Diel vertical migration in zooplankton: rapid individual response to predators

While diel vertical migration in zooplankton has been shownrecently to be a predator avoidance behavior, the mechanismby which predators induce and maintain such behavior has beendebated. We report results of an in situ predator manipulationexperiment during which enclosed populations of the marine planktomccopepod Acaraa hudsonica rapidly changed their vertical distributionand diel migration behavior depending on presence or absenceof the planktivorous fish Casterosteus aculeatus These resultspoint unambiguously to phenotypic behavioral plasticity of individualplanktonic prey, not, as previously hypothesized, population-geneticlevel behavioral changes caused by selective fish predation,as the mechanism underlying changes in diel vertical migrationin this copepod.     

The Role of the Predaceous Copepod Parabroteas Sarsi in the Pelagic Food Web of a Large Deep Andean Lake

Parabroteas sarsi is a predaceous calanoid copepod that inhabits both shallow temporary fishless ponds and deep fish lakes of Patagonia and Antarctica. The aim of this study was to analyse the effect of P. sarsi on the plankton structure of a deep Andean lake (>100 m depth) and the zooplankton vertical distribution in order to asses a possible vertical refuge of the predatory copepod against visual fish predation. We tested the extent to which the trophic cascade effect of this predator propagates through the food web. We carried out a vertical sampling in Lake Rivadavia (Patagonia, Argentina) in order to assess zooplankton distribution. P. sarsi showed a vertical distribution towards deeper layers of the water column both at midday and at night, indicating that the copepod had an effective refuge against visual predation. Additionally, we carried out both field and laboratory experiments with the presence of P. sarsi. The predator was observed to affect significantly the survival of the copepod Boeckella michaelseni both in laboratory and field experiments. On the contrary, rotifers and adults of Daphnia cf. commutata were not substantially affected by the predator. B. michaelseni mouthparts revealed an omnivorous diet; therefore a broad phytoplanktonic size spectrum could be affected by this copepod. However, no cascade effect was observed due to the presence of P. sarsi despite the decrease of B. michaelseni abundance.     

Ovigerity,selective predation,and variable diel vertical migration in Euchaeta elongata (Copepoda: Calanoida)

Summary We present a statistical analysis of a previously published (Yen, 1983) but heretofore unanalyzed data set on the vertical distributions and diel vertical migration (DVM) of adult females of the marine planktonic copepod Euchaeta elongata in Dabob Bay, Washington, USA. Non-ovigerous females were strongly migratory on all four dates sampled, residing between 75–175 m during the day and at shallower depths during the night, commonly entering the upper 50 m of the water column. In contrast, ovigerous females were non-migratory or weakly migratory, largely remaining between 100–175 m both day and night, and entering the upper 50 m of the water column only rarely. Thus non-ovigerous females always migrated much more strongly, as measured by both amplitude of migration and the proportion of animals migrating, than did ovigerous females. These results led us to hypothesize that differential susceptibility to visually orienting predators was the cause of these differences in DVM behavior in female E. elongata, and we subsequently undertook an experimental study of the feeding selectivity of the copepod's natural predator, Pacific herring (Clupea harengus pallasi). Pacific herring exhibited a highly significant preference for ovigerous over nonovigerous adult female E. elongata. The demographic consequences of variable DVM in adult female E. elongata were investigated by way of life table analyses. Results indicated that under conditions of thermal stratification of the water column there is a distinct demographic disadvantage (reduced rate of realized population growth) incurred by non-migratory or weakly migratory ovigerous females due to delayed egg development at cooler subsurface temperatures. We conclude that ovigerous female E. elongata remain at depth both day and night to avoid visually orienting predators, and that such behavior must afford the copepod a demographic advantage of no less than a 26% reduction in adult mortality to offset the demographic cost of delayed egg development.     

Differential responses of populations of the copepod Acartia hudsonica to toxic and nutritionally insufficient food algae

Nutritional insufficiency and toxicity are deleterious effects of phytoplankton on grazers. We hypothesize that toxic food is likely to have stronger evolutionary selective effects on grazers than nutritionally insufficient food. We explore this hypothesis in comparative studies of egg production and egg hatching of the copepod Acartia hudsonica challenged with both a toxic and a nutritionally insufficient alga. Experiments lasting 6 days, in which mixtures of different proportions of the suspect and a control alga were offered as food to female copepods, showed that the dinoflagellate Alexandrium fundyense, which bears paralytic shellfish toxins, was toxic to A. hudsonica. In contrast, the diatom Phaeodactylum tricornutum was nutritionally insufficient to A. hudsonica. In another set of experiments, the effects of A. fundyense and P. tricornutum, respectively, as sole foods on egg production and egg hatching success of two geographically separated populations (Maine and Connecticut) of the copepod A. hudsonica were examined in common-environment experiments, after being raised under identical conditions for two generations. The location in Maine regularly experiences toxic blooms of Alexandrium sp. whereas the location in Connecticut does not. During a 6-day period, A. fundyense reduced the egg production rates of the Connecticut copepod population, but not of the Maine population. In contrast, the diatom P. tricornutum reduced the egg production of both populations. These results of this study are consistent with the hypothesis of local adaptation to toxic food, but not to nutritionally insufficient food.     

Diel and seasonal vertical distribution of meiobenthic copepods in muddy sediments of a eutrophic lagoon (fish ponds of Arcachon Bay)

The vertical distribution of meiobenthic copepods was investigated within muddy sediments of a eutrophic lagoon (fish ponds of Arcachon Bay, France). The aim of the study was to determine if in muddy sediments, as previously established in sandy sediments, meiobenthic copepods migrate vertically according to the seasons or diel periods. Two experimental approaches were used, viz: a three-season comparison was made of the diel vertical distribution of the harpacticoid Canuella perplexa T. & A. Scott (1893) and secondly the depth distribution of a meiobenthic copepod assemblage was followed for a 24 h period, in shallow water subtidal locations. The harpacticoid C. perplexa vertically migrated through the top three centimeters of the sediment, showing diel and seasonal variations in depth distribution. The differential vertical distributions shown by the dominant meiobenthic populations suggest that emergence into the water column may mainly concern surface dwelling copepods. The physical and biological factors affecting seasonal and diel changes in the copepod assemblage of the fish ponds are discussed.     

Caridina nilotica in Lake Victoria: abundance, biomass, and diel vertical migration

Caridina nilotica (Decapoda: Atyidae) in offshore waters of Lake Victoria were investigated with both day and night sampling over a period of two years. Offshore populations are mainly planktonic rather than benthic, and the animals exhibit diel vertical migrations into near-surface waters at night. These changes in diel abundance as well as the size-frequency distribution of the migrating shrimp suggest that the migratory behavior is in response to visual planktivory, because only the very smallest individuals (2–4 mm) remain in surface waters during the day. During October 1992, abundances were estimated both by vertical net sampling and by underwater video transect methods. Concordance was established between abundances estimated by the two methods. Only about 9% (night) to 14% (day) of the Caridina population appeared to be epibenthic. We suggest that the behavior of the animal is consistent with the hypothesis that it is not a strict detritivore as previously reported; rather it may engage in facultative planktivory, especially at night.     

Diel vertical migration of the copepod <Emphasis Type="Italic">Thermocyclops inversus</Emphasis> (Kiefer, 1936) in a tropical reservoir: the role of oxygen and the spatial overlap with <Emphasis Type="Italic">Chaoborus</Emphasis>

The effect of water transparency, dissolved oxygen concentration and the invertebrate predator Chaoborus brasiliensis on the day–night vertical distribution of the copepod cyclopoid Thermocyclops inversus was investigated in a shallow tropical reservoir, Nado Reservoir, Belo Horizonte, Brazil. Diel cycles were carried out over a period of 12 consecutive months, between October 1999 and September 2000. The different developmental stages of T. inversus exhibited diel vertical migration (DVM) and displayed a clear ontogenetic trend, with the amplitude of DVM increasing with the age of the organism, and ranging from 0.4 m to 0.8 m for nauplii, 0.4 m to 1.2 m for copepodite, and 1.1 m to 2.1 m for adults. We observed that seasonal changes in dissolved oxygen and C. brasiliensis directly influenced the vertical distribution of the copepod population in this reservoir. Furthermore, it was showed that the diurnal vertical migration is an important predator avoidance behavior since it diminished the spatial overlap between prey and its potential predator. This finding supports the hypothesis that the vertical migration is a defense mechanism against predation. Thus, T. inversus is able to remain in the anoxic layers during day light hours, and at night they move upwards avoiding hypolimnetic waters to escape from predation by Chaoborus.     

Predator-induced diet vertical migration in a planktonic copepod

Predator evasion is the most commonly hypothesized reason fordiel vertical migrations undertaken by a wide variety of planktonicorganisms in lakes and seas, yet direct evidence remains elusive.We tested the predation hypothesis by exposing enclosed populationsof a marine copepod Acartia hudsonica to caged or free-rangingindividuals of their natural predator, the planktivorous fishGasterosteus aculeatus. After little more than a week, adultcopepods changed their vertical distribution and migration behaviordepending on the presence or absence of predation. Only free-rangingfish induced vertical migration in the copepod population. Cagedfish had no effect, indicating that vertical migration was nota simple chemically mediated response of copepods to the predator.Rather, copepods seemed to react to the presence of predatorsby other means, perhaps visual or mechanical stimuli, and toexhibit a downward escape response which, because encounterswith visually orienting fish occur chiefly in the daytime, effectivelylimited the copepods' occurrence in the upper water column tothe night-time hours. Alternatively, because fish imposed heavymortality on copepods, it is possible that selective predationaltered the proportions of individuals with fixed, geneticallydetermined migration behaviors. We suggest experiments to distinguishthese alternatives.     

Effect of the cyclopoid copepod Mesocyclops thermocyclopoides on the interactions between the predatory rotifer Asplanchna intermedia and its prey Brachionus calyciflorus and B. angularis

In many shallow, eutrophic subtropical ponds, brachionid rotifers are common prey of the predatory copepod Mesocyclops thermocyclopoides. The predatory rotifer Asplanchna intermedia, which is itself a potential prey of the copepod, also feeds preferentially on brachionids. We studied in the laboratory the population dynamics of two mutually competing prey species, Brachionus angularis and B. calyciflorus, in the presence of the two predators A. intermedia and M. thermocyclopoides. The experimental design included separate population dynamics studies with one prey–one predator, two prey–one predator, one prey–two predator, and two prey–two predator systems. These combinations were compared with controls, in which both the prey species (B. angularis and B. calyciflorus) were grown separately and in combination with each other. In the absence of any predator, B. angularis generally eliminated the larger B. calyciflorus. Selective predation by the copepod allowed B. calyciflorus to persist longer in competition with B. angularis. Feeding by M. thermocyclopoides on A. intermedia reduced the predation pressure on B. calyciflorus. However, given enough time, the cyclopoid copepod was able to eliminate both the brachionids as well as the predatory Asplanchna.     

Variability and possible adaptive significance of day-time vertical distribution ofLeptodora kindtii (Focke) (Cladocera) in a shallow eutrophic lake

The day-time vertical distribution of different size classes ofLeptodora kindtii in Tjeukemeer was studied during two contrasting years: 1978 and 1979. During the first year (1978) the predation pressure exerted by the planktivorous fish was rather high, whilst this was ca. 15 times lower during 1979. The diel vertical migration of different size classes ofLeptodora, was studied twice during 1979. Both studies support the predator avoidance hypothesis and also emphasize the idea that diel vertical migration is a dynamic rather than a fixed behaviour trait within a population.     

Latitudinal differentiation in the effects of the toxic dinoflagellate Alexandrium spp. on the feeding and reproduction of populations of the copepod Acartia hudsonica

Blooms of the dinoflagellate Alexandrium spp. increase in their frequency, toxicity and historical presence with increasing latitude from New Jersey (USA) to the Gaspé peninsula (Canada). Biogeographic variation in these blooms results in differential exposure of geographically separate copepod populations to toxic Alexandrium. We hypothesize that the ability of copepods to feed and reproduce on toxic Alexandrium should be higher in copepods from regions that are frequently exposed to toxic Alexandrium blooms. We tested this hypothesis with factorial common environment experiments in which female adults of the copepod Acartia hudsonica from five separate populations ranging from New Jersey to New Brunswick were fed toxic and non-toxic strains of Alexandrium, and the non-toxic flagellate Tetraselmis sp. Consistent with the hypothesis, when fed toxic Alexandrium we observed significantly higher ingestion and egg production rates in the copepods historically exposed to toxic Alexandrium blooms relative to copepods from regions in which Alexandrium is rare or absent. Such differences among copepod populations were not observed when copepods were fed non-toxic Alexandrium or Tetraselmis sp. These results were also supported by assays in which copepods from populations both historically exposed and naïve to toxic Alexandrium blooms were fed mixtures of toxic Alexandrium and Tetraselmis sp. Two-week long experiments demonstrated that when copepods from populations naïve to toxic Alexandrium were fed a toxic strain of Alexandrium they failed to acclimate, such that their ingestion rates remained low throughout the entire two-week period. The differences observed among populations suggest that local adaptation of populations of A. hudsonica from Massachusetts (USA) to New Brunswick (Canada) has occurred, such that some populations are resistant to toxic Alexandrium.     

Vertical, lateral and longitudinal movement of zooplankton in a large river

1. The spatial distribution and movement patterns of zooplankton in large rivers are little known compared with those in lake environments. We conducted a series of studies in the Ohio River (U.S.A.) during the low flow period to assess diel vertical (DVM), longitudinal and lateral movement of crustacean zooplankton. 2. The dominant large zooplankter, the copepod Eurytemora affinis, showed a consistent vertical migration pattern of daytime ascent and night‐time descent during all sampling periods – the reverse of the most common migratory pattern of zooplankton in lakes. The cladoceran Bosmina migrated in a similar way in two of the three sampling periods. Surveys taken longitudinally in the river showed similar trends for both taxa. 3. During the lateral surveys, E. affinis was significantly more abundant in the shallow littoral zone during the night than in the daytime. The combination of vertical and lateral movement patterns along with the diel distribution of zooplanktivorous fish suggest that these movements are a predator‐avoidance mechanism. 4. Sampling programmes in large rivers should consider that larger zooplankton such as E. affinis may not be randomly distributed in the river channel and behaviours such as diel vertical migration may be just as evident in river habitats as in lakes.     

Predator-dependent diel migration by <Emphasis Type="Italic">Halocaridina rubra</Emphasis> shrimp (Malacostraca: Atyidae) in Hawaiian anchialine pools

Diel migration is a common predator avoidance mechanism commonly found in temperate water bodies and increasingly in tropical systems. Previous research with only single day and night samples suggested that the endemic shrimp, Halocaridina rubra, may exhibit diel migration in Hawaiian anchialine pools to avoid predation by introduced mosquito fish, Gambusia affinis, and perhaps reverse migration to avoid the predatory invasive Tahitian prawn, Macrobrachium lar. To examine this phenomenon in greater detail, we conducted a diel study of H. rubra relative abundance and size at 2-h intervals in three anchialine pools that varied in predation regime on the Kona-Kohala Coast of Hawai‘i Island. We found two distinct patterns of diel migration. In two pools dominated by visually feeding G. affinis, the abundance of H. rubra present on the pool bottom or swimming in the water column was very low during the day, increased markedly at sunset and remained high until dawn. In contrast, in a pool dominated by the nocturnal predator M. lar, H. rubra density was significantly lower during the night than during the day (i.e., a pattern opposite to that of shrimp in pools containing fish). In addition, we observed that the mean body size of the shrimp populations varied among pools depending upon predator type and abundance, but did not vary between day and night in any pools. Our results are consistent with the hypothesis that H. rubra diel migratory behavior and size distributions are influenced by predation regime and suggest that diel migration may be a flexible strategy for predator avoidance in tropical pools where it may be a significant adaptive response of endemic species to introduced predators.     

Effects of Protoceratium reticulatum yessotoxin on feeding rates of Acartia hudsonica: A bioassay using artificial particles coated with purified toxin

Paralytic shellfish toxins produced by dinoflagellates are known to deter copepod grazing. Dinoflagellate species, including Protoceratium reticulatum, also produce disulfated polyether yessotoxins that were previously referred to as diarrheic shellfish toxins. However, the role of yessotoxins in predator–prey relationships is not yet clear. In the present study, the effects of purified yessotoxin (YTX) on feeding activities of Acartia hudsonica (Copepoda, Calanoida) were experimentally investigated. Polystyrene fluorescent microspheres (10 μm in diameter) colored bright blue or yellow-green were coated with cell extracts of P. reticulatum that do not produce yessotoxins. The bright blue microspheres were further coated with YTX, and the yellow-green microspheres were used as the reference. The microspheres were then given to the copepods separately or in combination to measure clearance rates and feeding selectivity. A. hudsonica was found to feed on the yellow-green microspheres without YTX at twice the rate of the bright blue microspheres with YTX. We also confirmed that microsphere color per se did not affect the feeding rates. The bright blue microspheres adsorbed 1.8–43.3 pg of YTX per microsphere, which is similar to the cell-specific yessotoxin content of toxic P. reticulatum found in natural environments. These results suggest that production of yessotoxin is advantageous for P. reticulatum by deterring predation by copepods.     

Daphnia size structure,vertical migration,and phosphorus redistribution

The timing and magnitude of diel migration in two daphnid assemblages were determined from a series of vertical profiles of daphnid size distribution. Animals were collected concurrently for gut fullness determination. Only large daphnids (> 1.4 mm) migrated, but these animals could account for substantial vertical and diel differences in phosphorus excretion rate. Gut fullness measurements and time courses of diel vertical migration suggested that large Daphnia can cause a net downward flux of phosphorus during summer in thermally stratified lakes.     

The swimming and feeding behavior of Mesocyclops

The swimming and feeding behaviors of Mesocyclops are described from a review of the literature and personal observations. Mesocyclops exhibits considerable behavioral flexibility in response to environmental stimuli. Mesocyclops edax exhibits an increase in horizontal looping behavior at high prey densities, and performs a tight vertical looping behavior in response to the loss of captured prey. Ingestion rates by Mesocyclops are a complex function of prey density, morphology, and behavior in addition to prey size. Vertebrate predators induce a rapid escape response in Mesocyclops and may be responsible at least in part for their extensive diel vertical migrations. The complex behavioral patterns of Mesocyclops suggest that its distribution and abundance in nature will be distinctly nonrandom and influenced as much by its own behavioral responses as by other external physical factors such as water circulation patterns.     

The role of prey stratification in the predation pressure by the cydippid ctenophore Mertensia ovum in the Barents Sea

The cydippid ctenophore Mertensia ovum occurs throughout the Norwegian arctic regions at least from the ice edge to the Arctic Circle. Using new data from the Barents and Greenland Seas, a simple model is constructed in which the upper boundary conditions for the trophic impact of Mertensia on populations of Calanus in this area are explored. Based on abundance data from MOCNESS and vertical net samples, experimental data on feeding and a range of typical values for the abundance of the principal copepod species, the range of probable predation pressure on copepods is calculated. Using typical abundances of the copepods and ctenophores in the Barents Sea, M. ovum appears to be capable of consuming a maximum of ca 1–5% d^–1 of the copepods in the water where it occurs. Vertical and horizontal spatial coupling probably plays a significant role in determining the extent of predation for this predator. Predation by other ctenophores may be a significant factor in its own biology.     

Diel and tidal changes in the distribution and feeding habits of Japanese temperate bass Lateolabrax japonicus juveniles in the surf zone of Ariake Bay

Japanese temperate bass Lateolabrax japonicus juveniles recruit to the surf zone and grow by feeding on commonly occurring coastal copepods. However, little is known about diel and tidal patterns in their migration and feeding habits. We sampled wild juveniles during the neap and spring tides, over periods of 24 h, with small seine nets in the sand flat of the eastern part of Ariake Bay, Kyushu, western Japan. In both the neap and spring tides, abundance of juveniles significantly increased during the daytime, being highest around the time of high tide. The relative gut fullness indices of juveniles drastically increased in the morning (0700–0900) and during the flood tide in the daytime, while major prey copepod (Paracalanus spp.) density in the ambient water was relatively constant. We summarized that L. japonicus juveniles would migrate to the surf zone after sunrise to feed on copepods, and then emigrate from the surf zone after sunset. The migratory behavior of L. japonicus juveniles would be influenced by light (daytime) and feeding activity influenced by both light (morning) and tidal condition (flood tide). The intertidal region of the tidal flat was recognized to be one of the important habitats for L. japonicus during their early life history.     

Chemical, mechanical and visual cues in the vertical migration behavior of the marine planktonic copepod Acartia hudsonica

Recent experimental evidence in both marine and freshwater systemsindicates that predators can induce vertical migration behaviorin individual zooplankters, yet the specific cues by which zooplankterssense their predators appear to vary. In situ manipulation experimentswere carried out with enclosed populations of the marine planktoniccopepod Acartia hudsonica to re-examine the potential role ofchemical cues in the behavior of A.hudsonica, and to test explicitlyfor the role of mechanical or visual stimuli in triggering verticalmigration behavior in this species. Adult female copepods wereinduced to vertically migrate (descend) when exposed to fishmimics during the day, but no such response occurred when thecopepods were exposed to Fish mimics during the night. Moreover,copepods exhibited no changes in vertical distribution whenexposed to water which, having recently held a natural predator(the threespine stickleback, Gasterosteus aculeatus), was presumedto be laden with predator-produced chemical exudates. Predator-mediatedmechanical or visual cues, or a hierarchy of both, are responsiblefor eliciting vertical migration behavior in adult female A.hudsonica.These results, together with those of other investigations demonstratingthe inducing role of chemical exudates, indicate that the stimulieliciting vertical migration in zooplankton can be expectedto vary between species.     

Top-down control in pelagic systems: a role for invertebrate predation

Limnologists have long recognized the importance of predation in freshwater communities. The majority of study of predator effects has involved vertebrate predators, with emphasis on planktivorous fish. Documented effects of planktivorous fish have been so dramatic that manipulations of their populations are seen by many as potential tools in lake management. However, the success of such manipulations is often less than desired due to the ubiquitous complexity of food webs and the pervasiveness of compensatory responses to food web manipulation. Recently, enormous effort has been applied to the Lake Kinneret pelagic food web in effort to reduced the abundance of the planktivorous Kinneret bleak Acanthobrama terraesanctae and thereby increase the biomass of herbivorous zooplankton in the hopes of increasing water clarity. We compared potential predation pressure on Lake Kinneret herbivorous zooplankton by bleak and the other major zooplankton predators in the lake, the cyclopoid copepods Mesocyclops ogunnus and Thermocyclops dybowskii. We found that, despite having much lower biomass, cyclopoid copepods accounted for a greater portion of the predation mortality on herbivorous zooplankton than bleak. Our results suggest that reductions in predation pressure by bleak will not yield subsequent increases in herbivorous zooplankton biomass. Rather, reductions in bleak predation pressure may allow for increases in cyclopoid copepod abundance and thereby a net increase in predation pressure on herbivorous zooplankton.