Loligo Opalescens Research Articles

Environment, krill and squid in the Monterey Bay: from fisheries to life histories and back again

The fishery for market squid in California is extremely valuable and only recently subject to regulations (in that sense, it is one of the last great open-access fisheries on the western coast of North America). We briefly review the history of the fishery for Loligo opalescens, on an annual time scale. Within-season analyses suggest that cohorts of squid persist offshore and move inshore for reproduction throughout the season. In order to predict the timing of inshore movement of squid, we develop a life history model using stochastic dynamic programming. This model allows us to link squid growth and reproduction with environmental factors, particularly, upwelling, temperature, and food abundance, in a consistent Darwinian framework. Using the model, we predict the timing of squid movement inshore in cold and warm environments, and the amount of biomass inshore in weekly intervals. We compare the model predictions with unpublished fishery-dependent data subsampled from landings and discuss the implications of our work for management of the squid fishery.

Advances in defining the life histories of myopsid squid

Recent years have seen the emergence of extensive studies of myopsid squid growth of the family Loliginidae. This has greatly advanced our understanding of their life histories. Growth data have accumulated from both statolith-based field studies and culture work. Validation studies on loliginids continue to support that statolith increments are laid down daily. Ageing work has also revealed that short lifespans are typical, with nine of the 21 species studied having lifespans <200 days, eight species with lifespans between 200 days and about 1 year and only three species with lifespans >1 year. While growth is continuous and non-asymptotic, the marked plasticity in size-at-age has hindered the development of a general model to describe squid growth. Many loliginids are multiple spawners that continue to feed while growing and reproducing, although there has been some documented loss of conditon in mature individuals. An exception is Loligo opalescens, which has a terminal spawning strategy with a marked loss of condition and post-spawning mortality. Quantification of the cost of living and the energetics of loliginids are likely to be best achieved by combining field and culture studies on a species such as the Indo-Pacific squid Sepioteuthis lessoniana.

Acoustic detectability of squid egg beds

Egg beds of the market squid (Loligo opalescens) on the bottom of Monterey Bay seem to have been detected by means of sidescan sonar at 420 kHz. Evidence for this is presented in the form of sidescan sonar images and egg-bed distribution maps from the same area, as prepared from camera surveys by scuba divers. The general detectability issue is also considered, with specific reference made to preliminary physical measurements performed on two egg capsules. [Work supported by Sea Grant.]

A walk though vertebrate and invertebrate protamines.

An updated comparative analysis of protamines and their corresponding genes is presented, including representative organisms from each of the vertebrate classes and one invertebrate (squid, Loligo opalescens). Special emphasis is placed on the implications for sperm chromatin organization and the evolutionary significance. The review is based on some of the most recent publications in the field and builds upon previously published reviews on this topic.

The effects of an extraordinary El Niño / La Niña event on the size and growth of the squid Loligo opalescens off Southern California

The population structure of the California market squid Loligo opalescens was studied for the Channel Islands region off Southern California between June 1998 and March 2000. During this time Californian waters were exposed to an extraordinary El Nino event that was possibly the most dramatic change in oceanographic conditions that occurred last century. There was then a rapid transition to record cool La Nina conditions. Statolith increments were used to determine age parameters and increment periodicity was validated for the first 54 days of life. Based on statolith increment counts, the oldest males and females were 257 and 225 days respectively and individuals matured as young as 129 and 137 days respectively. No distinct hatching period was detected. There was a general trend of increasing body size throughout the study period. Squid that hatched and grew through the El Nino were strikingly smaller and had slower growth rates compared to squid that grew through the La Nina. This was related to oceanography and associated productivity. There was a positive correlation between squid mantle length and upwelling index and a negative correlation between mantle length and sea temperature. The 'live-fast die-young' life history strategy of squid makes them ideal candidates for following the effects of the dramatic changes in oceanographic conditions off California. We propose that squid can serve as ecosystem recorders and productivity integrators over time and space and are useful organisms to tie oceanography to biology.

Tank culture of yellowfin tuna, Thunnus albacares: developing a spawning population for research purposes

Abstract A land-based culture facility for research on yellowfin tuna, Thunnus albacares , was developed at the Achotines Laboratory in the Republic of Panama. Six concrete tanks, and seawater and life support systems were built to maintain a yellowfin broodstock. On average, 50% of the yellowfin caught survived capture and handling, and approximately 30% became broodstock in Tank 1 (17 m diameter, 6 m depth) or Tank 2 (8.5 m diameter, 3 m depth). Each fish was tagged with a microchip implant tag, then weighed, measured, and injected with oxytetracycline (OTC) prior to stocking. Daily rations of primarily market squid, Loligo opalescens , and Pacific thread herring, Opisthonema spp., were regulated based on the feeding activity and energy requirements of the fish. Feeding activity of the broodstock decreased when the water temperatures decreased, and the fish ate decreasing daily rations and increasing calories with increasing size. Spawning occurred in both tanks within 6–8 months of capture. Spawning first occurred in Tank 1 when 24 females ranged in size from 6 to 16 kg and 65 to 93 cm fork length (FL). Spawning was intermittent during the first 2 months and occurred near daily thereafter. Tank size appeared to affect survival rates, the types of mortalities that occurred, and the growth of the fish. Survival rates after 1 year in captivity were higher, and the fish were larger, on average, in Tank 1 than in Tank 2. Most of the mortalities in Tank 1 were the result of wall strikes, which occurred more frequently after the fish reached their highest density of 0.64 kg m −3 and sizes greater than 96 cm FL and 19 kg. Non-linear growth models were fitted to the initial stocking sizes and final sizes of fish that died or were removed from Tank 1 during 1996–1999. Estimated growth rates in length (11–48 cm year −1 ) for fish between 51 and 150 cm FL decreased with increasing length. Estimated growth rates in weight ranged from 9 to 19 kg year −1 for fish less than 19 kg and 20–23 kg year −1 for fish greater than 19 kg. The results of this work demonstrate that the stable environment of a land-based culture facility may be the preferred system for long-term maintenance of a yellowfin broodstock.

Expression of Ca 2+-ATPase and Na +/Ca 2+-exchanger is upregulated during epithelial Ca 2+ transport in hypodermal cells of the isopod Porcellio scaber

It is thought that a plasma membrane Ca 2+-transport ATPase (PMCA) and a Na +/Ca 2+-exchange (NCE) mechanism are involved in epithelial Ca 2+ transport (ECT) in a variety of crustacean epithelia. The sternal epithelium of the terrestrial isopod Porcellio scaber was used as a model for the analysis of Ca 2+-extrusion mechanisms in the hypodermal epithelium. Using RT-PCR, we amplified a cDNA fragment of 1173 bp that encodes a protein sequence possessing 72% identity to the PMCA from Drosophila melanogaster and a cDNA fragment of 791 bp encoding a protein sequence with 50% identity to the NCE from Loligo opalescens. Semiquantitative RT-PCR revealed that the expression of both mRNAs increases from the non-Ca 2+-transporting condition to the stages of CaCO 3 deposit formation and degradation. During Ca 2+-transporting stages, the expression of PMCA and NCE was larger in the anterior sternal epithelium (ASE) than in the posterior sternal epithelium (PSE). The results demonstrate for the first time the expression of a PMCA and a NCE in the hypodermal epithelium of a crustacean and indicate a contribution of these transport mechanisms in ECT.

Distribution of squid paralarvae, Loligo opalescens (Cephalopoda: Myopsida), in the Southern California Bight in the three years following the 1997-1998 El Niño

Large numbers of paralarvae of the California market squid, Loligo opalescens (10,560 paralarvae from 422 plankton samples), were collected in the Southern California Bight in 1999, 2000, and 2001 during the spawning season. Paralarval abundance increased dramatically (P<0.0041) from 1.5 squid/1,000m3 in 1999 to 77.9 squid/1,000m3 in 2000, and 73.6 squid/1,000m3 in 2001, following the El Nino of 1997–1998. The effects on the squid fishery of the 1997–1998 El Nino were thus extended for two years, with larval abundance reduced until the 1999–2000 spawning season. Paralarvae were abundant close to shore for up to a month after hatching in 2000 (P<0.003), with tidal surface currents adjacent to shore in the Channel Islands strongly affecting paralarval abundance. Tidally reversing currents within 1–3 km of shore created a boundary layer of "sticky water" within which paralarvae remained entrained inshore immediately after hatching. Neritic currents farther from shore dispersed older paralarvae within the Southern California Bight. The greatest change in paralarval abundance, for all transects, was observed within 1 km of the transition between these two flow regimes. Age of paralarvae (from statolith increments) entrained within the Catalina Island boundary layer averaged 13–16 days, but some individuals remained nearshore for up to a month. Paralarvae in the boundary layer occurred above 80 m depth both day and night, and exhibited a statistically significant pattern of vertical diel migration (P<0.01). Paralarvae at sea were disproportionately abundant adjacent to fronts associated with uplifted isotherms.

Optimizing rearing conditions of hatchling loliginid squid

Eggs laid by the California market squid (Loligoopalescens) were collected from spawning grounds and reared in the laboratory. The eggs were maintained in a rearing tank that was part of a closed, recirculating system. The system included seven 220-l circular tanks with attached filtration. Five experiments were conducted to test hatchling survival. One of them evaluated survival on three different food types: (a) enriched Artemia sp. nauplii, (b) wild zooplankton and (c) a mixture of a and b plus mysid shrimp. This mixture of food types (c) was offered to the hatchlings in the other four experiments. High mortality occurred in all experiments between days 1 and 15 post-hatching. However, survival over the entire time span of the experiments (45–60 days) was between 36% and 60%. These survival rates are well above previously reported survival rates for the same time period, and overall are up to 35% better than any survival results ever attained for the routine culture of Loligo spp. squid. Results suggest that high survival can be achieved by: (1) rearing hatchlings in a recirculating system consisting of small round tanks designed to maintain water quality and pH within narrow limits (8.1–8.4), (2) maintaining low current speed (1.0–1.4 cm s–1) to reduce skin damage and to enhance hatchling–prey interactions, (3) increasing feeding rate by feeding small amounts of food at regular intervals (every 2–3 h) during day time hours and keeping prey densities above 50 prey l–1, (4) feeding hatchlings with enriched Artemia nauplii during days 1–30 post-hatching and (5) feeding a variety of prey types and sizes to match the different sizes and hunting abilities of same-aged but heterogeneously developing hatchlings. The results from this study will enhance future culturing efforts for the commercially important loliginid squid.

Aerobic respiratory costs of swimming in the negatively buoyant brief squid Lolliguncula brevis.

Because of the inherent inefficiency of jet propulsion, squid are considered to be at a competitive disadvantage compared with fishes, which generally depend on forms of undulatory/oscillatory locomotion. Some squid, such as the brief squid Lolliguncula brevis, swim at low speeds in shallow-water complex environments, relying heavily on fin activity. Consequently, their swimming costs may be lower than those of the faster, more pelagic squid studied previously and competitive with those of ecologically relevant fishes. To examine aerobic respiratory swimming costs, O(2) consumption rates were measured for L. brevis of various sizes (2-9 cm dorsal mantle length, DML) swimming over a range of speeds (3-30 cm s(-1)) in swim tunnel respirometers, while their behavior was videotaped. Using kinematic data from swimming squid and force data from models, power curves were also generated. Many squid demonstrated partial (J-shaped) or full (U-shaped) parabolic patterns of O(2) consumption rate as a function of swimming speed, with O(2) consumption minima at 0.5-1.5 DML s(-1). Power curves derived from hydrodynamic data plotted as a function of swimming speed were also parabolic, with power minima at 1.2-1.7 DML s(-1). The parabolic relationship between O(2) consumption rate/power and speed, which is also found in aerial flyers such as birds, bats and insects but rarely in aquatic swimmers because of the difficulties associated with low-speed respirometry, is the result of the high cost of generating lift and maintaining stability at low speeds and overcoming drag at high speeds. L. brevis has a lower rate of O(2) consumption than the squid Illex illecebrosus and Loligo opalescens studied in swim tunnel respirometers and is energetically competitive (especially at O(2) consumption minima) with fishes, such as striped bass, mullet and flounder. Therefore, the results of this study indicate that, like aerial flyers, some negatively buoyant nekton have parabolic patterns of O(2) consumption rate/power as a function of speed and that certain shallow-water squid using considerable fin activity have swimming costs that are competitive with those of ecologically relevant fishes.

Microsatellites reveal high levels of gene flow among populations of the California squid Loligo opalescens.

Information on the extent of genetic differentiation among populations of the squid Loligo opalescens is crucial for the conservation of this commercially utilized species. We analysed six highly variable microsatellite loci in 11 collections of L. opalescens from different locations and spawning seasons to estimate the relative influence of two major evolutionary forces, gene flow and genetic drift. Microsatellite allele frequency patterns suggest that gene flow prevents population differentiation in L. opalescens. Tests for genetic differentiation showed homogeneity of the samples with an overall FST/RST of 0.0028/-0.0013. Genetic uniformity among samples from different year classes indicates that allele frequency patterns in L. opalescens are relatively stable over time. However, a more complete and detailed picture of fine-scale allele frequency shifts in this species will require a systematic microsatellite analysis of local populations over consecutive spawning cycles.

Mass spectrometric survey of peptides in cephalopods with an emphasis on the FMRFamide-related peptides.

A matrix-assisted laser desorption/ionization (MALDI) mass spectrometric (MS) survey of the major peptides in the stellar, fin and pallial nerves and the posterior chromatophore lobe of the cephalopods Sepia officinalis, Loligo opalescens and Dosidicus gigas has been performed. Although a large number of putative peptides are distinct among the three species, several molecular masses are conserved. In addition to peptides, characterization of the lipid content of the nerves is reported, and these lipid peaks account for many of the lower molecular masses observed. One conserved set of peaks corresponds to the FMRFamide-related peptides (FRPs). The Loligo opalescens FMRFa gene has been sequenced. It encodes a 331 amino acid residue prohormone that is processed into 14 FRPs, which are both predicted by the nucleotide sequence and confirmed by MALDI MS. The FRPs predicted by this gene (FMRFa, FLRFa/FIRFa and ALSGDAFLRFa) are observed in all three species, indicating that members of this peptide family are highly conserved across cephalopods.

The behaviour of Loligo opalescens (Mollusca: Cephalopoda) as observed by a remotely operated vehicle (ROV)

The behaviour of Loligo opalescens as observed by a remotely operated vehicle (ROV) was analysed. Thirty-nine behavioural components were identified and classed into four categories: chromatic, postural, locomotory, and inking. The frequency with which components were expressed was correlated to whether or not an individual was schooling, shoaling, alone with the ROV, or in the presence of other species. Behaviours observed were compared to those reported for other Loligo species. Observations of schooling and feeding behaviour, and reactions to other species are included.

Role of prey-capture experience in the development of the escape response in the squid Loligo opalescens: a physiological correlate in an identified neuron.

Although extensively used for biophysical studies, the squid giant axon system remains largely unexplored in regard to in vivo function and modulation in any biologically relevant context. Here we show that successful establishment of the recruitment pattern for the giant axon in the escape response elicited by a brief electrical stimulus depends on prey-capture experience early in life. Juvenile squid fed only slow-moving, easy-to-capture prey items (Artemia salina) develop deficits in coordinating activity in the giant axon system with that of a parallel set of non-giant motor axons during escape responses. These deficits are absent in cohorts fed fast-moving, challenging prey items (copepods). These results suggest that the acquisition of inhibitory control over the giant axon system is experience-dependent and that both prey-capture and escape behavior depend on this control.

Effects of temperature on escape jetting in the squid Loligo opalescens.

In Loligo opalescens, a sudden visual stimulus (flash) elicits a stereotyped, short-latency escape response that is controlled primarily by the giant axon system at 15 C. We used this startle response as an assay to examine the effects of acute temperature changes down to 6 C on behavioral and physiological aspects of escape jetting. In free-swimming squid, latency, distance traveled and peak velocity for single escape jets all increased as temperature decreased. In restrained squid, intra-mantle pressure transients during escape jets increased in latency, duration and amplitude at low temperature. Recordings of stellar nerve activity revealed repetitive firing of the giant motor axon accompanied by increased activity in the non-giant motor axons that run in parallel. Selective stimulation of giant and non-giant motor axons in isolated nerve-muscle preparations failed to show the effects seen in vivo, i.e. increased peak force and increased neural activity at low temperature. Taken together, these results suggest that L. opalescens is able to compensate escape jetting performance for the effects of acute temperature reduction. A major portion of this compensation appears to occur in the central nervous system and involves alterations in the recruitment pattern of both the giant and non-giant axon systems.

Highly Variable Microsatellites in the California Market Squid Loligo opalescens.

: Attempts to study the genetic population structure of cephalopods are impeded by the low levels of genetic variation in these species. We have developed polymerase chain reaction (PCR) primers for six hypervariable microsatellite markers in order to analyze the molecular population structure in the Californian market squid Loligo opalescens. Each of these genomic loci has been cloned and fully sequenced. Here we report the sequence and properties of the six PCR primer sets for the amplification of hypervariable microsatellites. Heterozygosity levels in six squid samples from different locations are high for all loci tested.

Bacterial Symbionts Colonize the Accessory Nidamental Gland of the Squid Loligo opalescens via Horizontal Transmission.

The accessory nidamental gland (AN gland), a reproductive organ of the mature female squid Loligo opalescens, harbors a dense culture of bacteria of unknown function. A multilayered sheath surrounding the L. opalescens egg case is similarly colonized by bacteria that presumably originate in the AN gland, as evidenced by their presence in the egg case at oviposition. This study investigates how these bacteria are transmitted to juvenile squid and examines some morphological consequences of bacterial colonization of AN gland tissues. By observing the structure of the AN gland in adults and the development and bacterial colonization of the gland in juveniles raised in captivity, we determined that the AN gland was absent in newly hatched squid and did not appear until 87 days post-hatching. At 129 days posthatching, the organ displayed tubules composed of a single layer of epithelial cells and expressing numerous cilia and microvilli. These tubules were not yet fully formed and thus were open to the mantle cavity and external seawater, possibly to aid in the acquisition of microorganisms. Since the AN gland developed a considerable time after hatching, it most likely acquires its symbionts horizontally from environmental seawater and not vertically from the egg case sheath. The switch from expression of cilia to production of microvilli on the epithelial cell surface may dictate the competence of the tissue for bacterial colonization. Electron microscopic examination of juvenile and adult AN glands revealed that an analogous process occurs during the development of the related light organ of other cephalopod species that harbor symbiotic bacteria.

A Family of Delayed Rectifier Kv1 cDNAs Showing Cell Type-Specific Expression in the Squid Stellate Ganglion/Giant Fiber Lobe Complex

Squid giant axons are formed by giant fiber lobe (GFL) neurons of the stellate ganglion (SG). Other large motoneurons in the SG form a parallel system. A small family of cDNAs (SqKv1A-D) encoding Kv1 alpha-subunits was identified in a squid (Loligo opalescens) SG/GFL library. Members have distinct 5' untranslated regions (UTRs) and initial coding regions, but beyond a certain point (nucleotide 34 of SqKv1A) only nine differences exist. 3' UTRs are identical. Predicted alpha-subunits are nearly identical, and only the N termini differ significantly, primarily in length. RNase protection assays that use RNA isolated from specific SG regions show that SqKv1A mRNA is expressed prominently in the GFL but not in the SG proper. SqKv1B yields the opposite pattern. SqKv1D also is expressed only in the SG. SqKv1C expression was not detectable. In situ hybridizations confirm these results and reveal that SqKv1B mRNA is abundant in many large neurons of the SG, whereas SqKv1D expression is limited to small isolated clusters of neurons. SqKv1A and B are thus the predominant Kv1 mRNAs in the SG/GFL complex. Activation properties of SqKv1A and B channels expressed in oocytes are very similar to one another and compare favorably with properties of native delayed rectifier channels in GFL neurons and large SG neurons. The Kv1 complement in these squid neurons thus seems to be relatively simple. Several differences exist between cloned and native channels, however, and may reflect differences in the cellular environments of oocytes and neurons.

Post-hatching development of circular mantle muscles in the squid Loligo opalescens.

Post-hatching development of the circular muscles in the mantle of squid was studied morphometrically to identify structural changes and to quantify hyperplasia and hypertrophy of the muscle fibers. Superficial, mitochondria-rich (SMR) fibers and central, mitochondria-poor (CMP) fibers are present at hatching. Although both fiber types increase in size and, even more so, in number during post-hatching development, CMP fibers increase at a much higher rate than do SMR fibers. As a result, the relative proportion of SMR to CMP fibers shifts from about 1:1 in a hatchling to about 1:6 in an 8-week-old animal; it then apparently remains constant to adulthood. These structural changes are consistent with developmental changes in muscular activity. During slow, jet-propelled swimming, 1-week-old animals show mantle contractions that have twice the relative amplitude and frequency of those in adults. The presence of Na-channel protein in mantle muscle was detected bio-chemically by using site-directed antibodies; the protein was found to be preferentially expressed in CMP fibers. These results suggest that SMR fibers are an important source of locomotory power at hatching, but become progressively less important during the first 8 weeks of development as CMP fibers assume the dominant role in jet locomotion.

Sightings and Strandings of Guadalupe Fur Seals in Central and Northern California, 1988-1995

The Guadalupe fur seal ( Arctocephalus townsendi ) was hunted to near extinction before its natural history was well known. The last known population is currently centered on Guadalupe Island, Mexico, but in recent years northern extralimital records from California have become more frequent. We report 14 new records (3 adults, 11 juveniles) of Guadalupe fur seals stranded (nine) or sighted (five) along the central and northern coast of California. These northern records appear to correspond with El Nino events, seasonal currents in California, and to dispersal behavior in this species. Dietary items retrieved from stomachs and feces included otoliths from Citharichthys sordidus, Lampanyctus, Protomyctophum , and Scopelogadus , and beaks of the squids Loligo opalescens, Gonatopsis , and Onychoteuthis borealojaponica . Emaciation commonly was associated with stranding, but other findings included an umbilical hernia, septicemia, and bacterial pneumonia. Three of the stranded individuals had experienced entanglement in fishing gear or marine debris.