FISH PARASITOLOGY - ORIGINAL PAPER
Anisakid andRaphidascaridid parasites inTrachurus trachurus:
infection drivers andpossible eﬀects onthehost’s condition
FabioMacchioni1 · PerlaTedesco2· VanessaCocca1· AndreaMassaro3· PaoloSartor4· AlessandroLigas4·
CarloPretti1· GianfrancaMonni1· FrancescaCecchi1· MonicaCaara2
Received: 24 February 2021 / Accepted: 27 May 2021
© The Author(s) 2021
This study investigated the distribution of nematode larvae of Anisakidae and Raphidascarididae (genera Anisakis and Hys-
terothylacium) in Trachurus trachurus (Linnaeus, 1758) in the Ligurian and central-northern Tyrrhenian Seas. The relation-
ship between the number of parasites and the length and weight parameters of the ﬁsh was assessed, and the possible eﬀect
of the parasites on the condition factor was evaluated. A total of 190T. trachurus specimens were collected in July 2019.
Parasites were found in 70 individuals. A total of 161 visible larvae were collected in the viscera. Morphological analysis
revealed the presence of Anisakis spp. in 55 ﬁsh and Hysterothylacium spp. in 15 ﬁsh, while 5 ﬁsh showed coinfection with
both genera. The specimens subjected to PCR (n = 67) showed that 85% of the Anisakis larvae analyzed belonged to the
species A. pegreﬃi, while the remaining 15% belonged to hybrids of A. pegreﬃi-A. simplex (s.s.). A total of 58% (n = 7) of
the Hysterothylacium larvae analyzed belonged to the species H. fabri, while 42% belonged to the species H. aduncum. Our
results support the hypothesis that infection with these parasites does not aﬀect the condition of the ﬁsh host analyzed, and
that body size and depth are major drivers in determining infection levels with Anisakid and Raphidascaridid nematodes.
Keywords Anisakis spp.· Hysterothylacium spp.· Trachurus trachurus· Infection drivers· Fish condition· Mediterranean
Anisakidosis is a ﬁsh-borne zoonosis following ingestion of
the third larval stage of nematodes of the family Anisakidae.
Within the Anisakis simplex Rudolphi, 1809 complex, the
species A. simplex (s.s.) and A. pegreﬃi Campana-Rouget
and Biocca, 1955 (Mattiucci etal. 2014) are recognized as
the main causative agents of anisakiasis, a condition related
to the consumption of raw, marinated, or undercooked ﬁsh
ﬁlets infected by the third-stage larvae of these parasites. In
Mediterranean waters, the species A. pegreﬃi is dominant
and is also the main etiological agent of anisakiasis and
is distributed in numerous paratenic and deﬁnitive hosts
(Mattiucci and D’Amelio 2014; Mattiucci etal. 2019).
Species of the genus Hysterothylacium Ward and Magath,
1917, formerly belonging to the Anisakidae and currently
assigned to the family Raphidascarididae, are common para-
sites in diﬀerent marine and freshwater ﬁsh species (Bezerra
etal. 2020). H. aduncum Rudolphi, 1802 and H. fabri Rudol-
phi, 1819 are the most frequently reported species in teleost
ﬁsh from the Mediterranean region (Roca‐Geronès etal.
2018; Tedesco etal. 2018). Evidence of the direct conse-
quences of Hysterothylacium infection on ﬁsh health is lim-
ited: parasites of this genus are considered only mildly patho-
genic for adult ﬁsh (Ishikura etal. 1993; Yagi etal. 1996;
Valero etal. 2003; Cavallero etal. 2012); however, mortal-
ity episodes in larval and juvenile ﬁsh have been reported
Francesca Cecchi and Monica Caﬀara equally contributed to this
Section Editor: Federica Marcer
* Fabio Macchioni
1 Department ofVeterinary Sciences, University ofPisa, Pisa,
2 Department ofVeterinary Medical Sciences, Alma Mater
Studiorum, University ofBologna, Bologna, Italy
3 APLYSIA, Livorno, Italy
4 CIBM, Inter-University Center ofMarine Biology
andApplied Ecology “G. Bacci”, Livorno, Italy
/ Published online: 14 August 2021
Parasitology Research (2021) 120:3113–3122
(Bristow 1990; Balbuena etal. 2000). Although generally
not listed among ﬁsh-borne zoonotic agents, preliminary evi-
dence on the allergenic potential of Hysterothylacium species
(Fernández-Caldas etal. 1998; Valero etal. 2003) suggests
their importance in relation to food safety and human health.
Monitoring the occurrence of Anisakis and Hysterothy-
lacium in wild ﬁsh for human consumption is therefore nec-
essary, particularly regarding selected species (Debenedetti
etal. 2019) considered at higher risk of infection. Further-
more, the high parasite load reported in susceptible ﬁsh spe-
cies (Manfredi etal. 2000; Angelucci etal. 2011) highlights
the need to investigate the eﬀects of parasites on the host’s
Among Mediterranean ﬁsh species at high risk of Anisak-
ids and Raphidascaridids, the Atlantic horse mackerel Tra-
churus trachurus Linnaeus, 1758 (Trachuridae, Carangidae)
is a gregarious bentho-pelagic species, widely distributed
throughout the Mediterranean Sea including the Black Sea
(Bini 1967) and eastern Atlantic from Iceland to Senegal
(Abaunza etal. 2008), and supports large ﬁsheries (Abaunza
etal. 2003), both as target and by-catch species. This spe-
cies feeds on small ﬁsh and planktonic crustaceans and may
become infected by both Anisakis and Hysterothylacium
larvae by consuming euphausiids, which are intermediate
hosts of these nematodes (Smith 1983; Adroher etal. 1996).
In the present study, we surveyed the occurrence and
distribution of Anisakis spp. and Hysterothylacium spp.
in the Atlantic horse mackerel, T. trachurus, caught in the
FAO-GFCM Geographic Sub-area 9 (GSA9), Ligurian
Sea and central-northern Tyrrhenian Sea, investigating the
eﬀect of infection on the host’s condition and the inﬂuence
of diﬀerent biological (total length, total weight, sex) and
environmental (depth) variables.
Atlantic horse mackerel specimens were sampled in July
2019 in the Ligurian and central-northern Tyrrhenian Seas
(FAO-GFCM Geographic Sub-area 9) (Fig.1) by trawling
at depths ranging from 18 to 330m during the implemen-
tation of the EU-funded Mediterranean international trawl
survey (MEDITS project, Spedicato etal. 2019). After cap-
ture, samples were frozen immediately on board and trans-
ported to the Centro Interuniversitario di Biologia Marina
“A. Bacci” (CIBM) labs for the analysis.
Fish samples andparasitological examination
For each specimen, total length (TL, to 0.5cm below) from
the tip of the snout to the end of the tail and total weight (TW,
g) (weighing scale precision 0.1g) were recorded. Sex was
determined through macroscopical examination of gonads.
Length–weight relationship was analyzed by means of
the power equation W = aTLb, where W is the total weight
and TL is the total length. The Le Cren (1951) relative
condition factor (Kn), expressing the condition of a ﬁsh in
numerical terms, was calculated from the observed total
weight and theoretical weight (EW, g) estimated from “a”
and “b” parameters of the length–weight relation.
Fig. 1 Map of the study area in the Ligurian and northern and central Tyrrhenian Seas (FAO-GFCM GSA9)
3114 Parasitology Research (2021) 120:3113–3122
For the parasitological examination, the abdominal cav-
ity was examined by visual inspection, while the internal
organs were observed under a stereomicroscope (magniﬁ-
cation 8– × 35) for the presence of third-stage larvae (L3)
of Anisakid and Raphidascaridid nematodes.
All collected larvae were identiﬁed at the genus level
according to their general morphology (Hartwich 2009;
Gibbons 2010), through observation under light micros-
copy. The prevalence, mean intensity (MI), and mean
abundance (MA) values of larvae belonging to each genus
were calculated according to Bush etal. (1997).
Genomic DNA was extracted from the central part of the
larvae body by the PureLink® Genomic DNA Kit (Life
Technologies, Carlsbad, CA) following the manufactur-
er’s instructions. Ampliﬁcation of the complete ITS rDNA
region was performed with primers NC5_f (5′-GTA GGT
GAA CCT GCG GAA GGA TCA TT-3′) and NC2_r (5′-TTA
GTT TCT TCC TCC GCT -3′) (Zhu etal. 1998). The PCR
products were electrophoresed on 1% agarose gel stained
with SYBR Safe DNA Gel Stain (Thermo Fisher Scien-
tiﬁc, Carlsbad, CA) in 0.5X TBE. For the polymerase
chain reaction-restriction fragment length polymorphism
(PCR–RFLP), 10µl of the PCR product were digested
with 1.5µl of restriction enzymes HinfI, HaeIII, and AluI
(D’Amelio etal. 2000; Tedesco etal. 2018), in a volume of
20µl at 37°C for 90min (Abollo etal. 2003). The restric-
tion fragments were separated in 3% agarose gel stained
with SYBR Safe DNA Gel Stain in 0.5X TBE. Sequenced
A. pegreﬃi and A. simplex (s.s.) were used as positive con-
trols in every reaction. After the electrophoresis, some
specimens showed hybrid restriction patterns; therefore,
in order to exclude the possibility of incomplete digestion,
they were digested for longer time (240min).
Sequenced A. pegreﬃi and A. simplex (s.s.) were used
as positive controls (K +) in every reaction.
The Chi-square test (signiﬁcance level 0.05) was per-
formed to assess possible signiﬁcant diﬀerences in the
prevalence of Anisakid and Raphidascaridid parasites
between male and female ﬁsh and also to test the relation-
ship between the prevalence of nematode parasites and
The analysis was performed using the JMP statistical
package (SAS, Jmp 2007).
Regarding the length–weight relationship, Student’s t-test
was applied to test allometric growth (“b” = 3) (Pauly 1984)
and diﬀerences between sexes.
Data exploration was performed to check correlation
among variables (TL, TW, sex, Kn, and number of para-
sites), and a graphic output was produced (pairplot); the
relationship between the number of parasites and biological
parameters (TL, TW, sex) was tested by ANOVA. The pos-
sible eﬀect of parasites on the condition factor was evaluated
by Student’s t-test.
The prevalence of single or multiple infections of nema-
todes larvae with a 95% conﬁdence level, based on the results
of microscopic analysis, was calculated for the whole sample.
The prevalence of Anisakids and Raphidascaridids in both
ﬁsh sexes was subjected to statistical analysis, using the Chi-
square test, and was considered signiﬁcant at P < 0.05.
A total of 190 specimens of T. trachurus were collected dur-
ing the MEDITS survey in July 2019, of which 107 were
female and 83 were male. Body size ranged from 10.0 to
31.0cm TL in females and from 10.0 to 31.5cm TL in
Parasites were found in 70 individuals: 30 males and 40
females; prevalence, mean intensity, and mean abundance of
parasites recorded for all specimens are reported in Table1.
A total of 161 visible larvae were collected in the viscera.
Morphological analysis revealed the presence of 129 (28%)
Anisakis spp. larvae in 55 ﬁsh: 21 males and 34 females and
31 larvae (10.5%) Hysterothylacium spp. in 15 ﬁsh: 9 males
and 6 females, while 5 ﬁsh showed coinfection with both.
All the values are reported in Table2.
Table 1 Number of ﬁsh (NF), number of parasitized ﬁsh (NPF), prevalence (%), CI 95% conﬁdence interval, range of intensity (I), min–max
(average) (RI), abundance (A), number of parasites (NP)
NF NFP % CI RI A NP
Males 83 30 36.14 29.20–43.09 1–6 (2.2) 1.12 93
Females 107 40 37.38 30.39–44.37 1–8 (2.36) 0.63 68
Total 190 70 37.89 29.87–43.81 1–8 (2.29) 0.85 161
3115Parasitology Research (2021) 120:3113–3122
Statistical analysis showed that the ﬁsh were more signiﬁ-
cantly infected with Anisakis larvae than with Hysterothy-
lacium spp. (p = 0.032); however, no statistically signiﬁcant
diﬀerences in infection values were observed between sexes.
Length–weight relationship was calculated by sex and
the results are shown in Fig.2a and b and Table3. The “b”
parameter diﬀered signiﬁcantly for each sex: females showed
positive allometric growth, while males showed isometric
growth. Statistically signiﬁcant diﬀerences between sexes
were not detected (t-value 0.498; p > 0.05).
The condition factor (Kn) ranged from 0.80 to 1.98:
the minimum values were 0.81 and 0.80 for males and
females, respectively, while the maximum values were
1.98 for males and 1.27 for females. No statistically signif-
icant diﬀerences in the condition factor emerged between
males and females (t = 0.190; p > 0.05) and between
Table 2 Number of ﬁsh parasitized by Anisakis (FPA), number of ﬁsh
parasitized by Hysterothylacium (FPH), prevalence (%), CI 95% con-
ﬁdence intervals, range of intensity (RI), min–max (average), abun-
dance (A), number of Anisakis (NA), number of Hysterothylacium
(NH). P = 0.032
FPA % CI RI/min-max A NA FPH % CI RI/min–max A NH
21 25.30 19.02–31.58 1–6 (2.47) 0.57 47 9 10.84 2.22–19.46 1–4 (2.33) 0.253 21
34 31.77 25.05–38.50 1–8 (2.24) 0.77 83 6 5.61 1.64–9.58 1–3 (1.67) 0.0935 10
55 28.95 22.39–35.50 1–8 (2.35) 0.68 130 15 7.89 3.24–12.55 1–4 (2.07) 0.1632 31
Fig. 2 a Length–weight rela-
tionship in males of Trachurus
trachurus. b Length–weight
relationship in females of Tra-
3116 Parasitology Research (2021) 120:3113–3122
parasitized and non-parasitized individuals (t = 0.986;
p = 0.325). Variations in the condition factor in relation to
total length are shown in Table3.
A preliminary data exploration highlighted a relation-
ship between total length and total weight with the number
of parasites (Pearson correlation coeﬃcient (PCC) = 0.5);
there was also a correlation between total length and total
weight (PCC = 0.9).
A significant and positive correlation was found
between the number of parasites and total length (t = 7.532;
p < 0.05) and total weight (t = 8.786; p < 0.05), while sex
was not signiﬁcantly correlated (t = 0.925; p > 0.05).
The prevalence of nematode parasites was signiﬁcantly
higher (P < 0.0001) in horse mackerels caught at depths
below 250m (47.6%) compared to those captured above
250m (23.5%). All (100%) the parasitized ﬁsh from deeper
waters (> 250m) were infected with Anisakis spp., while
only one ﬁsh (1.9%) showed coinfection with Hysterothy-
lacium spp. In contrast, the parasitized ﬁsh from shallower
waters (< 250m) were more frequently infected with Hys-
terothylacium spp. (70%) and less by Anisakis spp. (25%).
With regard to molecular analyses, all the specimens sub-
jected to PCR (n = 67) were successfully ampliﬁed, showing
bands of ~ 1000bp. The PCR–RFLP showed that 85%
(n = 47) of the Anisakis larvae analyzed belonged to the spe-
cies A. pegreﬃi, while in the remaining 15% (n = 8), hybrids
of A. pegreﬃi-A. simplex (s.s.) were detected (Fig.3a).
A total of 58% (n = 7) of the Hysterothylacium larvae
analyzed belonged to the species H. fabri, while 42%
(n = 5) belonged to the species H. aduncum (Fig.3b and
c). For conﬁrmation, the hybrids were re-digested with the
same enzymes for 240min.
The present study provides information on the distribution of
third-stage larvae of A pegreﬃi, H. aduncum, and H. fabri in
T. trachurus from the Ligurian and Tyrrhenian Seas (west-
ern Mediterranean), correlating the infection data with the
biological and biometric features of the hosts.
Our results highlighted that the genus Anisakis (28.95%)
was more prevalent than Hysterothylacium (7.89%). This
coinfection pattern is in accordance with other parasitologi-
cal investigations on T. trachurus from the Mediterranean
and Extra-Mediterranean regions. Fioravanti etal. (2003)
reported a higher prevalence of Anisakis (33.7%) compared
to Hysterothylacium (12.2%) in T. trachurus from the cen-
tral Adriatic Sea. With respect to the Ligurian Sea, in horse
mackerels Serracca etal. (2013) reported a prevalence of
15.6% for Anisakis and 9.3% for Hysterothylacium larvae.
Manfredi etal. (2000) reported higher prevalence values
(80–100%) only for Anisakis spp. In a survey carried out on
Trachurus spp. caught oﬀ the coast of Sardinia, Angelucci
etal. (2011) reported prevalences of 52.5% for Anisakis spp.
Table 3 Length–weight relationship parameters for males and
females of Trachurus trachurus. a and b are the parameters of the
power function; SE(b), the standard error of b; r2, the coeﬃcient of
determination; and t-value, the value of the t-test
a b SE(b) r2t-value
Males 0.0102 2.937 0.052 0.977 56.35
Females 0.0053 3.145 0.038 0.985 83.28
Fig. 3 Restriction fragment length polymorphism patterns (molecular
weight marker 100 base pairs) obtained with a restriction enzymes
HinfI (lanes 1, 3, 5, 7, 9, and 11) and HaeIII (lanes 2, 4, 6, 8, 10, and
12), lanes 1–6 Anisakis pegreﬃi, lanes 7–8 Anisakis pegreﬃi/Anisakis
simplex hybrid, lanes 9–10 positive control (K +) = A. pegreﬃi, lanes
11–12 K + = Anisakis simplex; b restriction enzymes HinfI (lanes
1, 3, 5, 7, 9, and 11) and HaeIII (lanes 2, 4, 6, 8, 10, and 12), lanes
9–10 K + = Hysterothylacium aduncum, lanes 11–12 K + H. fabri;
and c restriction enzymes HinfI (lanes 1, 3, 5, 7, and 9) and AluI
(lanes 2, 4, 6, 8, and 10), lanes 1–2 H. aduncum, lanes 3–6 H. fabri,
lanes 7–8K + = H. aduncum, lanes 9–10K + = H. fabri
3117Parasitology Research (2021) 120:3113–3122
and 77.9% for Hysterothylacium spp. In T. trachurus ﬁshed
oﬀ the coasts of Sicily, Costa etal. (2016) found a 6.7%
prevalence for H. aduncum. Goﬀredo etal. (2019) reported
prevalence values of 50.8% for Anisakis and 0.54% for Hys-
terothylacium in T. trachurus from the Ionian Sea. MacKen-
zie etal. (2008) analyzed the parasite fauna of T. trachurus
in diﬀerent sampling stations across the northeastern Atlan-
tic and Mediterranean Seas, reporting that Anisakis spp. and
H. aduncum were the most common parasites detected in
horse mackerel. Their results also highlighted the usefulness
of Anisakis spp. and Hysterothylacium spp. as biological
tags for distinguishing diﬀerent horse mackerel stocks and
identifying migration patterns.
The high prevalence of Anisakis is probably also related
to the common practice of local ﬁshermen, who discard the
ﬁsh viscera directly at sea. These viscera then become a food
source for a variety of ﬁsh, cetaceans, and seabirds, which
can thus ingest any larvae of Anisakis that may be present
(Oro and Ruiz 1997; Morton and Yuen 2000; Arcos etal.
2001; Bozzano and Sardà 2002). In the Ligurian Sea, it is
also possible that the high prevalence of Anisakis is linked
to the presence of the “Pelagos Sanctuary,” a marine pro-
tected area with a high density of marine mammals which
are deﬁnitive hosts of this genus (Mattiucci etal. 2004; Mat-
tiucci and Nascetti 2006, 2008).
Concerning the molecular analysis, the PCR–RFLP iden-
tiﬁed A. pegreﬃi and hybrids A pegreﬃi-A. simplex and H.
fabri and H. aduncum. The hybrid A. pegreﬃi-A. simplex
(s.s.) has been described in T. trachurus from the Cantabrian
Sea (Abollo etal. 2003) and from the coasts oﬀ Sardinia
(Meloni etal. 2011).
The results are in agreement with the evidence that A.
pegreﬃi is the dominant Anisakis species in the Mediter-
ranean Sea, as highlighted by Mattiucci etal. (2018). The
occurrence of hybrids in the Mediterranean Sea, detected
through PCR–RFLP of the ITS region of rDNA and other
molecular markers, has also been reported by numerous
studies in other ﬁsh species and in marine mammals (Abollo
etal. 2003; Meloni etal. 2011; Cavallero etal. 2012; 2014).
The reason for the spread of hybrid genotypes in the Medi-
terranean is still unclear (Meloni etal. 2011). In the north-
eastern Atlantic and in the western Mediterranean, A. simplex
(s.s.) and A. pegreﬃi are known to occur in sympatry (Abollo
etal. 2001; 2003) and may undergo interspeciﬁc hybridiza-
tion. However it is unclear whether this phenomenon results
in a higher or lower ﬁtness of hybrids compared to parental
species and therefore in a higher or lower infectivity or the
possibility of parasitizing diﬀerent host species. Future inves-
tigations considering multiple molecular markers (Mattiucci
etal. 2018) may shed further light on these aspects.
With respect to the biological and biometric features
of the T. trachurus examined, the “b” values for females
3.145) showed positive allometric growth, with the
growth in length proportionally bigger than the growth in
weight. For males (b = 2.937) and the total sample, isomet-
ric growth was recorded. Similar results have been found in
other areas of the western (Gancitano etal. 2011; Ligas etal.
2012; Spedicato etal. 2012) and eastern (Lembo etal. 2012;
Carbonara etal. 2012; Santojanni etal. 2013) Italian Seas.
Le Cren’s condition factor was applied to assess the ﬁsh
welfare linked with the length–weight relationship, which
can be inﬂuenced by parasites (Dias etal. 2015; Silva etal.
2013; Santos etal. 2013) as well as factors such as gonad
maturation and feeding (Verani etal. 1997).
A strong correlation (P < 0.0001) was found between the
number of nematode parasites in the viscera and the body
size. However, our results suggest that Anisakid and Raphi-
dascaridid parasites do not inﬂuence the state of health of the
horse mackerel in terms of body condition. This result is in
accordance with the results of a previous study (Ichalal etal.
2015) which failed to detect a negative impact of A. simplex
and H. aduncum on the condition of T. trachurus based on
the analysis of Fulton’s condition index. In fact, very few
studies have explored the eﬀect of Anisakis infection on the
body condition of ﬁsh and with contrasting results (Podolska
and Horbowy 2003; Lagrue and Poulin 2015).
In our study, a trend in Kn value was observed in rela-
tion to the length, but it did not diﬀer from 1. Kn increased
between 16.5 and 18.0cm TL and then decreased. A similar
trend was recorded by Alegria-Hernandez (1994) and Šantić
etal. (2011), which is linked to the development and matu-
ration of the gonads: after length at ﬁrst maturity, 18.8cm
in GSA9, (MEDISEH 2013), Kn values decrease due to the
high energy demand required by reproduction. Diﬀerences in
the maturity stage of the ﬁsh could therefore mask the eﬀect
of parasitic infections on the body condition of the ﬁsh host
and result in the contrasting evidence found in the literature.
With respect to body size, we found a positive correlation
between ﬁsh size and the prevalence of Anisakis, in accordance
with the results of several parasitological surveys on diﬀer-
ent ﬁsh species (Mattiucci etal. 2018 and references therein),
suggesting that ﬁsh size could be a good predictor of infection
with Anisakis spp. and of the associated risk of anisakiasis in
humans (Madrid etal. 2016). However, other research failed
to detect any relationship between ﬁsh length and the number
of Anisakis larvae in the edible parts of ﬁsh (Karl etal. 2011).
In addition, the time after capture and storage tempera-
ture can play an important role in deﬁning the distribution
of Anisakis larvae in ﬁsh ﬁlets (Cipriani etal. 2016). The
relationship between ﬁsh size and the zoonotic potential of
Anisakis in the ﬁsh host is therefore not always obvious.
Fish age, which is positively correlated to body size, is one
of the main factors to be considered in the analysis of infection
levels in long-lived parasites, such as Anisakis spp. (Abaunza
etal. 1995). Higher infection levels in older and larger ﬁsh
are the result of a bioaccumulation of parasites throughout
3118 Parasitology Research (2021) 120:3113–3122
the ﬁsh’s life span and, possibly, of ontogenetic dietary shifts.
Furthermore, larger ﬁsh feed at a higher rate with a variety of
potential intermediate/paratenic hosts, thus favoring higher
parasitization levels (Abattouy etal. 2011). In fact, larger
ﬁsh tend to occupy higher levels in the food chain with the
increased possibility of ingesting intermediate/paratenic hosts
parasitized with Anisakids (Strømnes and Andersen 2000).
In the present study, the sampled ﬁsh were stratiﬁed
according to the depth of capture (< 250m and > 250m).
Our results showed a statistically signiﬁcant correlation
values (P < 0.0001) between depth and prevalence of nema-
tode parasites, which are more prevalent in ﬁsh from deeper
waters (> 250m). Such a correlation could be explained
by the presence of larger (thus more parasitized) ﬁsh at a
greater depth. However, this variable appears to be a main
risk factor for Anisakid and Raphidascaridid infection in
commercially important marine ﬁsh, as previously reported
in a variety of teleost species (e.g., Sardina pilchardus,
Engraulis encrasicolus, Phycis blennoides) independently of
ﬁsh size (Pulleiro-Potel etal. 2015). Speciﬁc oceanographic
and ecological factors, such as temperature, oceanic cur-
rents, depth, salinity, and primary production, have been
identiﬁed as the main variables aﬀecting the distribution of
Anisakis spp. (Højgaard 1998; Kuhn etal. 2016).
In conclusion, our study provides information on the infec-
tion pattern of Anisakis and Hysterothylacium larvae in
T. trachurus from the Ligurian and Tyrrhenian Seas, and
the occurrence of the species A. pegreﬃi together with A.
pegreﬃi/A. simplex (s.s.) hybrids, and H. aduncum and H.
fabri, identiﬁed by molecular methods. Our results also sup-
port the hypothesis that infection with these parasites does
not aﬀect the condition of the ﬁsh host analyzed, and that
body size and depth are major drivers in determining infec-
tion levels with Anisakid and Raphidascaridid nematodes.
Author contribution Conceived the study: FM; designed the experi-
ment: FM, CP, PS, AM, MC; performed the ﬁeld activities and sam-
pling: VC, AM; performed the laboratory work: FM, VC, PT, AM,
GM; analyzed and interpreted the data: FM, FC, VC, PT, MC, AM,
AL; wrote the original draft of the manuscript: FM, PT, AM, MC, AL;
reviewed and edited the ﬁnal version of the manuscript: FM, PT, VC,
AM, PS, AL, CP, MG, FC, MC; supervision: FM.
Funding Open access funding provided by Università di Pisa within
the CRUI-CARE Agreement.
Data availability Not applicable.
Code availability Not applicable.
Ethics approval Not applicable.
Consent to participate Not applicable.
Consent for publication Not applicable.
Conflict of interest The authors declare no competing interests.
Open Access This article is licensed under a Creative Commons Attri-
bution 4.0 International License, which permits use, sharing, adapta-
tion, distribution and reproduction in any medium or format, as long
as you give appropriate credit to the original author(s) and the source,
provide a link to the Creative Commons licence, and indicate if changes
were made. The images or other third party material in this article are
included in the article’s Creative Commons licence, unless indicated
otherwise in a credit line to the material. If material is not included in
the article’s Creative Commons licence and your intended use is not
permitted by statutory regulation or exceeds the permitted use, you will
need to obtain permission directly from the copyright holder. To view a
copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/.
Abattouy N, Valero A, Benajiba MH, Lozano J, Martin-Sanchez J
(2011) Anisakis simplex s.l. parasitization in mackerel (Scomber
japonicus) caught in the North of Morocco – prevalence and
analysis of risk factors. Int J Food Microbiology 150:136–139.
https:// doi. org/ 10. 1016/j. ijfoo dmicro. 2011. 07. 026
Abaunza P, Villamor B, Pérez JR (1995) Infestation by larvae of
Anisakis simplex (Nematoda: Ascaridata) in horse mackerel,
Trachurus trachurus, and Atlantic mackerel, Scomber scombrus,
in ICES Divisions VIIIb, VIIIc and IXa (NNW of Spain). Sci
Abaunza P, Gordo L, Karlou-Riga C, Murta A, Eltink ATGW, San-
tamaría MG, Molloy J (2003) Growth and reproduction of horse
mackerel, Trachurus trachurus (Carangidae). Rev Fish Biol Fish
13(1):27–61. https:// doi. org/ 10. 1023/A: 10263 34532 390
Abaunza P, Murta AG, Campbell N, Cimmaruta R, Comesaña AS,
Dahle G, Comesañae AS, Dahle G, García SM, Gordo LS,
Iversen SA, MacKenzie K, Magoulas A, Mattiucci S, Molloy J,
Nascetti G, Pintob AL, Quinta R, Ramos P, Sanjuane A, Santos
AT, Stransky C, Zimmermann C (2008) Stock identity of horse
mackerel (Trachurus trachurus) in the Northeast Atlantic and
Mediterranean Sea: integrating the results from diﬀerent stock
identiﬁcation approaches. Fish Res 89(2):196–209. https:// doi.
org/ 10. 1016/j. ﬁshr es. 2007. 09. 022
Abollo E, Gestal C, Pascual S (2001) Anisakis infestation in marine ﬁsh
and cephalopods from Galician waters: an updated perspective.
Parasitol Res 87:492–499. https:// doi. org/ 10. 1007/ s0043 60100 389
Abollo E, Paggi L, Pascual S, D’Amelio S (2003) Occurrence of
recombinant genotypes of Anisakis simplex s.s. and Anisa-
kis pegreﬃi (Nematoda: Anisakidae) in an area of sympatry.
Infect Genet Evol 3(3):175–181. htt ps:// doi. org/ 10. 1016/ s1567-
Adroher FJ, Valero A, Ruiz-Valero J, Iglesias L (1996) Larval ani-
sakids (Nematoda: Ascaridoidea) in horse mackerel (Trachurus
trachurus) from the ﬁsh market in Granada (Spain). Parasitol Res
82(3):253–256. https:// doi. org/ 10. 1007/ s0043 60050 105
3119Parasitology Research (2021) 120:3113–3122
Alegria-Hernandez V (1994) Reproductive cycle and changes in con-
ditions of the horse mackerel (Trachurus trachurus L.) from the
Adriatic Sea. Acta Adriat 35:59–67
Angelucci G, Meloni M, Merella P, Sardu F, Madeddu S, Marrosu R,
Petza F, Salati F (2011) Prevalence of Anisakis spp. and Hyster-
othylacium spp. larvae in teleosts and cephalopods sampled from
waters oﬀ Sardinia. J Food Prot 74(10):1769–1775. https:// doi.
org/ 10. 4315/ 0362- 028x. jfp- 10- 482
Arcos JM, Oro D, Sol D (2001) Competition between the yellow-leg-
ged gull Larus cachinnans and Audouin’s gull Larus audouinii
associated with commercial ﬁshing vessels: the inﬂuence of sea-
son and ﬁshing ﬂeet. Mar Biol 139:807–816. https:// doi. org/ 10.
1007/ s0022 70100 651
Balbuena JA, Karlsbakk E, Kvenseth AM, Saksvik M, Nylund A (2000)
Growth and migration of third-stage larvae of Hysterothylacium
aduncum (Nematoda: Anisakidae) in larval herring Clupea haren-
gus. J Parasitol 86:1271–1275. https:// doi. org/ 10. 2307/ 32850 12
Bini G (1967). Atlante dei pesci delle coste italiane. Osteitti (Perci-
formi: Trichiuroidei, Scombroidei, Stromatoidei, Callionimoidei,
Ammoditoidei, Blennioidei) Mondo Sommerso, Roma
Bozzano A, Sardà FF (2002) Discard consumption rate and scaveng-
ing activity in the northwestern Mediterranean Sea. J Mar Sci
59:15–28. https:// doi. org/ 10. 1006/ jmsc. 2001. 1142
Bezerra TN, Decraemer W, Eisendle-Flöckner U, Hodda M, Holo-
vachov O, Leduc D, Miljutin D, Mokievsk V, Peña Santiago R,
Sharma J, Smol N, Tchesunov A, Venekeym V, Zhao Z, Vanreusel
A (2020) Nemys: world database of nematodes. Hysterothylacium
Ward & Magath, 1917 world wide. Accessed at: http:// www. marin
espec ies. org/ aphia. php?p= taxde tails & id= 19962
Bristow GA (1990) Dødelighet hos kveitelarver og yngel i startfôrings-
fasen. Norsk Fiskeoppdrett 15:40–43
Bush AO, Laﬀerty KD, Lotz JM, Shostak AW (1997) Parasitology
meets ecology on its own terms: Margolis etal. revisited. J Para-
sitol 83(4):575–583. https:// doi. org/ 10. 2307/ 32842 27
Carbonara P, Casciaro L, Bitetto I, Spedicato MT (2012) Reproductive
cycle and length at ﬁrst maturity of Trachurus trachurus in the
central-western Mediterranean seas/ciclo riproduttivo e taglia di
prima maturitá di Trachurus trachurus nei mari del mediterraneo
centro-occidentale. Biol Mar Mediterr 19(1):204–205
Cavallero S, Ligas A, Bruschi F, D’Amelio S (2012) Molecular iden-
tiﬁcation of Anisakis spp. from ﬁshes collected in the Tyrrhenian
Sea (NW Mediterranean). Vet Parasitol 187:563–566. https:// doi.
org/ 10. 1016/j. vetpar. 2012. 01. 033
Cavallero S, Costa A, Caracappa S, Gambetta B, D’Amelio S (2014)
Putative hybrids between two Anisakis cryptic species: molecular
genotyping using high resolution melting. Exp Parasitol 146:87–
93. https:// doi. org/ 10. 1016/j. exppa ra. 2014. 08. 017
Cipriani P, Acerra V, Bellisario B, Sbaraglia GL, Cheleschi R, Nascetti
G, Mattiucci S (2016) Larval migration of the zoonotic parasite
Anisakis pegreﬃi (Nematoda: Anisakidae) in European anchovy,
Engraulis encrasicolus: implications to seafood safety. Food Con-
trol 59:148–157. https:// doi. org/ 10. 1016/j. foodc ont. 2015. 04. 043
Costa A, Cammilleri G, Graci S, Buscemi MD, Vazzana M, Principato
D, Giangrosso G, Ferrantelli V (2016) Survey on the presence of
A. simplex s.s. and A. pegreﬃi hybrid forms in Central-Western
Mediterranean Sea. Parasitol Int 65:696–701. https:// doi. org/ 10.
1016/j. parint. 2016. 08. 004
D’Amelio S, Mathiopoulos K, Santos CP, Pugachev ON, Webb SC,
Picanco M, Paggi L (2000) Genetic markers in ribosomal DNA for
the identiﬁcation of members of the genus Anisakis (Nematoda:
Ascaridoidea) deﬁned by polymerase chain reaction-based restric-
tion fragment length polymorphism. Int J Parasitol 30:223–226.
https:// doi. org/ 10. 1016/ s0020- 7519(99) 00178-2
Debenedetti ÁL, Madrid E, Trelis M, Codes FJ, Gil-Gómez F, Sáez-
Durán S, Fuentes MV (2019) Prevalence and risk of anisakid
larvae in fresh ﬁsh frequently consumed in Spain: an overview.
Fishes 4(1):13. https:// doi. org/ 10. 3390/ ﬁshe s4010 013
Dias MKR, Neves LR, Marinho RDGB, Pinheiro DA, Tavares-Dias
M (2015) Parasitismo em tambatinga (Colossoma macropomum
x Piaractus brachypomus, Characidae) cultivados na Amazônia.
Brasil Acta Amazon 45(2):231–238. https:// doi. org/ 10. 1590/
1809- 43922 01400 974
Fernández-Caldas E, Quirce S, Marañó F, Gómez MLD, Botella HG,
Román RL (1998) Allergenic cross-reactivity between third stage
larvae of Hysterothylacium aduncum and Anisakis simplex. J
Allergy Clin Immunol 104(4):554–555. https:// doi. org/ 10. 1016/
S0091- 6749(98) 70364-1
Fioravanti ML, Gavaudan S, Vagnini V, and Tonucci F (2003) Indagine
sulla diﬀusione di larve di Anisakis e Hysterothylacium (Nema-
toda, Anisakidae) in pesci del mar Adriatico Centrale. Atti Soc It
Sci Vet LVII: 213–214. Ischia (Napoli)
Gancitano V, Basilone G, Bonanno A, Cuttitta A, Garofalo G, Giusto GB,
Gristina M, Mazzola S, Patti B, Sinacori G, Fiorentino F (2011) - GSA
16. Stretto di Sicilia. In Rapporto annuale sullo stato delle risorse bio-
logiche dei mari circostanti l’Italia: anno 2009. 19 (Suppl. 1): 90–116
Gibbons LM (2010) Keys to the nematode parasites of vertebrates,
supplementary volume. CAB International, Wallingford, p 416
Goﬀredo E, Azzarito L, Di Taranto P, Mancini ME, Normano G,
Didona A, Faleo S, Occhiochiuso G, D’Attoli L, Pedarra C, Pinto
P, Camilleri G, Graci S, Sciortino S, Costa A (2019) Prevalence of
anisakid parasites in ﬁsh collected from Apulia region (Italy) and
quantiﬁcation of nematode larvae in ﬂesh. Int J Food Microbiol
292:159–170. https:// doi. org/ 10. 1016/j. ijfoo dmicro. 2018. 12. 025
Hartwich G (2009) Ascaridoidea. In: Anderson RC, Chabaud AG,
Willmott S (eds) Keys to the nematode parasites of vertebrates:
archival volume. CAB International, Wallingford, pp 309–323
Højgaard DP (1998) Impact of temperature, salinity and light on hatch-
ing of eggs of Anisakis simplex (Nematoda, Anisakidae), isolated
by a new method, and some remarks on survival of larvae. Sarsia
83(1):21–28. https:// doi. org/ 10. 1080/ 00364 827. 1998. 10413 666
Ichalal K, Ramdane Z, Ider D, Kacher M, Iguerouada M, Trilles JP,
Courcot L, Amara R (2015) Nematodes parasitizing Trachurus
trachurus (L.) and Boops boops (L.) from Algeria. Parasitol Res
114(11):4059–4068. https:// doi. org/ 10. 1007/ s00436- 015- 4633-6
Ishikura H, Kikuchi K, Nagasawa K, Ooiwa T, Takamiya H, Sato N,
Sugane K (1993) Anisakidae and anisakidosis. Prog Clin Parasitol
3:43–102. https:// doi. org/ 10. 1007/ 978-1- 4612- 2732-8_3
Karl H, Baumann F, Ostermeyer U, Kuhn T, Klimpel S (2011) Ani-
sakis simplex (ss) larvae in wild Alaska salmon: no indication of
post-mortem migration from viscera into ﬂesh. Dis Aquat Org
94(3):201–209. https:// doi. org/ 10. 3354/ dao02 317
Kuhn T, Cunze S, Kochmann J, Klimpel S (2016) Environmental vari-
ables and deﬁnitive host distribution: a habitat suitability mod-
elling for endohelminth parasites in the marine realm. Sci Rep
6(1):1–14. https:// doi. org/ 10. 1038/ srep3 0246
Lagrue C, Poulin R (2015) Measuring ﬁsh body condition with or with-
out parasites: does it matter? J Fish Biol 87(4):836–847. https://
doi. org/ 10. 1111/ jfb. 12749
Le Cren ED (1951) The length-weight relationship and seasonal cycle
in gonad weight and condition in the perch (Perca ﬂuviatilis). J
Anim Ecol 20:201–219. https:// doi. org/ 10. 2307/ 1540
Ligas A, Mannini A, Carpentieri P, Mancusi C, Sartor P, De Ranieri S
(2012) Length-weight relationship in demersal species from Ligu-
rian and northern-central Tyrrhenian Sea. Relazione taglia-peso in
specie demersali del Mar Ligure e Tirreno centro-settentrionale.
Biol Mar Mediterr 19(1):212
Lembo G, Spedicato MT, Carbonara P, Casciaro L, Bitetto I, Facchini
MT, Zupa W, & Gaudio P (2012) Programma Nazionale Italiano
per la Raccolta di Dati alieutici 2012. Campionamento biologico
delle catture. Sezioni C ed E. Rapporto Finale. GSA 18 Adriatico
3120 Parasitology Research (2021) 120:3113–3122
Meridionale, COISPA Tecnologia e Ricerca, Italia. (Technical
MacKenzie K, Campbell N, Mattiucci S, Ramos P, Pinto AL, Abaunza
P (2008) Parasites as biological tags for stock identification
of Atlantic horse mackerel Trachurus trachurus L. Fish Res
89(2):136–145. https:// doi. org/ 10. 1016/j. ﬁshr es. 2007. 09. 031
Madrid E, Gil F, García M, Debenedetti AL, Trelis M, Fuentes MV
(2016) Potential risk analysis of human anisakiasis through the
consumption of mackerel, Scomber scombrus, sold at Spanish
supermarkets. Food Control 66:300–305. https:// doi. org/ 10.
1016/j. foodc ont. 2016. 02. 025
Manfredi MT, Crosa G, Galli P, Ganduglia S (2000) Distribution of
Anisakis simplex in ﬁsh caught in the Ligurian Sea. Parasitol Res
86(7):551–553. https:// doi. org/ 10. 1007/ s0043 60000 202
Mattiucci S, Nascetti G (2006) Molecular systematics, phylogeny and
ecology of anisakid nematodes of the genus Anisakis Dujardin,
1845: an update. Parasite 13:99–113. https:// doi. org/ 10. 1051/
paras ite/ 20061 32099
Mattiucci S, Nascetti G (2008) Advances and trends in the molecular
systematics of anisakid nematodes, with implications for their
evolutionary ecology and host parasite co-evolutionary processes.
Adv in Parasitol 66:47–148. https:// doi. org/ 10. 1016/ S0065-
Mattiucci S, D’Amelio S (2014) Anisakiasis. In: Bruschi F (ed)
Helminth infections and their impact on global public health.
Springer, Vienna, pp 325–365. https:// doi. org/ 10. 1007/ 978-3-
7091- 1782-8_ 11
Mattiucci S, Abaunza P, Ramadori L, Nascetti G (2004) Genetic iden-
tiﬁcation of Anisakis larvae in European hake from Atlantic and
Mediterranean waters for stock recognition. J Fish Biol 65:495–
510. https:// doi. org/ 10. 1111/j. 0022- 1112. 2004. 00465.x
Mattiucci S, Cipriani P, Webb SC, Paoletti M, Marcer F, Bellisario
B, Gibson DI, Nascetti G (2014) Genetic and morphological
approaches distinguish the three sibling species of the Anisakis
simplex species complex, with a species designation as Anisakis
berlandi n. sp. for A. simplex sp. C (Nematoda: Anisakidae). J
Parasitol 100(2):199–214. https:// doi. org/ 10. 1645/ 12- 120.1
Mattiucci S, Cipriani P, Levsen A, Paoletti M, Nascetti G (2018)
Molecular epidemiology of Anisakis and anisakiasis: an ecologi-
cal and evolutionary road map. Adv Parasitol 99:93–263. https://
doi. org/ 10. 1016/ bs. apar. 2017. 12. 001
Mattiucci S, Bello E, Paoletti M, Webb SC, Timi JT, Levsen A, Cip-
riani P, Nascetti G (2019) Novel polymorphic microsatellite loci
in Anisakis pegreﬃi and A. simplex (s.s.) (Nematoda: Anisaki-
dae): implications for species recognition and population genetic
analysis. Parasitology 146(11):1387–1403. https:// doi. org/ 10.
1017/ S0031 18201 90007 4X
MEDISEH (2013) Mediterranean Sensitive Habitats. Giannoulaki,
M., Belluscio, A., Colloca, F., Fraschetti, S., Scardi, M., Smit,
C., Panayotidis, P., Valavanis, V., Spedicato, M. T., DG MARE
speciﬁc contract SI2.600741, ﬁnal report, 557 pp.
Meloni M, Angelucci G, Merella P, Siddi R, Deiana C, Orru G, Salati
F (2011) Molecular characterization of Anisakis larvae from ﬁsh
caught oﬀ Sardinia. Journal Parasitol 97:908–914. https:// doi. org/
10. 1645/ GE- 2742.1
Morton B, Yuen WY (2000) The feeding behaviour and competition
for carrion between two sympatric scavengers on a sandy shore
in Hong Kong: the gastropod, Nassarius festivus (Powys) and the
hermit crab, Diogenes edwardsii (De Haan). J Exp Mar Bio Ecol
246:1–29. https:// doi. org/ 10. 1016/ s0022- 0981(99) 00170-7
Oro D, Ruiz X (1997) Exploitation of trawler discards by breeding
seabirds in the north-western Mediterranean: diﬀerences between
the Ebro Delta and the Balearic Islands areas. ICES J Mar Sci
54:695–707. https:// doi. org/ 10. 1006/ jmsc. 1997. 0246
Pauly D (1984) Fish population dynamics in tropical waters: a manual
for use with programmable calculators. ICLARM studies and
reviews 8. International Center for Living Aquatic Resources
Management, Manila, Philippines, 325.
Podolska M, Horbowy J (2003) Infection of Baltic herring (Clupea
harengus membras) with Anisakis simplex larvae, 1992–1999:
a statistical analysis using generalized linear models. J Mar Sci
60:85–93. https:// doi. org/ 10. 1006/ jmsc. 2002. 1323
Pulleiro-Potel L, Barcala E, Mayo-Hernández E, Muñoz P (2015) Sur-
vey of anisakids in commercial teleosts from the western Mediter-
ranean Sea: infection rates and possible eﬀects of environmental
and ecological factors. Food Control 55:12–17. https:// doi. org/ 10.
1016/j. foodc ont. 2015. 02. 020
Roca-Geronès X, Montoliu I, Godínez-González C, Fisa R, Shamsi
S (2018) Morphological and genetic characterization of Hyster-
othylacium Ward e Magath, 1917 (Nematoda: Raphidascarididae)
larvae in horse mackerel, blue whiting and anchovy from Spanish
Atlantic and Mediterranean waters. J Fish Dis 41(10):1463–1475.
https:// doi. org/ 10. 1111/ jfd. 12825
Šantić M, Rađa B, Paladin A (2011) Condition and length-weight rela-
tionship of the horse mackerel (Trachurus trachurus L.) and the
Mediterranean horse mackerel (Trachurus mediterraneus L.) from
the eastern Adriatic Sea. Arch Biol Sci 63(2): 421–428. https://
doi. org/ 10. 2298/ ABS11 02421S
Santojanni A, Angelini S, Belardinelli A, Carpi P, Cingolani N, Colella
S, Croci C, Donato F, Martinelli M, Panﬁli M (2013) - Programma
Nazionale per la raccolta dei dati alieutici. Campionamento Bio-
logico delle catture della pesca professionale di demersali e pic-
coli pelagici in Alto e Medio Adriatico (GSA 17). Anno 2012.
Progetto del Ministero Italiano delle Politiche Agricole, Alimen-
tari e Forestali. ISMAR-CNR. Relazione Finale: 205 pp. (Techni-
Santos EF, Tavares-Dias M, Pinheiro DA, Neves LR, Marinho RDGB,
Dias MKR (2013) Fauna parasitária de tambaqui Colossoma
macropomum (Characidae) cultivado em tanque-rede no estado
do Amapá. Amazônia Oriental Acta Amaz 43(1):105–111. https://
doi. org/ 10. 1590/ S0044- 59672 01300 01000 13
SAS, JMP (2007) User’s guide, ver. 7.0 SAS Inst. Cary, NC, USA
Serracca L, Cencetti E, Battistini R, Rossini I, Prearo M, Pavoletti E,
Ercolini C (2013) Survey on the presence of Anisakis and Hys-
terothylacium larvae in ﬁshes and squids caught in Ligurian Sea.
Vet Parasitol 196(3–4):547–551. https:// doi. org/ 10. 1016/j. vetpar.
2013. 02. 024
Silva RM, Tavares-Dias M, Dias MWR, Dias MKR, Marinho RDGB
(2013) Parasitic fauna in hybrid tambacu from ﬁsh farms. Pesqui
Agropecu Bras 48(8):1049–1057. https:// doi. org/ 10. 1590/ S0100-
204X2 01300 08000 34
Smith JW (1983) Larval Anisakis simplex (Rudolphi, 1809, det.
Krabbe, 1878) and larval Hysterothylacium sp. (Nematoda:
Ascaridoidea) in euphausiids (Crustacea: Malacostraca) in the
north-east Atlantic and northern North Sea. J Helminthol 57(2):
167–177. https:// doi. org/ 10. 1017/ S0022 149X0 00094 33
Spedicato MT, Lembo G, Carbonara C, Casciaro L, Bitetto I, Facchini
MT, Zupa W, Gaudio P (2012) -Programma Nazionale Italiano
per la raccolta di dati alieutici 2012. Campionamento Biologico
delle catture. Sezioni C ed E. Rapporto Finale, GSA 10 - Tirreno
centro-meridionale. COISPA Tecnologia e Ricerca, Italia 140 pp.
Spedicato MT, Massutí E, Mérigot B, Tserpes G, Jadaud A, Relini G
(2019) The MEDITS trawl survey speciﬁcations in an ecosystem
approach to ﬁshery management. Sci Mar 83S1: 9–20. https:// doi.
org/ 10. 3989/ scimar. 04915. 11X
Strømnes E, Andersen K (2000) “Spring rise” of whaleworm (Anisakis
simplex; Nematoda, Ascaridoidea) third-stage larvae in some ﬁsh
3121Parasitology Research (2021) 120:3113–3122
species from Norwegian waters. Parasitol Res 86:619–624. https://
doi. org/ 10. 1007/ pl000 08541
Tedesco P, Gustinelli A, Caﬀara M, Patarnello P, Terlizzi A, Fioravanti
ML (2018) Hysterothylacium fabri (Nematoda, Raphidascaridi-
dae) in Mullus surmuletus (Perciformes, Mullidae) and Uranosco-
pus scaber (Perciformes, Uranoscopidae) from the Mediterranean.
J Parasitol 104(3):262–274. https:// doi. org/ 10. 1645/ 17- 115
Valero A, Terrados S, Díaz V, Reguera V, Lozano J (2003) Determi-
nation of IgE in the serum of patients with allergic reactions to
four species of ﬁsh-parasite anisakids. J Investig Allergol Clin
Verani JR, Sato Y, Fenerich-Verani N, Vieira LJS (1997) Avaliação de
fêmeas de espécies ícticas aptas à indução reprodutiva: critério
embasado no fator de condição relativo. Seminário Regional De
Yagi K, Nagasawa K, Ishikura H, Nakagawa A, Sato N, Kikuchi K,
Ishikura H (1996) Female worm Hysterothylaicum aduncum
excreted from human: a case report. Jpn J Parasitol 45:12–23
Zhu XQ, Gasser RB, Podolska M, Chilton NB (1998) Characterisa-
tion of anisakid nematodes with zoonotic potential by nuclear
ribosomal DNA sequences. Int J Parasitol 28:1911–1921. https://
doi. org/ 10. 1016/ S0020- 7519(98) 00150-7
Publisher’s note Springer Nature remains neutral with regard to
jurisdictional claims in published maps and institutional aﬃliations.
3122 Parasitology Research (2021) 120:3113–3122
Terms and Conditions
Springer Nature journal content, brought to you courtesy of Springer Nature Customer Service Center GmbH (“Springer Nature”).
Springer Nature supports a reasonable amount of sharing of research papers by authors, subscribers and authorised users (“Users”), for small-
scale personal, non-commercial use provided that all copyright, trade and service marks and other proprietary notices are maintained. By
purposes, Springer Nature considers academic use (by researchers and students) to be non-commercial.
These Terms are supplementary and will apply in addition to any applicable website terms and conditions, a relevant site licence or a personal
subscription. These Terms will prevail over any conflict or ambiguity with regards to the relevant terms, a site licence or a personal subscription
(to the extent of the conflict or ambiguity only). For Creative Commons-licensed articles, the terms of the Creative Commons license used will
We collect and use personal data to provide access to the Springer Nature journal content. We may also use these personal data internally within
ResearchGate and Springer Nature and as agreed share it, in an anonymised way, for purposes of tracking, analysis and reporting. We will not
otherwise disclose your personal data outside the ResearchGate or the Springer Nature group of companies unless we have your permission as
While Users may use the Springer Nature journal content for small scale, personal non-commercial use, it is important to note that Users may
use such content for the purpose of providing other users with access on a regular or large scale basis or as a means to circumvent access
use such content where to do so would be considered a criminal or statutory offence in any jurisdiction, or gives rise to civil liability, or is
falsely or misleadingly imply or suggest endorsement, approval , sponsorship, or association unless explicitly agreed to by Springer Nature in
use bots or other automated methods to access the content or redirect messages
override any security feature or exclusionary protocol; or
share the content in order to create substitute for Springer Nature products or services or a systematic database of Springer Nature journal
In line with the restriction against commercial use, Springer Nature does not permit the creation of a product or service that creates revenue,
royalties, rent or income from our content or its inclusion as part of a paid for service or for other commercial gain. Springer Nature journal
content cannot be used for inter-library loans and librarians may not upload Springer Nature journal content on a large scale into their, or any
other, institutional repository.
content on this website and may remove it or features or functionality at our sole discretion, at any time with or without notice. Springer Nature
may revoke this licence to you at any time and remove access to any copies of the Springer Nature journal content which have been saved.
To the fullest extent permitted by law, Springer Nature makes no warranties, representations or guarantees to Users, either express or implied
with respect to the Springer nature journal content and all parties disclaim and waive any implied warranties or warranties imposed by law,
including merchantability or fitness for any particular purpose.
Please note that these rights do not automatically extend to content, data or other material published by Springer Nature that may be licensed
from third parties.
If you would like to use or distribute our Springer Nature journal content to a wider audience or on a regular basis or in any other manner not
expressly permitted by these Terms, please contact Springer Nature at