, gut contents would be about 3 ng pigment per copepod and pellet size about 1.5 x 1 O6 pm3 (Fig. 2b). However, in the subarctic Pacific Ocean, gut contents typically are between 0.5 and 1.5 ng pigment per copepod, suggesting that fecal pellets produced by N. plumchrus in this region would be smaller than any produced by N. plumchrus in our experiments. All indications are that N. plumchrus is a major grazer in this region, but we would not expect the vertical flux of fecal pellets from this copepod to be large because food concentrations are always very low. In conclusion, although large copepods generally produce larger, and therefore faster sinking, fecal pellets than small copepods, the size and density of fecal pellets produced by a copepod are related to the available food concentration. Fecal pellets produced by a large copepod under conditions of low food availability are smaller, less compact

6 Fecal pellet size 1071 and more fragile, and therefore less likely to sink out of the euphotic zone than pellets produced by the same copepod under conditions of higher food availability. Furthermore, under conditions of low food availability the euphotic zone is typically deeper than under more eutrophic conditions, and pellet residence time will be increased accordingly. References BIENFANG, P. K Herbivore diet affects fecal pellet settling. Can. J. Fish. Aquat. Sci. 37: BOYD, C. M., S. L. SMITH, AND T. J. COWLES Grazing patterns of copepods in the upwelling system off Peru. Limnol. Oceanogr. 25: CORNER, E. D., R. N. HEAD, AND C. C. KILVINGTON On the nutrition and metabolism of zooplankton. 8. The grazing of Biddulphia cells by Calanus helgolandicus. J. Mar. Biol. Assoc. U.K. 52: DAGG, M. J A method for the determination of copepod feeding rates during short time intervals. Mar. Biol. 75: The effects of food limitation on diel migratory behavior in marine zooplankton. Ergeb. Limnol. 21: AND OTHERS Grazing and excretion by zooplankton in the Peru upwelling system during April Deep-Sea Res. 27: FROST, B. W Effects of size and concentration of food particles on the feeding behavior of the marine planktonic copepod Calanus paczjicus. Limnol. Oceanogr. 17: FULTON, J Some aspects of the life history of Calanus plumchrus in the Strait of Georgia. J. Fish. Res. Bd. Can. 30: 81 l HONJO, S., AND M. R. ROMAN Marine copepod fecal pellets: Production, preservation and sedimentation. J. Mar. Res. 36: KOMAR, P. D., A. P. MORSE, L. F. SMALL, AND S. W. FOWLER An analysis of sinking rates of natural copepod and euphausiid fecal pellets. Limnol. Oceanogr. 26: LOREN~EN, C. J., AND N. A. WELSCHMEYER The in situ sinking rates of herbivore fecal pellets. J. Plankton Res. 5: MILLER, C. B., B. W. FROST, H. P. BATCHELDER, M. J. CLEMONS, AND R. E. CONWAY Life histories of large, grazing copepods in a subarctic ocean gyre: Neocalanus plumchrus, Neocalanus cristatus, and Eucalanus bungii in the northeast Pacific. Prog. Oceanogr. 13: MULLIN, M. M., AND E. R. IJROOKS Some consequences of distributional heterogeneity of phytoplankton and zooplankton. Limnol. Oceanogr. 21: , E. F. STEWART, AND F. J. FUGLISTER Ingestion by planktonic grazers as a function of concentration of food. Limnol. Oceanogr. 20: PAFFENH~FER, G. A., AND S. C. KNOWLES Ecological implications of fecal pellet size, production and consumption by copepods. J. Mar. Res. 37: POULET, S. A Comparison between five coexisting species of marine copepods feeding on naturally occurring particulate matter. Limnol. Oceanogr. 23: 1126-l 143. SIMARD, Y., G. LACROIX, AND L. LEGENDRE In situ twilight grazing rhythm during diel vertical migrations of a scattering layer of Calanus finmarchicus. Limnol. Oceanogr. 30: SMALL, L. F., S. W. FOWLER, AND M. Y. UNLU Sinking rates of natural copepod fecal pellets. Mar. Biol. 51: TURNER, J. T., AND J. G. FERRANTE Zooplankton fecal pellets in aquatic ecosystems. Bioscience 29: URR~RE, M. A., AND G. A. KNAUER Zooplankton fecal pellet fluxes and vertical transport of particulate organic material in the pelagic environment. J. Plankton Res. 3: WELSCHMEYER, N. A., AND C. J. LORENZEN Chlorophyll budgets: Zooplankton grazing in a temperate fjord and the Central Pacific Gyres. Limnol. Oceanogr. 30: Submitted: 10 September I985 Accepted: 4 April 1986