Black Abalone Haliotis Cracherodii Research Articles

Dietary Patterns in Black Abalone Haliotis cracherodii Leach, 1814 as Indicated by Observation of Drift Algal and Seagrass Capture at San Nicolas Island, California, USA, 1982 to 2019

Black abalone Haliotis cracherodii Leach, 1814 are known to feed on drift plant macrodetritus moved about in the intertidal zone by waves and currents. Drift capture is a trait shared by at least several other abalone species. Drift materials are entrapped beneath the anterior foot and held for ingestion. The quantitative significance of feeding on entrapped drift macrodetritus for black abalone is unknown. Furthermore, there are no published data on the extent to which local and mesoscale spatial distributions of source plant populations influence the composition of drift plant material in black abalone diet as acquired by entrapment. From February 1982 through March 2019, occurrences of macrodetrital entrapment by black abalone were observed in nine rocky intertidal study plots, with a summed surface area of 2,054 m2, on the periphery of San Nicolas Island (SNI), California (Island centroid at ∼33.25°, –119.50°). A small preliminary survey and 27 complete surveys were performed during the study period (mean of ∼1.4 y between complete surveys). During the study, more than 1.5 × 105 black abalone were examined. The total likely included repeated observations of many individuals as a result of the known longevity and limited mobility of the species. Of those observed, ∼1.65 × 103 black abalone were recorded as apparently ingesting entrapped items. Frequency data were dominated (∼95% of all records) by three species of kelp Macrocystis pyrifera (Linnaeus) C. Agardh; commonly known as “giant kelp”, Egregia menziesii (Turner), and Eisenia arborea Areschoug. Of those, giant kelp was the most frequently observed entrapped category (∼76%). Living, attached giant kelp is rarely observed in intertidal habitats at SNI, and it follows that utilization of giant kelp by black abalone requires physical importation of the kelp from other locations. Frequencies of occurrence of giant kelp entrapment by individual study site were clearly associated with the relative surface canopy sizes and persistence patterns of offshore kelp forests adjacent (≤2 km) to the respective study sites. The pattern suggests that subsidies of drift giant kelp to black abalone diet involve mesoscale physical processes largely proximate to SNI but probably not subsidies from more distant locations such as other islands or the California mainland. Utilization of other frequently recorded kelps as food by black abalone likely involves spatial subsidies as well, but on smaller scales of distance (∼10–100 m for E. arborea; ∼0–100 m for E. menziesii). In the context of the imperiled status of black abalone, recovery actions may include outplants of captive-reared animals or transplantation of wild animals from other populations. For such actions, data from SNI suggest a need for consideration of scales of separation among release locations and nearby populations of the three apparently predominant kelp species in black abalone diet.

Hyperparasitism by the bacteriophage (Caudovirales) infecting Candidatus Xenohaliotis californiensis (Rickettsiales-like prokaryote) parasite of wild abalone Haliotis fulgens and Haliotis corrugata from the Peninsula of Baja California, Mexico

Candidatus Xenohaliotis californiensis (CXc) is a Rickettsiales-like prokaryote that is considered the causal agent of Withering Syndrome (WS), a chronic disease of abalone, from the west coast of North America and it is listed by the International Organization for Animal Health (OIE) as a reportable agent due to its pathogenicity. This bacterium in red abalone Haliotis rufescens, black abalone Haliotis cracherodii, and yellow abalone Haliotis corrugata from California, US and Baja California, Mexico has been found to be infected by a bacteriophage. To date, there is no information on the epizootiology of CXc and its bacteriophage in natural populations of abalone; furthermore, it is unknown if the bacteriophage was also present in CXc infecting blue abalone Haliotis fulgens. The objective of this study was to determine the distribution, prevalence and intensity of CXc, as well as to determine the distribution and prevalence of the bacteriophage and to study interactions between host sex and hyperparasitism in blue abalone and yellow abalone. Tissue samples were obtained from seven localities where the commercial capture of wild abalone is carried out. Samplings were conducted throughout the 2012–2013 capture seasons and a total of 182 blue abalone and 170 yellow abalone were obtained. The prevalence and intensity of CXc and the prevalence of the bacteriophage were determined by histology. The identity of CXc was confirmed by PCR, product sequence analysis and in situ hybridization while the identity of the bacteriophage was corroborated by TEM. The prevalence of CXc infected and uninfected by the bacteriophage was 80% in blue abalone and 62% in yellow abalone. Low infection intensities were found in 86% of blue abalone and 82% of yellow abalone. Infection intensity was significantly higher in undifferentiated yellow abalone. The bacteriophage in CXc showed a prevalence of 22% and 31% in blue abalone and yellow abalone respectively. These results show that CXc and its bacteriophage are widely distributed in the peninsula of Baja California and that they are well established in natural populations of blue abalone and yellow abalone. Additionally, this data constitutes the first record of a bacteriophage in blue abalone.

Recruitment failure and shifts in community structure following mass mortality limit recovery prospects of black abalone

Mass mortalities of species can fundamentally alter the structure of natural communi- ties, which can in turn negatively impact species' recovery. Beginning in 1994, some of the largest remaining populations of black abalone Haliotis cracherodii on the mainland coast of California, experienced mass mortalities due to the fatal disease called 'withering syndrome', which led to its listing as a species of concern by the USA National Marine Fisheries Service. We have been monitor- ing black abalone populations along the coast of southern and central California since 1992, and detection of withering syndrome at our southernmost site prompted us to investigate how the impending decline of this dominant grazer might correlate with changes in black abalone recruit- ment and the rocky intertidal community in which it lives. Quantitative surveys before and after mass mortalities revealed that, after black abalone declined, there was a shift in the composition of the intertidal species assemblage from one dominated by bare rock and crustose coralline algae (good quality abalone habitat) to one with increased cover of sessile invertebrates and sea urchins. Declines in abalone abundance were also correlated with a lack of recruitment to areas affected by withering syndrome, despite the presence of healthy adult populations only tens of kilometers away. This sug- gests that abalone recruitment might be limited by dispersal, a lack of quality habitat for settlement and early survival, or the continued presence of the disease agent. Recruitment failure and these dra- matic shifts in habitat quality indicate that the outlook for recovery of black abalone is poor.

Continued declines of black abalone along the coast of California: are mass mortalities related to El Niño events?

The intertidal black abalone Haliotis cracherodii has experienced mass mortalities along the coast of California, USA, since the mid-1980s. Mortality is due to infection by a pathogen that leads to a fatal wasting disease called 'withering syndrome', where the foot of the abalone atrophies until it can no longer adhere to the substratum. Massive die-offs due to withering syndrome were first noted on the Channel Islands in 1986, and by 1992 withering syndrome was observed near Point Conception on the mainland and was suspected to be spreading northward up the coast of California. The timing of the initial mass mortalities following the strong 1982 to 1983 El Nino and an isolated outbreak of withering syndrome in 1988 at Diablo Cove, north of Point Conception, following warm water dis- charge from a power plant, led to the hypothesis that the onset of mass mortalities due to withering syndrome may be triggered by elevated seawater temperatures. We surveyed black abalone popula- tions at 7 sites along the mainland coast of California (including 3 where withering syndrome was al- ready present) from 1992 to 2001, a period spanning 2 El Nino events, to determine whether (1) with- ering syndrome and associated declines of black abalone were spreading northward up the coast; and (2) these mass mortalities of black abalone could be related to elevated seawater temperatures during El Nino events. Mass mortalities of black abalone due to withering syndrome were observed at the 5 most southern sites (>90% decline in numbers in all size classes), but not at the 2 most northern sites, and there was a clear pattern of decline from south to north over time. Massive die-offs of abalone were not exclusively associated with times of elevated sea surface temperatures due to El Nino. Nev- ertheless, rapid declines of abalone at 2 sites coincided with the strong 1997 to 1998 El Nino, and de- clines during El Nino events were faster than those during non-El Nino years. Abalone at the 2 most northern sites, where only slight declines occurred during the 1997 to 1998 El Nino, may not have been infected by disease. It appears, therefore, that in the presence of the pathogen, warm water conditions associated with El Nino may accelerate the development of withering syndrome and the rate of decline of black abalone. Consequently, anthropogenic disturbances, such as discharges of heated water or global warming, may increase the incidence of this fatal disease.

Withering Syndrome in Farmed Red Abalone Haliotis rufescens: Thermal Induction and Association with a Gastrointestinal Rickettsiales-like Prokaryote.

Withering syndrome (WS) is a chronic wasting disease responsible for mass mortality in wild populations of black abalone Haliotis cracherodii. The etiology of WS is uncertain with limited evidence for the role of a gastrointestinal Rickettsiales-like prokaryote (RLP). We documented for the first time the occurrence of animals with clinical signs of WS and associated morphological changes in another haliotid species, the red abalone H. rufescens. In this study, 60 juvenile red abalone (8 cm) were randomly selected from a farmed population raised at 14°C that was known to have low-intensity RLP infections but lacked clinical signs of WS. The abalone were held in triplicate containers receiving water of approximately 14.7°C (Control, Co) or 18.5°C (elevated temperature, ET) and were fed equally for 220 d. Survival was 100% (30/30) for the Co group and 67% (20/30) for the ET group. The ET group animals had higher RLP infection intensities and showed more clinical signs (mantle retraction, lower weight gain, lower condition index) and morphological changes (digestive gland degeneration) associated with WS. In trials conducted immediately before termination of the experiment, ET group animals fed at half the rate of Co group animals. Among ET group animals, the intensity of RLP infections in the posterior portion of the esophagus was positively correlated with WS clinical signs and morphological changes, whereas no correlations were present among Co group animals. During 1997-1998 and in conjunction with elevated seawater temperatures associated with El Niño, several abalone farms in California experienced a dramatic increase in the proportion of red abalone showing signs of WS. Examination of 66 red abalone from five commercial farms revealed that animals with more advanced RLP infections had more severe WS clinical signs and associated morphological changes. Collectively, these data demonstrate that RLP infection plays a key role in the etiology of WS in red abalone and that warm water enhances the severity of the pathogenic effects of RLP infection.

Recent declines of black abalone Haliotis cracherodii on the mainland coast of central California

Recent declines of black abalone Haliotis cracherodii on the mainland coast of central California

Association of Prokaryotes with Symptomatic Appearance of Withering Syndrome in Black Abalone Haliotis cracherodii

Withering syndrome (WS) is an epizootic fatal wasting disease that is devastating California Channel Island populations of block abalone Haliotis cracherodii. Our studies suggest a strong pathogen-disease association. The pathogen is an intracellular prokaryote that infects epithelial cells lining the gut and enzyme secreting cells of the digestive diverticula. It multiplies by binary fission in round to oval, basophilic, membrane-bound colonies teeming in the cytoplasm. Infection of the digestive diverticula is accompanied by a complete loss of digestive enzyme granules and metaplasia of enzyme secretory cells to a morphology similar to epithelium lining the gut. Extensive infection of digestive diverticular cells and the resultant deficiency in digestive enzymes correlates to the degree of pedal muscle atrophy and the severity of signs associated with WS. Electron microscopically the intracellular pathogen is a rodshaped, ribosome-rich, gram-negative, prokaryote with a trilaminar cell wall consistent with the order Rickettsiales. Microbiological and protozoological methods produced no patterns that implicated other types of microbes. Chemical analysis of tissue from animals from a population with WS did not support an association between WS and environmental pollutant exposure to polycyclic aromatic hydrocarbons, polychlorinated biphenyls, or chlorinated pesticides.

Morphological variation along intertidal gradients in a population of black abalone Haliotis cracherodii Leach 1814

Temporal patterns of morphological variation in multivariate size and shape in a population of black abalone Haliotis cracherodii Leach 1814 in an intertidal boulder field in southern California was examined. From July 1983 to May 1985, 707 individuals were tagged and measured for six shell traits. The extent and pattern of morphological variation in allometric size, tremata (= respiratory pore) number, and relative tremata size was similar among surveys. Shore-level gradients in morphology varied temporally and involved independent variation in both shell size and shape. In the summer and fall, individuals with relatively fewer smaller tremata occurred higher on the shore than individuals with relatively more larger tremata. Seasonal variation in intertidal distribution and the incidence of Octopus-drilled abalone shells indicated that declines in abalone abundance were due to predation by Octopus in the summer and fall. Shore-level gradients were thus associated with opposing selective regimes, predation in the low intertidal and desiccation in the high intertidal. These results support the hypothesis that shore-level gradients in morphology result from movement and differential growth and are a dynamic response of individuals to temporal changes in physical stresses and predation which vary along intertidal gradients.

Stacking behavior of an intertidal abalone: an adaptive response or a consequence of space limitation?

Intertidal populations of black abalone Haliotis cracherodii Leach at Santa Cruz Island, California, vary in density among surge channels from < 1 to 126 abalone/m 2. Dense populations are characterized by high levels of intraspecific secondary substratum use (“stacking”) for attachment surfaces, though it is rare in low density areas. Use of shell surfaces by black abalone appears not to be an evolved adaptive strategy. Individuals in stacks fed significantly more than expected, yet solitary abalone next to stacks shared food trapped by stacks. In the laboratory, starvation did not increase the propensity of an abalone to stack. Stacks were equally common in the breeding and non-breeding seasons, suggesting that stacking behavior was not a mechanism to enhance reproductive success. Stacking did not enhance avoidance of predators or competitors. Laboratory experiments showed that stacking is density dependent and probably the result of limitation of primary attachment space. Removals of significant predators (sea otters and Chumash Indians) of adult abalone during the past two centuries probably led to increased densities of black abalone, which in turn has had an indirect effect on the prevalence of stacking.

Comparative biochemistry of Haliotis pigmentation: Unusual bilipeptides of Haliotis cracherodii

1. 1. The outer prismatic layer of the black abalone Haliotis cracherodii has been shown to contain two highly acidic bilipeptides, both with different bilin chromophores: 2. 2. The blue peptide (0.41 mg/g shell weight) has a mol. wt 5600, with approx 36% of the residues composed of aspartic acid and glycine in an approx 1:1 molar ratio. 3. 3. The green peptide (1.31 mg/g shell weight) has a mol. wt 5300, and contains approx 83% aspartic acid and glycine in a 3:2 molar ratio. 4. 4. These results are discussed in relation to the hypothesis that suggests that repeating sequences of the (Asp-Y) n type are involved in shell calcification.

Chromosomes of the black abalone (Haliotis cracherodii)

The chromosomes of the black abalone Haliotis cracherodii are described for the first time. The diploid number is 36, with no apparent sexual dimorphism.