Invertebrate Biology 134(1): 38–47. © 2015, The American Microscopical Society, Inc. DOI: 10.1111/ivb.12075 Clumping behavior and byssus production as strategies for substrate competition in Mytilus edulis Vyacheslav V. Khalamana and Peter A. Lezin White Sea Biological Station, Zoological Institute, Russian Academy of Sciences, St. Petersburg 199034, Russia Abstract. Laboratory experiments showed that the mussel Mytilus edulis aggregated more intensely around living organisms (the bivalve Hiatella arctica and the solitary ascidian Styela rustica, which commonly co-occur with mussels in fouling communities) than around inanimate objects. When exposed to an inanimate object, mussels attached their byssal threads primarily to the substrate, close to the object, but when exposed to a living organ- ism, they attached their byssal threads directly to the organism. The ascidian was more intensely covered with byssal threads than was the bivalve. Mussel attachment to the ascidi- ans was apparently determined by the physical characteristics of the tunic and to a lesser extent by the excretion-secretion products released by S. rustica. This study indicates that mussels can use byssus threads as a means of entrapment of potential competitors for space. It remains unclear why mussels preferentially attached to ascidians compared to the bivalve. This can be explained either by competitive interactions, or by attractiveness of the ascidian tunic as an attachment substratum. Additional key words: Hiatella arctica, Styela rustica Competition for space is one of the most impor- et al. 2005). When different mussel species compete tant processes that shapes the structure and succes- with one another, behavioral characteristics and differ- sion of epibenthic communities (Connell 1970; ences in their resistance to environmental factors are of Dayton 1971; Buss 1986; Underwood 1992; Fairfull paramount importance (Harger 1972; Kennedy 1984; & Harriott 1999). This phenomenon has been Schneider et al. 2005; Nicastro et al. 2008). explored mainly in modular organisms (bryozoans, A certain degree of mobility and continuous sponges, and corals), because the competitive suc- production of byssal threads could provide mussels cess of these animals is relatively easy to quantify with advantages over sessile organisms that lack these by measuring colony growth and overgrowth of abilities. Behavioral responses have been shown to other organisms (Buss 1979; Suchanek & Green play a crucial part in protecting mussels from preda- 1981; Russ 1982; Nandakumar & Tanaka 1994). tors. These responses include throwing drilling whelks Among sedentary solitary animals, recruitment is off the shell (Wayne 1987), intensive clumping an important indicator of success in colonizing the (Dolmer 1998; Cot^ e & Jelnicar 1999), increase in substratum, as is the somatic growth of individual byssus production and provision of a more secure organisms (Suchanek 1978; Bushek 1988; Petraitis attachment to the substratum (Cot^ e 1995; Kulakow- 1995; Khalaman 2005a; McQuaid & Lindsay 2007). ski & Lezin 1999; Cheung et al. 2009; Brown et al. Some of these animals retain some ability to move 2011), and entrapment of predatory snails with byssal throughout their adult life. Among these, various spe- threads (Petraitis 1987; Wayne 1987; Day et al. 1991; cies of mussels are important components of epibenthic Davenport et al. 1996; Ishida & Iwasaki 1999). How- communities. Behavioral responses of adult individuals ever, it is unknown whether behavior can also provide may have a great significance for these bivalves in com- advantages in competitive interactions of mussels with petition for space with other types of sedentary and other sessile organisms. To address this question, we sessile organisms (Khalaman & Lezin 2004; Schneider performed experiments focused on two species that compete in the fouling communities in the White Sea, aAuthor for correspondence. the blue mussel Mytilus edulis LINNAEUS 1758 and the E-mail: [email protected] solitary ascidian Styela rustica LINNAEUS 1767. Competitive clumping behavior in mussels 39 Competitive interactions between mussels and vari- threads and died within a month; this was not seen ous ascidian species in fouling communities are well when blue mussels were held together with H. arc- known. These interactions have recently acquired tica, or when S. rustica was kept with H. arctica increasing importance because of the problem of bio- (Khalaman & Komendantov 2007). logical invasions by species such as Ciona intestinalis The proximate causes and the biological role of LINNAEUS 1767 and Styela clava HERDMAN 1882, and the increased byssus production of mussels in the because of the damage that ascidians cause to mussel presence of S. rustica are not well understood and farms (Lesser et al. 1992; LeBlanc et al. 2007; Raj- require further investigation. Specifically, it remains banshi & Pederson 2007; Arsenault et al. 2009). In unclear whether this response is a behavioral adap- the White Sea, native S. rustica and M. edulis form tation to suppress competitors, or a by-product of long-lasting fouling communities in the terminal the increased search time for an appropriate perma- stages of succession. Blue mussels dominate in the nent attachment site by mussels in the presence of top, sun-warmed, layer of water, not deeper than S. rustica. To address this question, we examined 1.5 m, while S. rustica is better adapted to cold waters whether clumping behavior and patterns of byssus and dominates at depths over 5 m (Oshurkov attachment differ when mussels aggregate around 1985,2000 ; Khalaman 2001b, 2005a). Within the nar- living organisms (the ascidian S. rustica and the row depth range from 1 to 5 m, mussels and ascidians bivalve H. arctica) or around inanimate objects co-occur and compete for space. More or less regular (plastic molds of S. rustica and H. arctica). The fluctuations in dominance are observed, where popu- bivalve H. artica was used because it commonly lations of S. rustica replace those of M. edulis, and co-occurs in fouling communities with M. edulis and vice versa. The duration of each stage varies from 3 to S. rustica but is not considered a strong competitor 15 years (Oshurkov 1992, 2000; Khalaman 2001b, of either species (Khalaman 2001a, 2005b, 2010). 2005a, 2010, 2013). The alternation of dominant taxa We also determined whether the physical properties is explained by the fact that both M. edulis and S. rus- of animal surfaces or chemical substances released tica lack in-advance mass recruitment that might by a competitor affect the attachment of the mus- replace members of the aging population. At the same sels, and whether mussels demonstrate taxis toward time, juveniles of the competing species are success- the strong competitor S. rustica. fully introduced as the aging population of its competitor is gradually degraded (Khalaman 2005a). Methods These changes can be described by inhibition model of succession (Connell & Slatyer 1977; Dean & Hurd The study was conducted at the White Sea Biological 1980). Station, Zoological Institute, Russian Academy Earlier studies showed that substances released of Sciences (Chupa Inlet, Kandalaksha Bay: into the water by S. rustica cause an increase in the 66°20.2300 N; 33°38.9720 E). The experiments were number of byssal plaques deposited by blue mussels performed using the solitary ascidian Styela rustica before they find a permanent attachment site (Lezin and the bivalves Mytilus edulis and Hiatella arctica. & Khalaman 2007; Khalaman et al. 2009). Blue The study species were collected from fouling mussels respond in a similar way to the excretory- communities on artificial substrata submersed at a secretory products (ESP) of the predatory starfish depth of 2–3 m. Only epibiont-free individuals were Asterias rubens LINNAEUS 1758 and the toxic sponge sampled. Mussels were 2–3 years old and 25–30 mm Halichondria panicea PALLAS 1766 (Khalaman et al. long. Styela rustica and H. arctica were comparable 2009). In contrast, substances released by conspecif- in size: average body lengths were 24.5Æ1.8 mm (SE) ics and other fouling organisms, such as the bivalve and 25.4Æ0.9 mm, respectively. Animals were main- mollusk Hiatella arctica LINNAEUS 1767 and the tained and experiments were carried out in a tempera- ascidian Molgula citrina ALDER &HANCOCK 1848, ture controlled room. Prior to experimentation, the do not cause an increase in byssus production animals were allowed to acclimate to the laboratory (Lezin & Khalaman 2007; Khalaman et al. 2009). conditions (temperature 10°C, salinity 25 ppt, con- Neither H. arctica nor M. citrina successfully com- stant illumination and active aeration, no food) for pete with M. edulis for substratum, nor do they 3 d, but experiments were performed in the tanks dominate in long-standing fouling communities in with still water, without active aeration. Laboratory depths from 1 to 5 m (Oshurkov 1985; Maximovich conditions were equivalent for all experiments and & Morozova 2000; Khalaman 2001a). In a field resemble those from the abiotic environment (temper- experiment, ascidians (S. rustica) placed into a cage ature 12–13°C, salinity 25 ppt, Arctic day). Three ser- with mussels became densely covered by byssal ies of experiments were conducted. Invertebrate Biology vol. 134, no. 1, March 2015 40 Khalaman & Lezin Mussel clumping and attachment to organisms and inanimate objects Ten mussels were placed in plexiglas tanks (10910 cm bottom area) and randomly distributed