Plankton Benthos Res 9(4): 189–196, 2014 Plankton & Benthos Research © The Japanese Association of Benthology

Host switching improves survival rate of the symbiotic

HIROKI TOKAJI, KOTARO NAKAHARA & SEIJI GOSHIMA*

Laboratory of Marine Biology, Graduate School of Fisheries Sciences, Hokkaido University, Hakodate, Hokkaido 041–8611, Japan Received 3 April 2013; Accepted 10 October 2014

Abstract: The symbiotic scale worm polychaete Arctonoe vittata mainly exploits the limpet Niveotectura pallida and the sea star Asterias amurensis as hosts in southern Hokkaido, Japan. Its size distribution was different between the two host , in which smaller individuals were often observed on the sea star, while larger ones were in the mantle cavity of the limpet. The host exploitation pattern of the scale worm was examined by several experiments. Scale worms infesting the sea star and the limpet showed significantly higher survival rates than those detached from the hosts under a risk of crab . Larger scale worms showed significantly higher survival rates in the limpet than in the sea star. In competition trials for the limpet host, relatively larger scale worms won and smaller ones sometimes died probably due to severe struggle. These results suggest that the scale worm switches its host species from the sea star to the limpet as it increases in body size, because smaller individuals improve their survival rate in the sea star, while larger ones are able to guard their host limpet from conspecifics and improve their chances of sur- vival. The achievement of optimal host exploitation in Arctonoe vittata therefore seems to be closely correlated to on- togenic growth.

Key words: competition, host guarding, host switching, polychaete, symbiosis

mately reproductive success are potential benefits of the Introduction host guarding and host switching behavior (Baeza & Thiel Symbiosis refers to a close association whereby two spe- 2007). cies live together, and the two species in the association are Any activity performed by a symbiont to secure a host categorized as symbiont and host (Martin & Britayev against intruders is called host guarding (Wilson 1975), 1998, Leung & Poulin 2008). The host is usually larger and this behavior is predicted to evolve when hosts are than the symbiont, receives neither benefit nor harm from scarce and defendable (Baeza & Thiel 2007). The move- the association, and becomes the refuge and/or the terri- ment of symbionts among hosts is known as host switch- tory for the symbiont. The symbiont is usually smaller and ing, a behavior which should increase in frequency with always derives benefits from the host such as improved decreasing predation risk and/or increasing host abun- survival rate and/or reproductive success (Poulin 2007). dance, assuming all other factors to be neutral (Baeza & Symbiont species often exploit more than one host. Be- Thiel 2007). The optimal behaviors of symbionts fall in the cause each host has different characteristics, the benefits range where the net benefit or benefit-to-cost ratio is the that symbionts obtain from hosts are variable. The symbi- largest under prevailing ecological conditions (Maynard- onts achieve optimal host exploitation to maximize bene- Smith 1978). Although the symbionts that exploit several fits from their hosts (Maynard-Smith 1978, Baeza & Thiel hosts are expected to achieve optimal host exploitation by 2007, Ocampo et al. 2012). Host guarding and host switch- host guarding and host switching, there are few studies ex- ing are examples of behaviors that result in optimal host amining this hypothesis, especially regarding host switch- exploitation. Increases in survivorship, growth or ulti- ing behavior in marine invertebrates (Knowlton 1980, Baeza & Stotz 2001, Baeza & Thiel 2003). * Corresponding author: Seiji Goshima; E-mail, goshima@fish.hokudai.ac.jp There are many symbiotic species of polychaete (Martin 190 H. Tokaji et al.

& Britayev 1998). The scale worm Arctonoe vittata at Vostok Bay, Sea of Japan (Britayev 1991), the scale (Grube) is widely distributed in the coastal area of the worm reproduces in summer but not in winter. The sam- North Pacific, and is a symbiotic species that exploits 30 pling area was divided into four sites: site 1 (2–3 m in known host species such as sea stars, sea cucumbers and depth), site 2 (3–4 m in depth), site 3 (4–5 m in depth), and gastropods (Martin & Britayev 1998). In northern Japan, site 4 (5–7 m in depth). Sites 1–3 were situated in a rock A. vittata mainly exploits the limpet Niveotectura pallida reef area where the limpet Niveotectura pallida was fre- (Gould) and the sea star Asterias amurensis Lütken. The quently found, and site 4 was in a sand bottom area, where limpet harbors only one scale worm in the mantle cavity the sea star Asterias amurensis was distributed. Limpets because of limited space, while the sea star harbors multi- were collected from sites 1–3, and sea stars from site 4. In ple scale worms in the ambulacral groove and around the sites 1–3, specimens were collected within three quadrats oral area (Britayev 1991, Martin & Britayev 1998). Since each in summer and within two quadrats each in winter (a the scale worm uses multiple sympatric hosts, their use total of 15 quadrats). In site 4, specimens were collected may represent optimal host exploitation. Arctonoe vittata is within nine quadrats in summer and within six quadrats in widely studied for experiments on population dynamics, winter (a total of 15 quadrats). The data recorded were the reproductive and ontogenetic biology, host selection behav- number of the limpets (sites 1–3) and sea stars (site 4), shell ior, association with hosts, and its life cycle (Davenport length of the limpets (mm), major radius length of the sea 1950, Gerber & Stout 1968, Palmer 1968, Dimock & Di- stars (mm), number of potential host specimens (i.e., with mock 1969, Wagner et al. 1979, Britayev 1991, Phillips & or without a scale worm), and body length of the scale Pernet 1996, Pernet 1998, 2000). However, there are few worms (mm) in each quadrat. studies examining the behavior of A. vittata after host se- To analyze the factors influencing the infestation rate of lection, that is, host guarding and host switching in relation the host, all quadrat data were pooled for each host spe- to its life history from the viewpoint of behavioral ecology. cies, and then used in a generalized linear model (GLM) The present study focuses on the host exploitation of the with a binomial error distribution. The response variable scale worm A. vittata and examines the hypothesis that the was with or without symbionts (yes=1, no=0) for both scale worm shows optimal host exploitation. Field research hosts. The explanatory variables were shell length, season was first conducted on host species and their infestation (summer=1, winter=2), and site (site 1=1, site 2=2, site 3 rates by the scale worm. Laboratory experiments were then =3) for the limpet. For the sea star, the explanatory vari- used to test the hypothesis that, as the scale worm grows, it ables were major radius length and season (summer=1, switches hosts from the sea star to the limpet to improve winter=2). To examine the relationship between host size the benefits gained from the hosts, such as increased sur- and body length of the scale worm, a regression analysis vival rate. was used for both hosts. Finally, Welch’s t-test was used to compare the body length of the scale worms among the host species. Image analysis software (Image J; National Materials and Methods Institute of Health, Bethesda, MA, USA) was used to mea- sure the size of all specimens, and the statistical software, Hosts of the scale worm R (ver. 2.14.1; R Development Core Team) was used for all Sampling was conducted in the western subtidal slope at statistical analyses. Usujiri Fisheries Station, Hokkaido University, Hakodate, Predator experiment 1: comparison of survival rates southern Hokkaido, Japan (41°56.17′N, 140°56.97′E). Mul- between symbiotic and non-host scale worms tiple surveys of equal effort were conducted in different habitat types to examine host species of the scale worm in This experiment was conducted in July 2012 in circular September 2011, with effort unified as the use of the same tanks with running seawater (diameter 29 cm, height amount of air while SCUBA diving (12 L air tank, 15 cm, depth 6.5 cm, with a plughole in the center). Indi- 100 MPa). The survey was conducted on a continuous viduals of the potential predatory crab Telmessus acu- slope which was divided into three habitat types: shallow tidens (hereafter, crab) were collected from Usujiri Fishing rock reef (2–4 m in depth); a boundary area composed of Port adjacent to the sampling area before the experiment rocks in a sand area between the rock reef and sand flat (June 2012, n=21), and were individually maintained in (4–5 m in depth); and a deeper sand area (5–7 m in depth). plastic bottles (diameter 9.6 cm, height 16.4 cm, with many The survey recorded host species and their abundance, and small holes to enable exchange of seawater) immersed in a infestation rate of the host species by the scale worm. large tank receiving an open circulation of seawater. The crabs were fed every other day on bivalves Septifer virga- Factors influencing infestation rate tus (Wiegmann) of shell length ＞30 mm . Three groups of To examine factors influencing infestation rates of the scale worms were used (n=21 each): 1) scale worms associ- scale worm, the surveys were conducted in June and July ated with a limpet (hereafter, worm-limpet); 2) scale (summer) and December (winter) 2011 by SCUBA diving worms associated with a sea star (hereafter, worm-sea using a quadrat (2 m×2 m). According to a previous study star); and 3) randomly selected scale worms detached from Host exploitation by symbiotic polychaete 191 their host limpet or sea star (hereafter, worm-no host). As- water. Worm-limpet pairs were collected from the sam- sociated individuals were collected only from the sampling pling area and measured. Randomly pairs of worm-limpets area and measured for size. The day after capture, experi- were then taken and the scale worms carefully removed mental were placed in the circular tanks to accli- using a small spoon-like tool and measured. One of the mate for 30 minutes prior to experimentation. At the start scale worms was then returned to its original host limpet of the experiment a crab was placed into the tank, and as a ‘symbiotic’ scale worm and the other was assigned as after 24 hours the status (dead or alive) of each scale worm an ‘intruder’ without a host. A total of 53 experimental was recorded. Scale worms that had died or disappeared pairs of symbiotic and intruder scale worms were prepared after 24 hours were classified as “dead”. One crab was re- for the experiment. peatedly used in all three groups in a consistent pattern First, the worm-limpet was placed in a tank to be accli- (i.e., in order like any one of worm-limpet, worm-sea star, mated for 10 minutes before the experiment. An intruder worm-no host; worm-sea star, worm-no host, worm-lim- worm without a host was then placed in the tank and after pet; or worm-no host, worm-limpet, worm-sea star). The 24 hours it was noted which scale worm was infesting the three patterns were repeated seven times. After 24 hours, limpet. The scale worms in each pair were differentiated all tanks were washed out with fresh water and the experi- by differences in their body size, body color, and scale ment was repeated. To compare the survival rates among color. Since the focus of the experiment was mainly on the the three groups, multiple comparisons were conducted effects of owner advantage and body length difference on using the Steel-Dwass method. the outcome of the competition, the larger worm was the main subject. The outcome was recorded as “win” or “lose” Predator experiment 2: comparison of survival rates according to whether it was the larger or smaller worm, re- between large scale worms in the limpet and the sea spectively, infesting the limpet at the end of trial. If both star worms infested the limpet, it was recorded as “draw”. This experiment was conducted in July 2012 using the To analyze the factors influencing the competition out- same circular tanks with running seawater as in experi- comes, GLM was used with a binomial error distribution. ment 1, using two groups of scale worms (n=22 each): 1) The response variable was outcomes of the large scale large scale worms (over 30 mm in body length) induced to worm (win=2, draw=1, lose=0). The explanatory variables infest a limpet; and 2) large scale worms (over 30 mm in were size differences between the large and small scale body length) induced to infest a sea star. These large worms (large–small), and the situation of the large scale worms were collected only from limpets in the field be- worm, that is, symbiotic scale worm or intruder without a cause the sea star was not associated with large worms (see host. The mean shell length of the limpet used in this ex- Results), and were randomly assigned to a limpet or a sea periment was 46.4±6.4 SD mm. These hosts were large star. Originally associated pairs of a scale worm and a lim- enough to be infested by any scale worm (H. Tokaji, per- pet in the field were not used in the experiment to avoid sonal observation). any effects of owner advantage. Host switching experiment The predatory crabs Telmessus acutidens were collected in June 2012 and maintained in the same way as for exper- This experiment was conducted in August 2012 using iment 1, but different individuals were used. The crabs the same circular tanks with running seawater. Worm-lim- were repeatedly used in both groups. The order of which pets and worm-sea stars were collected from the sampling group would start first for each experimental crab was de- area and measured. The symbiotic scale worms were care- cided in advance. Similar to the predator experiment 1, fully extracted from the hosts and measured for body worms associated with a limpet or a sea star were collected length. The worm-limpet and worm-sea star were then ran- from the sampling area, their body size was measured, and domly paired, and one scale worm was returned to the they were then induced to harbor within their assigned original host, while the other was eliminated (worm-limpet limpet or sea star. On the next day, the induced pairs of and symbiont-free sea star pair, n=40; worm-sea star and scale worm and host were placed in circular tanks to accli- symbiont-free limpet pair, n=46). First, the occupied host mate for 30 minutes prior to experimentation. A crab was was placed in a tank to acclimate for 30 minutes prior to then placed in each tank and the status of each scale worm experimentation. To start the experiment a symbiont-free (dead or alive) was recorded after 24 hours. As in experi- host was placed in the tank and after 24 hours it was re- ment 1, all tanks were then washed out with fresh water, corded which host was infested by the scale worm. and the next set of individuals were tested. Fisher’s exact Fisher’s exact test was used to examine any difference in test was used to compare the survival rates between both switching rates between the limpet and the sea star. Addi- groups. tionally, focussing on the scale worm occupying the sea star and the symbiont-free limpet group (where relatively Competition experiment high switching rates were observed) GLM was conducted This experiment was conducted in September and Octo- with a binomial error distribution to analyze the factors in- ber 2012 using the same circular tanks with running sea- fluencing switching. The response variable was whether 192 H. Tokaji et al.

Table 1. Host species associated with the polychaete Arctonoe vittata at three habitat types. The equal effort survey was conducted at each habitat by SCUBA diving. Values indicate percentage of host individuals associated with the scale worm (infestation rate) and num- ber of the infested individuals/number of the possible hosts examined in parentheses.

Infestation rate Host species Rock reef (2–4 m deep) Border (4–5 m deep) Sand (5–7 m deep)

Mollusca Niveotectura pallida limpet 54.8% (92/168) 77.9% (81/104) 54.5% (6/11) Tugalina gigas limpet 100% (1/1) 100% (1/1) －(0/0) Echinodermata Asterias amurensis sea star －(0/0) 23.1% (3/13) 49.2% (55/112) Evasterias retifera sea star －(0/0) 100% (2/2) 100% (3/3) Apostichopus japonicus sea cucumber 0% (0/8) 23.1% (6/26) 28.6% (2/7)

Table 2. Percentage of host individuals of the limpet Niveotectura pallida and the sea star Asterias amurensis associated with the scale worm Arctonoe vittata (infestation rate) at four sites in summer and winter. Values indicate infestation rates (%) and number of the in- fested individuals/number of the possible hosts examined in parentheses. *includes one sea star which was infested with three scale worms.

Infestation rate

Site (depth) Summer Winter

Limpet Sea star Limpet Sea star

1 (2–3 m) 23.1% (3/13) ̶ 100% (5/5) ̶ 2 (3–4 m) 26.7% (16/60) ̶ 100% (9/9) ̶ 3 (4–5 m) 40.7% (24/59) ̶ 63.6% (7/11) ̶ 4 (5–7 m) ̶ 72.2% (13/18) ̶ 19.0% (8/42)*

Total 32.6% (43/132) 72.2% (13/18) 84.0% (21/25) 19.0% (8/42) the worm switched host (yes=1, no=0). The explanatory quency of infestation of 54.8%. Niveotectura pallida was variables were body length of the scale worm (mm), major also the most abundant species (n=104) in the border area radius length of the sea star (mm), shell length of the lim- between rock reef and sand area, and its rate of infestation pet (mm), and sea stars with or without other scale worms was 77.9%. All the limpets observed harbored only one (yes=1, no=0). In the pairs of worm-sea star and symbiont- scale worm in their mantle cavity. The next most abundant free limpet group, the shell length of the limpet was species were the sea cucumber Apostichopus japonicus 48.2±7.8 SD mm, and the major radius length of sea star Selenka (n=26) and the sea star Asterias amurensis (n=13) was 96.0±20.7 mm. In the worm-limpet and symbiont-free in the border area. In the sand area, the sea star A. amuren- sea star group, the shell length of the limpet was sis was the most abundant species (n=112), and the fre- 47.1±8.0 mm, and major radius length of the sea star was quency of A. amurensis and N. pallida infestation by the 94.6±17.2 mm. These hosts were large enough to be in- scale worm was 49.2% and 54.5%, respectively. The sea fested by any scale worm (H. Tokaji, personal observation). star sometimes harbored several scale worms, while the sea cucumber harbored only one worm. Only a small num- ber of individuals in other host species was observed Results (Table 1), thus the focus of experiments in the present study was on the limpet N. pallida and the sea star A. amu- Hosts of the scale worm rensis. Host species, abundance and percentage of the host indi- Factors influencing infestation rate viduals of associated with the scale worm (infestation rate) are presented in Table 1, and species that were never found Table 2 shows the infestation rates (percentages of the to be associated with the scale worm in this survey were host individuals of the limpet and the sea star harboring excluded. In the rock reef area, the limpet Niveotectura the scale worm) at four sites in summer and winter. There pallida was the most abundant species (n=168), with a fre- was no significant influence of the season or the site on the Host exploitation by symbiotic polychaete 193 infestation rate (GLM, n=157, summer vs. winter; z= significant correlation was detected between the major ra- －0.171, P=0.864, site 1 vs. site 2; z=0.260, P=0.795, site 1 dius length of the sea star and the length of the scale worm vs. site 3; z=0.379, P=0.705). The infestation rate in the (n=23, r2=0.149, P=0.069, Fig. 2b). There was a significant limpet was significantly influenced by the limpet shell difference in the length of symbiotic scale worms between length (GLM, n=157, z=5.889, P＜0.001): the frequency of the limpet and the sea star hosts (Welch’s t-test, limpet; symbiotic limpets increased with increasing shell length, n=61, sea star; n=23, t=－12.861, P＜0.001; Fig. 3): scale and limpets with over 30 mm shell length were almost all worms infesting a limpet were frequently over 30 mm in infested by the scale worm (Fig. 1). The infestation rate in length, while those infesting a sea star were less than the sea star was significantly influenced by the season 30 mm in length (limpet; mean±SD=32.7±13.1 mm, sea (summer infection rate=13/18; winter, 8/42) (GLM, n=60, star; 12.0±6.2 mm). z=－3.616, P＜0.001), but there was no significant influence Predator experiment 1: comparison of survival rates of the major radius length on the infestation rate (GLM, between symbiotic and non-host scale worms n=60, z=1.740, P=0.082). There was a significant correla- tion between the limpet shell length and the length of the In both host groups, symbionts showed high survival scale worm (n=61, r2=0.423, P＜0.001; Fig. 2a), while no rates (worm-limpet; 18 out of 21 cases, 85.7%, worm-sea star; all 21 cases, 100%), while those in the no host group showed low survival rate (3 out of 21 cases, 14.3%), under a risk of crab predation. These proportions were signifi- cantly different between worms in the worm-limpet and no host groups (Steel-Dwass, t=4.574, P＜0.001), and between worms in the worm-sea star and worm-no host groups (Steel-Dwass, t=5.545, P＜0.001). However, there was no significant difference between worms in the worm-limpet and worm-sea star groups (Steel-Dwass, t=1.7759, P= 0.178). Shells of the limpets that had harbored worms that were preyed upon were not broken by the predatory crabs, and the scale worms were eaten by the crab while they were appearing from under the limpet shell. Predator experiment 2: comparison of survival rates between large scale worms in the limpet and the sea star The survival rate of symbionts was 59.1% (13 out of 22 Fig. 1. Relationship between shell length of the limpet with or cases) in the sea star group, and 90.9% (20 out of 22 cases) without a symbiont in the field (with=1, without=0). The curve in the limpet group, under a risk of crab predation. These shows a trend of changing frequency of symbiosis, suggesting proportions were significantly different between the two that the frequency becomes higher with increasing shell length of groups (Fisher’s exact test, P＜0.05). In the sea star group, the limpet (z=5.889, P＜0.001). many worms were preyed on by the crabs on the aboral

Fig. 2. Relationship between host size and body length of the scale worm in the limpet (a) and the sea star (b). The line of (a) shows a positive correlation between shell length of the limpet and body length of the infesting scale worm (n=61, r2=0.423, P＜0.001), and no significant correlation was detected for the sea star (n=23, r2=0.149, P=0.069). 194 H. Tokaji et al.

Fig. 5. Relationship between scale worm body length and host Fig. 3. Size distribution of the scale worm in two host species switching rate in sea stars. The y-axis shows whether or not the of the sea star and the limpet. The body lengths of the scale scale worm switched from the sea star (yes=1, no=0). The curve worm were significantly different between the sea star and the shows a trend of changing switching rate, suggesting that fre- limpet (t=－12.861, P＜0.001). quency of host switching increases with increasing scale worm body length (z=1.970, P＜0.05).

ing worms associated with the limpet were found within the shell. Competition experiment In the competition between symbiotic worm (owner of the host) and intruder without a host, the outcome was sig- nificantly influenced by differences in body length be- tween large and small worms (GLM, n=53, z=4.960, P＜ 0.001), but was not influenced by the situation of the large worm: owner of the host or intruder without a host (GLM, n=53, z=0.000 P=0.999). The were more likely to win contests when they were larger (Fig. 4). Smaller worms died or disappeared in 10 of the 53 cases at the end of the competition experiment. Host switching experiment In the worm-sea star and symbiont-free limpet group, 50% of the scale worms switched to the limpet (23 out of Fig. 4. Outcomes of competition in the larger scale worm over 46 cases, Fig. 5). In the worm-limpet and symbiont-free a limpet host. The x-axis shows the difference in body length be- sea star group, only 5% of the scale worms switched to the tween the large and small worms, and the y-axis shows outcomes sea star (2 out of 40 cases). These proportions were signifi- of the competition for the large scale worm (win=2, draw=1, cantly different between the two groups (Fisher’s exact lose=0). The circle plots show the outcomes of the symbiotic test, P＜0.001). Thus, the scale worms in the sea star scale worm. The cross plots show the outcomes of the intruder. switched more frequently to the limpet host than vice The curve shows a trend of changing outcomes, suggesting that versa. In the worm-sea star and symbiont-free limpet the outcomes are strongly influenced by the body length of the scale worm, with larger individual winning more frequently group, the frequency of scale worm migration was signifi- (z=4.960, P＜0.001). cantly influenced by the body length of the scale worm (GLM, n=46, body length of the scale worm; z=1.970, P＜0.05, shell length; z=－0.015, P=0.988, major radius side of the sea star. About a half of the surviving symbi- length; z=0.131, P=0.896, with or without other scale onts associated with the sea star (7 out of 13 cases) were worms in the sea star; z=1.107, P=0.268) (Fig. 5). This in- found on the aboral side of the sea stars and the other 6 dicates that scale worms infesting sea stars switched host surviving worms were found on the oral side. All surviv- more frequently when they were larger. Host exploitation by symbiotic polychaete 195

the host switching from the sea star to the limpet, but not Discussion by the difference of growth rate in the two host species. This study tested the hypothesis that the scale worm The two host species, sea stars and limpets, occupy dif- Arctonoe vittata would switch hosts from the sea star Aste- ferent habitats: sandy areas and rocky reefs, respectively, rias amurensis to the limpet Niveotectura pallida in rela- but these areas were contiguous. The sea cucumber Apos- tion to growth to improve the obtaining of benefits from tichopus japonicus was found in all three habitat types, but their hosts. Predator experiments 1 and 2 showed that it was mainly distributed in the border habitat (Table 1). smaller scale worms had high survival rates in sea stars, Thus, even if scale worms cannot switch directly from sea but larger scale worms that had been forced to live in sea stars to limpets, they may finally switch to the limpet by stars had low survival rates. This is because large individ- exploiting intermediate host species such as A. japonicus uals cannot physically enter the ambulacral groove and and Evasterias retifera. These species were found to be in- oral area of the sea star due to limited space (the oral side fested by scale worms in the border area (Table 1). It seems is more protected against potential predators). Conse- likely that some individuals of A. vittata switch hosts from quently they harbored in the aboral side which offers less sea stars to limpets directly and others switch through in- safety. In fact, scale worms were often found on the aboral termediate host species, according to growth in the field. side of the sea star in the predator experiment 2 because of This might be a way to decrease costs otherwise incurred the limited space, which might be the reason for lower sur- from intruders and to improve their survival rate. vival rate for worms on sea stars. A possible explanation for this host switching behavior Smaller individuals died or disappeared at the end of the is that predation risk in sea stars is high for large individu- competition experiment (10 out of 53 cases). According to als and/or the benefit in the limpet is sufficiently high, for observations, larger conspecifics preyed on smaller indi- example protection against predators or reproductive suc- viduals. Previous studies have also reported that A. vittata cess (Baeza & Thiel 2007). In turn, scale worm needs to individuals frequently compete over hosts and that this be large enough when switching in order to be able to competition sometimes leads to death (Palmer 1968, guard the new limpet host. This is the first report of a sym- Britayev 1991). When two individuals locate a limpet, biotic polychaete that shows host switching behavior to competition over the host would incur a higher cost for the maximize benefits from hosts. Because there are many smaller individual. polychaetes like A. vittata that exploit several hosts (Mar- The larger worm won in intraspecific competition. In tin & Britayev 1998), it is also quite likely that others other words, larger symbiotic scale worms succeeded in would show similar adaptive host switching behavior. Con- host guarding, and larger intruder worms succeeded in sequently there must be a body size threshold predicting host deprivation. A possible explanation for why host the event of switching to occupy the host of higher quality. guarding behavior has evolved could be that: survival rate Britayev (1991) has reported on the life history of A. vit- in the limpet is sufficiently high for large individuals, and tata, a species which mostly settles on sea stars and mi- uninfested limpets which are sufficiently large to harbor grates to limpets as a result of intraspecific competition. scale worms are scarce (Fig. 1). Additionaly, the limpet The present study now offers more behavioral information shell structure is morphologically simple to defend for on the scale worm life history. The field research and labo- large scale worms (Baeza & Thiel 2007). The scale worm ratory experiments reported here have shown that (1) lim- improves its survival rate both by infesting sea stars when pets over 30 mm in length were almost all infested by scale they are smaller and limpets when they are larger. worms (Fig. 1), (2) there was a positive correlation between The host switching experiment showed that the scale limpet shell length and scale worm body length (Fig. 2a), worm in the limpet almost never switched to the sea star, and (3) smaller scale worms would be preyed on or driven but those in the sea star frequently switched to the limpet. away by larger conspecifics in competition over a host. Further, there was a trend for larger individuals to switch These results suggest that A. vittata attempts to monopo- more frequently from sea stars to limpets, and almost all lize its limpet host and that intraspecific competition over individuals over 20 mm length switched (Fig. 5). This limpets in the wild might be intense. It is therefore de- trend is in accordance with the observed infestation rates duced that small scale worms can improve their survival of various sized scale worms in the field (Fig. 3), in which rate by settling on sea stars instead of inside limpets; and larger worms infested limpets and smaller ones sea stars. as they grow, they switch to a limpet host where reproduc- If the scale worm did not switch host, an alternative expla- tion takes place. This life history pattern is the result of op- nation may come from growth differences in the two host timal host exploitation. Arctonoe vittata is distributed over species. Scale worms larger then 20 mm in body length a wide range throughout the coastal North Pacific, and ex- (the minimum size of sexually mature adults; Pernet 1998) ploits various hosts in these regions (Davenport 1950; were mostly associated with limpet hosts (Fig. 3). If host Martin & Britayev 1998). Its life history pattern may there- switching behavior did not occur, no worms could repro- fore vary among different locations (Sotka 2005), but it is duce while exploiting the sea star as host. Thus, the ob- expected to show similar adaptive life history traits served size distribution in the field would be explained by through optimal host exploitation as revealed in this study. 196 H. Tokaji et al.

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