No Effect of Recent Sympatry with Invasive Zebra Mussel on The
Total Page：16
File Type：pdf, Size：1020Kb
Hydrobiologia (2017) 794:153–166 DOI 10.1007/s10750-017-3089-3 PRIMARY RESEARCH PAPER No effect of recent sympatry with invasive zebra mussel on the oviposition decisions and reproductive success of the bitterling fish, a brood parasite of unionid mussels Veronika Barta´kova´ . Martin Reichard Received: 11 August 2016 / Revised: 2 January 2017 / Accepted: 4 January 2017 / Published online: 10 January 2017 Ó Springer International Publishing Switzerland 2017 Abstract The presence of non-native species can preferred to oviposit into non-infested unionid hosts. affect coevolved relationships. However, rapid recip- However, neither bitterling population completely rocal changes in coevolutionary associations provide avoided oviposition into infested unionids and three the potential to quickly respond to a new situation. We ovipositions into zebra mussels were observed. Over- studied a system where bitterling fish (Rhodeus all, there was a clear negative relationship between the amarus) parasitize unionid mussels by laying their number of zebra mussels on unionid host shells and the eggs onto their gills. This association is affected by the number of juvenile bitterling emerging from the infestation of unionid shells by the non-native zebra mussels. Our study demonstrated a lack of rapid mussel (Dreissena polymorpha). In a series of exper- evolutionary response to adaptively modulate ovipo- iments under experimental, semi-natural and natural sition choice after recent zebra mussel invasion. conditions, we compared the behavioural response to zebra mussel infestation of unionid shells, its effect on Keywords Ecological naivety Á Population oviposition decisions and their population conse- consequences Á Rapid adaptation Á Unio Á Unionida quences between bitterling populations naı¨ve to zebra mussels and those recently sympatric with zebra mussels. We found no effect of recent sympatry on bitterling preoviposition behaviour and oviposition Introduction decisions and only a weak effect on their reproductive success. Bitterling from both populations inspected Human-mediated range expansions and invasions infested and non-infested mussels at the same rate but threaten many aspects of biodiversity, including interspecific ecological relationships (Shine, 2012; Lockwood et al., 2013; Simberloff et al., 2013; Handling editor: Katya E. Kovalenko Ricciardi et al., 2013). Many interspecific relation- ships involve coevolution (Kiers et al., 2010). Inter- ´ ´ & V. Bartakova Á M. Reichard ( ) acting species often coexist in spatially structured Institute of Vertebrate Biology, Academy of Sciences of the Czech Republic, Kveˇtna´ 8, 603 65 Brno, Czech populations that may coevolve at different rates, Republic producing a geographic mosaic of adaptations and e-mail: [email protected] counter-adaptations with local coevolutionary hot- spots and coldspots (Thompson, 2005). For example, V. Barta´kova´ Department of Botany and Zoology, Faculty of Science, the corolla tube length of the plant Zaluzianskya Masaryk University, Brno, Czech Republic 123 154 Hydrobiologia (2017) 794:153–166 microsiphon (Kuntze) and the proboscis length of its water to obtain food and oxygen. Zebra mussels attach main pollinator, a long-tongued fly, Prosoeca gan- to hard substrates and preferentially use the shells of glbaueri Lichtwardt, 1910, vary significantly among living unionids as attachment substrate (Le- sites in strong correspondence (Anderson & Johnson, wandowski, 1976; Schloesser et al., 1996; Lucy 2007). Likewise, the level of tetrodotoxin resistance in et al., 2014). This fouling of unionid shells is the garter snake Thamnophis sirtalis (Linnaeus, 1758) specifically targeted near the siphons that lead into covaries spatially with the presence of toxic newts of the gill cavity, which interferes with unionid feeding the genus Taricha. Where the newts are absent or (Pilotto et al., 2016). At the same time, it also nontoxic, T. sirtalis resistance to tetrodotoxin is decreases the ability of bitterling to parasitize the minimal (Brodie et al., 2002). These and other unionid by depositing their eggs in the mussel gills (zu examples demonstrate that coevolutionary dynamics Ermgassen & Aldridge, 2010;Vrtı´lek & Reichard, can occur at a fine scale. 2012). In a series of experiments under laboratory, Human-induced changes to coevolutionary rela- semi-natural and natural conditions, we expanded on tionships may also be extremely rapid. The shift to a previous studies (zu Ermgassen & Aldridge, 2010; novel host plant species used by a host-specialist Vrtı´lek & Reichard, 2012) and tested whether evolu- butterfly was observed over a period of less than tionary changes following recent sympatry (approxi- 10 years, following a change in plant community mately 10 generations) affected bitterling oviposition caused by a major human disturbance (Singer et al., decisions and the reproductive consequences of using 1993). Such rapid disturbances and human-assisted unionids infested with zebra mussels. species translocations may have dramatic impact on The European bitterling is small fish that reaches non-native species, mediated by a shift in coevolu- sexual maturity after its first winter at a size of tionary state between native and novel partners (Car- 30–35 mm (Reichard & Jurajda, 1999). Its reproduc- roll et al., 1998; Prior et al., 2015; Dunphy et al., 2016). tion is dependent on the use of live freshwater mussels For example, a parasite species can spread from a as incubation sites for their embryos (Smith et al., region of long-term sympatry with its host (where it is 2004). During the reproductive period (typically subject to a coevolutionary arms race of adaptation and 6 weeks in spring), males develop bright nuptial counter-adaptation) into a new area with naı¨ve hosts coloration and defend territories. Female bitterling resulting in benefits to the parasite from the coevolu- cyclically extend long ovipositors as they ovulate a set tionary lag. A nematode parasite of East Asian eels, of eggs. Females with extended ovipositors are Anguillicoloides crassus (Kuwahara, Niimi & Hagaki, courted by males who lead them to unionid mussels 1974), introduced to Europe with its native host, in their territories. Fish thoroughly inspect the siphons Japanese eel, Anquilla japonica Temminck & Sch- of potential hosts and make sophisticated host choices legel, 1846, imported for aquaculture, infected local based on the host quality (Smith et al., 2000a, 2001; populations of the European eel, Anguilla anguilla Candolin & Reynolds, 2001). On deciding to spawn, (Linnaeus, 1758). This has led to their massive the female inserts her ovipositor into the mussel gills mortality as A. crassus was too virulent in the non- via the exhalant siphon and lays a batch of eggs (Smith coevolved European eel hosts (Taraschewski, 2006). et al., 2004). The eggs are fertilized by sperm released Similar cases often involve long-distance range expan- over the inhalant siphon of the host, discharged both sion, with species colonizing habitats with fundamen- before and after oviposition (Reichard et al., 2004a). tally different biological communities (Lockwood Water filtered by the mussel then carries the sperm et al., 2013; Jana´c et al., 2016), but subsequent range through the gills and fertilizes the eggs (Smith et al., expansions are often incremental (Sousa et al., 2014). 2004). Here, we study the coevolutionary relationship The European bitterling co-occurs with one to four between a freshwater fish, the European bitterling, mussel species (Smith et al., 2004), Anodonta cygnea Rhodeus amarus (Bloch, 1782), freshwater unionid (Linnaeus, 1758), Anodonta anatina (Linnaeus, 1758), mussels (Unionidae) that serve as hosts that brood Unio pictorum (Linnaeus, 1758) and Unio tumidus bitterling embryos, and the invasive zebra mussel Philipsson, 1788, all of which may serve as their hosts Dreissena polymorpha (Pallas, 1771). Unionid mus- (Reynolds et al., 1997). However, bitterling display sels live in benthic sediment and filter the surrounding preferences both among unionid species and among 123 Hydrobiologia (2017) 794:153–166 155 individual mussels (Smith et al., 2000a) that maximize mussels. These unionid populations are frequently their reproductive success (Smith et al., 2000b; Mills exploited by European bitterling. In a study from & Reynolds, 2002). Host choice is likely related to Great Britain, where both zebra mussels and bitterling oxygen conditions in the mussel gills (Smith et al., are non-native, zu Ermgassen and Aldridge (2010) 2001) and mussel’s ventilation rate (Mills & Rey- demonstrated that even a small number of zebra nolds, 2002). Female bitterling often abandon a mussels may have negative impact on bitterling mussel following inspection when its perceived qual- reproductive success. Non-infested unionids con- ity is suboptimal (Spence et al., 2013). tained significantly larger numbers of bitterling The zebra mussel is a small freshwater bivalve with embryos than zebra mussel infested unionids, regard- planktonic larvae that settles on hard sediment and less of whether the zebra mussels were alive or filters food particles from water column. It is one of the artificially glued dead shells (zu Ermgassen & most detrimental invasive species (DAISIE, 2016) and Aldridge, 2010). This has been largely confirmed by causes substantial changes to aquatic ecosystems Vrtı´lek and Reichard (2012) from the middle Danube worldwide due to its high filtration activity (MacIsaac, basin (Czech Republic), where the European bitterling