Escape behavior of Acartia hudsonica copepods during interactions with scyphomedusae

Calanoid copepods possess remarkable abilities to detect andescape from hydrodynamic disturbances, such as those createdby approaching predators. At the same time, a number of studiesin coastal ecosystems have suggested that gelatinous predators,including medusae in the Class Scyphozoa, exert top-down controlon copepod populations. Although prey escape behavior playsa critical role in predation models, we have relatively littleempirical data on how copepods respond to encounters with scyphomedusae.In this study, I used video to quantify encounter rates andescape behaviors of the copepod Acartia hudsonica during interactionswith two scyphomedusae, Aurelia aurita and Cyanea sp., in twoflow regimes. Escapes were complex, variable and effective.Fewer than 1% of encounters resulted in ingestion. Typically,A.hudsonica avoided contact by responding when predators remainedseveral body lengths (4 to 10 mm) distant and stringing togethermany escape jumps at submaximum velocities (33 to 59 mm s^–1).In addition, copepodite stages behaved passively—or failedto respond—following encounters with medusae more oftenthan did adults. Because escape behavior exhibited by A.hudsonicawas so variable, it is unlikely that medusae capture copepodsusing a single, quantifiable mechanism. A range of responseswithin populations and individuals may be the best strategyfor zooplankton faced with strong predation pressure from avariety of predators.     

Effect of prey size on vulnerability of copepods to predation by the scyphomedusae Aurelia aurita and Cyanea sp.

A growing number of studies correlate changes in zooplanktonpopulations with abundance of medusae, but we cannot yet explainor predict the specific factors driving these interactions.This study demonstrates that the size of copepods has a significantinfluence on their vulnerability to predation by scyphomedusae.This finding is important because prey size, independent ofbehavior, has been neglected in theoretical models of predationby medusae. In experiments in a planktonkreisel, we used liveand heat-killed prey (Acartia hudsonica adults and copepodites)to separate the effects of copepod size and behavior on feedingrates by two medusae (Aurelia aurita and Cyanea sp.). Resultsrevealed that: differences in copepod size had a significantimpact on feeding rates, and thus small size can provide a refugefrom predation; behavior of adults diminished the liabilityassociated with larger size; and medusae with different morphologiesingested A.hudsonica at similar rates. Other experiments demonstratedthat medusae digested copepods at different rates based on preysize and predator species, findings that have implications forall future laboratory and field studies that assess feedingby scyphomedusae. Finally, this study illustrates how laboratorystudies serve as critical supplements to field observations.The effect of prey size on feeding rates can be confounded bydifferences in prey behavior, yet explains why small copepodswere typically ingested at relatively low rates by medusae.Size was clearly a dominant factor influencing copepod vulnerabilityacross scyphomedusan species, even those with very differentmorphologies. Future work should focus on the mechanisms ofsize selection, or the factors influencing contact and retentionrates.     

Capture mechanisms used by the lobate ctenophore, Mnemiopsis leidyi, preying on the copepod Acartia tonsa

Although the lobate ctenophore Mnemiopsis leidyi is an influentialplanktonic predator, the mechanisms enabling it to capture itscharacteristically wide range of prey have not been systematicallyexamined. We recorded interactions between free-swimming M.leidyiand two stages (nauplii, adults) of the calanoid copepod Acartiatonsa in order to determine a mechanistic explanation of thisfeeding process. Prey encounter with Mnemiopsis involved twodifferent processes. The first depended on fluid motions createdby the nearly continuous beating of cilia lining the four auricles.These cilia created a low-velocity flow in which A.tonsa naupliiwere entrained (94% of naupliar encounters) and transportedpast the oral lobes onto the tentillae (oral tentacles). Thenauplii, although capable of rapid escape responses, generallyappeared to be insensitive to the current in which they werecarried. The second process relied upon the collision of swimmingprey with the inner surfaces of the oral lobes and was not obviouslyinfluenced by the auricular feeding currents. Adult A.tonsawere rarely entrained in the auricular flow, but, instead, propelledthemselves into contact with the oral lobes (97% of adult encounters).Both prey capture processes functioned simultaneously. The synergisticfunctioning of these processes probably explains the broad patternsof prey ingestion found by in situ studies of Mnemiopsis feeding.     

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     

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.     

A rare predator exploits prey escape behavior: the role of tail-fanning and plumage contrast in foraging of the painted redstart (Myioborus pictus)

Escape response, triggered by an approaching predator, is acommon antipredatory adaptation of arthropods against insectivores.The painted redstart, Myioborus pictus, represents insectivorousbirds that exploit such antipredatory behaviors by flushing,chasing, and preying upon flushed arthropods. In field experimentsI showed that redstarts evoke jump and flight in prey by spreadingwings and tail: this display increased frequency of aerial chasesby redstarts. Artificial models with spread tails also elicitedescape responses more often than models with closed tails and wings.The white patches on black wings and tails additionally help:the frequency of chases decreased when the white patches werecovered with black dye. Black models also tended to elicit escaperesponse less often than black-and-white models did, at leastin some situations. Hence, the prey's ability to detect birdsand to flee could cause the evolution of predators specializedat using conspicuous behavior and contrast in body colorationto elicit and exploit such antipredatory responses. Redstartsconstitute only a small proportion of the predatory guild, andtheir adaptations to exploit the prey's behavior illustratethe theoretically modeled "rare enemy" effect present in multispeciespredator-prey systems. This is the first experimental studyof morphological and behavioral adaptations of a rare predatorthat both elicits and exploits antipredator escape behaviorof its prey against more common predators. Hence, the studydocuments a behavior that could be evolutionarily explainedonly if indirect interactions in predator-prey communities aretaken into account.     

Effect of cannibalism on predation,oviposition and longevity of the predacious mite,Agistemus exsertus Gonzalez (Acari: Stigmaeidae)

Cannibalism (intraspecific predation) on conspecific eggs was investigated in the predatory stigmaeid mite, Agistemus exsertus Gonzalez in the absence of eggs of Tetranychus urticae Koch (no-choice tests) and presence of three densities of prey eggs simultaneously (choice tests) in the laboratory. Data show that cannibalism occurs in immatures and adult females of the predator, which successfully developed and reproduced on conspecific eggs as an alternative prey in the absence of prey eggs. In no-choice tests, cannibalism rate on conspecific eggs by A. exsertus stages was significantly lower than the predation rate on T. urticae eggs. The predatory mite exhibited a marked decline in oviposition rate when preyed on conspecific eggs compared with feeding on prey eggs. The developmental duration and longevity of A. exsertus females were significantly longer 1.9 and 1.7 times, respectively, when fed on conspecific eggs than feeding on T. urticae eggs. The propensity of the predator towards cannibalism depends on the prey density, when T. urticae eggs and conspecific eggs are present simultaneously. Provision of increased densities of prey eggs significantly decreased cannibalism and predation by A. exsertus stages, which fed generally less on conspecific eggs than on T. urticae eggs in choice tests. The oviposition rate of the predator increased significantly, as the egg density of the prey increased. The developmental period and longevity of A. exsertus females showed significantly gradual shortness with increasing egg density of the prey.     

Food supply and prey selection in planktivorous cyprinidae

Summary In small Bavarian lakes, the gut contents of the Cyprinid fish roach (Rutilus rutilus), rudd (Scardinius erythrophtalamus), bream (Abramis brama) and bleak (Alburnus alburnus), and the actural food supply during the fish's feeding period were examined in relation to the species composition of zooplankton. Accompanied by feeding experiments in the laboratory, the selective effect of fish predation could be attributed to the distribution patterns of prey and predator in time and space, to the prey's specific visibility and escape ability and, to some extent, to the fish's active choice. The possibility that the species composition of zooplankton is regulated was indicated only in the fish's positively abundance-dependent preference for the prey types and restricted to only a few plankter species.     

Piscivorous cyprinid fish modulates suction feeding kinematics to capture elusive prey

Previous studies have shown that evasive prey generally elicit a different kinematical pattern of prey capture from suction feeding fish compared to non-evasive types of prey. However, no evidence exists that predatory fish can modulate their prey capture kinematics in response to whether or not an elusive prey performs an escape response. Here, we analyse prey capture kinematics of a specialist piscivore (asp, Aspius aspius) during feeding on untethered, live goldfish, which regularly displayed escape attempts when attacked by the asp. Significant modulation occurred in function of the escape attempts of prey: mouth opening was prolonged and increased in magnitude, and one individual also showed an increased hyoid depression when feeding on prey trying to escape. As the orientation of the prey with respect to the predator prior to the start of mouth opening was related to the probability of observing an escape attempt, asp could theoretically perform this type of modulation by a priori choosing a pre-programmed motor pattern. However, since contact between the prey and the asp's mouth appeared to be a factor improving the timing of mouth closing, this fine-tuning of prey capture kinematics is more likely to be caused by reflexive neural feedback control.     

Dynamics of prey-flock escaping behavior in response to predator's attack

The dynamic behavior of prey-flock in response to predator's attack was investigated by using molecular dynamics (MD) simulations in a two-dimensional (2D) continuum model. By locally applying interactive forces between prey individuals (e.g. attraction, repulsion, and alignment), a coherently moving state in the same direction was obtained among individuals in prey-flock. When a single predator was introduced to the prey population, the prey-flock was correspondingly deformed by the predator's continuous attacks towards the prey-flock's center. In response to the predator's attack, three regimes in the flock size (compression (Regime I), expansion (Regime II), compression (Regime III)) were revealed if the predator's attack speed (kappa) was comparatively low to the escape speed of prey-flock. If noise was added to the predator's attacking course, a higher degree of variation was observed in the patterns of compression and expansion in the prey-flock size. However, the scaling behavior in the changes in prey-flock size was present in different levels of noise with the increase in predation risk (R) when kappa takes an appropriately low value. During the procedure of escaping, order breaking in alignment (phi) of prey population was observed, while the degree of alignment was dependent upon the changes in parameters of kappa and R.     

Diel periodicity and selectivity in the feeding rate of the predatory copepod Mesocyclops edax

The diel periodicity and selectivity in the feeding behaviorof the predatory cyclopoid copepod Mesocyclops edax was investigatedat 3 h intervals over two 24 h sampling periods in nature. Gutcontent analyses revealed an increase in gut fullness at 11.30and 20.30 in July, and at 20.30 in August. The increase in gutfullness at these times could not be explained by an increasein prey density, changes in predator-prey overlap or differencesin prey vulnerability. We suggest that M.edax exhibits a truediel periodicity in the intensity of its predatory activities,although the alternative hypothesis of a diel periodicity ingut passage time cannot be ruled out. Vanderploeg and Scavia'sE^* selectivity index indicated a preference for rotifer andcladoceran prey over copepods.     

Behavioral interactions between a cyclopoid copepod predator and its prey

Behavioral observations on the predatory interactions betweenMesocyclops edax and several different types and sizes of preyrevealed that prey size alone was less important than otherspecific morphological and behavioral characteristics of theprey in deterring successful predation by the copepod. The behavioralresponses of Bosmina and Asplanchna to an attacking copepodwere passive and consisted of a simple retraction of vulnerableswimming appendages which made the prey more difficult to grasp.Daphnia and Diaphanosoma on the other hand exhibited very activeswimming escape responses. Tropocyclops usually avoided M. edaxby fleeing before the larger predator could detect them. Thehard carapaces of Daphnia, Bosmina and Keratella were effectiveat reducing ingestion following capture by M. edax. The resultsof these behavioral observations were supported by enclosureexperiments in which the predator was offered a choice betweentwo prey simultaneously. Cyclopoid copepods are capable of successfullyattacking, capturing and ingesting prey organisms several timestheir own body length. Although size alone may influence thepreference of cyclopoid copepods on large and small individualsof the same or similar prey species, it is not a dependabledeterminant of the preference of cyclopoids on multispecificprey assemblages. ¹Present address: Department of Biology, Williams Hall No. 31,Lehigh University, Bethlehem, PA 18015, USA     

Modelling the attack success of planktonic predators: patterns and mechanisms of prey size selectivity

A mathematical model of the attack success of planktonic predators(fish larvae and carnivorous copepods) is proposed. Based ona geometric representation of attack events, the model considershow the escape reaction characteristics (speed and direction)of copepod prey affect their probability of being captured.By combining the attack success model with previously publishedhydrodynamic models of predator and prey perception, we examinehow predator foraging behaviour and prey perceptive abilityaffect the size spectra of encountered and captured copepodprey. We examine food size spectra of (i) a rheotactic cruisingpredator, (ii) a suspension-feeding hovering copepod and (iii)a larval fish. For rheotactic predators such as carnivorouscopepods, a central assumption of the model is that attack istriggered by prey escape reaction, which in turn depends onthe deformation rate of the fluid created by the predator. Themodel demonstrates that within a species of copepod prey, theability of larger stages to react at a greater distance fromthe predator results in increased strike distance and, hence,lower capture probability. For hovering copepods, the vorticityfield associated with the feeding current also acts in modifyingthe prey escape direction. The model demonstrates that the reorientationof the prey escape path towards the centre of the feeding current'sflow field results in increased attack success of the predator.Finally, the model examines how variability in the kineticsof approach affects the strike distance of larval fish. In caseswhere observational data are available, model predictions closelyfit observations.     

Foraging behavior of the predaceous cladoceran, Leptodora kindti, and escape responses of their prey

Using silhouette video photography we have made the first quantitativeobservations of foraging behavior in Leptodora kindti, a predaceouscladoceran (Haplopoda). Leptodora swims with a mean velocityof 13.4?4.0 mm s^–1 and initiates an attack only upon directcontact with potential prey. The attack sequence is as follows:Leptodora swims randomly through the water column with all fivepairs of thorac appendages spread to form a ‘feeding basket’and, seemingly by chance, encounters prey. Shortly after preymake contact with any part of Leptodora's body (usually ventral),the abdomen is rapidly pulled forward, clamping itself underthe feeding basket so that the telson closes it at the posteriorend. The duration of this movement is always the same and weconclude that it is an indiscriminate reflex. If the prey isencountered anywhere but a short distance directly in frontand slightly below the Leptodora, it is not captured. The speedof copepod escape responses effectively allows them to avoidcontact with the predator. Daphnia's escape response, particularlythat of juveniles, is slower and leaves them far more susceptibleto Leptodora predation.     

The influence of zooplankton defenses on prey selection by young Chaoborus larvae

Prey exhibiting a variety of morphological and behavioral antipredatordefenses were examined for susceptibility to first through thirdinstar Chaoborus americanus larvae. Synchaeta sp. was highlyvulnerable to these predators due to high encounter rates, itsrelatively soft cuticle, and lack of a precontact defense. Keratellatestudo exhibited postcontact defenses and was more susceptibleto predators than were prey of comparable size that exhibitedprecontact escape behaviors (Hexarthra mira and Diaptomus birgeinauplii). Ontogenetic changes were observed in the escape responseof D.birgei and the foraging success of C.americanus larvae.Chaoborus was observed to prey on the protists Bursaria andVolvox. Precontact defenses were more effective than postcontactdefenses in the prey species examined; however, the relativeeffectiveness of prey defenses cannot be generalized by preygenus nor by the defensive tactics employed. Present address: Department of Entomology, University of California,Riverside, CA 92521, USA     

Subtle cues of predation risk: starlings respond to a predator's direction of eye-gaze

For prey animals to negotiate successfully the fundamental trade-off between predation and starvation, a realistic assessment of predation risk is vital. Prey responses to conspicuous indicators of risk (such as looming predators or fleeing conspecifics) are well documented, but there should also be strong selection for the detection of more subtle cues. A predator's head orientation and eye-gaze direction are good candidates for subtle but useful indicators of risk, since many predators orient their head and eyes towards their prey as they attack. We describe the first explicit demonstration of a bird responding to a live predator's eye-gaze direction. We present wild-caught European starlings (Sturnus vulgaris) with human 'predators' whose frontal appearance and gaze direction are manipulated independently, and show that starlings are sensitive to the predator's orientation, the presence of eyes and the direction of eye-gaze. Starlings respond in a functionally significant manner: when the predator's gaze was averted, starlings resumed feeding earlier, at a higher rate and consumed more food overall. By correctly assessing lower risk and returning to feeding activity earlier (as in this study), the animal gains a competitive advantage over conspecifics that do not respond to the subtle predator cue in this way.     

Influence of Age and Size on the Response to Novel Prey by Fry of the Cichlid Fish Cichlasoma managuense (Pisces: Cichlidae)

The response to a novel prey item was investigated during the first month of feeding of the cichlid fish Cichlasoma managuense. The relative contribution of size and age to improvement in predatory behavior was addressed. Group I (control) was fed nauplii of Artemia salina and group II a manufactured flakefood diet. Group II fish were tested for their ability to prey on a novel diet, the nauplii of Artemia salina. Latency to respond to the presence of novel prey decreased and the number of capture attempts increased with increasing experience with the artificial diet and with age. As size increased so did the number of capture attempts, but the latency did not change. Size and experiential and maturational factors may affect parts of the predatory behavior differentially. During the first month of feeding, age may be more important than size for the decrease in latency and the increase in the number of capture attempts. The number of capture attempts during the first 30 s of the observation period and the capture success increased faster than the latency decreased. Latency to respond to novel prey may mature at a slower rate than the number of capture attempts.     

Magnitude of food reward affects escape behavior and acceptable risk in Balearic lizards, Podarcis lilfordi

During encounters with predators, prey must balance the degreeof risk against the loss of fitness-enhancing benefits suchas feeding and social activities. Most studies of tradeoffsbetween risk and cost of escaping have measured flight initiationdistance and time to emerge from refuge, for which theory providesrobustly supported predictions. Tradeoffs involving other aspectsof encounters, including distance fled and time between escapeand return to a food source, have received little theoreticalor empirical attention. By adapting models of flight initiationdistance and time between entry into refuge and emergence, wepredict effects of predation risk and cost on distance fledand time to return to a source of benefit after fleeing. Actingas simulated predators that approached at a fixed speed, weconducted an experimental field study to test the hypothesesthat flight initiation distance, distance fled, and time toreturn to food by Balearic lizards (Podarcis lilfordi) decreasewith the presence and amount of insect food. Predictions ofthe models were strongly supported, including those for distancefled and return time, but predictions for other cost factorsand predation risk factors remain to be tested.     

Predation by a carnivorous marine copepod, Euchaeta elongata Esterly, on eggs and larvae of the Pacific hake, Merluccius productus

The predatory behavior of the carnivorous marine copepod, adultfemale Euchaeta elongata Esterly, feeding on eggs and larvaeof the Pacific hake, Merluccius productus, was examined in thelaboratory and in a natural setting. E. elongata did not feedon eggs. Predation on larvae is believed to depend on larvalswimming behavior: (1) predation rates were low on early stageyolk-sac larvae which are inactive swimmers and are relativelyundetected by the predator; (2) rates were high on middle stageyolk-sac larvae which are more active swimmers yet have a poorlydeveloped escape response; and (3) rates were low on largerlarvae which are able to escape the predator effectively. Starvedhake larvae were more vulnerable to predation due to a poorescape ability although they were less active and not easilydetected. The presence of naturally occurring alternative prey,Pseudocalanus sp., depressed the rate of E. elongata predationon hake larvae. In an analysis of field data, hake larvae andE. elongata were found to occupy the same depths in Dabob Bay.A high percentage of E. elongata collected had apparently beenfeeding on hake larvae, as indicated by the presence of pigmentsin their guts. Survival of hake larvae in late spring appearsto be relatively poor compared with early spring; poorer survivalin late spring may be due partly to an increase in the abundanceof invertebrate predators, such as E. elongata. ^*Current address: Northwest and Alaska Fisheries Center, 2725Montlake Blvd, Seattle, WA 98112, USA.     

Plesiomorphic Escape Decisions in Cryptic Horned Lizards (Phrynosoma) Having Highly Derived Antipredatory Defenses

Escape theory predicts that the probability of fleeing and flight initiation distance (predator–prey distance when escape begins) increase as predation risk increases and decrease as escape cost increases. These factors may apply even to highly cryptic species that sometimes must flee. Horned lizards (Phrynosoma) rely on crypsis because of coloration, flattened body form, and lateral fringe scales that reduce detectability. At close range they sometimes squirt blood‐containing noxious substances and defend themselves with cranial spines. These antipredatory traits are highly derived, but little is known about the escape behavior of horned lizards. Of particular interest is whether their escape decisions bear the same relationships to predation risk and opportunity costs of escaping as in typical prey lacking such derived defenses. We investigated the effects of repeated attack and direction of predator turning on P. cornutum and of opportunity cost of fleeing during a social encounter in P. modestum. Flight initiation distance was greater for the second of two successive approaches and probability of fleeing decreased as distance between the turning predator and prey increased, but was greater when the predator turned toward than away from a lizard. Flight initiation distance was shorter during social encounters than when lizards were solitary. For all variables studied, risk assessment by horned lizards conforms to the predictions of escape theory and is similar to that in other prey despite their specialized defenses. Our findings show that these specialized, derived defenses coexist with a taxonomically widespread, plesiomorphic method of making escape decisions. They suggest that escape theory based on costs and benefits, as intended, applies very generally, even to highly cryptic prey that have specialized defense mechanisms.