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Plasticity and Cognition in Spiders

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Abstract

Spiders can be a particularly important model for the study of cognition. Their close interaction with niche-constructed environmental features, such as webs, cocoons, draglines or retreats, allows for the experimental manipulation of these silken structures, and thus for a controlled study of the cognitive machinery that underlie the use and construction of these structures. There are contrasting theories about cognition, and we explore particularly the opposition between the traditional approach, the one that requires information to be processed solely within the central nervous system (CNS), and the extended cognition approach, which is less restrictive. Here we review the literature on spider cognition with an eye to the experimental data that allows the contrast between these theories of cognition, and conclude that spiders evolved to process information prior to reaching the nervous system: they use their webs to decide whether to attack or not a prey item, and we can experimentally alter their decision by manipulating web properties, such as radii tension. The experimental manipulation of web threads also alters the attentional state of the web building spider so that she predictably ignores important cues for decisions taken during the building process. Together, the experimental evidence shows that spiders extend their cognitive machinery outside the bounds of their CNS, making use of the external silken structures to offload cognitive processing. This insight may help to explain graded changes in brain/body allometry, because smaller animals could rely more on extended cognition so as not to be behaviourally limited by a relatively small brain. Extended cognition could also help explain the emergence of new levels of organisation, particularly the transition from solitary to social life. In general, extended cognition emerges as a natural bridge between two traditionally separate research agendas: the area of cognitive development (learning mechanisms) and that of evolution through natural selection.

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Notes

  1. 1.

    Information has at least three broad meanings: the statistical, the semantic, and the physical (Harms 2006). We use the semantic sense to characterize “knowledge of” or “meaning” in both the referential properties of symbols and instructional aspects of knowledge in natural biological systems.

  2. 2.

    The actual meaning of a piece of information depends not only on the referent (the external object), but also on the internal state of the system. In the first case, meaning involves a denotative relation between a sign and its counterpart in the external world (the referent). In the second case, meaning involves a connotative relation between the sign and the internal elements of the system, a relationship that ensures an interpretation, that leads to a procedure or a path of action within the system (Harms 2004, 2006). This second, interpretive side of information requires a characterization of the connectivity between the internal elements of the system, and is thus by definition a relational conception of information. This idea of a system of mutual relations is also relevant to naturalize important properties of any cognitive system, such as agency and normativity (Moreno and Mossio 2015).

  3. 3.

    The radial threads modulate the resonance and the attenuation of prey vibrations, as well as the velocity of their propagation, and thereby promote signal transformation through the web (Landolfa and Barth 1996). Tense threads increase the amplitude of some, and reduce the amplitude of other prey vibration frequencies (Mortimer et al. 2015).

  4. 4.

    Although it is notoriously difficult to detect novelty in a lifelong, complete repertoire of actions (because some performances could be simply rare in place of nonexistent), sometimes novelty is the only possibility, for example when the behaviour is impossible without a particular experimental manipulation. This is the case of the reeling attack tactic, whereby the spider reels a dry thread so that an entangled prey comes close enough to be wrapped. Reeling attack is the default foraging strategy for a whole family of cobweavers, but orbweavers cannot possibly attack through reeling under natural conditions, because their orbweb’s radii are firmly attached to the frame (and thus cannot be reeled). Surprisingly, orbweavers on experimental orbwebs (with a radii artificially cut free from the frame) do promptly reel-attack their prey in the very first trial; this new behaviour is stable, occurring predictably in the experimental orbwebs, and in all the species studied (Penna-Gonçalves et al. 2008). Since orbweavers never attack naturally through reeling, and considering this behaviour is impossible in normal orbwebs, this experimental result requires explanation, because these spiders cannot possibly have an adapted neural network for controlling a reeling attack. The explanation is rather simple: orbweavers do reel threads in natural circumstances, but only when building their webs, and never in a foraging context (prey attack). Thus, the cut-free radius of the experimentally modified orbweb provides the opportunity for the spider to perform a known behavior within a novel, prey-attack context. This is precisely the case of self-organization discussed above. A novelty (predatory reeling in orbweavers) emerges and stabilizes through an environmental (cut-free radius) modification that allows a feedback between two existing neural networks. The cut-free radius allows the co-occurrence of a (natural) web-building behaviour (reeling) with an attack behaviour (prey-wrapping), with the consequent emergence of a new foraging tactic: the reel-attack. This exemplifies how self-organization can produce new and stable behaviors; in this case, the evolutionary appearance of the reel-attack requires only the evolution of a specific environmental feature (a detachable radius), and this is precisely what occurred in the transition from ancestral orbwebs to derived cobwebs.

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Correspondence to Hilton F. Japyassú .

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Japyassú, H.F. (2017). Plasticity and Cognition in Spiders. In: Viera, C., Gonzaga, M. (eds) Behaviour and Ecology of Spiders. Springer, Cham. https://doi.org/10.1007/978-3-319-65717-2_14

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