Ángel Guerra

A review of reproductive strategies in cephalopods

Cephalopod reproductive strategies are reviewed in order to clarify their current, confusing status. Based on the type of ovulation, spawning pattern and growth between egg batches or spawning periods, five comprehensive and flexible cephalopod reproductive strategies are defined. Accordingly, with these three factors the following classification is proposed. (a) Spawning once (formerly semelparity) consisting of simultaneous terminal spawning, with synchronous ovulation, monocyclic spawning and absence of growth between egg batches. (b) Spawning more than once (formerly iteroparity) including: (i) polycyclic spawning with egg‐laying occurring in separate batches during the spawning season and growth occurring between production of egg batches and spawning seasons; (ii) multiple spawning, with group‐synchronous ovulation, monocyclic spawning and growth between egg batches; (iii) intermittent terminal spawning, with group‐synchronous ovulation, monocyclic spawning and no growth between egg batches; (iv) continuous spawning, with asynchronous ovulation, monocyclic spawning and growth between egg batches. Examples of species exhibiting each of these reproductive strategies are given. The large amount of inter‐species variation in several life‐history traits related to reproductive events is discussed.

Extensive population subdivision of the cuttlefish Sepia officinalis (Mollusca: Cephalopoda) around the Iberian Peninsula indicated by microsatellite DNA variation

The Atlantic Ocean-Mediterranean Sea junction has been proposed as an important phylogeographical area on the basis of concordance in genetic patterns observed at allozyme, mtDNA and microsatellite DNA markers in several marine species. This study presents microsatellite DNA data for a mobile invertebrate species in this area, the cuttlefish Sepia officinalis, allowing comparison of this relatively new class of DNA marker with previous allozyme results, and examination of the relative effects on gene flow of the Strait of Gibraltar and the Almería-Oran oceanographic front. Genetic variation at seven microsatellite loci screened in six samples from NE Atlantic and Mediterranean coasts of the Iberian Peninsula was high (mean Na = 9.6, mean He = 0.725). Microsatellites detected highly significant subpopulation structuring (FST= 0.061; RST = 0.104), consistent with an isolation-by-distance model of low levels of gene flow. Distinct and significant clinal changes in allele frequencies between Atlantic and Mediterranean samples found at five out of seven loci, however indicate these results might be also consistent with an alternative model of secondary contact and introgression between previously isolated and divergent populations, as previously proposed for other marine species from the Atlantic-Mediterranean area. A pronounced ‘step’ change between SW Mediterranean samples associated with the Almería-Oran front suggests this oceanographic feature may represent a contemporary barrier to gene flow.

A review of cephalopod—environment interactions in European Seas

Cephalopods are highly sensitive to environmental conditions and changes at a range of spatial and temporal scales. Relationships documented between cephalopod stock dynamics and environmental conditions are of two main types: those concerning the geographic distribution of abundance, for which the mechanism is often unknown, and those relating to biological processes such as egg survival, growth, recruitment and migration, where mechanisms are sometimes known and in a very few cases demonstrated by experimental evidence. Cephalopods seem to respond to environmental variation both ‘actively’ (e.g. migrating to areas with more favoured environmental conditions for feeding or spawning) and ‘passively’ (growth and survival vary according to conditions experienced, passive migration with prevailing currents). Environmental effects on early life stages can affect life history characteristics (growth and maturation rates) as well as distribution and abundance. Both large-scale atmospheric and oceanic processes and local environmental variation appear to play important roles in species–environment interactions. While oceanographic conditions are of particular significance for mobile pelagic species such as the ommastrephid squids, the less widely ranging demersal and benthic species may be more dependent on other physical habitat characteristics (e.g. substrate and bathymetry). Coastal species may be impacted by variations in water quality and salinity (related to rainfall and river flow). Gaps in current knowledge and future research priorities are discussed. Key research goals include linking distribution and abundance to environmental effects on biological processes, and using such knowledge to provide environmental indicators and to underpin fishery management.

Stock assessment methods used for cephalopod fisheries

Abstract Cephalopods are of increasing importance as a fishery resource and many species are taken in directed and bycatch fisheries around the world. Owing to the short life-cycles and variable growth rates of most cephalopods, stocks may be highly volatile, both highly susceptible to recruitment overfishing and, conversely, capable of rapid recovery. Many species have protracted spawning seasons so that multiple microcohorts may be present in the population at any one time. Many assessment methods have been applied to cephalopod stocks, including stock-recruitment relationships (e.g. the Japanese Todarodes pacificus stock), recruitment indices (e.g. Saharan Bank cephalopod stocks), swept-area biomass estimates (e.g. Northwest Atlantic stocks of the squids Loligo pealei and Illex illecebrosus), production models (e.g. Saharan Bank cephalopod stocks), cohort analysis (e.g. Illex argentinus in the Falkland islands), yield-per-recruit models (e.g. Northwest Atlantic squid stocks), length-based cohort analysis (e.g. Dosidicus gigas in the Gulf of California), and depletion estimates of stock size (e.g. Illex argentinus in the Falkland islands). Despite the widespread application of assessment methods, few stocks are rigorously managed, and the best example of a regulated fishery is the Falkland islands squid fishery. In contrast, although a number of assessment methods are used in the Japanese Todarodes fishery, management activities are designed to ensure harmonious operation on the industry rather than maintain stock size. Fisheries for Loligo forbesi and Loligo vulgaris in the Northeast Atlantic are mainly based on by-catches, although there is some directed fishing, particularly artisanal jig fishing in coastal waters. There is currently no assessment and minimal management for these species, and available management options are constrained by the nature of the fishery and the generally poor quality of available data.

The life history of Loligo vulgaris and Loligo forbesi (Cephalopoda: Loliginidae) in Galician waters (NW Spain)

Abstract The population biology of Loligo vulgaris and Loligo forbesi in Galician waters is described based on monthly samples from the fishery obtained during the period February 1991–June 1992. Maturity was assessed using a maturity scale and indices. The estimated number of oocytes in mature females varied from 782 to 21 885 in L. vulgaris and from 1317 to 14 956 in L. forbesi , and showed a slight positive correlation with the length of the mantle ( ML ) for both species. Oocytes in the ovaries fall into three discrete size classes, which suggests that L. vulgaris and L. forbesi are intermittent or multiple spawning species. In L. vulgaris males mature at two different modal sizes, hence perhaps at two different ages, while in L. forbesi this occurs in both males and females. Males mature earlier in the season than females in both species. The maximum number of spermatophores found was 1010 and 1000 in two L. vulgaris males with 119 mm and 400 mm ML respectively, and 1035 in a L. forbesi male with 150 mm ML . In both species, spermatophore length increases with ML . Loligo forbesi males maturing at a larger size produce fewer but larger spermatophores than those maturing at a small size. Loligo vulgaris spawn throughout the year, but the period of more intensive spawning extends from December to April. The breeding season of L. forbesi extends from December to May, the more intensive spawning extending from December to February. Sex ratios were variable for both species. Age and growth for both species and sexes were estimated by examining growth increments in the statoliths. Like-sized individuals had different ages in both species. The life span of L. vulgaris was estimated at about 1 year while L. forbesi seems to reach an age of 15–16 months. A list of prey species found in gastric contents of both species is given. The diet of L. vulgaris comprises fish (86.8%), cephalopods (6.0%), crustaceans (3.0%) and polychaetes (1.8%), and the diet of L. forbesi includes fish (75.6%), crustaceans (18.5%) and cephalopods (4.4%).

Fishery by-catches of marine mammals in Galician waters: results from on-board observations and an interview survey of fishermen

Rates of cetacean by-catch were investigated in Galician waters (NW Spain) using a combination of observer trips on fishing vessels, a carcase recovery scheme and an interview survey of fishermen, carried out over two years (1998–1999). All these data sources are suspected of underestimating by-catch due to the sample of co-operating fishermen being, necessarily, self-selecting. No by-catches were seen during observer trips, although not all sectors of the fishery could be covered. The carcass recovery scheme yielded seventeen cetacean carcases over two years, which compares to around 35 by-caught cetaceans recorded annually by the Galician strandings network. Analysis of interview data suggested that around 200 cetaceans might be caught annually in inshore waters and around 1500 in offshore waters. Confidence limits were wide for all estimates. The highest by-catch rates were estimated for gillnets and offshore trawling. The majority of by-catches are small dolphins, probably mainly Delphinus delphis. Smaller numbers of Tursiops truncatus and Globicephala melas are also reported. Comparing the interview estimates of by-catch rates with minimum estimates of population size, it is suggested that by-catches of D. delphis and T. truncatus may be unsustainably high and that routine monitoring of fishery by-catches in Galician fisheries is required. # 2003 Elsevier Science Ltd. All rights reserved.

Feeding ecology of Cuvier's beaked whale (Ziphius cavirostris): A review with new information on the diet of this species

Published information on the diet of Cuviers beaked whales Ziphius cavirostris (Odontoceti: Ziphiidae) is reviewed and new information on the stomach contents of three animals: two stranded in Galicia (north-west Spain) in February 1990 at A Lanzada, and in February 1995 at Portonovo; and the third stranded in February 1999 in North Uist (Scotland), is presented. The whale stranded in 1990 was a male; the other two were adult females, All animals were > 5 m long. The limited published information on the diet of this species indicates that it feeds primarily on oceanic cephalopods although some authors also found remains of oceanic fish and crustaceans. Food remains from the three new samples consisted entirely of cephalopod beaks. The Scottish sample set is the largest recorded to date for this species. The prey identified consisted of oceanic cephalopods, mainly squid (Cephalopoda: Teuthoidea). The most frequently occurring species were the squid Teuthowenia megalops, Mastigoteuthis schmidti and Taonius pavo (for the Galician whale stranded in 1990), Teuthowenia megalops and Histioteuthis reversa (for the second Galician whale) and T. megalops, Gonatus sp. and Taonius pavo (for the Scottish whale). Other prey included the squid Histioteuthis bonnellii, Histioteuthis arcturi and Todarodes sagittatus as well as Vampiroteuthis infernalis (Cephalopoda: Vampyromorpha), Stauroteuthis syrtensis and Japetella diaphana (Cephalopoda: Octopoda). The squid eaten (estimated from the measurement of the lower beaks) included juvenile and mature individuals of the most important species (Teuthowenia megalops, Gonatus sp.). The range of species found in the diet of Z. cavirostris is greater than that reported for sperm whales and bottlenosed whales in the north-east Atlantic.

Diets of marine mammals stranded on the northwestern Spanish Atlantic coast with special reference to Cephalopoda

Abstract Stomach contents from 59 marine mammals, 28 Delphinus delphis , 14 Tursiops truncatus , three Grampus griseus , four Stenella coeruleoalba , three Globicephala melas , one Ziphius cavirostris , four Phocoena phocoena , one Physeter macrocephalus and one Balaenoptera acutorostrata stranded on the northwestern Spanish Atlantic coast from December 1990 to March 1993 were examined. A total of 9076 fish otoliths and 654 cephalopod upper and lower beaks were collected. The otoliths were identified only to family level, representing by number 65% Gadidae, 24% Gobiidae, 6% Atherinidae, 2% Ammodytidae, 1.5% Clupeidae and the rest Carangidae, Labridae, Argentinidae, Macroramphosidae and Bothidae. The cephalopod beaks belonged to 12 species of nine families. The cephalopod families contributing food of these marine mammals, in order of contribution by number of specimens are, the Loliginidae (56.9%), the Octopodidae (25.3%), the Ommastrephidae (11.9%), the Sepiolidae (2.4%), the Histioteuthidae (0.9%), the Chiroteuthidae (0.9%), the Cranchiidae (0.8%), the Mastigoteuthidae (0.3%) and the Gonatidae (0.15%). The great part of the cephalopods observed in the stomach contents were small in size, except for some octopods in Grampus griseus and Globicephala melas , and Mastigoteuthis sp. in Physeter macrocephalus . The results indicated that D. delphis, T. truncatus and Phocoena phocoena are primarily fish-eating, while Grampus griseus, Globicephala melas and Physeter macrocephalus had only cephalopod remains in their stomachs.

Growth increments and biomineralization process in cephalopod statoliths

A study on morphological, structural and biochemical composition of Sepia officinalis and Loligo vulgaris statoliths and statocyst endolymph was undertaken with the aim of determining the major factors affecting the deposition process of statolith formation and to clarify the cause for the poor definition of the growth increments in S. officinalis statoliths. It is suggested that the different biochemical composition of the statocyst endolymph found in the two species accounts for distinct statolith crystallisation processes, which results in a different microstructure. This explains the better definition of growth increments in L. vulgaris statoliths comparing with those of S. officinalis. The protein content as well as Ca(2+) and Mg(2+) concentrations in the endolymph are more implicated in growth increments formation than Sr(2+) ion concentration. Moreover, the daily variations of the three factors mentioned, allowed us to formulate a working hypothesis to explain the daily deposition of growth increments: a dark ring (rich in organic matter) is deposited during daylight whereas a light ring (rich in CaCO(3)) during darkness. These results are discussed in the light of alternative hypotheses explaining the deposition mechanisms in statoliths.

Reproduction and condition of female Octopus mimus (Mollusca: Cephalopoda)

The relationship between reproduction and condition was studied in a 15 mo sample of 919 maturing, mature and post-spawning female Octopus mimus (388 to 3714 g) caught in Iquique (North Chile). O. mimus is a semelparous species, with reproduction taking place all year round. Investment in reproductive tissues was, on average, 9.9% of mature female body weight, independent of season. However, somatic growth during maturation was dependent on season and varied between 26 and 63% of the whole-body growth in weight. The condition of females did not vary markedly until spawning, although seasonal variations were apparent, winter being the most unfavourable. Condition deteriorated dramatically after spawning, during parental care of the eggs. During this period, somatic-tissue depletion, mainly from the muscles, was >25% of the total body weight of mature females. The fecundity of O. mimus was probably limited by the costs associated with parental care of the eggs.