Plankton Benthos Res 17(4): 393–405, 2022

Plankton & Benthos
Research© The Plankton Society of Japan

Host-epibiont relationship between calanoid copepods
and suctorian ciliates in the northern North Paciﬁc Ocean
Yoshinari Endo1,2,3,*, Yuma Sato1,4, Atsushi Yamaguchi5 & Igor Dovgal6
1

Laboratory of Biological Oceanography, Graduate School of Agricultural Science, Tohoku University, Sendai 980–8572, JapanThe Open University of Japan, Sendai 980–8577, Japan3
3–28–1, Katsura, Izumi-ku, Sendai 981–3134, Japan,
4
Kaneryo Sea Vegetable Corp., Osato Town 981–3522, Japan
5
Marine Biology Laboratory, Graduate School of Fisheries Sciences, Hokkaido University, Hakodate 041–8611, Japan
6
Kovalevsky Institute of Biology of the Southern Seas, Sevastopol 299011, Russian Federation
2

Received 11 June 2022; Accepted 14 October 2021 Responsible Editor: Koichi Ara
doi: 10.3800/pbr.17.393
Abstract: This study investigated the host-epibiont relationship between calanoid copepods and suctorian ciliates
collected widely from the northern North Paciﬁc Ocean. Mid- and deep-water adult female calanoids without dormant
stages were found to be infested with suctorians, probably because of their larger size, longer intermolt duration andlongevity in comparison to males and surface water species. A total of 259 calanoids belonging to sixteen species
were infested with ﬁve suctorian species. Among them, Candacia columbiae, Gaetanus minutus, Lucicutia bicornuta,
Metridia similis, Pleuromamma scutullata, and Racovitzanus antarcticus were reported to be infested with suctorians
for the ﬁrst time in the present study. Ephelota coronata infested only Metridia paciﬁca and displayed a strong host
preference, whereas the other suctorians displayed a weaker host preference. Any suctorian species that infested Metridia paciﬁca and M. similis attached almost exclusively to their urosome. Suctorians might avoid or could not stayattached to the anterior parts of these fast-swimming copepods. The attachment sites of Actinocyathula pleuromammae and Paracineta gaetani extended to the anterior part of the copepod body as the number of attached suctorians
increased, suggesting they were obliged to attach to suboptimal parts that were exposed to faster ﬂow speed.
Key words: calanoid copepods, epibiosis, North Paciﬁc, suctorian ciliates

Introduction
Epibiotic relationships involving planktonic crustaceans
as basibionts (i.e. hosts) are widespread in marine environments and include a variety of organisms as epibionts,
including bacteria, algae, and ciliates (Utz & Coats 2005).
The body surface of the crustaceans is one of the few
hard surfaces available for these small and soft-bodied
organisms to colonize. Copepods are probably the mostnumerous multicellular organisms on Earth and have amajor inﬂuence in the design and functioning of marine
ecosystems (Mauchline 1998). Suctorian ciliates are oneof the most species-rich groups among Ciliophora andare known to infest various marine organisms, including* Corresponding author: Yoshinari Endo; E-mail, yoshinari.endo.d2@
tohoku.ac.jp

plants and animals (Dovgal 2002). Their life cycle consistsof a free-swimming larval stage (swarmers) that possesses
locomotor ciliature, crawling swarmers that lack ciliature[e.g., genus Rhabdophrya (Chatton & Collin, 1910)] (Dovgal
2002), or even crawling swarmers that possess ciliature(Ephelota gigantea Noble, 1929) (Noble 1929, Kobayashi
et al. 2011). The swarmer attaches to a substrate suitable
for settlement and undergoes metamorphosis, which involves the resorption of the ciliature and development of
the stalk, lorica (if present) and tentacles (Dovgal 2002).
Fernandez-Leborans & Tato-Port (2000) examined previous
reports and showed that 46 copepod species have beenfound to be infested with 39 species of suctorian ciliates.
A study on copepods in the coastal waters of the Gulf ofMaine revealed that adult female Metridia lucens Boeck,1864 was found to be heavily infested with suctorians(Sherman & Schaner 1965). Additionally, the seasonal

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Y. Endo et al.

change in infestation rate and attachment sites of suctorians on copepods in the North Paciﬁc Ocean were alsostudied (cf. Yamaguchi & Ikeda 2001, Yamaguchi 2006).
However, extensive studies on the epibiotic relationshipbetween suctorians and a taxonomic group of host organisms with diﬀerent behavioral and ecological characteristics are quite limited. A good example of such studies isnematodes, which are the most abundant, ubiquitous anddiverse meiofaunal group and serve as ideal basibionts formany suctorians (cf. Baldrighi et al. 2020). Baldrighi et al.
(2020) compiled reports from various parts of the worldthat covered 33 species of nematodes that host 20 suctorianspecies. They explored the eﬀects of epibiosis on nematodes and suctorians, and host-epibiont species speciﬁcity
and found that most nematodes were basibiont only for one
epibiont species. Addintionally, half of the studied nematodes were colonized on the posterior body part, and the
majority of basibionts were adult nematodes which do notmolt anymore. Such studies may provide us with important
information on the host and attachment-site preferencesof suctorians, which may be determined by the mutual
relationship between them.
We sampled calanoid copepods widely from the northern North Paciﬁc Ocean and the Bering Sea, including as
many as 16 calanoid species infested with suctorians. The
biological characteristics of these copepods, such as their
vertical distribution, diel vertical migration, feeding habits, and body size, were examined in relation to suctorianinfestation. Additionally, the attachment sites of suctorians on these copepods were investigated for each copepod
and suctorian species. Based on these examinations, thecharacteristics of copepods that are conducive for suctorian infestation and the host- and attachment-site preference of suctorian species were outlined. The attachment
site of newly settling suctorians may be restricted by theexistence of pre-attached suctorians. Therefore, we inves-tigated how attachment sites extended with an increase in
the number of attached suctorians.
Materials and Methods
Zooplankton samples were collected using a ring net
with a mouth diameter of 80 cm and mesh width of 335 μm
during the T.S. Oshoro Maru cruise to the northern North
Paciﬁc Ocean and the Bering Sea from June to August2012 (Fig. 1). The net was vertically hauled from either
150 m or 1000 m to the surface. Calanoid copepods werechecked for infestation with suctorians under a dissecting
microscope on board ship and the infested copepods were
picked up from 22 stations and ﬁxed with 99.5% ethanol or
5% formalin seawater together with attached suctorians.
At the land laboratory, these copepods were observed
under a light microscope (Olympus BX53) or an inverted
microscope (Olympus IX70) to ascertain the number ofattached suctorians on each of the 7 body parts of the copepods, namely, the antennules, cephalosome, mouth appendages, metasome, swimming legs, urosome, and caudal rami.
The prosome length of the copepods and body size of suctorians were measured with an eye-piece micrometer under alight microscope. The measurements were made at least six
months after these copepods and suctorians were ﬁxed.
The shape of the macronucleus of an unknown suctorianthat attached to Paraeuchaeta birostrata Brodsky, 1950
and Paraeuchaeta elongata (Esterly, 1913) and bore a resemblance to the genus Acineta Ehrenberg, 1834 or Pelagacineta Jankowski, 1978 was determined by staining itwith Mayerʼs hematoxylin.
The feeding habits and distributional characteristics ofinfested calanoids were checked to ascertain whether thesefactors bore a relationship with suctorian infestation. The
feeding pattern of copepods was classiﬁed into three types
based on Arashkevichʼs (1969) and Ohtsuka & NishidaʼsFig. 1. Station map of the present study during the cruise of the T.S. Oshoro Maru to the northern North Paciﬁc Ocean. Stations wereclassiﬁed into 4 sea areas according to temperature-salinity proﬁles based on Favorite et al. (1976). *: Bering Current System, ●: Subarctic
Current System, ▲: Transition Domain, ○: Alaska Current System, ★: unknown area (lack of CTD casts).

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Epibiosis of suctorians and copepods(1997) classiﬁcations: i.e., suspension feeders, detritivores and carnivores. For information on the distributional
depth we referred to Brodskii (1967), Deevey & Brooks(1977) and Haury et al. (2000), and for performance ofvertical migration by copepods we referred to Vervoort(1965), Minoda (1971), Madhupratap & Haridas (1990) andYamaguchi et al. (2002, 2004, 2020).
CTD casts were performed at 19 stations out of the 22
stations in this study, and these stations were divided into
four oceanographic areas, as deﬁned by Favorite et al.
(1976) based on their temperature-salinity relationship.
We performed ANOVA to compare the eﬀect of preservatives on the body size of copepods and suctorians.
Results
Eﬀect of preservatives on sizes of copepods and suctorians
We used two preservatives to ﬁx copepods, namely, 5%formalin-seawater and 99.5% ethanol. The body shrinkage
of copepods and suctorians may diﬀer based on the preservatives used on them. Therefore, we compared the prosome length of three abundant copepod species, Gaetanus
simplex Brodsky, 1950, Metridia paciﬁca Brodsky, 1950
and Paraeuchaeta elongata, ﬁxed with both preservatives.
The ANOVA showed no signiﬁcant diﬀerence in the prosome length of these three copepod species between thetwo preservatives (Table 1). However, signiﬁcant preservative-induced diﬀerences were observed in the total length(body length + stalk length) of Actinocyathula pleuromammae (Steuer, 1928) which infested M. paciﬁca, andParacineta gaetani Sewell, 1951 which infested G. simplex(Table 1). The shrinkage was more pronounced in ethanolpreserved suctorians than in formalin-preserved ones. Speciﬁcally, when preserved with 99.5% ethanol as opposed to
5% formalin-seawater, the total length of A. pleuromammae, which attached to M. paciﬁca, was 14.5% shorter, andthat of P. gaetani, which attached to G. simplex, was 15.0%
shorter. In the present study, most of the infested copepods
were preserved with 99.5% ethanol and the body size ofsuctorians was used only when they were compared withthe length of the host copepod.
Hydrography of the study area
Four sea areas were identiﬁed using Favorite et al.ʼs(1976) temperature-salinity relations framework. These included: Transition Domain (6 stations), Subarctic Current
System (4 stations), Alaska Current System (3 stations),
and Bering Current System (7 stations, Fig. 1). At two stations, Extra-1 and Extra-2, CTD casts were not performed.
Therefore, the sea areas could not be determined for thesestations.
Symbioses between calanoids and suctorians
A total of 259 calanoid individuals belonging to 16 species were found to be infested with suctorians (Table 2).
Almost all of them were adult females: C6F (256 ind), C6M(2 ind), and C5M (1 ind). Four species of suctorian ciliates
were identiﬁed, Actinocyathula pleuromammae, Paracineta gaetani, Ephelota coronata Kent, 1881, and Rhabdophrya truncata (Dons, 1915) (Fig. 2). One unknown species
that attached to Paraeuchaeta birostrata and P. elongata
and showed a resemblance to the genera Acineta or Pelagacineta proved to have a spherical, not ramiﬁed, macronucleus by hematoxylin staining (Fig. 2f). Therefore, itdoes not belong to the genus Pelagacineta according to
Dovgal (2002), and we treated this species as Acineta sp.
The demographic and ecological features of these 16
calanoid copepods infested with suctorian ciliates are listed in Table 3. They are large-sized copepods, the smallest of which is Racovitzanus antarcticus Giesbrecht, 1902,
which has a female prosome length of 1.75 mm. These 16
species are mid- or deep-water species. Nine out of 16
species perform vertical migration. The feeding habits ofthese copepods also vary. Eight of them are suspension
feeders, whereas two are detritivores and six are carnivores.
Among the suctorian ciliates, E. coronata infested
only Metridia paciﬁca (Table 2). Rhabdophrya truncata
infested three species, Candacia columbiae Campbell,
1929, Lucicutia paciﬁca Brodsky, 1950 and Paraeuchaeta

Table 1. ANOVA to test the diﬀerence in copepod prosome length and suctorian total length between the two preservatives, 5% formalinseawater and 99.5% ethanol. Number of individuals measured are shown in parentheses.
Mean body size (μm)

FP2925.0 (10)2122.7 (22)5066.7 (6)

1.11
0.03
2.66

0.299
0.855
0.114

132.3 (24)112.6 (14)

4.49
9.4

0.038
0.003

99% Ethanol

5% Formalin2895.5 (33)2128.2 (63)4896.0 (25)113.1 (40)95.7 (78)

Copepods
Gaetanus simplex
Metridia paciﬁca
Paraeuchaeta elongata
Suctorians
Actinocyathula pleuromammae that infested Metridia paciﬁca
Paracineta gaetani that infested Gaetanus simplex

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Y. Endo et al.

Table 2. Species and developmental stages of copepods infested with suctorian ciliates. Occurrence areas of suctorians are also shown.
For the two suctorian species that attached to a copepod species and had diﬀerent occurrence areas, the areas are shown separately for eachsuctorian species by attaching * or **. C: copepodite stage, F: female, M: male.
Copepod species

Stage: number

Arietellus giesbrechti
Candacia columbiae

C6F: 1
C6F: 3Gaetanus simplex
Gaetanus minutus
Heterorhabdus tanneri
Heterostylites major
Lucicutia bicornuta
Lucicutia paciﬁca
Metridia paciﬁca

C6F: 114,
C5M: 1
C6F: 2
C6F: 1, C6M: 1
C6F: 1
C6F: 1
C6M: 1
C6F: 84

Metridia similisParaeuchaeta birostrata
Paraeuchaeta elongata

C6F: 1
C6F: 13
C6F: 30

Pleuromamma abdominalis C6F: 2
abdominalis
Pleuromamma scutullata
C6F: 1
Racovitzanus antarcticus
C6F: 1
Scaphocalanus magnus
C6F: 1

Suctorian species
Paracineta gaetani
Paracineta gaetani, Rhabdophrya truncata
Actinocyathula pleuromammae*, Paracineta gaetani**
Actinocyathula pleuromammae
Paracineta gaetani
Paracineta gaetani
Paracineta gaetani
Rhabdophrya truncata
Actinocyathula pleuromammae*, Ephelota
coronata**

Occurrence area of suctorians
Transition
Subarctic
Bering*,**, Subarctic*,**, Alaska*, Transition*, Unknown*,**Subarctic
Subarctic
Subarctic
Transition
Transition
Bering*,**, Subarctic*,**, Transition**,Unknown*

Paracineta gaetani
Acineta sp.
Acineta sp.*, Rhabdophrya truncata**

Transition
Subarctic, Alaska, Transition
Bering**, Subarctic*,**, Alaska*,**,
Transition**, Unknown*,**Actinocyathula pleuromammae

Transition

Actinocyathula pleuromammae
Paracineta gaetani
Paracineta gaetani

AlaskaSubarctic
AlaskaFig. 2. Photographs of 5 suctorian species found to have infested calanoid copepods in the present study. a: Paracineta gaetani, b: Actinocyathula pleuromammae, c: Acineta sp., d: Rhabdophrya truncata, e: Ephelota coronata, f: Acineta sp. stained with hematoxylin. Arrowshows macronucleus. White scale bar shows 100 μm.

elongata. Acineta sp. infested only two species of the genus Paraeuchaeta, namely, P. birostrata and P. elongata;
both of these species are carnivores but only the latter spe-

cies is a migrator (Table 3). Paracineta gaetani infested
as many as nine species of calanoids with widely ranging
feeding habits and with/without vertical migration. Lastly,397

Epibiosis of suctorians and copepods

Table 3. Size, distribution depth, performance of diel vertical migration (DVM) and food habit of the copepods infested with suctorianciliates. ○: presence DVM, ×: absence DVM.
Species
Arietellus giesbrechti
Candacia columbiae
Gaetanus simplex
Gaetanus minutus
Heterorhabdus tanneri
Heterostylites major
Lucicutia bicornuta
Lucicutia paciﬁca
Metridia paciﬁca
Metridia similisParaeuchaeta birostrata
Paraeuchaeta elongata
Pleuromamma abdominalis abdominalis
Pleuromamma scutullata
Racovitzanus antarcticus
Scaphocalanus magnus

Prosome length (mm)1)

4.70–5.70
3.30–3.65
2.70–3.05
2.75–2.95
2.60–2.85
2.90
4.25
2.28
1.75–2.38
2.30
5.45–6.00
4.50–5.35
2.70–2.75
2.55
1.75
4.30

Distribution depth (m)2)

500–1,000
200–1,0003)> 4003)> 2003)
500–2,0003)
1,000–4,0003)> 1,5003)
1,000–4,0003)> 503)
1,000–4,0003)
200–1,0003)
200–5003)
0–6004)1,000–4,0003)
400–5003)
100–4,0003)

DVM

Food habit

○
○6)
○7)
×7)
○6)
×8)
○9)
×8)
○7)
×8)
×7)
○7)
○4)
○7)
×8)
×8)

carnivore11)
carnivore11),12)
suspension feeder11)
suspension feeder11)
carnivore11),12)
carnivore11),12)
suspension feeder12)
suspension feeder12)
suspension feeder11),12)
suspension feeder11),12)
carnivore11),12)
carnivore11),12)
suspension feeder11),12)
suspension feeder11),12)
detritivore11)
detritivore11)

5)

1)

Ohtsuka (1997), body length, 2) Deevey & Brooks (1977), 3) Brodskii (1967), 4) Haury et al. (2000), 5) Vervoort (1965), 6) Minoda (1971),
Yamaguchi et al. (2004), 8) Yamaguchi et al. (2002), 9) Madhupratap & Haridas (1990), 10) Yamaguchi et al. (2020), 11) Ohtsuka & Nishida(1997), 12) Arashkevich (1969)7)

A. pleuromammae infested ﬁve species of copepods thatare all suspension feeders.
The number of each suctorian species per copepod
varied widely from 1 ind of E. coronata that infested M.
paciﬁca to 513 ind of P. gaetani that infested Gaetanus
simplex (Table 4). The mean numbers of Acineta sp. and R.
truncata per copepod were relatively small; 6.3–22.8 ind
for the former and 1.0–20.1 ind for the latter. Compared tothese suctorians, the number of P. gaetani and A. pleuromammae per copepod were larger; 16.0–102.0 ind for theformer and 15.0–76.9 ind for the latter.
The relationship between the mean total length of thesuctorian species and mean prosome length of the copepods infested with suctorians is presented in Fig. 3. Since
most of the copepods were preserved with 99.5% ethanol, only ethanol-preserved samples were used, except forA. pleuromammae infesting Gaetanus minutus (Brodsky,1950), which was preserved with formalin. Excluding E.
coronata, which infested M. paciﬁca and is disproportionately large for the host copepod, there was a statisticallysigniﬁcant correlation between copepod length and suctorian length (r = 0.782, p = 0.002). Even when the total
length of A. pleuromammae that infested G. minutus wascalibrated to ethanol-preserved values (16.9% shorter), a
statistically signiﬁcant correlation was obtained (r = 0.781,
p = 0.002). Actinocyathula pleuromammae and P. gaetani
infested ﬁve or more species, but there was no signiﬁcantcorrelation between the length of these two suctorians andcopepod length (r = 0.057, p = 0.927 for A. pleuromammae, r = 0.323, p = 0.677 for P. gaetani), which indicatesthat the size of A. pleuromammae and P. gaetani did not

diﬀer among their host copepod species. Actinocyathula
pleuromammae infested smaller copepods in comparison to P. gaetani. The exception was R. truncata; it waslarger when attached to P. elongata (prosome length was
4.50–5.35 mm) than when attached to L. paciﬁca (prosome
length was 2.28 mm) and C. columbiae (prosome length
was 3.45 mm). Acineta sp. infested only large copepod species with prosome length ≧4.93 mm.
Attachment site of suctorians
The body part to which suctorian ciliates attached themselves diﬀered based on copepod species as well as suctorian species (Fig. 4). Ephelota coronata attached almost
exclusively to the dorsal side of the urosome of Metridia
paciﬁca. Rhabdophrya truncata infested three species ofcopepods, Candacia columbiae, Lucicutia paciﬁca andParaeuchaeta elongata; its attachment site was more restricted than that of other suctorian species, as it only attached to the urosome of Lucicutia paciﬁca (only one copepod, therefore not shown) and P. elongata and only tothe dorsal part of the metasome of C. columbiae. Acineta
sp. attached to all three parts of Paraeuchaeta birostrata,
namely, cephalosome, metasome and urosome. A higher
percentage of its population attached to the metasome andmouth appendages of P. elongata.
Paracineta gaetani and Actinocyathula pleuromammae
attached to a similar site on Gaetanus simplex, which was
the most heavily infested copepod in the present study.
The metasome was the most common attachment site ofthese two suctorians, followed by swimming legs and urosome. There seemed to be no diﬀerence in the attachment

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Table 4.

Y. Endo et al.

Attached number (mean and range) of each suctorian ciliate to copepod species.
Suctorians

Paracineta gaetani

Actinocyathula pleuromammae

Acineta sp.
Rhabdophrya truncata

Ephelota coronata

Copepods

Mean

Range

N

Candacia columbiae
Gaetanus simplex
Heterorhabdus tanneri
Heterostylites major
Lucicutia bicornuta
Metridia similis
Racovitzanus antarcticus
Scaphocalanus magnus
Gaetanus simplex
Gaetanus minutus
Metridia paciﬁca
Pleuromamma abdominalis abdominalis
Pleuromamma scutullata
Paraeuchaeta birostrata
Paraeuchaeta elongata
Candacia columbiae
Lucicutia paciﬁca
Paraeuchaeta elongata
Metridia paciﬁca

92.7
83.0
34.0
50.0
102.0
26.0
16.0
16.0
76.1
20.5
76.9
48.0
15.0
22.8
6.3
2.0
1.0
20.1
1.1

64–130
8–513
34
50
102
26
16
16
1–339
16–25
3–268
23–73
15
3–46
1–19
2
1
1–45
1–2

3
45
1
1
1
1
1
1
69
2
79
2
1
13
7
2
1
30
8

Fig. 3. Mean total length of suctorian species (μm) plottedagainst prosome length (μm) of the calanoid species to which eachsuctorian species was attached.

sites based on sea areas.
Colonization of suctorians on copepod bodies
In order to estimate to which part of copepod bodysuctorians attach ﬁrst before spreading to other parts, theattached number of suctorians were checked across various parts of the host copepod body at several infestationlevels. For this purpose, we selected two heavily infested
copepod species, namely, Gaetanus simplex, which was infested with Actinocyathula pleuromammae and Paracineta
gaetani, and Metridia paciﬁca, which was infested with A.
pleuromammae. Copepods were grouped separately basedon the total number of suctorians attached to them, namely,
less than 25, from 25 to 50, from 50 to 100, and over
100 ind per copepod (Fig. 5).
Most of A. pleuromammae attached to the urosome of
M. paciﬁca. When the total number of A. pleuromammae was small (less than 50 ind), nearly 80% of them attached to the urosome, but when the total number exceeded
100 ind, slightly more than 60% of them attached to theurosome and the rest attached to the metasome and cephalosome (Fig. 5). On the other hand, A. pleuromammae
mainly attached to the metasome of G. simplex. When theattached number of A. pleuromammae was small (less than
25 ind), about 56% of this suctorian attached to the metasome and the rest attached to the urosome and swimming
legs. However, when the total attached number was larger,
the percentage that were attached to the metasome slightly
decreased and the percentage that attached to the cephalosome increased.
Paracineta gaetani mainly attached to the metasome of
G. simplex. About 50% of P. gaetani attached to the metasome when their total number was less than 100 ind, while
the rest attached to the swimming legs and urosome, butwhen the total number exceeded 100 ind, the percentagethat attached to the metasome decreased to 42%, and thepercentage that attached to the cephalosome increased.
Therefore, in all these three cases, the percentage of suctorians that attached to the anterior part of the copepod bodyrather than their peak attachment site increased as the total
number of attached suctorians increased.

Epibiosis of suctorians and copepods

Fig. 4. Average percentage of each suctorian species that attached to seven body parts of each calanoid species.

399

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Y. Endo et al.

Fig. 5. Average percentage of attached suctorians to seven body parts of a calanoid copepod at four infestation levels (<25, 25–50, 50–
100, >100 per copepod) for Actinocyathula pleuromammae that attached to Gaetanus simplex and Metridia paciﬁca, and Paracineta gaetanithat attached to Gaetanus simplex.

Discussion
Calanoids and infested suctorians
A total of 16 calanoid species were found to be infested with suctorians in the present study. Among them,six species were reported to be infested with suctorians
for the ﬁrst time in the present study: Candacia columbiae, Gaetanus minutus, Lucicutia bicornuta Wolfenden,
1911, Metridia similis Brodsky, 1950, Pleuromamma scutullata Brodsky, 1950, and Racovitzanus antarcticus. On
the other hand, many suctorian ciliates found in the present study have already been reported to infest copepods.
Namely, Paracineta gaetani has been reported to infest
Gaetanus antarcticus Wolfenden, 1905, and G. curvicornis
Sars, 1905 (Fernandez-Leborans & Tato-Port 2000), Metridia longa (Lubbock, 1854) and M. lucens Boeck, 1864
(Sherman & Schaner 1965). Type A of Yamaguchi (2006),
which is thought to be Paracineta gaetani, was reported
to have infested Gaetanus armiger Giesbrecht, 1888, G.

simplex, G. minutus, Heterorhabdus tanneri (Giesbrecht,
1895), Heterostylites major (Dahl, 1894), Metridia pacifica, Paraeuchaeta birostrata, P. elongata, P. rubra Brodsky, 1950, and Scaphocalanus magnus (T.Scott, 1894).
Actinocyathula pleuromammae (=Paracineta pleuromammae) has been reported to infest Pleuromamma abdominalis abdominalis and P. xiphias (Giesbrecht, 1889) by Steuer(1928), Metridia longa and M. lucens by Sherman & Schaner (1965). Yamaguchiʼs (2006) type B, which is thought
to be Ephelota coronata, was reported to have infested
Metridia paciﬁca. Yamaguchi & Ikedaʼs (2001) “shooting
star,” which is thought to be Rhabdophrya truncata, wasreported to have infested Paraeuchaeta elongata.
Calanoids infested with suctorians
Almost all copepods (98.8%, 256/259) infested with suctorians in the present study were adult females (Table 2).
These copepods are relatively large, and the smallest ofthem is Racovitzanus antarcticus, which has a prosome
length of 1.75 mm. Sedlacek et al. (2013) also reported that

Epibiosis of suctorians and copepods

epibionts including suctorians are found signiﬁcantly more
frequently on female deep-sea harpacticoid copepods thanmales. Adult female calanoids are generally larger thanmales. A larger size may be necessary for suctorian infestation, as suggested in the case of deep-sea isopods (Ólafsdóttir & Svavarsson 2002). Furthermore, copepods show
strongly female-skewed sex ratios both naturally and in therearing condition, probably because of the higher longevity in females in comparison to males, and the sex change
induced by environmental conditions (Gusmão et al. 2013).
In the case of Scaphocalanus magnus, adult males do not
feed and have shorter life spans than females, skewing theadult sex ratio towards females (Yamaguchi et al. 2020).
These may be the reasons why adult female copepods werethe main target of suctorians.
All the calanoids infested with suctorians in the present study were mid- or deep-water species. This may be
because surface water species are generally small (Grice& Hulsemann 1965, Mauchline 1972). For instance, in descending order of abundance, the surface water copepods
whose distributional depth is limited to the surface 200 mof the western subarctic Paciﬁc Ocean include Cyclopoida, Paracalanus parvus (Claus, 1863), Calanus paciﬁcus
Brodsky, 1948, Scolecithricella minor (Brady, 1883), Pseudocalanus newmani Frost, 1989, Acartia longiremis (Lilljeborg, 1853), Candacia bipinnata Giesbrecht, 1889, andMesocalanus tenuicornis (Dana, 1849)(Yamaguchi et al.
2002). In descending order of abundance, the surface water
copepods in the Bering Sea include Cyclopoida, Metridia
paciﬁca, Eucalanus bungii Giesbrecht, 1892, Pseudocalanus newmani, P. minutus (Krøyer, 1845), P. mimus Frost,
1989, Neocalanus plumchrus (Marukawa, 1921), Pseudocalanus moultoni Frost, 1989, Calanus paciﬁcus, andAcartia longiremis (Homma & Yamaguchi 2010). Amongthese surface water species, those larger than 2 mm inbody length are as follows: Aetideus paciﬁcus Brodsky,
1950, Candacia bipinnata, C. columbiae, Eucalanus bungii, Neocalanus plumchrus, Neocalanus ﬂemingeri Miller,
1988, Neocalanus cristatus (Kröyer, 1848), and Calanus
paciﬁcus (Brodskii 1967, Toda 1997). Besides Aetideus
paciﬁcus, Candacia bipinnata and C. columbiae, theselarger species have dormant stages (Mauchline 1998). Speciﬁcally, their C5 stage is characterized by the cessation of
feeding, reduced metabolic rates, high lipid reserves andinactivity (Hirche 1996). Therefore, these copepods can beruled out as hosts for suctorians, because they cannot provide a good condition for suctorians to get nutrition. The
abundance of A. paciﬁcus and C. bipinnata may be too low
and their size may be not large enough for suctorians to infest, which may be why these two species did not appear as
basibionts in the present study. C. columbiae was found to
be infested in the present study. Therefore, suctorians may
have infested larger mid- or deep-water calanoids. The
deep ocean is generally characterized by its lower watertemperatures, which makes the intermolt periods and longevity of copepods longer than in the surface waters.

401

The performance of vertical migration and feeding habits of copepods do not seem to be related to the infestationof suctorians.
Host preference of suctorians
Paracineta gaetani attached to as many as nine speciesof calanoids and appeared in all ﬁve sea areas (including the unknown area, Table 2). Actinocyathula pleuromammae infested ﬁve species of copepods and appearedin all ﬁve sea areas. Therefore, these two suctorian species do not seem to have any host preferences. On theother hand, Ephelota coronata infested only Metridia paciﬁca and appeared in the four sea areas where M. paciﬁca
were infested with a suctorian species (except the Alaska
Current System). This suggests that this suctorian has astrong host preference. Rhabdophrya truncata appeared inall ﬁve sea areas and attached to three calanoid species,
Candacia columbiae, Lucicutia paciﬁca and Paraeuchaeta
elongata; therefore, it displayed some host preference. Yamaguchi & Ikeda (2001) also reported the infestation ofthis suctorian (as “shooting star”) to P. elongata. R. truncata was originally reported in brown algae Desmarestia viridis (O.F. Müller), the hydroid Abietinaria abietina(Linnaeus, 1758) (reported as Diphasia abietina) and red
algae by Dons (1915). Other species of the genus Rhabdophrya have been reported to infest various organisms:
Rhabdophrya trimorpha Chatton & Collin, 1910 infested
a burrowing harpacticoid copepod Cletodes longicaudatus
Boeck, 1872 (Chatton & Collin 1910), Rhabdophrya populiformis (Gassovsky, 1916) infested the bryozoan Caberea
ellisii (Fleming, 1814), the hydrozoan Halecium sp. and an
isopod Idothea (Gassovsky 1916), and Rhabdophrya nymphonis (Gassovsky, 1916) infested a Pantopoda (sea spider)
Nymphon sp. (Gassovsky 1916). Considering these facts,
R. truncata does not seem to have attached to host species
with particular biological characteristics. Acineta sp. attached to only one genus Paraeuchaeta, the species being
P. birostrata and P. elongata. Acineta sp. did not appear
in the Bering Current System, even though P. elongata
infested with other suctorians were found there. Therefore,
this suctorian shows some host preference but may have alimited geographical distribution.
Host speciﬁcity is fairly well established for peritrich
ciliates (Nenninger 1948, Lust 1950), but not for suctorians. Baldrighi et al. (2020) reported that most of theirsuctorian species were found only on nematodes, and mostnematodes were found to be basibiont only for one epibiont
species; only a few nematodes could recruit diﬀerent epibionts in diﬀerent environments. Most species of suctorians
colonize a broad range of substrates, both inert and living(Cook et al. 1998). In the present study, large-sized suctorian species tended to show some host preference. However, size alone cannot explain the epibiotic relation because Ephelota coronata infested only the relatively small
Metridia paciﬁca. Further research is needed to clarify thehost preference/speciﬁcity of suctorian ciliates.

402

Y. Endo et al.

Attachment site of suctorians
Ephelota coronata mainly attached to the urosome of
Metridia paciﬁca. Yamaguchi (2006) also noted that thissuctorian (as Type B suctorian) mainly attached to the urosome and metasome of M. paciﬁca. Holt (1891) showedthat E. coronata (as Hemiophrya dalyelli) attached mainly
to the urosome and egg strings of a Caligidae copepod,
Caligus rapax Milne Edwards, 1840, which is parasitic onmarine ﬁshes and adult females possess two egg strings.
Therefore, the posterior part of the copepod body seems to
be a preferred attachment site for E. coronata. Rhabdophrya truncata attached only to the dorsal part of the metasome of Candacia columbiae, and only to the urosomeof Paraeuchaeta elongata. Yamaguchi & Ikeda (2001) reported that R. truncata attached mainly to the last somiteof the metasome and the urosome of P. elongata. There are
two other studies that reported that Rhabdophrya species
attached to copepods but the attachment site was not mentioned (Chatton & Collin 1910, Wailes 1932). For large suctorians such as E. coronata and R. truncata, which might
be prone to receive greater impact from the water ﬂow
around the host body, the attachment site might be restricted to the posterior part of copepod body where water ﬂow
is slower.
Acineta sp. in the present study attached to all threeparts of Paraeuchaeta birostata, but a higher percentage
of its population was attached to the cephalosome (mainly
mouth appendages) and metasome of P. elongata. Therefore, this species may be able to attach to various parts ofa copepodʼs body. The “Bell”-shaped and “Flask”-shaped
suctorians of Yamaguchi & Ikeda (2001) are thought to be
Acineta euchaetae Sewell, 1951 and were reported to haveattached mainly to the last somite of the metasome andthe urosome of P. birostarata and P. rubra. Kahl (1934)
reported that Acineta schulzi Kahl, 1934 attached to theurosome of copepods.
Actinocyathula pleuromammae attached mainly to themetasome of Gaetanus simplex and Pleuromamma scutullata but to the urosome of Metridia paciﬁca and Pleuromamma abdominalis abdominalis in the present study.
Steuer (1928) and Sewell (1951) also reported that A. pleuromammae attached to the last somite of the metasome andthe urosome of copepods of the genus Pleuromamma.
Paracineta gaetani attached mainly to the metasome of
G. simplex, urosome of Metridia similis, and antennule of
Scaphocalanus magnus. On the other hand, this species
attached rather evenly to various body parts of C. columbiae, Heterorhabdus tanneri, Heterostylites major, Lucicutia bicornuta and Racovitzanus antarcticus. Sewell (1951)
reported that P. gaetani attached mainly to the anterior
appendages of two Gaetanus species. Therefore, P. gaetani
may be able to attach to various parts of a copepodʼs body.
It is interesting that all suctorian species attached themselves mainly to the urosome of Metridia species. M. paciﬁca has been reported to have a fairly high swimming
speed of 8–25 mm s –1 (Enright 1977). It is probable thatsuctorians cannot endure larger ﬂow speeds when attachedto the anterior body part of this copepod.
As the number of attached suctorians increases, the at-

Fig. 6. Photograph of Actinocyathula pleuromammae with posteriorly-bent stalks that attached to the dorsal surface of the cephalosome
and metasome of Metridia paciﬁca. White scale bar shows 100 μm.

403

Epibiosis of suctorians and copepods

tachment site may extend to other body parts of copepods.
In all three cases examined in the present study, the attachment was conﬁned to the metasome (G. simplex) or
urosome (M. paciﬁca) when the number of suctorians was
small (Fig. 5). When the number of attached suctorians
was large, more suctorians were found to have attachedthemselves to the anterior part of the copepodʼs body; thepercentage attached to the cephalosome increased in thecase of G. simplex, whereas those attached to the metasome increased in the case of M. paciﬁca. A similar extension of attachment sites to the anterior part of the copepod
body with an increase in suctorians was suggested for Metridia lucens collected from the Gulf of Maine (Sherman &Schaner 1965). The movement of suctorians from one copepod individual to another would take place when swarmers are formed and copepods make close contact (such as
during copulation (Dovgal 2002)). The common contact
location during copepod copulation is the urosome (Gauld
1957, Blades & Youngbluth 1980). Swarmers would moveto another copepod individual and settle at these contact
locations. When a suitable attachment site had been already occupied by other individuals, the late-coming
swarmers had to attach to neighboring suboptimal sites on
the copepodʼs body. A similar situation would occur when
the attached suctorians reproduce and release swarmers
on the same copepod individual. It has been shown thatthe ﬂow speed is slower at the urosome than the anterior
part both when feeding (Yen & Strickler 1996) and when
free swimming (Gemmell et al. 2014). The anterior part ofthe copepod body is thus susceptible to faster ﬂow speed.
Suctorians with a posteriorly bent stalk were found whenmany suctorians attached to these parts (Fig. 6). At posterior parts such as the urosome, however, such suctorians
with a uniformly posteriorly bent stalk were not found.
The stalk development of suctorians has not been observed
in detail, but may take a short time, say, less than a day
as observed in the case of Ephelota gigantea (Kobayashi
et al. 2011), and the bent stalks found in the present study
may be formed during their development.
Attached suctorians should be feeding and when theyattain maturation they may reproduce. Dovgal (2013)
compiled observations on suctorian feeding: eight suctorian species have been observed to feed on free-swimming
ciliates and in some cases ﬂagellates (e.g., Hickson &Wadsworth 1909), and three species were even cultured
using ciliates as a prey (e.g., Nerad & Daggett 1992, Evanset al. 1995). Those suctorians, however, are all freshwater
species that attached to immotile basibionts. To ourknowledge, there is no such observation on the feeding ofmarine suctorians, or the suctorians that attach to motile
basibionts. The processes of migratory stage formation anddetachment of ciliates from hosts are known for peritrich
ciliates (Bickel et al. 2012), but have hardly ever been
observed in the case of suctorian ciliates. Budding andswarmer formation processes were observed in Ephelota
gemmipara (Hertwig, 1875) that attached to a hydroid Eu-

dendrium racemosum (Cavolini, 1785) (Tazioli & Di Camillo 2013). Processes of budding, swarmer formation anddevelopment after settlement of Ephelota gigantea that attached to a seaweed Undaria pinnatiﬁda (Harvey) Suringar were described by Kobayashi et al. (2011). A steadyincrease of body width of Ehelota plana Wailes, 1925 wasobserved with the molt stage development of its basibiont,
the North Paciﬁc krill Euphausia paciﬁca Hansen, 1911
(Endo et al. 2017). Budding individuals ﬁrst appeared at
the early premolt stage and increased toward the late premolt stage, suggesting that the life cycle of E. plana is
adapted to the molt cycle of E. paciﬁca. Life history studies on other species of suctorians are necessary to characterise their settlement and growth on host copepods.
Acknowledgements
We appreciate the help by crew members of the T.S.
Oshoro Maru during the cruise. Refereesʼ comments greatly improved out manuscript. This work was supported inpart by Tohoku Universityʼs Global COE programme ʻEcosystem Adaptability Science for the Futureʼ (no. J03) toYE. Part of this study was supported by Grants-in-Aid for
Challenging Research (Pioneering) 20K20573, and Scientiﬁc Research 20H03054 (B), 19H03037 (B), and 17H01483(A) from the Japan Society for the Promotion of Science(JSPS) to AY. This work was partially supported by the
Arctic Challenge for Sustainability II (ArCS II), Program
Grant Number JPMXD140318865 to AY. Fourth authorʼs(ID) work was made within the framework of researchissue of A.O. Kovalevsky Institute of Biology of the Southern Seas RASNo.121040500247-0.
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