ethology international journal of behavioural biology Ethology RESEARCH PAPER Turbidity Hampers Mate Choice in a Pipefish Josefin Sundin*, Anders Berglund* & Gunilla Rosenqvist * Department of Ecology and Evolution ⁄ Animal Ecology, Uppsala University, Uppsala, Sweden Department of Biology, Centre for Conservation Biology, Norwegian University of Science and Technology (NTNU), Trondheim, Norway Correspondence Abstract Josefin Sundin, Department of Ecology and Evolution ⁄ Animal Ecology, Norbyva¨ gen 18 D, European coastal waters have in recent years become more turbid as SE 752 36 Uppsala, Sweden. algal growth has increased, probably due to eutrophication, global E-mail: josefi[email protected] warming and changes in fish communities. Turbidity reduces visibility, and such changes may in turn affect animal behaviour as well as evolu- Received: February 8, 2010 tionary processes that are dependent on visual stimuli. In this study we Initial acceptance: March 25, 2010 experimentally manipulated water visibility and olfactory cues to inves- Final acceptance: April 13, 2010 (M. Herberstein) tigate mate choice using the sex role-reversed broad-nosed pipefish Syngnathus typhle as our study organism. We show that males spent sig- doi: 10.1111/j.1439-0310.2010.01787.x nificantly longer time assessing females when they had access to full visual cues, compared to when visibility was reduced. Presence or absence of olfactory cues from females did not affect mate choice, sug- gesting that the possible use of smell could not make up for a reduction in visibility. This implies that mate choice is environmentally dependent and that an increased turbidity may affect processes of sexual selection through an impaired possibility for visually based mate choice. multiple signals is particularly beneficial because of Introduction the complexity involved in conveying individual Adaptive mate choice requires honest signalling, but quality, and multiple sensory modalities are there- also that the receiver accurately perceives the signal fore often used in sexual communication (Partan & (Maynard Smith & Harper 2003). A transmission Marler 1999). failure can impair mate choice, lowering the fitness Sexually selected signals as well as mating systems of the sender and ⁄ or the receiver, thereby poten- can be affected by human-induced environmental tially reducing population viability (Andersson changes (Møller 2004; Gaston et al. 2005; Torti & 1994). Environmental change may alter signal trans- Dunn 2005). Costal aquatic ecosystems may be par- mission, one example being a reduction in the trans- ticularly sensitive to human-induced environmental mission of visual signals because of increased water changes, and sexual selection in these communities turbidity. Animals may also adjust the signal to the can be affected by eutrophication and chemical habitat, which makes signals vulnerable to environ- pollution (Seehausen et al. 1997; van Doorn et al. mental change (Marten & Marler 1977; Endler 1992; 1998; Ja¨rvenpa¨a¨ & Lindstro¨ m 2004; Genner & Turner Bradbury & Verhencamp 1998). If mate choice is 2005; Fisher et al. 2006; Candolin et al. 2007, 2008; visually based a reduction in visibility can decrease Candolin & Heuschele 2008). Eutrophication leads the possibility for individuals to perform an adaptive to extreme plant growth and phytoplankton blooms mate choice, or to successfully compete for mates. (Smith 2003), which makes the water turbid. Algal- However, if sexual selection on visual signals is induced turbidity decreases water transparency and impaired, other signals, such as chemical or auditory obscures objects in the water. It also reduces the signals might be targeted or become more important light intensity and narrows the light spectrum (Heuschele et al. 2009). In mate choice, relying on (Jerlov 1976; Seehausen & van Alphen 1998). The Ethology 116 (2010) 1–9 ª 2010 Blackwell Verlag GmbH 1 Turbidity Hampers Mate Choice in a Pipefish J. Sundin et al. reduced visibility may cause changes in the mate Methods choice and reproductive behaviour of fishes (Luyten & Liley 1985, 1991; Seehausen et al. 1997; Seehau- Experimental Design sen & van Alphen 1998; Ja¨rvenpa¨a¨ & Lindstro¨ m 2004; Heubel & Schlupp 2006; Candolin et al. 2007, All experiments were carried out at Sven Love´n cen- 2008; Engstro¨ m-O¨ st & Candolin 2007; Wong et al. tre for marine sciences, Kristineberg, at the west 2007; Candolin & Heuschele 2008). coast of Sweden during April to June in 2009. Syn- The eutrophied North Sea suffers an increased gnathus typhle were caught in shallow (<10 m depth) abundance of planktonic algae (Reid et al. 2003; meadows of eelgrass, Zostera marina, in bays of the Beaugrand et al. 2003; Beaugrand & Reid 2003; Gullmar Fjord, nearby the centre (58º15¢N, 11º28¢E), Lindahl 2003; Erlandsson et al. 2006; Rosenberg et using a small beam trawl (mesh size 4 mm) pulled al. 2009), leading to decreased visibility (Secchi- by a boat. Trawling was conducted before the onset depth; Enebjo¨ rk & Fra¨nne 2006). Pipefishes (Syn- of the breeding season. In the laboratory the pipefish gnathidae) belong to a family of highly visually ori- were kept in 200-l barrels, with the sexes separated. ented fishes (Berglund et al. 1986b; Rosenqvist The barrels were equipped with continuously 1990; Collin & Collin 1999; Mosk et al. 2007; Silva renewed seawater and artificial eelgrass for shelter. et al. 2007). In the broad-nosed pipefish Syngnathus Temperature and salinity followed the natural condi- typhle the importance of visual cues in mate choice tions in the area (temperature 12–20°C, salinity 18– is well known (Berglund et al. 1986a,b; Rosenqvist 20&), and the light cycle was L16 h:D8 h, also close 1990; Berglund & Rosenqvist 1993, 2001a,b; Ro- to natural conditions. The fish were fed three times senqvist & Johansson 1995; Sandvik et al. 2000; a day with living Artemia sp., frozen mysid shrimp Silva et al. 2006, 2007; Widemo 2006), but the use and Artemia sp. The barrels were cleaned daily. of other signals, such as chemical or auditory cues, We first ran a mate choice experiment using mate is poorly understood (but see Ripley & Foran 2007; choice trial aquaria (40 · 60 · 70 cm) divided into Ratterman et al. 2009). In this species both males three compartments by plastic sheets. At the back of and females choose between mates if given the each aquarium there were two compartments and opportunity (Berglund et al. 1986b; Sandvik et al. each contained one stimulus female. At the front, 2000). Females and males prefer large partners over one large compartment contained the focal (choos- small ones, and fecundity increases with size ing) male. To prevent any interaction, visual or (Berglund et al. 1986a,b; Sandvik et al. 2000). Mat- olfactory, between the females their compartments ing preference for large body size is very common were separated by an opaque white Perspex sheet, (Andersson 1994), and can potentially be assessed allowing no water exchange between the females. independently using several different sensory We manipulated the visual and olfactory cues modalities, such as visual (Long & Houde 1989), from the females to the male at two visibility levels chemical (Marco et al. 1998), electrical (Curtis & (full vision or impaired vision, as if the water was Stoddard 2003), sound (Arak 1988), or the lateral turbid) and at two olfactory levels (no smell or line system (Hassan 1989). Fish are known to be smell), producing four treatments. A divider between able to use only non-visual cues to assess mate the male and the females was designed according to body size (Plath et al. 2007), and to use olfactory the different treatments. The treatment allowing full cues to assess other indicators of mate quality (Re- vision and smell to reach the male employed a clear usch et al. 2001; Shohet & Watt 2004; Fisher & Ro- Perspex divider, attached with silicone into the senthal 2006). aquaria. Six holes (5 mm in diameter) in the divider, Here, we experimentally investigated the conse- 10 cm from the bottom of the aquaria, allowed quences of a decrease in visibility, simulating the water to pass from the females (Fig. 1). The treat- effects of turbidity, for adaptive mate choice in the ment allowing full vision but no smell employed the broad-nosed pipefish Syngnathus typhle. Specifically same design without holes. we considered the role of visual and chemical cues The impaired vision treatments, simulating turbid using a mate choice trial design where males were water, was achieved using a semitransparent divider allowed to choose mates with access to varying lev- between the females and the male. Semi-transparency els of visual and olfactory cues. By this, we are test- was obtained by attaching an adhesive plastic film ing whether an increase in water turbidity (Alkor-Ve´nilia alcor DecoDesign; Vitrodecor, Gra¨felf- influences mate choice patterns and if olfactory sig- ing, Germany) to the clear divider. The semitranspar- nals can counter effects from reduced visibility. ent divider obscured objects on the other side of it, 2 Ethology 116 (2010) 1–9 ª 2010 Blackwell Verlag GmbH J. Sundin et al. Turbidity Hampers Mate Choice in a Pipefish Water flow non-olfactory treatments Water flow olfactory treatments Transparent: -holes or no holes Semitransparent: -holes or no holes Choice zone Fig. 1: The design of the mate choice aqua- ria with a manipulation of visual and olfactory cues at two levels. with decreasing visibility at greater distance, giving a To measure the difference between the clear and the Secchi disc depth of 3 m (measured in clear water semi-transparent dividers a densitometer scanner was using a Whipple sector disc). This lies within the natu- used (GS-800 Calibrated Densitometer; Bio-Rad Labo- ral range in the area where the pipefish were caught ratories, Hemel Hempstead, United Kingdom). The (2.8–9.4 m, Enebjo¨ rk & Fra¨nne 2006). Previous stud- optical density was measured in white light (400– ies manipulating turbidity have typically used some 750 nm) transmission mode (background subtraction algae suspension to experimentally increase turbidity.