The predator and prey behaviors of crabs: from ecology to neural adaptations

Abstract

Predator avoidance and prey capture are among the most vital of animal behaviors. They require fast reactions controlled by comparatively straightforward neural circuits often containing giant neurons, which facilitates their study with electrophysiological techniques. Naturally occurring avoidance behaviors, in particular, can be easily and reliably evoked in the laboratory, enabling their neurophysiological investigation. Studies in the laboratory alone, however, can lead to a biased interpretation of an animal's behavior in its natural environment. In this Review, we describe current knowledge - acquired through both laboratory and field studies - on the visually guided escape behavior of the crab Analyses of the behavioral responses to visual stimuli in the laboratory have revealed the main characteristics of the crab's performance, such as the continuous regulation of the speed and direction of the escape run, or the enduring changes in the strength of escape induced by learning and memory. This work, in combination with neuroanatomical and electrophysiological studies, has allowed the identification of various giant neurons, the activity of which reflects most essential aspects of the crabs' avoidance performance. In addition, behavioral analyses performed in the natural environment reveal a more complex picture: crabs make use of much more information than is usually available in laboratory studies. Moreover, field studies have led to the discovery of a robust visually guided chasing behavior in Here, we describe similarities and differences in the results obtained between the field and the laboratory, discuss the sources of any differences and highlight the importance of combining the two approaches.

Multielectrode Recordings From Identified Neurons Involved in Visually Elicited Escape Behavior

“…Contrasting with the three previous classes, which responses to looming stimuli consist of a firing rate increase that follows the dynamic of image expansion, the BLG2 neuron strongly responds at the very beginning of looming stimulation and inactivates with further image expansions. The time course of the BLG2 activity to looming stimuli approximately coincides with transient freezing observed in the animal before initiating the escape (Oliva, personal communication), suggesting a role of this neuron in that behavioral component (Tomsic et al, 2017 ).…”

“…The crab Neohelice is a well established invertebrate model for investigating the neurobiology of visually guided behaviors, including learning and memory processes. Over the last two decades a great deal of knowledge about different lobula giant neurons that play central roles in the crab’s escape behavior from visual threats has been acquired (Tomsic et al, 2017 ). The characterization of these LG neurons has been made by in vivo intracellular recording and staining.…”

“…This study represents our first approach to using multielectrode recording in the crab. For this reason, we included in our experiments stimuli that proved to be effective both for identifying different lobula neurons (Medan et al, 2015 ; Tomsic et al, 2017 ; Scarano et al, 2018 , 2020 ) and for eliciting a variety of behavioral responses in this animal, such as escape response (Oliva and Tomsic, 2012 ; Scarano and Tomsic, 2014 ), predatory response (Gancedo et al, 2020 ) and optomotor response (Barnatan et al, 2019 ). Computer-generated visual stimuli were projected on a computer screen (Samsung S20C300L) placed at a distance of 20 cm, covering the frontolateral right side of the animal.…”

“…It is a highly visual semiterrestrial crab that inhabits densely populated mudflat environments. In nature, the crab is regularly engaged in social interactions that include burrow defense, courtship, chasing after smaller individuals and being chased by larger ones (Fathala and Maldonado, 2011 ; Sal Moyano et al, 2016 ; Tomsic et al, 2017 ; Gancedo et al, 2020 ), all activities that are guided by sight. The crab also uses vision to detect and avoid aerial predators (Magani et al, 2016 ).…”

“…Neurobiological studies on Neohelice mainly focused on the crab’s escape response to visual threats and encompassed different aspects such as visuomotor transformation, response modulation, and learning and memory. The studies were performed with a variety of methodologies that include behavioral analyses, neuroanatomy, pharmacology, molecular biology, electrophysiology, and calcium imaging (for reviews see Tomsic and Romano, 2013 ; Tomsic, 2016 ; Tomsic et al, 2017 ). An important step in the establishment of the crab as an invertebrate model for studying the neural control of behavior has been the identification and characterization of a group of giant neurons from the lobula (3rd optic neuropil of arthropods), which were shown to be key elements for visually-elicited avoidance behaviors.…”