Approaches to resolving cephalopod movement and migration patterns

Cephalopod movement occurs during all phases of the life history, with the abundance and location of cephalopod populations strongly influenced by the prevalence and scale of their movements. Environmental parameters, such as sea temperature and oceanographic processes, have a large influence on movement at the various life cycle stages, particularly those of oceanic squid. Tag recapture studies are the most common way of directly examining cephalopod movement, particularly in species which are heavily fished. Electronic tags, however, are being more commonly used to track cephalopods, providing detailed small- and large-scale movement information. Chemical tagging of paralarvae through maternal transfer may prove to be a viable technique for tracking this little understood cephalopod life stage, as large numbers of individuals could be tagged at once. Numerous indirect methods can also be used to examine cephalopod movement, such as chemical analyses of the elemental and/or isotopic signatures of cephalopod hard parts, with growing interest in utilising these techniques for elucidating migration pathways, as is commonly done for fish. Geographic differences in parasite fauna have also been used to indirectly provide movement information, however, explicit movement studies require detailed information on parasite-host specificity and parasite geographic distribution, which is yet to be determined for cephalopods. Molecular genetics offers a powerful approach to estimating realised effective migration rates among populations, and continuing developments in markers and analytical techniques hold the promise of more detailed identification of migrants. To date genetic studies indicate that migration in squids is extensive but can be blocked by major oceanographic features, and in cuttlefish and octopus migration is more locally restricted than predictions from life history parameters would suggest. Satellite data showing the location of fishing lights have been increasingly used to examine the movement of squid fishing vessels, as a proxy for monitoring the movement of the squid populations themselves, allowing for the remote monitoring of oceanic species.     

How intelligent is a cephalopod? Lessons from comparative cognition

The soft-bodied cephalopods including octopus, cuttlefish, and squid are broadly considered to be the most cognitively advanced group of invertebrates. Previous research has demonstrated that these large-brained molluscs possess a suite of cognitive attributes that are comparable to those found in some vertebrates, including highly developed perception, learning, and memory abilities. Cephalopods are also renowned for performing sophisticated feats of flexible behaviour, which have led to claims of complex cognition such as causal reasoning, future planning, and mental attribution. Hypotheses to explain why complex cognition might have emerged in cephalopods suggest that a combination of predation, foraging, and competitive pressures are likely to have driven cognitive complexity in this group of animals. Currently, it is difficult to gauge the extent to which cephalopod behaviours are underpinned by complex cognition because many of the recent claims are largely based on anecdotal evidence. In this review, we provide a general overview of cephalopod cognition with a particular focus on the cognitive attributes that are thought to be prerequisites for more complex cognitive abilities. We then discuss different types of behavioural flexibility exhibited by cephalopods and, using examples from other taxa, highlight that behavioural flexibility could be explained by putatively simpler mechanisms. Consequently, behavioural flexibility should not be used as evidence of complex cognition. Fortunately, the field of comparative cognition centres on designing methods to pinpoint the underlying mechanisms that drive behaviours. To illustrate the utility of the methods developed in comparative cognition research, we provide a series of experimental designs aimed at distinguishing between complex cognition and simpler alternative explanations. Finally, we discuss the advantages of using cephalopods to develop a more comprehensive reconstruction of cognitive evolution.     

Applying new tools to cephalopod trophic dynamics and ecology: perspectives from the Southern Ocean Cephalopod Workshop, February 2–3, 2006

A two day workshop on Southern Ocean cephalopods was held in Hobart, Tasmania, Australia prior to the triennial 2006 Cephalopod International Advisory Council (CIAC) symposium. The workshop provided a second international forum to present the current state of research and new directions since the last Southern Ocean cephalopod meeting held in 1993. A major focus of the workshop was trophic ecology and the use of a variety of tools that can be applied in Southern Ocean trophic studies for both cephalopod and predator researchers. New tools that are being used as trophic indicators and tracers in food chain pathways include stable isotope, heavy metal and fatty acid signature analysis. Progress is also being made on understanding squid population dynamics in relation to other key components of the ecosystem by incorporating squid data in ecosystem models. Genetic barcoding is now of great value to fish taxonomy as well as other groups and it is expected that a cephalopod barcoding initiative will be an important tool for cephalopod taxonomy. There is a current initiative to produce a new cephalopod beak identification guide to assist predator biologists in identifying cephalopod prey items. There were also general discussions on specific taxonomic issues, Southern Ocean Cephalopod paralarvae and parasites, and suggestions for future CIAC workshop topics.     

Cephalopod neurobiology: an introduction for biologists working in other model systems

This paper concisely summarizes major aspects of cephalopod biology, behavior, and ecology providing a backdrop against which neurobiology of these animals can be interpreted. Reproduction, camouflage, motor control, memory, learning, and behavioral ecology are introduced, and thorough literature reviews of these subjects are cited for further reading. The aim of this paper is to provide a general introduction to cephalopods for use by workers currently focused on other model systems.     

Behaviour as a tool in the assessment of animal welfare

A central issue in animal welfare research is how to assess the welfare state of animals objectively and scientifically. I argue that this issue can be approached by asking two key questions: 1) is the animal physically healthy and 2) does the animal have what it wants? Behaviour is used to answer both of these questions. In the assessment of physical health, it can be used for clinical and pre-clinical diagnosis. In the assessment of what animals want, it has a major role through choice and preference testing. It is particularly important that applied ethologists develop methods for assessing welfare in situ--in the places where concern for animal welfare is greatest such as on farms and in zoos.     

Animal Suffering: An Invertebrate Perspective

Consideration of the welfare of other animals often is anthropocentric, focusing usually on mammals similar to humans. This article argues the necessity of evaluating the extension of such consideration more widely to invertebrates. Although unlike humans, some groups such as cephalopod molluscs probably have the potential for pain and suffering. In addition, a morality of care, rather than one of rights, and the damage humans do to themselves by cruel treatment of animals both argue for the extension of consideration to all animal species. This consideration predicts extension of basic care of cephalopods from simple housing and feeding into areas such as behavioral enrichment.     

Cephalopods in neuroscience: regulations,research and the 3Rs

Cephalopods have been utilised in neuroscience research for more than 100 years particularly because of their phenotypic plasticity, complex and centralised nervous system, tractability for studies of learning and cellular mechanisms of memory (e.g. long-term potentiation) and anatomical features facilitating physiological studies (e.g. squid giant axon and synapse). On 1 January 2013, research using any of the about 700 extant species of “live cephalopods” became regulated within the European Union by Directive 2010/63/EU on the “Protection of Animals used for Scientific Purposes”, giving cephalopods the same EU legal protection as previously afforded only to vertebrates. The Directive has a number of implications, particularly for neuroscience research. These include: (1) projects will need justification, authorisation from local competent authorities, and be subject to review including a harm-benefit assessment and adherence to the 3Rs principles (Replacement, Refinement and Reduction). (2) To support project evaluation and compliance with the new EU law, guidelines specific to cephalopods will need to be developed, covering capture, transport, handling, housing, care, maintenance, health monitoring, humane anaesthesia, analgesia and euthanasia. (3) Objective criteria need to be developed to identify signs of pain, suffering, distress and lasting harm particularly in the context of their induction by an experimental procedure. Despite diversity of views existing on some of these topics, this paper reviews the above topics and describes the approaches being taken by the cephalopod research community (represented by the authorship) to produce “guidelines” and the potential contribution of neuroscience research to cephalopod welfare.     

The journey of squid sperm

Sperm storage is common in internally fertilizing animals, but is also present in several external fertilizers, such as many cephalopods. Cephalopod males attach sperm packets (spermatangia) to female conspecifics during mating. Females of eight externally fertilizing families comprising 25% of cephalopod biodiversity have sperm-storage organs (seminal receptacles) in their buccal area, which are not in direct physical contact with the deposited spermatangia. The mechanism of sperm transmission between the implantation site and the storage organ has remained a major mystery in cephalopod reproductive biology. Here, jumbo squid females covering almost the entire life cycle, from immature to a laboratory spawned female, were used to describe the internal structure of the seminal receptacles and the process of sperm storage. Seminal fluid was present between the spermatangia and seminal receptacles, but absent in regions devoid of seminal receptacles. The sperm cellular component was formed by spermatozoa and round cells. Although spermatozoa were tracked over the buccal membrane of the females to the inner chambers of the seminal receptacles, round cells were not found inside the seminal receptacles, suggesting that spermatozoa are not sucked up by the muscular action of the seminal receptacles. This finding supports the hypothesis that spermatozoa are able to actively migrate over the female skin. Although further experimental support is needed to fully confirm this hypothesis, our findings shed light on the elusive process of sperm storage in many cephalopods, a process that is fundamental for understanding sexual selection in the sea.     

Renal organs of cephalopods: a habitat for dicyemids and chromidinids

The renal organs of 32 species of cephalopods (renal appendage of all cephalopods, and renal and pancreatic appendages in decapods) were examined for parasite fauna and for histological comparison. Two phylogenetically distant organisms, dicyemid mesozoans and chromidinid ciliates, were found in 20 cephalopod species. Most benthic cephalopods (octopus and cuttlefish) were infected with dicyemids. Two pelagic cephalopod species, Sepioteuthis lessoniana and Todarodes pacificus, also harbored dicyemids. Chromidinid ciliates were found only in decapods (squid and cuttlefish). One dicyemid species was found in branchial heart appendages of Rossia pacifica. Dicyemids and chromidinids occasionally occurred simultaneously in Euprymna morsei, Sepia kobiensis, S. peterseni, and T. pacificus. The small-sized cephalopod species, Idiosepius paradoxus and Octopus parvus, harbored no parasites. Comparative histology revealed that the external surface of renal organs varies morphologically in various cephalopod species. The small-sized cephalopod species have a simple external surface. In contrast, the medium- to large-sized cephalopod species have a complex external surface. In the medium- to large-sized cephalopod species, their juveniles have a simple external surface of the renal organs. The external surface subsequently becomes complicated as they grow. Dicyemids and chromidinids attach their heads to epithelia or insert their heads into folds of renal appendages, pancreatic appendages, and branchial heart appendages. The rugged and convoluted external surface provides a foothold for dicyemids and chromidinids with a conical head. They apparently do not harm these tissues of their host cephalopods.     

Host defense mechanisms of cephalopods

Humoral and cellular mechanisms of defense have been described for cephalopods, a relatively advanced group of mollusks. Typical of other mollusks, cephalopod agglutinins are the most documented component of humoral immunity. Lectins, which have agglutinating properties, have been described and characterized from octopuses. Agglutinins from cephalopod hemolymph have also been shown to agglutinate a variety of vertebrate red blood cells, as well as potential bacterial pathogens. Hemocytes are the primary component of cellular immunity. Although the hemocyte role in phagocytosis has been extensively studied in other mollusks, the mechanisms of phagocytosis have not been described extensively for cephalopods. Cephalopod hemocytes have phagocytic capabilities and may function in encapsulation and neutralization of foreign substances; however, the effects of environmental factors and the full extent of phagocytic capabilities of cephalopod hemocytes have not been reported. Hemocytes from cephalopods have a role in wound healing and inflammation which have been reported in detail by several investigators.     

IACUC Challenges in Invertebrate Research

With billions of individuals and possibly hundreds of thousands of genera, invertebrates represent the largest number and greatest diversity of all animals used in research. Although the capacity for nociception is recognized in many invertebrate taxa, researchers and IACUC members are challenged by a lack of clear understanding of invertebrate welfare and by differing standards of moral concern for these taxa. In practice this has led IACUCs to consider invertebrates in two major groups: species worthy of increased moral concern approximating that shown to vertebrate species (this group includes cephalopods and to some extent decapod crustaceans) and all others. This dichotomy has led to differences in how invertebrate research is regulated and documented. This article presents two case studies illustrating specific concerns in invertebrate research protocols and then provides relevant information to address practical IACUC matters related to regulatory and ethical issues, sourcing and record keeping, risk management, assessment of pain and nociception in invertebrates, housing and husbandry, invasive procedures, veterinary care, and humane endpoints.     

Reflecting on ethical and legal issues in wildlife disease

Disease in wildlife raises a number of issues that have not been widely considered in the bioethical literature. However, wildlife disease has major implications for human welfare. The majority of emerging human infectious diseases are zoonotic: that is, they occur in humans by cross‐species transmission from animal hosts. Managing these diseases often involves balancing concerns with human health against animal welfare and conservation concerns. Many infectious diseases of domestic animals are shared with wild animals, although it is often unclear whether the infection spills over from wild animals to domestic animals or vice versa. Culling is the standard means of managing such diseases, bringing economic considerations, animal welfare and conservation into conflict. Infectious diseases are also major threatening processes in conservation biology and their appropriate management by culling, vaccination or treatment raises substantial animal ethics issues. One particular issue of great significance in Australia is an ongoing research program to develop genetically modified pathogens to control vertebrate pests including rabbits, foxes and house mice. Release of any self‐replicating GMO vertebrate pathogen gives rise to a whole series of ethical questions. We briefly review current Australian legal responses to these problems. Finally, we present two unresolved problems of general importance that are exemplified by wildlife disease. First, to what extent can or should ‘bioethics’ be broadened beyond direct concerns with human welfare to animal welfare and environmental welfare? Second, how should the irreducible uncertainty of ecological systems be accounted for in ethical decision making?     

Molecular phylogeny of coleoid cephalopods (Mollusca: Cephalopoda) inferred from three mitochondrial and six nuclear loci: a comparison of alignment, implied alignment and analysis methods

Recent molecular studies investigating higher-level phylogeneticsof coleoid cephalopods (octopuses, squids and cuttlefishes)have produced conflicting results. A wide range of sequencealignment and analysis methods are used in cephalopod phylogeneticstudies. The present study investigated the effect of commonlyused alignment and analysis methods on higher-level cephalopodphylogenetics. Two sequence homology methods: (1) eye alignment,(2) implied alignment, and three analysis methods: (1) parsimony,(2) maximum likelihood, (3) Bayesian methodologies, were employedon the longest sequence dataset available for the coleoid cephalopods,comprising three mitochondrial and six nuclear loci. The datawere also tested for base composition heterogeneity, which wasdetected in three genes and resolved using RY coding. The Octopoda,Argonautoidea, Oegopsida and Ommastrephidae are monophyleticin the phylogenies resulting from each of the alignment andanalysis combinations. Furthermore, the Bathyteuthidae are thesister taxon of the Oegopsida in each case. However many relationshipswithin the Coleoidea differed depending upon the alignment andanalysis method used. This study demonstrates how differencesin alignment and analysis methods commonly used in cephalopodphylogenetics can lead to different, but often highly supported,relationships. (Received 15 December 2006; accepted 1 September 2007)     

Ethics and invertebrates: a cephalopod perspective

This paper first explores 3 philosophical bases for attitudes to invertebrates, Contractarian/Kantian, Utilitarian, and Rights-based, and what they lead us to conclude about how we use and care for these animals. We next discuss the problems of evaluating pain and suffering in invertebrates, pointing out that physiological responses to stress are widely similar across the animal kingdom and that most animals show behavioral responses to potentially painful stimuli. Since cephalopods are often used as a test group for consideration of pain, distress and proper conditions for captivity and handling, we evaluate their behavioral and cognitive capacities. Given these capacities, we then discuss practical issues: minimization of their pain and suffering during harvesting for food; ensuring that captive cephalopods are properly cared for, stimulated and allowed to live as full a life as possible; and, lastly, working for their conservation.     

Zoo Animal Welfare: The Human Dimension

ABSTRACT

Standards and policies intended to safeguard nonhuman animal welfare, whether in zoos, farms, or laboratories, have tended to emphasize features of the physical environment. However, research has now made it clear that very different welfare outcomes are commonly seen in facilities using similar environments or conforming to the same animal welfare requirements. This wide variation is almost certainly due, at least in part, to the important effects of the actions of animal care staff on animal welfare. Drawing mostly on the farm animal literature, we propose that this “human dimension” of animal welfare involves seven components: (1) positive human–animal interaction, (2) consistency and familiarity of keepers, (3) treating animals as individuals and taking account of their personalities, (4) the attitudes and personalities of keepers, (5) the keepers’ knowledge and experience, (6) the keepers’ own well-being, and (7) the influence of facility design on how keepers and others interact with the animals. We suggest that attention to these human factors provides major scope for improving the welfare of animals in zoos.     

Pelagic cephalopods from eastern Australia: species composition, horizontal and vertical distribution determined from the diets of pelagic fishes

The distribution and relative biomass of cephalopods from pelagic waters off eastern Australia was examined between 1997 and 2004 from stomach contents of swordfish, yellowfin tuna and dolphinfish taken in the domestic longline fishery. A total of 38 taxa from 19 families were identified. Comparison of the species composition of the three predators indicated pronounced differences in cephalopod species composition. In swordfish, species of the family Ommastrephidae, particularly Ommastrephes bartramii (Lesueur 1821) and Nototodarus gouldi (McCoy 1888) dominated, whereas a more diverse mix of species was identified from yellowfin-sampled cephalopods. Todaropsis eblanae (Ball 1841) was the main cephalopod sampled from the surface-dwelling dolphinfish. For swordfish-sampled cephalopods, significant relationships were found between biomass and season, fluorescence and year. In yellowfin tuna, cephalopod biomass was significantly correlated with season, area and sea surface temperature. Significant factors differed between predator-sampler, possibly reflecting the limits of the predator, but could also give insights into individual cephalopod species distributions. However, the increase in cephalopod biomass over summer in both swordfish and yellowfin tuna suggested cephalopod biomass was higher over summer in the region.     

Cannibalism in cephalopods

Cannibalism refers to the action of consuming a member of the same species and is common in many taxa. This paper reviews the available literature on cannibalism in cephalopods. All species of the class Cephalopoda are predators and cannibalism is common in most species whose diet has been studied. Cannibalism in cephalopods is density-dependent due to their aggressive predatory and in case of the octopuses territorial nature. It also depends upon local and temporal food availability and of the reproductive season. Cannibalistic behaviour is positively related to the size of both cannibal and victim. It can affect population dynamics of cephalopods in periods of low food availability and/or high population abundance. Cephalopods are generally restricted in their ability to store energy. It is thus assumed that cannibalism is part of a population energy storage strategy enabling cephalopod populations to react to favourable and adverse environmental conditions by increasing and reducing their number. Finally, we propose five orientation points for future research on cannibalism in cephalopods.     

Validation of the water offloading technique for diet assessment: an experimental study with Cory’s shearwaters ( Calonectris diomedea )

We examined the effect of prey type, repeated stomach flushing, digestion time, and meal size on the assessment of dietary intake of captive adult Cory’s shearwaters (Calonectris diomedea). For each of Cory’s shearwaters’ main prey type (fish, cephalopod, and crustacea), we used three different meal sizes and four digestion times, stomach-flushing the birds 1, 4, 8, or 16 h after feeding. On average, fish and cephalopods showed similar percentages of mass recovery (between 23% and 33%), whereas crustaceans showed a recovery about 10–15% greater. Conversely, fish and crustaceans showed similar percentages of items recovered (between 52% and 77%), whereas cephalopods showed about 10–35% greater recovery rates. We found no significant differences in the percentage of individual prey items recovered and the interval between ingestion and recovery, over intervals ranging from 1 to 16 h.L.R. Monteiro was tragically killed in a plane crash in the Azores in December 1999.     

动物福利在研究生实验动物学教学中的应用初探

在医学研究中,实验动物具有不可替代的地位和作用,越来越多的人开始关心动物福利。各医学院校是培养未来科研工作者的机构,实验动物在医学院校的使用量非常大,因此,在课堂教学中,培养医学生树立保护动物福利的观念具有重要意义。本文从课堂教育、实验动物处理、3R原则的实施等方面探讨了如何在教学过程中开展动物福利教育。     

Cephalopod and Groundfish Landings: Evidence for Ecological Change in Global Fisheries?

Cephalopod fisheries are among the few still with some local potential for expansion; in fact, as groundfish landings have declined globally, cephalopod landings have increased. We propose the hypothesis that, although increased cephalopod landings may partly reflect increased market demand, overfishing groundfish stocks has positively affected cephalopod populations. Data from 15 key FAO areas reveal that, with the exception of the north- east Atlantic, cephalopod landings have increased significantly over the last 25 years while groundfish have risen more slowly, remained stable, or declined. In terms of volume, cephalopods have not replaced groundfish. This is hypothesized as owing to the shorter life cycle of cephalopods, and rapid turnover and lower standing stocks than for longer-lived finfish species. Under high fishing pressure, groundfish are probably poor competitors, having less opportunity for spawning and replacement. In West Africa, the Gulf of Thailand and Adriatic there is strong circumstantial evidence that fishing pressure has changed ecological conditions and cephalopod stocks have increased as predatory fish have declined. We recommend that this hypothesis be tested thoroughly in other areas where suitable data exist. Most coastal and shelf cephalopod fisheries are likely to be fully exploited or overexploited, and current annual fluctuations in cephalopod landings are probably largely environmentally-driven.