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Crassicauda boopis in a fin whale (Balaenoptera physalus) ship-struck in the eastern North Atlantic Ocean

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On 9 November 2015, a juvenile male fin whale of 11·60 m length was observed on the bulb of a merchant vessel in the Channel Terneuzen – Ghent (The Netherlands – Belgium). A severe parasitosis was present in the right heart ventricle and caudal caval vein. Parasites were identified as Crassicauda boopis based on macroscopic and microscopic observations. The sequence of the 18S rRNA gene obtained from the parasite samples was 100% similar to the sequence of the 18S rRNA gene from Crassicauda magna available on GenBank. While adults of C. boopis and C. magna are morphologically distinct and found at different locations in the body, the molecular analysis of the 18S rRNA gene seems insufficient for reliable species identification. Although numerous C. boopis were found, the cause of death was identified as due to the collision with the ship, as suggested by the presence of a large haematoma, and the absence of evidence of renal failure. The young age of this whale and the absence of severe chronic reaction may suggest that the infestation was not yet at an advanced chronic stage.
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Crassicauda boopis in a n whale (Balaenoptera physalus)
ship-struck in the eastern North Atlantic Ocean
LAETITIA LEMPEREUR
1
*, MORGAN DELOBELLE
1
, MARJAN DOOM
2
,
JAN HAELTERS
3
, ETIENNE LEVY
4
, BERTRAND LOSSON
1
and THIERRY JAUNIAUX
4
1
Faculty of Veterinary Medicine,University of Liège,Center for Fundamental and Applied Research for Animal and
Health (FARAH),Laboratory of Parasitology and Parasitic Diseases,Quartier Vallée 2,Av de Cureghem,6 B43a-4000
Liège,Belgium
2
Faculty of Veterinary Medicine,Department of Morphology,University of Ghent,Salisbuylaan 133,9820 Merelbeke,
Belgium
3
Royal Belgian Institute of Natural Sciences,Operational Directorate Natural Environment,3de en 23ste
Linieregimentsplein,B-8400 Ostend,Belgium
4
Faculty of Veterinary Medicine,University of Liège,Center for Fundamental and Applied Research for Animal and
Health (FARAH),Pathology Unit,Quartier Vallée 2,Av de Cureghem,6 B43a-4000 Liège,Belgium
(Received 23 January 2017; revised 14 June 2017; accepted 14 June 2017)
SUMMARY
On 9 November 2015, a juvenile male n whale of 11·60 m length was observed on the bulb of a merchant vessel in the
Channel Terneuzen Ghent (The Netherlands Belgium). A severe parasitosis was present in the right heart ventricle
and caudal caval vein. Parasites were identied as Crassicauda boopis based on macroscopic and microscopic observations.
The sequence of the 18S rRNA gene obtained from the parasite samples was 100% similar to the sequence of the 18S rRNA
gene from Crassicauda magna available on GenBank. While adults of C. boopis and C. magna are morphologically distinct
and found at dierent locations in the body, the molecular analysis of the 18S rRNA gene seems insucient for reliable
species identication. Although numerous C. boopis were found, the cause of death was identied as due to the collision
with the ship, as suggested by the presence of a large haematoma, and the absence of evidence of renal failure. The
young age of this whale and the absence of severe chronic reaction may suggest that the infestation was not yet at an
advanced chronic stage.
Key words: Crassicauda boopis,n whale, kidney, caudal caval vein.
INTRODUCTION
The n whale (Balaenoptera physalus) is a marine
mammal belonging to the suborder of baleen
whales (Cetacea, Mysticeti). It is the second-largest
animal on earth after the blue whale (Balaenoptera
musculus). Although n whales are found in all
major oceans and a number of seas, from polar to
tropical waters, it is rare in the southern North
Sea, and in most cases solitary animals are seen
(Camphuysen and Peet, 2006). It feeds by
ltering a large volume of seawater, enabling to
harvest large zooplankton mainly Northern krill
(Meganyctiphanes norvegica) but also small schooling
sh such as herring (Clupea harengus), squid and
crustaceans including copepods (Lambertsen,
1986; Ruys and Soulier, 2013). Cetaceans serve as
hosts to numerous parasites, including many nema-
tode species such as crassicaudids (Nematoda,
Spirurida) (Lambertsen, 1986). Crassicauda spp.
occur under the skin or in deep tissues of the
mammary glands, in cranial sinuses and the urogeni-
tal system (Geraci and St. Aubin, 1987; Lambertsen,
1986; Zucca et al. 2004; Jabbar et al. 2015). Three
nominal species of adult Crassicauda have been
described in the urogenital system of the n whale,
namely C. crassicauda,C. boopis and C. pacica
(Lambertsen, 1985,1986). The former is the smal-
lest of the three, and occupies the lower urinary
tract (urethra), whereas the latter two infect the
kidneys and are considered as taxonomically syn-
onymous as morphologically indistinguishable
(Lambertsen, 1985).
Crassicauda boopis (Tetrameridae, Baylis, 1920) is
a round worm attaining a length of approximately
1·52 m. The parasite shows a large anterior part
(5 mm wide), which is often observed protruding
in the blood ow and an attenuated posterior
portion (1 mm wide) traversing the ureteric epithe-
lium and lying free within renal ducts. Larvated
eggs are observed and larvae can be found in urine
of infected animals (Rees, 1953; Lambertsen,
1985). Of several known crassicaudid infections,
those caused by C. boopis are highly pathogenic.
Infections with adult C. boopis can be associated
with a marked thrombophlebitis of the vascular
system draining the kidneys. The tissue reaction
* Corresponding author: Faculty of Veterinary Medicine,
Laboratory of Parasitology and Parasitic Diseases,
University of Liège, Quartier Vallée 2, Av de Cureghem,
6 B43a, 4000 Liège, Belgium. E-mail: llempereur@ulg.
ac.be
1
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can cause multiple obstructions of the primary renal
veins. The osmotic stress experienced by the whale
in its naturally saline environment is then aggravated
by a pathologic stress to the kidneys. Consequently,
severe infections with C. boopis could reduce blood
ow from the kidneys to such a level that the whale
succumbs to congestive renal failure. Moreover,
the nding of intravascular parasitic masses and
associated thrombi supports the possibility of a
thromboembolism in crassicaudiosis. This is espe-
cially true in case of pulmonary lesions with parasite
fragments and mineralized lesions (Lambertsen,
1992).
The life cycle of C. boopis is not entirely known
yet. It is largely hypothetical based on the pattern
of lesions observed, and the frequent report of het-
eroxenous transmission for marine Spirurida
(Lambertsen, 1986; Rhode, 2005). This suggests a
somatic migration of C. boopis larvae from the gut
after their ingestion by the whale. The primary
infective route is assumed to involve penetration of
the wall of the gastrointestinal tract by C. boopis
larvae that are ingested by the whale and migration
of these larvae up the mesenteric arteries and the
aorta (Lambertsen, 1986; Díaz-Delgado et al.
2016). Entry of C. boopis into the kidneys, its deni-
tive habitat, could well involve larval movements via
two dierent routes: from the aorta directly within
the wall of the arterial system or by the arterial
blood ow. Thereafter, the developing larvae
would have easy access to both the urinary ductwork
and the renal veins. Finally, by further developing in
the venous system of the kidney, the adult stage
could then extend from the urinary ducts to the
caval vein. Persistent larvae migrans are suggested
by lesions induced by developing C. boopis larvae
that are not carried by the arterial bloodstream to
the kidneys but rather lodge in the capillaries of
other tissues (Lambertsen, 1992).
The nding of larvae and larvated eggs in the
urine suggest that the primary portal of exit is the
urinary tract. The presence of eggs in the pulmonary
airspace is also compatible with low levels of shed-
ding via the whales blow (Lambertsen, 1986).
Krill, such as M. norvegica, which is the principal
prey of n whales in the northern Atlantic Ocean,
could potentially play a role as an intermediate
host (Lambertsen, 1985; Sigurjonsson and
Vikingsson, 1995; William et al. 2009).
The nding of young calves infected with C.
boopis suggests either a transplacental transmission
or the urinary contamination of the environment fol-
lowed by an oral infection of the calf before being
able to feed by itself. Finally, galactogenic transmis-
sion cannot entirely be disregarded (Díaz-Delgado
et al.2016).
This paper aims at describing a rarely reported
case of C. boopis in n whale and its molecular
screening for parasite identication improvement.
MATERIALS AND METHODS
On 9 November 2015, a n whale was observed on
the bulb of a vessel in the Channel Terneuzen
Ghent (The Netherlands Belgium). According to
the captain of the vessel, the whale had not been
present on the bulb 2 days prior to the observation
(Jan Haelters, personal communication). The ship
(204 m long, cruising speed of 1820 kts) had
sailed from Porto de Santos (Brazil) to Ghent in 12
days. The n whale was removed from the bulb in
the port of Ghent and transported to shore for nec-
ropsy (Fig. 1) following a standardized procedure
(Jauniaux et al. 2002).
Parasites from veins and kidneys were preserved
in 80% alcohol for morphological and molecular
identication. Cephalic and genital regions of the
parasite were microscopically investigated after
clearing in lactophenol. Renal tissue was preserved
in 10% buered formaline and embedded in
paran wax. Sections were stained with haematoxy-
lin and eosin for histopathological examination.
Molecular identication
Genomic DNA was isolated from 10 worms using
DNeasy Blood & tissue kit (Qiagen, Germany) fol-
lowing the manufacturers recommendations. The
18S rRNA gene was amplied from genomic DNA
by PCR using G18S4-F (5-GCTTGTCTCAA
AGATTAAGCC-3) and reverse 136-R (5TG
ATCCTTCTGCAGGTTCACCTAC-3) primers
(Nadler et al. 2007; Jabbar et al. 2015).
PCRs were conducted in 25 µL volumes con-
taining Taq polymerase master mix (Qiagen,
Germany). PCR cycling conditions were 94 °C for
5 min, then 35 cycles of 94 °C for 30 s, 55 °C
for 30 s and 72 °C for 80 s, followed by 72 °C for
7 min. Amplicons were observed on 2% agarose
gel. A PCR amplifying internal portion of the
18S rRNA gene was designed using primers
Crassic1160R (5-CAGGTGAGTTTTCCCGTG
TT-3) and reverse Crassic352F (5-AAACGGCT
ACCACATCCAAG-3) in order to facilitate the
sequencing. Examination of PCR amplicons was
done on a 2% agarose gel. PCR products were subse-
quently puried using MinElute PCR purication
kit (Qiagen, Germany) and subjected to automated
DNA sequencing in both directions (Giga genomic
platform, University of Liège). Sequences were
aligned using Clustal Omega (http://www.ebi.ac.
uk) and a consensus was submitted to Blastn
(http://blast.ncbi.nlm.nih.gov).
RESULTS
Clinical presentation and post-mortem ndings
The n whale was a juvenile male of 11·60 m length
showing a slight emaciation with a blubber thickness
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of 50 mm (dorsal), 35 mm (median) and 35 mm
(ventral) (Fig. 1). The eyes were clear, with a trans-
parent lens and the presence of gas bubbles, which
suggested, together with observation reported by
the captain, that the time of the death was about
23 days ago. External observations of the body
showed an impact zone with cutaneous lacerations
of about 1·65 m wide. When the abdominal cavity
was opened, an associated free haemorrhagic and
brinous liquid was present. An intestinal haema-
toma of 40 cm in length was observed at the
impact zone. A thrombus was observed in the right
lung and parasite fragments were present in the pul-
monary vessels (Fig. 2). A severe parasitosis was
present in the lumens of the right heart ventricle
and the caudal caval vein (Fig 2). These parasites
(approximately 50) were white to reddish round
worms of approximately 1 m long and 5 mm in
diameter. A renal thrombosis was also observed,
with the presence of round worms of 20 cm in
length and 1 mm in diameter (Fig. 2).
Microscopic observations
Several parasites found in the caudal caval vein were
observed microscopically. A cephalic extremity was
found on a large striated worm portion of 5 mm in
diameter with a tapering apex (Fig. 3). The head
was located at the very tip of this tapering section
and exhibited a constriction; the mouth bore two
lateral lips (Fig. 3). Worms found in the renal
veins showed a typical posterior extremity on an
attenuated worm section (1 mm in diameter). The
posterior extremity of female worms was distin-
guished by the presence of a constriction before a
rectangular end (Fig. 3). No male posterior extrem-
ity was observed. Larvated eggs measuring 50 µMin
length were found on the parasite cuticle (Fig. 4).
These observations allowed us to identify two frag-
ments most probably belonging to C. boopis.
Parasite fragments found in the lungs were not
preserved.
Microscopically, signicant lesions were located
in the kidneys. In the renal thrombosis, a nematode
with larvated eggs was observed in an arteriole
(Fig. 4). A subacute arteritis and periarteritis was
characterized by the inltration of lymphocytes
and macrophages in and around the blood vessel.
In the renal interstitial tissue, worms were sur-
rounded by an area of lymphocytes and macrophages
with the presence of a multinucleate giant cell
(Fig. 4).
Molecular identication
Amplicons of about 1700 bp and an internal portion
of 808 bp were visualized on 2% agarose gel. A con-
sensus sequence (GenBank KY263809) was made
based on sequences obtained from these PCR pro-
ducts and was submitted to Blastn (http://blast.
ncbi.nlm.nih.gov) showing 100% similarity with
Crassicauda magna (GenBank KM233410).
DISCUSSION
Crassicaudiosis is one of the main parasitic diseases
of n whales (Lambertsen, 1986). The diculties
in eld sampling, limited possibilities for experi-
mental work and diculties to observe these
specimens in the marine environment make infor-
mation on C. boopis scarce (Lambertsen, 1985;
Balbuena and Simpkin, 2014; Jabbar et al. 2015).
The life cycle is not yet entirely elucidated, and
little is known about potential intermediate hosts.
Fig. 1. Fin whale (Balaenoptera physalus) on the necropsy site.
3Crassicauda boopis in a n whale (Balaenoptera physalus) ship-struck in the eastern North Atlantic Ocean
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Moreover, transmission to calves, which are regu-
larly and heavily infested (Lambertsen, 1992), is sus-
pected to be transplacental, whereas galactogenic
transmission has to be considered even though up
to now no larvae were found in milk or mammary
tissue (Díaz-Delgado et al.2016). Direct transmis-
sion to calves by urine contamination was evoked
(Lambertsen, 1986), which suggests emission of
infective larvae in the environment and therefore a
bypass in the need of an intermediate host. This
suggestion seems unlikely because of the obvious
thick shells of the eggs of C. boopis usually encoun-
tered in environmentally resistant eggs and the fact
that habronematoids are known to use arthropod
intermediate hosts consistently (Anderson, 2000).
In this present case, the size of the juvenile n
whale corresponds to a recently weaned n whale,
in which weaning occurs at an age of 67 months
and a body size of 1113 m (William et al. 2009).
Therefore, the present report supports the theory
that infestation could occur transplacentally or
during lactation.
Fig. 2. Nematode segments found in lungs (top), the
caudal caval vein (middle) and the renal vein (bottom) of
the n whale.
Fig. 3. Anterior extremity (20×) (top), (400×) (middle)
and posterior extremity of female Crassicauda boopis (20×)
(bottom).
4Laetitia Lempereur and others
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Crassicaudiosis due to C. boopis is typically a
chronic disease and has proven to be potentially
lethal, mainly due to congestive kidney failure, or
to cause substantial morbidity in those animals
which survive (Lambertsen, 1985,1992; Jauniaux
et al. 2000; Díaz-Delgado et al.2016). In some indi-
viduals, a more acute inammatory reaction sur-
rounds the parasites with exudate or pus. Lesions
associated with C. boopis occur less commonly in
the lungs, which can contain necrotic fragments of
nematodes, as described in this present case, with
mineral deposits (Lambertsen, 1992). Although
numerous C. boopis and lesions similar to those
described by Lambertsen (1986) and Jauniaux
et al.(2000) were found in the n whale case pre-
sented here, the cause of death could be established
as the collision with the ship on the basis of the pres-
ence of large haematoma at the impact zone and the
absence of evidence of renal failure. The young age
of this whale and the absence of severe reaction
may suggest that the infestation was not at an
advanced chronic stage yet.
Crassicauda genus is represented by large size
nematodes with C. boopis as the second longest
nematode in whales. Consequently, obtaining intact
specimens from host tissues is a real challenge and
the species is frequently only described from frag-
ments, leading to uncertainty in their identication.
Therefore, molecular biology could be useful in
the identication of these specimens. Consensus
sequence of 18S rRNA gene obtained from these
present samples was similar to the sequence obtained
from parasites found in subcutaneous tissues of a
pygmy sperm whale (Kogia breviceps) and identied
as C. magna (Jabbar et al. 2015). Additionally, this
sequence was similar to the partial sequence of a
worm located in the kidney of a Cuviers beaked
whale (Ziphius cavirostris) (Díaz-Delgado et al.
2016). While adults of C. boopis and C. magna are
morphologically distinct and found in dierent
body sites, molecular analysis of the 18S rRNA
gene seems insucient for reliable species identica-
tion. This could be a major restriction mainly for
larvae identication.
It is noteworthy that all morphological classica-
tions to date have included Crassicauda spp. in the
order Spirurida, superfamily Habronematoidea,
family Tetrameridae and subfamily Crassicaudinae
(Lambertsen, 1985; Jabbar et al. 2015), while
recent phylogenetic analysis based on the 18S
rRNA gene showed C. magna as a member of the
Acuarioidea superfamily (Jabbar et al. 2015). The
18S rRNA gene shows highly conserved regions,
and although this gene is often used for deep
phylogenetic relationship investigation, multigene
analysis should be performed to rene this phylo-
genetic analysis.
This n whale arrived in Belgium probably after a
ship-strike in the Bay of Biscay or in the Western
English Channel, given the track of the ship and
the estimation of period of death. Fin whales
are large, long-distance swimmers that often occur
far oshore, and not many causes of natural mortal-
ity are known, such as predation or starvation which
are probably of minor signicance. However, decline
of major zooplankton populations (Steinberg and
Landry, 2017) could lead to poor nutrition and
therefore to an increase in the severity of endemic
parasitism by compromising disease resistance
(Lambertsen, 1992). For this reason, Lambertsen
(1986) suggested that diseases like crassicaudiosis
may be the most signicant mortality factor in
large balaenopterid whales (Raga et al. 1997).
Further research should be able to collect informa-
tion on animals infected by parasites especially
C. boopis in order to implement a model including
the eect of parasitism in calf and adult whale
populations.
Conclusion
Crassicaudiosis is potentially the most signicant
mortality factor in large balaenopterid and reported
Fig. 4. Larvated eggs of Crassicauda boopis (400×) (top);
histopathological examination of renal tissue: nematode
with larvated eggs in an arteriole. The subacute arteritis
and periarteritis is characterized by inltration of
lymphocytes and macrophages (bottom).
5Crassicauda boopis in a n whale (Balaenoptera physalus) ship-struck in the eastern North Atlantic Ocean
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cases are scarce. Further research is surely needed in
order to elucidate the life cycle of the parasite, its
taxonomy and impact on whale populations.
However, the present report supports the theory
that infestation could occur transplacentally or
during lactation.
The species is frequently only described from
fragments, leading sometimes to uncertainty in
their identication. Therefore, molecular biology
could be useful in the identication of these speci-
mens with multigene analysis helping to rene iden-
tication and phylogenetic analysis.
ACKNOWLEDGEMENTS
The authors are very grateful to Allison Balin, Jurgen
Decraene, Bart De Pauw, Françoise Maréchal, Michael
Sarlet and Patrick Vervaet. The authors also thank the
volunteers of the veterinary Faculty of Ghent University
and the veterinary Faculty of Liege University. They are
grateful for the excellent cooperation with the crew of
the Premium do Brasil, the local authorities of the city of
Ghent, port authorities, the Federal public service
health, food chain safety and environment, Citrosuco
(and in particular Jean-Pierre Vandecasteele), the Civil
Protection Unit, and many others for their role in securing
the animal and making the scientic investigation possible.
FINANCIAL SUPPORT
This research did not receive any specic grant from
funding agencies in the public, commercial or not-for-
prot sectors. The work was carried out in the framework
of the Marine Animals Research and Intervention
Network (MARIN), coordinated by the RBINS.
CONFLICT OF INTEREST
None.
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... A similar parasite related granulomatous reaction was also seen in the mesenteries close to the kidney in three CIBs and is presumed to be caused by the same parasite. Neither invasion of the lungs, significant thromboembolism or vasculitis were appreciated in these cases such as is seen 24 by a similar parasites, C. boopis in large whales including blue whales (Balaenoptera musculus), humpback whales (Megaptera novaeangliae), and fin whales (Balaenoptera physalus) and C. sp. with closest identification as C. magna in Cuvier's beaked whales (Lempereur et al, 2017, Díaz-Delgado et al. 2016. The mild eosinophilic vasculitis described above could be due to C. giliakiana; however, it is much less severe than cases described with C. boopis and C. magna-like parasites. ...
... These parasites were not identified to species but were likely the commonly reported Anisakis giliakiana has been diagnosed in human patients after eating raw squid or fish and manifests as abdominal pain and/or a skin rash (Makino et al. 2014, Ohnishi et al. 2018 Alternatively, there may be direct transmission from cow-to-calf, either transplacental or through milk contaminated with urine. This has been hypothesized due to the presence of adult nematodes, C. boopis, a closely related parasite, in recently weaned fin whale calves (Lambertsen 1986, Lempereur et al. 2017. Crassicauda giliakiana has not been found in very young CIBs. ...
... In stranded CIBs, this parasite is not thought to be the primary cause of death; however, in 16 of 23 cases of stranded CIBs it was thought to be a possible contributory factor. Large whales, particularly fin whales with C. boopis and Cuvier's beaked whales with C. magnalike parasite, have severe lesions in kidneys and cardiovascular system that are suspected to contribute to mortality, particularly C. boopis in juvenile fin whales(Lambertsen 1986, Lempereur et al. 2017, Díaz-Delgado et al. 2016).This prevalence of C. giliakiana in CIBS is higher than in other Alaska beluga populations(Stimmelmayr et al. 2022). C. giliakiana has been reported at very low levels in northern Alaska in the eastern Chukchi Sea stock, in Canada's eastern Beaufort Sea stock, and has been documented in the North Pacific Ocean, Okhotsk Sea, and Amur River (Burek-Huntington et al. 2015, Measures et al. 2015, Stimmelmayr et al. 2022). ...
... In this regard, current evidence suggests that nematode species belonging to the Crassicauda genus, which are exclusively cetacean parasites (Raga and Balbuena, 1990) and known to result in substantial cetacean morbidity and mortality, may play an important regulatory role in cetacean populations (Balbuena and Simpkin, 2014). Infections by this genus have been noted in several cetaceans, such as in the penis of a male long-finned pilot whale (Globicephala melas) stranded off the Spanish Mediterranean coast (Raga and Balbuena, 1990), the right heart ventricle and caudal caval vein of a juvenile male fin whale (Balaenoptera physalus) in the Channel Terneuzen-Ghent, in Belgium (Lempereur et al., 2017), and in the skulls of pantropical spotted dolphins (Stenella attenuata) in the eastern tropical Pacific (Perrin and Powers, 1980). Some publications are available concerning Crassicauda sp. ...
Article
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A female Cuvier's Beaked Whale (Ziphius cavirostris) specimen measuring 580 cm in length died after being stranded in Southeastern Brazil. Following a necropsy, organ samples were obtained, fixed in 10% neutral buffered formalin and histopathologically analyzed. A severe and generalized hypodermis infection by Phyllobothrium delphini (Phyllobothriidae) was observed, resulting in granulomatous panniculitis. Severe renal and arterial lesions were also noted, including a severe bone metaplasia in the aorta artery, associated with a massive infection by Crassicauda sp, (Tetrameridae). A significant thoracic hemorrhage due to thoracic aorta artery rupture was noted, also likely due to this infection, resulting in a fatal injury. This study contributes towards knowledge on histopathologic changes in the scarcely studied Cuvier's Beaked Whale, is the first to associate a Crassicauda sp. infection in this whale species in the Brazilian region and also the first to indicate a resulting osseous metaplasia due to this parasitism and granulomatous dermatitis associated with Phyllobothrium delphini. Furthermore, this is also, to the best of our knowledge, the first report of Phyllobothrium delphini cysts in a Ziphius cavirostris specimen to date.
... It is particularly challenging to obtain information about life cycles due to the cryptic nature of these animals, the difficulties of field sampling and the virtual impossibility of experimental approaches (e.g. HERMOSILLA et al. 2015;LEMPEREUR et al. 2017). However, it is worth making an effort to undertake a biological and ecological study of these parasites, not only for the reasons stated above, but also because parasites of cetaceans are models of great interest to investigate coevolutionary phenomena in the marine environment, especially oceanic. ...
... Введение. Нематоды подотряда Spirurida рода Crassicauda паразитируют у китообразных и локализуются преимущественно в урогенитальной системе или в мускулатуре [1][2][3]. При значительной вариабельности размеров взрослых крассикауд (4 см -3,7 м) размеры яиц остаются практически неизменными (0,045 × 0,030 мм, толщина оболочки: 0,003-0,006 мм). Описанные яйца, как правило, получены непосредственно из самок, посмертно по отношению к дефинитивному хозяину. ...
Article
Crassicauda sp. eggs were found in the feces of pacific bottlenose dolphin (Tursiops truncatus gillii) for the first time. The material was volunteered from spontaneously infested 7-year-old female using a sterile, single-use Suyun gastric tube (Unicorn Med) at the Moskvarium. Feces were studied in the Center for Oceanography and Marine Biology laboratory (Moscow) as a native smear using Mikmed-5 light microscope (LOMO) and in the St. Petersburg State Academy of Veterinary Medicine Laboratory (St. Petersburg) using a wet mount technique and simple flotation with Darling’s solution and Mikmed-6 light microscope (LOMO). Along with the morphometrically equal thickness of the multilayer egg membrane, the elongated part of the intact egg was optically inhomogeneous, which was even more noticeable in the damaged egg. Eggs with polar concavities of the inner layer only or even all of the layers of the membrane were found. The eggs morphology indicates pliability of the polar structures of the membrane, which may be important when the larva emerges.
... Indeed, parasites have been studied from mysticete feces (Hughes-Hanks et al. 2005;Hunt et al. 2013). Anisakis spp., Crassicauda spp., and other endoparasites are known from the two baleen whale species that this study focused on: bowhead (Migaki et al. 1982;Heckmann et al. 1987;Sheffield et al. 2016) and fin whales (Lempereur et al. 2017). ...
Article
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Baleen, a unique oral α-keratin, has flat cortical layers enclosing hollow horn tubules. Baleen grows continuously to replace erosive loss from feeding-related wear. This is essential for maintaining efficient filtration over a whale’s long life history. Baleen fragments are seen in stomach contents and feces. We focused on fin (Balaenoptera physalus) and bowhead whales (Balaena mysticetus), but examined eleven mysticete species. Histological features including variably sized tubules plus differential growth along plate axes (growing faster along the medial fringed edge) and between plates of a rack (central plates growing faster than others) relate to baleen strength and flexibility. Sheet-like cortical layers provide strength and probably hinder erosive shedding, whereas medullary (tubular/intertubular) keratin provides flexibility and likely promotes shedding. To calculate amounts of grown/lost baleen, we considered both erosive wear and basal growth, recognizing that each plate represents several years of growth. We estimate average annual loss of 70–100,000 cm2 (20–40,000 cm3) of baleen in balaenids and 25–50,000 cm2 (7–14,000 cm3) in balaenopterids. Baleen growth rates depend on age, size, and other life history parameters; the most reliable calculations come from morphometric data with plate dimensions measured along full racks. We argue that baleen turnover has been under-rated and baleen growth rates underestimated in the published literature. Baleen turnover maintains filter integrity/porosity, while gut passage possibly clears gastrointestinal tracts of endoparasites. Large volumes of shed keratin hold potential ecological consequences by providing food for microbial decomposers and detritivores throughout ocean ecosystems, especially in polar regions where most mysticete feeding occurs.
... Infestation by C. boopis can cause serious illness in baleen whales, since the localization of adult worms in the vascular and urinary system can lead to severe renal dysfunction and death. This species has been recorded in fin whales from the Atlantic and Pacific Oceans, but has not yet been identified to species in the Mediterranean (Lambertsen 1986, 1992, Lempereur et al. 2017. ...
Article
Mediterranean fin whales Balaenoptera physalus face many threats to their conservation, including both anthropogenic and natural issues. There are few records of the parasitic fauna of this species in this geographical area. To partially fill in this gap of knowledge, we investigated the presence and potential impact of parasitic diseases in Mediterranean fin whales. Seven animals stranded along Italian coastlines between 2006 and 2015 were submitted for necropsy and parasitological examination. The protozoan parasite Toxoplasma gondii was detected in 1 fin whale and, for the first time in mysticetes, it was successfully genotyped as a type II strain with 15 microsatellite markers. One crustacean (Pennella spp.) and 4 helminth taxa (Crassicauda boopis, Ogmogaster antarcticus, Tetrabothrius ruudi and Bolbosoma sp.) were detected and morphologically identified. Different degrees of ectoparasitism by adult P. balaenoptera were recorded. Immature stages of Pennella sp. were also detected in 2 animals and are described here for the first time in cetaceans. Infestation by C. boopis was confirmed or suspected in 5 cases. Parasitic thrombi, involving renal veins and caudal vena cava, and fibrosis of renal parenchyma were associated with C. boopis and likely resulted in some degree of renal dysfunction. Larval nematodes were found within foci of mesenteric endarteritis. Further research to evaluate the prevalence of this potentially fatal endoparasitosis in Mediterranean fin whales is warranted.
Article
Full-text available
The vascular system of Cuvier’s beaked whales (CBW) (Ziphius cavirostris; family Ziphiidae), an extremely deep, prolonged-diving cetacean, is increasingly receiving anatomic and physiologic study due to possible anthropogenic interactions; however, vascular pathology rarely has been reported in this species. Thirteen CBW stranded in the Canary Islands from June 2008 to June 2014 were autopsied. A careful dissection of the thoracic and abdominal vasculature was performed on these animals. All had moderate to severe and extensive chronic fibrosing arteritis with aneurysms, hemorrhages, and thrombosis primarily involving the mesenteric and gastroepiploic arteries and the thoracic and abdominal aorta. Microscopically, the lesions varied from subacute subintimal hemorrhages and severe neutrophilic, eosinophilic, and histiocytic dissecting arteritis with intralesional nematode larvae to marked, chronic, fibrosing arteritis with thickening and distortion of the vascular wall with calcification and occasional cartilage metaplasia. In addition, adult nematodes in renal arteries and veins, renal parenchyma and/or ureter were identified morphologically as Crassicauda sp. Nucleic acid sequenced from renal nematodes from 2 animals yielded closest nucleotide identity to C. magna. The pathogenesis is proposed to involve a host response to larval migration from the intestine to the kidney through the mesenteric arteries, abdominal aorta, and renal arteries. Severe consequences for such lesions are possible and could vary from reduced vascular compliance to chronic renal disease and predisposition to the development of disseminated intravascular coagulation and multiorgan failure. Severe chronic arteritis in CBW is associated with renal parasitism by Crassicauda spp.
Article
Full-text available
Evaluating the effect of parasites on population size is essential for designing management and conservation plans of wild animal populations. Although knowledge in this area is scarce in cetaceans, current evidence suggests that species of the nematode genus Crassicauda may play an important regulatory role in some populations. In the present study, a semiparametric regression technique was applied to a previously published dataset to re-examine the role of Crassicauda sp. in natural mortality of pantropical spotted dolphins Stenella attenuata. The resulting model indicated parasite-induced mortality at ages between 6.5 and 9 yr and at roughly 12 yr. The maximum mortality estimates obtained could represent 2 to 4% of natural mortality in dolphins 6 to 8 yr old. This estimate is substantially smaller than previously published values, but in contrast with previous research, our model provides clear statistical evidence for parasite-induced mortality because the bootstrapped 95% confidence intervals of the estimated mortality rates excluded the 0 value. We also evaluated, through simulations, how potential sampling biases of infected dolphins could overestimate parasite-induced mortality. Small differences in sampling selectivity between infected and uninfected animals could substantially reduce the mortality estimates. However, the simulated models also supported the notion of statistically significant mortality in juvenile dolphins. Given that dolphins older than 16 yr were poorly represented in the dataset, further research is needed to establish whether Crassicauda sp. causes meaningful mortality for population dynamics among adult individuals.
Article
Marine zooplankton comprise a phylogenetically and functionally diverse assemblage of protistan and metazoan consumers that occupy multiple trophic levels in pelagic food webs. Within this complex network, carbon flows via alternative zooplankton pathways drive temporal and spatial variability in production-grazing coupling, nutrient cycling, export, and transfer efficiency to higher trophic levels. We explore current knowledge of the processing of zooplankton food ingestion by absorption, egestion, respiration, excretion, and growth (production) processes. On a global scale, carbon fluxes are reasonably constrained by the grazing impact of microzooplankton and the respiratory requirements of mesozooplankton but are sensitive to uncertainties in trophic structure. The relative importance, combined magnitude, and efficiency of export mechanisms (mucous feeding webs, fecal pellets, molts, carcasses, and vertical migrations) likewise reflect regional variability in community structure. Climate change is expected to broadly alter carbon cycling by zooplankton and to have direct impacts on key species. Expected final online publication date for the Annual Review of Marine Science Volume 9 is January 03, 2017. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.
Book
An overview of sightings and strandings of cetaceans in the southern North Sea (with emphasis on The Netherlands and Belgium)
Article
Eighty-seven fin whales taken from the North Atlantic were systematically nec-ropsied to investigate the occurrence, levels, and mechanisms of disease which could cause mortality in this species. Crassicauda infection was found to be prevalent, deeply invasive, and probably capable of causing death. The giant nematode Crassicauda boopis was present in 82 (94.3%) of the whales examined. Adult C. boopis presented with their tails in the renal ductwork and their bodies in the renal veins and vena cava. The bodies of the worms were typically enveloped by exuberent tissue reactions which in some whales obstructed multiple renal veins. Transmission of this parasite was by environmental contamination and involved shedding of larvae in the urine. Ingestion of larvae, followed by somatic larval migration to the kidney, was strongly suggested by the finding of extensive inflammatory lesions of the mesenteric arteries in which nematode larvae occurred. From these observations it appears that truly severe C. boopis infections in fin whales could be lethal by inducing congestive renal failure, and that moderate infections cause extensive injury to the vascular system. This implies that the yearly feeding migration of fin whales into circumpolar waters is associated with a definite pathological risk.
Article
Members of the genus Crassicauda (Nematoda: Spirurida) are parasites of the body tissues of whales and dolphins. Owing to the large size of worms and difficulties in the recovery of entire nematodes from the tissues of hosts, limited information is available on morphological descriptions of both male and female worms. Furthermore, there are currently no available sequence data for this genus to assist with such identifications. This paper describes for the first time features of the anterior extremity and the male tail of Crassicauda magna, suggesting that Crassicauda duguyi may be a synonym of this species. In addition, molecular data are presented for the genus for the first time suggesting that the genus belongs within the superfamily Acuarioidea rather than within the Habronematoidea, in which it is currently placed.
Article
The first edition of this book was published in 1992 (see Helminthological Abstracts (1993) 62 , abstract 1457). This new enlarged edition includes additional relevant information from some 450 articles published between 1989 and 1998 (with a few from 1999), and some articles overlooked or unavailable for the first edition. The number of species covered has been increased by 34 (total now 595). As before, the book is in 2 parts, the Secernentea and Adenophorea, which are now regarded as classes rather than subclasses. The Secernentea covers the orders Rhabditida, Strongylida, Oxyurida, Ascaridida and Spirurida (suborders Camallanina and Spirurina), and the Adenophorea covers the order Enoplida, with the Dioctophymina and Trichinellina now treated as separate suborders. The aim of the book remains "to summarize and synthesize knowledge of the basic features of the development and transmission of parasitic nematodes of vertebrates, and to place this information in the context of the modern classification as found in the CIH Keys to the Nematode Parasites of Vertebrates " [but see the 2 departures from these keys as noted above]. Nematode parasites of humans, domestic animals and wildlife (including fish) are covered. Each chapter or part begins with an overview of the mode of feeding, habitat and life cycles of the group. This is followed by descriptions and illustrations of larval stages of named specific examples. The number of illustrations has been increased from 33 to 43. Comprehensive bibliographies appear at the end of the sections on each order or suborder.
Article
This communication briefly reviews knowledge of the systemic disease caused by Crassicauda boopis in blue whales (Balaenoptera musculus), fin whales (B. physalus) and humpback whales (Megaptera novaeangliae). Infections with this giant nematode characteristically incite a chronic inflammatory reaction of the blood vessels which drain the kidneys. In this critical location, the parasite-induced lesion can cause complete vascular occlusion and kidney failure. Whale calves and juveniles typically suffer the heaviest parasite burdens following transplacental infection of the developing whale foetus. There is also probable whale-to-whale transmission post-partum, involving urinary contamination of the environment with C. boopis eggs and larvae. The frequency of the infection can exceed 95%. Haematological findings suggest that systemic pathological effects are typical at the population level. Gradual development of occlusive lesions in the renal veins appears to correlate with a major peak in natural mortality at about one year of age. To date, all findings support the conclusion that premature death caused by C. boopis infection is potentially a major impediment to population recovery of affected whale species. This suggests the interesting possibility of actively encouraging the population recovery of three species of large baleen whales. Such a restoration effort would entail remotely-deployed anthelminthic therapy administered, at sea, to infected whale cows and calves.
Article
This report examines the broad range of organisms which can parasitize marine mammals, and identifies those which we feel have the greatest impact on individuals and populations.Many parasites colonize and damage the integument in some way. Only the sucking lice of seals are associated with debilitating disease. In addition, at least one species, E. horridus can serve as intermediate host of the seal heartworm, D. spirocauda.Of the few protozoa, the one deserving most attention is Sarcocystis sp. Its ubiquitous distribution challenges our understanding of coccidian life cycles as currently perceived.Acanthocephalans and cestodes are rarely associated with clinically significant illness. It is intriguing that cetaceans and pinnipeds serve as mammalian intermediate hosts for larval tetraphyllidians destined to mature in elasmobranchs.Digeneans occupy the gastrointestinal tract and severely damage liver and pancreas of cetaceans. Nasitrema sp. infects cranial sinuses of small odontocetes, and enters the brain, thereby leading to stranding and death in selected populations.Nematodes represent the broadest group of parasites. Pseudaliids often infect the respiratory system, causing sufficient damage to affect survival. There is no evidence that Stenums sp., a pseudaliid inhabiting the cranial sinuses of some whales and dolphins, plays any role in mass strandings, as has been popularly suggested. Filarioids are highly pathogenic in pinnipeds and are probably responsible for significant mortality, especially in young animals. Anisakine nematodes in the stomach are of little consequence to the host. The role of marine mammals in transmitting the parasites to commercially exploited fish stocks is a public health issue. The only other parasite which represents a threat to humans is Trichinella spiralis, which is widespread in Arctic mammals.The Crassicaudinae are the largest nematodes in cetaceans. Evidence is accumulating that the damage they cause in cranial bone, mammary tissue and the urinary tract may influence productivity and survival among certain groups.Most of our understanding of the parasites of marine mammals derives from studies on specimens which come ashore. The information is fragmentary, and suffers from our inability to follow the progress of infection and the overall condition of the parasitized animal. Yet we might conclude that the parasitism we see is as advanced as can be tolerated by the host. Weak animals retreat from the protection of the herd, become vulnerable to predators, and probably cannot survive in an environment which places heavy demands on thermoregulation, respiration and mobility.