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Effects of Competitors, Predators, and Prey on the Grazing Behavior of Herbivorous Calanoid Copepods

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Effects of Competitors, Predators, and Prey on the Grazing Behavior of Herbivorous Calanoid Copepods BULLETIN OF MARINE SCIENCE, 43(3): 573-582, \988 EFFECTS OF COMPETITORS, PREDATORS, AND PREY ON THE GRAZING BEHAVIOR OF HERBIVOROUS CALANOID COPEPODS C Kim Wong ABSTRACT Gut fluorescence was measured to test the effects of potential competitors, predators, and alternate animal prey on the short term (1,5-2 h) herbivorous feeding rates of the marine calanoid copepods Calanus pac!ficus Brodsky, Pseudocalanus minutus (Kroyer), and Metridia pacl}ica Brodsky. The diatoms Thalassiossira weissjlogii and Coscinodiscus perforatus were used as food. The presence of the predatory copepod Euchaeta elongata Esterly affected the swimming behavior and caused a significant reduction in the gut fullness of Pseudocalanus. Neither the presence of conspecifics nor other herbivorous grazers affected the gut fullness of any of the copepods, Feeding on algae by the omnivore Metridia was not significantly affected by the presence of Artemia nauplii as alternate prey, despite the fact that Artemia were ingested along with algae. Grazing by zooplankton may influence the growth and abundance of phyto- plankton (Riley, 1946; Steele, 1974). Because calanoid copepods are important grazers in the ocean, many factors that affect their feeding performance have been studied to estimate the grazing impact on the phytoplankton community. The most intensively studied are food concentration, size and quality of food particles, size and previous feeding history of the copepods, temperature, and light (reviewed by Conover and Huntley, 1980; Frost, 1980). While many of these studies were carried out in single-species experiments where the grazers were excluded from other animals, zooplankton typically occur in patches that are multi-species ag- gregates (Haury and Wiebe, 1982). Both the density and species composition of zooplankton patches can vary over a wide range of temporal scales. Thus, a herbivorous zooplankter must often survive and feed in an environment where encounter rates with potential competitors and predators are high. The feeding efficiency of a herbivorous zooplankter can be affected by the presence of other animals in several ways. First, food concentration may be reduced as a result of exploitation by other grazers. Second, feeding activity may be reduced as a result of direct behavioral interference. For example, the grazing rate of the freshwater copepod Diaptomus tyrrelli was decreased by chemicals produced by its potential competitor and predator Epischura lacustris (Folt and Goldman, 1981). Copepods also avoid physical contacts with other zooplankters by jumping away (Strickler, 1975). The jumping frequency of Diaptomus minutus is altered by the presence of other zooplankters (Wong et al., 1986). In areas of high animal density, avoidance reactions may exact a cost by reducing time available for feeding. Herbivorous copepods generate feeding currents to capture algae (Koehl and Strickler, 1981). Because the hydromechanical signals from these feeding currents may be sensed by tactile predators, potential prey may stop all feeding movements to reduce the risk of predation. Finally, omnivorous copepods may switch from herbivory to carnivory during periods of high prey density and low algal abundance (Landry, 1981). Even for copepods that are predominantly herbivorous, feeding on animals may reduce the need and time for grazing on phytoplankton. Omnivorous calanoid copepods may change their swimming pattern when exposed to zooplankton prey (Wong 573 574 BULLETIN OF MARINE SCIENCE, VOL. 43, NO.3, 1988 and Sprules, 1986). Some swimming behaviors that facilitate the capture of zoo- plankton prey (e.g. ambush behavior) may decrease the efficiency of grazing on phytoplankton. Thus, it is somewhat surprising that the impact of other zoo- plankters on the feeding performance of herbivorous calanoid copepods has rarely been examined. The purpose of this research is to study the effects of other zooplankters on the grazing behavior of the marine calanoid copepods Pseudocalanus minutus (Kroy- er), Calanus pacificus Brodsky, and Metridia pacifica Brodsky. The specific ques- tions addressed in this study are: (1) Is the grazing behavior of Pseudocalanus, Calanus, and Metridia affected by the density of conspecifics? (2) Is the grazing behavior of Pseudocalanus, Cala nus, and Metridia affected by the presence of other grazers? (3) Is the grazing behavior of the omnivore Metridia (Haq, 1967) affected by the presence of alternate animal prey? (4) Is the grazing and swimming behavior of Pseudocalanus affected by the presence of its predator Euchaeta elon- gata Esterly (Yen, 1985). MATERIALS AND METHODS Calanoid copepods were collected between April and August 1986 from Saanich Inlet, Vancouver Island, B.c. (48°39'N, I 23°30'W). Pseudocalanus minutus, Calanus pacijicus, and Metridia pacifica were collected from 120-m daytime vertical hauls (0.2- or 0.3-mm mesh, 0.5-m mouth diameter). The zooplankton samples were immediately diluted with surface seawater in 15 liter carboys. Euchaeta elongata was caught in 150-m daytime oblique hauls (0.5-mm mesh, I-m mouth diameter) and sorted into 2 liter glass jars (1 to 5 copepods per jar) containing seawater from 20 to 30 m (temperature below 15°C). All animals were kept at 12°C under a reversed 14L: 10D light cycle in the laboratory. Concentrated surface phytoplankton from Saanich Inlet was added to the carboys to feed the herbiv- orous copepods every 1 or 2 days. Euchaeta were fed small zooplankters. The copepods were allowed at least 3 days to acclimatize to the conditions in the laboratory. Only copepods kept in the laboratory for more than 3 days but less than 10 days were used for experiments. Grazing experiments were carried out in 450-ml glass fleakers (Corning) containing 250 ml of filtered (1.5 I'm Whatman 934AH fiber glass filters) surface seawater. Experimental animals were sorted and transferred to the fleakers with wide-bore glass pipets. Pseudocalanus (prosome length 0.7-1.0 mm) was sorted under a stereomicroscope. Calanus (prosome length 2.0-2.6 mm), Metridia (prosome length 1.7-2.0 mm), Euchaeta (prosome length 4.6-5.4 mm), and Artemia nauplii (2-3 days post-hatch) were usually sorted without optical aids. With the exception of a few C5 and adult male Calanus, only adult female copepods were used. The animals were allowed a 0.5 to 1 h acclimation period. Because estimates of gut passage time were 0.4 h for Pseudocalanus (Wong, unpubl.), 0.4 h for Calanus and 0.6 h for Metridia (Mackas and Burns, 1986), animals were assumed to have empty guts when algal monocultures of Thalassiossira weissjlogii (8-12 I'm) or Coscinodiscus perforatus (70-80 I'm) were added to the fleakers to initiate grazing experiments. Both acclimation and grazing were carried out in darkness at 12°C. All experiments were performed between 1000 and 1500 h, and lasted from 1.5 to 2 h. For experiments with Coscinodiscus, the contents of the fleakers were stirred every 30 min to keep cells in suspension. Food concentration never changed more than 10% over the short duration of the experiment. At the end of each experiment, the contents of each fleaker were poured through a 102-l'm mesh. Copepods on the mesh were washed with filtered seawater and kept frozen in closed petri dishes until analysis. The amount of chlorophyll and its derived pigments in the guts was used as an index of the amount of phytoplankton ingested in the short interval prior to the termination of the grazing period. Copepods were removed from the filter and soaked overnight in 90% aqueous acetone. The fluorescence of the acetone extract before and after acidification with 5% BCL was measured with a Turner Designs fluorometer. Gut fullness (chlorophyll + phaeopigment) was calculated using the equations from Dagg (1983). The method assumes that chlorophyll-a was converted to phaeophorbide-a with 100% molar efficiency, and that no fluorescing compounds were lost due to digestion. Some authors (Dagg and Grill, 1980; Kiorboe et aI., 1982; 1985) have found close agreement between ingestion rates determined by gut fluorescence method and other direct measurements of filtration rates. Others argue that more than 90% of chlorophyll-derived pigment may at times be lost due to digestive processes (Conover et aI., 1986a; Wang and Conover, 1986). If pigment was indeed lost, the gut fluorescence method underestimated the amount of chlorophyll ingested. I assumed that the chemical process of pigment destruction during gut passage was not related to treatment effects such as density of copepods and WONG: EFFECTS OF COMPETITORS AND PREDATORS ON GRAZING 575 1.6 20 A c b B b 16 b b b b 1.2 b 6 ~ 12 b b " 6. .8 6. 8 6. f! b 6. 6. .4~ ~ ~~ll~ " o ~ . ._. II b 6. b o ~ , o l' i , 1 2 3 4 5 6 7 8 34 6789 123456789 copepod· fleaker-1 Figure 1. Relationship between gut pigment content and copepod density. A) Calanus fed Thalas- siossira at 7.5 /lg Chla'liter-I; regression: Y = -0.18X + 10.56, t = -0.42, df = 30, P > 0.5. B) it1etridia fed Thalassiossira at 9.7 /lg Chla'liter-I; regression: Y = -0.70X + 15.25, t = -1.36, df = I 24, P > 0.1. C) Pseudocalanus fed Thalassiossira at 1.9 /lg Chla'liter- ; regression: Y = 0.02X + 0.26, t = 1.17, df= 32, P > 0.2. At I Pseudocalanus per fleaker, each point represents the average of two animals. All other points in this figure represent the mean for a given fleaker. presence of predators, and the fraction of pigment lost did not vary between treatment and control animals. One or two water samples (2-5 ml) from each fleaker were filtered with 0.45-/lm Millipore filters. Thc filters were extracted overnight in 90% aqueous acetone. Food concentration was measured fluorometrically as chlorophyll-a concentration.
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