Acclimation and captivity can be critical in obtaining scientifically valid results, yet preventing and mitigating the effects of stress in an experimental scenario can be costly, and difficult to prevent. This may contribute to the tendency for researchers to focus on a handful of studied species where baseline behaviour is already established. Such a focus on a limited range of representatives from any taxon can, however lead to misinformation about that taxon when focal species possess traits that are species-specific and not shared among the wider
group. This study begins to establish baseline observations about the behavioural patterns of a
native New Zealand octopus, P. cordiformis, in efforts to expand current knowledge on
cephalopod behaviour, which is classically dominated by only a few well-studied species (e.g. Octopus vulgaris, O. cyanea and O. bimaculoides; Yarnall, 1969; Fiorito, et al., 1990; Mather & O’Dor, 1991; Fiorito & Scotto, 1992; Forsythe & Hanlon, 1997; Boal et al., 2000; Sinn, et al. 2001; Hochner et al., 2003; Mather & Mather, 2004; Brown et al., 2006; Hvorecny et al., 2007; Anderson, et al., 2008; Gutnick et al., 2011). The robust responses of P. cordiformis to acclimation and captivity in this study highlight the species’ viability for laboratory-based investigation, and offer opportunities for researchers to examine octopus behaviour outside the realm of better-studied species. Results from these experiments highlight several departures from the conclusions of previous work on other octopus species (e.g. Brown et al., 2006), which reinforces the need for taxonomical diversity in behavioural studies.
The results from sleep deprivation trials conducted on P. cordiformis in this study support the presence of NREM-like rest states in octopuses, as shown by Brown et al. (2006). However, these results also suggest that P. cordiformis does not fulfil all of the established criteria for “true sleep” (McNamara et al., 2009). This is unsurprising, and echoes the tremendous diversity of sleep patterns observed in vertebrates, which vary according to ecotype (Capellini et al., 2008; 2009) and life stage (McNamara et al., 2009). The literature examining sleep in invertebrate species is sparse compared with that on vertebrates (McNamara et al., 2009). Yet the high level of octopus intelligence (Mather, 2008), and neural parallels to vertebrates that are being discovered in cephalopods (Bullock & Başar, 1984; Hochner et al., 2003; Brown et al., 2006), suggest that cephalopod brains are subject to evolutionarily parallel differentiation of neural substrates to facilitate function. Rattenborg et al. (2009) suggested that “the convergent evolution of homeostatically regulated SWS (slow wave sleep) in mammals and birds was directly linked to the convergent evolution of large, heavily interconnected brains capable of performing complex cognitive processes in each group”. REM sleep in many young and developing mammals is expressed at much higher levels than in adults, supporting the suggestions by some researchers that sleep state is important in brain development (Siegel, 2005). If there are strong parallels in the evolution of the brains of cephalopods and higher vertebrates, examining the expression of low-voltage REM vs. high-amplitude slow wave NREM activity in octopuses across age gradients would be a viable method of testing the convergence of octopus brain and sleep structure on those of higher vertebrates. Forging together current video playback and animation technology with recent neurological advances
will enable researchers to examine the brains of the most intelligent invertebrates in a comparative context, in turn helping to elucidate the process by which intelligence evolves in all animals.
Although behavioural studies are very valuable, the examination of P. cordiformis
acclimation, sleep deprivation and video playback responses would all benefit from a focused examination of physiological aspects, using more robust indicators of stress and neural activity. This, however, would require a much more extensive and potentially invasive sampling effort, which is not currently achievable. Instantaneous blood sampling and cannulation are unsuitable due to restrictions on mobility imposed by cannulae and the tendency for octopus stress hormone levels to spike during handling (Malham et al., 2002). In the event that acclimation, for instance, has not occurred within the three-day timeframe that was set in this study, future studies should use a longer acclimation period to examine long-
term effects, integrating blood-chemistry assessment as technology permits. The need for
further metrics by which sleep deprivation effects are tested could also be addressed by examining the influence of sleep deprivation on parameters such as heart-rate, ventilation, blood-hormone levels (Siegel, 2008), as well as the use of EEG (Brown et al., 2006) to provide a clearer indication of the potential influence (or lack) of sleep deprivation in P. cordiformis.
Finally, the lack of realistic motion, pressure, acoustic and olfactory cues in the current studies is a clear drawback, and a consideration for future efforts. In this study, the movement of digital seals was linear, while the motion of the predator in the archival ‘real seal’ clip changed velocity and direction abruptly. Realistic motion requires the capture of biologically relevant movement patterns (Woo & Riecau, 2008). Furthermore, an examination of additional sensory modalities would allow researchers to establish a hierarchy of sensory inputs, and also to test the ways in which these sensory modalities interact. It is apparent that video playback can elicit responses from octopuses, and consequently refining these techniques will provide researchers with a means to test octopuses in a broad range of hypotheses in different areas, including mate selection (e.g. Clark & Uetz, 1993; Rosenthal et al., 1996; Witte & Klink, 2005), intraspecific aggression (Rowland et al., 1995; McKinnon & McPhail, 1996), communication (Hanlon & Messenger, 1996; Messenger, 2001) and learning (Boal et al., 2000; Mather, 2008b). Marrying video playback to neural imaging techniques (e.g. Brown et al., 2006) enables experimenters to manipulate stimulus parameters with high
specificity and simultaneously to effectively map response activity to specific regions of the brain, revealing the differences and parallels in the structure and function of cephalopod brains with those of vertebrates.