Zalophus Californianus Research Articles

Quantifying animals' perception of environmental predictability using anticipatory behavior.

Animals under human care often experience predictable daily husbandry events, which can promote the development of anticipatory behavior. Previous research suggests even short delays in the arrival of a predictable, desired outcome can lead to negative welfare outcomes for animals. As such, providing reliable information to animals regarding the onset of important events may be a simple but useful method to support positive welfare. Here we evaluated the quantitative characteristics of anticipatory behavior of a California sea lion at the San Francisco Zoo in three situations (1) when the animal had accurate information about the occurrence of the event (temporally predictable training sessions), (2) when the information was semi-reliable (unscheduled training session), and (3) when a reliable signal was offered before unscheduled sessions. Results showed that providing a reliable cue resulted in a stronger temporal correlation of anticipation before the beginning of the unscheduled session, similar to the temporally predictable training session. However, providing a reliable cue did not reduce the intensity of the anticipatory behavior. We propose to take into account two aspects of the quantitative characteristics of anticipatory behavior: correlation with time until a desired event (correlation) and intensity, where the correlation indicates the ability of an individual animal to predict the occurrence of an event, and the intensity indicates the degree of sensitivity of the animal to reward. We discuss the implications for animal welfare and husbandry.

Quantifying the linkages between California sea lion (Zalophus californianus) strandings and particulate domoic acid concentrations at piers across Southern California

Domoic acid-producing blooms of the diatom genus Pseudo-nitzschia are pervasive in coastal environments globally. Domoic acid, a neurotoxin, accumulates via trophic transfer into marine food webs and is often associated with mass marine mammal mortality and stranding events. In Southern California, California sea lions (Zalophus californianus) are an indicator species for food web impacts of domoic acid because they are abundant secondary consumers, sensitive to domoic acid intoxication, and are actively monitored by stranding networks. However, domoic acid exposure may occur a distance from where a sea lion ultimately strands. This spatiotemporal variation complicates coupling domoic acid observations in water to strandings. Therefore, we sought to quantify whether monitoring data from four pier sites across the region, covering nearly 700 km of coastline from 2015-2019, could be used to predict adult and subadult sea lion strandings along the 68 km Orange County coastline surveyed by the Pacific Marine Mammal Center. We found that increased sea lion strandings were often observed just prior to an increase in particulate domoic acid at the piers, confirming that clusters of subadult and adult sea lion strandings with clinical signs of domoic acid intoxication serve as indicators of bloom events. In addition, domoic acid concentrations at Stearns Wharf, nearly 200 km from stranding locations, best predicted increased total sea lion strandings, and strandings of sea lions with domoic acid intoxication symptoms. Particulate domoic acid concentrations greater than 0.05 μg/L at Stearns Wharf were linked to stranding probabilities in Orange County ranging from 2.2% to 55% per week, and concentrations of 0.25 μg/L resulted in weekly stranding probabilities ranging from 16% to 81% depending on the stranding scenario modeled.

Molecular Detection and Characterization of Mycoplasma spp. in Marine Mammals, Brazil.

Mycoplasma spp. are wall-less bacteria able to infect mammals and are classified as hemotropic (hemoplasma) and nonhemotropic. In aquatic mammals, hemoplasma have been reported in California sea lions (Zalophus californianus) and river dolphins (Inia spp.). We investigated Mycoplasma spp. in blood samples of West Indian manatees (Trichechus manatus), pinnipeds (5 species), and marine cetaceans (18 species) that stranded or were undergoing rehabilitation in Brazil during 2002-2022. We detected Mycoplasma in blood of 18/130 (14.8%) cetaceans and 3/18 (16.6%) pinnipeds. All tested manatees were PCR-negative for Mycoplasma. Our findings indicate that >2 different hemoplasma species are circulating in cetaceans. The sequences from pinnipeds were similar to previously described sequences. We also detected a nonhemotropic Mycoplasma in 2 Franciscana dolphins (Pontoporia blainvillei) that might be associated with microscopic lesions. Because certain hemoplasmas can cause disease and death in immunosuppressed mammals, the bacteria could have conservation implications for already endangered aquatic mammals.

Osteofluorosis in free ranging California sea lions (Zalophus californianus)

We report the first case series of osteofluorosis in free ranging marine mammals and documentation of baseline bone fluoride concentrations in this population; however, the exact source is not known. A stranded subadult male California sea lion, one subadult male carcass, and one partial carcass, presumably adult male, demonstrated osseous (bony) proliferations on various appendicular and axial bones. The most severe lesions were from the index case with symmetrical segmental circumferential periosteal new bone proliferation on the diaphysis of both femurs and humeri. This case, and the second case, also had significant segmental periosteal new bone proliferation on the mandibles as well as increased tooth wear with dull enamel. Total fluoride concentrations in various bones of the cases ranged from 3,700 to 9,700 ppm dw, with a mean of 5,431 ppm dw, approximately twice the concentration in adult cattle with osteofluorosis. Ribs from four control California sea lions of various ages and both sexes had an average total fluoride of 1,575 ppm dw, which is three times as high as the bone fluoride concentration of normal adult cattle, but four times lower than the mean rib fluoride concentrations in the cases. This is the first report of osteofluorosis in free ranging marine mammals and documentation of baseline bone fluoride concentrations in this population. The exact source of the excessive fluoride levels is not known as male California sea lions have a large range and varied diet.

Fatal hepatic sarcocystosis in three captive and one free-ranging pinniped

Fatal hepatic sarcocystosis was diagnosed as the cause of death in four pinnipeds: two captive Hawaiian monk seals (Monachus schauinslandi), a captive, and a free-ranging California sea lion (Zalophus californianus). Based on necropsy, histopathology, electron microscopy and DNA sequencing, intralesional protozoal schizonts were determined to have caused the necrotizing hepatitis observed. Transmission Electron Microscopy (TEM) revealed schizonts similar to Sarcocystis canis in hepatocytes. PCR-DNA sequencing and phylogenetic analysis at the conserved 18S rRNA and variable ITS1 gene markers within the nuclear rRNA gene array from schizont-laden tissue established that the parasites were indistinguishable from Sarcocystis canis at the 18S rRNA locus. However, six distinct single nucleotide polymorphisms (SNPs) were resolved at ITS1 suggesting that the parasites infecting pinnipeds were distinct from S. canis, which commonly infects bears and dogs. We hypothesize that the parasite represents a novel Sarcocystis variant that we refer to as S. canis-like that infects pinnipeds. The definitive host of S. canis is enigmatic and its life cycle incomplete. These findings document a critical need to identify the life cycle(s), definitive host(s), and all susceptible marine and terrestrial intermediate hosts of S. canis and the S. canis-like variant infecting pinnipeds.

Mercury and selenium concentrations in lanugo of free-ranging California sea lions in the southern Gulf of California, Mexico

Total mercury ([THg]) and selenium ([TSe]) concentrations were determined in California sea lion (Zalophus californianus) lanugo from the Gulf of California in 2021 and 2022. Relationships with sex, morphometrics, and year were evaluated. Following toxicological thresholds of concern for piscivorous mammals, most pups had a [THg] < 10 ppm, one pup (2021) had a [THg] > 20 ppm, no pups had a [THg] > 30 ppm. Females had significantly higher [TSe] than males; sex did not influence [THg]. [THg] and [TSe] in 2022 were significantly higher in the general population and male cohorts compared to 2021. Significant negative correlations were observed between [THg], [TSe], and morphometrics (2021). These results indicate that, compared to other pinniped species, regional California sea lions may have a decreased likelihood of experiencing Hg-related adverse health effects. Year-related changes in element concentrations suggest continued monitoring of this population to assess pinniped, environmental, and potentially, human health.

Survival improvements of marine mammals in zoological institutions mirror historical advances in human longevity.

An intense public debate has fuelled governmental bans on marine mammals held in zoological institutions. The debate rests on the assumption that survival in zoological institutions has been and remains lower than in the wild, albeit the scientific evidence in support of this notion is equivocal. Here, we used statistical methods previously applied to assess historical improvements in human lifespan and data on 8864 individuals of four marine mammal species (harbour seal, Phoca vitulina; California sea lion, Zalophus californianus; polar bear, Ursus maritimus; common bottlenose dolphin, Tursiops truncatus) held in zoos from 1829 to 2020. We found that life expectancy increased up to 3.40 times, and first-year mortality declined up to 31%, during the last century in zoos. Moreover, the life expectancy of animals in zoos is currently 1.65-3.55 times longer than their wild counterparts. Like humans, these improvements have occurred concurrently with advances in management practices, crucial for population welfare. Science-based decisions will help effective legislative changes and ensure better implementation of animal care.

How otariids walk: a comparative axial analysis of the hind limb movements of California and South American sea lions

AbstractSeals exist at the intersection of land and water. This is especially true of eared seals (otariids), which are both highly adapted to forelimb swimming and retain the ability to walk on land. The precise nature and evolutionary history of their walking ability remains obscure, however. Here, we use axial analysis to compare the hind limb movements of California and South American sea lions with those of terrestrial plantigrades mammals. We show that, despite notable differences in foot orientation and joint position, all of our study species employ similar movements around the same centers of rotation. Our results suggest that otariid hind limbs and, in particular, the hallux play a substantial role in supporting and propelling the body during walking.

The symptomatology and diagnosis of domoic acid toxicosis in stranded California sea lions (Zalophus californianus): a review and evaluation of 20 years of cases to guide prognosis.

Domoic acid (DA) is a glutaminergic excitatory neurotoxin that causes the morbidity and mortality of California sea lions (Zalophus californianus; CSL) and other marine mammals due to a suite of effects mostly on the nervous and cardiac systems. Between 1998 and 2019, 11,737 live-stranded CSL were admitted to The Marine Mammal Center (TMMC; Sausalito, CA, USA), over 2,000 of which were intoxicated by DA. A plethora of clinical research has been performed over the past 20 years to characterize the range of toxic effects of DA exposure on CSLs, generating the largest dataset on the effects of natural exposure to this toxin in wildlife. In this study, we review published methods for diagnosing DA intoxication, clinical presentation, and treatment of DA-intoxicated CSL and present a practical, reproducible scoring system called the neuroscore (NS) to help assess whether a DA-affected CSL is fit for release to the wild following rehabilitation. Logistic regression models were used to assess the relationships between outcome (released vs. euthanized or died) and multiple variables to predict the outcome for a subset of 92 stranded CSLs. The largest proportion of DA-intoxicated CSLs was adult females (58.6%). The proportions of acute and chronic cases were 63.5 and 36.5% respectively, with 44% of affected CSL released and 56% either dying naturally or euthanized. The average time in rehabilitation was 15.9 days (range 0-169) for all outcomes. The best-performing model (85% accuracy; area under the curve = 0.90) assessing the relationship between outcome and predictor variables consisted of four variables: final NS, change in NS over time, whether the animal began eating in rehabilitation, and the state of nutrition on admission. Our results provide longitudinal information on the symptomatology of CSL intoxicated by domoic acid and suggest that a behavioral scoring system is a useful tool to assess the fitness for the release of DA-intoxicated CSL.

Maternal behavior of California sea lions in different abundance and tourist activity scenarios

Maternal behavior of California sea lions in different abundance and tourist activity scenarios

Comparison of de novo assembly using long-read shotgun metagenomic sequencing of viruses in fecal and serum samples from marine mammals.

Viral diseases of marine mammals are difficult to study, and this has led to a limited knowledge on emerging known and unknown viruses which are ongoing threats to animal health. Viruses are the leading cause of infectious disease-induced mass mortality events among marine mammals. In this study, we performed viral metagenomics in stool and serum samples from California sea lions (Zalophus californianus) and bottlenose dolphins (Tursiops truncates) using long-read nanopore sequencing. Two widely used long-read de novo assemblers, Canu and Metaflye, were evaluated to assemble viral metagenomic sequencing reads from marine mammals. Both Metaflye and Canu assembled similar viral contigs of vertebrates, such as Parvoviridae, and Poxviridae. Metaflye assembled viral contigs that aligned with one viral family that was not reproduced by Canu, while Canu assembled viral contigs that aligned with seven viral families that was not reproduced by Metaflye. Only Canu assembled viral contigs from dolphin and sea lion fecal samples that matched both protein and nucleotide RefSeq viral databases using BLASTx and BLASTn for Anelloviridae, Parvoviridae and Circoviridae families. Viral contigs assembled with Canu aligned with torque teno viruses and anelloviruses from vertebrate hosts. Viruses associated with invertebrate hosts including densoviruses, Ambidensovirus, and various Circoviridae isolates were also aligned. Some of the invertebrate and vertebrate viruses reported here are known to potentially cause mortality events and/or disease in different seals, sea stars, fish, and bivalve species. Canu performed better by producing the most viral contigs as compared to Metaflye with assemblies aligning to both protein and nucleotide databases. This study suggests that marine mammals can be used as important sentinels to surveil marine viruses that can potentially cause diseases in vertebrate and invertebrate hosts.

Assessing of the use of proteins A, G, and chimeric protein AG to detect marine mammal immunoglobulins.

In recent years, there has been an increase in infectious diseases in marine mammals, including brucellosis, infections of morbillivirus, herpesvirus, and poxvirus. Several serological diagnostic methods, including enzyme-linked immunosorbent assays, immunofluorescence assays (ELISA), and western blotting, have been used to detect antibodies against pathogens in marine mammals. However, options for commercial secondary antibodies used to detect antibodies in marine mammals are limited; therefore, the use of proteins A, G, or chimeric protein AG may provide a suitable alternative. This study aimed to assess the use of proteins A, G, and chimeric protein AG to detect marine mammal immunoglobulins. Currently, there are no comparative studies on the use of proteins A, G, and chimeric protein AG for the detection of immunoglobulins in marine mammals. In this study, we used ten pinnipeds' species (Baikal seal, California sea lion, harbor seal, northern fur seal, ringed seal, South American fur seal, South American sea lion, spotted seal, Steller sea lion, and walrus) and five cetacean species (beluga whale, bottlenose dolphin, harbor porpoise, killer whale, and Pacific white-sided dolphin) and compare binding ability to proteins A, G, or chimeric protein AG by ELISA. The results revealed that the immunoglobulins from pinniped and cetacean species reacted more strongly to protein A than protein G. In addition, the immunoglobulins of pinnipeds and cetaceans showed a strong binding ability to chimeric protein AG. These results suggest that proteins A, G, and chimeric protein AG would be used to help further develop serological assays.

Underwater Sound Detection Thresholds (0.031-80 kHz) of Two California Sea Lions (Zalophus californianus) and a Revised Generic Audiogram for the Species

Unmasked behavioral audiograms of two California sea lions (Zalophus californianus), an adult female (F01) and a subadult male (M02), were recorded using narrow-band frequency-modulated hearing test signals. Signals had a duration of 1 s and center frequencies ranging from 0.031 to 80 kHz. Hearing thresholds were measured by varying test signal amplitude according to the up-down staircase method. The resulting underwater audiograms (50% detection thresholds) of the two sea lions were similar and showed the typical mammalian U-shape. Maximum hearing sensitivity (58 and 57 dB re 1 mPa) occurred at 11.3 kHz for F01 and at 8 kHz for M02, respectively. The range of best hearing (defined as &lt; 10 dB from the maximum sensitivity) was from 1 to 16 kHz (four octaves). The detection thresholds for hearing test signal frequencies 0.031, 0.040, and 0.050 kHz were lower than expected, possibly caused by a shift in perceptional modality from auditory to vibrotactile, or due to the difficulty in measuring accurate SPLs of such low frequencies in a pool. Measurements of particle motion deemed detection of these very low frequencies via the vibrissae unlikely. The present study extends the frequency range for which the hearing of California sea lions has been tested. Based on the two audiograms of the present study and audiograms reported by Reichmuth et al. (2013) and Cunningham &amp; Reichmuth (2016), a revised generic audiogram for California sea lions is proposed.

Disentanglement and multi‐year survival of a free‐ranging California sea lion (Zalophus californianus) with an upper airway stoma secondary to fishing net entanglement

AbstractCalifornia sea lions (Zalophus californianus) are susceptible to entanglement in fishing gear and marine debris. Over time, entanglement material can become deeply embedded and disrupt underlying tissue layers, including skin, blubber, muscle, and regional structures. In the neck, chronic circumferential entanglement can result in airway laceration. We present a case study of an adult female California sea lion with an upper airway stoma secondary to chronic monofilament fishing net entanglement. The animal was disentangled in a remote field setting without access to surgical and rehabilitation facilities, and was released without additional treatment. Satellite telemetry data from the 5 months following disentanglement revealed movements comparable to those of other adult female California sea lions. Subsequent visual sightings ('resights') documented a minimum 2‐year survival following disentanglement.

Bacterial dysbiosis and epithelial status of the California sea lion (Zalophus californianus) in the Gulf of California.

Despite the high incidence of urogenital carcinoma (UGC) in California sea lions stranded along California, no UGC has been reported in other areas of their distribution; however, cell morphologies typical of premalignant states have been found. Risk factors for UGC include high of organochlorines and infection with a gammaherpesvirus, OtHV-1, but the importance of the bacteriome for epithelial status remains unknown. We characterized the genital bacteriome of adult female California sea lions along their distribution in the Gulf of California and examined whether the diversity and abundance of the bacteriome varied spatially, whether there were detectable differences in the bacteriome between healthy and altered epithelia, and whether the bacteriome was different in California sea lions infected with OtHV-1 or papillomavirus. We detected 2270 ASVs in the genital samples, of which 35 met the criteria for inclusion in the core bacteriome. Fusobacteriia and Clostridia were present in all samples, at high abundances, and Actinobacteria, Alphaproteobacteria, and Campylobacteria were also well-represented. Alpha diversity and abundance of the California sea lion genital bacteriome varied geographically. The abundance of bacterial ASVs varied depending on the genital epithelial status and inflammation, with differences driven by classes Fusobacteriia, Clostridia, Campylobacteria and Alphaproteobacteria. Alpha diversity and abundance were lowest in samples in which OtHV-1 was detected, and highest those with papillomavirus. Our study is the first investigation of how the bacteriome is related to epithelial status in a wild marine species prone to developing cancer.

Auditory masking in odobenid and otariid carnivoresa).

As the only living species within the odobenid lineage of carnivores, walruses (Odobenus rosmarus) have no close relatives from which auditory information can be extrapolated. Sea lions and fur seals in the otariid lineage are the nearest evolutionary outgroup. To advance understanding of odobenid and otariid hearing, we conducted behavioral testing with two walruses and one California sea lion (Zalophus californianus). Detection thresholds for airborne sounds were measured from 0.08 to at least 16 kHz in ambient noise conditions and then re-measured in the presence of octave-band white masking noise. Walruses were more sensitive than the sea lion at lower frequencies and less sensitive at higher frequencies. Critical ratios for the walruses ranged from 20 dB at 0.2 kHz to 32 dB at 10 kHz, while critical ratios for the sea lion ranged from 16 dB at 0.2 kHz to 35 dB at 32 kHz. The masking values for these species are comparable to one another and to those of terrestrial carnivores, increasing by about 3 dB per octave with increasing frequency. Despite apparent differences in hearing range and sensitivity, odobenids and otariids have a similar ability to hear signals in noisy conditions.

Associations between urogenital carcinoma and DECA-BDE (BDE-209) among wild California Sea lions (Zalophus californianus) and Steller Sea lions (Eumetopias jubatus)

Urogenital carcinoma (UGC) is prevalent among California sea lions (Zalophus californianus), while less is known concerning UGC among Steller sea lions (Eumetopias jubatus). Our objective was to investigate associations between UGC and polybrominated diphenyl ethers (PBDEs) among both sea lion species. Twenty-nine California sea lions and 20 Steller sea lions were lethally removed from the Columbia River Basin, Oregon, USA between 2020 and 2021, under Section 120 of the Marine Mammal Protection Act. UGC was diagnosed through gross necropsy and histopathology. Forty PBDE congeners were analyzed in blubber, including BDE-209, a potential carcinogen. Twenty (69 %) California sea lions and one (5 %) Steller sea lion were diagnosed with UGC. All cases were identified as early stage UGC, aside from one California sea lion with more advanced stage UGC. Among California sea lions, associations between PBDEs and UGC were analyzed using logistic regression. In the adjusted model, BDE-209 (log2-transformed) was associated with increased odds of UGC [Odds Ratio (OR): 4.68, 95 % confidence interval: 1.04, 21.0, OR p-value = 0.044). This is the first study to report BDE-209 concentrations in sea lion blubber. The percentages of California and Steller sea lions diagnosed with UGC were higher than expected for wild (non-stranded) sea lions. Our results suggested blubber BDE-209 was potentially associated with UGC in California sea lions in the Columbia River Basin.

Input compensation of dolphin and sea lion auditory brainstem responses using frequency-modulated up-chirps.

Frequency-modulated "chirp" stimuli that offset cochlear dispersion (i.e., input compensation) have shown promise for increasing auditory brainstem response (ABR) amplitudes relative to traditional sound stimuli. To enhance ABR methods with marine mammal species known or suspected to have low ABR signal-to-noise ratios, the present study examined the effects of broadband chirp sweep rate and level on ABR amplitude in bottlenose dolphins and California sea lions. "Optimal" chirps were designed based on previous estimates of cochlear traveling wave speeds (using high-pass subtractive masking methods) in these species. Optimal chirps increased ABR peak amplitudes by compensating for cochlear dispersion; however, chirps with similar (or higher) frequency-modulation rates produced comparable results. The optimal chirps generally increased ABR amplitudes relative to noisebursts as threshold was approached, although this was more obvious when sound pressure level was used to equate stimulus levels (as opposed to total energy). Chirps provided progressively less ABR amplitude gain (relative to noisebursts) as stimulus level increased and produced smaller ABRs at the highest levels tested in dolphins. Although it was previously hypothesized that chirps would provide larger gains in sea lions than dolphins-due to the lower traveling wave speed in the former-no such pattern was observed.

Metal-specific biomagnification and trophic dilution in the coastal foodweb of the California sea lion (Zalophus californianus) off Bahía Magdalena, Mexico: The role of the benthic-pelagic foodweb in the trophic transfer of trace and toxic metals

Trace metals concentrations along with stable isotopes ratios were measured in marine algae, sea grass, sponges, echinoderms, mollusks, crustaceans, fishes, and the California sea lion, to assess the bioaccumulation potential and detect potential risks for top predators off Bahia Magdalena, Mexico. We assessed the trophic magnification factor (TMF) to determine the potential for biomagnification of 11 trace metals. The concentrations of Fe and Zn were one order of magnitude higher than all other metals. Concentrations of As, Cu, Cd, Co, Cr, Fe, Mn and Ni correlated negatively with trophic level, supporting trophic dilution (TMF < 1, p > 0.05), while Zn and Hg had significant trophic magnification (TMF > 1, p < 0.05) when assessing only the benthic-pelagic foodweb. This research provides a baseline concentration of metals in multiple species, metal-specific foodweb bioaccumulation and biomagnification of mercury, underscoring the key role of the macrobenthic community as biovectors for trophic transfer of Hg through the foodweb to the California sea lion.

A multi-predator trophic database for the California Current Large Marine Ecosystem

The California Current Trophic Database (CCTD) was developed at NOAA Southwest Fisheries Science Center in collaboration with numerous diet data contributors. We compiled the CCTD from twenty-four data sets, representing both systematic collections and directed trophic studies. Diet composition data, including stomach and scat samples, were obtained from 105,694 individual predators among 143 taxa collected throughout the California Current Large Marine Ecosystem (CCLME) from 1967–2019. Predator taxa consist of squids (n = 5), elasmobranchs (n = 13), bony fishes (n = 118), and marine mammals (n = 7). Extensive time series are available for some predators (e.g., California Sea Lion, Pacific Hake, Chinook Salmon). The CCTD represents the largest compilation of raw trophic data within the CCLME, allowing for more refined analyses and modeling studies within this region. Our intention is to further augment and periodically update the dataset as additional historical or contemporary data become available to increase its utility and impact.