Carnivorous Gastropods Research Articles

Ingestion of paralytic shellfish toxins in a carnivorous gastropod (Chorus giganteus): effects on their elemental composition and reproductive traits

The producer of paralytic shellfish toxin (PST), Alexandrium catenella, is one of the main generators of HABs in the coasts of Chile. Its presence produces ecological and economic damage, directly affecting filter-feeding organisms, and indirectly to other organism through the trophic chain. The objective of this research was to identify the effect of a toxic diet on the energetic and reproductive parameters of the carnivorous snail Chorus giganteus. Two groups of snails were used, one fed with toxic prey (bivalves fed with A. catenella), and the other fed with non-toxic prey. Both treatments were maintained under these conditions for 63 days, then, elemental composition (C, N) and energy content were estimated, and fecundity parameters were analyzed. The results indicate that snails fed with toxic prey had a lower percentage of C and C/N ratio. The energy content was significantly lower in intoxicated snails. Regarding fecundity parameters, a higher number of egg-masses were produced by toxic snails, however, only 62% of these showed embryonic development, with 57% hatching success. A negative relationship was identified between the mean PST concentration, quantified in snails, and the number of egg-masses produced per aquarium. In the aquarium where the snails had highest average PST concentration (1200 ± 820 μg STX.2HCL eq. Kg−1) there was no oviposition, while egg-masses were only produced by snails in aquaria where the average concentration did not exceed 360 ± 160 μg STX.2HCL eq. Kg−1. It is likely that, with low levels of accumulated PST, C. giganteus activates its oviposition process as a response to toxin-induced stress, generating a higher energy expenditure supported by a redirection of its reserves. However, when the intoxication presents higher levels, the reproductive process could be inhibited, similar to what has been identified in other molluscs.

Respiratory paralysis in a patient with myasthenia gravis after ingestion of marine carnivorous gastropods: A case report.

The salivary glands of marine carnivorous gastropods contain tetramines, which usually cause mild symptoms of poisoning. However, these symptoms may be fatal in rare cases. A 58-year-old woman with a history of myasthenia gravis complained of dyspnea after consuming marine carnivorous gastropods with intact salivary glands. Upon arrival at the hospital, her blood gas analysis revealed type II respiratory failure with a pCO2 of 154 mmHg. Tracheal intubation was immediately performed. Her respiratory condition improved the following day, and she therefore could be weaned off the ventilator. Tetramine poisoning can be fatal for patients with certain underlying medical conditions.

Labral tooth loss in the carnivorous gastropod Acanthina monodon: Recovery capacity and incidence in the feeding process

The temporary loss of an animal feeding structure can often be replaced by a new one. During that replacement period, however, the animal can be limited in its ability to feed. The muricid gastropod Acanthina monodon can sometimes lose its labral tooth naturally; recovering the tooth will typically take between 14 and 21 days. Our studies show that the volume, length and area of the recovered tooth are equal to or greater than the characteristics of the original tooth. However, the recovered teeth were seen to grow differently and have different shapes than those of the original teeth. Moreover, less force was required to break the newly formed teeth, to an extent based on the shape of the new tooth. Although the toothless snails continued to feed in our study, the absence of the labral tooth had a negative impact on the size of attacked prey, although not on the number of prey attacked. Thus, the ingestion rate was lower in specimens with recovered teeth than in snails with the original intact teeth. Snails that lost the labral tooth also displayed alterations in the feeding process, including lower energy income and potential energetic repercussions, at least during the recovery period of the lost structure.

Chromosome-level genome assembly of the caenogastropod snail Rapana venosa

The carnivorous gastropod Rapana venosa (Valenciennes, 1846) is one of the most notorious ecological invaders worldwide. Here, we present the first high-quality chromosome-scale reference R. venosa genome obtained via PacBio sequencing, Illumina paired-end sequencing, and high-throughput chromosome conformation capture scaffolding. The assembled genome has a size of 2.30 Gb, with a scaffold N50 length of 64.63 Mb, and is anchored to 35 chromosomes. It contains 29,649 protein-coding genes, 77.22% of which were functionally annotated. Given its high heterozygosity (1.41%) and large proportion of repeat sequences (57.72%), it is one of the most complex genome assemblies. This chromosome-level genome assembly of R. venosa is an important resource for understanding molluscan evolutionary adaption and provides a genetic basis for its biological invasion control.

Influence of abiotic and biotic factors on benthic marine community composition, structure and stability: a multidisciplinary approach to molluscan assemblages from the Miocene of northern Germany

AbstractThe Miocene mica‐clay deposits of Groß Pampau (northern Germany) are well known for their diverse assemblages of marine mammals. Despite numerous systematic and biostratigraphic studies, an in‐depth palaeoecological analysis of its molluscan assemblages and a comprehensive palaeoenvironmental reconstruction are lacking. Here, we integrate new faunal, sedimentological and geochemical data to reconstruct the marine palaeoecosystem of the Upper Miocene sedimentary succession of Groß Pampau, and to identify the drivers controlling the composition, ecological structure and temporal dynamics of its macrobenthic molluscan assemblages. Fossil evidence, coupled with analyses of clay mineral composition, grain size distribution and geochemical data (total organic carbon, total nitrogen, δ13C, δ18O, δ15N of sediment and shells), suggests a warm–temperate, mesotrophic, low‐energy, offshore marine setting mostly below storm wave base and a pronounced surface‐to‐bottom water temperature gradient. Low variability in sedimentological and geochemical signals indicates generally stable physicochemical conditions, whereas the occurrence of the opportunistic species Varicorbula gibba suggests occasionally unfavourable bottom conditions, possibly related to transient hypoxia. Canonical correspondence analysis indicates that the distribution of molluscan assemblages correlates with total organic carbon and nitrogen content, suggesting organic matter availability at the sea floor as a controlling factor. A pattern of repetitive punctuated stasis of molluscan assemblages is defined by the temporal persistence in taxonomic and ecological composition, occasionally interrupted by shifts to a different faunal configuration. We suggest that both stable environmental conditions and biotic interactions (i.e. the top‐down control exerted by carnivorous gastropods and environmental modification by ubiquitous burrowing deposit feeders) probably contributed to the observed temporal stability.

First record of the exotic Indothais lacera (Gastropoda, Muricidae) in Brazil

Bioinvasions are one of the main causes of the decline of native biodiversity. Indothais lacera (Born, 1778) is a carnivorous gastropod, native to the Indo-Pacific. We present the first records of I. lacera on the Brazilian coast and the first record of this invasive species in the Western Atlantic. The specimens were found in two locations in the Baía de Todos os Santos, Bahia state, northeast of Brazil. Live specimens were collected in the Itapagipe Peninsula, in Ribeira, Salvador, and dry samples (empty shells) were collected in the extreme north of Itaparica Island. Molecular analyses indicate that there was more than one event of introduction of I. lacera in the bay and alert to the potential impacts that this species can have on the benthic community in the region. We suspect that this exotic species is affecting a native population of Thaisella, which was previously locally abundant but has since become rare.

Integrated mRNA and miRNA transcriptomic analysis reveals the response of Rapana venosa to the metamorphic inducer (juvenile oysters)

Metamorphosis, as a critical developmental event, controls the population dynamics of most marine invertebrates, especially some carnivorous gastropods that feed on bivalves, whose population dynamics not only affect the maintenance of the ecological balance but also impact the protection of bivalve resources; therefore, the metamorphosis of carnivorous gastropods deserve attention. Here, we investigated the mechanism underlying the response of the carnivorous gastropod Rapana venosa to its metamorphic inducer juvenile oysters through integrated analysis of miRNA and mRNA profiles. According to the results, we speculated that the AMPK signaling pathway may be the critical regulator in the response to juvenile oysters in R. venosa competent larvae. The NF-kB and JAK-STAT signaling pathways that regulated apoptosis were also activated by the metamorphic inducer, which may result in the degeneration of the velum. Additionally, the significant changes in the expression of the SARP-19 precursor gene and protein cibby homolog 1-like gene may indicate that these signaling pathways also regulate growth and development during metamorphosis. This study provides further evidence that juvenile oysters can induce metamorphosis of R. venosa at the transcriptional level, which expands our understanding of the metamorphosis mechanism in carnivorous gastropods.

테트라민 중독 사망사례 분석

Tetramethylammonium(TMA, tetramine) is a toxic quaternary ammonium compound, consisting of four methyl groups attached to a central nitrogen atom. TMA has been detected in a number of marine organism that are eaten by humans. In the past, most cases of TMA intoxication have occurred through eating seafood containing TMA, such as carnivorous gastropods. Nowadays, TMA hydroxide(TMAH) that decomposes to produce TMA is used widely in the manufacture of semiconductors and liquid crystal displays (LCDs). As a result, the case of TMA intoxication is increasing. TMA acts directly on nicotinic and muscarinic receptors that are responsible for depolarization and, at high doses, blockage of depolarization. TMA may cause nausea, vomiting, headache, impaired vision, temporary blindness, salivation, lacrimation, fasciculation and convulsion and motor paralysis. The symptoms of TMA intoxication generally are mild and transient because of rapid elimination of TMA from the body. However, in severe cases, paralysis of the respiratory muscles can occur and this causes death. In this study, we analyzed TMA in femoral blood, heart blood and gastric contents of victim. The concentrations of TMA in femoral blood and heart blood were 7.95 mg/L and 13.1 mg/L, respectively. This case can be considered as a good reference when studying the relationship between TMA-induced death and blood concentration.

Chemical contamination in coastal areas alters shape, resistance and composition of carnivorous gastropod shells

Morphological, structural and compositional alterations in shells of molluscs have been proposed as putative biomarkers of chemical contamination in coastal zones. Despite this, few studies were carried out using top predator gastropods which tend to be more susceptible to contamination exposure. Thus, the present study assessed disturbances on shells of Stramonita brasiliensis considering compression resistance and organic and mineralogical matrix composition, related to morphometric alterations. Results showed reductions in compression resistance and organic matrix content associated with higher contaminated sites. In addition, a predominance of calcite polymorphs was seen in shells obtained in polluted areas. Such outputs were consistent with local contamination levels which may have induced the observed alterations. Thus, changes in mollusc shells showed good performance as potential biomarkers of coastal contamination, being probably observed in other species of carnivorous gastropods around the world.

Mollusc shell shape as pollution biomarkers: Which is the best biological model?

Alterations in mollusc shells have been proposed contamination biomarkers. We used geometric morphometrics analyses associated with analytical determinations of contaminants to select suitable biological models among species widely distributed on coastal zones. The study was carried out using Lottia subrugosa (herbivore limpet), Crassostrea brasiliana (filter-feeder bivalve), and Stramonita brasiliensis (carnivore gastropod) obtained along a marked contamination gradient at Santos Estuarine System (Brazil). L. subrugosa and S. brasiliensis presented distinct shapes along the gradient, while no significant differences in shell form were seen for C. brasiliana. Indeed, limpets and snails presented morphometric parameters consistent with measured contamination levels hazardous substances. Based on cross-validation models, the reliability of morphometric responses was over 75% for the herbivore and carnivore species. In addition, for S. brasiliensis, a 95.2% confidence was detected in most contaminated sites. Therefore, shell alterations on carnivorous gastropods should be further investigated, seeking to be effectively employed as pollution biomarkers.

Age and growth of one of the world's largest carnivorous gastropods, the Florida Horse Conch, Triplofusus giganteus (Kiener, 1840), a target of unregulated, intense harvest.

The Florida Horse Conch, Triplofusus giganteus, one of the largest marine gastropods in the world, has been intensely exploited by shell collectors, curio dealers, and commercial harvest for over a century and is now in decline. Effective management of horse conch populations requires better data on commercial and recreational harvest intensities but also on the species’ intrinsic capacity to recover. Here, we use stable oxygen and carbon isotope sclerochronology to investigate the horse conch’s life history, including its maximum life span, growth rates, age at first spawning, and number of lifetime spawning seasons. The largest two shells studied (460 and 475 mm linear shell length) grew for 13 and 11 years, respectively. Growth curves for these shells, extrapolated out to the length of the record size shell (606 mm linear shell length) predict a maximum age of just 16 years. Carbon isotopes and field photographs of spawning females suggest that females mature relatively late in life. However, the largest horse conchs remaining in the wild are also smaller and younger than those studied here. Thus, the largest females left in the wild could have few lifetime spawning events. High fecundity can buffer horse conchs from overfishing but only if females reach spawning age and reproductive-age females are protected. Our study highlights the usefulness of stable isotope sclerochronology for characterizing the life histories of molluscan species now too uncommon to study through traditional mark and recapture approaches.

Long-term effects of contrasting pCO2 levels on the scope for growth in the carnivorous gastropod Concholepas concholepas

We evaluated the effect of contrasting pCO2 levels: lower (390 μatm), moderate (700 μatm) and extreme (1000 μatm), on the scope for growth of the keystone snail Concholepas concholepas over an exposure period of 6 months. Juvenile snails were collected from rocky intertidal habitats and acclimated for 5 months to those pCO2 levels. Subsequently, three groups of snails were randomly taken (n = 7 for each treatment) and reared for an additional 1 month for each of the three pCO2 levels. Physiological traits related with energy gain and energy expenditure were quantified. The scope for growth index decreased significantly with increases in pCO2, yielding negative values throughout the experimental period for the snails exposed to 1000 μatm pCO2, probably due to the extra energy required to maintain their metabolic functions in balance. This suggests that future climate change scenarios with elevated pCO2 levels could threaten the growth and other basic functions of juvenile snails of this species.

The significance of trophic transfer in the uptake of microplastics by carnivorous gastropod Reishia clavigera

The present study compared the relative significance of prey consumption and respiration as routes of microplastic (MP) intake in a carnivorous muricid gastropod, Reishia clavigera. The time-dependent accumulation of MPs within 14-day exposure and their removal through depuration were also investigated for two forms of MPs (fibre, fragment) at an environmentally relevant concentration (10 items L−1) and two higher concentrations (100 and 1000 items L−1). At 1000 items L−1, the number of MPs in R. clavigera on Day 14 was 1.8 ± 0.2 fibres individual−1 or 0.8 ± 0.3 fragments individual−1, equivalent to 64.6% of the fibres or 9.4% of the fragments retained by the variable mussel Brachidontes variabilis, a prey of R. clavigera. Consumption of B. variabilis was the most important route of MP intake in R. clavigera, although a small number of MPs were adhered to the gills during ventilation. Depuration in clean seawater without MPs was very effective in eliminating MPs in the body of R. clavigera but the possibility of long-term bioaccumulation of MPs could not be ruled out. The high percentage of MPs transferred from the prey to predator indicates the potential of trophic transfer as a significant route of uptake for MPs in higher predators.

Tetramine Contents in the Salivary Glands from 16 Species of Marine Carnivorous Gastropods Collected along Japanese Coasts

Tetramine (tetramethyl ammonium ion), a neurotoxin, is present at high levels in the salivary glands of buccinid gastropods and is responsible for human intoxication due to consumption of the gastropods. We used LC-MS/MS to examine the tetramine contents of salivary glands from 16 species of carnivorous gastropods collected along Japanese coasts. Tetramine was detected in all specimens except for Babylonia japonica. High levels of tetramine were detected in whelks, Neptunea lamellosa (1,380-9,410 μg/g of salivary gland) and N. purpurea (1,190-7,400 μg/g of salivary gland). Although consumption of N. lamellosa is well-known cause of foodborne tetramine poisoning, it was newly discovered that N. purpurea has tetramine. In addition, we found 7 other species of gastropods containing tetramine: Siphonalia cassidariaeformis (117-135 μg/g), S. fusoides (204 μg/g), Buccinum inclytum (2.94-3.40 μg/g), and B. aniwanum (0.700 μg/g) of the family Buccinidae, and Fusinus perplexus (397 μg/g), F. ferrugineus (105 μg/g), and F. forceps salisburyi (67.5 μg/g) of the family Fasciolariidae. The present study, together with previous studies, shows that gastropods with salivary glands containing more than 1,000 μg tetramine/g of salivary gland, including the genus Neptunea as well as Fusitriton oregonesis and Hemifusus tuba, carry a high risk of tetramine poisoning, and their salivary glands should be removed before consumption to prevent food poisoning.

Symbiotic microbiome and metabolism profiles reveal the effects of induction by oysters on the metamorphosis of the carnivorous gastropod Rapana venosa

Most marine mollusks have a pelagic larval phase, and they need to undergo metamorphosis to develop into adults. Metamorphosis is affected by many factors, including abiotic factors such as temperature, salinity and illumination as well as biological factors such as food and microorganisms. In our previous study, we found that the metamorphosis of Rapana venosa requires induction by juvenile oysters, which are the food source of R. venosa. However, the regulatory mechanism of this induction is largely unknown. In the present study, we evaluated the impacts of induction by juvenile oysters on competent larvae of R. venosa. Competent larvae were experimentally divided into two pools, and scallop shells without juvenile oysters and scallop shells with juvenile oysters were added for 2 h and 12 h to monitor alterations in critical gene expression, symbiotic microbiota and metabolomic responses. The carboxypeptidase gene was increased while the cellulase gene was decreased, which may mean that the food habit transition was induced by juvenile oysters. Meanwhile, critical genes in the neuroendocrine system were also significantly altered in juvenile oysters. Furthermore, dramatic changes in the symbiotic microbiota and metabolism profiles were observed, with many of them associated with the digestive system and neuroendocrine system. In conclusion, juveniles as food resources may induce metamorphosis in R. venosa by regulating the neuroendocrine system and promoting the development of the digestive system and changes in digestive enzymes. This study may provide evidence that induction by juvenile oysters can promote food habit transition and metamorphosis in R. venosa by regulating the metabolome and microbiome and further altering the digestive and neuroendocrine systems of R. venosa, which expands our understanding of the regulatory mechanism of metamorphosis in R. venosa. However, further studies are needed to explore the specific substance inducing metamorphosis released by juvenile oysters.

Ontogenetic Shifts of Predatory Strategies by the Carnivorous Gastropod Acanthina monodon (Pallas, 1774)

Predatory strategies used by carnivorous gastropods may change during their ontogeny. In muricid gastropods attack mechanisms include an accessory boring organ (ABO), radula, labral tooth and/or pedal muscle. However, these mechanisms and their patterns of use in relation to the ontogeny of the carnivorous gastropod remain uncertain. We studied the occurrence of shifts in predatory strategies through the ontogeny of the gastropod Acanthina monodon preying on the mytilid Perumytilus purpuratus. Our results showed a direct relationship between predator and prey size. During attack, the small-sized snails (up to 18 mm shell length, SL) used exclusively the ABO, and medium-sized snails (18–20 mm SL) shifted to using the radula for rasping shells. Meanwhile, the largest-sized snails (> 20 mm SL) used the radula, but also occasionally the pedal muscle and labral tooth, to attack their prey. The site selectivity on the mytilid shell varied according to predatory mechanisms used. The small-sized gastropods used the ABO to drill the center of the prey valves, whereas mid-sized and large-sized snails used the radula and the labral tooth on the valve edges. Occasionally, large-sized snails also used ABO. Shifts in predatory strategies and attacked areas are influenced by the development and consolidation of structures involved in the attack as predator size increased. The incorporation of trace elements during rachidian teeth growth may enable major resistance to friction against carbonate prey valves, as well as the appearance and development of the labral tooth, play relevant roles in the predatory mechanism shifts, which allows the consumption of larger prey. These patterns described evidences the gastropod's predatory behaviour in terms of energetic gain while minimizing the risk of the predator itself being preyed on.

The Characteristic of Critical Genes in Neuroendocrine System and Their Regulation on Food Habit Transition and Metamorphosis of Veined Rapa Whelk Rapana venosa (Valenciennes, 1846)

Metamorphosis is a critical developmental event in mollusks, and neuroendocrine system plays an essential role in this process. Rapana venosa is an economically important shellfish in China, but the artificial technology of R. venosa aquaculture is limited by metamorphosis. As a carnivorous gastropod, food habit transition makes the mechanism of R. venosa metamorphosis more complex. To investigate the changes in the neuroendocrine system and to reveal its role in regulating the food habit transition and metamorphosis of R. venosa, we cloned the cDNA sequences encoding 5-hydroxytryptamine receptor (Rv-5HTR), nitric oxide synthetase (Rv-NOS) and cholecystokinin receptor (Rv-CCKR), and investigated their expression by quantitative real-time PCR analysis, and explore the spatio-temporal changes of 5-HT protein expression using Immunohistochemical (IHC) analysis. The expression of the three geens was significantly increased in the early intramembrane veliger stage, which indicates that the three genes are related to the development of digestive system. Additionally, expression of the three genes was decreased after metamorphosis, while Rv-NOS and Rv-CCKR were increasingly expressed in competent larvae, which may help the larvae find suitable environments and promote digestive system development for metamorphosis, and the result of 5-HT IHC analysis also reflects the development of neuroendocrine system. Furthermore, results show that CCK can effect the expression of digestive enzyme, NOS and 5-HT receptor. Finally, based on the present results, we hypothesized that CCK and CCK receptor may be critical regulatory factors of food habit transition and metamorphosis. These results might provide information on the development of neuroendocrine system of R. venosa, and new insight into the regulation of the food habit transition and metamorphosis of gastropods.

A review of extantTudivasumRosenberg & Petit, 1987 (Neogastropoda: Turbinellidae) and description of three new species from Western Australia

ABSTRACTTudivasum Rosenberg & Petit, 1987 is a morphologically distinct gastropod genus of low diversity. All but one species are known from Australia and they occur from the intertidal zone down to hundreds of metres on the continental shelf. These carnivorous gastropods are thought to have intracapsular development. The six currently recognized extant species are reviewed here and their geographical ranges clarified. Two new species, Tudivasum chaneyi n. sp. and T. ashmorense n. sp., are described from Ashmore Reef, Western Australia, and are characterized by differences in protoconch colour and shell sculpture. The third new species, T. westrale n. sp., is described from the mid-west coast of Western Australia, where it has long been misidentified as T. spinosum (H. Adams & A. Adams, 1864). We generated a molecular phylogeny based on mitochondrial DNA sequence data to test morphological species concepts and reconstruct relationships among four of the described species. High levels of divergence within one of the new species could indicate an additional cryptic species.

Temporal variations in the bioenergetic reserves of Concholepas concholepas (Gastropoda: Muricidae) in contrasting coastal environments from the Humboldt current system

Changes in environmental conditions play an important role in essential biological processes such as reproduction, which is partially driven by an organism's diet. Here, we evaluate spatio-temporal variations in the bioenergetic reserves (lipids and fatty acids) of the fishery resource Concholepas concholepas (Loco), a prominent benthic carnivorous gastropod. We used data from summer (January) and winter (July) from two coastal localities that shown contrasting environmental conditions in central Chile (Quintay and Las Cruces). The results indicate that there is a correlation between the fatty acid profiles and the interactions between seasonality and locality. This was particularly evident among the fatty acid concentrations of docosahexaenoic (DHA, C22:6n-3), eicosapentaenoic (EPA, C20:5n-3) and arachidonic (ARA, C20:4n-6) acids, which were high in winter, in both localities. Contrastingly, palmitic (C16:0) and stearic (C18:0) acids were present among all comparisons at stable concentrations. These findings suggest an influence of environmental conditions on the availability and quality of the prey of C. concholepas, in both localities. Moreover, the high concentration of essential fatty acids during winter, could suggest an adaptive physiological response, to ensure reproductive success. This knowledge is indispensable to improve regulatory measures for the extraction periods of marine resources, towards a more sustainable fishery, in the Humboldt Current System.

Food web biomagnification of the neurotoxin β-N-methylamino-L-alanine in a diatom-dominated marine ecosystem in China

The neurotoxin β-N-methylamino-L-alanine (BMAA) reported in some cyanobacteria and eukaryote microalgae is a cause of concern due to its potential risk of human neurodegenerative diseases. Here, BMAA distribution in phytoplankton, zooplankton, and other marine organisms was investigated in Jiaozhou Bay, China, a diatom-dominated marine ecosystem, during four seasons in 2019. Results showed that BMAA was biomagnified in the food web from phytoplankton to higher trophic levels. Trophic magnification factors (TMFs) for zooplankton, bivalve mollusks, carnivorous crustaceans and carnivorous gastropod mollusks were ca. 4.58, 30.1, 42.5, and 74.4, respectively. Putative identification of β-amino-N-methylalanine (BAMA), an isomer of BMAA, was frequently detected in phytoplankton samples. A total of 56 diatom strains of the genera Pseudo-nitzschia, Thalassiosira, Chaetoceros, Planktoniella, and Minidiscus isolated from the Chinese coast were cultured in the laboratory, among which 21 strains contained BMAA mainly in precipitated bound form at toxin concentrations ranging from 0.11 to 3.95 µg/g dry weight. Only 2,4-diaminobutyric acid (DAB) but not BMAA or BAMA was detected in seven species of bacteria isolated from the gut of gastropod Neverita didyma, suggesting that this benthic vector of BMAA may have accumulated this compound via trophic transfer.