Host characteristics and infection level of an intestinal parasite Corynosoma strumosum (Acanthocephala) in the Kuril harbor seal of Erimo Cape, Hokkaido, Japan

Parasitology International 67 (2018) 237–244

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Host characteristics and infection level of an intestinal parasite Corynosoma strumosum (Acanthocephala) in the Kuril harbor seal of Erimo Cape, Hokkaido, Japan

T

Tadashi Kaimotoa, Takuya Hirazawaa, Takahito Masubuchia, Aya Morohoshia, ⁎ Hirotaka Katahiraa,b,c, , Mari Kobayashia a b c

Department of Aqua-Bioscience and Industry, Faculty of Bioindustry, Tokyo University of Agriculture, Abashiri, Hokkaido 099-2493, Japan Faculty of Environmental Earth Science, Hokkaido University, N10W5, Sapporo, Hokkaido 060-0810, Japan NPO Marine Wildlife Center of Japan, 8-14-8 Shiomi, Abashiri, Hokkaido 093-0042, Japan

A R T I C L E I N F O

A B S T R A C T

Keywords: Kuril harbor seal Parasite Biological indicator Feeding habits

The Kuril harbor seal around Hokkaido is presently recovering from a resource crisis while conflicts with local fisheries have become a concern. However, its feeding habits, which are fundamental information for taking proper preventive measures, are still poorly understood. We thus examined the infection status of a trophicallytransmitted parasite, Corynosoma strumosum in the seals of Erimo Cape, to assess the host's feeding habits with a practical view of the parasite as a biological indicator. A total of 2802 worms were found from 20 male and 20 female by-caught animals in salmon set nets within local fisheries during August to November 2014. The parasite abundance was explained mainly by the host's developmental stage and intestinal length while weakly affected by gender and body size, through an estimation of generalized linear models combined with hierarchical partitioning. Considering the past records that demersal fishes are the probable main sources of infection, the infection level may owe to individual host differences regarding these sources and/or feeding grounds with relating the host characteristics. This supports that the resource management of Kuril harbor seals requires careful consideration of the individual differences in feeding behavior.

1. Introduction The Kuril harbor seal Phoca vitulina stejnegeri Allen, 1902 is a subspecies of P. vitulina Linnaeus, 1758, with a distribution from the tip of the Alaskan Peninsula, through the Aleutian Islands, Kamchatka, Kuril Islands and down to the Erimo Cape in southeastern Hokkaido, Japan [1–3]. This seal is known to exhibit sedentary habitation at a preferred landing place (i.e. haulout site) [4], where individuals use it for resting, reproduction and molting [5]. On the shores of Hokkaido, 8 of 11 haulout sites have so far been recognized as breeding sites (two haulout sites were already collapsed) [6–7], and population censuses have been conducted every year since the 1970's [8] (see also [7]). According to an outdated record by Inukai [9], a total of 1500–4800 individuals were thought to have been originally distributed in Hokkaido [8], but they had declined to less than a few hundred in the early 1970's due to anthropogenic disturbances (e.g. overhunting) [8,10]. Thereafter, population size in Hokkaido has gradually been increasing over the last four decades [7], in large part due to ⁎

protection under the Revised Birds and Mammals Protection Law of 2002 (Ministry of the Environment, Government of Japan; http:// law.e-gov.go.jp/htmldata/H14/H14F18001000028.html). With a recovering population size, however, conflicts between the seals and local fisheries have become a serious issue [12]; indeed, economic losses have been calculated for salmon set net fishing (e.g. [13–16]). A triune consensus among scientists, administrators and local people was thus required for the proper management (see [11,17–19]), but it has not reached a conclusion as of yet because insufficient information is currently available for ecological features of this seal under wild conditions. Most of the information, concerning these animals such as predator-prey interactions and behavior around the haulout sites, are showing little progress despite a surge in the conservation awareness from the late 1980's (see [6]). To construct a better compromise between seal conservation and local economic activities, further investigation, especially on the feeding habits of these seals are needed. Parasites are sometimes used as tags or indicators to provide biological information on their hosts [20–21]. In particular, endoparasite species, which have trophically-transmitted life cycles, infecting via

Corresponding author at: Department of Aqua-Bioscience and Industry, Faculty of Bioindustry, Tokyo University of Agriculture, Abashiri, Hokkaido 099-2493, Japan. E-mail address: [email protected] (H. Katahira).

https://doi.org/10.1016/j.parint.2017.12.008 Received 24 December 2015; Received in revised form 9 April 2017; Accepted 28 December 2017 Available online 30 December 2017 1383-5769/ © 2017 Elsevier B.V. All rights reserved.

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was opened in turn using forceps, and parasite specimens were collected using tweezers under visual check. To prevent overlooking any parasite specimens, each section was subsequently washed with tap water and the intestinal contents were placed in plastic bottles; after the sediment settled at the bottom, it was extracted and put into a petri dish, and checked under a stereomicroscope. For confirmation of the species identification, some specimens were randomly collected, fixed with 70% ethanol under slight pressure and kept as flattened specimens with made transparent by 70% glycerin-ethanol solution or stained with alum carmine. The stained samples were subsequently dehydrated in a series of ascending concentrations of ethanol, cleared in xylene and mounted in Canada balsam. The remaining specimens were preserved in a bottle filled with 70% ethanol, and separated according to intestinal section. Identification was based on the morphological character of proboscis shape, number of hook rows and hooks per row on the proboscis, hook size and covering range of the trunk spine, following the previous descriptions [44–48], by using an Olympus BX51 light microscope with phase contrast optics. Drawings of specimens were made with the aid of a drawing tube. Measurements were taken using an ocular micrometer; all measurement values were provided as the mean followed by the range in parenthesis.

predator-prey relationships, can provide useful insights into the feeding habits of the targeted hosts in a given food web [20,22–23]. Under the circumstances in which quantitative data of a host's feeding habits is hard to be obtained due to difficulty of field sampling, the parasitological approach has the potential to support stomach content surveys and stable isotope analysis as an alternative method. Corynosoma strumosum (Rudolphi, 1802) (Acanthocephala: Polymorphidae) is an intestinal parasite commonly found in pinnipeds in the northern hemisphere [24–27]. This species has also been reported in the seals off the coast of Japan (see [28–29]), including the Kuril harbor seal [30–31]. Its life cycle is known as a complex type, using marine amphipods as its first intermediate host (e.g. [32]) and coastal fishes as paratenic hosts (e.g. [33–34]); seals are definitive hosts for this parasite, with infection via feeding on the intermediate host organisms. We recently investigated infection status of C. strumosum in the Kuril harbor seals by-caught from Erimo Cape of Hokkaido, Japan, while considering the practical aspects of parasites as biological indicators. This paper describes the details of its host utilization and relationships between the parasite infection and host's characteristics. Based on these findings, feeding habits of this seals are discussed. 2. Material and methods

2.4. Statistical analyses 2.1. Study site and host collection Infection indices, i.e. prevalence (percentage of infected host individuals), abundance (number of individual parasites from examined host), intensity (number of individual parasites from infected host) and abundance (number of individual parasites from examined host), were used in accordance with the definition of Bush et al. [49]. To elucidate the relationship between parasite infection and host characteristics, hierarchical partitioning (HP) and generalized linear models (GLMs) were applied to the abundance data. In these analyses, eight explanatory variables were initially assumed as candidates; those were gender (male or female), developmental stage (yearling, sub-adult and adult), age (year), TL (cm), W (kg), IL (m), B (cm) and Fulton's condition factor (K) calculated as W/TL3 × 106 (see [50]). Negative binomial error distribution with log link function was employed for the model fitting, by following the known law that macroparasites generally represent aggregated distribution in a given host population (e.g. [51]). HP was firstly performed to check independent and conjoint importance of explanatory variables in explaining variance of the response variable (i.e. the parasite abundance) [52–54]. This analysis jointly uses all possible models, represented as combinations of explanatory variables, in GLMs, and averages the improvement in fit for each variable, both independently and jointly, across all these models [52–55]. Independent and conjoint contribution of each variable is provided as percentage explaining variation in the response variable; conjoint values can be negative when the effect of the variables is suppressed by the presence of other variables [52–53]. A shape parameter (i.e. theta) of the negative binomial distribution, obtained from the full model fitting the parasite abundance, was tentatively postulated in our estimation. Significance of the independent effect was estimated as Z-score, with upper 95% confidence limit > 1.65, using 1000 times of randomization procedure [56]. Since HP approach just provides the contribution of explanatory variables to the response variables, detail relationships between the effective variables and the parasite abundance were supplied by GLMs fitting; the accuracy of the independent contribution in HP was additionally confirmed by a model selection in GLMs. Due to a possibility of multi-collinearity between these candidate variables, we checked their correlations and variance inflation factor (VIF) prior to applying GLMs. The candidate models were ranked by Akaike's information criterion (AIC; [57]). The difference in AIC value (ΔAIC) between a constructed model and an optimal model with the lowest AIC value was

Erimo Cape (41°55′28″N, 143°14′57″E) is a locality corresponding to the southwestern limit of the distribution in the Kuril harbor seal [6]. This is the largest haulout site in Hokkaido with a population size up to 500 individuals [7]. The details of this site are available elsewhere (e.g. supplemental article in Kobayashi et al. 2014); the seal population at this site is about 200 km away from other haulout sites in the eastern Hokkaido, and due to this geographic distance, it is isolated from other sites [35–38]. In this area, many seals are accidentally caught with salmon set nets during the commercial fishing season [15]. The individuals examined in our survey (i.e. 20 males and 20 females) were randomly obtained as a subset of individuals from these by-caught ones during 19 August 2014 to 17 November 2014. All dead-seals were immediately measured for total length (TL), weight (W) and thickness of dorsal blubber (B), sampled their whole skulls for age determination and dissected to remove the digestive tract for the parasite examination. The digestive tracts were further separated into stomach and intestine and preserved in a freezer. The frozen intestines were brought to laboratories in Abashiri city (i.e. Tokyo University of Agriculture) or Sapporo city (i.e. Hokkaido University) where they were examined for parasites at a later date. 2.2. Age determination For age determination, upper right canine teeth were taken from each skull, sectioned 10 μm by cryostat (Leica co. Ltd) and stained by Delafield's hematoxylin, following the fundamental methods in the textbook [39–40]. Ages were estimated based on a count of cemntum annuli [41]. The assumed mean birth date was set in May [42]. Ages were calculated to add the 0, 0.5 or 1 year old to accommodate differences in the timing of collections. After age determination, we classified their growth stage (i.e. yearlings were 0 and 0.5 year olds, sub-adults were from 1 to 2 year olds and adults were 5 or older in males and 4 or older in females [43]) by estimated age. 2.3. Parasite sampling After thawing the frozen intestines, their length (IL) was measured in meters (m). Each sample of the intestine was subdivided equally into 10 sections, and numbered from stomach side to anal side. Each section 238

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Min.–max. intensity (mean ± SD)

1–58 (23.2 ± 19.5) 2–125 (36.3 ± 44.7) 136–613 (374.5 ± 337.3) 24–147 (56.6 ± 41.2) 12–180 (53.3 ± 58.1) 5–742 (373.5 ± 521.1) 9 (90) 6 (75) 2 (100) 13 (86.7) 3 (100) 2 (100) 15.9–22.7 15.6–26.9 21.8–26.4 16.2–23.4 17.2–21.6 20.9–28.0

(18.8 (20.2 (24.1 (19.3 (19.3 (24.5

± ± ± ± ± ±

1.8) 3.1) 3.2) 2.3) 2.2) 5.0)

In the 40 individuals examined, male seals consisted of 10 yearlings, 8 youths, and 2 adults, while the female was composed of 15, 3 and 2, respectively (Table 1). Body weight ranged from 22 to 132 kg (mean ± SD = 47.4 ± 22.5 kg); the individual that weighed the least was a female yearling, while the heaviest individual was an adult male. Intestinal length ranged from 15.6 to 28.0 m (mean ± SD = 20.0 ± 2.9 m), with longer length at later growth stages.

31.0–35.5 (33.6 ± 1.6) 49.0–67.0 (58.6 ± 6.0) 89.0–132.0 (110.5 ± 30.4) 22.0–48.5 (35.7 ± 9.1) 48.0–58.0 (52.3 ± 5.1) 67.0–110.0 (88.5 ± 30.4) (125.9 (149.6 (182.2 (124.3 (142.8 (163.0

± ± ± ± ± ±

5.7) 3.9) 17.0) 10.6) 6.3) 4.2)

Of the 40 individuals, 35 (prevalence, 87.5%) were infected with an acanthocephalan (Table 1). All parasite specimens randomly collected were identical to C. strumosum (Fig. 1a,b), with the proboscis containing 18–20 (usually 18) longitudinal rows of 10 or 11 (usually 10) hooks each. Morphological details of each of the five stained mature males and gravid females were as follows; body length was 6.0 (5.4–6.9) mm and 7.3 (7.0–8.0) mm in males and females, respectively; the size of the proboscis was 537 (465–620) μm and 617 (585–640) μm in males and females, respectively; the hindmost hook in the anterior five or six (rarely seven) hooks of each row were largest in size and had prominent simple roots (74 [70–80] μm in male and 81.5 [77.5–85] μm in female) longer than the projecting thorn (60.5 [55–65] μm in male and 73 [67.5–75] μm in female); at a short distance behind these largest-sized hooks, near the proximal end of the proboscis was further armed with four or five hooks having small roots in the shape of an inverted Y; the trunk could be distinguished into anterior swollen and posterior cylindrical parts; the trunk spine was limited to the middle of the anterior swollen part on the dorsal side while extended to about one third of the posterior cylindrical portion on the ventral side, and appeared again on the end of the trunk; the size of the trunk spine in the vicinity of the neck was 30.5 (30–32.5) μm and 34 (32.5–35) μm in males and females, respectively; eggs (n = 10) of gravid females represented elliptical shape, with 99.8 (95–107.5) μm in length and 27.3 (25–30) μm in width (measurements taken through body-wall of mounted gravid females). A total of 2802 worms were recovered from the infected seals. The parasite individuals were mainly found from the latter part of the intestine (Fig. 2). Mean intensity and abundance of C. strumosum was 80.06 and 70.05 individuals, respectively. The maximum intensity was 742 individuals found in an adult female (with TL 166 cm and 110 kg) (Table 1, Fig. 3). 3.3. Infection level and host characteristics The parasite abundance similarly varied with host characteristics, especially in developmental stage, age, TL, W, IL, B and K (Fig. 3), but HP analysis differentiated that the independent effect of age (31.9%)

Female

10 8 2 15 3 2 Male

Yearling (0) Sub-adult (1–2) Adult (6, 12) Yearling (0) Sub-adult (1–2) Adult (4, 32)

115.4–135.4 141.8–153.8 170.1–194.2 111.0–144.6 137.7–149.9 160.0–166.0

Min.–max. W (kg)(mean ± SD)

3. Results

3.2. Parasite occurrence

No. of examined

Min.–max. TL (cm)(mean ± SD)

checked for the model selections; as a rule of thumb, a model with ΔAIC < 2 is substantially supported and can be considered in making data inference (see [57]). In all models with ΔAIC < 2, relative coefficient values of the selected variables were estimated including two standard deviations, i.e. 95% confidence interval (CI). Incidentally, since one male and female with the largest body size in each gender showed extremely high abundance of the parasite infection, there was concern that the model fittings might be biased. We thus additionally used subset data in which those individuals were removed to compare with whole data analysis. All statistical tests were performed by using R. 3.3.2 [58], with MASS package for GLMs construction, hier.part package for HP, DAAG package for VIF and coefplot package for estimation of 95.45% CI in the selected variables.

3.1. Host data

Developmental stage (Age) Gender

Table 1 Infection status of Corynosoma strumosum (Rudolphi, 1802) in the Kuril harbor Seal of Erimo Cape in Hokkaido, Japan.

Min.–max. IL (m)(mean ± SD)

No. of infected (%)

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239

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Abundance

200 150 100 50 0 I

II

III IV V VI VII VIII IX X

Intestinal canal Fig. 2. Longitudinal distribution of Corynosoma strumosum along the intestinal canal of Kuril harbor seals, presented as a boxplot. The boxes represent median and interquartile ranges, and error bars indicate the total range or 1.5 times the length of the interquartile range. Values outside these limits are marked with open circles.

were selected as substantially supported models with ΔAIC < 2 (Fig. 5a). The upper-ranked models, except for several cases, provided common tendencies where 1) the infection level increased with IL (average coefficient ranged from 0.12 to 0.27, with an overall mean 0.17) and 2) the yearlings represented higher infection level (average coefficient ranged from 0.59 to 1.72, with an overall mean 1.12) than that in the young individuals, while the cases in adults weren't always higher (average coefficient ranged from − 0.28 to 1.84, with an overall mean 0.97) against youth. The other variables were selected in the ranked models as the probable runner-up; 3) females had higher infection level than males (average coefficient ranged from 0.54 to 0.82, with an overall mean 0.65) and 4) the infection level slightly increased with W (average coefficient ranged from 0.018 to 0.056, with an overall mean 0.030) and age (average coefficient ranged from 0.043 to 0.077, with a mean 0.060). The remaining variables (B and K) were also selected as probable factors affecting the parasite abundance in a ranked model, but it didn't show clear effects as suggested in HP. The result in the subset data provided similar tendencies as well as that in the whole data (Fig. 5b), except for the relationship between sub-adult and adult because of the data exclusion of the largest male and female with heavy infection. 4. Discussion 4.1. Infection status in Erimo Cape Since C. strumosum is widely distributed in holoarctic and arctic regions, its quantitative surveys not only on prevalence but also intensity, are available from various pinniped hosts and localities. For example, Popov and Fortunato [26] describes that harbor seals are commonly infected with this parasite with astonishingly high prevalence (100%) and intensity (> 1000 worms per individual) in the Sea of Okhotsk located in the north east of Hokkaido and in the Bering Sea. Helle and Valtonen [59] also reported high levels in both values of prevalence (almost 100%) and intensity (up to 324 worms per individual with a mean of 66 in Autumn) from ringed seals, Pusa hispida botnica (Gmelin, 1788), in the Bothnian Bay of the northern Baltic Sea. In the case of the grey seal Halichoerus grypus grypus (Fabricius, 1791) from northeastern Ireland, acanthocephalans infected 100% of the animals with a mean intensity of 416 individuals and a maximum of 846 [60]. The infection level, especially of young-adult and adult individuals, in the present locality is thus comparative to the previous studies in other localities. Since the Kuril harbor seal is the dominant pinniped in Erimo Cape, C. strumosum does not have much choice but to use it as the main definitive host. Although the seal population collapsed in the early 1970's, this parasite may also have overcome the crisis together with the host seal.

Fig. 1. Corynosoma strumosum (Rudolphi, 1802) from the Kuril harbor seal. (a) Whole body of male, (b) enlarged view of the proboscies. Scale bar; 2 mm and 200 μm, respectively.

represented the highest contribution to explain the variation of parasite abundance (Fig. 4a). That of weight (21.7%), developmental stage (17.3%), intestinal length (12.1%) and body length (10.5%) was the next in order. Conjoint effect of gender only represented a slight negative value (− 0.12%). In the subset data excluding the largest male and female, only two variables (i.e. developmental stage and intestinal length) were estimated as effective (Fig. 4b). Since VIF calculation from the full model in GLMs fitting showed high values in TL (58.1) and W (62.3), we had to choose between the two in the subsequent model selection to avoid multi-collinearity; both variables also showed strong correlation (R2 = 0.92, p < 0.001). The present case excluded the former variables because the higher contribution obtained from the latter in HP analysis (Fig. 4a), and accordingly used the remaining seven variables. As a consequence of GLMs fitting, 15 cases of variables combination 240

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Gender

Stage

Fig. 3. Relationship between the parasite infection and the host's characters.

TL (cm)

Age

600 400

Abundance

200 0 Male

Female

W (kg)

Y S A Y S A

0

IL (m)

B (cm)

Male

Female

600

10

20

120

160

K (W/TL3 106)

400 200 0 20

60

100

16

20

24

0.5

1.5

2.5

14

18

22

cases when several species co-occur in the intestinal tract, habitat use of the species is sometimes deviated from its original distribution because of inter-species interaction [61]. Given the situation that no other intestinal living parasites were found from the seals in the present survey (Kaimoto, unpublished data), C. strumosum appears to represent its fundamental distribution within the tract and to be rather affected with intra-species interaction (e.g. [63]). 4.2. Probable source of infection around Hokkaido Information about intermediate- and paratenic-hosts is useful to discriminate the main source of infection in C. strumosum for the definitive host seal. However, the previous work around Erimo Cape was confined to anecdotal reports of paratenic-host findings. Araki & Machida [64] recovered this parasite from the Japanese smelt Hypomesus japonicus (Brevoort, 1856), far eastern staghorn sculpin Gymnocanthus herzensteini Jordan et Starks, 1904 great sculpin Myoxocephalus polyacanthocephalus (Pallas, 1814) (recognized as Ainocottus ensiger) and barfin flounder Varasper moseri Jordan et Gilbert, 1898 from Samani located about 40 km north west of Erimo Cape, but they do not provide any comments for quantitative data. In addition to these fishes, Fujita [65] describes sishamo smelt Spirinchus lanceolatus (Hikita, 1913) as a probable paratenic host of this acanthocephalan; he wrote about his sampling data as 12 worms recovered from 50 host individuals, which had migrated up from sea to river (i.e. the Mukawa River located about 130 km north west of the Cape), but provided no other information such as prevalence and intensity. Though apart from the present locality, Zhukov's [33] report from

Fig. 4. Independent and conjoint contributions, provided as the percentage of the total explained residual-error, of the eight variables explaining parasite abundance. Asterisk indicates the significance level of independent contribution for each variable with Zscore > 1.65. (a) whole data, (b) subset data.

As is usual with other intestinal parasites, acanthocephalan species generally represent species-specific habitat use within the digestive tract of the definitive host (see [61]). C. strumosum is known to occurmainly in the middle portion of the small intestine while the other congener C. semerse (Forssell, 1904) limitedly use the large intestine and rectum [48,62]. The present distribution of C. strumosum found in the latter part of intestine is in accordance with past reports. In the

Estimated coefficient (a) -2 0 2 -4 0 4 -4 0 4 -0.2 0 0.2 -0.1 0 0.1 -0.5 0 0.5 -1 0 1 -0.3 0 0.3 Rank1

Rank15

(b) -2 0 2 -6 0 6 -12 0 12 -3 0 3 -0.1 0 0.1 -0.4 0 0.4 -1 0 1 -0.3 0 0.3 Rank1

Rank9

Gender ( )

Yearling Adult Stage

Age

W

B

IL

241

K

Fig. 5. Coefficient values of candidate explanatory variables estimated by GLM. Models represented ΔAIC < 2 were nominated from top to bottom as making data inference. Error bar indicates 95.45% confidence interval.

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intestinal length, are considered as significant courses of parasite infection, while gender, age and body weight are weakly associate if at all. For the developmental stage, it is noteworthy that the yearling individuals have a higher burden than the expected level in sub-adults. The yearling individuals after weaning often consume benthic crustaceans, including amphipods, as the first intermediate hosts of C. strumosum (Masubuchi, unpublished data). Such a feeding habit in the yearlings may reflect the difference in the parasite burden observed from sub-adults. The complex life cycles of metazoan parasites are sometimes flexible; alternative routes of infections are frequently described (e.g. [76–77]). The infection route from the first intermediate host to the yearling seals, without going through paratenic hosts, is thus conceivable to complete the parasite's life cycle. Further confirmation is needed to demonstrate the life history polymorphism (i.e. several routes of infection) in the parasite, associating with the host's ontogenetic differences in diet use. Subtle difference between sub-adults and adults may partly be due to spatial use around the haul-out site. In the Daikoku Island located east of the present locality, ontogenetic differences in the home range size have been confirmed by using telemetry tracking (Kobayashi & Haneda, unpublished data). In the present locality, Erimo Cape, detail usage around haul-out site is currently being investigated, but availability and/or accessibility to prey organisms, including the main source of infection, may well differ between sub-adults and adults, corresponding with their habitat use. In addition to these probable ontogenetic differences, the present result also suggests a possibility that unknown host characteristics are still remaining and further research deserves attentions. Such research may include, for example, body size effect whereby the larger individuals can ensure acquisition of a better feeding ground, and age effect on how long the older ones are capable of efficient hunting. Intestinal length is strongly correlated with basal metabolic rate of marine mammals [78]. The metabolic rate further affects food requirement [79–80]. Therefore, a longer intestine indicates higher food intake, eventually resulting in a high chance of acquiring the sources of infection (see [81]). It is thus reasonable that the burden of the foodtransmitted parasite is explained by this variable. In this context, the higher burden in females may also be due to the higher energy requirement compared to males, to compensate for the energy loss from reproduction, breeding and molting [82–85], besides behavioral differences [86–90]. Both HP analysis and GLMs also suggest that thickness of the dorsal blubber and condition index K may not be important for infection whatsoever. Food energy, ingested by an individual, is partly used for growth [85] and stored as blubber serving roles of insulator and energy sore [85,91]. Parasites are often expected to act as stressors on their hosts by harming health relating to these variables [92–93]. However, the present result suggests that C. strumosum infection is less detrimental for the host seal. Since this is just the numerical analysis between the number of worms and blubber status or length-weight-based condition, further investigation on physiological response and immunocompetence, including cost estimation, are needed to understand the details of tolerance for parasite infection [94].

the Shikotan Island located just east of Hokkaido provides valuable quantitative data of C. strumosum infection in the paratenic-host fishes. According to his work, demersal species are frequently infected with C. strumosum (prevalence ranged from 40 to 54.5%): those are rock greenling Hexagrammos lagocephalus (Pallas, 1810), Japanese sandfish Arctoscopus japonicus (Steindachner, 1881), shaggy sea raven Hemitripterus villosus (Pallas, 1814) and snowy sculpin Myoxocephalus brandtii (Steindachner, 1867). On the contrary, shoreline and pelagic fishes, such as pond smelt Hypomesus olidus (Pallas, 1814), whitespotted charr Salvelinus leucomaenis leucomaenis (Pallas, 1814), saffron cod Eleginus gracilis (Tilesius, 1810), threestripe rockfish Sebastes trivittatus Hilgendorf, 1880, masked greenling Hexagrammos octogrammus (Pallas, 1814), stichaeid fish Pholidapus dybowskii (Steindachner, 1880), starry flounder Platichthys stellatus (Pallas, 1787) and black plaice Pleuronectes obscurus Herzenstein, 1890 represent low prevalence at only 4–14.2% [33]. Extensively low prevalence (0.3%) was also confirmed in pacific salmons, i.e. chum and pink salmon, from the southwestern coast of Sakhalin [66], as well as the outdated report in the neighboring localities [67]. Therefore, considering this circumstantial evidence, infections in Kuril harbor seals appears to be mainly a result from feeding on demersal fishes; it is noteworthy that the masked greenling, which is a closely related species to He. lagocephalus but inhabits shallower areas as compared to the latter, has represented lower values of prevalence (13.3 vs 45.0%) [33]. This heterogeneous occurrence of C. strumosum along with depth of habitation is also found in the single species surveys; individuals inhabiting deeper areas represent higher value of both prevalence and intensity in the American Plaice Hippoglossoides platessoides (Fabricius, 1780) and Atlantic cod Gadus morhua Linnaeus, 1758 from Gulf of Saint Lawrence [68–69]. In a diet survey on the Kuril harbor seal in the Nemuro district of eastern Hokkaido, preferred prey items actually include the probable paratenic-hosts, frequently infected with C. strumosum as mentioned above, such as rock greenling and shaggy sea raven (see [70]). Furthermore, even in the present locality, Japanese sandfish, possibly harboring this acanthocephalan (see [33]), is found as a preferred food item, together with saffron cod Eleginus gracilis (Tilesius, 1810) and several species of sclupins and cephalopods(Kobayashi, unpublished data). Thus, vulnerability to parasite infection may change with a dependence on demersal fish (i.e. probable source of infection). 4.3. Parasitological implication for host's feeding habits According to a telemetry-tracking survey [36], the Kuril harbor seals in Erimo Cape usually use coastal areas shallower than 50 m of depth as their main feeding grounds. This habit has also been reported from the harbor seals in other localities, i.e. the Moray Firth of Scotland [71–72] and western Hudson Bay of Canada [73]. The infection level of C. strumosum changing with the host's characteristics suggests that the individual seals have spatiotemporal differences in their feedings, even though the foraging depth is narrow. In the coastal areas of Erimo Cape, protruding south to the Pacific Ocean, a large number of seals have been found in and around the salmon set nets on the east side compared to those on the west [74]. The east side of the cape has a larger shallow area (< 40 m) than the west, and the biased economical damage toward the east is considerable due to this accessible feeding ground [74]. The east area has complex submarine topography where the rock greenling, which is one of the sources of C. strumosum infection, can be found on discontinuous ledge points (Masubuchi personal communication). On the west side, however, there is a large spawning ground for Japanese sandfish nearby (i.e. Hidaka subgroup [75]); which is the preferable paratenic-hosts of C. strumosum as above mentioned. Therefore, the parasite burden can change with usability and/or accessibility to prey organisms around the cape. The infection level apparently originated from a complication of various factors. Two host variables, i.e. developmental stage and

4.4. Conclusion The present study found that infection level of the food-borne parasite C. strumosum in the Kuril harbor seal changed with the individual characteristics of the hosts themselves. This suggests that the seal has individual variation in feeding habits within a limited range of foraging depth, as is the cases in other localities [71–73]. Further attention to individual difference may provide new insights into stomach contents analysis and telemetry surveys although quantitative data is hard to obtain. In the Erimo Cape, an economic loss as of 2014 caused by the Kuril harbor seal is estimated at about 42 million yen per year (Hokkaido Government; http://www.pref.hokkaido.lg.jp/ks/skn/ 242

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azarashi/kanrikeikaku.pdf). Individual differences in the dependence on salmon set net [95–96] may also be important in causing the differences of the parasite infection. If the individual seals depend on trapped salmon in the local set-nets, the expected infection level would be low because Pacific salmon aren't a preferred paratenic-hosts for C. strumosum as mentioned above (see [33,66–67]). Hereafter, as economic losses increase, momentum for the extermination of the seals will rise in order to suppress conflict with the local fisheries. In so doing, detail information on the feeding habits of this seal, as is the present case with a distinction of individual difference, should come in useful to direct operation policy.

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Acknowledgements We are grateful to staffs of the local fishery cooperative and supporters (K Oono, K Ito, D Nagashima and M. Maezawa) in Erimo town and researchers of Field Science Center for Northern Biosphere, Hokkaido University (Y. Mitani and S. Katayama) for kind assistance and cooperation in the field sampling. We also thanks M. Kanaiwa of laboratory of fisheries resource management, Tokyo University of Agriculture, for helping our study, K. Katakura, Laboratory of Parasitology, Department of Disease Control, Graduate School of Veterinary Medicine, Hokkaido University, for assistance our collections of the relevant literatures, and C. G. Ayer and J. Anders, Faculty of Environmental Earth Science, Hokkaido University, for providing suggestions. This work was financially supported by Grants-in-Aid for JSPS Fellows (No. 254625 to H.K.) and by the Environment Research and Technology Development Fund (H25-27 4-1301 to M.K.).

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