Prey Detection and Prey Capture in Copepod Nauplii

Copepod nauplii are either ambush feeders that feed on motile prey or they produce a feeding current that entrains prey cells. It is unclear how ambush and feeding-current feeding nauplii perceive and capture prey. Attack jumps in ambush feeding nauplii should not be feasible at low Reynolds numbers due to the thick viscous boundary layer surrounding the attacking nauplius. We use high-speed video to describe the detection and capture of phytoplankton prey by the nauplii of two ambush feeding species (Acartia tonsa and Oithona davisae) and by the nauplii of one feeding-current feeding species (Temora longicornis). We demonstrate that the ambush feeders both detect motile prey remotely. Prey detection elicits an attack jump, but the jump is not directly towards the prey, such as has been described for adult copepods. Rather, the nauplius jumps past the prey and sets up an intermittent feeding current that pulls in the prey from behind towards the mouth. The feeding-current feeding nauplius detects prey arriving in the feeding current but only when the prey is intercepted by the setae on the feeding appendages. This elicits an altered motion pattern of the feeding appendages that draws in the prey.     

Phylogenetic implications of the Crustacean nauplius

The plesiomorphic mode of crustacean development is widely accepted to be via a larva called the nauplius. Extant taxa like the Cephalocarida, Branchiopoda, Ostracoda, Mystacocarida, Copepoda, Cirripedia, Ascothoracida, Facetotecta, Euphausiacea and Penaeidea hatch from an egg as a free-living nauplius. Other crustaceans show an embryonic phase of development suggestive of a naupliar organization. Several features of the nauplius larva have been proposed as diagnostic characters for the Crustacea: a median (nauplius) eye; at least three pairs of head appendages (antennules, antennae, mandibles); a posteriorly directed fold (the labrum) extending over the mouth and a cephalic (nauplius) shield. The relationship between trilobite protaspis with at least four appendages and the crustacean nauplius remains unclear, but reports of a copepod orthonauplius with four appendages are rejected. Swimming is suggested to represent the underived mode of locomotion for the crustacean nauplius, and that naupliar swimming directly results in naupliar feeding which also is underived.     

Zur Biologie vonParamphiascella fulvofasciata (Copepoda,Harpacticoida)

The benthic harpacticoid copepodParamphiascella fulvofasciata Rosenfield & Coull was collected from holdfasts ofLaminaria hyperborea from a subtidal area of Helgoland (North Sea). All developmental stages ofP. fulvofasciata are raptorial feeders. The feeding of the nauplii is advanced by a marginal setule-crest of the labrum which prevents food-particles from being swept away. The oral appendages of the copepodites circumscribe a frustal space ventral to the mouth which facilitates uptake of food-particles. The nauplii are not able to swim and perform stalking movements with their antennal endopodites. Good swimming ability as well as digging-in-behaviour and negative phototaxis of the copepodites indicate epi- as well as inbenthic mode of life. Several life-cycle characters are described. Precopula lasts ca. one day. The mean egg-number is 27, and mean egg-diameter is 87 × 75 µm. The number of nauplii per egg (double)-sac amounts to 25–30. Developmental time at 19°C is 6–9 days (nauplii) and 20–24 days (copepodites). The whole developmental period lasts 28 days. The maximal lifespan in the laboratory is 193 days. Sex-ratio is almost balanced. Females produce egg-sacs more than 3.5 times during their life period. Seasonal effects on reproductive activity have not been detected in laboratory cultures.     

Appendage activity recordings of the sub-Antarctic copepod Drepanopus pectinatus in relation to its feeding behaviour

Summary Movements of the cephalic appendages of nauplii (stages 3 and 4), copepodites (stage 4) and adult female Drepanopus pectinatus were investigated using a computerized micro-impedance unit. Direct measurements and visual observations of the behaviour of restrained copepods were made in the presence of filtered seawater, naturally occurring phytoplankton of different sizes, prefiltered extracts of phytoplankton and seston. The normal appendage movements recorded in filtered seawater were similar for adult females and copepodites. Traces for nauplii were different compared with those of the two other developmental stages. Appendage movements were modified when adult females were offered particles of different sizes and extracts of phytoplankton, showing significant changes in the frequency of the limb beats in relation to each stimulus. Impedance traces distinguished between activity of copepod appendages related to feeding and to swimming such as: flicking, stroking, jerking, combing, handling and rejecting particles. Prolonged recordings of restrained females in association with visual observations suggested that the activity of the mandibular palp was related to gut fullness and peristaltic movements, and to fecal pellet formation and evacuation. These results indicated that D. pectinatus is an intermittent beater responding to the physical and chemical characteristics of food.     

Naupliar and Metanaupliar Development of Thysanoessa raschii (Malacostraca,Euphausiacea) from Godth?bsfjord,Greenland, with a Reinstatement of the Ancestral Status of the Free-Living Nauplius in Malacostracan Evolution

The presence of a characteristic crustacean larval type, the nauplius, in many crustacean taxa has often been considered one of the few uniting characters of the Crustacea. Within Malacostraca, the largest crustacean group, nauplii are only present in two taxa, Euphauciacea (krill) and Decapoda Dendrobranchiata. The presence of nauplii in these two taxa has traditionally been considered a retained primitive characteristic, but free-living nauplii have also been suggested to have reappeared a couple of times from direct developing ancestors during malacostracan evolution. Based on a re-study of Thysanoessa raschii (Euphausiacea) using preserved material collected in Greenland, we readdress this important controversy in crustacean evolution, and, in the process, redescribe the naupliar and metanaupliar development of T. raschii. In contrast to most previous studies of euphausiid development, we recognize three (not two) naupliar (= ortho-naupliar) stages (N1-N3) followed by a metanauplius (MN). While there are many morphological changes between nauplius 1 and 2 (e.g., appearance of long caudal setae), the changes between nauplius 2 and 3 are few but distinct. They involve the size of some caudal spines (largest in N3) and the setation of the antennal endopod (an extra seta in N3). A wider comparison between free-living nauplii of both Malacostraca and non-Malacostraca revealed similarities between nauplii in many taxa both at the general level (e.g., the gradual development and number of appendages) and at the more detailed level (e.g., unclear segmentation of naupliar appendages, caudal setation, presence of frontal filaments). We recognize these similarities as homologies and therefore suggest that free-living nauplii were part of the ancestral malacostracan type of development. The derived morphology (e.g., lack of feeding structures, no fully formed gut, high content of yolk) of both euphausiid and dendrobranchiate nauplii is evidently related to their non-feeding (lecithotrophic) status.     

Distinctly different behavioral responses of a copepod,Temora longicornis,to different strains of toxic dinoflagellates,Alexandrium spp.

Zooplankton responses to toxic algae are highly variable, even towards taxonomically closely related species or different strains of the same species. Here, the individual level feeding behavior of a copepod, Temora longicornis, was examined which offered 4 similarly sized strains of toxic dinoflagellate Alexandrium spp. and a non-toxic control strain of the dinoflagellate Protoceratium reticulatum. The strains varied in their cellular toxin concentration and composition and in lytic activity. High-speed video observations revealed four distinctly different strain-specific feeding responses of the copepod during 4 h incubations: (i) the ‘normal’ feeding behavior, in which the feeding appendages were beating almost constantly to produce a feeding current and most (90%) of the captured algae were ingested; (ii) the beating activity of the feeding appendages was reduced by ca. 80% during the initial 60 min of exposure, after which very few algae were captured and ingested; (iii) capture and ingestion rates remained high, but ingested cells were regurgitated; and (iv) the copepod continued beating its appendages and captured cells at a high rate, but after 60 min, most captured cells were rejected. The various prey aversion responses observed may have very different implications to the prey and their ability to form blooms: consumed but regurgitated cells are dead, captured but rejected cells survive and may give the prey a competitive advantage, while reduced feeding activity of the grazer may be equally beneficial to the prey and its competitors. These behaviors were not related to lytic activity or overall paralytic shellfish toxins (PSTs) content and composition and suggest that other cues are responsible for the responses.     

The Nauplius Larva of Crustaceans: Functional Diversity and the Phylotypic Stage

SYNOPSIS. The crustacean nauplius larva is a development stagecharacterized by the presence of three pairs of head appendages.All crustaceans pass through the naupliar stage whether embryonicallyor as freeliving larvae. The nauplius is thought to be the phylotypicstage and represent a fundamental developmental constraint incrustaceans. However, free-living nauplii are primitive andI present evidence that this form is functionally plastic, e.g.,locomotory modes are diverse even in closely related species.I argue that this functional plasticity allowed the persistenceof nauplii in the early evolution of crustaceans and, as a consequence,naupliar development became a deep-seated feature of crustaceans.Thus, we see nauplii as phylotypic. This suggests that, in spiteof the presence of phylotypic stages in various phyla, phylotypyitself may not represent a similar, underlying developmentalconstraint in every case.     

Transitions from Drag-based to Lift-based Propulsion in Mammalian Swimming

The evolution of fully aquatic mammals from quadrupedal, terrestrialmammals was associated with changes in morphology and swimmingmode. Drag is minimized by streamlining body shape and appendages.Improvement in speed, thrust production and efficiency is accomplishedby a change of swimming mode. Terrestrial and semiaquatic mammalsemploy drag-based propulsion with paddling appendages, whereasfully aquatic mammals use lift-based propulsion with oscillatinghydrofoils. Aerobic efficiencies are low for drag-based swimming,but reach a maximum of 30% for lift-based propulsion. Propulsiveefficiency is over 80% for lift-based swimming while only 33%for paddling. In addition to swimming mode, the transition tohigh performance propulsion was associated with a shift fromsurface to submerged swimming providing a reduction in transportcosts. The evolution of aquatic mammals from terrestrial ancestorsrequired increased swimming performance with minimal compromiseto terrestrial movement. Examination of modern analogs to transitionalswimming stages suggests that only slight modification to theneuromotor pattern used for terrestrial locomotion is requiredto allow for a change to lift-based propulsion.     

Larval development of Japanese 'conchostracans': part 1, larval development of Eulimnadia braueriana (Crustacea, Branchiopoda, Spinicaudata, Limnadiidae) compared to that of other limnadiids

As a part of a project to compare phylogenetically the larval or embryonic development of all major taxa of the Branchiopoda (Crustacea), the larval development of the Japanese spinicaudatan clam shrimp Eulimnadia braueriana Ishikawa, 1895, is described. Seven naupliar stages are recognized, based mainly on significant morphological differences between them, but in one case, on size alone. The seven stages range in length from 156 µm to 760 µm. Nauplius 1 is nonfeeding with incompletely developed and nonfunctional feeding structures. Nauplius 2 has apparently functional feeding structures, including a well-developed mandibular gnathobase, setulate protopodal endites of the antennae, and setules on various setae involved in swimming and food manipulation. Nauplius 3 is morphologically identical to Nauplius 2, but more than 50% larger. In nauplius 4, the coxal endite (naupliar process) of the antennae develops a bifid tip. Nauplius 5 has a lateral pair of primordial carapace lobes, and the first 4–5 pairs of trunk limb buds are weakly developed, making the anterior part of the trunk wider than the posterior. In nauplius 6, five pairs of trunk limb buds are visible externally and a small carapace has appeared, reaching approximately to trunk limbs 2; also, the pair of large buds behind the mandibles in previous stages has become divided into a large, anterior, setose bud and two smaller, posterior buds. The identities of these structures as either paragnaths or maxillules/maxillae remain uncertain. In nauplius 7, about six pairs of trunk limb buds are visible externally. The general morphology of the nauplius larvae of E. braueriana is much like those of the well-known Limnadia lenticularis (Linnaeus, 1758) and Eulimnadia texana Packard, 1871, including an elongate, lanceolate labrum; however, because of various heterochronies, the correspondence between the larval sequences of these species is not perfect. There is even less correspondence with the 5-stage larval development reported for Limnadia stanleyana King, 1855, and the spatulate labra of that species and Jmnadia spp. are different from those of other known limnadiid nauplii. The larvae of E. braueriana possess many typical (and synapomorphic) branchiopod features, such as the general morphology of the appendages involved in feeding and the mode of trunk limb development, while the small buds of the first antennae and the exact number and development of the parts of the trunk limbs are typical for the Spinicaudata.     

The scaling and structure of aquatic animal wakes

Animal generated water movements are visualized and quantifiedusing two-dimensional particle image velocimetry (PIV). Theresulting vector flow fields allow for the study of the distributionof velocity, vorticity and vortices. Structural and temporalaspects of animal-induced flows covering a range of Reynolds(Re) numbers between less than 1 to more than 10⁴ are presented. Maps of flow induced by continuous foraging and intermittentescape responses of tethered nauplius and copepodid stages ofthe marine copepod Temora longicornis offer insight in viscosity-dominatedflow regimes. Fast escape responses of the equally sized largestnauplius stage and the smallest copepodid stage are compared.The nauplius moves by generating a viscous flow pattern withhigh velocities and vorticity; the copepodid moves by usinginertial effects to produce a vortex ring with a rearward jetthrough the center. Larvae and small adult fish (zebra danio) use a burst-and-coast-swimmingmode at Re numbers up to 6,000, shedding a vortex ring withthe associated jet at the tail during the burst phase. Flowpatterns during the coasting phase differ between the smalllarvae and larger adults due to the changes in importance ofviscosity. A 12 cm long mullet swimming in a continuous mode generatesa chain of vortex rings with a backward undulating jet throughthe centers of the rings at Re numbers of 4 x 10⁴ in inertia-dominatedregimes. Our empirical results provide realistic insight in the scaleeffects determining the morphology of the interactions betweenanimals and water.     

Swimming and cleaning in the free-swimming phase of Argulus larvae (crustacea, branchiura)--appendage adaptation and functional morphology

The free-swimming early larval stages of Argulus foliaceus (Linneaus) (Branchiura) are studied using digital video, light microscopy, and SEM. We analyze and document the mode of swimming in the hatching stage of A. foliaceus and the subsequent juvenile stages with fully developed thoracopods. We present new observations and an analysis of the functional morphology of a cleaning behavior in the first stage. This stage swims very efficiently using the large exopods of the second antennae in concert with the mandibular palp (naupliar limbs), while the subsequent stages use the now developed thoracopods for propulsion. This posterior shift in propulsion is similar to--but independent from--what is seen in other crustaceans. The hatching stage has previously been referred as a "metanauplius" but as the first and second maxillae are developed and active, and buds of all four thoracopods are present, it is too advanced to be included in the naupliar phase. The hooks of the first antennae and the distal hooks of the maxillae are demonstrated to function not only as attachment organs (to the host), but also to play a significant role in the cleaning of the naupliar swimming appendages. A digital video-based analysis of the swimming mode is provided. The larval swimming pattern is generally similar to that of other crustaceans such as Branchiopoda and Cirripedia, but autapomorphies of the Branchiura include the following: 1) While actively swimming, the naupliar appendages are almost straight during the recovery stroke and 2) they have a relatively small deflection during movement ( approximately 25 degrees or approximately 35 degrees for mandible and second antenna respectively), 3) the larval mandible has a uniramous palp which is the retained exopod. The morphological implications of the transition from the possibly nonfeeding pelagic, or free-swimming, first larval stage to the feeding, parasitic second stage are discussed and compared with other crustaceans.     

Predaceous feeding habits of Limnocalanus macrurus

Limnocalanus macrurus, a large, glacial-relict copepod, hasbeen assumed an omnivore or a herbivore; predaceous habits ofthe species are unknown. The predaceous feeding habits of Limnocalanusfrom Lake Michigan were studied in the laboratory using naturalprey. Predation rates were highest on copepod nauplii. Copepoditesof Diaptomus spp. and Cyclops spp. were preyed upon at lowerrates. Limnocalanus preyed selectively upon nauplii <300µm. Small cyclopoid copepodites (<–750 µm)were also selected over large copepodites. Experiments usingtwo prey types showed that nauplii were selected over all copepodites,and that no selectivity existed for either diaptomid or cyclopoidcopepodites. Predaceous feeding habits began in the fourth copepoditestage of Limnocalanus. Predaceous feeding rates of Limnocalanuschanged seasonally being highest in late spring and autumn andlowest in summer and early winter. Since Limnocalanus also feedson net-phytoplankton, predation rate changes may be relatedto changes in the relative abundance of large phytoplanktonand naupliar prey in nature. Limnocalanus predation may be animportant factor in structuring the zooplankton community. Present address: Great Lakes Research Division, University Michigan,Ann Arbor, MI 48109, USA     

Individual to population level effects of South Louisiana crude oil water accommodated hydrocarbon fraction (WAF) on a marine meiobenthic copepod

Acute toxicities of crude oil and crude oil water accommodated hydrocarbon fraction (WAF) are relatively well documented, but data on the biological effects of chronic exposures to WAF on species and populations are scarce. South Louisiana Sweet crude oil was used to assess the effects of crude oil WAF on the copepod Amphiascus tenuiremis' survival, development and reproduction. Effects were evaluated using a 96-well microplate full life-cycle toxicity test, a test that allows tracking of individuals from the nauplius stage to sexual maturation and reproduction. Briefly, 24-h hatched nauplii were followed to adulthood (n_i = ≥ 120 nauplii/treatment) in individual glass-coated microplate wells containing 200 μL of seawater solution. Treatments consisted of 10%, 30%, 50% and 100% Louisiana WAF, with seawater used as control. Nauplii were monitored through development to adulthood, and sexually mature virgin copepods were mated pairwise in wells containing original rearing treatments. Nauplius-to-copepodite survival was reduced by 57% in exposures to 100% WAF, relative to controls (88 ± 3%), and copepodite-to-adult survival was reduced by 18% in the 50% WAF, relative to controls (98 ± 3%). Analysis of development curves showed that nauplii in the 10% WAF developed significantly faster into copepodites, while nauplii in the 50% WAF developed significantly slower than controls. Although the naupliar developmental rate in the 100% WAF was not significantly different from the control, these nauplii showed an average 1.4 day delay in development into copepodites. Similarly, copepodite development into mature females and males was significantly enhanced by 1.2 to 1.8 days and delayed by 1.9 to 2.2 days (p < 0.05) in the 10% and 50% WAFs, respectively, compared to controls. Although the copepodite developmental rate in the 100% WAF was not significantly different from the control, these copepodites still showed an average 1.5 and 2.1 day delay in development into females and males, respectively. Analysis of reproductive endpoints showed that fertility was the only endpoint negatively affected by WAFs; reproductive failure increased by 30% and 41% in exposures to 30% and 100% WAF, respectively, compared to controls (3.33 ± 4.71%). Leslie matrix population projections based on empirical microplate data indicated lower production rates through three generations of exposure to WAFs. Furthermore, a comparison between NIST and Louisiana crude oil WAFs using the same life-cycle approach indicated a greater chronic toxicity for the Louisiana WAF and an overall developmental delay in exposures to high WAFs (50% and 100% WAFs) from both crude oil types.     

Propulsion in Cubomedusae: Mechanisms and Utility

Evolutionary constraints which limit the forces produced during bell contractions of medusae affect the overall medusan morphospace such that jet propulsion is limited to only small medusae. Cubomedusae, which often possess large prolate bells and are thought to swim via jet propulsion, appear to violate the theoretical constraints which determine the medusan morphospace. To examine propulsion by cubomedusae, we quantified size related changes in wake dynamics, bell shape, swimming and turning kinematics of two species of cubomedusae, Chironex fleckeri and Chiropsella bronzie. During growth, these cubomedusae transitioned from using jet propulsion at smaller sizes to a rowing-jetting hybrid mode of propulsion at larger sizes. Simple modifications in the flexibility and kinematics of their velarium appeared to be sufficient to alter their propulsive mode. Turning occurs during both bell contraction and expansion and is achieved by generating asymmetric vortex structures during both stages of the swimming cycle. Swimming characteristics were considered in conjunction with the unique foraging strategy used by cubomedusae.     

Feeding convergence in South American and African zooplanktivorous cichlids Geophagus brasiliensis and Tilapia rendalli

Synopsis Acará, Geophagus brasiliensis, and red-breasted bream, Tilapia rendalli, are important planktivorous cichlids in southern Brazilian lakes and reservoirs. In laboratory experiments, I quantified behavior and selectivity of different sizes of these two fish feeding on lake zooplankton. Feeding behavior depended on fish size. Fish < 30 mm were visual feeders. Fish 30–50 mm either visually fed or pump-filter fed depending on zooplankton size. Fish > 70 mm were pump-filter feeders. Replicate 1 h feeding trials revealed that, as the relative proportions of prey changed during an experiment, acará (30–42 mm, standard length) and tilapia (29–42 mm) shifted from visual feeding on large evasive copepods to filter feeding on small cladocerans and rotifers. Electivity and feeding rate increased with prey length, but were distinct for similar-sized cladocerans and copepods. Visual/filter-feeding fish had lowest electivities for small and poorly evasive rotifers and cyclopoid nauplii. They fed non-selectively on cyclopoid copepodites, had intermediate electivities for calanoid nauplii and small cladocerans, and had highest electivities for large cladocerans, cyclopoid adults, and calanoid copepodites and adults. Although belonging to different cichlid genera and native to South America and Africa, respectively, acará and red-breasted bream (= congo tilapia) exhibited similar selectivity for zooplankton. Apparently, few stereotyped feeding behaviors have evolved during the acquisition of microphagy in fish. Shift in feeding modes allows these two species to optimally exploit the variable and dynamic patchy distribution of planktonic resources.     

Morphological aspects of the development of swimming and feeding functions in the milkfishChanos chanos

Development of swimming and feeding abilities based on morphological development of larval and early juvenileChanos chanos was investigated. In larvae smaller than about 6.5 mm SL, mechanical supports of fins and branchial arches were in a primordial stage of development. Supports and rays of the vertical fins and branchial arches rapidly developed from 6.5 mm SL, and all components appeared by about 10.5 mm SL. Thereafter body depth proportion changed and the supports and rays of the paired fins and gill-rakers developed. These developmental events were nearly or totally completed by about 17 mm SL, and we concluded that the larvae transformed to juveniles at this size. By this time, the mode of swimming of the fish shifted from undulating locomotion to caudal propulsion and that of feeding from swallowing paniculate food to filtering and concentrating substrate food matters using gill-rakers and the epibranchial organ. One of the most characteristic, and well-known, phenomena in the life history ofChanos chanos is the mass occurrence in the surf zone of postlarvae of a limited size range. In view of the scheme of the development of mechanical supports of the body and fins, they may acquire a swimming ability strong enough to move against the current only upon reaching about 10.5 mm SL, and if active shoreward migration of the larvae occurs, it is only during the late period of their journey from the spawning grounds to the shore. The sudden disappearance from the surf zone of larvae larger than 15–16 mm SL is obviously related to a change in food habit.     

The effect of size and temperature on the frequency of limb beat of Temora longicornis Müller (Crustacea : Copepoda)

Copepods normally swim by rhythmically beating the cephalic limbs, so records of antennal movements represent their activity. The limb beat rate of Temora longicornis Müller was determined in relation to several factors. There was an inverse relationship between swimming rate and body size, and activity increased with environmental temperature up to 20–25°C. Copepods readily acclimated, as those kept at 15°C were less active than those kept at 5°C. The summer population was also less active in the low temperature range, but swimming reached a higher rate at higher temperatures than were tolerated by the winter population. No difference in rate of limb beat was found between similar sized males and females over a wide range of temperatures.     

Energetics of swimming by the ferret: consequences of forelimb paddling.

The domestic ferret (Mustela putorius furo) swims by alternate strokes of the forelimbs. This pectoral paddling is rare among semi-aquatic mammals. The energetic implications of swimming by pectoral paddling were examined by kinematic analysis and measurement of oxygen consumption. Ferrets maintained a constant stroke frequency, but increased swimming speed by increasing stroke amplitude. The ratio of swimming velocity to foot stroke velocity was low, indicating a low propulsive efficiency. Metabolic rate increased linearly with increasing speed. The cost of transport decreased with increasing swimming speed to a minimum of 3.59+/-0.28 J N(-1) m(-1) at U=0.44 m s(-1). The minimum cost of transport for the ferret was greater than values for semi-aquatic mammals using hind limb paddling, but lower than the minimum cost of transport for the closely related quadrupedally paddling mink. Differences in energetic performance may be due to the amount of muscle recruited for propulsion and the interrelationship hydrodynamic drag and interference between flow over the body surface and flow induced by propulsive appendages.