Two populations of the marine fish Porichthys notatus,one lacking in luciferin essential for bioluminescence

Porichthys notatus is a common benthic fish found along the Pacific coast of North America. It possesses more than 700 small dermal photophores on its head and trunk. When P. notatus collected in Monterey Bay, California, is injected subcutaneously with norepinephrine, the photophores emit a long-lasting luminescence that is readily visible to the dark-adapted eye. The light emission is due to the oxidation of luciferin (substrate) by molecular oxygen, catalyzed by luciferase. In contrast, P. notatus collected in Puget Sound, Washington, is nonluminous, even though the photophores do not differ ultrastructurally from those of the California fish. The inability of the Puget Sound fish to luminesce is due to lack of luciferin in its photophores. Luminescence capability, however, may be induced in the Puget Sound fish by the oral or intraperitoneal administration of a small amount of luciferin from the tiny luminescent marine ostracod crustacean, Vargula hilgendorfii, suggesting that the origin of luciferin in P. notatus may be from the diet. In this study, specimens of P. notatus were collected over the entire known range of the species, between November 1981 and September 1987, and the presence of luciferin in the photophores determined. The results indicate that there are two populations of P. notatus: a luciferin-deficient, nonluminescent population located north of northern California and a luciferin-containing, luminescent population extending south of Cape Mendocino, California, to Baja California, Mexico. At the northern end of the southern population, a mixture of luminescent and nonluminescent P. notatus was found.     

Disruptive counterillumination and its anti-predatory value in the plainfish midshipman Porichthys notatus

The plainfin midshipman Porichthys notatus Girard occurs in nearshore waters off the western coast of North America. We found that the ventrally directed photophores of juvenile laboratory-grown P. notatus function in counterillumination. Their bioluminescence matched downwelling light to obscure the silhouette as viewed from below. P. notatus did not obligatorily counterilluminate at all times in appropriate light. A hydrodynamic stimulus, in addition to appropriate downwelling light, was required to induce counterillumination. This is perhaps an adaptation to conserve its Vargula-type luciferin, which is obtained from its diet. The angular distribution of light produced by P. notatus approximated that typical of downwelling light in the ocean. There was a direct relationship between downwelling irradiance and the maximum intensity of P. notatus luminescence. Insufficient light was produced to replace the light blocked by the fish under lighting conditions typical of the natural environment. The luminescence was, however, effective in eliminating the silhouette of P. notatus as observed with an image-intensifying camera and by dark-adapted human observers. Consequently, the effectiveness of counterillumination probably originates in part from the disruptive pattern of the luminous photophores. P. notatus from the Puget Sound population, which lacks a luciferin source and is non-luminous, displayed counterillumination behavior when its luminescent system was activated by force-feeding the fish with dried Vargula hilgendorfi. Experiments using adult P. notatus as predators on a mixed population of non-luminous (Puget Sound) and luminous (Santa Barbara Channel) juvenile P. notatus revealed that under conditions of dim overhead illumination non-luminous P. notatus were preyed upon at twice the rate of luminous individuals. This is the first experimental evidence suggesting that counterillumination is effective as an anti-predatory strategy. Received: 25 August 1998 / Accepted: 25 March 1999     

Photopigment and spectral sensitivity in the bioluminescent fish Porichthys notatus

Digitonin extracts from retinas of the marine fish Porichthys notatus, from California and Puget Sound (USA), contain a single photopigment with maximum absorbance at 498 nm. In the presence of hydroxylamine the final product of bleaching absorbs maximally at 367 nm, indicating that the photopigment is based on retinal. Spectral sensitivity measurements performed on intact eyes and eye-cup preparations in darkadapted and selectively light-adapted states yield curves which suggest that the retina of P. notatus contains at least 3 different types of receptors. In the darkadapted state, the spectral sensitivity curve has a broad peak, with a maximum between 480 and 500 nm. In the blue and red light-adapted states, in addition to depressing the sensitivity, the shape of the sensitivity curve also changes. Under these conditions new peaks appear which suggest the presence of at least two different types of cones, with sensitivity maxima in the blue and the green regions of the spectrum, respectively. Comparison of the spectral sensitivity curves with the in vivo bioluminescence emission spectrum of the fish gives an especially good correspondence and suggests that the fish is able to perceive the bioluminescence of its own species.     

Dinoflagellate luminescence increases susceptibility of zooplankton to teleost predation

The burglar alarm theory of bioluminescence was investigated by determining predation rates of a nocturnal teleost predator,Porichthys notatus, on nonluminescent kelp mysids illuminated by dinoflagellate flashes, between the fall and spring of 1989/1990. Mysids (Holmesimysis costata) were placed in aquaria containing varying concentrations (0 to 40 cells/ml) of the dinoflagellatePyrocystis fusiformis and a single midshipman fish. Controls usedP. fusiformis during their luminescence-inhibited day phase. Mysid swimming movements readily stimulated dinoflagellate luminescence. Flashes and prey strikes were observed simultaneously by image-intensifying and infrared video cameras on a splitscreen monitor. Predation rates increased at dinoflagellate concentrations of 3 to 15 cells/ml and decreased below controls at levels>20 cells/ml. Videotape analysis showed that at low concentrations (2 to 5 cells/ml), strike success rates exceeded 75% if prey were previously illuminated by a flash, but dropped below 50% at higher cell densities. Increased predation was attributed to luminescence revealing prey position. The decrease at higher concentrations was considered to be due to greater flash frequency providing a more diffuse and confusing target. The study demonstrates the effects of secondary luminescence on zooplankton predation at normally encountered dinoflagellate concentrations.     

Ecological gradients and relative abundance of native (Mytilus trossulus) and invasive (Mytilus galloprovincialis) blue mussels in the California hybrid zone

Marine communities are experiencing unprecedented rates of species homogenization due to the increasing success of invasive species, but little is known about the mechanisms that allow a species to invade and persist in a new habitat. In central California, native (Mytilus trossulus Gould 1850) and invasive (Mytilus galloprovincialis Lamarck 1819) blue mussels and their hybrids co-exist, providing an opportunity to analyze the mechanisms that determine the distributions of these taxa. Spatial and temporal variation in temperature and salinity and the relative frequencies of these mussel taxa were examined between 2000 and 2004 at four sites in San Francisco Bay and four in Monterey Bay, which were chosen for their different positions along inferred estuarine/oceanic gradients in the hybrid zone. Mussels were genetically identified as the parent species or hybrids by amplifying regions of two species-specific loci: the adhesive byssal thread protein (Glu-5′) and the internal transcribed spacer region of ribosomal DNA (ITS 1). The proportion of M. trossulus at the eight hybrid zone sites correlated negatively with average salinity (R ²=0.60) and positively with maximal temperature (R ²≥0.72), a somewhat unexpected result given what is known about the phylogeography of this species. The proportion of M. galloprovincialis showed the opposite pattern. The proportion of hybrids was correlated neither with habitat temperature nor salinity. Genotypes of mussel populations at an additional 13 sites from Coos Bay, Oregon (latitude 43.35°N) to Long Beach, California (latitude 33.72°N), sampled at various intervals between 2000 and 2004, were also determined. This survey confirmed previous reports that the hybrid zone lies between Monterey and the Cape Mendocino region (latitudes 36.63°N–40.5°N). Within Monterey and San Francisco Bays, however, the temporal comparisons (1990s vs. 2000s) revealed abrupt changes in the proportions of the two parent species and their hybrids on annual and decadal time scales. These changes indicate that the blue mussel populations are in a highly dynamic state. The survey also showed that, regardless of habitat, M. trossulus is consistently of smaller average size than either M. galloprovincialis or hybrids.

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Hybridization between the blue mussels Mytilus galloprovincialis and M. trossulus along the Pacific coast of North America: evidence for limited introgression

Two species of blue mussel, Mytilus galloprovincialis and M. trossulus, co-occur and hybridize along the Pacific coast of North America. Using a set of polymerase chain-reaction (PCR)-based genetic markers which diagnostically identify these species, we show that they are sympatric from the Cape Mendocino region to the Monterey Peninsula in northern and central California, USA. Mussels with hybrid genotypes were detected in all populations sampled in the region of sympatry, and the frequency of hybrid genotypes in individual hybrid populations ranged from 13 to 44%. Significant frequencies of first-generation backcross genotypes were detected in two individual hybrid zone populations (Berkeley and Monterey Marina) and in the hybrid zone as a whole, indicating that the potential exists for introgression between M. galloprovincialis and M. trossulus. Despite this potential, we found no evidence of advanced introgression beyond first-generation backcrosses, suggesting that gene flow between M. galloprovincialis and M. trossulus has been quite limited. The frequency of mussels with M. trossulus and hybrid genotypes declined abruptly south of Monterey Peninsula, while the frequency of mussels with M. galloprovincialis and hybrid genotypes declined precipitously north of Cape Mendocino. These abrupt genetic discontinuities indicate that this blue mussel hybrid zone is presently positioned between two prominent coastal features and there is little, if any, export of alleles from the hybrid zone into bordering parental populations. Received: 20 August 1997 / Accepted: 26 October 1998     

Introduction and spread of Philine auriformis (Gastropoda: Opisthobranchia) from New Zealand to San Francisco Bay and Bodega Harbor

Specimens of Philine auriformis have been observed in the southern portion of San Francisco Bay, California, since summer 1992. Specimens from Bodega Harbor were first discovered from intertidal mudflats in April 1994 and probably represent the spread of the San Francisco Bay population to a neighboring estuary. Their numbers have increased steadily and the species is now well established in both estuaries. Examination of the anatomy of specimens collected from California was compared with that described from New Zealand. No significant differences in anatomy were detected in animals from these different localities. It is suggested that the species was introduced into California waters by release of ballast water from international shipping.     

PCR-based detection of mtDNA haplotypes of native and invading mussels on the northeastern Pacific coast: latitudinal pattern of invasion

Frequencies of mitochondrial haplotypes characteristic of native Mytilus trossulus and introduced M. galloprovincialis were determined in populations along the west coast of North America from San Diego, California, to the Aleutian Islands, Alaska. We also identified the haplotypes of mussels cultured from larvae arriving in Coos Bay, Oregon, during 1988–1990 from sites in Japan in the seawater ballast of ocean-going ships. All mussels from ballast-water samples were M. galloprovincialis. We found that sampled populations north of San Francisco Bay, including Coos Bay, were entirely composed of mussels with the M. trossulus haplotype, while haplotypes of both species were present in all sites in and south of San Francisco Bay. The presence of M. trossulus in southern sites is contrary to evidence from allozyme studies, and we suggest that mtDNA introgression from M. trossulus to M. galloprovincialis may explain this discordance. This study demonstrates that, despite continued transport and release, M. galloprovincialis has not become established in northern sites. Failure to invade the north coast of North America may reflect environmental unsuitability for M. galloprovincialis. However, invasion success may be probabilistic, and the continuing release of M. galloprovincialis larvae may foreshadow a future successful invasion.     

Allozyme and morphological evidence for a newly introduced species of Aurelia in San Francisco Bay,California

The jellyfish Aurelia aurita (Linnaeus, 1758) is usually considered to be a cosmopolitan species. Aurelia sp. medusae observed at Foster City, San Francisco Bay, California, USA, since 1988 are morphologically distinct from Aurelia sp. collected 200 km away in Monterey Bay, but are morphologically similar to aquarium-cultured Aurelia sp. from Japan. They differ consistently in radial canal morphology. In allozyme electrophoresis, significant differences at 12 of 14 polymorphic loci strongly suggest that Aurelia sp. from Foster City and Tokyo Bay belong to one species, while Aurelia sp. from Monterey Bay and Vancouver Island belong to a second species. We propose that Aurelia sp. at Foster City is a recent introduction, possibly from Japan via ships' ballast water. The identities and taxonomic affinities of the two Aurelia defined in this study, and their relationships with the Linnaen A. aurita described from the North Atlantic, will require genetic and morphological study of the currently recognized species A. aurita and A. limbata (Brandt, 1838) from several zoogeographical provinces.     

Genetic affinities of the bivalve Macoma balthica from the Pacific coast of North America: evidence for recent introduction and historical distribution

The tellinid bivalve Macoma balthica (L.) has an extensive geographic range that reaches from temperate to arctic coastal waters in the North Atlantic and North Pacific oceans. Recent studies have indicated that eastern and western North Atlantic populations are morphologically and genetically different from one another, and that they may have diverged as sibling species. To determine the genetic relationship between M. balthica from the Pacific and Atlantic coasts of North America, populations from each coast were examined at 11 enzyme loci using standard starch gel electrophoresis. Allele frequency data indicate that M. balthica populations from San Francisco Bay, California appear more closely related to western North Atlantic populations than to populations from Oregon. We suggest that San Francisco Bay populations were introduced relatively recently from western North Atlantic populations. The Oregon populations are probably a natural extension of northern populations that occur along Northern Asia and in the eastern North Atlantic.     

Genetic heterogeneity in a single year-class from a panmictic population of adult blue rockfish (<Emphasis Type="Italic">Sebastes mystinus</Emphasis>)

We used microsatellite genetic markers to investigate adult population structure and the formation of a new year-class in Sebastes mystinus (blue rockfish). Since S. mystinus may live as long as 45 years and reach reproductive age at approximately 5 years, the adult population may contain as many as eight generations of reproductive adults. We investigated whether the juveniles of the 2000 year-class and the adult population were genetically homogeneous along the California coast. We sampled approximately 100 juveniles from three sites, two sites along the Monterey Peninsula (Carmel and Monterey) in central California and one at Fort Ross in northern California, and approximately 50 adult S. mystinus from five sites throughout the population center. The adult sampling spanned approximately 700 km from the northern Channel Islands to Fort Bragg. The juveniles showed significant heterogeneity in allele frequencies among distant locations and genetic homogeneity among adjacent locations. In contrast, the adults showed genetic homogeneity over large distances (San Miguel Island to Fort Bragg), indicating little limitation of gene flow in this region. Allele frequencies of juveniles differed from adult samples and in some cases reduced genetic diversity indicative of sweepstakes recruitment (small sample of the adult reproductive potential). The genetic structure of the 2000 year-class suggests that despite a genetically homogenous adult population, settled juveniles can be genetically heterogeneous along the California coast. The results also suggest that the adults, with several year-classes, are capable of maintaining a panmictic population despite the genetic distinctiveness of individual year-classes.     

Population interconnectivity and implications for recovery of a species of concern, the Pacific hake of Georgia Basin

To aid the recovery of a species, understanding the extent to which populations are connected is useful for targeting conservation efforts. Pacific hake within waters of Puget Sound, Washington State, USA, and Georgia Strait, British Columbia, Canada are listed as a species of concern under the U.S. Endangered Species Act due to dramatic declines in the Puget Sound population. To assess the role of dispersal in the recovery of Pacific hake, we sought to quantify patterns of connectivity between populations in Puget Sound and Georgia Strait. Using natural chemical markers from otoliths of fish sampled from these two populations, we linked natal signatures of fish to signatures of individuals from known spawning grounds. Results indicated that 82 % of individuals collected from Puget Sound (n = 78) were estimated to have originated there, while 40 and 92 % of the individuals collected from two cohorts within Georgia Strait (n = 9 and 24, respectively) had originated from Puget Sound. A trend of “population abandonment” of fish from Puget Sound suggests that recovery of this Pacific hake population will depend on local management practices.     

Introduction,dispersal and potential impacts of the green crab Carcinus maenas in San Francisco Bay,California

The North Atlantic portunid crab Carcinus maenas (Linnaeus, 1758) has invaded the North Pacific Ocean following more than two centuries of global dispersal due to human activities. C. maenas was first collected in San Francisco Bay, California, in 1989–1990, where its distribution and prey selectivity were investigated in 1992–1994. It has become abundant in shallow, warm lagoons (which as favorable and retentive microhabitats may have served as invasion incubators) and spread throughout the north, central and south bays. It may have arrived in ballast water, on fouled ships, amongst algae with imported live bait or lobsters, or by intentional release; genetic comparisons of the Bay population with possible source populations may aid in defining the transport mechanism. C. maenas' eurytopic nature, its high breeding potential, and its diet and feeding behavior suggest the potential for extensive ecosystem alterations through predator-prey interactions, competition, disturbance, and indirect effects. Although both negative economic impacts through reduction or disruption of fisheries and positive impacts of providing bait and human-food fisheries have been documented in a few regions, the potential economic impacts in San Francisco Bay remain largely unknown.     

Larval development of the crabCancer magister in temperature regimes simulating outer-coast and inland-water habitats

Postlarval megalopae of the Dungeness crabCancer magister inhabiting offshore coastal waters along the west toast of North America are larger and settle earlier than do those occupying the inland waters of the Puget Sound basin (Washington, USA, and British Columbia, Canada). The Puget Sound habitat is characterized by low initial temperatures that steadily increase during the course of zoeal development, while offshore temperatures are more moderate and stable. Larvae were raised in the laboratory from hatching to megalopa in three temperature treatments: (1) constant 10 °C (CO), (2) a regime that temporally simulated temperatures found off the central California coast during the larval season (CA); and (3) a regime simulating temperatures found within the Puget Sound basin (PS). Zoeal duration was 44% longer in the PS treatment than in the other two, at least partially accounting for observed differentes between outer-toast and inland-water settlement times. Although differentes were measured in megalopal weights and carapace lengths among treatments, results do not explain differences in megalopal size observed between outer-toast and inland-water individuals. Survival to megalopa was highest in the PS treatment, with the difference due to significantly lower mortality than in CO and CA treatments during the terminal zoeal stage. Daily instantaneous mortality rates were lower in the PS than in CO or CA treatments, indicating Chat extended larval duration will not necessarily result in reduced settlement success.     

Distribution of male and female mtDNA lineages in populations of blue mussels,Mytilus trossulus and M. galloprovincialis,along the Pacific coast of North America

Geographic variation in mitochondrial large subunit (16S) ribosomal RNA haplotypes was examined for blue mussels, Mytilus trossulus Gould, 1850 and M. galloprovincialis Lamarck, 1819, sampled from ten sites along the Pacific coast of the USA in January of 1993. Using polymerase chain reaction/restriction fragment length polymorphism (PCR/RFLP) assays we determined haplotype frequencies for both the male and female mussel mitochondrial DNA (mtDNA) lineages. Populations from Morro Bay south to San Diego, California, contained only M. galloprovincialis male and female haplotypes, while those from Arcata Bay, California, north to Port Orford, Oregon, were fixed for M. trossulus haplotypes. Populations from Monterey Bay to Bodega Bay, California, contained a mixture of M. trossulus and M. galloprovincialis haplotypes. Overall only 2 of 97 heteroplasmic individuals had a mixed M. trossulus/M. galloprovincialis mitochondrial genotype indicating that hybridization is uncommon in the populations sampled. Further, there was no evidence of extensive introgression between these mussel taxa at the level of mtDNA. This is in contrast to previously published results which suggested the significant introgression of M. trossulus haplotypes into southern populations containing primarily M. galloprovincialis nuclear genotypes. We feel the discrepancy lies in the ability of our assays to detect haplotypes corresponding to both the male and female mtDNA lineages. Potential explanations for the lack of mtDNA introgression include, low levels of backcrossing between hybrids and parental taxa, epistatic interaction between nuclear and mitochondrial genes and the breakdown of a sex-specific inheritance pattern for mtDNA in hybrids.     

Spread and potential impact of the recently introduced European green crab,Carcinus maenas,in central California

Our study examines the potential impact of the European green crab Carcinus maenas on communities of coastal embayments of western North America. We document the current distribution and range expansion of this species beyond San Francisco Bay, where C. maenas first became established along this coast in 1989–1990, and we test the effect of C. maenas predation on different species and sizes of infaunal invertebrates in field and laboratory experiments. In our samples from eight coastal locations in central California collected between June 1993 and May 1994, we found no green crabs at the two closest embayments south of San Francisco Bay and found the crabs in all four embayments sampled within 120 km north of San Francisco Bay, up to and including Bodega Harbor. C. maenas was not present in samples from sites farther north. This northward range expansion is apparently the result of larval recruitment by a single cohort, corresponding to the predominant northern transport of surface waters and the approximate distance water moves during larval green crab development. At Bodega Harbor, the current northern range limit, the C. maenas population is now well established and reproducing. Females and males became sexually mature within their first year at 40 mm carapace width, molting approximately monthly from summer through fall, and females were ovigerous in late fall of their first year at 50 mm. We expect larvae from this population to recruit locally and to the north, promoting episodic range extensions as new populations are established and reproduce. Enclosure experiments conducted during the summer of 1993 at the intertidal sandflats of Bodega Harbor showed that C. maenas significantly reduced densities of the most abundant taxa, including the bivalves Transennella confusa and T. tantilla, the cumacean Cumella vulgaris, and the amphipod Corophium sp. Furthermore, Carcinus maenas selectively removed larger (>3 mm) rather than smaller (<1 mm) Transennella spp. in both field and laboratory experiments. Based on the available data from this and other studies of green crabs, and our 10 yr study of community dynamics at Bodega Harbor, we predict C. maenas will significantly alter community structure, ecological interactions, and evolutionary processes in embayments of western North America.     

Zinc and cadmium in the Pacific hake Merluccius productus off the western U.S. coast

Concentrations of zinc and cadmium in muscle tissue or whole Pacific hake, Merluccius productus (Ayres), increase with increasing total wet weight, especially for smaller fish. These trends appear to be related to the euphausiid diet of hake. Except for the isolated population in Puget Sound, no relationship between zinc or cadmium concentration and collection site is apparent.     

Short-term changes in feeding and digestion by the copepodCalanus pacificus

The planktonic marine copepodCalanus pacificus exhibits an enhanced feeding rate, or hunger response, when exposed to food following short periods of starvation. In a scries of laboratory experiments with copepods collected from the main basin of Puget Sound, Washington, during 1982 and 1984, we measured maximum ingestion rate, assimilation efficiency, and digestive enzyme activity to determine the time scales over which the feeding behavior ofC. pacificus responds to increases in food. These laboratory results were then compared to field studies of diel fluctuations in digestive enzymes and gut fluorescence ofC. pacificus in Dabod Bay, a fjord of Puget Sound, during September, 1980, and the closely relatedC. marshallae off the Washington coast, in August, 1981. Laboratory experiments demonstrated that the hunger response ofC. pacificus lasts approximately 6 h before ingestion rate returns to a steady state level of about one-half maximum. On the order of 12h of starvation were required to induce the maximum ingestion rate of the hunger response. Digestive enzyme activities did not change over these time scales. Assimilation efficiency peaked within a few hours of the onset of feeding, with low initial rates possibly related to the period of starvation prior to feeding. These results were consistent with diel patterns observed in the field. The hunger response ofC. pacificus appears to be controlled by processes within the gut, and our results are discussed in relation to recent studies of the digestive processes of calanoid copepods.Contribution No. 1772 from the School of Oceanography, University of Washington, Seattle, Washington 98195, USA     

Genetic population structure of the recently introduced Asian clam,Potamocorbula amurensis,in San Francisco Bay

The genetic population structure of the recently introduced Asian clam, Potamocorbula amurensis, in San Francisco Bay was described using starch gel electrophoresis at eight presumptive loci. Specimens were taken from five environmentally distinct sites located throughout the bay. The population maintains a high degree of genetic variation, with a mean heterozygosity of 0.295, a mean polymorphism of 0.75, and an average of 3.70 alleles per locus. The population is genetically homogeneous, as evidenced from genetic distance values and F-statistics. However, heterogeneity of populations was indicated from a contingency chi-square test. Significant deviations from Hardy-Weinberg equilibrium and heterozygote deficiencies were found at the Lap-1 locus for all populations and at the Lap-2 locus for a single population. High levels of variability could represent a universal characteristic of invading species, the levels of variability in the source population(s), and/or the dynamics of the introduction. Lack of differentiation between subpopulations may be due to the immaturity of the San Francisco Bay population, the general purpose phenotype genetic strategy of the species, high rates of gene flow in the population, and/or the selective neutrality of the loci investigated.