Larval parasite gene sequence data reveal cryptic trophic links in life cycles of porbeagle shark tapeworms

Randhawa, Haseeb S.; Brickle, Paul

doi:10.3354/meps09108

Cited by 23 publications

(25 citation statements)

References 40 publications

(60 reference statements)

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“…4 , Supplementary Table 1 ). In the 28S D2 rDNA analysis, the merocercoid from the fur seal, the delphini- and grimaldii-type merocercoids and the LP plerocercoids group in one clade with adults of the two Clistobothrium species C. montaukensis and C. carcharodoni as shown previously by several authors ( Agusti et al, 2005a ; Aznar et al, 2007 ; Jensen and Bullard, 2010 ; Randhawa, 2011 ; Randhawa and Brickle, 2011 ). This assignment to Clistobothrium was also verified using the near complete 18S rRNA gene for analysis, although with a smaller number of available taxa.…”

Section: Resultssupporting

confidence: 78%

“…Furthermore, sequence identity of more than 99.8% was also found between plerocercoids from the squid Doryteuthis gahi and Clistobothrium cf. montaukensis from porbeagle sharks ( Randhawa and Brickle, 2011 ), plerocercoids from the squid Illex coindetii (KT148970), deep sea oarfish Regalecus glesne (KM272991) and C. montaukensis from shortfin mako sharks (AF286957; Kuris et al, 2015 ) suggesting transmission of tapeworms between these species. Both cetaceans and pinnipeds represent a preferred prey of large sharks ( Long and Jones, 1996 ; Heithaus, 2001 ).…”

Section: Introductionmentioning

confidence: 99%

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Subcutaneous merocercoids of Clistobothrium sp. in two Cape fur seals (Arctocephalus pusillus pusillus)

Klotz¹,

Hirzmann

Bauer

et al. 2018

International Journal for Parasitology: Parasites and Wildlife

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Fur seals represent intermediate hosts of the cestode Clistobothrium. Large sharks are definitive hosts for these parasites. Two female, 25– and 27-year-old fur seals, caught in the 1980s at the South African coast, were examined pathomorphologically. Both animals showed multifocal, up to 1 cm in diameter large cavities of the thoracic and abdominal subcutaneous adipose tissue containing intraluminal metacestodes of tapeworms, which were surrounded by a locally extensive, pyogranulomatous panniculitis. The metacestodes (merocercoids) of one fur seal were isolated from the subcutaneous adipose tissue and characterized morphologically and for the first time from this host by molecular techniques. The morphometric data corresponded with ‘delphini'-morphotype merocercoids, but the sequence of the partial 28S ribosomal RNA gene identified them as conspecific with merocercoids of the morphotype ‘grimaldii’. These merocercoid types are morphologically Type XV metacestodes of marine tapeworms and represent different species of Clistobothrium. Sequence data were generated for 18S, ITS1, 5.8S, ITS2, partial 28S ribosomal DNA and partial mitochondrial cox1 gene and phylogenetic analysis of 18S rRNA and partial 28S rRNA genes identified the fur seal merocercoids as Clistobothrium species. However, it cannot yet be assigned to species level because of limited molecular data from adult stages. Most likely, both fur seals were infected as juveniles in their original habitat, the coastal regions of South Africa. The metacestode infection is probably an incidental finding, however, there is a chronic inflammatory reaction next to the subcutaneous merocercoids. It is noteworthy, that the merocercoids remain in a potentially infective stage even after more than 20 years.

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Section: Resultssupporting

confidence: 78%

Section: Introductionmentioning

confidence: 99%

Subcutaneous merocercoids of Clistobothrium sp. in two Cape fur seals (Arctocephalus pusillus pusillus)

Klotz¹,

Hirzmann

Bauer

et al. 2018

International Journal for Parasitology: Parasites and Wildlife

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“…fi shing down the food chain (Pauly et al 1998(Pauly et al , 2000, although this is not without exception (Essington et al 2006, Branch et al 2010, Wilen and Wilen 2012. In marine ecosystems, despite body size being a weak predictor of trophic level at the species level (Jennings et al 2001), larger individuals in a community feed at a higher trophic level (Sheldon et al 1972, Randhawa andBrickle 2011). Consequently, largerbodied sharks were likely encountered earlier than smaller sharks occupying lower trophic levels, consistent with our result that body size is a predictor of year of discovery.…”

Section: Discussionsupporting

confidence: 85%

“…Furthermore, as fi sheries now exploit depths surpassing the maxima recorded for sharks, there are no depth refugia remaining (Priede et al 2006). In marine ecosystems, despite body size being a weak predictor of trophic level at the species level (Jennings et al 2001), larger individuals in a community feed at a higher trophic level (Sheldon et al 1972, Randhawa andBrickle 2011). For instance, three species described in 2008 inhabit shallow coastal waters at depth Ͻ 20 m: Hemiscyllium galei , Orectolobus reticulatus , and Glyphis garricki .…”

Section: Discussionmentioning

confidence: 99%

Increasing rate of species discovery in sharks coincides with sharp population declines: implications for biodiversity

2014

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The global biodiversity of some taxonomic groups is poorly described, but thought to be decreasing rapidly. Surprisingly, this holds for a group of the world's most iconic large‐bodied animals: sharks. Our analysis shows rapid and steep contemporary population declines in sharks coinciding with an increasing rate in species discovery. Larger sharks occupying lower trophic positions with wide geographic distributions (latitudinal ranges) found in shallow waters tend to be discovered first. In light of this increasing trend in species discovery and a cumulative description record far from reaching an asymptote, models cannot predict the global number of sharks. Our results highlight that while our knowledge of shark diversity improves at an accelerating rate, this diversity is under threat and declining rapidly; most shark species are vulnerable to declines, especially smaller‐bodied sharks. This surprising finding may relate to mesopredator declines following periods of rapid expansion due to the demise of large sharks (apex predators). Furthermore, shark population declines are structured by phylogeny and, to a lesser extent, geography. Decline in sharks are likely to influence other species as well, e.g. via trophic cascades. The net result may be a greater loss of biodiversity in the oceans and could potentially explain why fewer extinction events are observed than predicted by models. Likewise, it is not inconceivable that species may be lost prior to their discovery.

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“…Despite having records of prey for the shark species examined here, the parasites of these prey items are generally unknown, and it remains uncertain whether these prey are actually intermediate hosts contributing to shark tapeworm richness. Indeed, a number of studies have pointed out that there are major gaps in our knowledge of the life cycles of elasmobranch tapeworms (Palm 2004, Jensen & Bullard 2010, Randhawa & Brickle 2011, Caira & Jensen 2014). These life cycles will need to be elucidated for a more in-depth understanding of the influence of diet breadth on tapeworm diversity.…”

Section: Discussionmentioning

confidence: 99%

Host diet influences parasite diversity: a case study looking at tapeworm diversity among sharks

Rasmussen¹,

Randhawa²

2018

Mar. Ecol. Prog. Ser.

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In theory, animal diets may act as important filters for different parasite species. However, there is currently a lack of empirical research looking at host diet as a potential predictor of parasite diversity among different host species. The aim of this study was to assess the influence of several host diet features (including diet breadth, diet composition, and trophic level) on tapeworm diversity in sharks, relative to other key factors, including host size, habitat, phylogeny, latitude, and depth. Data on these host features were compiled from a comprehensive analysis of literature records including 91 different shark species, and 3 measures of tapeworm diversity were examined: tapeworm species richness, tapeworm taxonomic distinctness (TD), and variance in tapeworm TD. The diet breadth of a shark species was revealed to be a better predictor of tapeworm species richness than other host features examined to date. Host size, trophic level, diet TD, latitudinal range, and the mid-point of a shark's depth range also significantly influenced tapeworm richness when analyses were ad justed to prevent confounding by phylogenetic re lation ships between hosts. The TD of tapeworm assemblages was influenced by diet breadth, diet TD, host size, and depth range when analysed independently of host phylogeny. Overall, our findings demonstrate that aspects of host diet have important consequences for parasite diversity in sharks. We em phasise that studies of parasite diversity in other systems should more seriously consider including aspects of host diet (particularly diet breadth) as potential key predictors of parasite diversity.

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Larval parasite gene sequence data reveal cryptic trophic links in life cycles of porbeagle shark tapeworms

Cited by 23 publications

References 40 publications

Subcutaneous merocercoids of Clistobothrium sp. in two Cape fur seals (Arctocephalus pusillus pusillus)

Subcutaneous merocercoids of Clistobothrium sp. in two Cape fur seals (Arctocephalus pusillus pusillus)

Increasing rate of species discovery in sharks coincides with sharp population declines: implications for biodiversity

Host diet influences parasite diversity: a case study looking at tapeworm diversity among sharks

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