Predation risk triggers copepod small-scale behavior in the Baltic Sea

Predators not only have direct impact on biomass but also indirect, non-consumptive effects on the behavior their prey organisms. A characteristic response of zooplankton in aquatic ecosystems is predator avoidance by diel vertical migration (DVM), a behavior which is well studied on the population level. A wide range of behavioral diversity and plasticity has been observed both between- as well as within-species and, hence, investigating predator–prey interactions at the individual level seems therefore essential for a better understanding of zooplankton dynamics. Here we applied an underwater imaging instrument, the video plankton recorder (VPR), which allows the non-invasive investigation of individual, diel adaptive behavior of zooplankton in response to predators in the natural oceanic environment, providing a finely resolved and continuous documentation of the organisms’ vertical distribution. Combing observations of copepod individuals observed with the VPR and hydroacoustic estimates of predatory fish biomass, we here show (i) a small-scale DVM of ovigerous Pseudocalanus acuspes females in response to its main predators, (ii) in-situ observations of a direct short-term reaction of the prey to the arrival of the predator and (iii) in-situ evidence of pronounced individual variation in this adaptive behavior with potentially strong effects on individual performance and ecosystem functioning

The chemical ecology of copepods

An increasing number of studies show the importance of chemical interactions in the aquatic environment. Our understanding of the role of chemical cues and signals in larger crustaceans has advanced in the last decades. However, for cope-pods, the most abundant metazoan zooplankton and essential for the functioning of the marine food web, much is still unknown. We synthesize current knowledge about chemical ecology of copepods including foraging, survival and reproduction. We also compile information on the sensory apparatus and new analytical approaches that may facilitate the identification of signal molecules. The review illustrates the importance of chemical interactions in many aspects of copepod ecology and identi-fies gaps in our knowledge, such as the lack of identified infochemicals and electro-physiological studies to confirm the function of sensory structures. We suggest approaches that are likely to further our understanding of the role of chemical inter-actions in the pelagic ecosystem

Swimming behaviour and prey perception in the calanoid copepod Clausocalanus furcatus.

Small planktonic copepods (The aim of this PhD thesis was to investigate some aspects of the swimming behaviour of C. furcatus adult female that could shed light on its small-scale interactions with the surrounding environment. In particular, the work was focused on the mechanisms regulating the perception and capture of prey items, in order to understand the success of this species in oligotrophic regions. To this purpose, four different approaches have been utilised: - the numerical characterization of the trajectories performed by freely swimming C. furcatus adult females in presence of dinoflagellate cells and in association with capture events; - the reconstruction of the perception area and of the mechanisms involved in the capture of prey items; - the morphological investigation of the sensory structures present on the first antennae, which bear mechano- and chemo-sensors involved in the perception of external cues; - the evaluation of the sensory performance of the mechanoreceptors on the first antennae by means of electrophysiological experiments. The results of these investigations concur in depicting a coherent scenario. In C. furcatus, the modalities of detecting and capturing prey seem to be forged to efficiently exploit food particles when they are grouped in small patches, and are aimed at maximising the success of C. furcatus in oligotrophic environments

Non-lethal effects of the predator Meganyctiphanes norvegica and influence of seasonal photoperiod and food availability on the diel feeding behaviour of the copepod Centropages typicus

Predators can induce changes in the diel activity patterns of marine copepods. Besides vertical migration, diel feeding rhythms have been suggested as an antipredator phenotypic response. We conducted experiments to assess the non-lethal direct effects of the predator Meganyctiphanes norvegica (northern krill) on the diel feeding patterns of the calanoid copepod Centropages typicus. We also analysed the influence of seasonal photoperiod and prey availability on the intensity of copepod feeding rhythms. We did not detect any large effect of krill presence on the diel feeding behaviour of copepods, either in day-night differences or total daily ingestions. Seasonal photoperiod and prey availability, however, significantly affected the magnitude of copepod feeding cycles, with larger diel differences in shorter days and at lower prey concentrations. Therefore, the role of non-lethal direct effects of predators on the diel feeding activity of marine copepods remain debatable and might not be as relevant as in freshwater zooplankton

Adaptive feeding behavior and functional responses in pelagic copepods

Corrigendum Adaptive feeding behavior and functional responses in zooplankton https://doi.org/10.1002/lno.1080414 pages, 5 figures, 2 tables, supporting information https://doi.org/10.1002/lno.10632Zooplankton may modify their feeding behavior in response to prey availability and presence of predators with implications to populations of both predators and prey. Optimal foraging theory predicts that such responses result in a type II functional response for passive foragers and a type III response for active foragers, with the latter response having a stabilizing effect on prey populations. Here, we test the theoretical predictions and the underlying mechanisms in pelagic copepods that are actively feeding (feeding‐current feeders), passively feeding (ambushers), or that can switch between the two feeding modes. In all cases, individual behaviors are consistent with the resulting functional response. Passive ambushing copepods have invariant foraging behavior and a type II functional response, as predicted. When foraging actively, the species with switching capability change its functional response from type II to III and modify its foraging effort in response to prey density and predation risk, also as predicted by theory. The obligate active feeders, however, follow a type II response inconsistent with the theoretical prediction. A survey of the literature similarly finds consistent type II response in ambush feeding copepods, but variable (II or III) responses in active feeders. We examine reasons for why observed behaviors at times deviate from predictions, and discuss the population dynamics and food web implications of the two types of functional responses and their underlying mechanismsThe Centre for Ocean Life is supported by the Villum Foundation. ES was funded by grant CGL2014-59227-R (MINECO/FEDER, UE), and P.T. by a sabbatical grant from University of GothenburgPeer Reviewe

Phenotypic responses of zooplankton to variable conditions

Organisms are continually challenged by multiple threats in the environment, and such threats are seldom constant in either time or space. Therefore, organisms must maintain physiological, behavioural, morphological and life- history adaptations across environments to prevent reductions in fitness. Freshwater ecosystems are particularly variable environments, and so organisms inhabiting lakes and ponds exhibit a range of different adaptations in order to survive and propagate. Despite this, the energetic constraints and potentially divergent responses required towards multiple threats creates the necessity to make trade-offs in their phenotypic repertoire. The outcomes of such phenotypic compromises are often difficult to predict and requires both a mechanistic understanding of the threats and responses involved, as well as insights into the resulting fitness consequences. Although this is relatively well understood with regards to some threats like predation for example, other biotic and abiotic stressors are less well studied. In this thesis I identify phenotypic compromises in behavioural, morphological and life-history traits of zooplankton with regards to variable environments.Behaviour is often considered one of the most labile traits and consequently it may provide a quick and inexpensive response to infrequent or rapidly changing contexts. Using 3D tracking, I focused on swimming behaviour of Daphnia magna in response to social context and found that females avoid males in a way that resembles a predation event. In a separate experiment I investigated how the presence of a high-density food patch altered the response to the abiotic threat ultraviolet radiation (UVR). Here I found that despite the potential fitness consequences of UVR the foraging opportunity reduced the avoidance response that has been classically described in Daphnia.UVR is a substantial threat in aquatic systems with documented physiological, behavioural, morphological and life- history responses. It is also a particularly variable stressor as it is absent during night and varies in intensity over the seasons. Despite its variable nature, studies have typically only addressed the presence or absence and not fluctuating UVR stress. I addressed this gap in the knowledge by tracking the survival, reproduction and behavioural response to both fluctuating and stable exposure of UVR. Simply by varying the scheduling but not the quantity of UVR stress, I identified fitness costs that appeared to be linked to the cost of the behavioural avoidance.In high-latitude environments, where phenotypic plasticity is promoted due to seasonal variability, copepods increase pigmentation in response to increased UVR but only in the absence of fish. I tested whether this response is ubiquitous at lower latitudes that experience less seasonality and have evolved with different predation regimes. Copepods from fishless environments had higher pigmentation than those with visually hunting predators. I also found that plasticity towards UVR removal was minor, but plasticity towards predation was mostly idiosyncratic. This suggests that plasticity does exist for the threats that are most variable and constitutive responses may have evolved towards ever present danger

Anti-Predator Responses of Squid Throughout Ontogeny

Multiple sensory modalities and a complex array of escape behaviors have evolved as components of anti-predator responses in squids. The goals of this study include: (1) examine the role of the lateral line analogue and vision in successful predator evasion; (2) measure kinematics of escape jetting; (3) document how chromatic patterning, posturing and inking in squid change in response to predators; and (4) investigate escape jet hydrodynamics of squid. Given that squids undergo considerable morphological, ecological, and behavioral changes throughout ontogeny, the goals above were all investigated across different life history stages. To test the respective roles of vision and the lateral line analogue, squid of different life stages were recorded in the presence of natural predators under light and dark conditions with their lateral line analogue intact and ablated via a pharmacological technique. Anti-predator behaviors of squid throughout ontogeny were studied in a series of predator-prey trials using high-speed videography. Additionally, the hydrodynamics and kinematics of high velocity escape jets in squid were examined using a combination of 2D/3D velocimetry. The lateral line analogue played a role in initiation of an escape response at the earliest life stages, and continued to contribute to successful evasion by aiding visual cues in juvenile/adult squid. Paralarvae relied heavily on stereotyped swimming behaviors and translucent coloration to avoid capture, while juvenile and adults used multiple cues associated with the predator’s approach to determine whether posturing or inking and escape jetting is the most suitable anti-predator behavior. Throughout ontogeny, squid produced two escape jet patterns: (1) escape jet I characterized by short rapid pulses resulting in vortex ring formation and (2) and escape jet II characterized by long high volume jets, often with a leading edge vortex ring. Paralarvae exhibited significantly higher propulsive efficiency (94.55%) than adult squid (87.71%) during jet ejection. These results indicate that all life stages of squid are well adapted for predator avoidance; they employ multiple sensory modalities for predator detection, use a variety of anti-predator behavioral responses, and utilize a highly efficient and flexible escape jet to maximize escape from predation

Transitions in morphologies, fluid regimes, and feeding mechanisms during development of the medusa Lychnorhiza lucerna

Author Posting. © The Author(s), 2016. This is the author's version of the work. It is posted here by permission of Inter-Research for personal use, not for redistribution. The definitive version was published in Marine Ecology Progress Series 557 (2016): 145-159, doi:10.3354/meps11855.The early ontogeny of scyphomedusae involves morphological and functional transitions in body plans that affect the predators’ propulsive and feeding strategies. We applied high-speed videography, digital particle image velocimetry (DPIV) and dye visualization techniques to evaluate alterations in swimming and feeding mechanisms during ontogeny of the rhizostome medusa Lychnorhiza lucerna Haeckel, 1880 (Scyphozoa, Rhizostomeae). During early ontogeny, the ephyral mouth lips develop into complex filtering structures along the oral arms. The viscous environments (Reynolds number <100) experienced by ephyrae constrain the feeding mechanisms that transport fluid during ephyral bell pulsations. In contrast, adult medusan fluid flows are dominated by inertial forces and bell pulsations effectively transport fluids and entrained prey toward the oral arms. The oral arm surfaces are covered by motile epidermal cilia that drive these entrained flows through filtering gaps in the oral arms where food particles are retained. In addition to this process within the oral arms, vortices generated during bell pulsation flow downstream along the outside of the medusae and continuously transport prey toward the exterior oral arm surfaces. Although calanoid copepods are capable of escape velocities that greatly exceed L. lucerna’s feeding current speeds, copepods often fail to detect the predator’s feeding currents or inadvertently jump into medusan capture surfaces during failed escape attempts. Consequently, the comparatively weak predator feeding currents successfully capture a portion of the copepods encountered by swimming medusae. These results clarify the processes that enable rhizostome medusae to play key roles as consumers in tropical and subtropical coastal environments.The study was partially funded by grants 2011/00436-8, 2013/19478-8, and 2014/00824-6 São Paulo Research Foundation (FAPESP), and CAPES PROEX2017-09-2

The function of mechanosensory systems in the startle behavior of planktonic larvae

The sensation of mechanical stimuli is a central function of all animal nervous systems. Mechanosensory systems are in charge of this function, using for that a set of specialized molecules and cells that transmit the signal to downstream circuits that initiate and guide a wide variety of behaviors, ranging from navigation, to social interactions. Despite the intensive study of mechanosensory systems in the main genetics models, a clear unified picture of these sensory systems is still lacking. Exploring mechanosensory systems in animals spread across the phylogeny may help reveal such common principles. To contribute towards this aim, the mechanosensory systems of the planktonic larva of the marine annelid Platynereis dumerilii are analysed in this work using genetics, circuit and behavioral approaches. At the behavioral level, a startle response elicited by mechanical stimuli is described in Platynereis larvae using high-speed recordings. This startle response is a fast and well-coordinated behavior involving the control of both the muscular and ciliary locomotor systems of the larva. The startle response is shown to be modulated according to the intensity and site of stimulation. Such responses have been observed in other planktonic organisms, but the mechanosensory cells responsible for initiating the response are not known. A group of penetrating uniciliated neurons in the Platynereis larva are shown by calcium imaging to respond to the mechanical stimuli eliciting the startle response. Their morphology is quite similar to putative mechanosensory cells found in other animals, thus suggesting a deep evolutionary conservation. It is not entirely understood what molecular and cellular mechanisms are required for transforming mechanical cues to cellular signals. Here it is shown that Platynereis has homologs to the main molecules that have been implicated in mechanotransduction. The ciliated hydrodynamic receptors identified in this study express PKD1-1 and PKD2-1, two members of the polycystin family that have been implicated in mechanotransduction in other animals. The CRISPR system is used to generate frame-shift mutations in these genes. The mutants no longer display the startle response upon mechanical stimulation, thus suggesting that PKD2-1 and PKD1-1 are essential for the transmission of the mechanical information to downstream circuitries. Startle behaviors generally have a role in avoiding, escaping or deterring predators. It is however not clear what specific adaptations are most useful to increase survival. Here, I used the mutants defective in the startle response to assess the survival value of this behavior. Competition experiments using a rheotactic planktonic predator showed that the mutants are predated more than their wildtype counterparts. These results show that seemingly simple behavioral adaptions can have a high adaptive value. Due to their relatively simplicity, startle responses such as the one described for Platynereis have been dissected at the circuit level. Here, the startle circuit of Platynereis larvae is reconstructed at the synapse level using serial transmission electron microscopy. The resulting circuit shows direct and indirect pathways that explain how ciliary bands and muscles are controlled in a coordinated and synchronous manner. A novel group of interneurons and motoneurons is described that provides candidates for further functional exploration of this circuit.Die Wahrnehmung mechanischer Reize ist eine zentrale Funktion der Nervensysteme aller Tiere. Mechanosensorische Systeme nutzen ein Set von speziellen Molekülen und Zellen, die das Signal des mechanischen Reizes an das postsynaptische neuronale Netzwerk weiterleiten und eine Vielzahl von Verhalten, von Navigation bis zu sozialer Interaktion, induzieren und beeinflussen. Trotz intensiver Forschung der mechanosensorischen Systeme in den wichtigsten genetischen Modelorganismen fehlt ein klares, einheitliches Bild. Dies kann durch die Untersuchung der mechanosensorischen Systeme in Tieren aus weiteren phylogenetischen Gruppen erweitert werden und hilft somit allgemeine Prinzipien hervorzuheben. Um sich diesem Ziel zu nähern, werden in dieser Arbeit die mechanosensorischen Systeme der planktischen Larve des marinen Ringelwurms Platynereis dumerilii, auf der Ebene von Genetik, neuronalen Schaltreisen und Verhalten, analysiert. Auf Verhaltensebene wird eine Schreckreaktion durch mechanische Reize in der Platynereis Larve ausgelöst und mit Hilfe von Hochgeschwindigkeitsaufnahmen beschrieben. Diese Schreckreaktion ist ein schnelles und gut koordiniertes Verhalten, welches die Kontrolle von Muskeln und Zilien in der Larve involviert und durch die Reizintensität und dem Ort der Reizapplikation verändert werden kann. Andere planktische Organismen zeigen ähnliche Reaktion, aber die mechanosensorischen Zellen, die dieses Verhalten verursachen, sind nicht bekannt. In Platynereis Larven konnte eine Gruppe von Nervenzellen mit je einer, die Kutikula durchdringenden, Zilie identifiziert werden. Durch Kalziumindikatoren konnte gezeigt werden, dass diese Neurone auf mechanische Reize reagieren, welche die Schreckreaktion auslösen. Ihre Morphologie ist den, in anderen Tieren gefundenen, mutmaßlichen mechanosensorischen Zellen sehr ähnlich, welches eine evolutionäre Konservierung annehmen lässt. Es ist nicht vollständig verstanden, welche molekularen und zellulären Mechanismen für die Umwandlung mechanischer Reize in zellulare Signale verantwortlich sind. Hier wird gezeigt, dass Platynereis Moleküle besitzt, welche homolog zu den Molekülen sind, denen eine Beteiligung an der Weiterleitung des mechanosensorischen Reizes nachgesagt wird. Die bewimperten hydrodynamischen Rezeptoren, die in dieser Studie identifiziert worden, exprimieren PKD1-1 und PKD2-1, zwei Mitglieder der Polycystin Familie, welche in anderen Tieren mutmaßlich an der mechanosensorischen Weiterleitung beteiligt sind. Larven mit einer Rastermutation auf diesen Genen, welche mittels dem CRISPR System erzeugt wurde, zeigen keine Schreckreaktion nach mechanischer Stimulation. Das lässt vermuten, dass PKD2-1 und PKD1-1 für die Weiterleitung der mechanischen Reizinformation an das postsynaptische neuronale Netzwerk essentiell sind. Schreckreaktionsverhalten spielt im allgemeinen eine Rolle in der Vermeidung, Flucht oder Abschreckung von Räubern. Jedoch ist nicht eindeutig geklärt welche spezifischen Adaptionen besonders nützlich für das Überleben sind. In der vorliegenden Studie werden die mutierten Larven ohne Schreckreaktion genutzt, um die Bedeutung des Verhaltens für das Überleben zu bewerten. Die Experimente mit einem rheotaktischen Räuber zeigen, dass mehr mutierte Larven als Wildtyp-Larven gefressen werden. Diese Ergebnisse zeigen, dass scheinbar einfache Verhaltensanpassungen einen großen Effekt haben können. Hier wird die Schreckreaktion in Platynereis Larven auf dem Level von neuronalen Schaltkreisen mit synaptischer Auflösung durch Serien-Transmission-Elektronen-Mikroskopie untersucht. Der daraus resultierende neuronale Schaltkreis zeigt direkte und indirekte Wege, die erklären wie Zilienbänder und Muskeln koordiniert und synchron kontrolliert werden. Außerdem wird eine neue Gruppe von Interneuronen und Motorneuronen beschrieben und liefert Kandidaten für weitere funktionale Erkundigungen des neuronalen Schaltkreises